Leah Acker; Erica N Pino; Edward S Boyden; Robert Desimone FEF inactivation with improved optogenetic methods Journal Article Proceedings of the National Academy of Sciences, 113 (46), pp. E7297–E7306, 2016. Abstract | Links | BibTeX @article{Acker2016,
title = {FEF inactivation with improved optogenetic methods},
author = {Leah Acker and Erica N Pino and Edward S Boyden and Robert Desimone},
url = {http://www.pnas.org/lookup/doi/10.1073/pnas.1610784113},
doi = {10.1073/pnas.1610784113},
year = {2016},
date = {2016-01-01},
journal = {Proceedings of the National Academy of Sciences},
volume = {113},
number = {46},
pages = {E7297--E7306},
abstract = {Optogenetic methods have been highly effective for suppressing neural activity and modulating behavior in rodents, but effects have been much smaller in primates, which have much larger brains. Here, we present a suite of technologies to use optogenetics effectively in primates and apply these tools to a classic question in oculomotor control. First, we measured light absorption and heat propagation in vivo, optimized the conditions for using the red-light-shifted halorhodopsin Jaws in primates, and developed a large-volume illuminator to maximize light delivery with minimal heating and tissue displacement. Together, these advances allowed for nearly universal neuronal inactivation across more than 10 mm(3) of the cortex. Using these tools, we demonstrated large behavioral changes (i.e., up to several fold increases in error rate) with relatively low light power densities (≤100 mW/mm(2)) in the frontal eye field (FEF). Pharmacological inactivation studies have shown that the FEF is critical for executing saccades to remembered locations. FEF neurons increase their firing rate during the three epochs of the memory-guided saccade task: visual stimulus presentation, the delay interval, and motor preparation. It is unclear from earlier work, however, whether FEF activity during each epoch is necessary for memory-guided saccade execution. By harnessing the temporal specificity of optogenetics, we found that FEF contributes to memory-guided eye movements during every epoch of the memory-guided saccade task (the visual, delay, and motor periods).},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Optogenetic methods have been highly effective for suppressing neural activity and modulating behavior in rodents, but effects have been much smaller in primates, which have much larger brains. Here, we present a suite of technologies to use optogenetics effectively in primates and apply these tools to a classic question in oculomotor control. First, we measured light absorption and heat propagation in vivo, optimized the conditions for using the red-light-shifted halorhodopsin Jaws in primates, and developed a large-volume illuminator to maximize light delivery with minimal heating and tissue displacement. Together, these advances allowed for nearly universal neuronal inactivation across more than 10 mm(3) of the cortex. Using these tools, we demonstrated large behavioral changes (i.e., up to several fold increases in error rate) with relatively low light power densities (≤100 mW/mm(2)) in the frontal eye field (FEF). Pharmacological inactivation studies have shown that the FEF is critical for executing saccades to remembered locations. FEF neurons increase their firing rate during the three epochs of the memory-guided saccade task: visual stimulus presentation, the delay interval, and motor preparation. It is unclear from earlier work, however, whether FEF activity during each epoch is necessary for memory-guided saccade execution. By harnessing the temporal specificity of optogenetics, we found that FEF contributes to memory-guided eye movements during every epoch of the memory-guided saccade task (the visual, delay, and motor periods). |
Hamed Zivari Adab; Ivo D Popivanov; Wim Vanduffel; Rufin Vogels Perceptual learning of simple stimuli modifies stimulus representations in posterior inferior temporal cortex Journal Article Journal of Cognitive Neuroscience, 26 (10), pp. 2187–2200, 2014. Abstract | Links | BibTeX @article{Adab2014,
title = {Perceptual learning of simple stimuli modifies stimulus representations in posterior inferior temporal cortex},
author = {Hamed Zivari Adab and Ivo D Popivanov and Wim Vanduffel and Rufin Vogels},
doi = {10.1162/jocn},
year = {2014},
date = {2014-01-01},
journal = {Journal of Cognitive Neuroscience},
volume = {26},
number = {10},
pages = {2187--2200},
abstract = {Practicing simple visual detection and discrimination tasks improves performance, a signature of adult brain plasticity. The neural mechanisms that underlie these changes in performance are still unclear. Previously, we reported that practice in discriminating the orientation of noisy gratings (coarse orientation discrimination) increased the ability of single neurons in the early visual area V4 to discriminate the trained stimuli. Here, we ask whether practice in this task also changes the stimulus tuning properties of later visual cortical areas, despite the use of simple grating stimuli. To identify candidate areas, we used fMRI to map activations to noisy gratings in trained rhesus monkeys, revealing a region in the posterior inferior temporal (PIT) cortex. Subsequent single unit record- ings in PIT showed that the degree of orientation selectivity was similar to that of area V4 and that the PIT neurons discriminated the trained orientations better than the untrained orientations. Unlike in previous single unit studies of perceptual learning in early visual cortex, more PIT neurons preferred trained compared with untrained orientations. The effects of training on the responses to the grating stimuli were also present when the animals were performing a difficult orthogo- nal task in which the grating stimuli were task-irrelevant, suggesting that the training effect does not need attention to be expressed. The PIT neurons could support orientation discrimination at low signal-to-noise levels. These findings suggest that extensive practice in discriminating simple grating stimuli not only affects early visual cortex but also changes the stimulus tuning of a late visual cortical area.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Practicing simple visual detection and discrimination tasks improves performance, a signature of adult brain plasticity. The neural mechanisms that underlie these changes in performance are still unclear. Previously, we reported that practice in discriminating the orientation of noisy gratings (coarse orientation discrimination) increased the ability of single neurons in the early visual area V4 to discriminate the trained stimuli. Here, we ask whether practice in this task also changes the stimulus tuning properties of later visual cortical areas, despite the use of simple grating stimuli. To identify candidate areas, we used fMRI to map activations to noisy gratings in trained rhesus monkeys, revealing a region in the posterior inferior temporal (PIT) cortex. Subsequent single unit record- ings in PIT showed that the degree of orientation selectivity was similar to that of area V4 and that the PIT neurons discriminated the trained orientations better than the untrained orientations. Unlike in previous single unit studies of perceptual learning in early visual cortex, more PIT neurons preferred trained compared with untrained orientations. The effects of training on the responses to the grating stimuli were also present when the animals were performing a difficult orthogo- nal task in which the grating stimuli were task-irrelevant, suggesting that the training effect does not need attention to be expressed. The PIT neurons could support orientation discrimination at low signal-to-noise levels. These findings suggest that extensive practice in discriminating simple grating stimuli not only affects early visual cortex but also changes the stimulus tuning of a late visual cortical area. |
Hamed Zivari Adab; Rufin Vogels Perturbation of posterior inferior temporal cortical activity impairs coarse orientation discrimination Journal Article Cerebral Cortex, 26 (9), pp. 3814–3827, 2016. Abstract | Links | BibTeX @article{Adab2016,
title = {Perturbation of posterior inferior temporal cortical activity impairs coarse orientation discrimination},
author = {Hamed Zivari Adab and Rufin Vogels},
doi = {10.1093/cercor/bhv178},
year = {2016},
date = {2016-01-01},
journal = {Cerebral Cortex},
volume = {26},
number = {9},
pages = {3814--3827},
abstract = {It is reasonable to assume that the discrimination of simple visual stimuli depends on the activity of early visual cortical neurons, because simple visual features are supposedly coded in these areas whereas more complex features are coded in late visual areas. Recently, we showed that training monkeys in a coarse orientation discrimination task modified the response properties of single neurons in the posterior inferior temporal (PIT) cortex, a late visual area. Here, we examined the contribution of PIT to coarse orientation discrimination using causal perturbation methods. Electrical stimulation (ES) of PIT with currents of at least 100 µA impaired coarse orientation discrimination in monkeys. The performance deterioration did not exclusively reflect a general impairment to perform a difficult perceptual task. However, high current (650 µA) but not low-current (100 µA) ES also impaired fine color discrimination. ES of temporal regions dorsal or anterior to PIT produced less impairment of coarse orientation discrimination than ES of PIT. Injections of the GABA agonist muscimol into PIT also impaired performance. These data suggest that the late cortical area PIT is part of the network that supports coarse orientation discrimination of a simple grating stimulus, at least after extensive training in this task at threshold.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
It is reasonable to assume that the discrimination of simple visual stimuli depends on the activity of early visual cortical neurons, because simple visual features are supposedly coded in these areas whereas more complex features are coded in late visual areas. Recently, we showed that training monkeys in a coarse orientation discrimination task modified the response properties of single neurons in the posterior inferior temporal (PIT) cortex, a late visual area. Here, we examined the contribution of PIT to coarse orientation discrimination using causal perturbation methods. Electrical stimulation (ES) of PIT with currents of at least 100 µA impaired coarse orientation discrimination in monkeys. The performance deterioration did not exclusively reflect a general impairment to perform a difficult perceptual task. However, high current (650 µA) but not low-current (100 µA) ES also impaired fine color discrimination. ES of temporal regions dorsal or anterior to PIT produced less impairment of coarse orientation discrimination than ES of PIT. Injections of the GABA agonist muscimol into PIT also impaired performance. These data suggest that the late cortical area PIT is part of the network that supports coarse orientation discrimination of a simple grating stimulus, at least after extensive training in this task at threshold. |
Jordi Aguila; Javier Cudeiro; Casto Rivadulla Effects of static magnetic fields on the visual cortex: Reversible visual deficits and reduction of neuronal activity Journal Article Cerebral Cortex, 26 , pp. 628–638, 2016. Abstract | Links | BibTeX @article{Aguila2016,
title = {Effects of static magnetic fields on the visual cortex: Reversible visual deficits and reduction of neuronal activity},
author = {Jordi Aguila and Javier Cudeiro and Casto Rivadulla},
doi = {10.1093/cercor/bhu228},
year = {2016},
date = {2016-01-01},
journal = {Cerebral Cortex},
volume = {26},
pages = {628--638},
