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eye tracking research

Non-Human Primate Publications

EyeLink Non-Human Primate Publications

All EyeLink non-human primate research publications up until 2022 (with some early 2023s) are listed below by year. You can search the publications using keywords such as Temporal Cortex, Macaque, Antisaccade, etc. You can also search for individual author names. If we missed any EyeLink non-human primate articles, please email us!

711 entries « ‹ 7 of 8 › »

2012

P. Christiaan Klink; Anna Oleksiak; Martin J. Lankheet; Richard J. A. Wezel

Intermittent stimulus presentation stabilizes neuronal responses in macaque area MT Journal Article

In: Journal of Neurophysiology, vol. 108, no. 8, pp. 2101–2114, 2012.

Abstract | Links | BibTeX

@article{Klink2012,
title = {Intermittent stimulus presentation stabilizes neuronal responses in macaque area MT},
author = {P. Christiaan Klink and Anna Oleksiak and Martin J. Lankheet and Richard J. A. Wezel},
doi = {10.1152/jn.00252.2012},
year = {2012},
date = {2012-01-01},
journal = {Journal of Neurophysiology},
volume = {108},
number = {8},
pages = {2101--2114},
abstract = {Repeated stimulation impacts neuronal responses. Here we show how response characteristics of sensory neurons in macaque visual cortex are influenced by the duration of the interruptions during intermittent stimulus presentation. Besides effects on response magnitude consistent with neuronal ad- aptation, the response variability was also systematically influenced. Spike rate variability in motion-sensitive area MT decreased when interruption durations were systematically increased from 250 to 2,000 ms. Activity fluctuations between subsequent trials and Fano factors over full response sequences were both lower with longer interruptions, while spike timing patterns became more regular. These variability changes partially depended on the response magnitude, but another significant effect that was uncorrelated with adaptation-in- duced changes in response magnitude was also present. Reduced response variability was furthermore accompanied by changes in spike-field coherence, pointing to the possibility that reduced spiking variability results from interactions in the local cortical network. While neuronal response stabilization may be a general effect of repeated sensory stimulation, we discuss its potential link with the phenomenon of perceptual stabilization of ambiguous stimuli as a result of interrupted presentation.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

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Repeated stimulation impacts neuronal responses. Here we show how response characteristics of sensory neurons in macaque visual cortex are influenced by the duration of the interruptions during intermittent stimulus presentation. Besides effects on response magnitude consistent with neuronal ad- aptation, the response variability was also systematically influenced. Spike rate variability in motion-sensitive area MT decreased when interruption durations were systematically increased from 250 to 2,000 ms. Activity fluctuations between subsequent trials and Fano factors over full response sequences were both lower with longer interruptions, while spike timing patterns became more regular. These variability changes partially depended on the response magnitude, but another significant effect that was uncorrelated with adaptation-in- duced changes in response magnitude was also present. Reduced response variability was furthermore accompanied by changes in spike-field coherence, pointing to the possibility that reduced spiking variability results from interactions in the local cortical network. While neuronal response stabilization may be a general effect of repeated sensory stimulation, we discuss its potential link with the phenomenon of perceptual stabilization of ambiguous stimuli as a result of interrupted presentation.

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  • doi:10.1152/jn.00252.2012

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Anders Ledberg; Anna Montagnini; Richard Coppola; Steven L. Bressler

Reduced variability of ongoing and evoked cortical activity leads to improved behavioral performance Journal Article

In: PLoS ONE, vol. 7, no. 8, pp. e43166, 2012.

Abstract | Links | BibTeX

@article{Ledberg2012,
title = {Reduced variability of ongoing and evoked cortical activity leads to improved behavioral performance},
author = {Anders Ledberg and Anna Montagnini and Richard Coppola and Steven L. Bressler},
doi = {10.1371/journal.pone.0043166},
year = {2012},
date = {2012-01-01},
journal = {PLoS ONE},
volume = {7},
number = {8},
pages = {e43166},
publisher = {10. 1371/journal.pone.0043166},
address = {e43166. doi},
abstract = {Sensory responses of the brain are known to be highly variable, but the origin and functional relevance of this variability have long remained enigmatic. Using the variable foreperiod of a visual discrimination task to assess variability in the primate cerebral cortex, we report that visual evoked response variability is not only tied to variability in ongoing cortical activity, but also predicts mean response time. We used cortical local field potentials, simultaneously recorded from widespread cortical areas, to gauge both ongoing and visually evoked activity. Trial-to-trial variability of sensory evoked responses was strongly modulated by foreperiod duration and correlated both with the cortical variability before stimulus onset as well as with response times. In a separate set of experiments we probed the relation between small saccadic eye movements, foreperiod duration and manual response times. The rate of eye movements was modulated by foreperiod duration and eye position variability was positively correlated with response times. Our results indicate that when the time of a sensory stimulus is predictable, reduction in cortical variability before the stimulus can improve normal behavioral function that depends on the stimulus.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

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Sensory responses of the brain are known to be highly variable, but the origin and functional relevance of this variability have long remained enigmatic. Using the variable foreperiod of a visual discrimination task to assess variability in the primate cerebral cortex, we report that visual evoked response variability is not only tied to variability in ongoing cortical activity, but also predicts mean response time. We used cortical local field potentials, simultaneously recorded from widespread cortical areas, to gauge both ongoing and visually evoked activity. Trial-to-trial variability of sensory evoked responses was strongly modulated by foreperiod duration and correlated both with the cortical variability before stimulus onset as well as with response times. In a separate set of experiments we probed the relation between small saccadic eye movements, foreperiod duration and manual response times. The rate of eye movements was modulated by foreperiod duration and eye position variability was positively correlated with response times. Our results indicate that when the time of a sensory stimulus is predictable, reduction in cortical variability before the stimulus can improve normal behavioral function that depends on the stimulus.

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  • doi:10.1371/journal.pone.0043166

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Kyoung-Min Lee; Kyung-Ha Ahn; Edward L. Keller

Saccade generation by the frontal eye fields in Rhesus monkeys is separable from visual detection and bottom-up attention shift Journal Article

In: PLoS ONE, vol. 7, no. 6, pp. e39886, 2012.

Abstract | Links | BibTeX

@article{Lee2012a,
title = {Saccade generation by the frontal eye fields in Rhesus monkeys is separable from visual detection and bottom-up attention shift},
author = {Kyoung-Min Lee and Kyung-Ha Ahn and Edward L. Keller},
doi = {10.1371/journal.pone.0039886},
year = {2012},
date = {2012-01-01},
journal = {PLoS ONE},
volume = {7},
number = {6},
pages = {e39886},
publisher = {10. 1371/journal.pone.0039886},
address = {e39886. doi},
abstract = {The frontal eye fields (FEF), originally identified as an oculomotor cortex, have also been implicated in perceptual functions, such as constructing a visual saliency map and shifting visual attention. Further dissecting the area's role in the transformation from visual input to oculomotor command has been difficult because of spatial confounding between stimuli and responses and consequently between intermediate cognitive processes, such as attention shift and saccade preparation. Here we developed two tasks in which the visual stimulus and the saccade response were dissociated in space (the extended memory-guided saccade task), and bottom-up attention shift and saccade target selection were independent (the four-alternative delayed saccade task). Reversible inactivation of the FEF in rhesus monkeys disrupted, as expected, contralateral memory-guided saccades, but visual detection was demonstrated to be intact at the same field. Moreover, saccade behavior was impaired when a bottom-up shift of attention was not a prerequisite for saccade target selection, indicating that the inactivation effect was independent of the previously reported dysfunctions in bottom-up attention control. These findings underscore the motor aspect of the area's functions, especially in situations where saccades are generated by internal cognitive processes, including visual short-term memory and long-term associative memory.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

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The frontal eye fields (FEF), originally identified as an oculomotor cortex, have also been implicated in perceptual functions, such as constructing a visual saliency map and shifting visual attention. Further dissecting the area's role in the transformation from visual input to oculomotor command has been difficult because of spatial confounding between stimuli and responses and consequently between intermediate cognitive processes, such as attention shift and saccade preparation. Here we developed two tasks in which the visual stimulus and the saccade response were dissociated in space (the extended memory-guided saccade task), and bottom-up attention shift and saccade target selection were independent (the four-alternative delayed saccade task). Reversible inactivation of the FEF in rhesus monkeys disrupted, as expected, contralateral memory-guided saccades, but visual detection was demonstrated to be intact at the same field. Moreover, saccade behavior was impaired when a bottom-up shift of attention was not a prerequisite for saccade target selection, indicating that the inactivation effect was independent of the previously reported dysfunctions in bottom-up attention control. These findings underscore the motor aspect of the area's functions, especially in situations where saccades are generated by internal cognitive processes, including visual short-term memory and long-term associative memory.

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  • doi:10.1371/journal.pone.0039886

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Patrick J. Mineault; Farhan A. Khawaja; Daniel A. Butts; Christopher C. Pack

Hierarchical processing of complex motion along the primate dorsal visual pathway Journal Article

In: Proceedings of the National Academy of Sciences, vol. 109, no. 16, pp. E972–E980, 2012.

Abstract | Links | BibTeX

@article{Mineault2012,
title = {Hierarchical processing of complex motion along the primate dorsal visual pathway},
author = {Patrick J. Mineault and Farhan A. Khawaja and Daniel A. Butts and Christopher C. Pack},
doi = {10.1073/pnas.1115685109},
year = {2012},
date = {2012-01-01},
journal = {Proceedings of the National Academy of Sciences},
volume = {109},
number = {16},
pages = {E972--E980},
publisher = {109, E972-E980},
abstract = {Neurons in the medial superior temporal (MST) area of the primate visual cortex respond selectively to complex motion patterns defined by expansion, rotation, and deformation. Consequently they are often hypothesized to be involved in important behavioral functions, such as encoding the velocities of moving objects and surfaces relative to the observer. However, the computations underlying such selectivity are unknown. In this work we have developed a unique, naturalistic motion stimulus and used it to probe the complex selectivity of MST neurons. The resulting data were then used to estimate the properties of the feed-forward inputs to each neuron. This analysis yielded models that successfully accounted for much of the observed stimulus selectivity, provided that the inputs were combined via a nonlinear integration mechanism that approximates a multiplicative interaction among MST inputs. In simulations we found that this type of integration has the functional role of improving estimates of the 3D velocity of moving objects. As this computation is of general utility for detecting complex stimulus features, we suggest that it may represent a fundamental aspect of hierarchical sensory processing.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

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Neurons in the medial superior temporal (MST) area of the primate visual cortex respond selectively to complex motion patterns defined by expansion, rotation, and deformation. Consequently they are often hypothesized to be involved in important behavioral functions, such as encoding the velocities of moving objects and surfaces relative to the observer. However, the computations underlying such selectivity are unknown. In this work we have developed a unique, naturalistic motion stimulus and used it to probe the complex selectivity of MST neurons. The resulting data were then used to estimate the properties of the feed-forward inputs to each neuron. This analysis yielded models that successfully accounted for much of the observed stimulus selectivity, provided that the inputs were combined via a nonlinear integration mechanism that approximates a multiplicative interaction among MST inputs. In simulations we found that this type of integration has the functional role of improving estimates of the 3D velocity of moving objects. As this computation is of general utility for detecting complex stimulus features, we suggest that it may represent a fundamental aspect of hierarchical sensory processing.

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  • doi:10.1073/pnas.1115685109

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Ryan E. B. Mruczek; David L. Sheinberg

Stimulus selectivity and response latency in putative inhibitory and excitatory neurons of the primate inferior temporal cortex Journal Article

In: Journal of Neurophysiology, vol. 108, no. 10, pp. 2725–2736, 2012.

Abstract | Links | BibTeX

@article{Mruczek2012,
title = {Stimulus selectivity and response latency in putative inhibitory and excitatory neurons of the primate inferior temporal cortex},
author = {Ryan E. B. Mruczek and David L. Sheinberg},
doi = {10.1152/jn.00618.2012},
year = {2012},
date = {2012-01-01},
journal = {Journal of Neurophysiology},
volume = {108},
number = {10},
pages = {2725--2736},
abstract = {The cerebral cortex is composed of many distinct classes of neurons. Numerous studies have demonstrated corresponding differences in neuronal properties across cell types, but these comparisons have largely been limited to conditions outside of awake, behaving animals. Thus the functional role of the various cell types is not well understood. Here, we investigate differences in the functional properties of two widespread and broad classes of cells in inferior temporal cortex of macaque monkeys: inhibitory interneurons and excitatory projection cells. Cells were classified as putative inhibitory or putative excitatory neurons on the basis of their extracellular waveform characteristics (e.g., spike duration). Consistent with previous intracellular recordings in cortical slices, putative inhibitory neurons had higher spontaneous firing rates and higher stimulus-evoked firing rates than putative excitatory neurons. Additionally, putative excitatory neurons were more susceptible to spike waveform adaptation following very short interspike intervals. Finally, we compared two functional properties of each neuron's stimulus-evoked response: stimulus selectivity and response latency. First, putative excitatory neurons showed stronger stimulus selectivity compared with putative inhibitory neurons. Second, putative inhibitory neurons had shorter response latencies compared with putative excitatory neurons. Selectivity differences were maintained and latency differences were enhanced during a visual search task emulating more natural viewing conditions. Our results suggest that short-latency inhibitory responses are likely to sculpt visual processing in excitatory neurons, yielding a sparser visual representation.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

The cerebral cortex is composed of many distinct classes of neurons. Numerous studies have demonstrated corresponding differences in neuronal properties across cell types, but these comparisons have largely been limited to conditions outside of awake, behaving animals. Thus the functional role of the various cell types is not well understood. Here, we investigate differences in the functional properties of two widespread and broad classes of cells in inferior temporal cortex of macaque monkeys: inhibitory interneurons and excitatory projection cells. Cells were classified as putative inhibitory or putative excitatory neurons on the basis of their extracellular waveform characteristics (e.g., spike duration). Consistent with previous intracellular recordings in cortical slices, putative inhibitory neurons had higher spontaneous firing rates and higher stimulus-evoked firing rates than putative excitatory neurons. Additionally, putative excitatory neurons were more susceptible to spike waveform adaptation following very short interspike intervals. Finally, we compared two functional properties of each neuron's stimulus-evoked response: stimulus selectivity and response latency. First, putative excitatory neurons showed stronger stimulus selectivity compared with putative inhibitory neurons. Second, putative inhibitory neurons had shorter response latencies compared with putative excitatory neurons. Selectivity differences were maintained and latency differences were enhanced during a visual search task emulating more natural viewing conditions. Our results suggest that short-latency inhibitory responses are likely to sculpt visual processing in excitatory neurons, yielding a sparser visual representation.

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  • doi:10.1152/jn.00618.2012

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Ioan Opris; Robert E. Hampson; Greg A. Gerhardt; Theodore W. Berger; Sam A. Deadwyler

Columnar processing in primate pFC: Evidence for executive control microcircuits Journal Article

In: Journal of Cognitive Neuroscience, vol. 24, no. 12, pp. 2334–2347, 2012.

Abstract | Links | BibTeX

@article{Opris2012,
title = {Columnar processing in primate pFC: Evidence for executive control microcircuits},
author = {Ioan Opris and Robert E. Hampson and Greg A. Gerhardt and Theodore W. Berger and Sam A. Deadwyler},
doi = {10.1162/jocn_a_00307},
year = {2012},
date = {2012-01-01},
journal = {Journal of Cognitive Neuroscience},
volume = {24},
number = {12},
pages = {2334--2347},
abstract = {A common denominator for many cognitive disorders of human brain is the disruption of neural activity within pFC, whose structural basis is primarily interlaminar (columnar) microcircuits or "minicolumns." The importance of this brain region for executive decision-making has been well documented; however, because of technological constraints, the minicolumnar basis is not well understood. Here, via implementation of a unique conformal multielectrode recording array, the role of interlaminar pFC minicolumns in the executive control of task-related target selection is demonstrated in nonhuman primates performing a visuomotor DMS task. The results reveal target-specific, interlaminar correlated firing during the decision phase of the trial between multielectrode recording array-isolated minicolumnar pairs of neurons located in parallel in layers 2/3 and layer 5 of pFC. The functional significance of individual pFC minicolumns (separated by 40 $mu$m) was shown by reduced correlated firing between cell pairs within single minicolumns on error trials with inappropriate target selection. To further demonstrate dependence on performance, a task-disrupting drug (cocaine) was administered in the middle of the session, which also reduced interlaminar firing in minicolumns that fired appropriately in the early (nondrug) portion of the session. The results provide a direct demonstration of task-specific, real-time columnar processing in pFC indicating the role of this type of microcircuit in executive control of decision-making in primate brain.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

A common denominator for many cognitive disorders of human brain is the disruption of neural activity within pFC, whose structural basis is primarily interlaminar (columnar) microcircuits or "minicolumns." The importance of this brain region for executive decision-making has been well documented; however, because of technological constraints, the minicolumnar basis is not well understood. Here, via implementation of a unique conformal multielectrode recording array, the role of interlaminar pFC minicolumns in the executive control of task-related target selection is demonstrated in nonhuman primates performing a visuomotor DMS task. The results reveal target-specific, interlaminar correlated firing during the decision phase of the trial between multielectrode recording array-isolated minicolumnar pairs of neurons located in parallel in layers 2/3 and layer 5 of pFC. The functional significance of individual pFC minicolumns (separated by 40 $mu$m) was shown by reduced correlated firing between cell pairs within single minicolumns on error trials with inappropriate target selection. To further demonstrate dependence on performance, a task-disrupting drug (cocaine) was administered in the middle of the session, which also reduced interlaminar firing in minicolumns that fired appropriately in the early (nondrug) portion of the session. The results provide a direct demonstration of task-specific, real-time columnar processing in pFC indicating the role of this type of microcircuit in executive control of decision-making in primate brain.

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  • doi:10.1162/jocn_a_00307

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Sarah L. Eagleman; Valentin Dragoi

Image sequence reactivation in awake V4 networks Journal Article

In: Proceedings of the National Academy of Sciences, vol. 109, no. 47, pp. 19450–19455, 2012.

Abstract | Links | BibTeX

@article{Eagleman2012,
title = {Image sequence reactivation in awake V4 networks},
author = {Sarah L. Eagleman and Valentin Dragoi},
doi = {10.1073/pnas.1212059109},
year = {2012},
date = {2012-01-01},
journal = {Proceedings of the National Academy of Sciences},
volume = {109},
number = {47},
pages = {19450--19455},
abstract = {In the absence of sensory input, neuronal networks are far from being silent. Whether spontaneous changes in ongoing activity reflect previous sensory experience or stochastic fluctuations in brain activity is not well understood. Here we describe reactivation of stimulus-evoked activity in awake visual cortical networks. We found that continuous exposure to randomly flashed image sequences induces reactivation in macaque V4 cortical networks in the absence of visual stimulation. This reactivation of previously evoked activity is stimulus-specific, occurs only in the same temporal order as the original response, and strengthens with increased stimulus exposures. Importantly, cells exhibiting significant reactivation carry more information about the stimulus than cells that do not reactivate. These results demonstrate a surprising degree of experience-dependent plasticity in visual cortical networks as a result of repeated exposure to unattended information. We suggest that awake reactivation in visual cortex may underlie perceptual learning by passive stimulus exposure.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

In the absence of sensory input, neuronal networks are far from being silent. Whether spontaneous changes in ongoing activity reflect previous sensory experience or stochastic fluctuations in brain activity is not well understood. Here we describe reactivation of stimulus-evoked activity in awake visual cortical networks. We found that continuous exposure to randomly flashed image sequences induces reactivation in macaque V4 cortical networks in the absence of visual stimulation. This reactivation of previously evoked activity is stimulus-specific, occurs only in the same temporal order as the original response, and strengthens with increased stimulus exposures. Importantly, cells exhibiting significant reactivation carry more information about the stimulus than cells that do not reactivate. These results demonstrate a surprising degree of experience-dependent plasticity in visual cortical networks as a result of repeated exposure to unattended information. We suggest that awake reactivation in visual cortex may underlie perceptual learning by passive stimulus exposure.

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  • doi:10.1073/pnas.1212059109

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Bryan J. Hansen; Mircea I. Chelaru; Valentin Dragoi

Correlated variability in laminar cortical circuits Journal Article

In: Neuron, vol. 76, no. 3, pp. 590–602, 2012.

Abstract | Links | BibTeX

@article{Hansen2012,
title = {Correlated variability in laminar cortical circuits},
author = {Bryan J. Hansen and Mircea I. Chelaru and Valentin Dragoi},
doi = {10.1016/j.neuron.2012.08.029},
year = {2012},
date = {2012-01-01},
journal = {Neuron},
volume = {76},
number = {3},
pages = {590--602},
publisher = {Elsevier Inc.},
abstract = {Despite the fact that strong trial-to-trial correlated variability in responses has been reported in many cortical areas, recent evidence suggests that neuronal correlations are much lower than previously thought. Here, we used multicontact laminar probes to revisit the issue of correlated variability in primary visual (V1) cortical circuits. We found that correlations between neurons depend strongly on local network context-whereas neurons in the input (granular) layers showed virtually no correlated variability, neurons in the output layers (supragranular and infragranular) exhibited strong correlations. The laminar dependence of noise correlations is consistent with recurrent models in which neurons in the granular layer receive intracortical inputs from nearby cells, whereas supragranular and infragranular layer neurons receive inputs over larger distances. Contrary to expectation that the output cortical layers encode stimulus information most accurately, we found that the input network offers superior discrimination performance compared to the output networks.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

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Despite the fact that strong trial-to-trial correlated variability in responses has been reported in many cortical areas, recent evidence suggests that neuronal correlations are much lower than previously thought. Here, we used multicontact laminar probes to revisit the issue of correlated variability in primary visual (V1) cortical circuits. We found that correlations between neurons depend strongly on local network context-whereas neurons in the input (granular) layers showed virtually no correlated variability, neurons in the output layers (supragranular and infragranular) exhibited strong correlations. The laminar dependence of noise correlations is consistent with recurrent models in which neurons in the granular layer receive intracortical inputs from nearby cells, whereas supragranular and infragranular layer neurons receive inputs over larger distances. Contrary to expectation that the output cortical layers encode stimulus information most accurately, we found that the input network offers superior discrimination performance compared to the output networks.

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  • doi:10.1016/j.neuron.2012.08.029

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Elias B. Issa; James J. DiCarlo

Precedence of the eye region in neural processing of faces Journal Article

In: Journal of Neuroscience, vol. 32, no. 47, pp. 16666–16682, 2012.

Abstract | Links | BibTeX

@article{Issa2012,
title = {Precedence of the eye region in neural processing of faces},
author = {Elias B. Issa and James J. DiCarlo},
doi = {10.1523/JNEUROSCI.2391-12.2012},
year = {2012},
date = {2012-01-01},
journal = {Journal of Neuroscience},
volume = {32},
number = {47},
pages = {16666--16682},
abstract = {Functional magnetic resonance imaging (fMRI) has revealed multiple subregions in monkey inferior temporal cortex (IT) that are selective for images of faces over other objects. The earliest of these subregions, the posterior lateral face patch (PL), has not been studied previously at the neurophysiological level. Perhaps not surprisingly, we found that PL contains a high concentration of "face-selective" cells when tested with standard image sets comparable to those used previously to define the region at the level of fMRI. However, we here report that several different image sets and analytical approaches converge to show that nearly all face-selective PL cells are driven by the presence of a single eye in the context of a face outline. Most strikingly, images containing only an eye, even when incorrectly positioned in an outline, drove neurons nearly as well as full-face images, and face images lacking only this feature led to longer latency responses. Thus, bottom-up face processing is relatively local and linearly integrates features-consistent with parts-based models-grounding investigation of how the presence of a face is first inferred in the IT face processing hierarchy.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

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Functional magnetic resonance imaging (fMRI) has revealed multiple subregions in monkey inferior temporal cortex (IT) that are selective for images of faces over other objects. The earliest of these subregions, the posterior lateral face patch (PL), has not been studied previously at the neurophysiological level. Perhaps not surprisingly, we found that PL contains a high concentration of "face-selective" cells when tested with standard image sets comparable to those used previously to define the region at the level of fMRI. However, we here report that several different image sets and analytical approaches converge to show that nearly all face-selective PL cells are driven by the presence of a single eye in the context of a face outline. Most strikingly, images containing only an eye, even when incorrectly positioned in an outline, drove neurons nearly as well as full-face images, and face images lacking only this feature led to longer latency responses. Thus, bottom-up face processing is relatively local and linearly integrates features-consistent with parts-based models-grounding investigation of how the presence of a face is first inferred in the IT face processing hierarchy.

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  • doi:10.1523/JNEUROSCI.2391-12.2012

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Ken-ichi Amemori; Ann M. Graybiel

Localized microstimulation of primate pregenual cingulate cortex induces negative decision-making Journal Article

In: Nature Neuroscience, vol. 15, no. 5, pp. 776–785, 2012.

Abstract | Links | BibTeX

@article{Amemori2012,
title = {Localized microstimulation of primate pregenual cingulate cortex induces negative decision-making},
author = {Ken-ichi Amemori and Ann M. Graybiel},
doi = {10.1038/nn.3088},
year = {2012},
date = {2012-01-01},
journal = {Nature Neuroscience},
volume = {15},
number = {5},
pages = {776--785},
abstract = {The pregenual anterior cingulate cortex (pACC) has been implicated in human anxiety disorders and depression, but the circuit-level mechanisms underlying these disorders are unclear. In healthy individuals, the pACC is involved in cost-benefit evaluation. We developed a macaque version of an approach-avoidance decision task used to evaluate anxiety and depression in humans and, with multi-electrode recording and cortical microstimulation, we probed pACC function as monkeys performed this task. We found that the macaque pACC has an opponent process-like organization of neurons representing motivationally positive and negative subjective value. Spatial distribution of these two neuronal populations overlapped in the pACC, except in one subzone, where neurons with negative coding were more numerous. Notably, microstimulation in this subzone, but not elsewhere in the pACC, increased negative decision-making, and this negative biasing was blocked by anti-anxiety drug treatment. This cortical zone could be critical for regulating negative emotional valence and anxiety in decision-making.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

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The pregenual anterior cingulate cortex (pACC) has been implicated in human anxiety disorders and depression, but the circuit-level mechanisms underlying these disorders are unclear. In healthy individuals, the pACC is involved in cost-benefit evaluation. We developed a macaque version of an approach-avoidance decision task used to evaluate anxiety and depression in humans and, with multi-electrode recording and cortical microstimulation, we probed pACC function as monkeys performed this task. We found that the macaque pACC has an opponent process-like organization of neurons representing motivationally positive and negative subjective value. Spatial distribution of these two neuronal populations overlapped in the pACC, except in one subzone, where neurons with negative coding were more numerous. Notably, microstimulation in this subzone, but not elsewhere in the pACC, increased negative decision-making, and this negative biasing was blocked by anti-anxiety drug treatment. This cortical zone could be critical for regulating negative emotional valence and anxiety in decision-making.

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  • doi:10.1038/nn.3088

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Timothy J. Buschman; Eric L. Denovellis; Cinira Diogo; Daniel Bullock; Earl K. Miller

Synchronous oscillatory neural ensembles for rules in the prefrontal cortex Journal Article

In: Neuron, vol. 76, no. 4, pp. 838–846, 2012.

Abstract | Links | BibTeX

@article{Buschman2012,
title = {Synchronous oscillatory neural ensembles for rules in the prefrontal cortex},
author = {Timothy J. Buschman and Eric L. Denovellis and Cinira Diogo and Daniel Bullock and Earl K. Miller},
doi = {10.1016/j.neuron.2012.09.029},
year = {2012},
date = {2012-01-01},
journal = {Neuron},
volume = {76},
number = {4},
pages = {838--846},
publisher = {Elsevier Inc.},
abstract = {Intelligent behavior requires acquiring and following rules. Rules define how our behavior should fit different situations. To understand its neural mechanisms, we simultaneously recorded from multiple electrodes in dorsolateral prefrontal cortex (PFC) while monkeys switched between two rules (respond to color versus orientation). We found evidence that oscillatory synchronization of local field potentials (LFPs) formed neural ensembles representing the rules: there were rule-specific increases in synchrony at " beta" (19-40 Hz) frequencies between electrodes. In addition, individual PFC neurons synchronized to the LFP ensemble corresponding to the current rule (color versus orientation). Furthermore, the ensemble encoding the behaviorally dominant orientation rule showed increased " alpha" (6-16 Hz) synchrony when preparing to apply the alternative (weaker) color rule. This suggests that beta-frequency synchrony selects the relevant rule ensemble, while alpha-frequency synchrony deselects a stronger, but currently irrelevant, ensemble. Synchrony may act to dynamically shape task-relevant neural ensembles out of larger, overlapping circuits.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

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Intelligent behavior requires acquiring and following rules. Rules define how our behavior should fit different situations. To understand its neural mechanisms, we simultaneously recorded from multiple electrodes in dorsolateral prefrontal cortex (PFC) while monkeys switched between two rules (respond to color versus orientation). We found evidence that oscillatory synchronization of local field potentials (LFPs) formed neural ensembles representing the rules: there were rule-specific increases in synchrony at " beta" (19-40 Hz) frequencies between electrodes. In addition, individual PFC neurons synchronized to the LFP ensemble corresponding to the current rule (color versus orientation). Furthermore, the ensemble encoding the behaviorally dominant orientation rule showed increased " alpha" (6-16 Hz) synchrony when preparing to apply the alternative (weaker) color rule. This suggests that beta-frequency synchrony selects the relevant rule ensemble, while alpha-frequency synchrony deselects a stronger, but currently irrelevant, ensemble. Synchrony may act to dynamically shape task-relevant neural ensembles out of larger, overlapping circuits.

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  • doi:10.1016/j.neuron.2012.09.029

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Brittany N. Bushnell; Anitha Pasupathy

Shape encoding consistency across colors in primate V4 Journal Article

In: Journal of Neurophysiology, vol. 108, no. 5, pp. 1299–1308, 2012.

Abstract | Links | BibTeX

@article{Bushnell2012,
title = {Shape encoding consistency across colors in primate V4},
author = {Brittany N. Bushnell and Anitha Pasupathy},
doi = {10.1152/jn.01063.2011},
year = {2012},
date = {2012-01-01},
journal = {Journal of Neurophysiology},
volume = {108},
number = {5},
pages = {1299--1308},
abstract = {Neurons in primate cortical area V4 are sensitive to the form and color of visual stimuli. To determine whether form selectivity remains consistent across colors, we studied the responses of single V4 neurons in awake monkeys to a set of two-dimensional shapes presented in two different colors. For each neuron, we chose two colors that were visually distinct and that evoked reliable and different responses. Across neurons, the correlation coefficient between responses in the two colors ranged from -0.03 to 0.93 (median 0.54). Neurons with highly consistent shape responses, i.e., high correlation coefficients, showed greater dispersion in their responses to the different shapes, i.e., greater shape selectivity, and also tended to have less eccentric receptive field locations; among shape-selective neurons, shape consistency ranged from 0.16 to 0.93 (median 0.63). Consistency of shape responses was independent of the physical difference between the stimulus colors used and the strength of neuronal color tuning. Finally, we found that our measurement of shape response consistency was strongly influenced by the number of stimulus repeats: consistency estimates based on fewer than 10 repeats were substantially underestimated. In conclusion, our results suggest that neurons that are likely to contribute to shape perception and discrimination exhibit shape responses that are largely consistent across colors, facilitating the use of simpler algorithms for decoding shape information from V4 neuronal populations.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

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Neurons in primate cortical area V4 are sensitive to the form and color of visual stimuli. To determine whether form selectivity remains consistent across colors, we studied the responses of single V4 neurons in awake monkeys to a set of two-dimensional shapes presented in two different colors. For each neuron, we chose two colors that were visually distinct and that evoked reliable and different responses. Across neurons, the correlation coefficient between responses in the two colors ranged from -0.03 to 0.93 (median 0.54). Neurons with highly consistent shape responses, i.e., high correlation coefficients, showed greater dispersion in their responses to the different shapes, i.e., greater shape selectivity, and also tended to have less eccentric receptive field locations; among shape-selective neurons, shape consistency ranged from 0.16 to 0.93 (median 0.63). Consistency of shape responses was independent of the physical difference between the stimulus colors used and the strength of neuronal color tuning. Finally, we found that our measurement of shape response consistency was strongly influenced by the number of stimulus repeats: consistency estimates based on fewer than 10 repeats were substantially underestimated. In conclusion, our results suggest that neurons that are likely to contribute to shape perception and discrimination exhibit shape responses that are largely consistent across colors, facilitating the use of simpler algorithms for decoding shape information from V4 neuronal populations.

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  • doi:10.1152/jn.01063.2011

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X. Cai; Camillo Padoa-Schioppa

Neuronal encoding of subjective value in dorsal and ventral anterior cingulate cortex Journal Article

In: Journal of Neuroscience, vol. 32, no. 11, pp. 3791–3808, 2012.

Abstract | Links | BibTeX

@article{Cai2012,
title = {Neuronal encoding of subjective value in dorsal and ventral anterior cingulate cortex},
author = {X. Cai and Camillo Padoa-Schioppa},
doi = {10.1523/JNEUROSCI.3864-11.2012},
year = {2012},
date = {2012-01-01},
journal = {Journal of Neuroscience},
volume = {32},
number = {11},
pages = {3791--3808},
abstract = {We examined the activity of individual cells in the primate anterior cingulate cortex during an economic choice task. In the experiments, monkeys chose between different juices offered in variables amounts and subjective values were inferred from the animals' choices. We analyzed neuronal firing rates in relation to a large number of behaviorally relevant variables. We report three main results. First, there were robust differences between the dorsal bank (ACCd) and the ventral bank (ACCv) of the cingulate sulcus. Specifically, neurons in ACCd but not in ACCv were modulated by the movement direction. Furthermore, neurons in ACCd were most active before movement initiation, whereas neurons in ACCv were most active after juice delivery. Second, neurons in both areas encoded the identity and the subjective value of the juice chosen by the animal. In contrast, neither region encoded the value of individual offers. Third, the population of value-encoding neurons in both ACCd and ACCv underwent range adaptation. With respect to economic choice, it is interesting to compare these areas with the orbitofrontal cortex (OFC), previously examined. While neurons in OFC encoded both pre-decision and post-decision variables, neurons in ACCd and ACCv only encoded post-decision variables. Moreover, the encoding of the choice outcome (chosen value and chosen juice) in ACCd and ACCv trailed that found in OFC. These observations indicate that economic decisions (i.e., value comparisons) take place upstream of ACCd and ACCv. The coexistence of choice outcome and movement signals in ACCd suggests that this area constitutes a gateway through which the choice system informs motor systems.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

We examined the activity of individual cells in the primate anterior cingulate cortex during an economic choice task. In the experiments, monkeys chose between different juices offered in variables amounts and subjective values were inferred from the animals' choices. We analyzed neuronal firing rates in relation to a large number of behaviorally relevant variables. We report three main results. First, there were robust differences between the dorsal bank (ACCd) and the ventral bank (ACCv) of the cingulate sulcus. Specifically, neurons in ACCd but not in ACCv were modulated by the movement direction. Furthermore, neurons in ACCd were most active before movement initiation, whereas neurons in ACCv were most active after juice delivery. Second, neurons in both areas encoded the identity and the subjective value of the juice chosen by the animal. In contrast, neither region encoded the value of individual offers. Third, the population of value-encoding neurons in both ACCd and ACCv underwent range adaptation. With respect to economic choice, it is interesting to compare these areas with the orbitofrontal cortex (OFC), previously examined. While neurons in OFC encoded both pre-decision and post-decision variables, neurons in ACCd and ACCv only encoded post-decision variables. Moreover, the encoding of the choice outcome (chosen value and chosen juice) in ACCd and ACCv trailed that found in OFC. These observations indicate that economic decisions (i.e., value comparisons) take place upstream of ACCd and ACCv. The coexistence of choice outcome and movement signals in ACCd suggests that this area constitutes a gateway through which the choice system informs motor systems.

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  • doi:10.1523/JNEUROSCI.3864-11.2012

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Steve W. C. Chang; Joseph W. Barter; R. Becket Ebitz; Karli K. Watson; Michael L. Platt

Inhaled oxytocin amplifies both vicarious reinforcement and self reinforcement in rhesus macaques (Macaca mulatta) Journal Article

In: Proceedings of the National Academy of Sciences, vol. 109, no. 3, pp. 959–964, 2012.

Abstract | Links | BibTeX

@article{Chang2012a,
title = {Inhaled oxytocin amplifies both vicarious reinforcement and self reinforcement in rhesus macaques (Macaca mulatta)},
author = {Steve W. C. Chang and Joseph W. Barter and R. Becket Ebitz and Karli K. Watson and Michael L. Platt},
doi = {10.1073/pnas.1114621109},
year = {2012},
date = {2012-01-01},
journal = {Proceedings of the National Academy of Sciences},
volume = {109},
number = {3},
pages = {959--964},
abstract = {People attend not only to their own experiences, but also to the experiences of those around them. Such social awareness profoundly influences human behavior by enabling observational learning, as well as by motivating cooperation, charity, empathy, and spite. Oxytocin (OT), a neurosecretory hormone synthesized by hypothalamic neurons in the mammalian brain, can enhance affiliation or boost exclusion in different species in distinct contexts, belying any simple mechanistic neural model. Here we show that inhaled OT penetrates the CNS and subsequently enhances the sensitivity of rhesus macaques to rewards occurring to others as well as themselves. Roughly 2 h after inhaling OT, monkeys increased the frequency of prosocial choices associated with reward to another monkey when the alternative was to reward no one. OT also increased attention to the recipient monkey as well as the time it took to render such a decision. In contrast, within the first 2 h following inhalation, OT increased selfish choices associated with delivery of reward to self over a reward to the other monkey, without affecting attention or decision latency. Despite the differences in species typical social behavior, exogenous, inhaled OT causally promotes social donation behavior in rhesus monkeys, as it does in more egalitarian and monogamous ones, like prairie voles and humans, when there is no perceived cost to self. These findings potentially implicate shared neural mechanisms.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

People attend not only to their own experiences, but also to the experiences of those around them. Such social awareness profoundly influences human behavior by enabling observational learning, as well as by motivating cooperation, charity, empathy, and spite. Oxytocin (OT), a neurosecretory hormone synthesized by hypothalamic neurons in the mammalian brain, can enhance affiliation or boost exclusion in different species in distinct contexts, belying any simple mechanistic neural model. Here we show that inhaled OT penetrates the CNS and subsequently enhances the sensitivity of rhesus macaques to rewards occurring to others as well as themselves. Roughly 2 h after inhaling OT, monkeys increased the frequency of prosocial choices associated with reward to another monkey when the alternative was to reward no one. OT also increased attention to the recipient monkey as well as the time it took to render such a decision. In contrast, within the first 2 h following inhalation, OT increased selfish choices associated with delivery of reward to self over a reward to the other monkey, without affecting attention or decision latency. Despite the differences in species typical social behavior, exogenous, inhaled OT causally promotes social donation behavior in rhesus monkeys, as it does in more egalitarian and monogamous ones, like prairie voles and humans, when there is no perceived cost to self. These findings potentially implicate shared neural mechanisms.

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  • doi:10.1073/pnas.1114621109

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Jan Churan; Daniel Guitton; Christopher C. Pack

Perisaccadic remapping and rescaling of visual responses in macaque superior colliculus Journal Article

In: PLoS ONE, vol. 7, no. 12, pp. e52195, 2012.

Abstract | Links | BibTeX

@article{Churan2012,
title = {Perisaccadic remapping and rescaling of visual responses in macaque superior colliculus},
author = {Jan Churan and Daniel Guitton and Christopher C. Pack},
doi = {10.1371/journal.pone.0052195},
year = {2012},
date = {2012-01-01},
journal = {PLoS ONE},
volume = {7},
number = {12},
pages = {e52195},
publisher = {10. 1371/journal.pone.0052195},
address = {e52195. doi},
abstract = {Visual neurons have spatial receptive fields that encode the positions of objects relative to the fovea. Because foveate animals execute frequent saccadic eye movements, this position information is constantly changing, even though the visual world is generally stationary. Interestingly, visual receptive fields in many brain regions have been found to exhibit changes in strength, size, or position around the time of each saccade, and these changes have often been suggested to be involved in the maintenance of perceptual stability. Crucial to the circuitry underlying perisaccadic changes in visual receptive fields is the superior colliculus (SC), a brainstem structure responsible for integrating visual and oculomotor signals. In this work we have studied the time-course of receptive field changes in the SC. We find that the distribution of the latencies of SC responses to stimuli placed outside the fixation receptive field is bimodal: The first mode is comprised of early responses that are temporally locked to the onset of the visual probe stimulus and stronger for probes placed closer to the classical receptive field. We suggest that such responses are therefore consistent with a perisaccadic rescaling, or enhancement, of weak visual responses within a fixed spatial receptive field. The second mode is more similar to the remapping that has been reported in the cortex, as responses are time-locked to saccade onset and stronger for stimuli placed in the postsaccadic receptive field location. We suggest that these two temporal phases of spatial updating may represent different sources of input to the SC.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

Visual neurons have spatial receptive fields that encode the positions of objects relative to the fovea. Because foveate animals execute frequent saccadic eye movements, this position information is constantly changing, even though the visual world is generally stationary. Interestingly, visual receptive fields in many brain regions have been found to exhibit changes in strength, size, or position around the time of each saccade, and these changes have often been suggested to be involved in the maintenance of perceptual stability. Crucial to the circuitry underlying perisaccadic changes in visual receptive fields is the superior colliculus (SC), a brainstem structure responsible for integrating visual and oculomotor signals. In this work we have studied the time-course of receptive field changes in the SC. We find that the distribution of the latencies of SC responses to stimuli placed outside the fixation receptive field is bimodal: The first mode is comprised of early responses that are temporally locked to the onset of the visual probe stimulus and stronger for probes placed closer to the classical receptive field. We suggest that such responses are therefore consistent with a perisaccadic rescaling, or enhancement, of weak visual responses within a fixed spatial receptive field. The second mode is more similar to the remapping that has been reported in the cortex, as responses are time-locked to saccade onset and stronger for stimuli placed in the postsaccadic receptive field location. We suggest that these two temporal phases of spatial updating may represent different sources of input to the SC.

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  • doi:10.1371/journal.pone.0052195

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T. S. Davis; R. A. Parker; Paul A. House; E. Bagley; S. Wendelken; R. A. Normann; Bradley Greger

Spatial and temporal characteristics of V1 microstimulation during chronic implantation of a microelectrode array in a behaving macaque Journal Article

In: Journal of Neural Engineering, vol. 9, no. 6, pp. 1–12, 2012.

Abstract | Links | BibTeX

@article{Davis2012,
title = {Spatial and temporal characteristics of V1 microstimulation during chronic implantation of a microelectrode array in a behaving macaque},
author = {T. S. Davis and R. A. Parker and Paul A. House and E. Bagley and S. Wendelken and R. A. Normann and Bradley Greger},
doi = {10.1088/1741-2560/9/6/065003},
year = {2012},
date = {2012-01-01},
journal = {Journal of Neural Engineering},
volume = {9},
number = {6},
pages = {1--12},
abstract = {OBJECTIVE: It has been hypothesized that a vision prosthesis capable of evoking useful visual percepts can be based upon electrically stimulating the primary visual cortex (V1) of a blind human subject via penetrating microelectrode arrays. As a continuation of earlier work, we examined several spatial and temporal characteristics of V1 microstimulation. APPROACH: An array of 100 penetrating microelectrodes was chronically implanted in V1 of a behaving macaque monkey. Microstimulation thresholds were measured using a two-alternative forced choice detection task. Relative locations of electrically-evoked percepts were measured using a memory saccade-to-target task. MAIN RESULTS: The principal finding was that two years after implantation we were able to evoke behavioural responses to electric stimulation across the spatial extent of the array using groups of contiguous electrodes. Consistent responses to stimulation were evoked at an average threshold current per electrode of 204 ± 49 µA (mean ± std) for groups of four electrodes and 91 ± 25 µA for groups of nine electrodes. Saccades to electrically-evoked percepts using groups of nine electrodes showed that the animal could discriminate spatially distinct percepts with groups having an average separation of 1.6 ± 0.3 mm (mean ± std) in cortex and 1.0° ± 0.2° in visual space. Significance. These results demonstrate chronic perceptual functionality and provide evidence for the feasibility of a cortically-based vision prosthesis for the blind using penetrating microelectrodes.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

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OBJECTIVE: It has been hypothesized that a vision prosthesis capable of evoking useful visual percepts can be based upon electrically stimulating the primary visual cortex (V1) of a blind human subject via penetrating microelectrode arrays. As a continuation of earlier work, we examined several spatial and temporal characteristics of V1 microstimulation. APPROACH: An array of 100 penetrating microelectrodes was chronically implanted in V1 of a behaving macaque monkey. Microstimulation thresholds were measured using a two-alternative forced choice detection task. Relative locations of electrically-evoked percepts were measured using a memory saccade-to-target task. MAIN RESULTS: The principal finding was that two years after implantation we were able to evoke behavioural responses to electric stimulation across the spatial extent of the array using groups of contiguous electrodes. Consistent responses to stimulation were evoked at an average threshold current per electrode of 204 ± 49 µA (mean ± std) for groups of four electrodes and 91 ± 25 µA for groups of nine electrodes. Saccades to electrically-evoked percepts using groups of nine electrodes showed that the animal could discriminate spatially distinct percepts with groups having an average separation of 1.6 ± 0.3 mm (mean ± std) in cortex and 1.0° ± 0.2° in visual space. Significance. These results demonstrate chronic perceptual functionality and provide evidence for the feasibility of a cortically-based vision prosthesis for the blind using penetrating microelectrodes.

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  • doi:10.1088/1741-2560/9/6/065003

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2011

Narcisse P. Bichot; Matthew T. Heard; Robert Desimone

Stimulation of the nucleus accumbens as behavioral reward in awake behaving monkeys Journal Article

In: Journal of Neuroscience Methods, vol. 199, no. 2, pp. 265–272, 2011.

Abstract | Links | BibTeX

@article{Bichot2011,
title = {Stimulation of the nucleus accumbens as behavioral reward in awake behaving monkeys},
author = {Narcisse P. Bichot and Matthew T. Heard and Robert Desimone},
doi = {10.1016/j.jneumeth.2011.05.025},
year = {2011},
date = {2011-01-01},
journal = {Journal of Neuroscience Methods},
volume = {199},
number = {2},
pages = {265--272},
publisher = {Elsevier B.V.},
abstract = {It has been known that monkeys will repeatedly press a bar for electrical stimulation in several different brain structures. We explored the possibility of using electrical stimulation in one such structure, the nucleus accumbens, as a substitute for liquid reward in animals performing a complex task, namely visual search. The animals had full access to water in the cage at all times on days when stimulation was used to motivate them. Electrical stimulation was delivered bilaterally at mirror locations in and around the accumbens, and the animals' motivation to work for electrical stimulation was quantified by the number of trials they performed correctly per unit of time. Acute mapping revealed that stimulation over a large area successfully supported behavioral performance during the task. Performance improved with increasing currents until it reached an asymptotic, theoretically maximal level. Moreover, stimulation with chronically implanted electrodes showed that an animal's motivation to work for electrical stimulation was at least equivalent to, and often better than, when it worked for liquid reward while on water control. These results suggest that electrical stimulation in the accumbens is a viable method of reward in complex tasks. Because this method of reward does not necessitate control over water or food intake, it may offer an alternative to the traditional liquid or food rewards in monkeys, depending on the goals and requirements of the particular research project.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

It has been known that monkeys will repeatedly press a bar for electrical stimulation in several different brain structures. We explored the possibility of using electrical stimulation in one such structure, the nucleus accumbens, as a substitute for liquid reward in animals performing a complex task, namely visual search. The animals had full access to water in the cage at all times on days when stimulation was used to motivate them. Electrical stimulation was delivered bilaterally at mirror locations in and around the accumbens, and the animals' motivation to work for electrical stimulation was quantified by the number of trials they performed correctly per unit of time. Acute mapping revealed that stimulation over a large area successfully supported behavioral performance during the task. Performance improved with increasing currents until it reached an asymptotic, theoretically maximal level. Moreover, stimulation with chronically implanted electrodes showed that an animal's motivation to work for electrical stimulation was at least equivalent to, and often better than, when it worked for liquid reward while on water control. These results suggest that electrical stimulation in the accumbens is a viable method of reward in complex tasks. Because this method of reward does not necessitate control over water or food intake, it may offer an alternative to the traditional liquid or food rewards in monkeys, depending on the goals and requirements of the particular research project.

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  • doi:10.1016/j.jneumeth.2011.05.025

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Brittany N. Bushnell; Philip J. Harding; Yoshito Kosai; Wyeth Bair; Anitha Pasupathy

Equiluminance cells in visual cortical area V4 Journal Article

In: Journal of Neuroscience, vol. 31, no. 35, pp. 12398–12412, 2011.

Abstract | Links | BibTeX

@article{Bushnell2011,
title = {Equiluminance cells in visual cortical area V4},
author = {Brittany N. Bushnell and Philip J. Harding and Yoshito Kosai and Wyeth Bair and Anitha Pasupathy},
doi = {10.1523/JNEUROSCI.1890-11.2011},
year = {2011},
date = {2011-01-01},
journal = {Journal of Neuroscience},
volume = {31},
number = {35},
pages = {12398--12412},
abstract = {We report a novel class of V4 neuron in the macaque monkey that responds selectively to equiluminant colored form. These "equiluminance" cells stand apart because they violate the well established trend throughout the visual system that responses are minimal at low luminance contrast and grow and saturate as contrast increases. Equiluminance cells, which compose ∼22% of V4, exhibit the opposite behavior: responses are greatest near zero contrast and decrease as contrast increases. While equiluminance cells respond preferentially to equiluminant colored stimuli, strong hue tuning is not their distinguishing feature-some equiluminance cells do exhibit strong unimodal hue tuning, but many show little or no tuning for hue. We find that equiluminance cells are color and shape selective to a degree comparable with other classes of V4 cells with more conventional contrast response functions. Those more conventional cells respond equally well to achromatic luminance and equiluminant color stimuli, analogous to color luminance cells described in V1. The existence of equiluminance cells, which have not been reported in V1 or V2, suggests that chromatically defined boundaries and shapes are given special status in V4 and raises the possibility that form at equiluminance and form at higher contrasts are processed in separate channels in V4.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

We report a novel class of V4 neuron in the macaque monkey that responds selectively to equiluminant colored form. These "equiluminance" cells stand apart because they violate the well established trend throughout the visual system that responses are minimal at low luminance contrast and grow and saturate as contrast increases. Equiluminance cells, which compose ∼22% of V4, exhibit the opposite behavior: responses are greatest near zero contrast and decrease as contrast increases. While equiluminance cells respond preferentially to equiluminant colored stimuli, strong hue tuning is not their distinguishing feature-some equiluminance cells do exhibit strong unimodal hue tuning, but many show little or no tuning for hue. We find that equiluminance cells are color and shape selective to a degree comparable with other classes of V4 cells with more conventional contrast response functions. Those more conventional cells respond equally well to achromatic luminance and equiluminant color stimuli, analogous to color luminance cells described in V1. The existence of equiluminance cells, which have not been reported in V1 or V2, suggests that chromatically defined boundaries and shapes are given special status in V4 and raises the possibility that form at equiluminance and form at higher contrasts are processed in separate channels in V4.

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  • doi:10.1523/JNEUROSCI.1890-11.2011

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Brittany N. Bushnell; Philip J. Harding; Yoshito Kosai; Anitha Pasupathy

Partial occlusion modulates contour-based shape encoding in primate area V4 Journal Article

In: Journal of Neuroscience, vol. 31, no. 11, pp. 4012–4024, 2011.

Abstract | Links | BibTeX

@article{Bushnell2011a,
title = {Partial occlusion modulates contour-based shape encoding in primate area V4},
author = {Brittany N. Bushnell and Philip J. Harding and Yoshito Kosai and Anitha Pasupathy},
doi = {10.1523/JNEUROSCI.4766-10.2011},
year = {2011},
date = {2011-01-01},
journal = {Journal of Neuroscience},
volume = {31},
number = {11},
pages = {4012--4024},
abstract = {Past studies of shape coding in visual cortical area V4 have demonstrated that neurons can accurately represent isolated shapes in terms of their component contour features. However, rich natural scenes contain many partially occluded objects, which have "accidental" contours at the junction between the occluded and occluding objects. These contours do not represent the true shape of the occluded object and are known to be perceptually discounted. To discover whether V4 neurons differentially encode accidental contours, we studied the responses of single neurons in fixating monkeys to complex shapes and contextual stimuli presented either in isolation or adjoining each other to provide a percept of partial occlusion. Responses to preferred contours were suppressed when the adjoining context rendered those contours accidental. The observed suppression was reversed when the partial occlusion percept was compromised by introducing a small gap between the component stimuli. Control experiments demonstrated that these results likely depend on contour geometry at T-junctions and cannot be attributed to mechanisms based solely on local color/luminance contrast, spatial proximity of stimuli, or the spatial frequency content of images. Our findings provide novel insights into how occluded objects, which are fundamental to complex visual scenes, are encoded in area V4. They also raise the possibility that the weakened encoding of accidental contours at the junction between objects could mark the first step of image segmentation along the ventral visual pathway.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

Past studies of shape coding in visual cortical area V4 have demonstrated that neurons can accurately represent isolated shapes in terms of their component contour features. However, rich natural scenes contain many partially occluded objects, which have "accidental" contours at the junction between the occluded and occluding objects. These contours do not represent the true shape of the occluded object and are known to be perceptually discounted. To discover whether V4 neurons differentially encode accidental contours, we studied the responses of single neurons in fixating monkeys to complex shapes and contextual stimuli presented either in isolation or adjoining each other to provide a percept of partial occlusion. Responses to preferred contours were suppressed when the adjoining context rendered those contours accidental. The observed suppression was reversed when the partial occlusion percept was compromised by introducing a small gap between the component stimuli. Control experiments demonstrated that these results likely depend on contour geometry at T-junctions and cannot be attributed to mechanisms based solely on local color/luminance contrast, spatial proximity of stimuli, or the spatial frequency content of images. Our findings provide novel insights into how occluded objects, which are fundamental to complex visual scenes, are encoded in area V4. They also raise the possibility that the weakened encoding of accidental contours at the junction between objects could mark the first step of image segmentation along the ventral visual pathway.

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  • doi:10.1523/JNEUROSCI.4766-10.2011

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Steve W. C. Chang; Amy A. Winecoff; Michael L. Platt

Vicarious reinforcement in rhesus macaques (Macaca mulatta) Journal Article

In: Frontiers in Neuroscience, vol. 5, pp. 27, 2011.

Abstract | Links | BibTeX

@article{Chang2011,
title = {Vicarious reinforcement in rhesus macaques (Macaca mulatta)},
author = {Steve W. C. Chang and Amy A. Winecoff and Michael L. Platt},
doi = {10.3389/fnins.2011.00027},
year = {2011},
date = {2011-01-01},
journal = {Frontiers in Neuroscience},
volume = {5},
pages = {27},
abstract = {What happens to others profoundly influences our own behavior. Such other-regarding outcomes can drive observational learning, as well as motivate cooperation, charity, empathy, and even spite. Vicarious reinforcement may serve as one of the critical mechanisms mediating the influence of other-regarding outcomes on behavior and decision-making in groups. Here we show that rhesus macaques spontaneously derive vicarious reinforcement from observing rewards given to another monkey, and that this reinforcement can motivate them to subsequently deliver or withhold rewards from the other animal. We exploited Pavlovian and instrumental conditioning to associate rewards to self (M1) and/or rewards to another monkey (M2) with visual cues. M1s made more errors in the instrumental trials when cues predicted reward to M2 compared to when cues predicted reward to M1, but made even more errors when cues predicted reward to no one. In subsequent preference tests between pairs of conditioned cues, M1s preferred cues paired with reward to M2 over cues paired with reward to no one. By contrast, M1s preferred cues paired with reward to self over cues paired with reward to both monkeys simultaneously. Rates of attention to M2 strongly predicted the strength and valence of vicarious reinforcement. These patterns of behavior, which were absent in non-social control trials, are consistent with vicarious reinforcement based upon sensitivity to observed, or counterfactual, outcomes with respect to another individual. Vicarious reward may play a critical role in shaping cooperation and competition, as well as motivating observational learning and group coordination in rhesus macaques, much as it does in humans. We propose that vicarious reinforcement signals mediate these behaviors via homologous neural circuits involved in reinforcement learning and decision-making.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

What happens to others profoundly influences our own behavior. Such other-regarding outcomes can drive observational learning, as well as motivate cooperation, charity, empathy, and even spite. Vicarious reinforcement may serve as one of the critical mechanisms mediating the influence of other-regarding outcomes on behavior and decision-making in groups. Here we show that rhesus macaques spontaneously derive vicarious reinforcement from observing rewards given to another monkey, and that this reinforcement can motivate them to subsequently deliver or withhold rewards from the other animal. We exploited Pavlovian and instrumental conditioning to associate rewards to self (M1) and/or rewards to another monkey (M2) with visual cues. M1s made more errors in the instrumental trials when cues predicted reward to M2 compared to when cues predicted reward to M1, but made even more errors when cues predicted reward to no one. In subsequent preference tests between pairs of conditioned cues, M1s preferred cues paired with reward to M2 over cues paired with reward to no one. By contrast, M1s preferred cues paired with reward to self over cues paired with reward to both monkeys simultaneously. Rates of attention to M2 strongly predicted the strength and valence of vicarious reinforcement. These patterns of behavior, which were absent in non-social control trials, are consistent with vicarious reinforcement based upon sensitivity to observed, or counterfactual, outcomes with respect to another individual. Vicarious reward may play a critical role in shaping cooperation and competition, as well as motivating observational learning and group coordination in rhesus macaques, much as it does in humans. We propose that vicarious reinforcement signals mediate these behaviors via homologous neural circuits involved in reinforcement learning and decision-making.

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  • doi:10.3389/fnins.2011.00027

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Jan Churan; Daniel Guitton; Christopher C. Pack

Context dependence of receptive field remapping in superior colliculus Journal Article

In: Journal of Neurophysiology, vol. 106, no. 4, pp. 1862–1874, 2011.

Abstract | Links | BibTeX

@article{Churan2011,
title = {Context dependence of receptive field remapping in superior colliculus},
author = {Jan Churan and Daniel Guitton and Christopher C. Pack},
doi = {10.1152/jn.00288.2011},
year = {2011},
date = {2011-01-01},
journal = {Journal of Neurophysiology},
volume = {106},
number = {4},
pages = {1862--1874},
abstract = {Our perception of the positions of objects in our surroundings is surprisingly unaffected by movements of the eyes, head, and body. This suggests that the brain has a mechanism for maintaining perceptual stability, based either on the spatial relationships among visible objects or internal copies of its own motor commands. Strong evidence for the latter mechanism comes from the remapping of visual receptive fields that occurs around the time of a saccade. Remapping occurs when a single neuron responds to visual stimuli placed presaccadically in the spatial location that will be occupied by its receptive field after the completion of a saccade. Although evidence for remapping has been found in many brain areas, relatively little is known about how it interacts with sensory context. This interaction is important for understanding perceptual stability more generally, as the brain may rely on extraretinal signals or visual signals to different degrees in different contexts. Here, we have studied the interaction between visual stimulation and remapping by recording from single neurons in the superior colliculus of the macaque monkey, using several different visual stimulus conditions. We find that remapping responses are highly sensitive to low-level visual signals, with the overall luminance of the visual background exerting a particularly powerful influence. Specifically, although remapping was fairly common in complete darkness, such responses were usually decreased or abolished in the presence of modest background illumination. Thus the brain might make use of a strategy that emphasizes visual landmarks over extraretinal signals whenever the former are available.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

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Our perception of the positions of objects in our surroundings is surprisingly unaffected by movements of the eyes, head, and body. This suggests that the brain has a mechanism for maintaining perceptual stability, based either on the spatial relationships among visible objects or internal copies of its own motor commands. Strong evidence for the latter mechanism comes from the remapping of visual receptive fields that occurs around the time of a saccade. Remapping occurs when a single neuron responds to visual stimuli placed presaccadically in the spatial location that will be occupied by its receptive field after the completion of a saccade. Although evidence for remapping has been found in many brain areas, relatively little is known about how it interacts with sensory context. This interaction is important for understanding perceptual stability more generally, as the brain may rely on extraretinal signals or visual signals to different degrees in different contexts. Here, we have studied the interaction between visual stimulation and remapping by recording from single neurons in the superior colliculus of the macaque monkey, using several different visual stimulus conditions. We find that remapping responses are highly sensitive to low-level visual signals, with the overall luminance of the visual background exerting a particularly powerful influence. Specifically, although remapping was fairly common in complete darkness, such responses were usually decreased or abolished in the presence of modest background illumination. Thus the brain might make use of a strategy that emphasizes visual landmarks over extraretinal signals whenever the former are available.

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  • doi:10.1152/jn.00288.2011

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Michael J. Koval; Stephen G. Lomber; Stefan Everling

Prefrontal cortex deactivation in macaques alters activity in the superior colliculus and impairs voluntary control of saccades Journal Article

In: Journal of Neuroscience, vol. 31, no. 23, pp. 8659–8668, 2011.

Abstract | Links | BibTeX

@article{Koval2011,
title = {Prefrontal cortex deactivation in macaques alters activity in the superior colliculus and impairs voluntary control of saccades},
author = {Michael J. Koval and Stephen G. Lomber and Stefan Everling},
doi = {10.1523/JNEUROSCI.1258-11.2011},
year = {2011},
date = {2011-01-01},
journal = {Journal of Neuroscience},
volume = {31},
number = {23},
pages = {8659--8668},
abstract = {The cognitive control of action requires both the suppression of automatic responses to sudden stimuli and the generation of behavior specified by abstract instructions. Though patient, functional imaging and neurophysiological studies have implicated the dorsolateral prefrontal cortex (dlPFC) in these abilities, the mechanism by which the dlPFC exerts this control remains unknown. Here we examined the functional interaction of the dlPFC with the saccade circuitry by deactivating area 46 of the dlPFC and measuring its effects on the activity of single superior colliculus neurons in monkeys performing a cognitive saccade task. Deactivation of the dlPFC reduced preparatory activity and increased stimulus-related activity in these neurons. These changes in neural activity were accompanied by marked decreases in task performance as evidenced by longer reaction times and more task errors. The results suggest that the dlPFC participates in the cognitive control of gaze by suppressing stimulus-evoked automatic saccade programs.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

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The cognitive control of action requires both the suppression of automatic responses to sudden stimuli and the generation of behavior specified by abstract instructions. Though patient, functional imaging and neurophysiological studies have implicated the dorsolateral prefrontal cortex (dlPFC) in these abilities, the mechanism by which the dlPFC exerts this control remains unknown. Here we examined the functional interaction of the dlPFC with the saccade circuitry by deactivating area 46 of the dlPFC and measuring its effects on the activity of single superior colliculus neurons in monkeys performing a cognitive saccade task. Deactivation of the dlPFC reduced preparatory activity and increased stimulus-related activity in these neurons. These changes in neural activity were accompanied by marked decreases in task performance as evidenced by longer reaction times and more task errors. The results suggest that the dlPFC participates in the cognitive control of gaze by suppressing stimulus-evoked automatic saccade programs.

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  • doi:10.1523/JNEUROSCI.1258-11.2011

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Alexander Maier; Christopher J. Aura; David A. Leopold

Infragranular sources of sustained local field potential responses in macaque primary visual cortex Journal Article

In: Journal of Neuroscience, vol. 31, no. 6, pp. 1971–1980, 2011.

Abstract | Links | BibTeX

@article{Maier2011,
title = {Infragranular sources of sustained local field potential responses in macaque primary visual cortex},
author = {Alexander Maier and Christopher J. Aura and David A. Leopold},
doi = {10.1523/JNEUROSCI.5300-09.2011},
year = {2011},
date = {2011-01-01},
journal = {Journal of Neuroscience},
volume = {31},
number = {6},
pages = {1971--1980},
abstract = {A local field potential (LFP) response can be measured throughout the visual cortex in response to the abrupt appearance of a visual stimulus. Averaging LFP responses to many stimulus presentations isolates transient, phase-locked components of the response that are consistent from trial to trial. However, stimulus responses are also composed of sustained components, which differ in their phase from trial to trial and therefore must be evaluated using other methods, such as computing the power of the response of each trial before averaging. Here, we investigate the basis of phase-locked and non-phase-locked LFP responses in the primary visual cortex of the macaque monkey using a novel variant of current source density (CSD) analysis. We applied a linear array of electrode contacts spanning the thickness of the cortex to measure the LFP and compute band-limited CSD power to identify the laminar sites of persistent current exchange that may be the basis of sustained visual LFP responses. In agreement with previous studies, we found a short-latency phase-locked current sink, thought to correspond to thalamocortical input to layer 4C. In addition, we found a prominent non-phase-locked component of the CSD that persisted as long as the stimulus was physically present. The latter was relatively broadband, lasted throughout the stimulus presentation, and was centered ∼500 $mu$m deeper than the initial current sink. These findings demonstrate a fundamental difference in the neural mechanisms underlying the initial and sustained processing of simple visual stimuli in the V1 microcircuit.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

A local field potential (LFP) response can be measured throughout the visual cortex in response to the abrupt appearance of a visual stimulus. Averaging LFP responses to many stimulus presentations isolates transient, phase-locked components of the response that are consistent from trial to trial. However, stimulus responses are also composed of sustained components, which differ in their phase from trial to trial and therefore must be evaluated using other methods, such as computing the power of the response of each trial before averaging. Here, we investigate the basis of phase-locked and non-phase-locked LFP responses in the primary visual cortex of the macaque monkey using a novel variant of current source density (CSD) analysis. We applied a linear array of electrode contacts spanning the thickness of the cortex to measure the LFP and compute band-limited CSD power to identify the laminar sites of persistent current exchange that may be the basis of sustained visual LFP responses. In agreement with previous studies, we found a short-latency phase-locked current sink, thought to correspond to thalamocortical input to layer 4C. In addition, we found a prominent non-phase-locked component of the CSD that persisted as long as the stimulus was physically present. The latter was relatively broadband, lasted throughout the stimulus presentation, and was centered ∼500 $mu$m deeper than the initial current sink. These findings demonstrate a fundamental difference in the neural mechanisms underlying the initial and sustained processing of simple visual stimuli in the V1 microcircuit.

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  • doi:10.1523/JNEUROSCI.5300-09.2011

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David M. Milstein; Michael C. Dorris

The relationship between saccadic choice and reaction times with manipulations of target value Journal Article

In: Frontiers in Neuroscience, vol. 5, pp. 122, 2011.

Abstract | Links | BibTeX

@article{Milstein2011,
title = {The relationship between saccadic choice and reaction times with manipulations of target value},
author = {David M. Milstein and Michael C. Dorris},
doi = {10.3389/fnins.2011.00122},
year = {2011},
date = {2011-01-01},
journal = {Frontiers in Neuroscience},
volume = {5},
pages = {122},
abstract = {Choosing the option with the highest expected value (EV; reward probability × reward magnitude) maximizes the intake of reward under conditions of uncertainty. However, human economic choices indicate that our value calculation has a subjective component whereby probability and reward magnitude are not linearly weighted. Using a similar economic framework, our goal was to characterize how subjective value influences the generation of simple motor actions. Specifically, we hypothesized that attributes of saccadic eye movements could provide insight into how rhesus monkeys, a well-studied animal model in cognitive neuroscience, subjectively value potential visual targets. In the first experiment, monkeys were free to choose by directing a saccade toward one of two simultaneously displayed targets, each of which had an uncertain outcome. In this task, choices were more likely to be allocated toward the higher valued target. In the second experiment, only one of the two possible targets appeared on each trial. In this task, saccadic reaction times (SRTs) decreased toward the higher valued target. Reward magnitude had a much stronger influence on both choices and SRTs than probability, whose effect was observed only when reward magnitude was similar for both targets. Across EV blocks, a strong relationship was observed between choice preferences and SRTs. However, choices tended to maximize at skewed values whereas SRTs varied more continuously. Lastly, SRTs were unchanged when all reward magnitudes were 1×, 1.5×, and 2× their normal amount, indicating that saccade preparation was influenced by the relative value of the targets rather than the absolute value of any single-target. We conclude that value is not only an important factor( )for deliberative decision making in primates, but also for the selection and preparation of simple motor actions, such as saccadic eye movements. More precisely, our results indicate that, under conditions of uncertainty, saccade choices and reaction times are influenced by the relative expected subjective value of potential movements.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

Choosing the option with the highest expected value (EV; reward probability × reward magnitude) maximizes the intake of reward under conditions of uncertainty. However, human economic choices indicate that our value calculation has a subjective component whereby probability and reward magnitude are not linearly weighted. Using a similar economic framework, our goal was to characterize how subjective value influences the generation of simple motor actions. Specifically, we hypothesized that attributes of saccadic eye movements could provide insight into how rhesus monkeys, a well-studied animal model in cognitive neuroscience, subjectively value potential visual targets. In the first experiment, monkeys were free to choose by directing a saccade toward one of two simultaneously displayed targets, each of which had an uncertain outcome. In this task, choices were more likely to be allocated toward the higher valued target. In the second experiment, only one of the two possible targets appeared on each trial. In this task, saccadic reaction times (SRTs) decreased toward the higher valued target. Reward magnitude had a much stronger influence on both choices and SRTs than probability, whose effect was observed only when reward magnitude was similar for both targets. Across EV blocks, a strong relationship was observed between choice preferences and SRTs. However, choices tended to maximize at skewed values whereas SRTs varied more continuously. Lastly, SRTs were unchanged when all reward magnitudes were 1×, 1.5×, and 2× their normal amount, indicating that saccade preparation was influenced by the relative value of the targets rather than the absolute value of any single-target. We conclude that value is not only an important factor( )for deliberative decision making in primates, but also for the selection and preparation of simple motor actions, such as saccadic eye movements. More precisely, our results indicate that, under conditions of uncertainty, saccade choices and reaction times are influenced by the relative expected subjective value of potential movements.

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  • doi:10.3389/fnins.2011.00122

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Robert Niebergall; Paul S. Khayat; Stefan Treue; Julio C. Martinez-Trujillo

Expansion of MT neurons excitatory receptive fields during covert attentive tracking Journal Article

In: Journal of Neuroscience, vol. 31, no. 43, pp. 15499–15510, 2011.

Abstract | Links | BibTeX

@article{Niebergall2011,
title = {Expansion of MT neurons excitatory receptive fields during covert attentive tracking},
author = {Robert Niebergall and Paul S. Khayat and Stefan Treue and Julio C. Martinez-Trujillo},
doi = {10.1523/JNEUROSCI.2822-11.2011},
year = {2011},
date = {2011-01-01},
journal = {Journal of Neuroscience},
volume = {31},
number = {43},
pages = {15499--15510},
abstract = {Primates can attentively track moving objects while keeping gaze stationary. The neural mechanisms underlying this ability are poorly understood. We investigated this issue by recording responses of neurons in area MT of two rhesus monkeys while they performed two different tasks. During the Attend-Fixation task, two moving random dot patterns (RDPs) translated across a screen at the same speed and in the same direction while the animals directed gaze to a fixation spot and detected a change in its luminance. During the Tracking task, the animals kept gaze on the fixation spot and attentively tracked the two RDPs to report a change in the local speed of one of the patterns' dots. In both conditions, neuronal responses progressively increased as the RDPs entered the neurons' receptive field (RF), peaked when they reached its center, and decreased as they translated away. This response profile was well described by a Gaussian function with its center of gravity indicating the RF center and its flanks the RF excitatory borders. During Tracking, responses were increased relative to Attend-Fixation, causing the Gaussian profiles to expand. Such increases were proportionally larger in the RF periphery than at its center, and were accompanied by a decrease in the trial-to-trial response variability (Fano factor) relative to Attend-Fixation. These changes resulted in an increase in the neurons' performance at detecting targets at longer distances from the RF center. Our results show that attentive tracking dynamically changes MT neurons' RF profiles, ultimately improving the neurons' ability to encode the tracked stimulus features.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

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Primates can attentively track moving objects while keeping gaze stationary. The neural mechanisms underlying this ability are poorly understood. We investigated this issue by recording responses of neurons in area MT of two rhesus monkeys while they performed two different tasks. During the Attend-Fixation task, two moving random dot patterns (RDPs) translated across a screen at the same speed and in the same direction while the animals directed gaze to a fixation spot and detected a change in its luminance. During the Tracking task, the animals kept gaze on the fixation spot and attentively tracked the two RDPs to report a change in the local speed of one of the patterns' dots. In both conditions, neuronal responses progressively increased as the RDPs entered the neurons' receptive field (RF), peaked when they reached its center, and decreased as they translated away. This response profile was well described by a Gaussian function with its center of gravity indicating the RF center and its flanks the RF excitatory borders. During Tracking, responses were increased relative to Attend-Fixation, causing the Gaussian profiles to expand. Such increases were proportionally larger in the RF periphery than at its center, and were accompanied by a decrease in the trial-to-trial response variability (Fano factor) relative to Attend-Fixation. These changes resulted in an increase in the neurons' performance at detecting targets at longer distances from the RF center. Our results show that attentive tracking dynamically changes MT neurons' RF profiles, ultimately improving the neurons' ability to encode the tracked stimulus features.