abstract = {Noninvasive brain stimulation techniques have been successfully used to modulate brain activity, have become a highly useful tool in basic and clinical research and, recently, have attracted increased attention due to their putative use as a method for neuro-enhancement. In this scenario, transcranial static magnetic stimulation (SMS) of moderate strength might represent an affordable, simple, and complementary method to other procedures, such as Transcranial Magnetic Stimulation or direct current stimulation, but its mechanisms and effects are not thoroughly understood. In this study, we show that static magnetic fields applied to visual cortex of awake primates cause reversible deficits in a visual detection task. Complementary experiments in anesthetized cats show that the visual deficits are a consequence of a strong reduction in neural activity. These results demonstrate that SMS is able to effectively modulate neuronal activity and could be considered to be a tool to be used for different purposes ranging from experimental studies to clinical applications.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Noninvasive brain stimulation techniques have been successfully used to modulate brain activity, have become a highly useful tool in basic and clinical research and, recently, have attracted increased attention due to their putative use as a method for neuro-enhancement. In this scenario, transcranial static magnetic stimulation (SMS) of moderate strength might represent an affordable, simple, and complementary method to other procedures, such as Transcranial Magnetic Stimulation or direct current stimulation, but its mechanisms and effects are not thoroughly understood. In this study, we show that static magnetic fields applied to visual cortex of awake primates cause reversible deficits in a visual detection task. Complementary experiments in anesthetized cats show that the visual deficits are a consequence of a strong reduction in neural activity. These results demonstrate that SMS is able to effectively modulate neuronal activity and could be considered to be a tool to be used for different purposes ranging from experimental studies to clinical applications. |
Ken Ichi Amemori; Ann M Graybiel Localized microstimulation of primate pregenual cingulate cortex induces negative decision-making Journal Article Nature Neuroscience, 15 (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}
}
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. |
Ken Ichi Amemori; Satoko Amemori; A M Graybiel Motivation and affective judgments differentially recruit neurons in the primate dorsolateral prefrontal and anterior cingulate cortex Journal Article Journal of Neuroscience, 35 (5), pp. 1939–1953, 2015. Abstract | Links | BibTeX @article{Amemori2015,
title = {Motivation and affective judgments differentially recruit neurons in the primate dorsolateral prefrontal and anterior cingulate cortex},
author = {Ken Ichi Amemori and Satoko Amemori and A M Graybiel},
url = {http://www.jneurosci.org/cgi/doi/10.1523/JNEUROSCI.1731-14.2015},
doi = {10.1523/JNEUROSCI.1731-14.2015},
year = {2015},
date = {2015-01-01},
journal = {Journal of Neuroscience},
volume = {35},
number = {5},
pages = {1939--1953},
abstract = {The judgment of whether to accept or to reject an offer is determined by positive and negative affect related to the offer, but affect also induces motivational responses. Rewarding and aversive cues influence the firing rates of many neurons in primate prefrontal and cingulate neocortical regions, but it still is unclear whether neurons in these regions are related to affective judgment or to motivation.To address this issue, we recorded simultaneously the neuronal spike activities of single units in the dorsolateral prefrontal cortex (dlPFC) and the anterior cingulate cortex (ACC) of macaque monkeys as they performed approach–avoidance (Ap–Av) and approach–approach (Ap–Ap) decision-making tasks that can behaviorally dissociate affective judgment and motivation. Notably, neurons having activity correlated with motivational condition could be distinguished from neurons having activity related to affective judgment, especially in the Ap–Av task. Although many neurons in both regions exhibited similar, selective patterns of task-related activity, we found a larger proportion of neurons activated in low motivational conditions in the dlPFC than in the ACC, and the onset of this activity was signifi- cantly earlier in the dlPFC than in the ACC. Furthermore, the temporal onsets of affective judgment represented by neuronal activities were significantly slower in the low motivational conditions than in the other conditions. These findings suggest that motivation and affective judgment both recruit dlPFC and ACC neurons but with differential degrees of involvement and timing.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
The judgment of whether to accept or to reject an offer is determined by positive and negative affect related to the offer, but affect also induces motivational responses. Rewarding and aversive cues influence the firing rates of many neurons in primate prefrontal and cingulate neocortical regions, but it still is unclear whether neurons in these regions are related to affective judgment or to motivation.To address this issue, we recorded simultaneously the neuronal spike activities of single units in the dorsolateral prefrontal cortex (dlPFC) and the anterior cingulate cortex (ACC) of macaque monkeys as they performed approach–avoidance (Ap–Av) and approach–approach (Ap–Ap) decision-making tasks that can behaviorally dissociate affective judgment and motivation. Notably, neurons having activity correlated with motivational condition could be distinguished from neurons having activity related to affective judgment, especially in the Ap–Av task. Although many neurons in both regions exhibited similar, selective patterns of task-related activity, we found a larger proportion of neurons activated in low motivational conditions in the dlPFC than in the ACC, and the onset of this activity was signifi- cantly earlier in the dlPFC than in the ACC. Furthermore, the temporal onsets of affective judgment represented by neuronal activities were significantly slower in the low motivational conditions than in the other conditions. These findings suggest that motivation and affective judgment both recruit dlPFC and ACC neurons but with differential degrees of involvement and timing. |
Satoko Amemori; Ken ichi Amemori; Margaret L Cantor; Ann M Graybiel A non-invasive head-holding device for chronic neural recordings in awake behaving monkeys Journal Article Journal of Neuroscience Methods, 240 , pp. 154–160, 2015. Abstract | Links | BibTeX @article{Amemori2015a,
title = {A non-invasive head-holding device for chronic neural recordings in awake behaving monkeys},
author = {Satoko Amemori and Ken ichi Amemori and Margaret L Cantor and Ann M Graybiel},
url = {http://dx.doi.org/10.1016/j.jneumeth.2014.11.006},
doi = {10.1016/j.jneumeth.2014.11.006},
year = {2015},
date = {2015-01-01},
journal = {Journal of Neuroscience Methods},
volume = {240},
pages = {154--160},
publisher = {Elsevier B.V.},
abstract = {Background: We have developed a novel head-holding device for behaving non-human primates that affords stability suitable for reliable chronic electrophysiological recording experiments. The device is completely non-invasive, and thus avoids the risk of infection and other complications that can occur with the use of conventional, surgically implanted head-fixation devices. New method: The device consists of a novel non-invasive head mold and bar clamp holder, and is customized to the shape of each monkey's head. The head-holding device that we introduce, combined with our recording system and reflection-based eye-tracking system, allows for chronic behavioral experiments and single-electrode or multi-electrode recording, as well as manipulation of brain activity. Results and comparison with existing methods: With electrodes implanted chronically in multiple brain regions, we could record neural activity from cortical and subcortical structures with stability equal to that recorded with conventional head-post fixation. Consistent with the non-invasive nature of the device, we could record neural signals for more than two years with a single implant. Importantly, the monkeys were able to hold stable eye fixation positions while held by this device, demonstrating the possibility of analyzing eye movement data with only the gentle restraint imposed by the non-invasive head-holding device. Conclusions: We show that the head-holding device introduced here can be extended to the head holding of smaller animals, and note that it could readily be adapted for magnetic resonance brain imaging over extended periods of time.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Background: We have developed a novel head-holding device for behaving non-human primates that affords stability suitable for reliable chronic electrophysiological recording experiments. The device is completely non-invasive, and thus avoids the risk of infection and other complications that can occur with the use of conventional, surgically implanted head-fixation devices. New method: The device consists of a novel non-invasive head mold and bar clamp holder, and is customized to the shape of each monkey's head. The head-holding device that we introduce, combined with our recording system and reflection-based eye-tracking system, allows for chronic behavioral experiments and single-electrode or multi-electrode recording, as well as manipulation of brain activity. Results and comparison with existing methods: With electrodes implanted chronically in multiple brain regions, we could record neural activity from cortical and subcortical structures with stability equal to that recorded with conventional head-post fixation. Consistent with the non-invasive nature of the device, we could record neural signals for more than two years with a single implant. Importantly, the monkeys were able to hold stable eye fixation positions while held by this device, demonstrating the possibility of analyzing eye movement data with only the gentle restraint imposed by the non-invasive head-holding device. Conclusions: We show that the head-holding device introduced here can be extended to the head holding of smaller animals, and note that it could readily be adapted for magnetic resonance brain imaging over extended periods of time. |
Britt Anderson; Ryan E B Mruczek; Keisuke Kawasaki; David Sheinberg Effects of familiarity on neural activity in monkey inferior temporal lobe Journal Article Cerebral Cortex, 18 (11), pp. 2540–2552, 2008. Abstract | Links | BibTeX @article{Anderson2008,
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 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}
}
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. |
Britt Anderson; David L Sheinberg Effects of temporal context and temporal expectancy on neural activity in inferior temporal cortex Journal Article Neuropsychologia, 46 (4), pp. 947–957, 2008. Abstract | Links | BibTeX @article{Anderson2008a,
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}
}
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. |
Evan G Antzoulatos; Earl K Miller Synchronous beta rhythms of frontoparietal networks support only behaviorally relevant representations Journal Article eLife, 5 (NOVEMBER2016), pp. 1–22, 2016. Abstract | Links | BibTeX @article{Antzoulatos2016,
title = {Synchronous beta rhythms of frontoparietal networks support only behaviorally relevant representations},
author = {Evan G Antzoulatos and Earl K Miller},
doi = {10.7554/eLife.17822},
year = {2016},
date = {2016-01-01},
journal = {eLife},
volume = {5},
number = {NOVEMBER2016},
pages = {1--22},