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  • doi:10.1523/JNEUROSCI.2822-11.2011

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Robert Niebergall; Paul S. Khayat; Stefan Treue; Julio C. Martinez-Trujillo

Multifocal attention filters targets from distracters within and beyond primate mt neurons' receptive field boundaries Journal Article

In: Neuron, vol. 72, no. 6, pp. 1067–1079, 2011.

Abstract | Links | BibTeX

@article{Niebergall2011a,
title = {Multifocal attention filters targets from distracters within and beyond primate mt neurons' receptive field boundaries},
author = {Robert Niebergall and Paul S. Khayat and Stefan Treue and Julio C. Martinez-Trujillo},
doi = {10.1016/j.neuron.2011.10.013},
year = {2011},
date = {2011-01-01},
journal = {Neuron},
volume = {72},
number = {6},
pages = {1067--1079},
publisher = {Elsevier Inc.},
abstract = {Visual attention has been classically described as a spotlight that enhances the processing of a behaviorally relevant object. However, in many situations, humans and animals must simultaneously attend to several relevant objects separated by distracters. To account for this ability, various models of attention have been proposed including splitting of the attentional spotlight into multiple foci, zooming of the spotlight over a region of space, and switching of the spotlight among objects. We investigated this controversial issue by recording neuronal activity in visual area MT of two macaques while they attended to two translating objects that circumvented a third distracter object located inside the neurons' receptive field. We found that when the attended objects passed through or nearby the receptive field, neuronal responses to the distracter were either decreased or remained unaltered. These results demonstrate that attention can split into multiple spotlights corresponding to relevant objects while filtering out interspersed distracters.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

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Visual attention has been classically described as a spotlight that enhances the processing of a behaviorally relevant object. However, in many situations, humans and animals must simultaneously attend to several relevant objects separated by distracters. To account for this ability, various models of attention have been proposed including splitting of the attentional spotlight into multiple foci, zooming of the spotlight over a region of space, and switching of the spotlight among objects. We investigated this controversial issue by recording neuronal activity in visual area MT of two macaques while they attended to two translating objects that circumvented a third distracter object located inside the neurons' receptive field. We found that when the attended objects passed through or nearby the receptive field, neuronal responses to the distracter were either decreased or remained unaltered. These results demonstrate that attention can split into multiple spotlights corresponding to relevant objects while filtering out interspersed distracters.

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  • doi:10.1016/j.neuron.2011.10.013

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Shinji Nishimoto; Jack L. Gallant

A three-dimensional spatiotemporal receptive field model explains responses of area MT neurons to naturalistic movies Journal Article

In: Journal of Neuroscience, vol. 31, no. 41, pp. 14551–14564, 2011.

Abstract | Links | BibTeX

@article{Nishimoto2011,
title = {A three-dimensional spatiotemporal receptive field model explains responses of area MT neurons to naturalistic movies},
author = {Shinji Nishimoto and Jack L. Gallant},
doi = {10.1523/JNEUROSCI.6801-10.2011},
year = {2011},
date = {2011-01-01},
journal = {Journal of Neuroscience},
volume = {31},
number = {41},
pages = {14551--14564},
abstract = {Area MT has been an important target for studies of motion processing. However, previous neurophysiological studies of MT have used simple stimuli that do not contain many of the motion signals that occur during natural vision. In this study we sought to determine whether views of area MT neurons developed using simple stimuli can account for MT responses under more naturalistic conditions. We recorded responses from macaque area MT neurons during stimulation with naturalistic movies. We then used a quantitative modeling framework to discover which specific mechanisms best predict neuronal responses under these challenging conditions. We find that the simplest model that accurately predicts responses of MT neurons consists of a bank of V1-like filters, each followed by a compressive nonlinearity, a divisive nonlinearity, and linear pooling. Inspection of the fit models shows that the excitatory receptive fields of MT neurons tend to lie on a single plane within the three-dimensional spatiotemporal frequency domain, and suppressive receptive fields lie off this plane. However, most excitatory receptive fields form a partial ring in the plane and avoid low temporal frequencies. This receptive field organization ensures that most MT neurons are tuned for velocity but do not tend to respond to ambiguous static textures that are aligned with the direction of motion. In sum, MT responses to naturalistic movies are largely consistent with predictions based on simple stimuli. However, models fit using naturalistic stimuli reveal several novel properties of MT receptive fields that had not been shown in prior experiments.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

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Area MT has been an important target for studies of motion processing. However, previous neurophysiological studies of MT have used simple stimuli that do not contain many of the motion signals that occur during natural vision. In this study we sought to determine whether views of area MT neurons developed using simple stimuli can account for MT responses under more naturalistic conditions. We recorded responses from macaque area MT neurons during stimulation with naturalistic movies. We then used a quantitative modeling framework to discover which specific mechanisms best predict neuronal responses under these challenging conditions. We find that the simplest model that accurately predicts responses of MT neurons consists of a bank of V1-like filters, each followed by a compressive nonlinearity, a divisive nonlinearity, and linear pooling. Inspection of the fit models shows that the excitatory receptive fields of MT neurons tend to lie on a single plane within the three-dimensional spatiotemporal frequency domain, and suppressive receptive fields lie off this plane. However, most excitatory receptive fields form a partial ring in the plane and avoid low temporal frequencies. This receptive field organization ensures that most MT neurons are tuned for velocity but do not tend to respond to ambiguous static textures that are aligned with the direction of motion. In sum, MT responses to naturalistic movies are largely consistent with predictions based on simple stimuli. However, models fit using naturalistic stimuli reveal several novel properties of MT receptive fields that had not been shown in prior experiments.

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  • doi:10.1523/JNEUROSCI.6801-10.2011

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Anna Oleksiak; P. Christiaan Klink; Albert Postma; Ineke J. M. Ham; Martin J. Lankheet; Richard J. A. Wezel

Spatial summation in macaque parietal area 7a follows a winner-take-all rule Journal Article

In: Journal of Neurophysiology, vol. 105, no. 3, pp. 1150–1158, 2011.

Abstract | Links | BibTeX

@article{Oleksiak2011,
title = {Spatial summation in macaque parietal area 7a follows a winner-take-all rule},
author = {Anna Oleksiak and P. Christiaan Klink and Albert Postma and Ineke J. M. Ham and Martin J. Lankheet and Richard J. A. Wezel},
doi = {10.1152/jn.00907.2010},
year = {2011},
date = {2011-01-01},
journal = {Journal of Neurophysiology},
volume = {105},
number = {3},
pages = {1150--1158},
abstract = {While neurons in posterior parietal cortex have been found to signal the presence of a salient stimulus among multiple items in a display, spatial summation within their receptive field in the absence of an attentional bias has never been investigated. This information, however, is indispensable when one investigates the mechanisms of spatial attention and competition between multiple visual objects. To examine the spatial summation rule in parietal area 7a neurons, we trained rhesus monkeys to fixate on a central cross while two identical stimuli were briefly displayed in a neuron's receptive field. The response to a pair of dots was compared with the responses to the same dots when they were presented individually. The scaling and power parameters of a generalized summation algorithm varied greatly, both across neurons and across combinations of stimulus locations. However, the averaged response of the recorded population of 7a neurons was consistent with a winner-take-all rule for spatial summation. A control experiment where a monkey covertly attended to both stimuli simultaneously suggests that attention introduces additional competition by facilitating the less optimal stimulus. Thus an averaging stage is introduced between ∼ 200 and 300 ms of the response to a pair of stimuli. In short, the summation algorithm over the population of area 7a neurons carries the signature of a winner-take-all operation, with spatial attention possibly influencing the temporal dynamics of stimulus competition, that is the moment that the "winner" takes "victory" over the "loser" stimulus.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

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While neurons in posterior parietal cortex have been found to signal the presence of a salient stimulus among multiple items in a display, spatial summation within their receptive field in the absence of an attentional bias has never been investigated. This information, however, is indispensable when one investigates the mechanisms of spatial attention and competition between multiple visual objects. To examine the spatial summation rule in parietal area 7a neurons, we trained rhesus monkeys to fixate on a central cross while two identical stimuli were briefly displayed in a neuron's receptive field. The response to a pair of dots was compared with the responses to the same dots when they were presented individually. The scaling and power parameters of a generalized summation algorithm varied greatly, both across neurons and across combinations of stimulus locations. However, the averaged response of the recorded population of 7a neurons was consistent with a winner-take-all rule for spatial summation. A control experiment where a monkey covertly attended to both stimuli simultaneously suggests that attention introduces additional competition by facilitating the less optimal stimulus. Thus an averaging stage is introduced between ∼ 200 and 300 ms of the response to a pair of stimuli. In short, the summation algorithm over the population of area 7a neurons carries the signature of a winner-take-all operation, with spatial attention possibly influencing the temporal dynamics of stimulus competition, that is the moment that the "winner" takes "victory" over the "loser" stimulus.

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  • doi:10.1152/jn.00907.2010

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K. Torab; T. S. Davis; D. J. Warren; Paul A. House; R. A. Normann; Bradley Greger

Multiple factors may influence the performance of a visual prosthesis based on intracortical microstimulation: Nonhuman primate behavioural experimentation Journal Article

In: Journal of Neural Engineering, vol. 8, no. 3, pp. 1–13, 2011.

Abstract | Links | BibTeX

@article{Torab2011,
title = {Multiple factors may influence the performance of a visual prosthesis based on intracortical microstimulation: Nonhuman primate behavioural experimentation},
author = {K. Torab and T. S. Davis and D. J. Warren and Paul A. House and R. A. Normann and Bradley Greger},
doi = {10.1088/1741-2560/8/3/035001},
year = {2011},
date = {2011-01-01},
journal = {Journal of Neural Engineering},
volume = {8},
number = {3},
pages = {1--13},
publisher = {10},
address = {doi},
abstract = {We hypothesize that a visual prosthesis capable of evoking high-resolution visual perceptions can be produced using high-electrode-count arrays of penetrating microelectrodes implanted into the primary visual cortex of a blind human subject. To explore this hypothesis, and as a prelude to human psychophysical experiments, we have conducted a set of experiments in primary visual cortex (V1) of non-human primates using chronically implanted Utah Electrode Arrays (UEAs). The electrical and recording properties of implanted electrodes, the high-resolution visuotopic organization of V1, and the stimulation levels required to evoke behavioural responses were measured. The impedances of stimulated electrodes were found to drop significantly immediately following stimulation sessions, but these post-stimulation impedances returned to pre-stimulation values by the next experimental session. Two months of periodic microstimulation at currents of up to 96 µA did not impair the mapping of receptive fields from local field potentials or multi-unit activity, or impact behavioural visual thresholds of light stimuli that excited regions of V1 that were implanted with UEAs. These results demonstrate that microstimulation at the levels used did not cause functional impairment of the electrode array or the neural tissue. However, microstimulation with current levels ranging from 18 to 76 µA (46 ± 19 µA, mean ± std) was able to elicit behavioural responses on eight out of 82 systematically stimulated electrodes. We suggest that the ability of microstimulation to evoke phosphenes and elicit a subsequent behavioural response may depend on several factors: the location of the electrode tips within the cortical layers of V1, distance of the electrode tips to neuronal somata, and the inability of nonhuman primates to recognize and respond to a generalized set of evoked percepts.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

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We hypothesize that a visual prosthesis capable of evoking high-resolution visual perceptions can be produced using high-electrode-count arrays of penetrating microelectrodes implanted into the primary visual cortex of a blind human subject. To explore this hypothesis, and as a prelude to human psychophysical experiments, we have conducted a set of experiments in primary visual cortex (V1) of non-human primates using chronically implanted Utah Electrode Arrays (UEAs). The electrical and recording properties of implanted electrodes, the high-resolution visuotopic organization of V1, and the stimulation levels required to evoke behavioural responses were measured. The impedances of stimulated electrodes were found to drop significantly immediately following stimulation sessions, but these post-stimulation impedances returned to pre-stimulation values by the next experimental session. Two months of periodic microstimulation at currents of up to 96 µA did not impair the mapping of receptive fields from local field potentials or multi-unit activity, or impact behavioural visual thresholds of light stimuli that excited regions of V1 that were implanted with UEAs. These results demonstrate that microstimulation at the levels used did not cause functional impairment of the electrode array or the neural tissue. However, microstimulation with current levels ranging from 18 to 76 µA (46 ± 19 µA, mean ± std) was able to elicit behavioural responses on eight out of 82 systematically stimulated electrodes. We suggest that the ability of microstimulation to evoke phosphenes and elicit a subsequent behavioural response may depend on several factors: the location of the electrode tips within the cortical layers of V1, distance of the electrode tips to neuronal somata, and the inability of nonhuman primates to recognize and respond to a generalized set of evoked percepts.

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  • doi:10.1088/1741-2560/8/3/035001

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James M. G. Tsui; Christopher C. Pack

Contrast sensitivity of MT receptive field centers and surrounds Journal Article

In: Journal of Neurophysiology, vol. 106, no. 4, pp. 1888–1900, 2011.

Abstract | Links | BibTeX

@article{Tsui2011,
title = {Contrast sensitivity of MT receptive field centers and surrounds},
author = {James M. G. Tsui and Christopher C. Pack},
doi = {10.1152/jn.00165.2011},
year = {2011},
date = {2011-01-01},
journal = {Journal of Neurophysiology},
volume = {106},
number = {4},
pages = {1888--1900},
abstract = {Neurons throughout the visual system have receptive fields with both excitatory and suppressive components. The latter are responsible for a phenomenon known as surround suppression, in which responses decrease as a stimulus is extended beyond a certain size. Previous work has shown that surround suppression in the primary visual cortex depends strongly on stimulus contrast. Such complex center-surround interactions are thought to relate to a variety of functions, although little is known about how they affect responses in the extrastriate visual cortex. We have therefore examined the interaction of center and surround in the middle temporal (MT) area of the macaque (Macaca mulatta) extrastriate cortex by recording neuronal responses to stimuli of different sizes and contrasts. Our findings indicate that surround suppression in MT is highly contrast dependent, with the strongest suppression emerging unexpectedly at intermediate stimulus contrasts. These results can be explained by a simple model that takes into account the nonlinear contrast sensitivity of the neurons that provide input to MT. The model also provides a qualitative link to previous reports of a topographic organization of area MT based on clusters of neurons with differing surround suppression strength. We show that this organization can be detected in the gamma-band local field potentials (LFPs) and that the model parameters can predict the contrast sensitivity of these LFP responses. Overall our results show that surround suppression in area MT is far more common than previously suspected, highlighting the potential functional importance of the accumulation of nonlinearities along the dorsal visual pathway.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

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Neurons throughout the visual system have receptive fields with both excitatory and suppressive components. The latter are responsible for a phenomenon known as surround suppression, in which responses decrease as a stimulus is extended beyond a certain size. Previous work has shown that surround suppression in the primary visual cortex depends strongly on stimulus contrast. Such complex center-surround interactions are thought to relate to a variety of functions, although little is known about how they affect responses in the extrastriate visual cortex. We have therefore examined the interaction of center and surround in the middle temporal (MT) area of the macaque (Macaca mulatta) extrastriate cortex by recording neuronal responses to stimuli of different sizes and contrasts. Our findings indicate that surround suppression in MT is highly contrast dependent, with the strongest suppression emerging unexpectedly at intermediate stimulus contrasts. These results can be explained by a simple model that takes into account the nonlinear contrast sensitivity of the neurons that provide input to MT. The model also provides a qualitative link to previous reports of a topographic organization of area MT based on clusters of neurons with differing surround suppression strength. We show that this organization can be detected in the gamma-band local field potentials (LFPs) and that the model parameters can predict the contrast sensitivity of these LFP responses. Overall our results show that surround suppression in area MT is far more common than previously suspected, highlighting the potential functional importance of the accumulation of nonlinearities along the dorsal visual pathway.

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  • doi:10.1152/jn.00165.2011

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Joris Vangeneugden; Patrick A. De Maziere; Marc M. Van Hulle; Tobias Jaeggli; Luc Van Van Gool; Rufin Vogels

Distinct mechanisms for coding of visual actions in macaque temporal cortex Journal Article

In: Journal of Neuroscience, vol. 31, no. 2, pp. 385–401, 2011.

Abstract | Links | BibTeX

@article{Vangeneugden2011,
title = {Distinct mechanisms for coding of visual actions in macaque temporal cortex},
author = {Joris Vangeneugden and Patrick A. De Maziere and Marc M. Van Hulle and Tobias Jaeggli and Luc Van Van Gool and Rufin Vogels},
doi = {10.1523/JNEUROSCI.2703-10.2011},
year = {2011},
date = {2011-01-01},
journal = {Journal of Neuroscience},
volume = {31},
number = {2},
pages = {385--401},
abstract = {Temporal cortical neurons are known to respond to visual dynamic-action displays. Many human psychophysical and functional imaging studies examining biological motion perception have used treadmill walking, in contrast to previous macaque single-cell studies. We assessed the coding of locomotion in rhesus monkey (Macacamulatta) temporal cortex using movies of stationary walkers,varying both form and motion (i.e.,different facing directions) or varying only the frame sequence (i.e.,forward vs backward walking). The majority of superiortemporal sulcus and inferior temporal neurons were selective for facing direction, whereas a minority distinguished forward from backward walking. Support vector machines using the temporal cortical population responses as input classified facing direction well, but forward and backward walking less so. Classification performance for the latter improved markedly when the within-action response modulation was considered, reflecting differences in momentarybody poses within the locomotion sequences. Responses to static pose presentations predicted the responses during the course of the action. Analyses of the responses to walking sequences wherein the start frame was varied across trials showed that some neurons also carried a snapshot sequence signal. Such sequence information was present in neurons that responded to static snapshot presen- tations and in neurons that required motion. Our data suggest that actions area nalyzed by temporal cortical neurons using distinct mechanisms. Most neurons predominantly signal momentary pose. In addition, temporal cortical neurons, including those responding to static pose, are sensitive to pose sequence, which can contribute to the signaling oflearned action sequences.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

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Temporal cortical neurons are known to respond to visual dynamic-action displays. Many human psychophysical and functional imaging studies examining biological motion perception have used treadmill walking, in contrast to previous macaque single-cell studies. We assessed the coding of locomotion in rhesus monkey (Macacamulatta) temporal cortex using movies of stationary walkers,varying both form and motion (i.e.,different facing directions) or varying only the frame sequence (i.e.,forward vs backward walking). The majority of superiortemporal sulcus and inferior temporal neurons were selective for facing direction, whereas a minority distinguished forward from backward walking. Support vector machines using the temporal cortical population responses as input classified facing direction well, but forward and backward walking less so. Classification performance for the latter improved markedly when the within-action response modulation was considered, reflecting differences in momentarybody poses within the locomotion sequences. Responses to static pose presentations predicted the responses during the course of the action. Analyses of the responses to walking sequences wherein the start frame was varied across trials showed that some neurons also carried a snapshot sequence signal. Such sequence information was present in neurons that responded to static snapshot presen- tations and in neurons that required motion. Our data suggest that actions area nalyzed by temporal cortical neurons using distinct mechanisms. Most neurons predominantly signal momentary pose. In addition, temporal cortical neurons, including those responding to static pose, are sensitive to pose sequence, which can contribute to the signaling oflearned action sequences.

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  • doi:10.1523/JNEUROSCI.2703-10.2011

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B. -E. Verhoef; Rufin Vogels; Peter Janssen

Synchronization between the end stages of the dorsal and the ventral visual stream Journal Article

In: Journal of Neurophysiology, vol. 105, no. 5, pp. 2030–2042, 2011.

Abstract | Links | BibTeX

@article{Verhoef2011,
title = {Synchronization between the end stages of the dorsal and the ventral visual stream},
author = {B. -E. Verhoef and Rufin Vogels and Peter Janssen},
doi = {10.1152/jn.00924.2010},
year = {2011},
date = {2011-01-01},
journal = {Journal of Neurophysiology},
volume = {105},
number = {5},
pages = {2030--2042},
abstract = {The end stage areas of the ventral (IT) and the dorsal (AIP) visual streams encode the shape of disparity-defined three-dimensional (3D) surfaces. Recent anatomical tracer studies have found direct reciprocal connections between the 3D-shape selective areas in IT and AIP. Whether these anatomical connections are used to facilitate 3D-shape perception is still unknown. We simultaneously recorded multi-unit activity (MUA) and local field potentials in IT and AIP while monkeys discriminated between concave and convex 3D shapes and measured the degree to which the activity in IT and AIP synchronized during the task. We observed strong beta-band synchronization between IT and AIP preceding stimulus onset that decreased shortly after stimulus onset and became modulated by stereo-signal strength and stimulus contrast during the later portion of the stimulus period. The beta-coherence modulation was unrelated to task-difficulty, regionally specific, and dependent on the MUA selectivity of the pairs of sites under study. The beta-spike-field coherence in AIP predicted the upcoming choice of the monkey. Several convergent lines of evidence suggested AIP as the primary source of the AIP-IT synchronized activity. The synchronized beta activity seemed to occur during perceptual anticipation and when the system has stabilized to a particular perceptual state but not during active visual processing. Our findings demonstrate for the first time that synchronized activity exists between the end stages of the dorsal and ventral stream during 3D-shape discrimination.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

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The end stage areas of the ventral (IT) and the dorsal (AIP) visual streams encode the shape of disparity-defined three-dimensional (3D) surfaces. Recent anatomical tracer studies have found direct reciprocal connections between the 3D-shape selective areas in IT and AIP. Whether these anatomical connections are used to facilitate 3D-shape perception is still unknown. We simultaneously recorded multi-unit activity (MUA) and local field potentials in IT and AIP while monkeys discriminated between concave and convex 3D shapes and measured the degree to which the activity in IT and AIP synchronized during the task. We observed strong beta-band synchronization between IT and AIP preceding stimulus onset that decreased shortly after stimulus onset and became modulated by stereo-signal strength and stimulus contrast during the later portion of the stimulus period. The beta-coherence modulation was unrelated to task-difficulty, regionally specific, and dependent on the MUA selectivity of the pairs of sites under study. The beta-spike-field coherence in AIP predicted the upcoming choice of the monkey. Several convergent lines of evidence suggested AIP as the primary source of the AIP-IT synchronized activity. The synchronized beta activity seemed to occur during perceptual anticipation and when the system has stabilized to a particular perceptual state but not during active visual processing. Our findings demonstrate for the first time that synchronized activity exists between the end stages of the dorsal and ventral stream during 3D-shape discrimination.

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  • doi:10.1152/jn.00924.2010

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Ye Wang; Bogdan F. Iliescu; Jianfu Ma; Kresimir Josic; Valentin Dragoi

Adaptive changes in neuronal synchronization in macaque V4 Journal Article

In: Journal of Neuroscience, vol. 31, no. 37, pp. 13204–13213, 2011.

Abstract | Links | BibTeX

@article{Wang2011b,
title = {Adaptive changes in neuronal synchronization in macaque V4},
author = {Ye Wang and Bogdan F. Iliescu and Jianfu Ma and Kresimir Josic and Valentin Dragoi},
doi = {10.1523/JNEUROSCI.6227-10.2011},
year = {2011},
date = {2011-01-01},
journal = {Journal of Neuroscience},
volume = {31},
number = {37},
pages = {13204--13213},
abstract = {A fundamental property of cortical neurons is the capacity to exhibit adaptive changes or plasticity. Whether adaptive changes in cortical responses are accompanied by changes in synchrony between individual neurons and local population activity in sensory cortex is unclear. This issue is important as synchronized neural activity is hypothesized to play an important role in propagating information in neuronal circuits. Here, we show that rapid adaptation (300 ms) to a stimulus of fixed orientation modulates the strength of oscillatory neuronal synchronization in macaque visual cortex (area V4) and influences the ability of neurons to distinguish small changes in stimulus orientation. Specifically, rapid adaptation increases the synchronization of individual neuronal responses with local population activity in the gamma frequency band (30-80 Hz). In contrast to previous reports that gamma synchronization is associated with an increase in firing rates in V4, we found that the postadaptation increase in gamma synchronization is associated with a decrease in neuronal responses. The increase in gamma-band synchronization after adaptation is functionally significant as it is correlated with an improvement in neuronal orientation discrimination performance. Thus, adaptive synchronization between the spiking activity of individual neurons and their local population can enhance temporally insensitive, rate-based-coding schemes for sensory discrimination.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

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A fundamental property of cortical neurons is the capacity to exhibit adaptive changes or plasticity. Whether adaptive changes in cortical responses are accompanied by changes in synchrony between individual neurons and local population activity in sensory cortex is unclear. This issue is important as synchronized neural activity is hypothesized to play an important role in propagating information in neuronal circuits. Here, we show that rapid adaptation (300 ms) to a stimulus of fixed orientation modulates the strength of oscillatory neuronal synchronization in macaque visual cortex (area V4) and influences the ability of neurons to distinguish small changes in stimulus orientation. Specifically, rapid adaptation increases the synchronization of individual neuronal responses with local population activity in the gamma frequency band (30-80 Hz). In contrast to previous reports that gamma synchronization is associated with an increase in firing rates in V4, we found that the postadaptation increase in gamma synchronization is associated with a decrease in neuronal responses. The increase in gamma-band synchronization after adaptation is functionally significant as it is correlated with an improvement in neuronal orientation discrimination performance. Thus, adaptive synchronization between the spiking activity of individual neurons and their local population can enhance temporally insensitive, rate-based-coding schemes for sensory discrimination.

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  • doi:10.1523/JNEUROSCI.6227-10.2011

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Zheng Wang; Anna W. Roe

Trial-to-trial noise cancellation of cortical field potentials in awake macaques by autoregression model with exogenous input (ARX) Journal Article

In: Journal of Neuroscience Methods, vol. 194, no. 2, pp. 266–273, 2011.

Abstract | Links | BibTeX

@article{Wang2011a,
title = {Trial-to-trial noise cancellation of cortical field potentials in awake macaques by autoregression model with exogenous input (ARX)},
author = {Zheng Wang and Anna W. Roe},
doi = {10.1016/j.jneumeth.2010.10.029},
year = {2011},
date = {2011-01-01},
journal = {Journal of Neuroscience Methods},
volume = {194},
number = {2},
pages = {266--273},
publisher = {Elsevier B.V.},
abstract = {Gamma band synchronization has drawn increasing interest with respect to its potential role in neuronal encoding strategy and behavior in awake, behaving animals. However, contamination of these recordings by power line noise can confound the analysis and interpretation of cortical local field potential (LFP). Existing denoising methods are plagued by inadequate noise reduction, inaccuracies, and even introduction of new noise components. To carefully and more completely remove such contamination, we propose an automatic method based on the concept of adaptive noise cancellation that utilizes the correlative features of common noise sources, and implement with AutoRegressive model with eXogenous Input (ARX). We apply this technique to both simulated data and LFPs recorded in the primary visual cortex of awake macaque monkeys. The analyses here demonstrate a greater degree of accurate noise removal than conventional notch filters. Our method leaves desired signal intact and does not introduce artificial noise components. Application of this method to awake monkey V1 recordings reveals a significant power increase in the gamma range evoked by visual stimulation. Our findings suggest that the ARX denoising procedure will be an important pre-processing step in the analysis of large volumes of cortical LFP data as well as high frequency (gamma-band related) electroencephalography/magnetoencephalography (EEG/MEG) applications, one which will help to convincingly dissociate this notorious artifact from gamma-band activity.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

Gamma band synchronization has drawn increasing interest with respect to its potential role in neuronal encoding strategy and behavior in awake, behaving animals. However, contamination of these recordings by power line noise can confound the analysis and interpretation of cortical local field potential (LFP). Existing denoising methods are plagued by inadequate noise reduction, inaccuracies, and even introduction of new noise components. To carefully and more completely remove such contamination, we propose an automatic method based on the concept of adaptive noise cancellation that utilizes the correlative features of common noise sources, and implement with AutoRegressive model with eXogenous Input (ARX). We apply this technique to both simulated data and LFPs recorded in the primary visual cortex of awake macaque monkeys. The analyses here demonstrate a greater degree of accurate noise removal than conventional notch filters. Our method leaves desired signal intact and does not introduce artificial noise components. Application of this method to awake monkey V1 recordings reveals a significant power increase in the gamma range evoked by visual stimulation. Our findings suggest that the ARX denoising procedure will be an important pre-processing step in the analysis of large volumes of cortical LFP data as well as high frequency (gamma-band related) electroencephalography/magnetoencephalography (EEG/MEG) applications, one which will help to convincingly dissociate this notorious artifact from gamma-band activity.

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  • doi:10.1016/j.jneumeth.2010.10.029

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Ben D. B. Willmore; James A. Mazer; Jack L. Gallant

Sparse coding in striate and extrastriate visual cortex Journal Article

In: Journal of Neurophysiology, vol. 105, no. 6, pp. 2907–2919, 2011.

Abstract | Links | BibTeX

@article{Willmore2011,
title = {Sparse coding in striate and extrastriate visual cortex},
author = {Ben D. B. Willmore and James A. Mazer and Jack L. Gallant},
doi = {10.1152/jn.00594.2010},
year = {2011},
date = {2011-01-01},
journal = {Journal of Neurophysiology},
volume = {105},
number = {6},
pages = {2907--2919},
abstract = {Theoretical studies of mammalian cortex argue that efficient neural codes should be sparse. However, theoretical and experimental studies have used different definitions of the term "sparse" leading to three assumptions about the nature of sparse codes. First, codes that have high lifetime sparseness require few action potentials. Second, lifetime-sparse codes are also population-sparse. Third, neural codes are optimized to maximize lifetime sparseness. Here, we examine these assumptions in detail and test their validity in primate visual cortex. We show that lifetime and population sparseness are not necessarily correlated and that a code may have high lifetime sparseness regardless of how many action potentials it uses. We measure lifetime sparseness during presentation of natural images in three areas of macaque visual cortex, V1, V2, and V4. We find that lifetime sparseness does not increase across the visual hierarchy. This suggests that the neural code is not simply optimized to maximize lifetime sparseness. We also find that firing rates during a challenging visual task are higher than theoretical values based on metabolic limits and that responses in V1, V2, and V4 are well-described by exponential distributions. These findings are consistent with the hypothesis that neurons are optimized to maximize information transmission subject to metabolic constraints on mean firing rate.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

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Theoretical studies of mammalian cortex argue that efficient neural codes should be sparse. However, theoretical and experimental studies have used different definitions of the term "sparse" leading to three assumptions about the nature of sparse codes. First, codes that have high lifetime sparseness require few action potentials. Second, lifetime-sparse codes are also population-sparse. Third, neural codes are optimized to maximize lifetime sparseness. Here, we examine these assumptions in detail and test their validity in primate visual cortex. We show that lifetime and population sparseness are not necessarily correlated and that a code may have high lifetime sparseness regardless of how many action potentials it uses. We measure lifetime sparseness during presentation of natural images in three areas of macaque visual cortex, V1, V2, and V4. We find that lifetime sparseness does not increase across the visual hierarchy. This suggests that the neural code is not simply optimized to maximize lifetime sparseness. We also find that firing rates during a challenging visual task are higher than theoretical values based on metabolic limits and that responses in V1, V2, and V4 are well-described by exponential distributions. These findings are consistent with the hypothesis that neurons are optimized to maximize information transmission subject to metabolic constraints on mean firing rate.

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  • doi:10.1152/jn.00594.2010

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Huihui Zhou; Robert Desimone

Feature-based attention in the Frontal Eye Field and area V4 during visual search Journal Article

In: Neuron, vol. 70, no. 6, pp. 1205–1217, 2011.

Abstract | Links | BibTeX

@article{Zhou2011,
title = {Feature-based attention in the Frontal Eye Field and area V4 during visual search},
author = {Huihui Zhou and Robert Desimone},
doi = {10.1016/j.neuron.2011.04.032},
year = {2011},
date = {2011-01-01},
journal = {Neuron},
volume = {70},
number = {6},
pages = {1205--1217},
publisher = {Elsevier Inc.},
abstract = {When we search for a target in a crowded visual scene, we often use the distinguishing features of the target, such as color or shape, to guide our attention and eye movements. To investigate the neural mechanisms of feature-based attention, we simultaneously recorded neural responses in the frontal eye field (FEF) and area V4 while monkeys performed a visual search task. The responses of cells in both areas were modulated by feature attention, independent of spatial attention, and the magnitude of response enhancement was inversely correlated with the number of saccades needed to find the target. However, an analysis of the latency of sensory and attentional influences on responses suggested that V4 provides bottom-up sensory information about stimulus features, whereas the FEF provides a top-down attentional bias toward target features that modulates sensory processing in V4 and that could be used to guide the eyes to a searched-for target.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

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When we search for a target in a crowded visual scene, we often use the distinguishing features of the target, such as color or shape, to guide our attention and eye movements. To investigate the neural mechanisms of feature-based attention, we simultaneously recorded neural responses in the frontal eye field (FEF) and area V4 while monkeys performed a visual search task. The responses of cells in both areas were modulated by feature attention, independent of spatial attention, and the magnitude of response enhancement was inversely correlated with the number of saccades needed to find the target. However, an analysis of the latency of sensory and attentional influences on responses suggested that V4 provides bottom-up sensory information about stimulus features, whereas the FEF provides a top-down attentional bias toward target features that modulates sensory processing in V4 and that could be used to guide the eyes to a searched-for target.

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  • doi:10.1016/j.neuron.2011.04.032

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Hamed Zivari Adab; Rufin Vogels

Practicing coarse orientation discrimination improves orientation signals in macaque cortical area V4 Journal Article

In: Current Biology, vol. 21, no. 19, pp. 1661–1666, 2011.

Abstract | Links | BibTeX

@article{ZivariAdab2011,
title = {Practicing coarse orientation discrimination improves orientation signals in macaque cortical area V4},
author = {Hamed Zivari Adab and Rufin Vogels},
doi = {10.1016/j.cub.2011.08.037},
year = {2011},
date = {2011-01-01},
journal = {Current Biology},
volume = {21},
number = {19},
pages = {1661--1666},
publisher = {Elsevier Ltd},
abstract = {Practice improves the performance in visual tasks, but mechanisms underlying this adult brain plasticity are unclear. Single-cell studies reported no [1], weak [2], or moderate [3, 4] perceptual learning-related changes in macaque visual areas V1 and V4, whereas none were found in middle temporal (MT) [5]. These conflicting results and modeling of human (e.g., [6, 7]) and monkey data [8] suggested that changes in the readout of visual cortical signals underlie perceptual learning, rather than changes in these signals. In the V4 learning studies, monkeys discriminated small differences in orientation, whereas in the MT study, the animals discriminated opponent motion directions. Analogous to the latter study, we trained monkeys to discriminate static orthogonal orientations masked by noise. V4 neurons showed robust increases in their capacity to discriminate the trained orientations during the course of the training. This effect was observed during discrimination and passive fixation but specifically for the trained orientations. The improvement in neural discrimination was due to decreased response variability and an increase of the difference between the mean responses for the two trained orientations. These findings demonstrate that perceptual learning in a coarse discrimination task indeed can change the response properties of a cortical sensory area.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

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Practice improves the performance in visual tasks, but mechanisms underlying this adult brain plasticity are unclear. Single-cell studies reported no [1], weak [2], or moderate [3, 4] perceptual learning-related changes in macaque visual areas V1 and V4, whereas none were found in middle temporal (MT) [5]. These conflicting results and modeling of human (e.g., [6, 7]) and monkey data [8] suggested that changes in the readout of visual cortical signals underlie perceptual learning, rather than changes in these signals. In the V4 learning studies, monkeys discriminated small differences in orientation, whereas in the MT study, the animals discriminated opponent motion directions. Analogous to the latter study, we trained monkeys to discriminate static orthogonal orientations masked by noise. V4 neurons showed robust increases in their capacity to discriminate the trained orientations during the course of the training. This effect was observed during discrimination and passive fixation but specifically for the trained orientations. The improvement in neural discrimination was due to decreased response variability and an increase of the difference between the mean responses for the two trained orientations. These findings demonstrate that perceptual learning in a coarse discrimination task indeed can change the response properties of a cortical sensory area.

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  • doi:10.1016/j.cub.2011.08.037

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Elsie Premereur; Wim Vanduffel; Peter Janssen

Functional heterogeneity of macaque lateral intraparietal neurons Journal Article

In: Journal of Neuroscience, vol. 31, no. 34, pp. 12307–12317, 2011.

Abstract | Links | BibTeX

@article{Premereur2011,
title = {Functional heterogeneity of macaque lateral intraparietal neurons},
author = {Elsie Premereur and Wim Vanduffel and Peter Janssen},
doi = {10.1523/JNEUROSCI.2241-11.2011},
year = {2011},
date = {2011-01-01},
journal = {Journal of Neuroscience},
volume = {31},
number = {34},
pages = {12307--12317},
abstract = {The macaque lateral intraparietal area (LIP) has been implicated in manycognitive processes, ranging from saccade planning and spatial attention to timing and categorization. Importantly, different research groups have used different criteria for including LIP neurons in their studies. While some research groups have selected LIP neurons based on the presence of memory-delay activity, other research groups have used other criteria such as visual, presaccadic, and/or memory activity. We recorded from LIP neurons that were selected based on spatially selective saccadic activity but regardless ofmemory-delay activity in macaque monkeys. To test anticipatory climbing activity, we used a delayed visually guided saccade task with a unimodal schedule ofgo-times, for which the conditional probability that the go-signal will occur rises monotonically as a function of time. A subpopulation of LIP neurons showed anticipatory activity that mimicked the subjective hazard rate ofthe go-signal when the animal was planning a saccade toward the receptive field. Alarge subgroup ofLIP neurons, however, did not modulate their firing rates according to the subjective hazard function. These non-anticipatory neurons were strongly influenced by salient visual stimuli appearing in their receptive field, but less so by the direction ofthe impending saccade. Thus, LIP contains a heterogeneous population ofneurons related to saccade planning or visual salience, and these neurons are spatially intermixed.Our results suggest that between-study differences in neuronal selectionmayhave contributed significantly to the findings of different research groups with respect to the functional role ofarea LIP.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

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The macaque lateral intraparietal area (LIP) has been implicated in manycognitive processes, ranging from saccade planning and spatial attention to timing and categorization. Importantly, different research groups have used different criteria for including LIP neurons in their studies. While some research groups have selected LIP neurons based on the presence of memory-delay activity, other research groups have used other criteria such as visual, presaccadic, and/or memory activity. We recorded from LIP neurons that were selected based on spatially selective saccadic activity but regardless ofmemory-delay activity in macaque monkeys. To test anticipatory climbing activity, we used a delayed visually guided saccade task with a unimodal schedule ofgo-times, for which the conditional probability that the go-signal will occur rises monotonically as a function of time. A subpopulation of LIP neurons showed anticipatory activity that mimicked the subjective hazard rate ofthe go-signal when the animal was planning a saccade toward the receptive field. Alarge subgroup ofLIP neurons, however, did not modulate their firing rates according to the subjective hazard function. These non-anticipatory neurons were strongly influenced by salient visual stimuli appearing in their receptive field, but less so by the direction ofthe impending saccade. Thus, LIP contains a heterogeneous population ofneurons related to saccade planning or visual salience, and these neurons are spatially intermixed.Our results suggest that between-study differences in neuronal selectionmayhave contributed significantly to the findings of different research groups with respect to the functional role ofarea LIP.

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  • doi:10.1523/JNEUROSCI.2241-11.2011

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Adam J. Sachs; Paul S. Khayat; Robert Niebergall; Julio C. Martinez-Trujillo

A metric-based analysis of the contribution of spike timing to contrast and motion direction coding by single neurons in macaque area MT Journal Article

In: Brain Research, vol. 1368, pp. 163–184, 2011.

Abstract | Links | BibTeX

@article{Sachs2011,
title = {A metric-based analysis of the contribution of spike timing to contrast and motion direction coding by single neurons in macaque area MT},
author = {Adam J. Sachs and Paul S. Khayat and Robert Niebergall and Julio C. Martinez-Trujillo},
doi = {10.1016/j.brainres.2010.09.001},
year = {2011},
date = {2011-01-01},
journal = {Brain Research},
volume = {1368},
pages = {163--184},
publisher = {Elsevier B.V.},
abstract = {Spike timing is thought to contribute to the coding of motion direction information by neurons in macaque area MT. Here, we examined whether spike timing also contributes to the coding of stimulus contrast. We applied a metric-based approach to spike trains fired by MT neurons in response to stimuli that varied in contrast, or direction. We assessed the performance of three metrics, Dspikeand Dproduct(containing spike count and timing information), and the spike count metric Dcount. We analyzed responses elicited during the first 200 msec of stimulus presentation from 205 neurons. For both contrast and direction, the large majority of neurons showed the highest mutual information using Dspike, followed by Dproduct, and Dcount. This was corroborated by the performance of a theoretical observer model at discriminating contrast and direction using the three metrics. Our results demonstrate that spike timing can contribute to contrast coding in MT neurons, and support previous reports of its potential contribution to direction coding. Furthermore, they suggest that a combination of spike count with periodic and non-periodic spike timing information (contained in Dspike, but not in Dproductand Dcountwhich are insensitive to spike counts and timing respectively) provides the largest coding advantage in spike trains fired by MT neurons during contrast and direction discrimination.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

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Spike timing is thought to contribute to the coding of motion direction information by neurons in macaque area MT. Here, we examined whether spike timing also contributes to the coding of stimulus contrast. We applied a metric-based approach to spike trains fired by MT neurons in response to stimuli that varied in contrast, or direction. We assessed the performance of three metrics, Dspikeand Dproduct(containing spike count and timing information), and the spike count metric Dcount. We analyzed responses elicited during the first 200 msec of stimulus presentation from 205 neurons. For both contrast and direction, the large majority of neurons showed the highest mutual information using Dspike, followed by Dproduct, and Dcount. This was corroborated by the performance of a theoretical observer model at discriminating contrast and direction using the three metrics. Our results demonstrate that spike timing can contribute to contrast coding in MT neurons, and support previous reports of its potential contribution to direction coding. Furthermore, they suggest that a combination of spike count with periodic and non-periodic spike timing information (contained in Dspike, but not in Dproductand Dcountwhich are insensitive to spike counts and timing respectively) provides the largest coding advantage in spike trains fired by MT neurons during contrast and direction discrimination.

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  • doi:10.1016/j.brainres.2010.09.001

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Navid G. Sadeghi; Vani Pariyadath; Sameer Apte; David M. Eagleman; Erik P. Cook

Neural correlates of subsecond time distortion in the middle temporal area of visual cortex Journal Article

In: Journal of Cognitive Neuroscience, vol. 23, no. 12, pp. 3829–3840, 2011.

Abstract | Links | BibTeX

@article{Sadeghi2011,
title = {Neural correlates of subsecond time distortion in the middle temporal area of visual cortex},
author = {Navid G. Sadeghi and Vani Pariyadath and Sameer Apte and David M. Eagleman and Erik P. Cook},
doi = {10.1162/jocn_a_00071},
year = {2011},
date = {2011-01-01},
journal = {Journal of Cognitive Neuroscience},
volume = {23},
number = {12},
pages = {3829--3840},
abstract = {How does the brain represent the passage of time at the subsecond scale? Although different conceptual models for time perception have been proposed, its neurophysiological basis remains unknown. We took advantage of a visual duration illusion produced by stimulus novelty to link changes in cortical activity in monkeys with distortions of duration perception in humans. We found that human subjects perceived the duration of a subsecond motion pulse with a novel direction longer than a motion pulse with a repeated direction. Recording from monkeys viewing identical motion stimuli but performing a different behavioral task, we found that both the duration and amplitude of the neural response in the middle temporal area of visual cortex were positively correlated with the degree of novelty of the motion direction. In contrast to previous accounts that attribute distortions in duration perception to changes in the speed of a putative internal clock, our results suggest that the known adaptive properties of neural activity in visual cortex contributes to subsecond temporal distortions.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

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How does the brain represent the passage of time at the subsecond scale? Although different conceptual models for time perception have been proposed, its neurophysiological basis remains unknown. We took advantage of a visual duration illusion produced by stimulus novelty to link changes in cortical activity in monkeys with distortions of duration perception in humans. We found that human subjects perceived the duration of a subsecond motion pulse with a novel direction longer than a motion pulse with a repeated direction. Recording from monkeys viewing identical motion stimuli but performing a different behavioral task, we found that both the duration and amplitude of the neural response in the middle temporal area of visual cortex were positively correlated with the degree of novelty of the motion direction. In contrast to previous accounts that attribute distortions in duration perception to changes in the speed of a putative internal clock, our results suggest that the known adaptive properties of neural activity in visual cortex contributes to subsecond temporal distortions.

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  • doi:10.1162/jocn_a_00071

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Swetha Shankar; Dino P. Massoglia; Dantong Zhu; M. Gabriela Costello; Terrence R. Stanford; Emilio Salinas

Tracking the temporal evolution of a perceptual judgment using a compelled-response task Journal Article

In: Journal of Neuroscience, vol. 31, no. 23, pp. 8406–8421, 2011.

Abstract | Links | BibTeX

@article{Shankar2011,
title = {Tracking the temporal evolution of a perceptual judgment using a compelled-response task},
author = {Swetha Shankar and Dino P. Massoglia and Dantong Zhu and M. Gabriela Costello and Terrence R. Stanford and Emilio Salinas},
doi = {10.1523/JNEUROSCI.1419-11.2011},
year = {2011},
date = {2011-01-01},
journal = {Journal of Neuroscience},
volume = {31},
number = {23},
pages = {8406--8421},
abstract = {Choice behavior and its neural correlates have been intensely studied with tasks in which a subject makes a perceptual judgment and indicates the result with a motor action. Yet a question crucial for relating behavior to neural activity remains unresolved: what fraction of a subject's reaction time (RT) is devoted to the perceptual evaluation step, as opposed to executing the motor report? Making such timing measurements accurately is complicated because RTs reflect both sensory and motor processing, and because speed and accuracy may be traded. To overcome these problems, we designed the compelled-saccade task, a two-alternative forced-choice task in which the instruction to initiate a saccade precedes the appearance of the relevant sensory information. With this paradigm, it is possible to track perceptual performance as a function of the amount of time during which sensory information is available to influence a subject's choice. The result-the tachometric curve-directly reveals a subject's perceptual processing capacity independently of motor demands. Psychophysical data, together with modeling and computer-simulation results, reveal that task performance depends on three separable components: the timing of the motor responses, the speed of the perceptual evaluation, and additional cognitive factors. Each can vary quickly, from one trial to the next, or can show stable, longer-term changes. This novel dissociation between sensory and motor processes yields a precise metric of how perceptual capacity varies under various experimental conditions and serves to interpret choice-related neuronal activity as perceptual, motor, or both.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

Choice behavior and its neural correlates have been intensely studied with tasks in which a subject makes a perceptual judgment and indicates the result with a motor action. Yet a question crucial for relating behavior to neural activity remains unresolved: what fraction of a subject's reaction time (RT) is devoted to the perceptual evaluation step, as opposed to executing the motor report? Making such timing measurements accurately is complicated because RTs reflect both sensory and motor processing, and because speed and accuracy may be traded. To overcome these problems, we designed the compelled-saccade task, a two-alternative forced-choice task in which the instruction to initiate a saccade precedes the appearance of the relevant sensory information. With this paradigm, it is possible to track perceptual performance as a function of the amount of time during which sensory information is available to influence a subject's choice. The result-the tachometric curve-directly reveals a subject's perceptual processing capacity independently of motor demands. Psychophysical data, together with modeling and computer-simulation results, reveal that task performance depends on three separable components: the timing of the motor responses, the speed of the perceptual evaluation, and additional cognitive factors. Each can vary quickly, from one trial to the next, or can show stable, longer-term changes. This novel dissociation between sensory and motor processes yields a precise metric of how perceptual capacity varies under various experimental conditions and serves to interpret choice-related neuronal activity as perceptual, motor, or both.

Close

  • doi:10.1523/JNEUROSCI.1419-11.2011

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Joo-Hyun Song; Robert D. Rafal; Robert M. McPeek

Deficits in reach target selection during inactivation of the midbrain superior colliculus Journal Article

In: Proceedings of the National Academy of Sciences, vol. 108, no. 51, pp. E1433–E1440, 2011.

Abstract | Links | BibTeX

@article{Song2011,
title = {Deficits in reach target selection during inactivation of the midbrain superior colliculus},
author = {Joo-Hyun Song and Robert D. Rafal and Robert M. McPeek},
doi = {10.1073/pnas.1109656108},
year = {2011},
date = {2011-01-01},
journal = {Proceedings of the National Academy of Sciences},
volume = {108},
number = {51},
pages = {E1433--E1440},
abstract = {Purposive action requires the selection of a single movement goal from multiple possibilities. Neural structures involved in movement planning and execution often exhibit activity related to target selection. A key question is whether this activity is specific to the type of movement produced by the structure, perhaps consisting of a competition among effector-specific movement plans, or whether it constitutes a more abstract, effector-independent selection signal. Here, we show that temporary focal inactivation of the primate superior colliculus (SC), an area involved in eye-movement target selection and execution, causes striking target selection deficits for reaching movements, which cannot be readily explained as a simple impairment in visual perception or motor execution. This indicates that target selection activity in the SC does not simply represent a competition among eye-movement goals and, instead, suggests that the SC contributes to a more general purpose priority map that influences target selection for other actions, such as reaches.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

Purposive action requires the selection of a single movement goal from multiple possibilities. Neural structures involved in movement planning and execution often exhibit activity related to target selection. A key question is whether this activity is specific to the type of movement produced by the structure, perhaps consisting of a competition among effector-specific movement plans, or whether it constitutes a more abstract, effector-independent selection signal. Here, we show that temporary focal inactivation of the primate superior colliculus (SC), an area involved in eye-movement target selection and execution, causes striking target selection deficits for reaching movements, which cannot be readily explained as a simple impairment in visual perception or motor execution. This indicates that target selection activity in the SC does not simply represent a competition among eye-movement goals and, instead, suggests that the SC contributes to a more general purpose priority map that influences target selection for other actions, such as reaches.

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  • doi:10.1073/pnas.1109656108

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C. D. Fiorillo

Transient activation of midbrain dopamine neurons by reward risk Journal Article

In: Neuroscience, vol. 197, pp. 162–171, 2011.

Abstract | Links | BibTeX

@article{Fiorillo2011,
title = {Transient activation of midbrain dopamine neurons by reward risk},
author = {C. D. Fiorillo},
doi = {10.1016/j.neuroscience.2011.09.037},
year = {2011},
date = {2011-01-01},
journal = {Neuroscience},
volume = {197},
pages = {162--171},
publisher = {Elsevier Inc.},
abstract = {Dopamine neurons of the ventral midbrain are activated transiently following stimuli that predict future reward. This response has been shown to signal the expected value of future reward, and there is strong evidence that it drives positive reinforcement of stimuli and actions associated with reward in accord with reinforcement learning models. Behavior is also influenced by reward uncertainty, or risk, but it is not known whether the transient response of dopamine neurons is sensitive to reward risk. To investigate this, monkeys were trained to associate distinct visual stimuli with certain or uncertain volumes of juice of nearly the same expected value. In a choice task, monkeys preferred the stimulus predicting an uncertain (risky) reward outcome. In a Pavlovian task, in which the neuronal responses to each stimulus could be measured in isolation, it was found that dopamine neurons were more strongly activated by the stimulus associated with reward risk. Given extensive evidence that dopamine drives reinforcement, these results strongly suggest that dopamine neurons can reinforce risk-seeking behavior (gambling), at least under certain conditions. Risk-seeking behavior has the virtue of promoting exploration and learning, and these results support the hypothesis that dopamine neurons represent the value of exploration.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

Dopamine neurons of the ventral midbrain are activated transiently following stimuli that predict future reward. This response has been shown to signal the expected value of future reward, and there is strong evidence that it drives positive reinforcement of stimuli and actions associated with reward in accord with reinforcement learning models. Behavior is also influenced by reward uncertainty, or risk, but it is not known whether the transient response of dopamine neurons is sensitive to reward risk. To investigate this, monkeys were trained to associate distinct visual stimuli with certain or uncertain volumes of juice of nearly the same expected value. In a choice task, monkeys preferred the stimulus predicting an uncertain (risky) reward outcome. In a Pavlovian task, in which the neuronal responses to each stimulus could be measured in isolation, it was found that dopamine neurons were more strongly activated by the stimulus associated with reward risk. Given extensive evidence that dopamine drives reinforcement, these results strongly suggest that dopamine neurons can reinforce risk-seeking behavior (gambling), at least under certain conditions. Risk-seeking behavior has the virtue of promoting exploration and learning, and these results support the hypothesis that dopamine neurons represent the value of exploration.

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  • doi:10.1016/j.neuroscience.2011.09.037

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Davis M. Glasser; James M. G. Tsui; Christopher C. Pack; Duje Tadin

Perceptual and neural consequences of rapid motion adaptation Journal Article

In: Proceedings of the National Academy of Sciences, vol. 108, no. 45, pp. E1080–E1088, 2011.

Abstract | Links | BibTeX

@article{Glasser2011,
title = {Perceptual and neural consequences of rapid motion adaptation},
author = {Davis M. Glasser and James M. G. Tsui and Christopher C. Pack and Duje Tadin},
doi = {10.1073/pnas.1101141108},
year = {2011},
date = {2011-01-01},
journal = {Proceedings of the National Academy of Sciences},
volume = {108},
number = {45},
pages = {E1080--E1088},
abstract = {Nervous systems adapt to the prevailing sensory environment, and the consequences of this adaptation can be observed in the responses of single neurons and in perception. Given the variety of timescales underlying events in the natural world, determining the temporal characteristics of adaptation is important to understanding how perception adjusts to its sensory environment. Previous work has shown that neural adaptation can occur on a timescale of milliseconds, but perceptual adaptation has generally been studied over relatively long timescales, typically on the order of seconds. This disparity raises important questions. Can perceptual adaptation be observed at brief, functionally relevant timescales? And if so, how do its properties relate to the rapid adaptation seen in cortical neurons? We address these questions in the context of visual motion processing, a perceptual modality characterized by rapid temporal dynamics. We demonstrate objectively that 25 ms of motion adaptation is sufficient to generate a motion aftereffect, an illusory sensation of movement experienced when a moving stimulus is replaced by a stationary pattern. This rapid adaptation occurs regardless of whether the adapting motion is perceived. In neurophysiological recordings from the middle temporal area of primate visual cortex, we find that brief motion adaptation evokes direction-selective responses to subsequently presented stationary stimuli. A simple model shows that these neural responses can explain the consequences of rapid perceptual adaptation. Overall, we show that the motion aftereffect is not merely an intriguing perceptual illusion, but rather a reflection of rapid neural and perceptual processes that can occur essentially every time we experience motion.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

Nervous systems adapt to the prevailing sensory environment, and the consequences of this adaptation can be observed in the responses of single neurons and in perception. Given the variety of timescales underlying events in the natural world, determining the temporal characteristics of adaptation is important to understanding how perception adjusts to its sensory environment. Previous work has shown that neural adaptation can occur on a timescale of milliseconds, but perceptual adaptation has generally been studied over relatively long timescales, typically on the order of seconds. This disparity raises important questions. Can perceptual adaptation be observed at brief, functionally relevant timescales? And if so, how do its properties relate to the rapid adaptation seen in cortical neurons? We address these questions in the context of visual motion processing, a perceptual modality characterized by rapid temporal dynamics. We demonstrate objectively that 25 ms of motion adaptation is sufficient to generate a motion aftereffect, an illusory sensation of movement experienced when a moving stimulus is replaced by a stationary pattern. This rapid adaptation occurs regardless of whether the adapting motion is perceived. In neurophysiological recordings from the middle temporal area of primate visual cortex, we find that brief motion adaptation evokes direction-selective responses to subsequently presented stationary stimuli. A simple model shows that these neural responses can explain the consequences of rapid perceptual adaptation. Overall, we show that the motion aftereffect is not merely an intriguing perceptual illusion, but rather a reflection of rapid neural and perceptual processes that can occur essentially every time we experience motion.

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  • doi:10.1073/pnas.1101141108

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Till S. Hartmann; Frank Bremmer; Thomas D. Albright; Bart Krekelberg

Receptive field positions in area MT during slow eye movements Journal Article

In: Journal of Neuroscience, vol. 31, no. 29, pp. 10437–10444, 2011.

Abstract | Links | BibTeX

@article{Hartmann2011,
title = {Receptive field positions in area MT during slow eye movements},
author = {Till S. Hartmann and Frank Bremmer and Thomas D. Albright and Bart Krekelberg},
doi = {10.1523/JNEUROSCI.5590-10.2011},
year = {2011},
date = {2011-01-01},
journal = {Journal of Neuroscience},
volume = {31},
number = {29},
pages = {10437--10444},
abstract = {Perceptual stability requires the integration of information across eye movements. We first tested the hypothesis that motion signals are integrated by neurons whose receptive fields (RFs) do not move with the eye but stay fixed in the world. Specifically, we measured the RF properties of neurons in the middle temporal area (MT) of macaques (Macaca mulatta) during the slow phase of optokinetic nystagmus. Using a novel method to estimate RF locations for both spikes and local field potentials, we found that the location on the retina that changed spike rates or local field potentials did not change with eye position; RFs moved with the eye. Second, we tested the hypothesis that neurons link information across eye positions by remapping the retinal location of their RFs to future locations. To test this, we compared RF locations during leftward and rightward slow phases of optokinetic nystagmus. We found no evidence for remapping during slow eye movements; the RF location was not affected by eye-movement direction. Together, our results show that RFs of MT neurons and the aggregate activity reflected in local field potentials are yoked to the eye during slow eye movements. This implies that individual MT neurons do not integrate sensory information from a single position in the world across eye movements. Future research will have to determine whether such integration, and the construction of perceptual stability, takes place in the form of a distributed population code in eye-centered visual cortex or is deferred to downstream areas.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

Perceptual stability requires the integration of information across eye movements. We first tested the hypothesis that motion signals are integrated by neurons whose receptive fields (RFs) do not move with the eye but stay fixed in the world. Specifically, we measured the RF properties of neurons in the middle temporal area (MT) of macaques (Macaca mulatta) during the slow phase of optokinetic nystagmus. Using a novel method to estimate RF locations for both spikes and local field potentials, we found that the location on the retina that changed spike rates or local field potentials did not change with eye position; RFs moved with the eye. Second, we tested the hypothesis that neurons link information across eye positions by remapping the retinal location of their RFs to future locations. To test this, we compared RF locations during leftward and rightward slow phases of optokinetic nystagmus. We found no evidence for remapping during slow eye movements; the RF location was not affected by eye-movement direction. Together, our results show that RFs of MT neurons and the aggregate activity reflected in local field potentials are yoked to the eye during slow eye movements. This implies that individual MT neurons do not integrate sensory information from a single position in the world across eye movements. Future research will have to determine whether such integration, and the construction of perceptual stability, takes place in the form of a distributed population code in eye-centered visual cortex or is deferred to downstream areas.

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  • doi:10.1523/JNEUROSCI.5590-10.2011

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Benjamin Y. Hayden; Sarah R. Heilbronner; John M. Pearson; Michael L. Platt

Surprise signals in anterior cingulate cortex: Neuronal encoding of unsigned reward prediction errors driving adjustment in behavior Journal Article

In: Journal of Neuroscience, vol. 31, no. 11, pp. 4178–4187, 2011.

Abstract | Links | BibTeX

@article{Hayden2011,
title = {Surprise signals in anterior cingulate cortex: Neuronal encoding of unsigned reward prediction errors driving adjustment in behavior},
author = {Benjamin Y. Hayden and Sarah R. Heilbronner and John M. Pearson and Michael L. Platt},
doi = {10.1523/JNEUROSCI.4652-10.2011},
year = {2011},
date = {2011-01-01},
journal = {Journal of Neuroscience},
volume = {31},
number = {11},
pages = {4178--4187},
abstract = {In attentional models of learning, associations between actions and subsequent rewards are stronger when outcomes are surprising, regardless of their valence. Despite the behavioral evidence that surprising outcomes drive learning, neural correlates of unsigned reward prediction errors remain elusive. Here we show that in a probabilistic choice task, trial-to-trial variations in preference track outcome surprisingness. Concordant with this behavioral pattern, responses of neurons in macaque (Macaca mulatta) dorsal anterior cingulate cortex (dACC) to both large and small rewards were enhanced when the outcome was surprising. Moreover, when, on some trials, probabilities were hidden, neuronal responses to rewards were reduced, consistent with the idea that the absence of clear expectations diminishes surprise. These patterns are inconsistent with the idea that dACC neurons track signed errors in reward prediction, as dopamine neurons do. Our results also indicate that dACC neurons do not signal conflict. In the context of other studies of dACC function, these results suggest a link between reward-related modulations in dACC activity and attention and motor control processes involved in behavioral adjustment. More speculatively, these data point to a harmonious integration between reward and learning accounts of ACC function on one hand, and attention and cognitive control accounts on the other.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

In attentional models of learning, associations between actions and subsequent rewards are stronger when outcomes are surprising, regardless of their valence. Despite the behavioral evidence that surprising outcomes drive learning, neural correlates of unsigned reward prediction errors remain elusive. Here we show that in a probabilistic choice task, trial-to-trial variations in preference track outcome surprisingness. Concordant with this behavioral pattern, responses of neurons in macaque (Macaca mulatta) dorsal anterior cingulate cortex (dACC) to both large and small rewards were enhanced when the outcome was surprising. Moreover, when, on some trials, probabilities were hidden, neuronal responses to rewards were reduced, consistent with the idea that the absence of clear expectations diminishes surprise. These patterns are inconsistent with the idea that dACC neurons track signed errors in reward prediction, as dopamine neurons do. Our results also indicate that dACC neurons do not signal conflict. In the context of other studies of dACC function, these results suggest a link between reward-related modulations in dACC activity and attention and motor control processes involved in behavioral adjustment. More speculatively, these data point to a harmonious integration between reward and learning accounts of ACC function on one hand, and attention and cognitive control accounts on the other.

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  • doi:10.1523/JNEUROSCI.4652-10.2011

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Benjamin Y. Hayden; John M. Pearson; Michael L. Platt

Neuronal basis of sequential foraging decisions in a patchy environment Journal Article

In: Nature Neuroscience, vol. 14, no. 7, pp. 933–939, 2011.

Abstract | Links | BibTeX

@article{Hayden2011a,
title = {Neuronal basis of sequential foraging decisions in a patchy environment},
author = {Benjamin Y. Hayden and John M. Pearson and Michael L. Platt},
doi = {10.1038/nn.2856},
year = {2011},
date = {2011-01-01},
journal = {Nature Neuroscience},
volume = {14},
number = {7},
pages = {933--939},
publisher = {Nature Publishing Group},
abstract = {Deciding when to leave a depleting resource to exploit another is a fundamental problem for all decision makers. The neuronal mechanisms mediating patch-leaving decisions remain unknown. We found that neurons in primate (Macaca mulatta) dorsal anterior cingulate cortex, an area that is linked to reward monitoring and executive control, encode a decision variable signaling the relative value of leaving a depleting resource for a new one. Neurons fired during each sequential decision to stay in a patch and, for each travel time, these responses reached a fixed threshold for patch-leaving. Longer travel times reduced the gain of neural responses for choosing to stay in a patch and increased the firing rate threshold mandating patch-leaving. These modulations more closely matched behavioral decisions than any single task variable. These findings portend an understanding of the neural basis of foraging decisions and endorse the unification of theoretical and experimental work in ecology and neuroscience.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

Deciding when to leave a depleting resource to exploit another is a fundamental problem for all decision makers. The neuronal mechanisms mediating patch-leaving decisions remain unknown. We found that neurons in primate (Macaca mulatta) dorsal anterior cingulate cortex, an area that is linked to reward monitoring and executive control, encode a decision variable signaling the relative value of leaving a depleting resource for a new one. Neurons fired during each sequential decision to stay in a patch and, for each travel time, these responses reached a fixed threshold for patch-leaving. Longer travel times reduced the gain of neural responses for choosing to stay in a patch and increased the firing rate threshold mandating patch-leaving. These modulations more closely matched behavioral decisions than any single task variable. These findings portend an understanding of the neural basis of foraging decisions and endorse the unification of theoretical and experimental work in ecology and neuroscience.

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  • doi:10.1038/nn.2856

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Sarah R. Heilbronner; Benjamin Y. Hayden; Michael L. Platt

Decision salience signals in posterior cingulate cortex Journal Article

In: Frontiers in Neuroscience, vol. 5, pp. 55, 2011.

Abstract | Links | BibTeX

@article{Heilbronner2011,
title = {Decision salience signals in posterior cingulate cortex},
author = {Sarah R. Heilbronner and Benjamin Y. Hayden and Michael L. Platt},
doi = {10.3389/fnins.2011.00055},
year = {2011},
date = {2011-01-01},
journal = {Frontiers in Neuroscience},
volume = {5},
pages = {55},
abstract = {Despite its phylogenetic antiquity and clinical importance, the posterior cingulate cortex (CGp) remains an enigmatic nexus of attention, memory, motivation, and decision making. Here we show that CGp neurons track decision salience - the degree to which an option differs from a standard - but not the subjective value of a decision. To do this, we recorded the spiking activity of CGp neurons in monkeys choosing between options varying in reward-related risk, delay to reward, and social outcomes, each of which varied in level of decision salience. Firing rates were higher when monkeys chose the risky option, consistent with their risk-seeking preferences, but were also higher when monkeys chose the delayed and social options, contradicting their preferences. Thus, across decision contexts, neuronal activity was uncorrelated with how much monkeys valued a given option, as inferred from choice. Instead, neuronal activity signaled the deviation of the chosen option from the standard, independently of how it differed. The observed decision salience signals suggest a role for CGp in the flexible allocation of neural resources to motivationally significant information, akin to the role of attention in selective processing of sensory inputs.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

Despite its phylogenetic antiquity and clinical importance, the posterior cingulate cortex (CGp) remains an enigmatic nexus of attention, memory, motivation, and decision making. Here we show that CGp neurons track decision salience - the degree to which an option differs from a standard - but not the subjective value of a decision. To do this, we recorded the spiking activity of CGp neurons in monkeys choosing between options varying in reward-related risk, delay to reward, and social outcomes, each of which varied in level of decision salience. Firing rates were higher when monkeys chose the risky option, consistent with their risk-seeking preferences, but were also higher when monkeys chose the delayed and social options, contradicting their preferences. Thus, across decision contexts, neuronal activity was uncorrelated with how much monkeys valued a given option, as inferred from choice. Instead, neuronal activity signaled the deviation of the chosen option from the standard, independently of how it differed. The observed decision salience signals suggest a role for CGp in the flexible allocation of neural resources to motivationally significant information, akin to the role of attention in selective processing of sensory inputs.

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  • doi:10.3389/fnins.2011.00055

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2010

Robert E. Hampson; Ioan Opris; S. A. Deadwyler

Neural correlates of fast pupil dilation in nonhuman primates: Relation to behavioral performance and cognitive workload Journal Article

In: Behavioural Brain Research, vol. 212, no. 1, pp. 1–11, 2010.

Abstract | Links | BibTeX

@article{Hampson2010,
title = {Neural correlates of fast pupil dilation in nonhuman primates: Relation to behavioral performance and cognitive workload},
author = {Robert E. Hampson and Ioan Opris and S. A. Deadwyler},
doi = {10.1016/j.bbr.2010.03.011},
year = {2010},
date = {2010-01-01},
journal = {Behavioural Brain Research},
volume = {212},
number = {1},
pages = {1--11},
publisher = {Elsevier B.V.},
abstract = {Pupil dilation in humans has been previously shown to correlate with cognitive workload, whereby increased frequency of dilation is associated with increased degree of difficulty of a task. It has been suggested that frontal oculomotor brain areas control cognitively related pupil dilations, but this has not been confirmed due to lack of animal models of cognitive workload and task-related pupil dilation. This is the first report of a wavelet analysis applied to continuous measures of pupil size used to detect the onset of abrupt pupil dilations and the frequency of those dilations in nonhuman primates (NHPs) performing a trial-unique delayed-match-to-sample (DMS) task. A unique finding shows that electrophysiological recordings in the same animals revealed firing of neurons in frontal cortex correlated to different components of pupil dilation during task performance. It is further demonstrated that the frequency of fast pupil dilations (but not rate of eye movements) correlated with cognitive workload during task performance. Such correlations suggest that frontal neuron encoding of pupil dilation provides critical feedback to other brain areas involved in the processing of complex visual information.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

Pupil dilation in humans has been previously shown to correlate with cognitive workload, whereby increased frequency of dilation is associated with increased degree of difficulty of a task. It has been suggested that frontal oculomotor brain areas control cognitively related pupil dilations, but this has not been confirmed due to lack of animal models of cognitive workload and task-related pupil dilation. This is the first report of a wavelet analysis applied to continuous measures of pupil size used to detect the onset of abrupt pupil dilations and the frequency of those dilations in nonhuman primates (NHPs) performing a trial-unique delayed-match-to-sample (DMS) task. A unique finding shows that electrophysiological recordings in the same animals revealed firing of neurons in frontal cortex correlated to different components of pupil dilation during task performance. It is further demonstrated that the frequency of fast pupil dilations (but not rate of eye movements) correlated with cognitive workload during task performance. Such correlations suggest that frontal neuron encoding of pupil dilation provides critical feedback to other brain areas involved in the processing of complex visual information.

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  • doi:10.1016/j.bbr.2010.03.011

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Benjamin Y. Hayden; Sarah R. Heilbronner; Michael L. Platt

Ambiguity aversion in rhesus macaques Journal Article

In: Frontiers in Neuroscience, vol. 4, pp. 166, 2010.