abstract = {Categorization has been associated with distributed networks of the primate brain, including the prefrontal (PFC) and posterior parietal cortices (PPC). Although category-selective spiking in PFC and PPC has been established, the frequency-dependent dynamic interactions of frontoparietal networks are largely unexplored. We trained monkeys to perform a delayed-match-to-spatial-category task while recording spikes and local field potentials from the PFC and PPC with multiple electrodes. We found category-selective beta- and delta-band synchrony between and within the areas. However, in addition to the categories, delta synchrony and spiking activity also reflected irrelevant stimulus dimensions. By contrast, beta synchrony only conveyed information about the task-relevant categories. Further, category-selective PFC neurons were synchronized with PPC beta oscillations, while neurons that carried irrelevant information were not. These results suggest that long-range beta-band synchrony could act as a filter that only supports neural representations of the variables relevant to the task at hand.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Categorization has been associated with distributed networks of the primate brain, including the prefrontal (PFC) and posterior parietal cortices (PPC). Although category-selective spiking in PFC and PPC has been established, the frequency-dependent dynamic interactions of frontoparietal networks are largely unexplored. We trained monkeys to perform a delayed-match-to-spatial-category task while recording spikes and local field potentials from the PFC and PPC with multiple electrodes. We found category-selective beta- and delta-band synchrony between and within the areas. However, in addition to the categories, delta synchrony and spiking activity also reflected irrelevant stimulus dimensions. By contrast, beta synchrony only conveyed information about the task-relevant categories. Further, category-selective PFC neurons were synchronized with PPC beta oscillations, while neurons that carried irrelevant information were not. These results suggest that long-range beta-band synchrony could act as a filter that only supports neural representations of the variables relevant to the task at hand. |
Mari Anzai; Soich Nagao Motor learning in common marmosets: Vestibulo-ocular reflex adaptation and its sensitivity to inhibitors of Purkinje cell long-term depression Journal Article Neuroscience Research, 83 , pp. 33–42, 2014. Abstract | Links | BibTeX @article{Anzai2014,
title = {Motor learning in common marmosets: Vestibulo-ocular reflex adaptation and its sensitivity to inhibitors of Purkinje cell long-term depression},
author = {Mari Anzai and Soich Nagao},
url = {http://dx.doi.org/10.1016/j.neures.2014.04.002},
doi = {10.1016/j.neures.2014.04.002},
year = {2014},
date = {2014-01-01},
journal = {Neuroscience Research},
volume = {83},
pages = {33--42},
publisher = {83},
abstract = {Adaptation of the horizontal vestibulo-ocular reflex (HVOR) provides an experimental model for cerebellum-dependent motor learning. We developed an eye movement measuring system and a paradigm for induction of HVOR adaptation for the common marmoset. The HVOR gain in dark measured by 10° (peak-to-peak amplitude) and 0.11-0.5. Hz turntable oscillation was around unity. The gain-up and gain-down HVOR adaptation was induced by 1. h of sustained out-of-phase and in-phase 10°-0.33. Hz combined turntable-screen oscillation in the light, respectively. To examine the role of long-term depression (LTD) of parallel fiber-Purkinje cell synapses, we intraperitonially applied T-588 or nimesulide, which block the induction of LTD in vitro or in vivo preparations, 1. h before the test of HVOR adaptation. T-588 (3 and 5. mg/kg body weight) did not affect nonadapted HVOR gains, and impaired both gain-up and gain-down HVOR adaptation. Nimesulide (3 and 6. mg/kg) did not affect nonadapted HVOR gains, and impaired gain-up HVOR adaptation dose-dependently; however, it very little affected gain-down HVOR adaptation. These findings are consistent with the results of our study of nimesulide on the adaptation of horizontal optokinetic response in mice (. Le et al., 2010), and support the view that LTD underlies HVOR adaptation.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Adaptation of the horizontal vestibulo-ocular reflex (HVOR) provides an experimental model for cerebellum-dependent motor learning. We developed an eye movement measuring system and a paradigm for induction of HVOR adaptation for the common marmoset. The HVOR gain in dark measured by 10° (peak-to-peak amplitude) and 0.11-0.5. Hz turntable oscillation was around unity. The gain-up and gain-down HVOR adaptation was induced by 1. h of sustained out-of-phase and in-phase 10°-0.33. Hz combined turntable-screen oscillation in the light, respectively. To examine the role of long-term depression (LTD) of parallel fiber-Purkinje cell synapses, we intraperitonially applied T-588 or nimesulide, which block the induction of LTD in vitro or in vivo preparations, 1. h before the test of HVOR adaptation. T-588 (3 and 5. mg/kg body weight) did not affect nonadapted HVOR gains, and impaired both gain-up and gain-down HVOR adaptation. Nimesulide (3 and 6. mg/kg) did not affect nonadapted HVOR gains, and impaired gain-up HVOR adaptation dose-dependently; however, it very little affected gain-down HVOR adaptation. These findings are consistent with the results of our study of nimesulide on the adaptation of horizontal optokinetic response in mice (. Le et al., 2010), and support the view that LTD underlies HVOR adaptation. |
Paul L Aparicio; Elias B Issa; James J DiCarlo Neurophysiological organization of the middle face patch in macaque inferior temporal cortex Journal Article Journal of Neuroscience, 36 (50), pp. 12729–12745, 2016. Abstract | Links | BibTeX @article{Aparicio2016,
title = {Neurophysiological organization of the middle face patch in macaque inferior temporal cortex},
author = {Paul L Aparicio and Elias B Issa and James J DiCarlo},
url = {http://www.jneurosci.org/lookup/doi/10.1523/JNEUROSCI.0237-16.2016},
doi = {10.1523/JNEUROSCI.0237-16.2016},
year = {2016},
date = {2016-01-01},
journal = {Journal of Neuroscience},
volume = {36},
number = {50},
pages = {12729--12745},
abstract = {While early cortical visual areas contain fine scale spatial organization of neuronal properties such as orientation preference, the spatial organization of higher-level visual areas is less well understood. The fMRI demonstration of face preferring regions in human ventral cortex (FFA, OFA) and monkey inferior temporal cortex ("face patches") raises the question of how neural selectivity for faces is organized. Here, we targeted hundreds of spatially registered neural recordings to the largest fMRI-identified face selective region in monkeys, the middle face patch (MFP) and show that the MFP contains a graded enrichment of face preferring neurons. At its center, as much as 93% of the sites we sampled responded twice as strongly to faces than to non-face objects. We estimate the maximum neurophysiological size of the MFP to be ∼6 mm in diameter, consistent with its previously reported size under fMRI. Importantly, face selectivity in the MFP varied strongly even between neighboring sites. Additionally, extremely face selective sites were ∼50x more likely to be present inside the MFP than outside. These results provide the first direct quantification of the size and neural composition of the MFP by showing that the cortical tissue localized to the fMRI defined region consists of a very high fraction of face preferring sites near its center, and a monotonic decrease in that fraction along any radial spatial axis.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
While early cortical visual areas contain fine scale spatial organization of neuronal properties such as orientation preference, the spatial organization of higher-level visual areas is less well understood. The fMRI demonstration of face preferring regions in human ventral cortex (FFA, OFA) and monkey inferior temporal cortex ("face patches") raises the question of how neural selectivity for faces is organized. Here, we targeted hundreds of spatially registered neural recordings to the largest fMRI-identified face selective region in monkeys, the middle face patch (MFP) and show that the MFP contains a graded enrichment of face preferring neurons. At its center, as much as 93% of the sites we sampled responded twice as strongly to faces than to non-face objects. We estimate the maximum neurophysiological size of the MFP to be ∼6 mm in diameter, consistent with its previously reported size under fMRI. Importantly, face selectivity in the MFP varied strongly even between neighboring sites. Additionally, extremely face selective sites were ∼50x more likely to be present inside the MFP than outside. These results provide the first direct quantification of the size and neural composition of the MFP by showing that the cortical tissue localized to the fMRI defined region consists of a very high fraction of face preferring sites near its center, and a monotonic decrease in that fraction along any radial spatial axis. |
Iñigo Arandia-Romero; Seiji Tanabe; Jan Drugowitsch; Adam Kohn; Rubén Moreno-Bote Multiplicative and additive modulation of neuronal tuning with population activity affects encoded information Journal Article Neuron, 89 (6), pp. 1305–1316, 2016. Abstract | Links | BibTeX @article{Arandia-Romero2016,
title = {Multiplicative and additive modulation of neuronal tuning with population activity affects encoded information},
author = {I{ñ}igo Arandia-Romero and Seiji Tanabe and Jan Drugowitsch and Adam Kohn and Rubén Moreno-Bote},
doi = {10.1016/j.neuron.2016.01.044},
year = {2016},
date = {2016-01-01},
journal = {Neuron},
volume = {89},
number = {6},
pages = {1305--1316},
abstract = {Numerous studies have shown that neuronal responses are modulated by stimulus properties and also by the state of the local network. However, little is known about how activity fluctuations of neuronal populations modulate the sensory tuning of cells and affect their encoded information. We found that fluctuations in ongoing and stimulus-evoked population activity in primate visual cortex modulate the tuning of neurons in a multiplicative and additive manner. While distributed on a continuum, neurons with stronger multiplicative effects tended to have less additive modulation and vice versa. The information encoded by multiplicatively modulated neurons increased with greater population activity, while that of additively modulated neurons decreased. These effects offset each other so that population activity had little effect on total information. Our results thus suggest that intrinsic activity fluctuations may act as a "traffic light" that determines which subset of neurons is most informative.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Numerous studies have shown that neuronal responses are modulated by stimulus properties and also by the state of the local network. However, little is known about how activity fluctuations of neuronal populations modulate the sensory tuning of cells and affect their encoded information. We found that fluctuations in ongoing and stimulus-evoked population activity in primate visual cortex modulate the tuning of neurons in a multiplicative and additive manner. While distributed on a continuum, neurons with stronger multiplicative effects tended to have less additive modulation and vice versa. The information encoded by multiplicatively modulated neurons increased with greater population activity, while that of additively modulated neurons decreased. These effects offset each other so that population activity had little effect on total information. Our results thus suggest that intrinsic activity fluctuations may act as a "traffic light" that determines which subset of neurons is most informative. |