Abstract | Links | BibTeX

@article{Hayden2010a,
title = {Ambiguity aversion in rhesus macaques},
author = {Benjamin Y. Hayden and Sarah R. Heilbronner and Michael L. Platt},
doi = {10.3389/fnins.2010.00166},
year = {2010},
date = {2010-01-01},
journal = {Frontiers in Neuroscience},
volume = {4},
pages = {166},
publisher = {10},
address = {doi},
abstract = {People generally prefer risky options, which have fully specified outcome probabilities, to ambiguous options, which have unspecified probabilities. This preference, formalized in economics, is strong enough that people will reliably prefer a risky option to an ambiguous option with a greater expected value. Explanations for ambiguity aversion often invoke uniquely human faculties like language, self-justification, or a desire to avoid public embarrassment. Challenging these ideas, here we demonstrate that a preference for unambiguous options is shared with rhesus macaques. We trained four monkeys to choose between pairs of options that both offered explicitly cued probabilities of large and small juice outcomes. We then introduced occasional trials where one of the options was obscured and examined their resulting preferences; we ran humans in a parallel experiment on a nearly identical task. We found that monkeys reliably preferred risky options to ambiguous ones, even when this bias was costly, closely matching the behavior of humans in the analogous task. Notably, ambiguity aversion varied parametrically with the extent of ambiguity. As expected, ambiguity aversion gradually declined as monkeys learned the underlying probability distribution of rewards. These data indicate that ambiguity aversion reflects fundamental cognitive biases shared with other animals rather than uniquely human factors guiding decisions.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

People generally prefer risky options, which have fully specified outcome probabilities, to ambiguous options, which have unspecified probabilities. This preference, formalized in economics, is strong enough that people will reliably prefer a risky option to an ambiguous option with a greater expected value. Explanations for ambiguity aversion often invoke uniquely human faculties like language, self-justification, or a desire to avoid public embarrassment. Challenging these ideas, here we demonstrate that a preference for unambiguous options is shared with rhesus macaques. We trained four monkeys to choose between pairs of options that both offered explicitly cued probabilities of large and small juice outcomes. We then introduced occasional trials where one of the options was obscured and examined their resulting preferences; we ran humans in a parallel experiment on a nearly identical task. We found that monkeys reliably preferred risky options to ambiguous ones, even when this bias was costly, closely matching the behavior of humans in the analogous task. Notably, ambiguity aversion varied parametrically with the extent of ambiguity. As expected, ambiguity aversion gradually declined as monkeys learned the underlying probability distribution of rewards. These data indicate that ambiguity aversion reflects fundamental cognitive biases shared with other animals rather than uniquely human factors guiding decisions.

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  • doi:10.3389/fnins.2010.00166

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Benjamin Y. Hayden; Michael L. Platt

Neurons in anterior cingulate cortex multiplex information about reward and action Journal Article

In: Journal of Neuroscience, vol. 30, no. 9, pp. 3339–3346, 2010.

Abstract | Links | BibTeX

@article{Hayden2010,
title = {Neurons in anterior cingulate cortex multiplex information about reward and action},
author = {Benjamin Y. Hayden and Michael L. Platt},
doi = {10.1523/JNEUROSCI.4874-09.2010},
year = {2010},
date = {2010-01-01},
journal = {Journal of Neuroscience},
volume = {30},
number = {9},
pages = {3339--3346},
abstract = {The dorsal anterior cingulate cortex (dACC) is thought to play a critical role in forming associations between rewards and actions. Currently available physiological data, however, remain inconclusive regarding the question of whether dACC neurons carry information linking particular actions to reward or, instead, encode abstract reward information independent of specific actions. Here we show that firing rates of a majority of dACC neurons in a population studied in an eight-option variably rewarded choice task were sensitive to both saccade direction and reward value. Furthermore, the influences of reward and saccade direction on neuronal activity were approximately equal in magnitude over the range of rewards tested and were statistically independent. Our results indicate that dACC neurons multiplex information about both reward and action, endorsing the idea that this area links motivational outcomes to behavior and undermining the notion that its neurons solely contribute to reward processing in the abstract.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

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The dorsal anterior cingulate cortex (dACC) is thought to play a critical role in forming associations between rewards and actions. Currently available physiological data, however, remain inconclusive regarding the question of whether dACC neurons carry information linking particular actions to reward or, instead, encode abstract reward information independent of specific actions. Here we show that firing rates of a majority of dACC neurons in a population studied in an eight-option variably rewarded choice task were sensitive to both saccade direction and reward value. Furthermore, the influences of reward and saccade direction on neuronal activity were approximately equal in magnitude over the range of rewards tested and were statistically independent. Our results indicate that dACC neurons multiplex information about both reward and action, endorsing the idea that this area links motivational outcomes to behavior and undermining the notion that its neurons solely contribute to reward processing in the abstract.

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  • doi:10.1523/JNEUROSCI.4874-09.2010

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Benjamin Y. Hayden; David V. Smith; Michael L. Platt

Cognitive control signals in posterior cingulate cortex Journal Article

In: Frontiers in Human Neuroscience, vol. 4, pp. 223, 2010.

Abstract | Links | BibTeX

@article{Hayden2010b,
title = {Cognitive control signals in posterior cingulate cortex},
author = {Benjamin Y. Hayden and David V. Smith and Michael L. Platt},
doi = {10.3389/fnhum.2010.00223},
year = {2010},
date = {2010-01-01},
journal = {Frontiers in Human Neuroscience},
volume = {4},
pages = {223},
publisher = {10},
address = {doi},
abstract = {Efficiently shifting between tasks is a central function of cognitive control. The role of the default network - a constellation of areas with high baseline activity that declines during task performance - in cognitive control remains poorly understood. We hypothesized that task switching demands cognitive control to shift the balance of processing toward the external world, and therefore predicted that switching between the two tasks would require suppression of activity of neurons within the posterior cingulate cortex (CGp). To test this idea, we recorded the activity of single neurons in CGp, a central node in the default network, in monkeys performing two interleaved tasks. As predicted, we found that basal levels of neuronal activity were reduced following a switch from one task to another and gradually returned to pre-switch baseline on subsequent trials. We failed to observe these effects in lateral intraparietal cortex, part of the dorsal fronto-parietal cortical attention network directly connected to CGp. These findings indicate that suppression of neuronal activity in CGp facilitates cognitive control, and suggest that activity in the default network reflects processes that directly compete with control processes elsewhere in the brain.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

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Efficiently shifting between tasks is a central function of cognitive control. The role of the default network - a constellation of areas with high baseline activity that declines during task performance - in cognitive control remains poorly understood. We hypothesized that task switching demands cognitive control to shift the balance of processing toward the external world, and therefore predicted that switching between the two tasks would require suppression of activity of neurons within the posterior cingulate cortex (CGp). To test this idea, we recorded the activity of single neurons in CGp, a central node in the default network, in monkeys performing two interleaved tasks. As predicted, we found that basal levels of neuronal activity were reduced following a switch from one task to another and gradually returned to pre-switch baseline on subsequent trials. We failed to observe these effects in lateral intraparietal cortex, part of the dorsal fronto-parietal cortical attention network directly connected to CGp. These findings indicate that suppression of neuronal activity in CGp facilitates cognitive control, and suggest that activity in the default network reflects processes that directly compete with control processes elsewhere in the brain.

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  • doi:10.3389/fnhum.2010.00223

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Paul S. Khayat; Robert Niebergall; Julio C. Martinez-Trujillo

Frequency-dependent attentional modulation of local field potential signals in macaque area MT Journal Article

In: Journal of Neuroscience, vol. 30, no. 20, pp. 7037–7048, 2010.

Abstract | Links | BibTeX

@article{Khayat2010,
title = {Frequency-dependent attentional modulation of local field potential signals in macaque area MT},
author = {Paul S. Khayat and Robert Niebergall and Julio C. Martinez-Trujillo},
doi = {10.1523/JNEUROSCI.0404-10.2010},
year = {2010},
date = {2010-01-01},
journal = {Journal of Neuroscience},
volume = {30},
number = {20},
pages = {7037--7048},
abstract = {Visual attention modulates neuronal responses in primate motion processing area MT. However, whether it modulates the strength local field potentials (LFP-power) within this area remains unexplored, as well as how this modulation relates to the one of the neurons' response. We investigated these issues by simultaneously recording LFPs and neuronal responses evoked by moving random dot patterns of varying direction and contrast in area MT of two male monkeys (Macaca mulatta) during different behavioral conditions. We found that: (1) LFP-power in the gamma (30-120 Hz), but not in the delta (2-4 Hz), (4-8 Hz), alpha (8-12 Hz), beta(1) (12-20 Hz), and beta(2) (20-30 Hz) frequency bands, was tuned for motion direction and contrast, similarly to the neurons' response, (2) shifting attention into a neuron's receptive field (RF) decreased LFP-power in the bands below 30 Hz (except the band), whereas shifting attention to a stimulus motion direction outside the RF had no effect in these bands, (3) LFP-power in the gamma band, however, exhibited both spatial- and motion direction-dependent attentional modulation (increase or decrease), which was highly correlated with the modulation of the neurons' response. These results demonstrate that in area MT, shifting attention into the RFs of neurons in the vicinity of the recording electrode, or to the direction of a moving stimulus located far away from these RFs, distinctively modulates LFP-power in the various frequency bands. They further suggest differences in the neural mechanisms underlying these types of attentional modulation of visual processing.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

Visual attention modulates neuronal responses in primate motion processing area MT. However, whether it modulates the strength local field potentials (LFP-power) within this area remains unexplored, as well as how this modulation relates to the one of the neurons' response. We investigated these issues by simultaneously recording LFPs and neuronal responses evoked by moving random dot patterns of varying direction and contrast in area MT of two male monkeys (Macaca mulatta) during different behavioral conditions. We found that: (1) LFP-power in the gamma (30-120 Hz), but not in the delta (2-4 Hz), (4-8 Hz), alpha (8-12 Hz), beta(1) (12-20 Hz), and beta(2) (20-30 Hz) frequency bands, was tuned for motion direction and contrast, similarly to the neurons' response, (2) shifting attention into a neuron's receptive field (RF) decreased LFP-power in the bands below 30 Hz (except the band), whereas shifting attention to a stimulus motion direction outside the RF had no effect in these bands, (3) LFP-power in the gamma band, however, exhibited both spatial- and motion direction-dependent attentional modulation (increase or decrease), which was highly correlated with the modulation of the neurons' response. These results demonstrate that in area MT, shifting attention into the RFs of neurons in the vicinity of the recording electrode, or to the direction of a moving stimulus located far away from these RFs, distinctively modulates LFP-power in the various frequency bands. They further suggest differences in the neural mechanisms underlying these types of attentional modulation of visual processing.

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  • doi:10.1523/JNEUROSCI.0404-10.2010

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Paul S. Khayat; Robert Niebergall; Julio C. Martinez-Trujillo

Attention differentially modulates similar neuronal responses evoked by varying contrast and direction stimuli in area MT. Journal Article

In: Journal of Neuroscience, vol. 30, no. 6, pp. 2188–2197, 2010.

Abstract | Links | BibTeX

@article{Khayat2010a,
title = {Attention differentially modulates similar neuronal responses evoked by varying contrast and direction stimuli in area MT.},
author = {Paul S. Khayat and Robert Niebergall and Julio C. Martinez-Trujillo},
doi = {10.1523/JNEUROSCI.5314-09.2010},
year = {2010},
date = {2010-01-01},
journal = {Journal of Neuroscience},
volume = {30},
number = {6},
pages = {2188--2197},
abstract = {The effects of attention on the responses of visual neurons have been described as a scaling or additive modulation independent of stimulus features and contrast, or as a contrast-dependent modulation. We explored these alternatives by recording neuronal responses in macaque area MT to moving stimuli that evoked similar firing rates but varied in contrast and direction. We presented two identical pairs of stimuli, one inside the neurons' receptive field and the other outside, in the opposite hemifield. One stimulus of each pair always had high contrast and moved in the recorded cell's antipreferred direction (AP pattern), while the other (test pattern) could either move in the cell's preferred direction and vary in contrast, or have the same contrast as the AP pattern and vary in direction. For different stimulus pairs evoking similar responses, switching attention between the two AP patterns, or directing attention from a fixation spot to the AP pattern inside or outside the receptive field, produced a stronger suppression of responses to varying contrast pairs, reaching a maximum ( approximately 20%) at intermediate contrast. For invariable contrast pairs, switching attention from the fixation spot to the AP pattern produced a modulation that ranged from 10% suppression when the test pattern moved in the cells preferred direction to 14% enhancement when it moved in a direction 90 degrees away from that direction. Our results are incompatible with a scaling or additive modulation of MT neurons' response by attention, but support models where spatial and feature-based attention modulate input signals into the area normalization circuit.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

The effects of attention on the responses of visual neurons have been described as a scaling or additive modulation independent of stimulus features and contrast, or as a contrast-dependent modulation. We explored these alternatives by recording neuronal responses in macaque area MT to moving stimuli that evoked similar firing rates but varied in contrast and direction. We presented two identical pairs of stimuli, one inside the neurons' receptive field and the other outside, in the opposite hemifield. One stimulus of each pair always had high contrast and moved in the recorded cell's antipreferred direction (AP pattern), while the other (test pattern) could either move in the cell's preferred direction and vary in contrast, or have the same contrast as the AP pattern and vary in direction. For different stimulus pairs evoking similar responses, switching attention between the two AP patterns, or directing attention from a fixation spot to the AP pattern inside or outside the receptive field, produced a stronger suppression of responses to varying contrast pairs, reaching a maximum ( approximately 20%) at intermediate contrast. For invariable contrast pairs, switching attention from the fixation spot to the AP pattern produced a modulation that ranged from 10% suppression when the test pattern moved in the cells preferred direction to 14% enhancement when it moved in a direction 90 degrees away from that direction. Our results are incompatible with a scaling or additive modulation of MT neurons' response by attention, but support models where spatial and feature-based attention modulate input signals into the area normalization circuit.

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  • doi:10.1523/JNEUROSCI.5314-09.2010

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Dhushan Thevarajah; Ryan Webb; Christopher Ferrall; Michael C. Dorris

Modeling the value of strategic actions in the superior colliculus Journal Article

In: Frontiers in Behavioral Neuroscience, vol. 3, pp. 57, 2010.

Abstract | Links | BibTeX

@article{Thevarajah2010,
title = {Modeling the value of strategic actions in the superior colliculus},
author = {Dhushan Thevarajah and Ryan Webb and Christopher Ferrall and Michael C. Dorris},
doi = {10.3389/neuro.08.057.2009},
year = {2010},
date = {2010-01-01},
journal = {Frontiers in Behavioral Neuroscience},
volume = {3},
pages = {57},
abstract = {In learning models of strategic game play, an agent constructs a valuation (action value) over possible future choices as a function of past actions and rewards. Choices are then stochastic functions of these action values. Our goal is to uncover a neural signal that correlates with the action value posited by behavioral learning models. We measured activity from neurons in the superior colliculus (SC), a midbrain region involved in planning saccadic eye movements, while monkeys performed two saccade tasks. In the strategic task, monkeys competed against a computer in a saccade version of the mixed-strategy game "matching-pennies". In the instructed task, saccades were elicited through explicit instruction rather than free choices. In both tasks neuronal activity and behavior were shaped by past actions and rewards with more recent events exerting a larger influence. Further, SC activity predicted upcoming choices during the strategic task and upcoming reaction times during the instructed task. Finally, we found that neuronal activity in both tasks correlated with an established learning model, the Experience Weighted Attraction model of action valuation (Camerer and Ho, 1999). Collectively, our results provide evidence that action values hypothesized by learning models are represented in the motor planning regions of the brain in a manner that could be used to select strategic actions.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

In learning models of strategic game play, an agent constructs a valuation (action value) over possible future choices as a function of past actions and rewards. Choices are then stochastic functions of these action values. Our goal is to uncover a neural signal that correlates with the action value posited by behavioral learning models. We measured activity from neurons in the superior colliculus (SC), a midbrain region involved in planning saccadic eye movements, while monkeys performed two saccade tasks. In the strategic task, monkeys competed against a computer in a saccade version of the mixed-strategy game "matching-pennies". In the instructed task, saccades were elicited through explicit instruction rather than free choices. In both tasks neuronal activity and behavior were shaped by past actions and rewards with more recent events exerting a larger influence. Further, SC activity predicted upcoming choices during the strategic task and upcoming reaction times during the instructed task. Finally, we found that neuronal activity in both tasks correlated with an established learning model, the Experience Weighted Attraction model of action valuation (Camerer and Ho, 1999). Collectively, our results provide evidence that action values hypothesized by learning models are represented in the motor planning regions of the brain in a manner that could be used to select strategic actions.

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  • doi:10.3389/neuro.08.057.2009

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James M. G. Tsui; J. N. Hunter; R. T. Born; Christopher C. Pack

The Role of V1 Surround Suppression in MT Motion Integration Journal Article

In: Journal of Neurophysiology, vol. 103, no. 6, pp. 3123–3138, 2010.

Abstract | Links | BibTeX

@article{Tsui2010,
title = {The Role of V1 Surround Suppression in MT Motion Integration},
author = {James M. G. Tsui and J. N. Hunter and R. T. Born and Christopher C. Pack},
doi = {10.1152/jn.00654.2009},
year = {2010},
date = {2010-01-01},
journal = {Journal of Neurophysiology},
volume = {103},
number = {6},
pages = {3123--3138},
abstract = {Neurons in the primate extrastriate cortex are highly selective for complex stimulus features such as faces, objects, and motion patterns. One explanation for this selectivity is that neurons in these areas carry out sophisticated computations on the outputs of lower-level areas such as primary visual cortex (V1), where neuronal selectivity is often modeled in terms of linear spatiotemporal filters. However, it has long been known that such simple V1 models are incomplete because they fail to capture important nonlinearities that can substantially alter neuronal selectivity for specific stimulus features. Thus a key step in understanding the function of higher cortical areas is the development of realistic models of their V1 inputs. We have addressed this issue by constructing a computational model of the V1 neurons that provide the strongest input to extrastriate cortical middle temporal (MT) area. We find that a modest elaboration to the standard model of V1 direction selectivity generates model neurons with strong end-stopping, a property that is also found in the V1 layers that provide input to MT. With this computational feature in place, the seemingly complex properties of MT neurons can be simulated by assuming that they perform a simple nonlinear summation of their inputs. The resulting model, which has a very small number of free parameters, can simulate many of the diverse properties of MT neurons. In particular, we simulate the invariance of MT tuning curves to the orientation and length of tilted bar stimuli, as well as the accompanying temporal dynamics. We also show how this property relates to the continuum from component to pattern selectivity observed when MT neurons are tested with plaids. Finally, we confirm several key predictions of the model by recording from MT neurons in the alert macaque monkey. Overall our results demonstrate that many of the seemingly complex computations carried out by high-level cortical neurons can in principle be understood by examining the properties of their inputs.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

Neurons in the primate extrastriate cortex are highly selective for complex stimulus features such as faces, objects, and motion patterns. One explanation for this selectivity is that neurons in these areas carry out sophisticated computations on the outputs of lower-level areas such as primary visual cortex (V1), where neuronal selectivity is often modeled in terms of linear spatiotemporal filters. However, it has long been known that such simple V1 models are incomplete because they fail to capture important nonlinearities that can substantially alter neuronal selectivity for specific stimulus features. Thus a key step in understanding the function of higher cortical areas is the development of realistic models of their V1 inputs. We have addressed this issue by constructing a computational model of the V1 neurons that provide the strongest input to extrastriate cortical middle temporal (MT) area. We find that a modest elaboration to the standard model of V1 direction selectivity generates model neurons with strong end-stopping, a property that is also found in the V1 layers that provide input to MT. With this computational feature in place, the seemingly complex properties of MT neurons can be simulated by assuming that they perform a simple nonlinear summation of their inputs. The resulting model, which has a very small number of free parameters, can simulate many of the diverse properties of MT neurons. In particular, we simulate the invariance of MT tuning curves to the orientation and length of tilted bar stimuli, as well as the accompanying temporal dynamics. We also show how this property relates to the continuum from component to pattern selectivity observed when MT neurons are tested with plaids. Finally, we confirm several key predictions of the model by recording from MT neurons in the alert macaque monkey. Overall our results demonstrate that many of the seemingly complex computations carried out by high-level cortical neurons can in principle be understood by examining the properties of their inputs.

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  • doi:10.1152/jn.00654.2009

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Joris Vangeneugden; Kathleen Vancleef; Tobias Jaeggli; VanGool. Luc; Rufin Vogels

Discrimination of locomotion direction in impoverished displays of walkers by macaque monkeys Journal Article

In: Journal of Vision, vol. 10, no. 4, pp. 1–19, 2010.

Abstract | Links | BibTeX

@article{Vangeneugden2010,
title = {Discrimination of locomotion direction in impoverished displays of walkers by macaque monkeys},
author = {Joris Vangeneugden and Kathleen Vancleef and Tobias Jaeggli and VanGool. Luc and Rufin Vogels},
doi = {10.1167/10.4.22},
year = {2010},
date = {2010-01-01},
journal = {Journal of Vision},
volume = {10},
number = {4},
pages = {1--19},
abstract = {A vast literature exists on human biological motion perception in impoverished displays, e.g., point-light walkers. Less is known about the perception of impoverished biological motion displays in macaques. We trained 3 macaques in the discrimination of facing direction (left versus right) and forward versus backward walking using motion-capture-based locomotion displays (treadmill walking) in which the body features were represented by cylinder-like primitives. The displays did not contain translatory motion. Discriminating forward versus backward locomotion requires motion information while the facing-direction/ view task can be solved using motion and/or form. All monkeys required lengthy training to learn the forward–backward task, while the view task was learned more quickly. Once acquired, the discriminations were specific to walking and stimulus format but generalized across actors. Although the view task could be solved using form cues, there was a small impact of motion. Performance in the forward–backward task was highly susceptible to degradations of spatiotemporal stimulus coherence and motion information. These results indicate that rhesus monkeys require extensive training in order to use the intrinsic motion cues related to forward versus backward locomotion and imply that extrapolation of observations concerning human perception of impoverished biological motion displays onto monkey perception needs to be made cautiously.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

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A vast literature exists on human biological motion perception in impoverished displays, e.g., point-light walkers. Less is known about the perception of impoverished biological motion displays in macaques. We trained 3 macaques in the discrimination of facing direction (left versus right) and forward versus backward walking using motion-capture-based locomotion displays (treadmill walking) in which the body features were represented by cylinder-like primitives. The displays did not contain translatory motion. Discriminating forward versus backward locomotion requires motion information while the facing-direction/ view task can be solved using motion and/or form. All monkeys required lengthy training to learn the forward–backward task, while the view task was learned more quickly. Once acquired, the discriminations were specific to walking and stimulus format but generalized across actors. Although the view task could be solved using form cues, there was a small impact of motion. Performance in the forward–backward task was highly susceptible to degradations of spatiotemporal stimulus coherence and motion information. These results indicate that rhesus monkeys require extensive training in order to use the intrinsic motion cues related to forward versus backward locomotion and imply that extrapolation of observations concerning human perception of impoverished biological motion displays onto monkey perception needs to be made cautiously.

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  • doi:10.1167/10.4.22

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Ben D. B. Willmore; Ryan J. Prenger; Jack L. Gallant

Neural representation of natural images in visual area V2 Journal Article

In: Journal of Neuroscience, vol. 30, no. 6, pp. 2102–2114, 2010.

Abstract | Links | BibTeX

@article{Willmore2010,
title = {Neural representation of natural images in visual area V2},
author = {Ben D. B. Willmore and Ryan J. Prenger and Jack L. Gallant},
doi = {10.1523/JNEUROSCI.4099-09.2010},
year = {2010},
date = {2010-01-01},
journal = {Journal of Neuroscience},
volume = {30},
number = {6},
pages = {2102--2114},
abstract = {Area V2 is a major visual processing stage in mammalian visual cortex, but little is currently known about how V2 encodes information during natural vision. To determine how V2 represents natural images, we used a novel nonlinear system identification approach to obtain quantitative estimates of spatial tuning across a large sample of V2 neurons. We compared these tuning estimates with those obtained in area V1, in which the neural code is relatively well understood. We find two subpopulations of neurons in V2. Approximately one-half of the V2 neurons have tuning that is similar to V1. The other half of the V2 neurons are selective for complex features such as those that occur in natural scenes. These neurons are distinguished from V1 neurons mainly by the presence of stronger suppressive tuning. Selectivity in these neurons therefore reflects a balance between excitatory and suppressive tuning for specific features. These results provide a new perspective on how complex shape selectivity arises, emphasizing the role of suppressive tuning in determining stimulus selectivity in higher visual cortex.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

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Area V2 is a major visual processing stage in mammalian visual cortex, but little is currently known about how V2 encodes information during natural vision. To determine how V2 represents natural images, we used a novel nonlinear system identification approach to obtain quantitative estimates of spatial tuning across a large sample of V2 neurons. We compared these tuning estimates with those obtained in area V1, in which the neural code is relatively well understood. We find two subpopulations of neurons in V2. Approximately one-half of the V2 neurons have tuning that is similar to V1. The other half of the V2 neurons are selective for complex features such as those that occur in natural scenes. These neurons are distinguished from V1 neurons mainly by the presence of stronger suppressive tuning. Selectivity in these neurons therefore reflects a balance between excitatory and suppressive tuning for specific features. These results provide a new perspective on how complex shape selectivity arises, emphasizing the role of suppressive tuning in determining stimulus selectivity in higher visual cortex.

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  • doi:10.1523/JNEUROSCI.4099-09.2010

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Theodoros P. Zanos; Patrick J. Mineault; Christopher C. Pack

Removal of spurious correlations between spikes and local field potentials Journal Article

In: Journal of Neurophysiology, vol. 105, pp. 474–486, 2010.

Abstract | Links | BibTeX

@article{Zanos2010,
title = {Removal of spurious correlations between spikes and local field potentials},
author = {Theodoros P. Zanos and Patrick J. Mineault and Christopher C. Pack},
doi = {10.1152/jn.00642.2010},
year = {2010},
date = {2010-01-01},
journal = {Journal of Neurophysiology},
volume = {105},
pages = {474--486},
abstract = {Single neurons carry out important sensory and motor functions related to the larger networks in which they are embedded. Under- standing the relationships between single-neuron spiking and network activity is therefore of great importance and the latter can be readily estimated from low-frequency brain signals known as local field potentials (LFPs). In this work we examine a number of issues related to the estimation of spike and LFP signals. We show that spike trains and individual spikes contain power at the frequencies that are typically thought to be exclusively related to LFPs, such that simple frequency-domain filtering cannot be effectively used to separate the two signals. Ground-truth simulations indicate that the commonly used method of estimating the LFP signal by low-pass filtering the raw voltage signal leads to artifactual correlations between spikes and LFPs and that these correlations exert a powerful influence on popular metrics of spike–LFP synchronization. Similar artifactual results were seen in data obtained from electrophysiological recordings in ma- caque visual cortex, when low-pass filtering was used to estimate LFP signals. In contrast LFP tuning curves in response to sensory stimuli do not appear to be affected by spike contamination, either in simulations or in real data. To address the issue of spike contamina- tion, we devised a novel Bayesian spike removal algorithm and confirmed its effectiveness in simulations and by applying it to the electrophysiological data. The algorithm, based on a rigorous math- ematical framework, outperforms other methods of spike removal on most metrics of spike–LFP correlations. Following application of this spike removal algorithm, many of our electrophysiological recordings continued to exhibit spike–LFP correlations, confirming previous reports that such relationships are a genuine aspect of neuronal activity. Overall, these results show that careful preprocessing is necessary to remove spikes from LFP signals, but that when effective spike removal is used, spike–LFP correlations can potentially yield novel insights about brain function.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

Single neurons carry out important sensory and motor functions related to the larger networks in which they are embedded. Under- standing the relationships between single-neuron spiking and network activity is therefore of great importance and the latter can be readily estimated from low-frequency brain signals known as local field potentials (LFPs). In this work we examine a number of issues related to the estimation of spike and LFP signals. We show that spike trains and individual spikes contain power at the frequencies that are typically thought to be exclusively related to LFPs, such that simple frequency-domain filtering cannot be effectively used to separate the two signals. Ground-truth simulations indicate that the commonly used method of estimating the LFP signal by low-pass filtering the raw voltage signal leads to artifactual correlations between spikes and LFPs and that these correlations exert a powerful influence on popular metrics of spike–LFP synchronization. Similar artifactual results were seen in data obtained from electrophysiological recordings in ma- caque visual cortex, when low-pass filtering was used to estimate LFP signals. In contrast LFP tuning curves in response to sensory stimuli do not appear to be affected by spike contamination, either in simulations or in real data. To address the issue of spike contamina- tion, we devised a novel Bayesian spike removal algorithm and confirmed its effectiveness in simulations and by applying it to the electrophysiological data. The algorithm, based on a rigorous math- ematical framework, outperforms other methods of spike removal on most metrics of spike–LFP correlations. Following application of this spike removal algorithm, many of our electrophysiological recordings continued to exhibit spike–LFP correlations, confirming previous reports that such relationships are a genuine aspect of neuronal activity. Overall, these results show that careful preprocessing is necessary to remove spikes from LFP signals, but that when effective spike removal is used, spike–LFP correlations can potentially yield novel insights about brain function.

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  • doi:10.1152/jn.00642.2010

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Xiaomo Chen; Katherine Wilson Scangos; Veit Stuphorn

Supplementary motor area exerts proactive and reactive control of arm movements Journal Article

In: Journal of Neuroscience, vol. 30, no. 44, pp. 14657–14675, 2010.

Abstract | Links | BibTeX

@article{Chen2010,
title = {Supplementary motor area exerts proactive and reactive control of arm movements},
author = {Xiaomo Chen and Katherine Wilson Scangos and Veit Stuphorn},
doi = {10.1523/JNEUROSCI.2669-10.2010},
year = {2010},
date = {2010-01-01},
journal = {Journal of Neuroscience},
volume = {30},
number = {44},
pages = {14657--14675},
abstract = {Adaptive behavior requires the ability to flexibly control actions. This can occur either proactively to anticipate task requirements, or reactively in response to sudden changes. Here we report neuronal activity in the supplementary motor area (SMA) that is correlated with both forms of behavioral control. Single-unit and multiunit activity and intracranial local field potentials (LFPs) were recorded in macaque monkeys during a stop-signal task, which elicits both proactive and reactive behavioral control. The LFP power in high- (60-150 Hz) and low- (25-40 Hz) frequency bands was significantly correlated with arm movement reaction time, starting before target onset. Multiunit and single-unit activity also showed a significant regression with reaction time. In addition, LFPs and multiunit and single-unit activity changed their activity level depending on the trial history, mirroring adjustments on the behavioral level. Together, these findings indicate that neuronal activity in the SMA exerts proactive control of arm movements by adjusting the level of motor readiness. On trials when the monkeys successfully canceled arm movements in response to an unforeseen stop signal, the LFP power, particularly in a low (10-50 Hz) frequency range, increased early enough to be causally related to the inhibition of the arm movement on those trials. This indicated that neuronal activity in the SMA is also involved in response inhibition in reaction to sudden task changes. Our findings indicate, therefore, that SMA plays a role in the proactive control of motor readiness and the reactive inhibition of unwanted movements.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

Adaptive behavior requires the ability to flexibly control actions. This can occur either proactively to anticipate task requirements, or reactively in response to sudden changes. Here we report neuronal activity in the supplementary motor area (SMA) that is correlated with both forms of behavioral control. Single-unit and multiunit activity and intracranial local field potentials (LFPs) were recorded in macaque monkeys during a stop-signal task, which elicits both proactive and reactive behavioral control. The LFP power in high- (60-150 Hz) and low- (25-40 Hz) frequency bands was significantly correlated with arm movement reaction time, starting before target onset. Multiunit and single-unit activity also showed a significant regression with reaction time. In addition, LFPs and multiunit and single-unit activity changed their activity level depending on the trial history, mirroring adjustments on the behavioral level. Together, these findings indicate that neuronal activity in the SMA exerts proactive control of arm movements by adjusting the level of motor readiness. On trials when the monkeys successfully canceled arm movements in response to an unforeseen stop signal, the LFP power, particularly in a low (10-50 Hz) frequency range, increased early enough to be causally related to the inhibition of the arm movement on those trials. This indicated that neuronal activity in the SMA is also involved in response inhibition in reaction to sudden task changes. Our findings indicate, therefore, that SMA plays a role in the proactive control of motor readiness and the reactive inhibition of unwanted movements.

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  • doi:10.1523/JNEUROSCI.2669-10.2010

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T. M. Desrochers; D. Z. Jin; N. D. Goodman; Ann M. Graybiel

Optimal habits can develop spontaneously through sensitivity to local cost Journal Article

In: Proceedings of the National Academy of Sciences, vol. 107, no. 47, pp. 20512–20517, 2010.

Abstract | Links | BibTeX

@article{Desrochers2010,
title = {Optimal habits can develop spontaneously through sensitivity to local cost},
author = {T. M. Desrochers and D. Z. Jin and N. D. Goodman and Ann M. Graybiel},
doi = {10.1073/pnas.1013470107},
year = {2010},
date = {2010-01-01},
journal = {Proceedings of the National Academy of Sciences},
volume = {107},
number = {47},
pages = {20512--20517},
abstract = {Habits and rituals are expressed universally across animal species. These behaviors are advantageous in allowing sequential behaviors to be performed without cognitive overload, and appear to rely on neural circuits that are relatively benign but vulnerable to takeover by extreme contexts, neuropsychiatric sequelae, and processes leading to addiction. Reinforcement learning (RL) is thought to underlie the formation of optimal habits. However, this theoretic formulation has principally been tested experimentally in simple stimulus-response tasks with relatively few available responses. We asked whether RL could also account for the emergence of habitual action sequences in realistically complex situations in which no repetitive stimulus-response links were present and in which many response options were present. We exposed naïve macaque monkeys to such experimental conditions by introducing a unique free saccade scan task. Despite the highly uncertain conditions and no instruction, the monkeys developed a succession of stereotypical, self-chosen saccade sequence patterns. Remarkably, these continued to morph for months, long after session-averaged reward and cost (eye movement distance) reached asymptote. Prima facie, these continued behavioral changes appeared to challenge RL. However, trial-by-trial analysis showed that pattern changes on adjacent trials were predicted by lowered cost, and RL simulations that reduced the cost reproduced the monkeys' behavior. Ultimately, the patterns settled into stereotypical saccade sequences that minimized the cost of obtaining the reward on average. These findings suggest that brain mechanisms underlying the emergence of habits, and perhaps unwanted repetitive behaviors in clinical disorders, could follow RL algorithms capturing extremely local explore/exploit tradeoffs.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

Habits and rituals are expressed universally across animal species. These behaviors are advantageous in allowing sequential behaviors to be performed without cognitive overload, and appear to rely on neural circuits that are relatively benign but vulnerable to takeover by extreme contexts, neuropsychiatric sequelae, and processes leading to addiction. Reinforcement learning (RL) is thought to underlie the formation of optimal habits. However, this theoretic formulation has principally been tested experimentally in simple stimulus-response tasks with relatively few available responses. We asked whether RL could also account for the emergence of habitual action sequences in realistically complex situations in which no repetitive stimulus-response links were present and in which many response options were present. We exposed naïve macaque monkeys to such experimental conditions by introducing a unique free saccade scan task. Despite the highly uncertain conditions and no instruction, the monkeys developed a succession of stereotypical, self-chosen saccade sequence patterns. Remarkably, these continued to morph for months, long after session-averaged reward and cost (eye movement distance) reached asymptote. Prima facie, these continued behavioral changes appeared to challenge RL. However, trial-by-trial analysis showed that pattern changes on adjacent trials were predicted by lowered cost, and RL simulations that reduced the cost reproduced the monkeys' behavior. Ultimately, the patterns settled into stereotypical saccade sequences that minimized the cost of obtaining the reward on average. These findings suggest that brain mechanisms underlying the emergence of habits, and perhaps unwanted repetitive behaviors in clinical disorders, could follow RL algorithms capturing extremely local explore/exploit tradeoffs.

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  • doi:10.1073/pnas.1013470107

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Alexander Maier; Geoffrey K. Adams; Christopher Aura; David A. Leopold

Distinct superficial and deep laminar domains of activity in the visual cortex during rest and stimulation Journal Article

In: Frontiers in Systems Neuroscience, vol. 4, pp. 1–11, 2010.

Abstract | Links | BibTeX

@article{Maier2010,
title = {Distinct superficial and deep laminar domains of activity in the visual cortex during rest and stimulation},
author = {Alexander Maier and Geoffrey K. Adams and Christopher Aura and David A. Leopold},
doi = {10.3389/fnsys.2010.00031},
year = {2010},
date = {2010-01-01},
journal = {Frontiers in Systems Neuroscience},
volume = {4},
pages = {1--11},
abstract = {Spatial patterns of spontaneous neural activity at rest have previously been associated with specific networks in the brain, including those pertaining to the functional architecture of the primary visual cortex (V1). However, despite the prominent anatomical differences between cortical layers, little is known about the laminar pattern of spontaneous activity in V1. We address this topic by investigating the amplitude and coherence of ongoing local field potential (LFP) signals measured from different layers in V1 of macaque monkeys during rest and upon presentation of a visual stimulus. We used a linear microelectrode array to measure LFP signals at multiple, evenly spaced positions throughout the cortical thickness. Analyzing both the mean LFP amplitudes and between-contact LFP coherences, we identified two distinct zones of activity, roughly corresponding to superficial and deep layers, divided by a sharp transition near the bottom of layer 4. The LFP signals within each laminar zone were highly coherent, whereas those between zones were not. This functional compartmentalization was found not only during rest, but also when the receptive field was stimulated during a visual task. These results demonstrate the existence of distinct superficial and deep functional domains of coherent LFP activity in V1 that may reflect the intrinsic interplay of V1 microcircuitry with cortical and subcortical targets, respectively.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

Spatial patterns of spontaneous neural activity at rest have previously been associated with specific networks in the brain, including those pertaining to the functional architecture of the primary visual cortex (V1). However, despite the prominent anatomical differences between cortical layers, little is known about the laminar pattern of spontaneous activity in V1. We address this topic by investigating the amplitude and coherence of ongoing local field potential (LFP) signals measured from different layers in V1 of macaque monkeys during rest and upon presentation of a visual stimulus. We used a linear microelectrode array to measure LFP signals at multiple, evenly spaced positions throughout the cortical thickness. Analyzing both the mean LFP amplitudes and between-contact LFP coherences, we identified two distinct zones of activity, roughly corresponding to superficial and deep layers, divided by a sharp transition near the bottom of layer 4. The LFP signals within each laminar zone were highly coherent, whereas those between zones were not. This functional compartmentalization was found not only during rest, but also when the receptive field was stimulated during a visual task. These results demonstrate the existence of distinct superficial and deep functional domains of coherent LFP activity in V1 that may reflect the intrinsic interplay of V1 microcircuitry with cortical and subcortical targets, respectively.

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  • doi:10.3389/fnsys.2010.00031

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John M. Pearson; Benjamin Y. Hayden; Michael L. Platt

Explicit information reduces discounting behavior in monkeys Journal Article

In: Frontiers in Psychology, vol. 1, pp. 237, 2010.

Abstract | Links | BibTeX

@article{Pearson2010,
title = {Explicit information reduces discounting behavior in monkeys},
author = {John M. Pearson and Benjamin Y. Hayden and Michael L. Platt},
doi = {10.3389/fpsyg.2010.00237},
year = {2010},
date = {2010-01-01},
journal = {Frontiers in Psychology},
volume = {1},
pages = {237},
publisher = {10},
address = {doi},
abstract = {Animals are notoriously impulsive in common laboratory experiments, preferring smaller, sooner rewards to larger, delayed rewards even when this reduces average reward rates. By contrast, the same animals often engage in natural behaviors that require extreme patience, such as food caching, stalking prey, and traveling long distances to high-quality food sites. One possible explanation for this discrepancy is that standard laboratory delay discounting tasks artificially inflate impulsivity by subverting animals' common learning strategies. To test this idea, we examined choices made by rhesus macaques in two variants of a standard delay discounting task. In the conventional variant, post-reward delays were uncued and adjusted to render total trial length constant; in the second, all delays were cued explicitly. We found that measured discounting was significantly reduced in the cued task, with discount parameters well below those reported in studies using the standard uncued design. When monkeys had complete information, their decisions were more consistent with a strategy of reward rate maximization. These results indicate that monkeys, and perhaps other animals, are more patient than is normally assumed, and that laboratory measures of delay discounting may overstate impulsivity.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

Animals are notoriously impulsive in common laboratory experiments, preferring smaller, sooner rewards to larger, delayed rewards even when this reduces average reward rates. By contrast, the same animals often engage in natural behaviors that require extreme patience, such as food caching, stalking prey, and traveling long distances to high-quality food sites. One possible explanation for this discrepancy is that standard laboratory delay discounting tasks artificially inflate impulsivity by subverting animals' common learning strategies. To test this idea, we examined choices made by rhesus macaques in two variants of a standard delay discounting task. In the conventional variant, post-reward delays were uncued and adjusted to render total trial length constant; in the second, all delays were cued explicitly. We found that measured discounting was significantly reduced in the cued task, with discount parameters well below those reported in studies using the standard uncued design. When monkeys had complete information, their decisions were more consistent with a strategy of reward rate maximization. These results indicate that monkeys, and perhaps other animals, are more patient than is normally assumed, and that laboratory measures of delay discounting may overstate impulsivity.

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  • doi:10.3389/fpsyg.2010.00237

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Emilio Salinas; Swetha Shankar; M. Gabriela Costello; Dantong Zhu; Terrence R. Stanford

Waiting is the hardest part: Comparison of two computational strategies for performing a compelled-response task Journal Article

In: Frontiers in Computational Neuroscience, vol. 4, pp. 153, 2010.

Abstract | Links | BibTeX

@article{Salinas2010,
title = {Waiting is the hardest part: Comparison of two computational strategies for performing a compelled-response task},
author = {Emilio Salinas and Swetha Shankar and M. Gabriela Costello and Dantong Zhu and Terrence R. Stanford},
doi = {10.3389/fncom.2010.00153},
year = {2010},
date = {2010-01-01},
journal = {Frontiers in Computational Neuroscience},
volume = {4},
pages = {153},
publisher = {10},
address = {doi},
abstract = {The neural basis of choice behavior is commonly investigated with tasks in which a subject analyzes a stimulus and reports his or her perceptual experience with an appropriate motor action. We recently developed a novel task, the compelled-saccade task, with which the influence of the sensory information on the subject's choice can be tracked through time with millisecond resolution, thus providing a new tool for correlating neuronal activity and behavior. This paradigm has a crucial feature: the signal that instructs the subject to make an eye movement is given before the cue that indicates which of two possible choices is the correct one. Previously, we found that psychophysical performance in this task could be accurately replicated by a model in which two developing oculomotor plans race to a threshold and the incoming perceptual information differentially accelerates their trajectories toward it. However, the task design suggests an alternative mechanism: instead of modifying an ongoing oculomotor plan on the fly as the sensory information becomes available, the subject could try to wait, withholding the oculomotor response until the sensory cue is revealed. Here, we use computer simulations to explore and compare the performance of these two types of model. We find that both reproduce the main features of the psychophysical data in the compelled-saccade task, but they give rise to distinct behavioral and neurophysiological predictions. Although, superficially, the waiting model is intuitively appealing, it is ultimately inconsistent with experimental results from this and other tasks.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

The neural basis of choice behavior is commonly investigated with tasks in which a subject analyzes a stimulus and reports his or her perceptual experience with an appropriate motor action. We recently developed a novel task, the compelled-saccade task, with which the influence of the sensory information on the subject's choice can be tracked through time with millisecond resolution, thus providing a new tool for correlating neuronal activity and behavior. This paradigm has a crucial feature: the signal that instructs the subject to make an eye movement is given before the cue that indicates which of two possible choices is the correct one. Previously, we found that psychophysical performance in this task could be accurately replicated by a model in which two developing oculomotor plans race to a threshold and the incoming perceptual information differentially accelerates their trajectories toward it. However, the task design suggests an alternative mechanism: instead of modifying an ongoing oculomotor plan on the fly as the sensory information becomes available, the subject could try to wait, withholding the oculomotor response until the sensory cue is revealed. Here, we use computer simulations to explore and compare the performance of these two types of model. We find that both reproduce the main features of the psychophysical data in the compelled-saccade task, but they give rise to distinct behavioral and neurophysiological predictions. Although, superficially, the waiting model is intuitively appealing, it is ultimately inconsistent with experimental results from this and other tasks.

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  • doi:10.3389/fncom.2010.00153

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Victor Sander; Brian Soper; Stefan Everling

Nonhuman primate event-related potentials associated with pro- and anti-saccades Journal Article

In: NeuroImage, vol. 49, no. 2, pp. 1650–1658, 2010.

Abstract | Links | BibTeX

@article{Sander2010,
title = {Nonhuman primate event-related potentials associated with pro- and anti-saccades},
author = {Victor Sander and Brian Soper and Stefan Everling},
doi = {10.1016/j.neuroimage.2009.09.038},
year = {2010},
date = {2010-01-01},
journal = {NeuroImage},
volume = {49},
number = {2},
pages = {1650--1658},
abstract = {Non-invasive event-related potential (ERP) recordings have become a popular technique to study neural activity associated with saccades in humans. To date, it is not known whether nonhuman primates exhibit similar saccade-related ERPs. Here, we recorded ERPs associated with the performance of randomly interleaved pro- and anti-saccades in macaque monkeys. Stimulus-aligned ERPs showed short-latency visual component with more negative P2 and N2 peak amplitudes on anti- than on pro-saccade trials. Saccade-aligned ERPs showed a larger presaccadic negativity on anti- than pro-saccade trials, and a presaccadic positivity on pro-saccade trials, which was attenuated or absent on anti-saccade trials. This was followed by sharp negative spike potential immediately prior to the movement. Overall, these findings demonstrate that macaque monkeys, like humans, exhibit task-related differences of visual ERPs associated with pro- and anti-saccades and furthermore share presaccadic positivity as well as a spike potential prior to these tasks. We suggest that the presaccadic positivity on pro-saccade trials is generated by a source in the contralateral frontal eye fields and that the more negative voltage on anti-saccade trials is the result of additional sources of opposite polarity in neighboring frontal areas.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

Non-invasive event-related potential (ERP) recordings have become a popular technique to study neural activity associated with saccades in humans. To date, it is not known whether nonhuman primates exhibit similar saccade-related ERPs. Here, we recorded ERPs associated with the performance of randomly interleaved pro- and anti-saccades in macaque monkeys. Stimulus-aligned ERPs showed short-latency visual component with more negative P2 and N2 peak amplitudes on anti- than on pro-saccade trials. Saccade-aligned ERPs showed a larger presaccadic negativity on anti- than pro-saccade trials, and a presaccadic positivity on pro-saccade trials, which was attenuated or absent on anti-saccade trials. This was followed by sharp negative spike potential immediately prior to the movement. Overall, these findings demonstrate that macaque monkeys, like humans, exhibit task-related differences of visual ERPs associated with pro- and anti-saccades and furthermore share presaccadic positivity as well as a spike potential prior to these tasks. We suggest that the presaccadic positivity on pro-saccade trials is generated by a source in the contralateral frontal eye fields and that the more negative voltage on anti-saccade trials is the result of additional sources of opposite polarity in neighboring frontal areas.

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  • doi:10.1016/j.neuroimage.2009.09.038

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Katherine Wilson Scangos; Veit Stuphorn

Medial frontal cortex motivates but does not control movement initiation in the countermanding task Journal Article

In: Journal of Neuroscience, vol. 30, no. 5, pp. 1968–1982, 2010.

Abstract | Links | BibTeX

@article{Scangos2010,
title = {Medial frontal cortex motivates but does not control movement initiation in the countermanding task},
author = {Katherine Wilson Scangos and Veit Stuphorn},
doi = {10.1523/JNEUROSCI.4509-09.2010},
year = {2010},
date = {2010-01-01},
journal = {Journal of Neuroscience},
volume = {30},
number = {5},
pages = {1968--1982},
abstract = {Voluntary control of behavior implies the ability to select what action is performed. The supplementary motor area (SMA) and pre-SMA are widely considered to be of central importance for this ability because of their role in movement initiation and inhibition. To test this hypothesis, we recorded from neurons in SMA and pre-SMA of monkeys performing an arm countermanding task. Temporal analysis of neural activity and behavior in this task allowed us to test whether neural activity is sufficient to control movement initiation or inhibition. Surprisingly, 99% (242 of 243) of movement-related neurons in SMA and pre-SMA failed to exhibit time-locked activity changes predictive of movement initiation in this task. We also found a second group of neurons that was more active during successful response cancelation. Of these putative inhibitory cells, 18% (7 of 40) responded early enough to be able to influence the cancelation of the movement. Thus, when tested with the countermanding task, the SMA/pre-SMA region may play a role in movement inhibition but does not appear to control movement initiation. However, the activity of 76% (202 of 267) of movement-related neurons was contingent on the expectation of reward and 42% of them reflected the amount of expected reward. These findings suggest that the movement-related activity in pre-SMA and SMA might represent the motivation for a specific action but does not determine whether or not that action is performed. This motivational signal in pre-SMA and SMA could provide an essential link between reward expectation and motor execution.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

Voluntary control of behavior implies the ability to select what action is performed. The supplementary motor area (SMA) and pre-SMA are widely considered to be of central importance for this ability because of their role in movement initiation and inhibition. To test this hypothesis, we recorded from neurons in SMA and pre-SMA of monkeys performing an arm countermanding task. Temporal analysis of neural activity and behavior in this task allowed us to test whether neural activity is sufficient to control movement initiation or inhibition. Surprisingly, 99% (242 of 243) of movement-related neurons in SMA and pre-SMA failed to exhibit time-locked activity changes predictive of movement initiation in this task. We also found a second group of neurons that was more active during successful response cancelation. Of these putative inhibitory cells, 18% (7 of 40) responded early enough to be able to influence the cancelation of the movement. Thus, when tested with the countermanding task, the SMA/pre-SMA region may play a role in movement inhibition but does not appear to control movement initiation. However, the activity of 76% (202 of 267) of movement-related neurons was contingent on the expectation of reward and 42% of them reflected the amount of expected reward. These findings suggest that the movement-related activity in pre-SMA and SMA might represent the motivation for a specific action but does not determine whether or not that action is performed. This motivational signal in pre-SMA and SMA could provide an essential link between reward expectation and motor execution.

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  • doi:10.1523/JNEUROSCI.4509-09.2010

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Jedediah M. Singer; David L. Sheinberg

Temporal cortex neurons encode articulated actions as slow sequences of integrated poses Journal Article

In: Journal of Neuroscience, vol. 30, no. 8, pp. 3133–3145, 2010.

Abstract | Links | BibTeX

@article{Singer2010,
title = {Temporal cortex neurons encode articulated actions as slow sequences of integrated poses},
author = {Jedediah M. Singer and David L. Sheinberg},
doi = {10.1523/JNEUROSCI.3211-09.2010},
year = {2010},
date = {2010-01-01},
journal = {Journal of Neuroscience},
volume = {30},
number = {8},
pages = {3133--3145},
abstract = {Form and motion processing pathways of the primate visual system are known to be interconnected, but there has been surprisingly little investigation of how they interact at the cellular level. Here we explore this issue with a series of three electrophysiology experiments designed to reveal the sources of action selectivity in monkey temporal cortex neurons. Monkeys discriminated between actions performed by complex, richly textured, rendered bipedal figures and hands. The firing patterns of neurons contained enough information to discriminate the identity of the character, the action performed, and the particular conjunction of action and character. This suggests convergence of motion and form information within single cells. Form and motion information in isolation were both sufficient to drive action discrimination within these neurons, but removing form information caused a greater disruption to the original response. Finally, we investigated the temporal window across which visual information is integrated into a single pose (or, equivalently, the timing with which poses are differentiated). Temporal cortex neurons under normal conditions represent actions as sequences of poses integrated over approximately 120 ms. They receive both motion and form information, however, and can use either if the other is absent.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

Form and motion processing pathways of the primate visual system are known to be interconnected, but there has been surprisingly little investigation of how they interact at the cellular level. Here we explore this issue with a series of three electrophysiology experiments designed to reveal the sources of action selectivity in monkey temporal cortex neurons. Monkeys discriminated between actions performed by complex, richly textured, rendered bipedal figures and hands. The firing patterns of neurons contained enough information to discriminate the identity of the character, the action performed, and the particular conjunction of action and character. This suggests convergence of motion and form information within single cells. Form and motion information in isolation were both sufficient to drive action discrimination within these neurons, but removing form information caused a greater disruption to the original response. Finally, we investigated the temporal window across which visual information is integrated into a single pose (or, equivalently, the timing with which poses are differentiated). Temporal cortex neurons under normal conditions represent actions as sequences of poses integrated over approximately 120 ms. They receive both motion and form information, however, and can use either if the other is absent.

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  • doi:10.1523/JNEUROSCI.3211-09.2010

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NaYoung So; Veit Stuphorn

Supplementary eye field encodes option and action value for saccades with variable reward Journal Article

In: Journal of Neurophysiology, vol. 104, pp. 2634–2653, 2010.

Abstract | Links | BibTeX

@article{So2010,
title = {Supplementary eye field encodes option and action value for saccades with variable reward},
author = {NaYoung So and Veit Stuphorn},
doi = {10.1080/07317131.2013.759831},
year = {2010},
date = {2010-01-01},
journal = {Journal of Neurophysiology},
volume = {104},
pages = {2634--2653},
abstract = {We recorded neuronal activity in the supplementary eye field (SEF) while monkeys made saccades to targets that yielded rewards of variable amount and uncertainty of delivery. Some SEF cells (29%) represented the anticipated value of the saccade target. These neurons encoded the value of the reward option but did not reflect the action necessary to obtain the reward. A plurality of cells (45%) represented both saccade direction and value. These neurons reflect action value, i.e., the value that is expected to follow from a specific saccade. Other cells (13%) represented only saccade direction. The SEF neurons matched the monkey's risk-seeking behavior by responding more strongly to the uncertain reward options than would be expected based on their response to the sure options and the cued outcome probability. Thus SEF neurons represented subjective, not expected, value. Across the SEF population, option-value signals developed early, ∼120 ms prior to saccade execution. Action-value and saccade direction signals developed ∼60 ms later. These results suggest that the SEF is involved in transforming option-value signals into action-value signals. However, in contrast to other oculomotor neurons, SEF neurons did not reach a constant level of activity before saccade onset. Instead the activity level of many (52%) SEF neurons still reflected value at the time just before saccade initiation. This suggests that SEF neurons guide the selection of a saccade based on value information but do not participate in the initiation of that saccade.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

We recorded neuronal activity in the supplementary eye field (SEF) while monkeys made saccades to targets that yielded rewards of variable amount and uncertainty of delivery. Some SEF cells (29%) represented the anticipated value of the saccade target. These neurons encoded the value of the reward option but did not reflect the action necessary to obtain the reward. A plurality of cells (45%) represented both saccade direction and value. These neurons reflect action value, i.e., the value that is expected to follow from a specific saccade. Other cells (13%) represented only saccade direction. The SEF neurons matched the monkey's risk-seeking behavior by responding more strongly to the uncertain reward options than would be expected based on their response to the sure options and the cued outcome probability. Thus SEF neurons represented subjective, not expected, value. Across the SEF population, option-value signals developed early, ∼120 ms prior to saccade execution. Action-value and saccade direction signals developed ∼60 ms later. These results suggest that the SEF is involved in transforming option-value signals into action-value signals. However, in contrast to other oculomotor neurons, SEF neurons did not reach a constant level of activity before saccade onset. Instead the activity level of many (52%) SEF neurons still reflected value at the time just before saccade initiation. This suggests that SEF neurons guide the selection of a saccade based on value information but do not participate in the initiation of that saccade.

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  • doi:10.1080/07317131.2013.759831

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Joo-Hyun Song; Robert M. McPeek

Roles of narrow- and broad-spiking dorsal premotor area neurons in reach target selection and movement production Journal Article

In: Journal of Neurophysiology, vol. 103, no. 4, pp. 2124–2138, 2010.

Abstract | Links | BibTeX

@article{Song2010,
title = {Roles of narrow- and broad-spiking dorsal premotor area neurons in reach target selection and movement production},
author = {Joo-Hyun Song and Robert M. McPeek},
doi = {10.1152/jn.00238.2009},
year = {2010},
date = {2010-01-01},
journal = {Journal of Neurophysiology},
volume = {103},
number = {4},
pages = {2124--2138},
abstract = {Most visual scenes are complex and crowded, with several different objects competing for attention and action. Thus a complete understanding of the production of goal-directed actions must incorporate the higher-level process of target selection. To examine the neural substrates of target selection for visually guided reaching, we recorded the activity of isolated neurons in the dorsal premotor area (PMd) of monkeys performing a reaction-time visual search task. In this task, monkeys reached to an odd-colored target presented with three distractors. We found that PMd neurons typically discriminate the target before movement onset, ∼150-200 ms after the appearance of the search array. In one subset of neurons, discrimination occurred at a consistent time after search array onset regardless of when the reaching movement occurred, suggesting that these neurons are involved in target selection. In a second group of neurons, discrimination time depended on reach reaction time, consistent with involvement in movement production but not in target selection. To look for physiological corroboration of these two functionally defined groups, we analyzed the extracellular spike waveforms of recorded neurons. This analysis showed a population of neurons with narrow action potentials that carried signals related to target selection. A second population with broader action potentials was more heterogeneous, with some neurons showing activity related to target selection and others showing only movement production activity. These results suggest that PMd contains signals related to target selection and movement execution and that different signals are carried by distinct neural subpopulations.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

Most visual scenes are complex and crowded, with several different objects competing for attention and action. Thus a complete understanding of the production of goal-directed actions must incorporate the higher-level process of target selection. To examine the neural substrates of target selection for visually guided reaching, we recorded the activity of isolated neurons in the dorsal premotor area (PMd) of monkeys performing a reaction-time visual search task. In this task, monkeys reached to an odd-colored target presented with three distractors. We found that PMd neurons typically discriminate the target before movement onset, ∼150-200 ms after the appearance of the search array. In one subset of neurons, discrimination occurred at a consistent time after search array onset regardless of when the reaching movement occurred, suggesting that these neurons are involved in target selection. In a second group of neurons, discrimination time depended on reach reaction time, consistent with involvement in movement production but not in target selection. To look for physiological corroboration of these two functionally defined groups, we analyzed the extracellular spike waveforms of recorded neurons. This analysis showed a population of neurons with narrow action potentials that carried signals related to target selection. A second population with broader action potentials was more heterogeneous, with some neurons showing activity related to target selection and others showing only movement production activity. These results suggest that PMd contains signals related to target selection and movement execution and that different signals are carried by distinct neural subpopulations.

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  • doi:10.1152/jn.00238.2009

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Terrence R. Stanford; Swetha Shankar; Dino P. Massoglia; M. Gabriela Costello; Emilio Salinas

Perceptual decision making in less than 30 milliseconds Journal Article

In: Nature Neuroscience, vol. 13, no. 3, pp. 379–385, 2010.

Abstract | Links | BibTeX

@article{Stanford2010,
title = {Perceptual decision making in less than 30 milliseconds},
author = {Terrence R. Stanford and Swetha Shankar and Dino P. Massoglia and M. Gabriela Costello and Emilio Salinas},
doi = {10.1038/nn.2485},
year = {2010},
date = {2010-01-01},
journal = {Nature Neuroscience},
volume = {13},
number = {3},
pages = {379--385},
publisher = {Nature Publishing Group},
abstract = {In perceptual discrimination tasks, a subject's response time is determined by both sensory and motor processes. Measuring the time consumed by the perceptual evaluation step alone is therefore complicated by factors such as motor preparation, task difficulty and speed-accuracy tradeoffs. Here we present a task design that minimizes these confounding factors and allows us to track a subject's perceptual performance with unprecedented temporal resolution. We find that monkeys can make accurate color discriminations in less than 30 ms. Furthermore, our simple task design provides a tool for elucidating how neuronal activity relates to sensory as opposed to motor processing, as demonstrated with neural data from cortical oculomotor neurons. In these cells, perceptual information acts by accelerating and decelerating the ongoing motor plans associated with correct and incorrect choices, as predicted by a race-to-threshold model, and the time course of these neural events parallels the time course of the subject's choice accuracy.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

In perceptual discrimination tasks, a subject's response time is determined by both sensory and motor processes. Measuring the time consumed by the perceptual evaluation step alone is therefore complicated by factors such as motor preparation, task difficulty and speed-accuracy tradeoffs. Here we present a task design that minimizes these confounding factors and allows us to track a subject's perceptual performance with unprecedented temporal resolution. We find that monkeys can make accurate color discriminations in less than 30 ms. Furthermore, our simple task design provides a tool for elucidating how neuronal activity relates to sensory as opposed to motor processing, as demonstrated with neural data from cortical oculomotor neurons. In these cells, perceptual information acts by accelerating and decelerating the ongoing motor plans associated with correct and incorrect choices, as predicted by a race-to-threshold model, and the time course of these neural events parallels the time course of the subject's choice accuracy.

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  • doi:10.1038/nn.2485

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2009

John M. Pearson; Benjamin Y. Hayden; Sridhar Raghavachari; Michael L. Platt

Neurons in posterior cingulate cortex signal exploratory decisions in a dynamic multioption choice task Journal Article

In: Current Biology, vol. 19, no. 18, pp. 1532–1537, 2009.

Abstract | Links | BibTeX

@article{Pearson2009,
title = {Neurons in posterior cingulate cortex signal exploratory decisions in a dynamic multioption choice task},
author = {John M. Pearson and Benjamin Y. Hayden and Sridhar Raghavachari and Michael L. Platt},
doi = {10.1016/j.cub.2009.07.048},
year = {2009},
date = {2009-01-01},
journal = {Current Biology},
volume = {19},
number = {18},
pages = {1532--1537},
publisher = {Elsevier Ltd},
abstract = {In dynamic environments, adaptive behavior requires striking a balance between harvesting currently available rewards (exploitation) and gathering information about alternative options (exploration) [1-4]. Such strategic decisions should incorporate not only recent reward history, but also opportunity costs and environmental statistics. Previous neuroimaging [5-8] and neurophysiological [9-13] studies have implicated orbitofrontal cortex, anterior cingulate cortex, and ventral striatum in distinguishing between bouts of exploration and exploitation. Nonetheless, the neuronal mechanisms that underlie strategy selection remain poorly understood. We hypothesized that posterior cingulate cortex (CGp), an area linking reward processing, attention [14], memory [15, 16], and motor control systems [17], mediates the integration of variables such as reward [18], uncertainty [19], and target location [20] that underlie this dynamic balance. Here we show that CGp neurons distinguish between exploratory and exploitative decisions made by monkeys in a dynamic foraging task. Moreover, firing rates of these neurons predict in graded fashion the strategy most likely to be selected on upcoming trials. This encoding is distinct from switching between targets and is independent of the absolute magnitudes of rewards. These observations implicate CGp in the integration of individual outcomes across decision making and the modification of strategy in dynamic environments.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

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In dynamic environments, adaptive behavior requires striking a balance between harvesting currently available rewards (exploitation) and gathering information about alternative options (exploration) [1-4]. Such strategic decisions should incorporate not only recent reward history, but also opportunity costs and environmental statistics. Previous neuroimaging [5-8] and neurophysiological [9-13] studies have implicated orbitofrontal cortex, anterior cingulate cortex, and ventral striatum in distinguishing between bouts of exploration and exploitation. Nonetheless, the neuronal mechanisms that underlie strategy selection remain poorly understood. We hypothesized that posterior cingulate cortex (CGp), an area linking reward processing, attention [14], memory [15, 16], and motor control systems [17], mediates the integration of variables such as reward [18], uncertainty [19], and target location [20] that underlie this dynamic balance. Here we show that CGp neurons distinguish between exploratory and exploitative decisions made by monkeys in a dynamic foraging task. Moreover, firing rates of these neurons predict in graded fashion the strategy most likely to be selected on upcoming trials. This encoding is distinct from switching between targets and is independent of the absolute magnitudes of rewards. These observations implicate CGp in the integration of individual outcomes across decision making and the modification of strategy in dynamic environments.

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  • doi:10.1016/j.cub.2009.07.048

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Stephen V. Shepherd; Jeffrey T. Klein; Robert O. Deaner; Michael L. Platt

Mirroring of attention by neurons in macaque parietal cortex Journal Article

In: Proceedings of the National Academy of Sciences, vol. 106, no. 23, pp. 9489–9494, 2009.

Abstract | Links | BibTeX

@article{Shepherd2009,
title = {Mirroring of attention by neurons in macaque parietal cortex},
author = {Stephen V. Shepherd and Jeffrey T. Klein and Robert O. Deaner and Michael L. Platt},
doi = {10.1093/joclec/nhs015},
year = {2009},
date = {2009-01-01},
journal = {Proceedings of the National Academy of Sciences},
volume = {106},
number = {23},
pages = {9489--9494},
abstract = {Macaques, like humans, rapidly orient their attention in the direction other individuals are looking. Both cortical and subcortical pathways have been proposed as neural mediators of social gaze following, but neither pathway has been characterized electrophysiologically in behaving animals. To address this gap, we recorded the activity of single neurons in the lateral intraparietal area (LIP) of rhesus macaques to determine whether and how this area might contribute to gaze following. A subset of LIP neurons mirrored observed attention by firing both when the subject looked in the preferred direction of the neuron, and when observed monkeys looked in the preferred direction of the neuron, despite the irrelevance of the monkey images to the task. Importantly, the timing of these modulations matched the time course of gaze-following behavior. A second population of neurons was suppressed by social gaze cues, possibly subserving task demands by maintaining fixation on the observed face. These observations suggest that LIP contributes to sharing of observed attention and link mirror representations in parietal cortex to a well studied imitative behavior.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

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Macaques, like humans, rapidly orient their attention in the direction other individuals are looking. Both cortical and subcortical pathways have been proposed as neural mediators of social gaze following, but neither pathway has been characterized electrophysiologically in behaving animals. To address this gap, we recorded the activity of single neurons in the lateral intraparietal area (LIP) of rhesus macaques to determine whether and how this area might contribute to gaze following. A subset of LIP neurons mirrored observed attention by firing both when the subject looked in the preferred direction of the neuron, and when observed monkeys looked in the preferred direction of the neuron, despite the irrelevance of the monkey images to the task. Importantly, the timing of these modulations matched the time course of gaze-following behavior. A second population of neurons was suppressed by social gaze cues, possibly subserving task demands by maintaining fixation on the observed face. These observations suggest that LIP contributes to sharing of observed attention and link mirror representations in parietal cortex to a well studied imitative behavior.

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  • doi:10.1093/joclec/nhs015

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Joo-Hyun Song; Robert M. McPeek

Eye-hand coordination during target selection in a pop-out visual search Journal Article

In: Journal of Neurophysiology, vol. 102, no. 5, pp. 2681–2692, 2009.

Abstract | Links | BibTeX

@article{Song2009,
title = {Eye-hand coordination during target selection in a pop-out visual search},
author = {Joo-Hyun Song and Robert M. McPeek},
doi = {10.1152/jn.91352.2008},
year = {2009},
date = {2009-01-01},
journal = {Journal of Neurophysiology},
volume = {102},
number = {5},
pages = {2681--2692},
abstract = {We examined the coordination of saccades and reaches in a visual search task in which monkeys were rewarded for reaching to an odd-colored target among distractors. Eye movements were unconstrained, and monkeys typically made one or more saccades before initiating a reach. Target selection for reaching and saccades was highly correlated with the hand and eyes landing near the same final stimulus both for correct reaches to the target and for incorrect reaches to a distractor. Incorrect reaches showed a bias in target selection: they were directed to the distractor in the same hemifield as the target more often than to other distractors. A similar bias was seen in target selection for the initial saccade in correct reaching trials with multiple saccades. We also examined the temporal coupling of saccades and reaches. In trials with a single saccade, a reaching movement was made after a fairly stereotyped delay. In multiple-saccade trials, a reach to the target could be initiated near or even before the onset of the final target-directed saccade. In these trials, the initial trajectory of the reach was often directed toward the fixated distractor before veering toward the target around the time of the final saccade. In virtually all cases, the eyes arrived at the target before the hand, and remained fixated until reach completion. Overall, these results are consistent with flexible temporal coupling of saccade and reach initiation, but fairly tight coupling of target selection for the two types of action.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

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We examined the coordination of saccades and reaches in a visual search task in which monkeys were rewarded for reaching to an odd-colored target among distractors. Eye movements were unconstrained, and monkeys typically made one or more saccades before initiating a reach. Target selection for reaching and saccades was highly correlated with the hand and eyes landing near the same final stimulus both for correct reaches to the target and for incorrect reaches to a distractor. Incorrect reaches showed a bias in target selection: they were directed to the distractor in the same hemifield as the target more often than to other distractors. A similar bias was seen in target selection for the initial saccade in correct reaching trials with multiple saccades. We also examined the temporal coupling of saccades and reaches. In trials with a single saccade, a reaching movement was made after a fairly stereotyped delay. In multiple-saccade trials, a reach to the target could be initiated near or even before the onset of the final target-directed saccade. In these trials, the initial trajectory of the reach was often directed toward the fixated distractor before veering toward the target around the time of the final saccade. In virtually all cases, the eyes arrived at the target before the hand, and remained fixated until reach completion. Overall, these results are consistent with flexible temporal coupling of saccade and reach initiation, but fairly tight coupling of target selection for the two types of action.

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  • doi:10.1152/jn.91352.2008

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Siddharth Srivastava; Guy A. Orban; Patrick A. De Maziere; Peter Janssen

A distinct representation of three-dimensional shape in macaque anterior intraparietal area: Fast, metric, and coarse Journal Article

In: Journal of Neuroscience, vol. 29, no. 34, pp. 10613–10626, 2009.

Abstract | Links | BibTeX

@article{Srivastava2009,
title = {A distinct representation of three-dimensional shape in macaque anterior intraparietal area: Fast, metric, and coarse},
author = {Siddharth Srivastava and Guy A. Orban and Patrick A. De Maziere and Peter Janssen},
doi = {10.1523/JNEUROSCI.6016-08.2009},
year = {2009},
date = {2009-01-01},
journal = {Journal of Neuroscience},
volume = {29},
number = {34},
pages = {10613--10626},
abstract = {Differences in the horizontal positions of retinal images—binocular disparity—provide important cues for three-dimensional object recognition and manipulation. We investigated the neural coding ofthree-dimensional shape defined by disparity in anterior intrapari- etal (AIP) area. Robust selectivity for disparity-defined slanted and curved surfaces was observed in a high proportion ofAIP neurons, emerging at relatively short latencies. The large majority of AIP neurons preserved their three-dimensional shape preference over different positions in depth, a hallmark of higher-order disparity selectivity. Yet both stimulus type (concave–convex) and position in depth could be reliably decoded from the AIP responses. The neural coding ofthree-dimensional shape was based on first-order (slanted surfaces) and second-order (curved surfaces) disparity selectivity. Many AIP neurons tolerated the presence ofdisparity discontinuities in the stimulus, but the population ofAIP neurons provided reliable information on the degree ofcurvedness ofthe stimulus. Finally, AIP neurons preserved their three-dimensional shape preference over different positions in the frontoparallel plane. Thus, AIP neurons extract or have access to three-dimensional object information defined by binocular disparity, consistent with previous functional magnetic resonance imaging data. Unlike the known representation ofthree-dimensional shape in inferior temporal cortex, the neural representation in AIP appears to emphasize object parameters required for the planning ofgrasping movements.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

Differences in the horizontal positions of retinal images—binocular disparity—provide important cues for three-dimensional object recognition and manipulation. We investigated the neural coding ofthree-dimensional shape defined by disparity in anterior intrapari- etal (AIP) area. Robust selectivity for disparity-defined slanted and curved surfaces was observed in a high proportion ofAIP neurons, emerging at relatively short latencies. The large majority of AIP neurons preserved their three-dimensional shape preference over different positions in depth, a hallmark of higher-order disparity selectivity. Yet both stimulus type (concave–convex) and position in depth could be reliably decoded from the AIP responses. The neural coding ofthree-dimensional shape was based on first-order (slanted surfaces) and second-order (curved surfaces) disparity selectivity. Many AIP neurons tolerated the presence ofdisparity discontinuities in the stimulus, but the population ofAIP neurons provided reliable information on the degree ofcurvedness ofthe stimulus. Finally, AIP neurons preserved their three-dimensional shape preference over different positions in the frontoparallel plane. Thus, AIP neurons extract or have access to three-dimensional object information defined by binocular disparity, consistent with previous functional magnetic resonance imaging data. Unlike the known representation ofthree-dimensional shape in inferior temporal cortex, the neural representation in AIP appears to emphasize object parameters required for the planning ofgrasping movements.