Wael F Asaad; Navaneethan Santhanam; Steven McClellan; David J Freedman High-performance execution of psychophysical tasks with complex visual stimuli in MATLAB Journal Article Journal of Neurophysiology, 109 (1), pp. 249–260, 2013. Abstract | Links | BibTeX @article{Asaad2013,
title = {High-performance execution of psychophysical tasks with complex visual stimuli in MATLAB},
author = {Wael F Asaad and Navaneethan Santhanam and Steven McClellan and David J Freedman},
url = {http://jn.physiology.org/cgi/doi/10.1152/jn.00527.2012},
doi = {10.1152/jn.00527.2012},
year = {2013},
date = {2013-01-01},
journal = {Journal of Neurophysiology},
volume = {109},
number = {1},
pages = {249--260},
abstract = {Behavioral, psychological, and physiological experiments often require the ability to present sensory stimuli, monitor and record subjects' responses, interface with a wide range of devices, and precisely control the timing of events within a behavioral task. Here, we describe our recent progress developing an accessible and full-featured software system for controlling such studies using the MATLAB environment. Compared with earlier reports on this software, key new features have been implemented to allow the presentation of more complex visual stimuli, increase temporal precision, and enhance user interaction. These features greatly improve the performance of the system and broaden its applicability to a wider range of possible experiments. This report describes these new features and improvements, current limitations, and quantifies the performance of the system in a real-world experimental setting.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Behavioral, psychological, and physiological experiments often require the ability to present sensory stimuli, monitor and record subjects' responses, interface with a wide range of devices, and precisely control the timing of events within a behavioral task. Here, we describe our recent progress developing an accessible and full-featured software system for controlling such studies using the MATLAB environment. Compared with earlier reports on this software, key new features have been implemented to allow the presentation of more complex visual stimuli, increase temporal precision, and enhance user interaction. These features greatly improve the performance of the system and broaden its applicability to a wider range of possible experiments. This report describes these new features and improvements, current limitations, and quantifies the performance of the system in a real-world experimental setting. |
Habiba Azab; Benjamin Y Hayden Correlates of decisional dynamics in the dorsal anterior cingulate cortex Journal Article PLoS Biology, 15 (11), pp. 1–25, 2017. Abstract | Links | BibTeX @article{Azab2017,
title = {Correlates of decisional dynamics in the dorsal anterior cingulate cortex},
author = {Habiba Azab and Benjamin Y Hayden},
doi = {10.1371/journal.pbio.2003091},
year = {2017},
date = {2017-01-01},
journal = {PLoS Biology},
volume = {15},
number = {11},
pages = {1--25},
abstract = {We hypothesized that during binary economic choice, decision makers use the first option they attend as a default to which they compare the second. To test this idea, we recorded activity of neurons in the dorsal anterior cingulate cortex (dACC) of macaques choosing between gambles presented asynchronously. We find that ensemble encoding of the value of the first offer includes both choice-dependent and choice-independent aspects, as if reflecting a partial decision. That is, its responses are neither entirely pre- nor post-decisional. In contrast, coding of the value of the second offer is entirely decision dependent (i.e., post-decisional). This result holds even when offer-value encodings are compared within the same time period. Additionally, we see no evidence for 2 pools of neurons linked to the 2 offers; instead, all comparison appears to occur within a single functionally homogenous pool of task-selective neurons. These observations suggest that economic choices reflect a context-dependent evaluation of attended options. Moreover, they raise the possibility that value representations reflect, to some extent, a tentative commitment to a choice.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
We hypothesized that during binary economic choice, decision makers use the first option they attend as a default to which they compare the second. To test this idea, we recorded activity of neurons in the dorsal anterior cingulate cortex (dACC) of macaques choosing between gambles presented asynchronously. We find that ensemble encoding of the value of the first offer includes both choice-dependent and choice-independent aspects, as if reflecting a partial decision. That is, its responses are neither entirely pre- nor post-decisional. In contrast, coding of the value of the second offer is entirely decision dependent (i.e., post-decisional). This result holds even when offer-value encodings are compared within the same time period. Additionally, we see no evidence for 2 pools of neurons linked to the 2 offers; instead, all comparison appears to occur within a single functionally homogenous pool of task-selective neurons. These observations suggest that economic choices reflect a context-dependent evaluation of attended options. Moreover, they raise the possibility that value representations reflect, to some extent, a tentative commitment to a choice. |
Sahand Babapoor-Farrokhran; Martin Vinck; Thilo Womelsdorf; Stefan Everling Theta and beta synchrony coordinate frontal eye fields and anterior cingulate cortex during sensorimotor mapping Journal Article Nature Communications, 8 , pp. 1–14, 2017. Abstract | Links | BibTeX @article{Babapoor-Farrokhran2017,
title = {Theta and beta synchrony coordinate frontal eye fields and anterior cingulate cortex during sensorimotor mapping},
author = {Sahand Babapoor-Farrokhran and Martin Vinck and Thilo Womelsdorf and Stefan Everling},
url = {http://dx.doi.org/10.1038/ncomms13967},
doi = {10.1038/ncomms13967},
year = {2017},
date = {2017-01-01},
journal = {Nature Communications},
volume = {8},
pages = {1--14},
publisher = {Nature Publishing Group},
abstract = {The frontal eye fields (FEFs) and the anterior cingulate cortex (ACC) are commonly coactivated for cognitive saccade tasks, but whether this joined activation indexes coordinated activity underlying successful guidance of sensorimotor mapping is unknown. Here we test whether ACC and FEF circuits coordinate through phase synchronization of local field potential and neural spiking activity in macaque monkeys performing memory-guided and pro- and anti-saccades. We find that FEF and ACC showed prominent synchronization at a 3–9 Hz theta and a 12–30 Hz beta frequency band during the delay and preparation periods with a strong Granger-causal influence from ACC to FEF. The strength of theta- and beta-band coherence between ACC and FEF but not variations in power predict correct task performance. Taken together, the results support a role of ACC in cognitive control of frontoparietal networks and suggest that narrow-band theta and to some extent beta rhythmic activity indexes the coordination of relevant information during periods of enhanced control demands.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
The frontal eye fields (FEFs) and the anterior cingulate cortex (ACC) are commonly coactivated for cognitive saccade tasks, but whether this joined activation indexes coordinated activity underlying successful guidance of sensorimotor mapping is unknown. Here we test whether ACC and FEF circuits coordinate through phase synchronization of local field potential and neural spiking activity in macaque monkeys performing memory-guided and pro- and anti-saccades. We find that FEF and ACC showed prominent synchronization at a 3–9 Hz theta and a 12–30 Hz beta frequency band during the delay and preparation periods with a strong Granger-causal influence from ACC to FEF. The strength of theta- and beta-band coherence between ACC and FEF but not variations in power predict correct task performance. Taken together, the results support a role of ACC in cognitive control of frontoparietal networks and suggest that narrow-band theta and to some extent beta rhythmic activity indexes the coordination of relevant information during periods of enhanced control demands. |
Dong Hyun Baek; Jeyeon Lee; Hang Jin Byeon; Hoseok Choi; In Young Kim; Kyoung-Min Lee; James Jungho Pak; Dong Pyo Jang; Sang Hoon Lee A thin film polyimide mesh microelectrode for chronic epidural electrocorticography recording with enhanced contactability Journal Article Journal of Neural Engineering, 11 (4), pp. 1–10, 2014. Abstract | Links | BibTeX @article{Baek2014,
title = {A thin film polyimide mesh microelectrode for chronic epidural electrocorticography recording with enhanced contactability},
author = {Dong Hyun Baek and Jeyeon Lee and Hang Jin Byeon and Hoseok Choi and In Young Kim and Kyoung-Min Lee and James Jungho Pak and Dong Pyo Jang and Sang Hoon Lee},
doi = {10.1088/1741-2560/11/4/046023},
year = {2014},
date = {2014-01-01},
journal = {Journal of Neural Engineering},
volume = {11},
number = {4},
pages = {1--10},
publisher = {IOP Publishing},
abstract = {Objective. Epidural electrocorticography (ECoG) activity may be more reliable and stable than single-unit-activity or local field potential. Invasive brain computer interface (BCI) devices are limited by mechanical mismatching and cellular reactive responses due to differences in the elastic modulus and the motion of stiff electrodes. We propose a mesh-shaped electrode to enhance the contactability between surface of dura and electrode. Approach. We designed a polyimide (PI) electrode with a mesh pattern for more conformal contact with a curved surface. We compared the contact capability of mesh PI electrodes with conventionally used sheet PI electrode. The electrical properties of the mesh PI electrode were evaluated for four weeks. We recorded the epidural ECoG (eECoG) activity on the surface of rhesus monkey brains while they performed a saccadic task for four months. Main results. The mesh PI electrode showed good contact with the agarose brain surface, as evaluated by visual inspection and signal measurement. It was about 87% accurate in predicting the direction of saccade eye movement. Significance. Our results indicate that the mesh PI electrode was flexible and good contact on the curved surface and can record eECoG activity maintaining close contact to dura, which was proved by in vivo and in vitro test.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Objective. Epidural electrocorticography (ECoG) activity may be more reliable and stable than single-unit-activity or local field potential. Invasive brain computer interface (BCI) devices are limited by mechanical mismatching and cellular reactive responses due to differences in the elastic modulus and the motion of stiff electrodes. We propose a mesh-shaped electrode to enhance the contactability between surface of dura and electrode. Approach. We designed a polyimide (PI) electrode with a mesh pattern for more conformal contact with a curved surface. We compared the contact capability of mesh PI electrodes with conventionally used sheet PI electrode. The electrical properties of the mesh PI electrode were evaluated for four weeks. We recorded the epidural ECoG (eECoG) activity on the surface of rhesus monkey brains while they performed a saccadic task for four months. Main results. The mesh PI electrode showed good contact with the agarose brain surface, as evaluated by visual inspection and signal measurement. It was about 87% accurate in predicting the direction of saccade eye movement. Significance. Our results indicate that the mesh PI electrode was flexible and good contact on the curved surface and can record eECoG activity maintaining close contact to dura, which was proved by in vivo and in vitro test. |