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  • doi:10.1523/JNEUROSCI.6016-08.2009

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T. S. Davis; K. Torab; Paul A. House; Bradley Greger

A minimally invasive approach to long-term head fixation in behaving nonhuman primates Journal Article

In: Journal of Neuroscience Methods, vol. 181, no. 1, pp. 106–110, 2009.

Abstract | Links | BibTeX

@article{Davis2009a,
title = {A minimally invasive approach to long-term head fixation in behaving nonhuman primates},
author = {T. S. Davis and K. Torab and Paul A. House and Bradley Greger},
doi = {10.1016/j.jneumeth.2009.04.012},
year = {2009},
date = {2009-01-01},
journal = {Journal of Neuroscience Methods},
volume = {181},
number = {1},
pages = {106--110},
abstract = {We have designed a device for long-term head fixation for use in behaving nonhuman primates that is robust yet minimally invasive and simple to use. This device is a modified version of the halo system that is used in humans for cervical traction and stabilization after spinal column injuries. This device consists of an aluminum halo with four titanium skull pins offset from the halo by aluminum posts. The titanium pins insert onto small segments of cranially reinforcing titanium plate, which are attached to the skull with titanium cortex screws. The surgery involves four scalp incisions, placement of the reinforcing plates, insertion of the pins for attachment of the halo, and incision closure. After the halo is attached, the animal's head can be fixed to a primate chair using a custom-built attachment arm that provides three degrees of adjustability for proper positioning during behavioral tasks. We have installed this device on two Macaque monkeys weighing 7 and 10 kg. The halos have been in place on these animals for up to 8 months without signs of discomfort or loss of fixation. Using this method of head fixation, we have been able to track the animals' eye positions with an accuracy of less than two visual degrees while they perform behavioral tasks.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

We have designed a device for long-term head fixation for use in behaving nonhuman primates that is robust yet minimally invasive and simple to use. This device is a modified version of the halo system that is used in humans for cervical traction and stabilization after spinal column injuries. This device consists of an aluminum halo with four titanium skull pins offset from the halo by aluminum posts. The titanium pins insert onto small segments of cranially reinforcing titanium plate, which are attached to the skull with titanium cortex screws. The surgery involves four scalp incisions, placement of the reinforcing plates, insertion of the pins for attachment of the halo, and incision closure. After the halo is attached, the animal's head can be fixed to a primate chair using a custom-built attachment arm that provides three degrees of adjustability for proper positioning during behavioral tasks. We have installed this device on two Macaque monkeys weighing 7 and 10 kg. The halos have been in place on these animals for up to 8 months without signs of discomfort or loss of fixation. Using this method of head fixation, we have been able to track the animals' eye positions with an accuracy of less than two visual degrees while they perform behavioral tasks.

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  • doi:10.1016/j.jneumeth.2009.04.012

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K. A. Ford; Stefan Everling

Neural activity in primate caudate nucleus associated with pro- and antisaccades Journal Article

In: Journal of Neurophysiology, vol. 102, no. 4, pp. 2334–2341, 2009.

Abstract | Links | BibTeX

@article{Ford2009,
title = {Neural activity in primate caudate nucleus associated with pro- and antisaccades},
author = {K. A. Ford and Stefan Everling},
doi = {10.1152/jn.00125.2009},
year = {2009},
date = {2009-01-01},
journal = {Journal of Neurophysiology},
volume = {102},
number = {4},
pages = {2334--2341},
abstract = {The basal ganglia (BG) play a central role in movement and it has been demonstrated that the discharge rate of neurons in these structures are modulated by the behavioral context of a given task. Here we used the antisaccade task, in which a saccade toward a flashed visual stimulus must be inhibited in favor of a saccade to the opposite location, to investigate the role of the caudate nucleus, a major input structure of the BG, in flexible behavior. In this study, we recorded extracellular neuronal activity while monkeys performed pro- and antisaccade trials. We identified two populations of neurons: those that preferred contralateral saccades (CSNs) and those that preferred ipsilateral saccades (ISNs). CSNs increased their firing rates for prosaccades, but not for antisaccades, and ISNs increased their firing rates for antisaccades, but not for prosaccades. We propose a model in which CSNs project to the direct BG pathway, facilitating saccades, and ISNs project to the indirect pathway, suppressing saccades. This model suggests one possible mechanism by which these neuronal populations could be modulating activity in the superior colliculus.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

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The basal ganglia (BG) play a central role in movement and it has been demonstrated that the discharge rate of neurons in these structures are modulated by the behavioral context of a given task. Here we used the antisaccade task, in which a saccade toward a flashed visual stimulus must be inhibited in favor of a saccade to the opposite location, to investigate the role of the caudate nucleus, a major input structure of the BG, in flexible behavior. In this study, we recorded extracellular neuronal activity while monkeys performed pro- and antisaccade trials. We identified two populations of neurons: those that preferred contralateral saccades (CSNs) and those that preferred ipsilateral saccades (ISNs). CSNs increased their firing rates for prosaccades, but not for antisaccades, and ISNs increased their firing rates for antisaccades, but not for prosaccades. We propose a model in which CSNs project to the direct BG pathway, facilitating saccades, and ISNs project to the indirect pathway, suppressing saccades. This model suggests one possible mechanism by which these neuronal populations could be modulating activity in the superior colliculus.

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  • doi:10.1152/jn.00125.2009

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Benjamin Y. Hayden; Jack L. Gallant

Combined effects of spatial and feature-based attention on responses of V4 neurons Journal Article

In: Vision Research, vol. 49, no. 10, pp. 1182–1187, 2009.

Abstract | Links | BibTeX

@article{Hayden2009,
title = {Combined effects of spatial and feature-based attention on responses of V4 neurons},
author = {Benjamin Y. Hayden and Jack L. Gallant},
doi = {10.1016/j.visres.2008.06.011},
year = {2009},
date = {2009-01-01},
journal = {Vision Research},
volume = {49},
number = {10},
pages = {1182--1187},
publisher = {Elsevier Ltd},
abstract = {Attention is thought to be controlled by a specialized fronto-parietal network that modulates the responses of neurons in sensory and association cortex. However, the principles by which this network affects the responses of these sensory and association neurons remains unknown. In particular, it remains unclear whether different forms of attention, such as spatial and feature-based attention, independently modulate responses of single neurons. We recorded responses of single V4 neurons in a task that controls both forms of attention independently. We find that the combined effects of spatial and feature-based attention can be described as the sum of independent processes with a small super-additive interaction term. This pattern of effects demonstrates that the spatial and feature-based aspects of the attentional control system can independently affect responses of single neurons. These results are consistent with the idea that spatial and feature-based attention are controlled by distinct neural substrates whose effects combine synergistically to influence responses of visual neurons.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

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Attention is thought to be controlled by a specialized fronto-parietal network that modulates the responses of neurons in sensory and association cortex. However, the principles by which this network affects the responses of these sensory and association neurons remains unknown. In particular, it remains unclear whether different forms of attention, such as spatial and feature-based attention, independently modulate responses of single neurons. We recorded responses of single V4 neurons in a task that controls both forms of attention independently. We find that the combined effects of spatial and feature-based attention can be described as the sum of independent processes with a small super-additive interaction term. This pattern of effects demonstrates that the spatial and feature-based aspects of the attentional control system can independently affect responses of single neurons. These results are consistent with the idea that spatial and feature-based attention are controlled by distinct neural substrates whose effects combine synergistically to influence responses of visual neurons.

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  • doi:10.1016/j.visres.2008.06.011

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Benjamin Y. Hayden; David V. Smith; Michael L. Platt

Electrophysiological correlates of default-mode processing in macaque posterior cingulate cortex Journal Article

In: Proceedings of the National Academy of Sciences, vol. 106, no. 14, pp. 5948–5953, 2009.

Abstract | Links | BibTeX

@article{Hayden2009a,
title = {Electrophysiological correlates of default-mode processing in macaque posterior cingulate cortex},
author = {Benjamin Y. Hayden and David V. Smith and Michael L. Platt},
doi = {10.1073/pnas.0812035106},
year = {2009},
date = {2009-01-01},
journal = {Proceedings of the National Academy of Sciences},
volume = {106},
number = {14},
pages = {5948--5953},
abstract = {During the course of daily activity, our level of engagement with the world varies on a moment-to-moment basis. Although these fluctuations in vigilance have critical consequences for our thoughts and actions, almost nothing is known about the neuronal substrates governing such dynamic variations in task engagement. We investigated the hypothesis that the posterior cingulate cortex (CGp), a region linked to default-mode processing by hemodynamic and metabolic measures, controls such variations. We recorded the activity of single neurons in CGp in 2 macaque monkeys performing simple tasks in which their behavior varied from vigilant to inattentive. We found that firing rates were reliably suppressed during task performance and returned to a higher resting baseline between trials. Importantly, higher firing rates predicted errors and slow behavioral responses, and were also observed during cued rest periods when monkeys were temporarily liberated from exteroceptive vigilance. These patterns of activity were not observed in the lateral intraparietal area, an area linked to the frontoparietal attention network. Our findings provide physiological confirmation that CGp mediates exteroceptive vigilance and are consistent with the idea that CGp is part of the "default network" of brain areas associated with control of task engagement.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

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During the course of daily activity, our level of engagement with the world varies on a moment-to-moment basis. Although these fluctuations in vigilance have critical consequences for our thoughts and actions, almost nothing is known about the neuronal substrates governing such dynamic variations in task engagement. We investigated the hypothesis that the posterior cingulate cortex (CGp), a region linked to default-mode processing by hemodynamic and metabolic measures, controls such variations. We recorded the activity of single neurons in CGp in 2 macaque monkeys performing simple tasks in which their behavior varied from vigilant to inattentive. We found that firing rates were reliably suppressed during task performance and returned to a higher resting baseline between trials. Importantly, higher firing rates predicted errors and slow behavioral responses, and were also observed during cued rest periods when monkeys were temporarily liberated from exteroceptive vigilance. These patterns of activity were not observed in the lateral intraparietal area, an area linked to the frontoparietal attention network. Our findings provide physiological confirmation that CGp mediates exteroceptive vigilance and are consistent with the idea that CGp is part of the "default network" of brain areas associated with control of task engagement.

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  • doi:10.1073/pnas.0812035106

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Todd M. Herrington; Nicolas Y. Masse; Karim J. Hachmeh; Jackson E. T. Smith; John A. Assad; Erik P. Cook

The effect of microsaccades on the correlation between neural activity and behavior in middle temporal, ventral intraparietal, and lateral intraparietal areas Journal Article

In: Journal of Neuroscience, vol. 29, no. 18, pp. 5793–5805, 2009.

Abstract | Links | BibTeX

@article{Herrington2009,
title = {The effect of microsaccades on the correlation between neural activity and behavior in middle temporal, ventral intraparietal, and lateral intraparietal areas},
author = {Todd M. Herrington and Nicolas Y. Masse and Karim J. Hachmeh and Jackson E. T. Smith and John A. Assad and Erik P. Cook},
doi = {10.1523/JNEUROSCI.4412-08.2009},
year = {2009},
date = {2009-01-01},
journal = {Journal of Neuroscience},
volume = {29},
number = {18},
pages = {5793--5805},
abstract = {It is widely reported that the activity of single neurons in visual cortex is correlated with the perceptual decision of the subject. The strength of this correlation has implications for the neuronal populations generating the percepts. Here we asked whether microsaccades, which are small, involuntary eye movements, contribute to the correlation between neural activity and behavior. We analyzed data from three different visual detection experiments, with neural recordings from the middle temporal (MT), lateral intraparietal (LIP), and ventral intraparietal (VIP) areas. All three experiments used random dot motion stimuli, with the animals required to detect a transient or sustained change in the speed or strength of motion. We found that microsaccades suppressed neural activity and inhibited detection of the motion stimulus, contributing to the correlation between neural activity and detection behavior. Microsaccades accounted for as much as 19% of the correlation for area MT, 21% for area LIP, and 17% for VIP. While microsaccades only explain part of the correlation between neural activity and behavior, their effect has implications when considering the neuronal populations underlying perceptual decisions.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

It is widely reported that the activity of single neurons in visual cortex is correlated with the perceptual decision of the subject. The strength of this correlation has implications for the neuronal populations generating the percepts. Here we asked whether microsaccades, which are small, involuntary eye movements, contribute to the correlation between neural activity and behavior. We analyzed data from three different visual detection experiments, with neural recordings from the middle temporal (MT), lateral intraparietal (LIP), and ventral intraparietal (VIP) areas. All three experiments used random dot motion stimuli, with the animals required to detect a transient or sustained change in the speed or strength of motion. We found that microsaccades suppressed neural activity and inhibited detection of the motion stimulus, contributing to the correlation between neural activity and detection behavior. Microsaccades accounted for as much as 19% of the correlation for area MT, 21% for area LIP, and 17% for VIP. While microsaccades only explain part of the correlation between neural activity and behavior, their effect has implications when considering the neuronal populations underlying perceptual decisions.

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  • doi:10.1523/JNEUROSCI.4412-08.2009

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F. A. Khawaja; James M. G. Tsui; Christopher C. Pack

Pattern motion selectivity of spiking outputs and local field potentials in macaque visual cortex Journal Article

In: Journal of Neuroscience, vol. 29, no. 43, pp. 13702–13709, 2009.

Abstract | Links | BibTeX

@article{Khawaja2009,
title = {Pattern motion selectivity of spiking outputs and local field potentials in macaque visual cortex},
author = {F. A. Khawaja and James M. G. Tsui and Christopher C. Pack},
doi = {10.1523/JNEUROSCI.2844-09.2009},
year = {2009},
date = {2009-01-01},
journal = {Journal of Neuroscience},
volume = {29},
number = {43},
pages = {13702--13709},
abstract = {The dorsal pathway of the primate visual cortex is involved in the processing of motion signals that are useful for perception and behavior. Along this pathway, motion information is first measured by the primary visual cortex (V1), which sends specialized projections to extrastriate regions such as the middle temporal area (MT). Previous work with plaid stimuli has shown that most V1 neurons respond to the individual components of moving stimuli, whereas some MT neurons are capable of estimating the global motion of the pattern. In this work, we show that the majority of neurons in the medial superior temporal area (MST), which receives input from MT, have this pattern-selective property. Interestingly, the local field potentials (LFPs) measured simultaneously with the spikes often exhibit properties similar to that of the presumptive feedforward input to each area: in the high-gamma frequency band, the LFPs in MST are as component selective as the spiking outputs of MT, and MT LFPs have plaid responses that are similar to the spiking outputs of V1. In the lower LFP frequency bands (beta and low gamma), component selectivity is very common, and pattern selectivity is almost entirely absent in both MT and MST. Together, these results suggest a surprisingly strong link between the sensory tuning of cortical LFPs and afferent inputs, with important implications for the interpretation of imaging studies and for models of cortical function.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

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The dorsal pathway of the primate visual cortex is involved in the processing of motion signals that are useful for perception and behavior. Along this pathway, motion information is first measured by the primary visual cortex (V1), which sends specialized projections to extrastriate regions such as the middle temporal area (MT). Previous work with plaid stimuli has shown that most V1 neurons respond to the individual components of moving stimuli, whereas some MT neurons are capable of estimating the global motion of the pattern. In this work, we show that the majority of neurons in the medial superior temporal area (MST), which receives input from MT, have this pattern-selective property. Interestingly, the local field potentials (LFPs) measured simultaneously with the spikes often exhibit properties similar to that of the presumptive feedforward input to each area: in the high-gamma frequency band, the LFPs in MST are as component selective as the spiking outputs of MT, and MT LFPs have plaid responses that are similar to the spiking outputs of V1. In the lower LFP frequency bands (beta and low gamma), component selectivity is very common, and pattern selectivity is almost entirely absent in both MT and MST. Together, these results suggest a surprisingly strong link between the sensory tuning of cortical LFPs and afferent inputs, with important implications for the interpretation of imaging studies and for models of cortical function.

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  • doi:10.1523/JNEUROSCI.2844-09.2009

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Dhushan Thevarajah; Areh Mikulić; Michael C. Dorris

Role of the superior colliculus in choosing mixed-strategy saccades Journal Article

In: Journal of Neuroscience, vol. 29, no. 7, pp. 1998–2008, 2009.

Abstract | Links | BibTeX

@article{Thevarajah2009,
title = {Role of the superior colliculus in choosing mixed-strategy saccades},
author = {Dhushan Thevarajah and Areh Mikulić and Michael C. Dorris},
doi = {10.1523/JNEUROSCI.4764-08.2009},
year = {2009},
date = {2009-01-01},
journal = {Journal of Neuroscience},
volume = {29},
number = {7},
pages = {1998--2008},
abstract = {Game theory outlines optimal response strategies during mixed-strategy competitions. The neural processes involved in choosing individual strategic actions, however, remain poorly understood. Here, we tested whether the superior colliculus (SC), a brain region critical for generating sensory-guided saccades, is also involved in choosing saccades under strategic conditions. Monkeys were free to choose either of two saccade targets as they competed against a computer opponent during the mixed-strategy game "matching pennies." The accuracy with which presaccadic SC activity predicted upcoming choice gradually increased in the time leading up to the saccade. Probing the SC with suprathreshold stimulation demonstrated that these evolving signals were functionally involved in preparing strategic saccades. Finally, subthreshold stimulation of the SC increased the likelihood that contralateral saccades were selected. Together, our results suggest that motor regions of the brain play an active role in choosing strategic actions rather than passively executing those prespecified by upstream executive regions.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

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Game theory outlines optimal response strategies during mixed-strategy competitions. The neural processes involved in choosing individual strategic actions, however, remain poorly understood. Here, we tested whether the superior colliculus (SC), a brain region critical for generating sensory-guided saccades, is also involved in choosing saccades under strategic conditions. Monkeys were free to choose either of two saccade targets as they competed against a computer opponent during the mixed-strategy game "matching pennies." The accuracy with which presaccadic SC activity predicted upcoming choice gradually increased in the time leading up to the saccade. Probing the SC with suprathreshold stimulation demonstrated that these evolving signals were functionally involved in preparing strategic saccades. Finally, subthreshold stimulation of the SC increased the likelihood that contralateral saccades were selected. Together, our results suggest that motor regions of the brain play an active role in choosing strategic actions rather than passively executing those prespecified by upstream executive regions.

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  • doi:10.1523/JNEUROSCI.4764-08.2009

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Joris Vangeneugden; Frank E. Pollick; Rufin Vogels

Functional differentiation of macaque visual temporal cortical neurons using a parametric action space Journal Article

In: Cerebral Cortex, vol. 19, no. 3, pp. 593–611, 2009.

Abstract | Links | BibTeX

@article{Vangeneugden2009,
title = {Functional differentiation of macaque visual temporal cortical neurons using a parametric action space},
author = {Joris Vangeneugden and Frank E. Pollick and Rufin Vogels},
doi = {10.1093/cercor/bhn109},
year = {2009},
date = {2009-01-01},
journal = {Cerebral Cortex},
volume = {19},
number = {3},
pages = {593--611},
abstract = {Neurons in the rostral superior temporal sulcus (STS) are responsive to displays of body movements. We employed a parametric action space to determine how similarities among actions are represented by visual temporal neurons and how form and motion information contributes to their responses. The stimulus space consisted of a stick-plus-point-light figure performing arm actions and their blends. Multidimensional scaling showed that the responses of temporal neurons represented the ordinal similarity between these actions. Further tests distinguished neurons responding equally strongly to static presentations and to actions ("snapshot" neurons), from those responding much less strongly to static presentations, but responding well when motion was present ("motion" neurons). The "motion" neurons were predominantly found in the upper bank/fundus of the STS, and "snapshot" neurons in the lower bank of the STS and inferior temporal convexity. Most "motion" neurons showed strong response modulation during the course of an action, thus responding to action kinematics. "Motion" neurons displayed a greater average selectivity for these simple arm actions than did "snapshot" neurons. We suggest that the "motion" neurons code for visual kinematics, whereas the "snapshot" neurons code for form/posture, and that both can contribute to action recognition, in agreement with computation models of action recognition.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

Neurons in the rostral superior temporal sulcus (STS) are responsive to displays of body movements. We employed a parametric action space to determine how similarities among actions are represented by visual temporal neurons and how form and motion information contributes to their responses. The stimulus space consisted of a stick-plus-point-light figure performing arm actions and their blends. Multidimensional scaling showed that the responses of temporal neurons represented the ordinal similarity between these actions. Further tests distinguished neurons responding equally strongly to static presentations and to actions ("snapshot" neurons), from those responding much less strongly to static presentations, but responding well when motion was present ("motion" neurons). The "motion" neurons were predominantly found in the upper bank/fundus of the STS, and "snapshot" neurons in the lower bank of the STS and inferior temporal convexity. Most "motion" neurons showed strong response modulation during the course of an action, thus responding to action kinematics. "Motion" neurons displayed a greater average selectivity for these simple arm actions than did "snapshot" neurons. We suggest that the "motion" neurons code for visual kinematics, whereas the "snapshot" neurons code for form/posture, and that both can contribute to action recognition, in agreement with computation models of action recognition.

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  • doi:10.1093/cercor/bhn109

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Karli K. Watson; Jason H. Ghodasra; Michael L. Platt

Serotonin transporter genotype modulates social reward and punishment in rhesus macaques Journal Article

In: PLoS ONE, vol. 4, no. 1, pp. e4156, 2009.

Abstract | Links | BibTeX

@article{Watson2009a,
title = {Serotonin transporter genotype modulates social reward and punishment in rhesus macaques},
author = {Karli K. Watson and Jason H. Ghodasra and Michael L. Platt},
doi = {10.1371/journal.pone.0004156},
year = {2009},
date = {2009-01-01},
journal = {PLoS ONE},
volume = {4},
number = {1},
pages = {e4156},
abstract = {BACKGROUND: Serotonin signaling influences social behavior in both human and nonhuman primates. In humans, variation upstream of the promoter region of the serotonin transporter gene (5-HTTLPR) has recently been shown to influence both behavioral measures of social anxiety and amygdala response to social threats. Here we show that length polymorphisms in 5-HTTLPR predict social reward and punishment in rhesus macaques, a species in which 5-HTTLPR variation is analogous to that of humans. METHODOLOGY/PRINCIPAL FINDINGS: In contrast to monkeys with two copies of the long allele (L/L), monkeys with one copy of the short allele of this gene (S/L) spent less time gazing at face than non-face images, less time looking in the eye region of faces, and had larger pupil diameters when gazing at photos of a high versus low status male macaques. Moreover, in a novel primed gambling task, presentation of photos of high status male macaques promoted risk-aversion in S/L monkeys but promoted risk-seeking in L/L monkeys. Finally, as measured by a "pay-per-view" task, S/L monkeys required juice payment to view photos of high status males, whereas L/L monkeys sacrificed fluid to see the same photos. CONCLUSIONS/SIGNIFICANCE: These data indicate that genetic variation in serotonin function contributes to social reward and punishment in rhesus macaques, and thus shapes social behavior in humans and rhesus macaques alike.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

BACKGROUND: Serotonin signaling influences social behavior in both human and nonhuman primates. In humans, variation upstream of the promoter region of the serotonin transporter gene (5-HTTLPR) has recently been shown to influence both behavioral measures of social anxiety and amygdala response to social threats. Here we show that length polymorphisms in 5-HTTLPR predict social reward and punishment in rhesus macaques, a species in which 5-HTTLPR variation is analogous to that of humans. METHODOLOGY/PRINCIPAL FINDINGS: In contrast to monkeys with two copies of the long allele (L/L), monkeys with one copy of the short allele of this gene (S/L) spent less time gazing at face than non-face images, less time looking in the eye region of faces, and had larger pupil diameters when gazing at photos of a high versus low status male macaques. Moreover, in a novel primed gambling task, presentation of photos of high status male macaques promoted risk-aversion in S/L monkeys but promoted risk-seeking in L/L monkeys. Finally, as measured by a "pay-per-view" task, S/L monkeys required juice payment to view photos of high status males, whereas L/L monkeys sacrificed fluid to see the same photos. CONCLUSIONS/SIGNIFICANCE: These data indicate that genetic variation in serotonin function contributes to social reward and punishment in rhesus macaques, and thus shapes social behavior in humans and rhesus macaques alike.

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  • doi:10.1371/journal.pone.0004156

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Luke Woloszyn; David L. Sheinberg

Neural dynamics in inferior temporal cortex during a visual working memory task Journal Article

In: Journal of Neuroscience, vol. 29, no. 17, pp. 5494–5507, 2009.

Abstract | Links | BibTeX

@article{Woloszyn2009,
title = {Neural dynamics in inferior temporal cortex during a visual working memory task},
author = {Luke Woloszyn and David L. Sheinberg},
doi = {10.1523/JNEUROSCI.5785-08.2009},
year = {2009},
date = {2009-01-01},
journal = {Journal of Neuroscience},
volume = {29},
number = {17},
pages = {5494--5507},
abstract = {Intelligent organisms are capable of tracking objects even when they temporarily disappear from sight, a cognitive capacity commonly referred to as visual working memory (VWM). The neural basis of VWM has been the subject of significant scientific debate, with recent work focusing on the relative roles of posterior visual areas, such as the inferior temporal cortex (ITC), and the prefrontal cortex. Here we reexamined the contribution of ITC to VWM by recording from highly selective individual ITC neurons as monkeys engaged in multiple versions of an occlusion-based memory task. As expected, we found strong evidence for a role of ITC in stimulus encoding. We also found that almost half of these selective cells showed stimulus-selective delay period modulation, with a small but significant fraction exhibiting differential responses even in the presence of simultaneously visible interfering information. When we combined the informational content of multiple neurons, we found that the accuracy with which we could decode memory content increased drastically. The memory epoch analyses suggest that behaviorally relevant visual memories were reinstated in ITC. Furthermore, we observed a population-wide enhancement of neuronal response to a match stimulus compared with the same stimulus presented as a nonmatch. The single-cell enhancement preceded any match effects identified in the local field potential, leading us to speculate that enhancement is the result of neural processing local to ITC. Moreover, match enhancement was only later followed by the more commonly observed match suppression. Altogether, the data support the hypothesis that, when a stimulus is held in memory, ITC neurons are actively biased in favor of task-relevant visual representations and that this bias can immediately impact subsequent recognition events.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

Intelligent organisms are capable of tracking objects even when they temporarily disappear from sight, a cognitive capacity commonly referred to as visual working memory (VWM). The neural basis of VWM has been the subject of significant scientific debate, with recent work focusing on the relative roles of posterior visual areas, such as the inferior temporal cortex (ITC), and the prefrontal cortex. Here we reexamined the contribution of ITC to VWM by recording from highly selective individual ITC neurons as monkeys engaged in multiple versions of an occlusion-based memory task. As expected, we found strong evidence for a role of ITC in stimulus encoding. We also found that almost half of these selective cells showed stimulus-selective delay period modulation, with a small but significant fraction exhibiting differential responses even in the presence of simultaneously visible interfering information. When we combined the informational content of multiple neurons, we found that the accuracy with which we could decode memory content increased drastically. The memory epoch analyses suggest that behaviorally relevant visual memories were reinstated in ITC. Furthermore, we observed a population-wide enhancement of neuronal response to a match stimulus compared with the same stimulus presented as a nonmatch. The single-cell enhancement preceded any match effects identified in the local field potential, leading us to speculate that enhancement is the result of neural processing local to ITC. Moreover, match enhancement was only later followed by the more commonly observed match suppression. Altogether, the data support the hypothesis that, when a stimulus is held in memory, ITC neurons are actively biased in favor of task-relevant visual representations and that this bias can immediately impact subsequent recognition events.

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  • doi:10.1523/JNEUROSCI.5785-08.2009

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2008

P. D. Thiem; Jessica A. Hill; K. -M. Lee; Edward L. Keller

Behavioral properties of saccades generated as a choice response Journal Article

In: Experimental Brain Research, vol. 186, no. 3, pp. 355–364, 2008.

Abstract | Links | BibTeX

@article{Thiem2008,
title = {Behavioral properties of saccades generated as a choice response},
author = {P. D. Thiem and Jessica A. Hill and K. -M. Lee and Edward L. Keller},
doi = {10.1007/s00221-007-1239-y},
year = {2008},
date = {2008-01-01},
journal = {Experimental Brain Research},
volume = {186},
number = {3},
pages = {355--364},
abstract = {The behavior characterizing choice response decision-making was studied in monkeys to provide background information for ongoing neurophysiological studies of the neural mechanisms underlying saccadic choice decisions. Animals were trained to associate a specific color from a set of colored visual stimuli with a specific spatial location. The visual stimuli (colored disks) appeared briefly at equal eccentricity from a central fixation position and then were masked by gray disks. The correct target association was subsequently cued by the appearance of a colored stimulus at the fixation point. The animal indicated its choice by saccading to the remembered location of the eccentric stimulus, which had matched the color of the cue. The number of alternative associations (NA) varied from 1 to 4 and remained fixed within a block of trials. After the training period, performance (percent correct responses) declined modestly as NA increased (on average 96, 93 or 84% correct for 1, 2 or 4 NA, respectively). Response latency increased logarithmically as a function of NA, thus obeying Hick's law. The spatial extent of the learned association between color and location was investigated by rotating the array of colored stimuli that had remained fixed during the learning phase to various different angles. Error rates in choice saccades increased gradually as a function of the amount of rotation. The learned association biased the direction of the saccadic response toward the quadrant associated with the cue, but saccade direction was always toward one of the actual visual stimuli. This suggests that the learned associations between stimuli and responses were not spatially exact, but instead the association between color and location was distributed with declining strength from the trained locations. These results demonstrate that the saccade system in monkeys also displays the characteristic dependence on NA in choice response latencies, while more basic features of the eye movements are invariant from those in other tasks. The findings also provide behavioral evidence that spatially distributed regions are established for the sensory-to-motor associations during training which are later utilized for choice decisions.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

The behavior characterizing choice response decision-making was studied in monkeys to provide background information for ongoing neurophysiological studies of the neural mechanisms underlying saccadic choice decisions. Animals were trained to associate a specific color from a set of colored visual stimuli with a specific spatial location. The visual stimuli (colored disks) appeared briefly at equal eccentricity from a central fixation position and then were masked by gray disks. The correct target association was subsequently cued by the appearance of a colored stimulus at the fixation point. The animal indicated its choice by saccading to the remembered location of the eccentric stimulus, which had matched the color of the cue. The number of alternative associations (NA) varied from 1 to 4 and remained fixed within a block of trials. After the training period, performance (percent correct responses) declined modestly as NA increased (on average 96, 93 or 84% correct for 1, 2 or 4 NA, respectively). Response latency increased logarithmically as a function of NA, thus obeying Hick's law. The spatial extent of the learned association between color and location was investigated by rotating the array of colored stimuli that had remained fixed during the learning phase to various different angles. Error rates in choice saccades increased gradually as a function of the amount of rotation. The learned association biased the direction of the saccadic response toward the quadrant associated with the cue, but saccade direction was always toward one of the actual visual stimuli. This suggests that the learned associations between stimuli and responses were not spatially exact, but instead the association between color and location was distributed with declining strength from the trained locations. These results demonstrate that the saccade system in monkeys also displays the characteristic dependence on NA in choice response latencies, while more basic features of the eye movements are invariant from those in other tasks. The findings also provide behavioral evidence that spatially distributed regions are established for the sensory-to-motor associations during training which are later utilized for choice decisions.

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  • doi:10.1007/s00221-007-1239-y

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Benjamin Y. Hayden; Sarah R. Heilbronner; Amrita C. Nair; Michael L. Platt

Cognitive influences on risk-seeking by rhesus macaques Journal Article

In: Judgment and Decision Making, vol. 3, no. 5, pp. 389–395, 2008.

Abstract | BibTeX

@article{Hayden2008,
title = {Cognitive influences on risk-seeking by rhesus macaques},
author = {Benjamin Y. Hayden and Sarah R. Heilbronner and Amrita C. Nair and Michael L. Platt},
year = {2008},
date = {2008-01-01},
journal = {Judgment and Decision Making},
volume = {3},
number = {5},
pages = {389--395},
abstract = {Humans and other animals are idiosyncratically sensitive to risk, either preferring or avoiding options having the same value but differing in uncertainty. Many explanations for risk sensitivity rely on the non-linear shape of a hypothesized utility curve. Because such models do not place any importance on uncertainty per se, utility curve-based accounts predict indifference between risky and riskless options that offer the same distribution of rewards. Here we show that monkeys strongly prefer uncertain gambles to alternating rewards with the same payoffs, demonstrating that uncertainty itself contributes to the appeal of risky options. Based on prior observations, we hypothesized that the appeal of the risky option is enhanced by the salience of the potential jackpot. To test this, we subtly manipulated payoffs in a second gambling task. We found that monkeys are more sensitive to small changes in the size of the large reward than to equivalent changes in the size of the small reward, indicating that they attend preferentially to the jackpots. Together, these results challenge utility curve-based accounts of risk sensitivity, and suggest that psychological factors, such as outcome salience and uncertainty itself, contribute to risky decision-making.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

Humans and other animals are idiosyncratically sensitive to risk, either preferring or avoiding options having the same value but differing in uncertainty. Many explanations for risk sensitivity rely on the non-linear shape of a hypothesized utility curve. Because such models do not place any importance on uncertainty per se, utility curve-based accounts predict indifference between risky and riskless options that offer the same distribution of rewards. Here we show that monkeys strongly prefer uncertain gambles to alternating rewards with the same payoffs, demonstrating that uncertainty itself contributes to the appeal of risky options. Based on prior observations, we hypothesized that the appeal of the risky option is enhanced by the salience of the potential jackpot. To test this, we subtly manipulated payoffs in a second gambling task. We found that monkeys are more sensitive to small changes in the size of the large reward than to equivalent changes in the size of the small reward, indicating that they attend preferentially to the jackpots. Together, these results challenge utility curve-based accounts of risk sensitivity, and suggest that psychological factors, such as outcome salience and uncertainty itself, contribute to risky decision-making.

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Benjamin Y. Hayden; Amrita C. Nair; Allison N. McCoy; Michael L. Platt

Posterior cingulate cortex mediates outcome-contingent allocation of behavior Journal Article

In: Neuron, vol. 60, no. 1, pp. 19–25, 2008.

Abstract | Links | BibTeX

@article{Hayden2008a,
title = {Posterior cingulate cortex mediates outcome-contingent allocation of behavior},
author = {Benjamin Y. Hayden and Amrita C. Nair and Allison N. McCoy and Michael L. Platt},
doi = {10.1016/j.neuron.2008.09.012},
year = {2008},
date = {2008-01-01},
journal = {Neuron},
volume = {60},
number = {1},
pages = {19--25},
abstract = {Adaptive decision making requires selecting an action and then monitoring its consequences to improve future decisions. The neuronal mechanisms supporting action evaluation and subsequent behavioral modification, however, remain poorly understood. To investigate the contribution of posterior cingulate cortex (CGp) to these processes, we recorded activity of single neurons in monkeys performing a gambling task in which the reward outcome of each choice strongly influenced subsequent choices. We found that CGp neurons signaled reward outcomes in a nonlinear fashion and that outcome-contingent modulations in firing rate persisted into subsequent trials. Moreover, firing rate on any one trial predicted switching to the alternative option on the next trial. Finally, microstimulation in CGp following risky choices promoted a preference reversal for the safe option on the following trial. Collectively, these results demonstrate that CGp directly contributes to the evaluative processes that support dynamic changes in decision making in volatile environments.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

Adaptive decision making requires selecting an action and then monitoring its consequences to improve future decisions. The neuronal mechanisms supporting action evaluation and subsequent behavioral modification, however, remain poorly understood. To investigate the contribution of posterior cingulate cortex (CGp) to these processes, we recorded activity of single neurons in monkeys performing a gambling task in which the reward outcome of each choice strongly influenced subsequent choices. We found that CGp neurons signaled reward outcomes in a nonlinear fashion and that outcome-contingent modulations in firing rate persisted into subsequent trials. Moreover, firing rate on any one trial predicted switching to the alternative option on the next trial. Finally, microstimulation in CGp following risky choices promoted a preference reversal for the safe option on the following trial. Collectively, these results demonstrate that CGp directly contributes to the evaluative processes that support dynamic changes in decision making in volatile environments.