David L Barack; Steve W C Chang; Michael L Platt Posterior cingulate neurons dynamically signal decisions to disengage during foraging Journal Article Neuron, 96 (2), pp. 339–347, 2017. Abstract | Links | BibTeX @article{Barack2017,
title = {Posterior cingulate neurons dynamically signal decisions to disengage during foraging},
author = {David L Barack and Steve W C Chang and Michael L Platt},
url = {https://doi.org/10.1016/j.neuron.2017.09.048},
doi = {10.1016/j.neuron.2017.09.048},
year = {2017},
date = {2017-01-01},
journal = {Neuron},
volume = {96},
number = {2},
pages = {339--347},
publisher = {Elsevier Inc.},
abstract = {Foraging for resources is a fundamental behavior balancing systematic search and strategic disengagement. The foraging behavior of primates is especially complex and requires long-term memory, value comparison, strategic planning, and decision-making. Here we provide evidence from two different foraging tasks that neurons in primate posterior cingulate cortex (PCC) signal decision salience during foraging to motivate disengagement from the current strategy. In our foraging tasks, salience refers to the difference between decision thresholds and the net harvested reward. Salience signals were stronger in poor foraging contexts than rich ones, suggesting low harvest rates recruit mechanisms in PCC that regulate strategic disengagement and exploration during foraging. Barack et al. report that foraging salience motivated strategic disengagement in two distinct tasks. Posterior cingulate neurons preferentially signaled salience and forecast divergent choices when reward rates were low, suggesting a role in the strategic control of behavior.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Foraging for resources is a fundamental behavior balancing systematic search and strategic disengagement. The foraging behavior of primates is especially complex and requires long-term memory, value comparison, strategic planning, and decision-making. Here we provide evidence from two different foraging tasks that neurons in primate posterior cingulate cortex (PCC) signal decision salience during foraging to motivate disengagement from the current strategy. In our foraging tasks, salience refers to the difference between decision thresholds and the net harvested reward. Salience signals were stronger in poor foraging contexts than rich ones, suggesting low harvest rates recruit mechanisms in PCC that regulate strategic disengagement and exploration during foraging. Barack et al. report that foraging salience motivated strategic disengagement in two distinct tasks. Posterior cingulate neurons preferentially signaled salience and forecast divergent choices when reward rates were low, suggesting a role in the strategic control of behavior. |
Jalal K Baruni; Brian Lau; Daniel C Salzman Reward expectation differentially modulates attentional behavior and activity in visual area V4 Journal Article Nature Neuroscience, 18 (11), pp. 1656–1663, 2015. Abstract | Links | BibTeX @article{Baruni2015,
title = {Reward expectation differentially modulates attentional behavior and activity in visual area V4},
author = {Jalal K Baruni and Brian Lau and Daniel C Salzman},
url = {http://dx.doi.org/10.1038/nn.4141},
doi = {10.1038/nn.4141},
year = {2015},
date = {2015-01-01},
journal = {Nature Neuroscience},
volume = {18},
number = {11},
pages = {1656--1663},
publisher = {Nature Publishing Group},
abstract = {Neural activity in visual area V4 is enhanced when attention is directed into neuronal receptive fields. However, the source of this enhancement is unclear, as most physiological studies have manipulated attention by changing the absolute reward associated with a particular location as well as its value relative to other locations. We trained monkeys to discriminate the orientation of two stimuli presented simultaneously in different hemifields while we independently varied the reward magnitude associated with correct discrimination at each location. Behavioral measures of attention were controlled by the relative value of each location. By contrast, neurons in V4 were consistently modulated by absolute reward value, exhibiting increased activity, increased gamma-band power and decreased trial-to-trial variability whenever receptive field locations were associated with large rewards. These data challenge the notion that the perceptual benefits of spatial attention rely on increased signal-to-noise in V4. Instead, these benefits likely derive from downstream selection mechanisms.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Neural activity in visual area V4 is enhanced when attention is directed into neuronal receptive fields. However, the source of this enhancement is unclear, as most physiological studies have manipulated attention by changing the absolute reward associated with a particular location as well as its value relative to other locations. We trained monkeys to discriminate the orientation of two stimuli presented simultaneously in different hemifields while we independently varied the reward magnitude associated with correct discrimination at each location. Behavioral measures of attention were controlled by the relative value of each location. By contrast, neurons in V4 were consistently modulated by absolute reward value, exhibiting increased activity, increased gamma-band power and decreased trial-to-trial variability whenever receptive field locations were associated with large rewards. These data challenge the notion that the perceptual benefits of spatial attention rely on increased signal-to-noise in V4. Instead, these benefits likely derive from downstream selection mechanisms. |
Charles B Beaman; Sarah L Eagleman; Valentin Dragoi Sensory coding accuracy and perceptual performance are improved during the desynchronized cortical state Journal Article Nature Communications, 8 (1), pp. 1–14, 2017. Abstract | Links | BibTeX @article{Beaman2017,
title = {Sensory coding accuracy and perceptual performance are improved during the desynchronized cortical state},
author = {Charles B Beaman and Sarah L Eagleman and Valentin Dragoi},
url = {http://dx.doi.org/10.1038/s41467-017-01030-4},
doi = {10.1038/s41467-017-01030-4},
year = {2017},
date = {2017-01-01},
journal = {Nature Communications},
volume = {8},
number = {1},
pages = {1--14},
publisher = {Springer US},
abstract = {Cortical activity changes continuously during the course of the day. At a global scale, population activity varies between the ‘synchronized' state during sleep and ‘desynchronized' state during waking. However, whether local fluctuations in population synchrony during wakefulness modulate the accuracy of sensory encoding and behavioral performance is poorly understood. Here, we show that populations of cells in monkey visual cortex exhibit rapid fluctuations in synchrony ranging from desynchronized responses, indicative of high alertness, to highly synchronized responses. These fluctuations are local and control the trial variability in population coding accuracy and behavioral performance in a discrimination task. When local population activity is desynchronized, the correlated variability between neurons is reduced, and network and behavioral performance are enhanced. These findings demonstrate that the structure of variability in local cortical populations is not noise but rather controls how sensory information is optimally integrated with ongoing processes to guide network coding and behavior.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Cortical activity changes continuously during the course of the day. At a global scale, population activity varies between the ‘synchronized' state during sleep and ‘desynchronized' state during waking. However, whether local fluctuations in population synchrony during wakefulness modulate the accuracy of sensory encoding and behavioral performance is poorly understood. Here, we show that populations of cells in monkey visual cortex exhibit rapid fluctuations in synchrony ranging from desynchronized responses, indicative of high alertness, to highly synchronized responses. These fluctuations are local and control the trial variability in population coding accuracy and behavioral performance in a discrimination task. When local population activity is desynchronized, the correlated variability between neurons is reduced, and network and behavioral performance are enhanced. These findings demonstrate that the structure of variability in local cortical populations is not noise but rather controls how sensory information is optimally integrated with ongoing processes to guide network coding and behavior. |
Joachim Bellet; Chih-Yang Chen; Ziad M Hafed Sequential hemifield gating of alpha and beta behavioral performance oscillations after microsaccades Journal Article Journal of Neurophysiology, 118 , pp. 2789–2805, 2017. Abstract | Links | BibTeX @article{Bellet2017,
title = {Sequential hemifield gating of alpha and beta behavioral performance oscillations after microsaccades},
author = {Joachim Bellet and Chih-Yang Chen and Ziad M Hafed},
url = {http://jn.physiology.org/lookup/doi/10.1152/jn.00253.2017},
doi = {10.1152/jn.00253.2017},
year = {2017},
date = {2017-01-01},
journal = {Journal of Neurophysiology},
volume = {118},
pages = {2789--2805},
abstract = {Microsaccades are tiny saccades that occur during gaze fixation. Even though visual processing has been shown to be strongly modulated close to the time of microsaccades, both at central and peripheral eccentricities, it is not clear how these eye movements might influence longer term fluctuations in brain activity and behavior. Here we found that visual processing is significantly affected and, in a rhythmic manner, even several hundreds of milliseconds after a microsaccade. Human visual detection efficiency, as measured by reaction time, exhibited coherent rhythmic oscillations in the ? - and ? -frequency bands for up to ~650–700 ms after a microsaccade. Surprisingly, the oscillations were sequentially pulsed across visual hemifields relative to microsaccade direction, first occurring in the same hemifield as the movement vector for ~400 ms and then the opposite. Such pulsing also affected perceptual detection performance. Our results suggest that visual processing is subject to long-lasting oscillations that are phase locked to microsaccade generation, and that these oscillations are dependent on microsaccade direction.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Microsaccades are tiny saccades that occur during gaze fixation. Even though visual processing has been shown to be strongly modulated close to the time of microsaccades, both at central and peripheral eccentricities, it is not clear how these eye movements might influence longer term fluctuations in brain activity and behavior. Here we found that visual processing is significantly affected and, in a rhythmic manner, even several hundreds of milliseconds after a microsaccade. Human visual detection efficiency, as measured by reaction time, exhibited coherent rhythmic oscillations in the ? - and ? -frequency bands for up to ~650–700 ms after a microsaccade. Surprisingly, the oscillations were sequentially pulsed across visual hemifields relative to microsaccade direction, first occurring in the same hemifield as the movement vector for ~400 ms and then the opposite. Such pulsing also affected perceptual detection performance. Our results suggest that visual processing is subject to long-lasting oscillations that are phase locked to microsaccade generation, and that these oscillations are dependent on microsaccade direction. |
Narcisse P Bichot; Matthew T Heard; Robert Desimone Stimulation of the nucleus accumbens as behavioral reward in awake behaving monkeys Journal Article Journal of Neuroscience Methods, 199 (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},
url = {http://dx.doi.org/10.1016/j.jneumeth.2011.05.025},
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}
}
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. |
Narcisse P Bichot; Matthew T Heard; Ellen M DeGennaro; Robert Desimone A source for feature-based attention in the prefrontal cortex Journal Article Neuron, 88 (4), pp. 832–844, 2015. Abstract | Links | BibTeX @article{Bichot2015,
title = {A source for feature-based attention in the prefrontal cortex},
author = {Narcisse P Bichot and Matthew T Heard and Ellen M DeGennaro and Robert Desimone},
url = {http://dx.doi.org/10.1016/j.neuron.2015.10.001},
doi = {10.1016/j.neuron.2015.10.001},
year = {2015},
date = {2015-01-01},
journal = {Neuron},
volume = {88},
number = {4},
pages = {832--844},
publisher = {Elsevier Inc.},
abstract = {In cluttered scenes, we can use feature-based attention to quickly locate a target object. To understand how feature attention is used to find and select objects for action, we focused on the ventral prearcuate (VPA) region of prefrontal cortex. In a visual search task, VPA cells responded selectively to search cues, maintained their feature selectivity throughout the delay and subsequent saccades, and discriminated the search target in their receptive fields with a time course earlier than in FEF or IT cortex. Inactivation of VPA impaired the animals' ability to find targets, and simultaneous recordings in FEF revealed that the effects of feature attention were eliminated while leaving the effects of spatial attention in FEF intact. Altogether, the results suggest that VPA neurons compute the locations of objects with the features sought and send this information to FEF to guide eye movements to those relevant stimuli.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
In cluttered scenes, we can use feature-based attention to quickly locate a target object. To understand how feature attention is used to find and select objects for action, we focused on the ventral prearcuate (VPA) region of prefrontal cortex. In a visual search task, VPA cells responded selectively to search cues, maintained their feature selectivity throughout the delay and subsequent saccades, and discriminated the search target in their receptive fields with a time course earlier than in FEF or IT cortex. Inactivation of VPA impaired the animals' ability to find targets, and simultaneous recordings in FEF revealed that the effects of feature attention were eliminated while leaving the effects of spatial attention in FEF intact. Altogether, the results suggest that VPA neurons compute the locations of objects with the features sought and send this information to FEF to guide eye movements to those relevant stimuli. |
T C Blanchard; J M Pearson; B Y Hayden Postreward delays and systematic biases in measures of animal temporal discounting Journal Article Proceedings of the National Academy of Sciences, 110 (38), pp. 15491–15496, 2013. Abstract | Links | BibTeX @article{Blanchard2013,
title = {Postreward delays and systematic biases in measures of animal temporal discounting},
author = {T C Blanchard and J M Pearson and B Y Hayden},
url = {http://www.pnas.org/cgi/doi/10.1073/pnas.1310446110},
doi = {10.1073/pnas.1310446110},
year = {2013},
date = {2013-01-01},
journal = {Proceedings of the National Academy of Sciences},
volume = {110},
number = {38},
pages = {15491--15496},
abstract = {Intertemporal choice tasks, which pit smaller/sooner rewards against larger/later ones, are frequently used to study time preferences and, by extension, impulsivity and self-control. When used in animals, many trials are strung together in sequence and an adjusting buffer is added after the smaller/sooner option to hold the total duration of each trial constant. Choices of the smaller/sooner option are not reward maximizing and so are taken to indicate that the animal is discounting future rewards. However, if animals fail to correctly factor in the duration of the postreward buffers, putative discounting behavior may instead reflect constrained reward maximization. Here, we report three results consistent with this discounting-free hypothesis. We find that (i) monkeys are insensitive to the association between the duration of postreward delays and their choices; (ii) they are sensitive to the length of postreward delays, although they greatly underestimate them; and (iii) increasing the salience of the postreward delay biases monkeys toward the larger/later option, reducing measured discounting rates. These results are incompatible with standard discounting-based accounts but are compatible with an alternative heuristic model. Our data suggest that measured intertemporal preferences in animals may not reflect impulsivity, or even mental discounting of future options, and that standard human and animal intertemporal choice tasks measure unrelated mental processes.},
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pubstate = {published},
tppubtype = {article}
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Intertemporal choice tasks, which pit smaller/sooner rewards against larger/later ones, are frequently used to study time preferences and, by extension, impulsivity and self-control. When used in animals, many trials are strung together in sequence and an adjusting buffer is added after the smaller/sooner option to hold the total duration of each trial constant. Choices of the smaller/sooner option are not reward maximizing and so are taken to indicate that the animal is discounting future rewards. However, if animals fail to correctly factor in the duration of the postreward buffers, putative discounting behavior may instead reflect constrained reward maximization. Here, we report three results consistent with this discounting-free hypothesis. We find that (i) monkeys are insensitive to the association between the duration of postreward delays and their choices; (ii) they are sensitive to the length of postreward delays, although they greatly underestimate them; and (iii) increasing the salience of the postreward delay biases monkeys toward the larger/later option, reducing measured discounting rates. These results are incompatible with standard discounting-based accounts but are compatible with an alternative heuristic model. Our data suggest that measured intertemporal preferences in animals may not reflect impulsivity, or even mental discounting of future options, and that standard human and animal intertemporal choice tasks measure unrelated mental processes. |
T C Blanchard; B Y Hayden Neurons in dorsal anterior cingulate cortex signal postdecisional variables in a foraging task Journal Article Journal of Neuroscience, 34 (2), pp. 646–655, 2014. Abstract | Links | BibTeX @article{Blanchard2014,
title = {Neurons in dorsal anterior cingulate cortex signal postdecisional variables in a foraging task},
author = {T C Blanchard and B Y Hayden},
url = {http://www.jneurosci.org/cgi/doi/10.1523/JNEUROSCI.3151-13.2014},
doi = {10.1523/JNEUROSCI.3151-13.2014},
year = {2014},
date = {2014-01-01},
journal = {Journal of Neuroscience},
volume = {34},
number = {2},
pages = {646--655},
abstract = {The dorsal anterior cingulate cortex (dACC) is a key hub of the brain's executive control system. Although a great deal is known about its role in outcome monitoring and behavioral adjustment, whether and how it contributes to the decision process remain unclear. Some theories suggest that dACC neurons track decision variables (e.g., option values) that feed into choice processes and is thus "predecisional." Other theories suggest that dACC activity patterns differ qualitatively depending on the choice that is made and is thus "postdecisional." To compare these hypotheses, we examined responses of 124 dACC neurons in a simple foraging task in which monkeys accepted or rejected offers of delayed rewards. In this task, options that vary in benefit (reward size) and cost (delay) appear for 1 s; accepting the option provides the cued reward after the cued delay. To get at dACC neurons' contributions to decisions, we focused on responses around the time of choice, several seconds before the reward and the end of the trial. We found that dACC neurons signal the foregone value of the rejected option, a postdecisional variable. Neurons also signal the profitability (that is, the relative value) of the offer, but even these signals are qualitatively different on accept and reject decisions, meaning that they are also postdecisional. These results suggest that dACC can be placed late in the decision process and also support models that give it a regulatory role in decision, rather than serving as a site of comparison.},
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The dorsal anterior cingulate cortex (dACC) is a key hub of the brain's executive control system. Although a great deal is known about its role in outcome monitoring and behavioral adjustment, whether and how it contributes to the decision process remain unclear. Some theories suggest that dACC neurons track decision variables (e.g., option values) that feed into choice processes and is thus "predecisional." Other theories suggest that dACC activity patterns differ qualitatively depending on the choice that is made and is thus "postdecisional." To compare these hypotheses, we examined responses of 124 dACC neurons in a simple foraging task in which monkeys accepted or rejected offers of delayed rewards. In this task, options that vary in benefit (reward size) and cost (delay) appear for 1 s; accepting the option provides the cued reward after the cued delay. To get at dACC neurons' contributions to decisions, we focused on responses around the time of choice, several seconds before the reward and the end of the trial. We found that dACC neurons signal the foregone value of the rejected option, a postdecisional variable. Neurons also signal the profitability (that is, the relative value) of the offer, but even these signals are qualitatively different on accept and reject decisions, meaning that they are also postdecisional. These results suggest that dACC can be placed late in the decision process and also support models that give it a regulatory role in decision, rather than serving as a site of comparison. |
Tommy C Blanchard; Andreas Wilke; Benjamin Y Hayden Hot-hand bias in rhesus monkeys Journal Article Journal of Experimental Psychology: Animal Behavior Processes, 40 (3), pp. 280–286, 2014. Abstract | Links | BibTeX @article{Blanchard2014a,
title = {Hot-hand bias in rhesus monkeys},
author = {Tommy C Blanchard and Andreas Wilke and Benjamin Y Hayden},
doi = {10.1037/xan0000033},
year = {2014},
date = {2014-01-01},
journal = {Journal of Experimental Psychology: Animal Behavior Processes},
volume = {40},
number = {3},
pages = {280--286},
abstract = {Human decision-makers often exhibit the hot-hand phenomenon, a tendency to perceive positive serial autocorrelations in independent sequential events. The term is named after the observation that basketball fans and players tend to perceive streaks of high accuracy shooting when they are demonstrably absent. That is, both observing fans and participating players tend to hold the belief that a player's chance of hitting a shot are greater following a hit than following a miss. We hypothesize that this bias reflects a strong and stable tendency among primates (including humans) to perceive positive autocorrelations in temporal sequences, that this bias is an adaptation to clumpy foraging environments, and that it may even be ecologically rational. Several studies support this idea in humans, but a stronger test would be to determine whether nonhuman primates also exhibit a hot-hand bias. Here we report behavior of 3 monkeys performing a novel gambling task in which correlation between sequential gambles (i.e., temporal clumpiness) is systematically manipulated. We find that monkeys have better performance (meaning, more optimal behavior) for clumped (positively correlated) than for dispersed (negatively correlated) distributions. These results identify and quantify a new bias in monkeys' risky decisions, support accounts that specifically incorporate cognitive biases into risky choice, and support the suggestion that the hot-hand phenomenon is an evolutionary ancient bias.},