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  • doi:10.1016/j.neuron.2008.09.012

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Peter Janssen; Siddharth Srivastava; Sien Ombelet; Guy A. Orban

Coding of shape and position in macaque lateral Iintraparietal area Journal Article

In: Journal of Neuroscience, vol. 28, no. 26, pp. 6679–6690, 2008.

Abstract | Links | BibTeX

@article{Janssen2008,
title = {Coding of shape and position in macaque lateral Iintraparietal area},
author = {Peter Janssen and Siddharth Srivastava and Sien Ombelet and Guy A. Orban},
doi = {10.1523/JNEUROSCI.0499-08.2008},
year = {2008},
date = {2008-01-01},
journal = {Journal of Neuroscience},
volume = {28},
number = {26},
pages = {6679--6690},
abstract = {The analysis of object shape is critical for both object recognition and grasping. Areas in the intraparietal sulcus of the rhesus monkey are important for the visuomotor transformations underlying actions directed toward objects. The lateral intraparietal (LIP) area has strong anatomical connections with the anterior intraparietal area, which is known to control the shaping of the hand during grasping, and LIP neurons can respond selectively to simple two-dimensional shapes. Here we investigate the shape representation in area LIP of awake rhesus monkeys. Specifically, we determined to what extent LIP neurons are tuned to shape dimensions known to be relevant for grasping and assessed the invariance of their shape preferences with regard to changes in stimulus size and position in the receptive field. Most LIP neurons proved to be significantly tuned to multiple shape dimensions. The population of LIP neurons that were tested showed barely significant size invariance. Position invariance was present in a minority of the neurons tested. Many LIP neurons displayed spurious shape selectivity arising from accidental interactions between the stimulus and the receptive field. We observed pronounced differences in the receptive field profiles determined by presenting two different shapes. Almost all LIP neurons showed spatially selective saccadic activity, but the receptive field for saccades did not always correspond to the receptive field as determined using shapes. Our results demonstrate that a subpopulation of LIP neurons encodes stimulus shape. Furthermore, the shape representation in the dorsal visual stream appears to differ radically from the known representation of shape in the ventral visual stream.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

The analysis of object shape is critical for both object recognition and grasping. Areas in the intraparietal sulcus of the rhesus monkey are important for the visuomotor transformations underlying actions directed toward objects. The lateral intraparietal (LIP) area has strong anatomical connections with the anterior intraparietal area, which is known to control the shaping of the hand during grasping, and LIP neurons can respond selectively to simple two-dimensional shapes. Here we investigate the shape representation in area LIP of awake rhesus monkeys. Specifically, we determined to what extent LIP neurons are tuned to shape dimensions known to be relevant for grasping and assessed the invariance of their shape preferences with regard to changes in stimulus size and position in the receptive field. Most LIP neurons proved to be significantly tuned to multiple shape dimensions. The population of LIP neurons that were tested showed barely significant size invariance. Position invariance was present in a minority of the neurons tested. Many LIP neurons displayed spurious shape selectivity arising from accidental interactions between the stimulus and the receptive field. We observed pronounced differences in the receptive field profiles determined by presenting two different shapes. Almost all LIP neurons showed spatially selective saccadic activity, but the receptive field for saccades did not always correspond to the receptive field as determined using shapes. Our results demonstrate that a subpopulation of LIP neurons encodes stimulus shape. Furthermore, the shape representation in the dorsal visual stream appears to differ radically from the known representation of shape in the ventral visual stream.

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  • doi:10.1523/JNEUROSCI.0499-08.2008

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Keisuke Kawasaki; David L. Sheinberg

Learning to recognize visual objects with microstimulation in inferior temporal cortex Journal Article

In: Journal of Neurophysiology, vol. 100, no. 1, pp. 197–211, 2008.

Abstract | Links | BibTeX

@article{Kawasaki2008,
title = {Learning to recognize visual objects with microstimulation in inferior temporal cortex},
author = {Keisuke Kawasaki and David L. Sheinberg},
doi = {10.1152/jn.90247.2008},
year = {2008},
date = {2008-01-01},
journal = {Journal of Neurophysiology},
volume = {100},
number = {1},
pages = {197--211},
abstract = {The malleability of object representations by experience is essential for adaptive behavior. It has been hypothesized that neurons in inferior temporal cortex (IT) in monkeys are pivotal in visual association learning, evidenced by experiments revealing changes in neural selectivity following visual learning, as well as by lesion studies, wherein functional inactivation of IT impairs learning. A critical question remaining to be answered is whether IT neuronal activity is sufficient for learning. To address this question directly, we conducted experiments combining visual classification learning with microstimulation in IT. We assessed the effects of IT microstimulation during learning in cases where the stimulation was exclusively informative, conditionally informative, and informative but not necessary for the classification task. The results show that localized microstimulation in IT can be used to establish visual classification learning, and the same stimulation applied during learning can predictably bias judgments on subsequent recognition. The effect of induced activity can be explained neither by direct stimulation-motor association nor by simple detection of cortical stimulation. We also found that the learning effects are specific to IT stimulation as they are not observed by microstimulation in an adjacent auditory area. Our results add the evidence that the differential activity in IT during visual association learning is sufficient for establishing new associations. The results suggest that experimentally manipulated activity patterns within IT can be effectively combined with ongoing visually induced activity during the formation of new associations.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

The malleability of object representations by experience is essential for adaptive behavior. It has been hypothesized that neurons in inferior temporal cortex (IT) in monkeys are pivotal in visual association learning, evidenced by experiments revealing changes in neural selectivity following visual learning, as well as by lesion studies, wherein functional inactivation of IT impairs learning. A critical question remaining to be answered is whether IT neuronal activity is sufficient for learning. To address this question directly, we conducted experiments combining visual classification learning with microstimulation in IT. We assessed the effects of IT microstimulation during learning in cases where the stimulation was exclusively informative, conditionally informative, and informative but not necessary for the classification task. The results show that localized microstimulation in IT can be used to establish visual classification learning, and the same stimulation applied during learning can predictably bias judgments on subsequent recognition. The effect of induced activity can be explained neither by direct stimulation-motor association nor by simple detection of cortical stimulation. We also found that the learning effects are specific to IT stimulation as they are not observed by microstimulation in an adjacent auditory area. Our results add the evidence that the differential activity in IT during visual association learning is sufficient for establishing new associations. The results suggest that experimentally manipulated activity patterns within IT can be effectively combined with ongoing visually induced activity during the formation of new associations.

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  • doi:10.1152/jn.90247.2008

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Edward L. Keller; Kyoung-Min Lee; Se-Woong Park; Jessica A. Hill

Effect of inactivation of the cortical frontal eye field on saccades generated in a choice response paradigm Journal Article

In: Journal of Neurophysiology, vol. 100, no. 5, pp. 2726–2737, 2008.

Abstract | Links | BibTeX

@article{Keller2008,
title = {Effect of inactivation of the cortical frontal eye field on saccades generated in a choice response paradigm},
author = {Edward L. Keller and Kyoung-Min Lee and Se-Woong Park and Jessica A. Hill},
doi = {10.1152/jn.90673.2008},
year = {2008},
date = {2008-01-01},
journal = {Journal of Neurophysiology},
volume = {100},
number = {5},
pages = {2726--2737},
abstract = {Previous studies using muscimol inactivations in the frontal eye fields (FEFs) have shown that saccades generated by recall from working memory are eliminated by these lesions, whereas visually guided saccades are relatively spared. In these experiments, we made reversible inactivations in FEFs in alert macaque monkeys and examined the effect on saccades in a choice response task. Our task required monkeys to learn arbitrary pairings between colored stimuli and saccade direction. Following inactivations, the percentage of choice errors increased as a function of the number of alternative (NA) pairings. In contrast, the percentage of dysmetric saccades (saccades that landed in the correct quadrant but were inaccurate) did not vary with NA. Saccade latency increased postlesion but did not increase with NA. We also made simultaneous inactivations in both FEFs. The results following bilateral lesions showed approximately twice as many choice errors. We conclude that the FEFs are involved in the generation of saccades in choice response tasks. The dramatic effect of NA on choice errors, but the lack of an effect of NA on motor errors or response latency, suggests that two types of processing are interrupted by FEF lesions. The first involves the formation of a saccadic intention vector from associate memory inputs, and the second, the execution of the saccade from the intention vector. An alternative interpretation of the first result is that a role of the FEFs may be to suppress incorrect responses. The doubling of choice errors following bilateral FEF lesions suggests that the effect of unilateral lesions is not caused by a general inhibition of the lesioned side by the intact side.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

Previous studies using muscimol inactivations in the frontal eye fields (FEFs) have shown that saccades generated by recall from working memory are eliminated by these lesions, whereas visually guided saccades are relatively spared. In these experiments, we made reversible inactivations in FEFs in alert macaque monkeys and examined the effect on saccades in a choice response task. Our task required monkeys to learn arbitrary pairings between colored stimuli and saccade direction. Following inactivations, the percentage of choice errors increased as a function of the number of alternative (NA) pairings. In contrast, the percentage of dysmetric saccades (saccades that landed in the correct quadrant but were inaccurate) did not vary with NA. Saccade latency increased postlesion but did not increase with NA. We also made simultaneous inactivations in both FEFs. The results following bilateral lesions showed approximately twice as many choice errors. We conclude that the FEFs are involved in the generation of saccades in choice response tasks. The dramatic effect of NA on choice errors, but the lack of an effect of NA on motor errors or response latency, suggests that two types of processing are interrupted by FEF lesions. The first involves the formation of a saccadic intention vector from associate memory inputs, and the second, the execution of the saccade from the intention vector. An alternative interpretation of the first result is that a role of the FEFs may be to suppress incorrect responses. The doubling of choice errors following bilateral FEF lesions suggests that the effect of unilateral lesions is not caused by a general inhibition of the lesioned side by the intact side.

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  • doi:10.1152/jn.90673.2008

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Xiaochuan Pan; Kosuke Sawa; Ichiro Tsuda; Minoru Tsukada; Masamichi Sakagami

Reward prediction based on stimulus categorization in primate lateral prefrontal cortex Journal Article

In: Nature Neuroscience, vol. 11, no. 6, pp. 703–712, 2008.

Abstract | Links | BibTeX

@article{Pan2008,
title = {Reward prediction based on stimulus categorization in primate lateral prefrontal cortex},
author = {Xiaochuan Pan and Kosuke Sawa and Ichiro Tsuda and Minoru Tsukada and Masamichi Sakagami},
doi = {10.1038/nn.2128},
year = {2008},
date = {2008-01-01},
journal = {Nature Neuroscience},
volume = {11},
number = {6},
pages = {703--712},
abstract = {To adapt to changeable or unfamiliar environments, it is important that animals develop strategies for goal-directed behaviors that meet the new challenges. We used a sequential paired-association task with asymmetric reward schedule to investigate how prefrontal neurons integrate multiple already-acquired associations to predict reward. Two types of reward-related neurons were observed in the lateral prefrontal cortex: one type predicted reward independent of physical properties of visual stimuli and the other encoded the reward value specific to a category of stimuli defined by the task requirements. Neurons of the latter type were able to predict reward on the basis of stimuli that had not yet been associated with reward, provided that another stimulus from the same category was paired with reward. The results suggest that prefrontal neurons can represent reward information on the basis of category and propagate this information to category members that have not been linked directly with any experience of reward.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

To adapt to changeable or unfamiliar environments, it is important that animals develop strategies for goal-directed behaviors that meet the new challenges. We used a sequential paired-association task with asymmetric reward schedule to investigate how prefrontal neurons integrate multiple already-acquired associations to predict reward. Two types of reward-related neurons were observed in the lateral prefrontal cortex: one type predicted reward independent of physical properties of visual stimuli and the other encoded the reward value specific to a category of stimuli defined by the task requirements. Neurons of the latter type were able to predict reward on the basis of stimuli that had not yet been associated with reward, provided that another stimulus from the same category was paired with reward. The results suggest that prefrontal neurons can represent reward information on the basis of category and propagate this information to category members that have not been linked directly with any experience of reward.

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  • doi:10.1038/nn.2128

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Britt Anderson; Ryan E. B. Mruczek; Keisuke Kawasaki; David L. Sheinberg

Effects of familiarity on neural activity in monkey inferior temporal lobe Journal Article

In: Cerebral Cortex, vol. 18, no. 11, pp. 2540–2552, 2008.

Abstract | Links | BibTeX

@article{Anderson2008a,
title = {Effects of familiarity on neural activity in monkey inferior temporal lobe},
author = {Britt Anderson and Ryan E. B. Mruczek and Keisuke Kawasaki and David L. Sheinberg},
doi = {10.1093/cercor/bhn015},
year = {2008},
date = {2008-01-01},
journal = {Cerebral Cortex},
volume = {18},
number = {11},
pages = {2540--2552},
abstract = {Long-term familiarity facilitates recognition of visual stimuli. To better understand the neural basis for this effect, we measured the local field potential (LFP) and multiunit spiking activity (MUA) from the inferior temporal (IT) lobe of behaving monkeys in response to novel and familiar images. In general, familiar images evoked larger amplitude LFPs whereas MUA responses were greater for novel images. Familiarity effects were attenuated by image rotations in the picture plane of 45 degrees. Decreasing image contrast led to more pronounced decreases in LFP response magnitude for novel, compared with familiar images, and resulted in more selective MUA response profiles for familiar images. The shape of individual LFP traces could be used for stimulus classification, and classification performance was better for the familiar image category. Recording the visual and auditory evoked LFP at multiple depths showed significant alterations in LFP morphology with distance changes of 2 mm. In summary, IT cortex shows local processing differences for familiar and novel images at a time scale and in a manner consistent with the observed behavioral advantage for classifying familiar images and rapidly detecting novel stimuli.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

Long-term familiarity facilitates recognition of visual stimuli. To better understand the neural basis for this effect, we measured the local field potential (LFP) and multiunit spiking activity (MUA) from the inferior temporal (IT) lobe of behaving monkeys in response to novel and familiar images. In general, familiar images evoked larger amplitude LFPs whereas MUA responses were greater for novel images. Familiarity effects were attenuated by image rotations in the picture plane of 45 degrees. Decreasing image contrast led to more pronounced decreases in LFP response magnitude for novel, compared with familiar images, and resulted in more selective MUA response profiles for familiar images. The shape of individual LFP traces could be used for stimulus classification, and classification performance was better for the familiar image category. Recording the visual and auditory evoked LFP at multiple depths showed significant alterations in LFP morphology with distance changes of 2 mm. In summary, IT cortex shows local processing differences for familiar and novel images at a time scale and in a manner consistent with the observed behavioral advantage for classifying familiar images and rapidly detecting novel stimuli.

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  • doi:10.1093/cercor/bhn015

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Britt Anderson; David L. Sheinberg

Effects of temporal context and temporal expectancy on neural activity in inferior temporal cortex Journal Article

In: Neuropsychologia, vol. 46, no. 4, pp. 947–957, 2008.

Abstract | Links | BibTeX

@article{Anderson2008,
title = {Effects of temporal context and temporal expectancy on neural activity in inferior temporal cortex},
author = {Britt Anderson and David L. Sheinberg},
doi = {10.1016/j.neuropsychologia.2007.11.025},
year = {2008},
date = {2008-01-01},
journal = {Neuropsychologia},
volume = {46},
number = {4},
pages = {947--957},
abstract = {Timing is critical. The same event can mean different things at different times and some events are more likely to occur at one time than another. We used a cued visual classification task to evaluate how changes in temporal context affect neural responses in inferior temporal cortex, an extrastriate visual area known to be involved in object processing. On each trial a first image cued a temporal delay before a second target image appeared. The animal's task was to classify the second image by pressing one of two buttons previously associated with that target. All images were used as both cues and targets. Whether an image cued a delay time or signaled a button press depended entirely upon whether it was the first or second picture in a trial. This paradigm allowed us to compare inferior temporal cortex neural activity to the same image subdivided by temporal context and expectation. Neuronal spiking was more robust and visually evoked local field potentials (LFP's) larger for target presentations than for cue presentations. On invalidly cued trials, when targets appeared unexpectedly early, the magnitude of the evoked LFP was reduced and delayed and neuronal spiking was attenuated. Spike field coherence increased in the beta-gamma frequency range for expected targets. In conclusion, different neural responses in higher order ventral visual cortex may occur for the same visual image based on manipulations of temporal attention.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

Timing is critical. The same event can mean different things at different times and some events are more likely to occur at one time than another. We used a cued visual classification task to evaluate how changes in temporal context affect neural responses in inferior temporal cortex, an extrastriate visual area known to be involved in object processing. On each trial a first image cued a temporal delay before a second target image appeared. The animal's task was to classify the second image by pressing one of two buttons previously associated with that target. All images were used as both cues and targets. Whether an image cued a delay time or signaled a button press depended entirely upon whether it was the first or second picture in a trial. This paradigm allowed us to compare inferior temporal cortex neural activity to the same image subdivided by temporal context and expectation. Neuronal spiking was more robust and visually evoked local field potentials (LFP's) larger for target presentations than for cue presentations. On invalidly cued trials, when targets appeared unexpectedly early, the magnitude of the evoked LFP was reduced and delayed and neuronal spiking was attenuated. Spike field coherence increased in the beta-gamma frequency range for expected targets. In conclusion, different neural responses in higher order ventral visual cortex may occur for the same visual image based on manipulations of temporal attention.

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  • doi:10.1016/j.neuropsychologia.2007.11.025

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Jan Churan; Farhan A. Khawaja; James M. G. Tsui; Christopher C. Pack

Brief motion stimuli preferentially activate surround-suppressed neurons in macaque visual area MT Journal Article

In: Current Biology, vol. 18, no. 22, pp. 1–6, 2008.

Abstract | Links | BibTeX

@article{Churan2008,
title = {Brief motion stimuli preferentially activate surround-suppressed neurons in macaque visual area MT},
author = {Jan Churan and Farhan A. Khawaja and James M. G. Tsui and Christopher C. Pack},
doi = {10.1016/j.cub.2008.10.003},
year = {2008},
date = {2008-01-01},
journal = {Current Biology},
volume = {18},
number = {22},
pages = {1--6},
abstract = {Intuitively one might think that larger objects should be easier to see, and indeed performance on visual tasks generally improves with increasing stimulus size [1,2]. Recently, a remarkable exception to this rule was reported [3]: when a high-contrast, moving stimulus is presented very briefly, motion perception deteriorates as stimulus size increases. This psychophysical surround suppression has been interpreted as a correlate of the neuronal surround suppression that is commonly found in the visual cortex [3-5]. However, many visual cortical neurons lack surround suppression, and so one might expect that the brain would simply use their outputs to discriminate the motion of large stimuli. Indeed previous work has generally found that observers rely on whichever neurons are most informative about the stimulus to perform similar psychophysical tasks [6]. Here we show that the responses of neurons in the middle temporal (MT) area of macaque monkeys provide a simple resolution to this paradox. We find that surround-suppressed MT neurons integrate motion signals relatively quickly, so that by comparison non-suppressed neurons respond poorly to brief stimuli. Thus, psychophysical surround suppression for brief stimuli can be viewed as a consequence of a strategy that weights neuronal responses according to how informative they are about a given stimulus. If this interpretation is correct, then it follows that any psychophysical experiment that uses brief motion stimuli will effectively probe the responses of MT neurons that have strong surround suppression.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

Intuitively one might think that larger objects should be easier to see, and indeed performance on visual tasks generally improves with increasing stimulus size [1,2]. Recently, a remarkable exception to this rule was reported [3]: when a high-contrast, moving stimulus is presented very briefly, motion perception deteriorates as stimulus size increases. This psychophysical surround suppression has been interpreted as a correlate of the neuronal surround suppression that is commonly found in the visual cortex [3-5]. However, many visual cortical neurons lack surround suppression, and so one might expect that the brain would simply use their outputs to discriminate the motion of large stimuli. Indeed previous work has generally found that observers rely on whichever neurons are most informative about the stimulus to perform similar psychophysical tasks [6]. Here we show that the responses of neurons in the middle temporal (MT) area of macaque monkeys provide a simple resolution to this paradox. We find that surround-suppressed MT neurons integrate motion signals relatively quickly, so that by comparison non-suppressed neurons respond poorly to brief stimuli. Thus, psychophysical surround suppression for brief stimuli can be viewed as a consequence of a strategy that weights neuronal responses according to how informative they are about a given stimulus. If this interpretation is correct, then it follows that any psychophysical experiment that uses brief motion stimuli will effectively probe the responses of MT neurons that have strong surround suppression.

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  • doi:10.1016/j.cub.2008.10.003

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David D. Cox; Alexander M. Papanastassiou; Daniel Oreper; Benjamin B. Andken; James J. DiCarlo

High-resolution three-dimensional microelectrode brain mapping using stereo microfocal x-ray imaging Journal Article

In: Journal of Neurophysiology, vol. 100, no. 5, pp. 2966–2976, 2008.

Abstract | Links | BibTeX

@article{Cox2008,
title = {High-resolution three-dimensional microelectrode brain mapping using stereo microfocal x-ray imaging},
author = {David D. Cox and Alexander M. Papanastassiou and Daniel Oreper and Benjamin B. Andken and James J. DiCarlo},
doi = {10.1152/jn.90672.2008},
year = {2008},
date = {2008-01-01},
journal = {Journal of Neurophysiology},
volume = {100},
number = {5},
pages = {2966--2976},
abstract = {Much of our knowledge of brain function has been gleaned from studies using microelectrodes to characterize the response properties of individual neurons in vivo. However, because it is difficult to accurately determine the location of a microelectrode tip within the brain, it is impossible to systematically map the fine three-dimensional spatial organization of many brain areas, especially in deep structures. Here, we present a practical method based on digital stereo microfocal X-ray imaging that makes it possible to estimate the three-dimensional position of each and every microelectrode recording site in "real time" during experimental sessions. We determined the system's ex vivo localization accuracy to be better than 50 microm, and we show how we have used this method to coregister hundreds of deep-brain microelectrode recordings in monkeys to a common frame of reference with median error of <150 microm. We further show how we can coregister those sites with magnetic resonance images (MRIs), allowing for comparison with anatomy, and laying the groundwork for more detailed electrophysiology/functional MRI comparison. Minimally, this method allows one to marry the single-cell specificity of microelectrode recording with the spatial mapping abilities of imaging techniques; furthermore, it has the potential of yielding fundamentally new kinds of high-resolution maps of brain function.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

Much of our knowledge of brain function has been gleaned from studies using microelectrodes to characterize the response properties of individual neurons in vivo. However, because it is difficult to accurately determine the location of a microelectrode tip within the brain, it is impossible to systematically map the fine three-dimensional spatial organization of many brain areas, especially in deep structures. Here, we present a practical method based on digital stereo microfocal X-ray imaging that makes it possible to estimate the three-dimensional position of each and every microelectrode recording site in "real time" during experimental sessions. We determined the system's ex vivo localization accuracy to be better than 50 microm, and we show how we have used this method to coregister hundreds of deep-brain microelectrode recordings in monkeys to a common frame of reference with median error of <150 microm. We further show how we can coregister those sites with magnetic resonance images (MRIs), allowing for comparison with anatomy, and laying the groundwork for more detailed electrophysiology/functional MRI comparison. Minimally, this method allows one to marry the single-cell specificity of microelectrode recording with the spatial mapping abilities of imaging techniques; furthermore, it has the potential of yielding fundamentally new kinds of high-resolution maps of brain function.

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  • doi:10.1152/jn.90672.2008

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Stephen V. David; Benjamin Y. Hayden; James A. Mazer; Jack L. Gallant

Attention to stimulus features shifts spectral tuning of V4 neurons during natural vision Journal Article

In: Neuron, vol. 59, no. 3, pp. 509–521, 2008.

Abstract | Links | BibTeX

@article{David2008,
title = {Attention to stimulus features shifts spectral tuning of V4 neurons during natural vision},
author = {Stephen V. David and Benjamin Y. Hayden and James A. Mazer and Jack L. Gallant},
doi = {10.1016/j.neuron.2008.07.001},
year = {2008},
date = {2008-01-01},
journal = {Neuron},
volume = {59},
number = {3},
pages = {509--521},
abstract = {Previous neurophysiological studies suggest that attention can alter the baseline or gain of neurons in extrastriate visual areas but that it cannot change tuning. This suggests that neurons in visual cortex function as labeled lines whose meaning does not depend on task demands. To test this common assumption, we used a system identification approach to measure spatial frequency and orientation tuning in area V4 during two attentionally demanding visual search tasks, one that required fixation and one that allowed free viewing during search. We found that spatial attention modulates response baseline and gain but does not alter tuning, consistent with previous reports. In contrast, feature-based attention often shifts neuronal tuning. These tuning shifts are inconsistent with the labeled-line model and tend to enhance responses to stimulus features that distinguish the search target. Our data suggest that V4 neurons behave as matched filters that are dynamically tuned to optimize visual search.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

Previous neurophysiological studies suggest that attention can alter the baseline or gain of neurons in extrastriate visual areas but that it cannot change tuning. This suggests that neurons in visual cortex function as labeled lines whose meaning does not depend on task demands. To test this common assumption, we used a system identification approach to measure spatial frequency and orientation tuning in area V4 during two attentionally demanding visual search tasks, one that required fixation and one that allowed free viewing during search. We found that spatial attention modulates response baseline and gain but does not alter tuning, consistent with previous reports. In contrast, feature-based attention often shifts neuronal tuning. These tuning shifts are inconsistent with the labeled-line model and tend to enhance responses to stimulus features that distinguish the search target. Our data suggest that V4 neurons behave as matched filters that are dynamically tuned to optimize visual search.

Close

  • doi:10.1016/j.neuron.2008.07.001

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K. -M. Lee; Edward L. Keller

Neural activity in the frontal eye fields modulated by the number of alternatives in target choice Journal Article

In: Journal of Neuroscience, vol. 28, no. 9, pp. 2242–2251, 2008.

Abstract | Links | BibTeX

@article{Lee2008,
title = {Neural activity in the frontal eye fields modulated by the number of alternatives in target choice},
author = {K. -M. Lee and Edward L. Keller},
doi = {10.1523/JNEUROSCI.3596-07.2008},
year = {2008},
date = {2008-01-01},
journal = {Journal of Neuroscience},
volume = {28},
number = {9},
pages = {2242--2251},
abstract = {Selection of identical responses may not use the same neural mechanisms when the number of alternatives (NA) for the selection changes, as suggested by Hick's law. For elucidating the choice mechanisms, frontal eye field (FEF) neurons were monitored during a color-to-location choice saccade task as the number of potential targets was varied. Visual responses to alternative targets decreased as NA increased, whereas perisaccade activities increased with NA. These modulations of FEF activities seem closely related to the choice process because the activity enhancements coincided with the timing of target selection, and the neural modulation was greater as NA increased, features expected of neural correlates for a choice process from the perspective of Hick's law. Our current observations suggest two novel notions of FEF neuronal behavior that have not been reported previously: (1) cells called "phasic visual" that do not discharge in the perisaccade interval in a delayed-saccade paradigm show such activity in a choice response task at the time of the saccade; and (2) the activity in FEF visuomotor cells display an inverse relationship between perisaccadic activity and the time of saccade triggering with higher levels of activity leading to longer saccade reaction times. These findings support the area's involvement in sensory-motor translation for target selection through coactivation and competitive interaction of neural populations that code for alternative action sets.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

Selection of identical responses may not use the same neural mechanisms when the number of alternatives (NA) for the selection changes, as suggested by Hick's law. For elucidating the choice mechanisms, frontal eye field (FEF) neurons were monitored during a color-to-location choice saccade task as the number of potential targets was varied. Visual responses to alternative targets decreased as NA increased, whereas perisaccade activities increased with NA. These modulations of FEF activities seem closely related to the choice process because the activity enhancements coincided with the timing of target selection, and the neural modulation was greater as NA increased, features expected of neural correlates for a choice process from the perspective of Hick's law. Our current observations suggest two novel notions of FEF neuronal behavior that have not been reported previously: (1) cells called "phasic visual" that do not discharge in the perisaccade interval in a delayed-saccade paradigm show such activity in a choice response task at the time of the saccade; and (2) the activity in FEF visuomotor cells display an inverse relationship between perisaccadic activity and the time of saccade triggering with higher levels of activity leading to longer saccade reaction times. These findings support the area's involvement in sensory-motor translation for target selection through coactivation and competitive interaction of neural populations that code for alternative action sets.

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  • doi:10.1523/JNEUROSCI.3596-07.2008

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Hans P. Op De Beeck; Jennifer A. Deutsch; Wim Vanduffel; Nancy Kanwisher; James J. DiCarlo

A stable topography of selectivity for unfamiliar shape classes in monkey inferior temporal cortex Journal Article

In: Cerebral Cortex, vol. 18, no. 7, pp. 1676–1694, 2008.

Abstract | Links | BibTeX

@article{OpDeBeeck2008,
title = {A stable topography of selectivity for unfamiliar shape classes in monkey inferior temporal cortex},
author = {Hans P. Op De Beeck and Jennifer A. Deutsch and Wim Vanduffel and Nancy Kanwisher and James J. DiCarlo},
doi = {10.1093/cercor/bhm196},
year = {2008},
date = {2008-01-01},
journal = {Cerebral Cortex},
volume = {18},
number = {7},
pages = {1676--1694},
abstract = {The inferior temporal (IT) cortex in monkeys plays a central role in visual object recognition and learning. Previous studies have observed patches in IT cortex with strong selectivity for highly familiar object classes (e.g., faces), but the principles behind this functional organization are largely unknown due to the many properties that distinguish different object classes. To unconfound shape from meaning and memory, we scanned monkeys with functional magnetic resonance imaging while they viewed classes of initially novel objects. Our data revealed a topography of selectivity for these novel object classes across IT cortex. We found that this selectivity topography was highly reproducible and remarkably stable across a 3-month interval during which monkeys were extensively trained to discriminate among exemplars within one of the object classes. Furthermore, this selectivity topography was largely unaffected by changes in behavioral task and object retinal position, both of which preserve shape. In contrast, it was strongly influenced by changes in object shape. The topography was partially related to, but not explained by, the previously described pattern of face selectivity. Together, these results suggest that IT cortex contains a large-scale map of shape that is largely independent of meaning, familiarity, and behavioral task.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

The inferior temporal (IT) cortex in monkeys plays a central role in visual object recognition and learning. Previous studies have observed patches in IT cortex with strong selectivity for highly familiar object classes (e.g., faces), but the principles behind this functional organization are largely unknown due to the many properties that distinguish different object classes. To unconfound shape from meaning and memory, we scanned monkeys with functional magnetic resonance imaging while they viewed classes of initially novel objects. Our data revealed a topography of selectivity for these novel object classes across IT cortex. We found that this selectivity topography was highly reproducible and remarkably stable across a 3-month interval during which monkeys were extensively trained to discriminate among exemplars within one of the object classes. Furthermore, this selectivity topography was largely unaffected by changes in behavioral task and object retinal position, both of which preserve shape. In contrast, it was strongly influenced by changes in object shape. The topography was partially related to, but not explained by, the previously described pattern of face selectivity. Together, these results suggest that IT cortex contains a large-scale map of shape that is largely independent of meaning, familiarity, and behavioral task.

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  • doi:10.1093/cercor/bhm196

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2007

Ryan E. B. Mruczek; David L. Sheinberg

Activity of inferior temporal cortical neurons predicts recognition choice behavior and recognition time during visual search Journal Article

In: Journal of Neuroscience, vol. 27, no. 11, pp. 2825–2836, 2007.

Abstract | Links | BibTeX

@article{Mruczek2007,
title = {Activity of inferior temporal cortical neurons predicts recognition choice behavior and recognition time during visual search},
author = {Ryan E. B. Mruczek and David L. Sheinberg},
doi = {10.1523/JNEUROSCI.4102-06.2007},
year = {2007},
date = {2007-01-01},
journal = {Journal of Neuroscience},
volume = {27},
number = {11},
pages = {2825--2836},
abstract = {Although the selectivity for complex stimuli exhibited by neurons in inferior temporal cortex is often taken as evidence of their role in visual perception, few studies have directly tested this hypothesis. Here, we sought to create a relatively natural task with few behavioral constraints to test whether activity in inferior temporal cortex neurons predicts whether or not a monkey will recognize and respond to a complex visual object. Monkeys were trained to freely view an array of images and report the presence of one of many possible target images previously associated with a hand response. On certain trials, the identity of the target was swapped during the monkeys' targeting saccade. Furthermore, the response association of the preswap target and the postswap target differed (e.g., right-to-left target swap). Neural activity in cells selective for the preswap target was significantly higher when the monkeys' response matched the hand association of the preswap target. Furthermore, the monkeys' response time was predicted by the magnitude of the presaccadic firing rate on nonswap trials. Our results provide additional support for the role of inferior temporal cortex in object recognition during natural behavior.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

Although the selectivity for complex stimuli exhibited by neurons in inferior temporal cortex is often taken as evidence of their role in visual perception, few studies have directly tested this hypothesis. Here, we sought to create a relatively natural task with few behavioral constraints to test whether activity in inferior temporal cortex neurons predicts whether or not a monkey will recognize and respond to a complex visual object. Monkeys were trained to freely view an array of images and report the presence of one of many possible target images previously associated with a hand response. On certain trials, the identity of the target was swapped during the monkeys' targeting saccade. Furthermore, the response association of the preswap target and the postswap target differed (e.g., right-to-left target swap). Neural activity in cells selective for the preswap target was significantly higher when the monkeys' response matched the hand association of the preswap target. Furthermore, the monkeys' response time was predicted by the magnitude of the presaccadic firing rate on nonswap trials. Our results provide additional support for the role of inferior temporal cortex in object recognition during natural behavior.

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  • doi:10.1523/JNEUROSCI.4102-06.2007

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Ryan E. B. Mruczek; David L. Sheinberg

Context familiarity enhances target processing by inferior temporal cortex neurons Journal Article

In: Journal of Neuroscience, vol. 27, no. 32, pp. 8533–8545, 2007.

Abstract | Links | BibTeX

@article{Mruczek2007a,
title = {Context familiarity enhances target processing by inferior temporal cortex neurons},
author = {Ryan E. B. Mruczek and David L. Sheinberg},
doi = {10.1523/JNEUROSCI.2106-07.2007},
year = {2007},
date = {2007-01-01},
journal = {Journal of Neuroscience},
volume = {27},
number = {32},
pages = {8533--8545},
abstract = {Experience-dependent changes in the response properties of ventral visual stream neurons are thought to underlie our ability to rapidly and efficiently recognize visual objects. How these neural changes are related to efficient visual processing during natural vision remains unclear. Here, we demonstrate a neurophysiological correlate of efficient visual search through highly familiar object arrays. Humans and monkeys are faster at locating the same target when it is surrounded by familiar compared with unfamiliar distractors. We show that this behavioral enhancement is driven by an increased sensitivity of target-selective neurons in inferior temporal cortex. This results from an increased "signal" for target representations and decreased "noise" from neighboring familiar distractors. These data highlight the dynamic properties of the inferior temporal cortex neurons and add to a growing body of evidence demonstrating how experience shapes neural processing in the ventral visual stream.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

Close

Experience-dependent changes in the response properties of ventral visual stream neurons are thought to underlie our ability to rapidly and efficiently recognize visual objects. How these neural changes are related to efficient visual processing during natural vision remains unclear. Here, we demonstrate a neurophysiological correlate of efficient visual search through highly familiar object arrays. Humans and monkeys are faster at locating the same target when it is surrounded by familiar compared with unfamiliar distractors. We show that this behavioral enhancement is driven by an increased sensitivity of target-selective neurons in inferior temporal cortex. This results from an increased "signal" for target representations and decreased "noise" from neighboring familiar distractors. These data highlight the dynamic properties of the inferior temporal cortex neurons and add to a growing body of evidence demonstrating how experience shapes neural processing in the ventral visual stream.

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  • doi:10.1523/JNEUROSCI.2106-07.2007

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