keywords = {},
pubstate = {published},
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Human decision-makers often exhibit the hot-hand phenomenon, a tendency to perceive positive serial autocorrelations in independent sequential events. The term is named after the observation that basketball fans and players tend to perceive streaks of high accuracy shooting when they are demonstrably absent. That is, both observing fans and participating players tend to hold the belief that a player's chance of hitting a shot are greater following a hit than following a miss. We hypothesize that this bias reflects a strong and stable tendency among primates (including humans) to perceive positive autocorrelations in temporal sequences, that this bias is an adaptation to clumpy foraging environments, and that it may even be ecologically rational. Several studies support this idea in humans, but a stronger test would be to determine whether nonhuman primates also exhibit a hot-hand bias. Here we report behavior of 3 monkeys performing a novel gambling task in which correlation between sequential gambles (i.e., temporal clumpiness) is systematically manipulated. We find that monkeys have better performance (meaning, more optimal behavior) for clumped (positively correlated) than for dispersed (negatively correlated) distributions. These results identify and quantify a new bias in monkeys' risky decisions, support accounts that specifically incorporate cognitive biases into risky choice, and support the suggestion that the hot-hand phenomenon is an evolutionary ancient bias. |
Tommy C Blanchard; Lauren S Wolfe; Ivo Vlaev; Joel S Winston; Benjamin Y Hayden Biases in preferences for sequences of outcomes in monkeys Journal Article Cognition, 130 (3), pp. 289–299, 2014. Abstract | Links | BibTeX @article{Blanchard2014b,
title = {Biases in preferences for sequences of outcomes in monkeys},
author = {Tommy C Blanchard and Lauren S Wolfe and Ivo Vlaev and Joel S Winston and Benjamin Y Hayden},
url = {http://dx.doi.org/10.1016/j.cognition.2013.11.012},
doi = {10.1016/j.cognition.2013.11.012},
year = {2014},
date = {2014-01-01},
journal = {Cognition},
volume = {130},
number = {3},
pages = {289--299},
publisher = {Elsevier B.V.},
abstract = {Movies, vacations, and meals are all examples of events composed of a sequence of smaller events. How do we go from our evaluations of each scene in a movie to an evaluation of the sequence as a whole$alpha$ In theory, we should simply average the values of the individual events. In practice, however, we are biased towards sequences where each element tends to be better than the previous, where the last value is large, and we overweight the best (or worst) part of the sequence. To study how general these biases are we examined monkeys' preferences for sequences of rewards in a novel reward repeat task. Monkeys were first given a sequence of rewards and then chose between repeating the sequence or receiving a standard comparator sequence. We found that, like humans, monkeys overweight events that happen later in a sequence, so much so that adding a small reward to the end of a sequence can paradoxically reduce its value. Monkeys were also biased towards sequences with large peak values (the highest value in the sequence), but only following a working memory challenge, suggesting that this preference may be driven by memory limitations. These results demonstrate the cross-species nature of biases in preferences for sequences of outcomes. In addition, monkeys' consistent preference for sequences in which large values occur later challenges the generality of discounting models of intertemporal choice in animals.},
keywords = {},
pubstate = {published},
tppubtype = {article}
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Movies, vacations, and meals are all examples of events composed of a sequence of smaller events. How do we go from our evaluations of each scene in a movie to an evaluation of the sequence as a whole$alpha$ In theory, we should simply average the values of the individual events. In practice, however, we are biased towards sequences where each element tends to be better than the previous, where the last value is large, and we overweight the best (or worst) part of the sequence. To study how general these biases are we examined monkeys' preferences for sequences of rewards in a novel reward repeat task. Monkeys were first given a sequence of rewards and then chose between repeating the sequence or receiving a standard comparator sequence. We found that, like humans, monkeys overweight events that happen later in a sequence, so much so that adding a small reward to the end of a sequence can paradoxically reduce its value. Monkeys were also biased towards sequences with large peak values (the highest value in the sequence), but only following a working memory challenge, suggesting that this preference may be driven by memory limitations. These results demonstrate the cross-species nature of biases in preferences for sequences of outcomes. In addition, monkeys' consistent preference for sequences in which large values occur later challenges the generality of discounting models of intertemporal choice in animals. |
Tommy C Blanchard; Benjamin Y Hayden Monkeys are more patient in a foraging task than in a standard intertemporal choice task Journal Article PLoS ONE, 10 (2), pp. 1–11, 2015. Abstract | Links | BibTeX @article{Blanchard2015,
title = {Monkeys are more patient in a foraging task than in a standard intertemporal choice task},
author = {Tommy C Blanchard and Benjamin Y Hayden},
doi = {10.1371/journal.pone.0117057},
year = {2015},
date = {2015-01-01},
journal = {PLoS ONE},
volume = {10},
number = {2},
pages = {1--11},
abstract = {Studies of animal impulsivity generally find steep subjective devaluation, or discounting, of delayed rewards - often on the order of a 50% reduction in value in a few seconds. Because such steep discounting is highly disfavored in evolutionary models of time preference, we hypothesize that discounting tasks provide a poor measure of animals' true time preferences. One prediction of this hypothesis is that estimates of time preferences based on these tasks will lack external validity, i.e. fail to predict time preferences in other contexts. We examined choices made by four rhesus monkeys in a computerized patch-leaving foraging task interleaved with a standard intertemporal choice task. Monkeys were significantly more patient in the foraging task than in the intertemporal choice task. Patch-leaving behavior was well fit by parameter-free optimal foraging equations but poorly fit by the hyperbolic discount parameter obtained from the intertemporal choice task. Day-to-day variation in time preferences across the two tasks was uncorrelated with each other. These data are consistent with the conjecture that seemingly impulsive behavior in animals is an artifact of their difficulty understanding the structure of intertemporal choice tasks, and support the idea that animals are more efficient rate maximizers in the multi-second range than intertemporal choice tasks would suggest.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Studies of animal impulsivity generally find steep subjective devaluation, or discounting, of delayed rewards - often on the order of a 50% reduction in value in a few seconds. Because such steep discounting is highly disfavored in evolutionary models of time preference, we hypothesize that discounting tasks provide a poor measure of animals' true time preferences. One prediction of this hypothesis is that estimates of time preferences based on these tasks will lack external validity, i.e. fail to predict time preferences in other contexts. We examined choices made by four rhesus monkeys in a computerized patch-leaving foraging task interleaved with a standard intertemporal choice task. Monkeys were significantly more patient in the foraging task than in the intertemporal choice task. Patch-leaving behavior was well fit by parameter-free optimal foraging equations but poorly fit by the hyperbolic discount parameter obtained from the intertemporal choice task. Day-to-day variation in time preferences across the two tasks was uncorrelated with each other. These data are consistent with the conjecture that seemingly impulsive behavior in animals is an artifact of their difficulty understanding the structure of intertemporal choice tasks, and support the idea that animals are more efficient rate maximizers in the multi-second range than intertemporal choice tasks would suggest. |
Tommy C Blanchard; Caleb E Strait; Benjamin Y Hayden Ramping ensemble activity in dorsal anterior cingulate neurons during persistent commitment to a decision Journal Article Journal of Neurophysiology, 114 (4), pp. 2439–2449, 2015. Abstract | Links | BibTeX @article{Blanchard2015a,
title = {Ramping ensemble activity in dorsal anterior cingulate neurons during persistent commitment to a decision},
author = {Tommy C Blanchard and Caleb E Strait and Benjamin Y Hayden},
url = {http://www.physiology.org/doi/10.1152/jn.00711.2015},
doi = {10.1152/jn.00711.2015},
year = {2015},
date = {2015-01-01},
journal = {Journal of Neurophysiology},
volume = {114},
number = {4},
pages = {2439--2449},
abstract = {We frequently need to commit to a choice to achieve our goals; however, the neural processes that keep us motivated in pursuit of delayed goals remain obscure. We examined ensemble responses of neurons in macaque dorsal anterior cingulate cortex (dACC), an area previously implicated in self-control and persistence, in a task that requires commitment to a choice to obtain a reward. After reward receipt, dACC neurons signaled reward amount with characteristic ensemble firing rate patterns; during the delay in anticipation of the reward, ensemble activity smoothly and gradually came to resemble the postreward pattern. On the subset of risky trials, in which a reward was anticipated with 50% certainty, ramping ensemble activity evolved to the pattern associated with the anticipated reward (and not with the anticipated loss) and then, on loss trials, took on an inverted form anticorrelated with the form associated with a win. These findings enrich our knowledge of reward processing in dACC and may have broader implications for our understanding of persistence and self-control.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
We frequently need to commit to a choice to achieve our goals; however, the neural processes that keep us motivated in pursuit of delayed goals remain obscure. We examined ensemble responses of neurons in macaque dorsal anterior cingulate cortex (dACC), an area previously implicated in self-control and persistence, in a task that requires commitment to a choice to obtain a reward. After reward receipt, dACC neurons signaled reward amount with characteristic ensemble firing rate patterns; during the delay in anticipation of the reward, ensemble activity smoothly and gradually came to resemble the postreward pattern. On the subset of risky trials, in which a reward was anticipated with 50% certainty, ramping ensemble activity evolved to the pattern associated with the anticipated reward (and not with the anticipated loss) and then, on loss trials, took on an inverted form anticorrelated with the form associated with a win. These findings enrich our knowledge of reward processing in dACC and may have broader implications for our understanding of persistence and self-control. |
Chadwick B Boulay; Florian Pieper; Matthew Leavitt; Julio Martinez-Trujillo; Adam J Sachs Single-trial decoding of intended eye movement goals from lateral prefrontal cortex neural ensembles Journal Article Journal of Neurophysiology, 115 (1), pp. 486–499, 2016. Abstract | Links | BibTeX @article{Boulay2016,
title = {Single-trial decoding of intended eye movement goals from lateral prefrontal cortex neural ensembles},
author = {Chadwick B Boulay and Florian Pieper and Matthew Leavitt and Julio Martinez-Trujillo and Adam J Sachs},
url = {http://jn.physiology.org/lookup/doi/10.1152/jn.00788.2015},
doi = {10.1152/jn.00788.2015},
year = {2016},
date = {2016-01-01},
journal = {Journal of Neurophysiology},
volume = {115},
number = {1},
pages = {486--499},
abstract = {Neurons in the lateral prefrontal cortex (LPFC) encode sensory and cognitive signals, as well as commands for goal-directed actions. Therefore, the LPFC might be a good signal source for a goal-selection brain-computer interface (BCI) that decodes the intended goal of a motor action previous to its execution. As a first step in the development of a goal-selection BCI, we set out to determine if we could decode simple behavioral intentions to direct gaze to eight different locations in space from single-trial LPFC neural activity. We recorded neuronal spiking activity from microelectrode arrays implanted in area 8A of the LPFC of two adult macaques while they made visually guided saccades to one of eight targets in a center-out task. Neuronal activity encoded target location immediately after target presentation, during a delay epoch, during the execution of the saccade, and every combination thereof. Many (40%) of the neurons that encoded target location during multiple epochs preferred different locations during different epochs. Despite heterogeneous and dynamic responses, the neuronal feature set that best predicted target location was the averaged firing rates from the entire trial and it was best classified using linear discriminant analysis (63.6$backslash$textendash96.9% in 12 sessions, mean 80.3%; information transfer rate: 21$backslash$textendash59, mean 32.8 bits/min). Our results demonstrate that it is possible to decode intended saccade target location from single-trial LPFC activity and suggest that the LPFC is a suitable signal source for a goal-selection cognitive BCI.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Neurons in the lateral prefrontal cortex (LPFC) encode sensory and cognitive signals, as well as commands for goal-directed actions. Therefore, the LPFC might be a good signal source for a goal-selection brain-computer interface (BCI) that decodes the intended goal of a motor action previous to its execution. As a first step in the development of a goal-selection BCI, we set out to determine if we could decode simple behavioral intentions to direct gaze to eight different locations in space from single-trial LPFC neural activity. We recorded neuronal spiking activity from microelectrode arrays implanted in area 8A of the LPFC of two adult macaques while they made visually guided saccades to one of eight targets in a center-out task. Neuronal activity encoded target location immediately after target presentation, during a delay epoch, during the execution of the saccade, and every combination thereof. Many (40%) of the neurons that encoded target location during multiple epochs preferred different locations during different epochs. Despite heterogeneous and dynamic responses, the neuronal feature set that best predicted target location was the averaged firing rates from the entire trial and it was best classified using linear discriminant analysis (63.6$backslash$textendash96.9% in 12 sessions, mean 80.3%; information transfer rate: 21$backslash$textendash59, mean 32.8 bits/min). Our results demonstrate that it is possible to decode intended saccade target location from single-trial LPFC activity and suggest that the LPFC is a suitable signal source for a goal-selection cognitive BCI. |
Scott L Brincat; Earl K Miller Frequency-specific hippocampal-prefrontal interactions during associative learning Journal Article Nature Neuroscience, 18 (4), pp. 576–581, 2015. Abstract | Links | BibTeX @article{Brincat2015,
title = {Frequency-specific hippocampal-prefrontal interactions during associative learning},
author = {Scott L Brincat and Earl K Miller},
url = {http://dx.doi.org/10.1038/nn.3954},
doi = {10.1038/nn.3954},
year = {2015},
date = {2015-01-01},
journal = {Nature Neuroscience},
volume = {18},
number = {4},
pages = {576--581},
publisher = {Nature Publishing Group},
abstract = {Much of our knowledge of the world depends on learning associations (for example, face-name), for which the hippocampus (HPC) and prefrontal cortex (PFC) are critical. HPC-PFC interactions have rarely been studied in monkeys, whose cognitive and mnemonic abilities are akin to those of humans. We found functional differences and frequency-specific interactions between HPC and PFC of monkeys learning object pair associations, an animal model of human explicit memory. PFC spiking activity reflected learning in parallel with behavioral performance, whereas HPC neurons reflected feedback about whether trial-and-error guesses were correct or incorrect. Theta-band HPC-PFC synchrony was stronger after errors, was driven primarily by PFC to HPC directional influences and decreased with learning. In contrast, alpha/beta-band synchrony was stronger after correct trials, was driven more by HPC and increased with learning. Rapid object associative learning may occur in PFC, whereas HPC may guide neocortical plasticity by signaling success or failure via oscillatory synchrony in different frequency bands.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Much of our knowledge of the world depends on learning associations (for example, face-name), for which the hippocampus (HPC) and prefrontal cortex (PFC) are critical. HPC-PFC interactions have rarely been studied in monkeys, whose cognitive and mnemonic abilities are akin to those of humans. We found functional differences and frequency-specific interactions between HPC and PFC of monkeys learning object pair associations, an animal model of human explicit memory. PFC spiking activity reflected learning in parallel with behavioral performance, whereas HPC neurons reflected feedback about whether trial-and-error guesses were correct or incorrect. Theta-band HPC-PFC synchrony was stronger after errors, was driven primarily by PFC to HPC directional influences and decreased with learning. In contrast, alpha/beta-band synchrony was stronger after correct trials, was driven more by HPC and increased with learning. Rapid object associative learning may occur in PFC, whereas HPC may guide neocortical plasticity by signaling success or failure via oscillatory synchrony in different frequency bands. |
Scott L Brincat; Earl K Miller Prefrontal cortex networks shift from external to internal modes during learning Journal Article Journal of Neuroscience, 36 (37), pp. 9739–9754, 2016. Abstract | Links | BibTeX @article{Brincat2016,
title = {Prefrontal cortex networks shift from external to internal modes during learning},
author = {Scott L Brincat and Earl K Miller},
url = {http://www.jneurosci.org/cgi/doi/10.1523/JNEUROSCI.0274-16.2016},
doi = {10.1523/JNEUROSCI.0274-16.2016},
year = {2016},
date = {2016-01-01},
journal = {Journal of Neuroscience},
volume = {36},
number = {37},
pages = {9739--9754},
abstract = {As we learn about items in our environment, their neural representations become increasingly enriched with our acquired knowledge. But there is little understanding of how network dynamics and neural processing related to external information changes as it becomes laden with "internal" memories. We sampled spiking and local field potential activity simultaneously from multiple sites in the lateral prefrontal cortex (PFC) and the hippocampus (HPC)-regions critical for sensory associations-of monkeys performing an object paired-associate learning task. We found that in the PFC, evoked potentials to, and neural information about, external sensory stimulation decreased while induced beta-band (∼11-27 Hz) oscillatory power and synchrony associated with "top-down" or internal processing increased. By contrast, the HPC showed little evidence of learning-related changes in either spiking activity or network dynamics. The results suggest that during associative learning, PFC networks shift their resources from external to internal processing.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
As we learn about items in our environment, their neural representations become increasingly enriched with our acquired knowledge. But there is little understanding of how network dynamics and neural processing related to external information changes as it becomes laden with "internal" memories. We sampled spiking and local field potential activity simultaneously from multiple sites in the lateral prefrontal cortex (PFC) and the hippocampus (HPC)-regions critical for sensory associations-of monkeys performing an object paired-associate learning task. We found that in the PFC, evoked potentials to, and neural information about, external sensory stimulation decreased while induced beta-band (∼11-27 Hz) oscillatory power and synchrony associated with "top-down" or internal processing increased. By contrast, the HPC showed little evidence of learning-related changes in either spiking activity or network dynamics. The results suggest that during associative learning, PFC networks shift their resources from external to internal processing. |
Kelly R Bullock; Florian Pieper; Adam J Sachs; Julio C Martinez-Trujillo Visual and presaccadic activity in area 8Ar of the macaque monkey lateral prefrontal cortex Journal Article Journal of Neurophysiology, 118 (1), pp. 15–28, 2017. Abstract | Links | BibTeX @article{Bullock2017,
title = {Visual and presaccadic activity in area 8Ar of the macaque monkey lateral prefrontal cortex},
author = {Kelly R Bullock and Florian Pieper and Adam J Sachs and Julio C Martinez-Trujillo},
url = {http://jn.physiology.org/lookup/doi/10.1152/jn.00278.2016},
doi = {10.1152/jn.00278.2016},
year = {2017},
date = {2017-01-01},
journal = {Journal of Neurophysiology},
volume = {118},
number = {1},
pages = {15--28},
abstract = {Common trends observed in many visual and oculomotor-related cortical areas include retinotopically organized receptive and movement fields exhibiting a Gaussian shape and increasing size with eccentricity. These trends are demonstrated in the frontal eye fields (FEF), many visual areas, and the superior colliculus (SC), but have not been thoroughly characterized in prearcuate area 8Ar of the prefrontal cortex. This is important since area 8Ar, located anterior to the FEF, is more cytoarchitectonically similar to prefrontal areas than premotor areas. Here we recorded the responses of 166 neurons in area 8Ar of two male macaques while the animals made visually guided saccades to a peripheral sine-wave grating stimulus positioned at one of 40 possible locations (8 angles along 5 eccentricities). To characterize the neurons' receptive and movement fields, we fit a bivariate Gaussian model to the baseline-subtracted average firing rate during stimulus presentation (early and late visual epoch) and prior to saccade onset (presaccadic epoch). 121/166 neurons showed spatially selective visual and presaccadic responses. Of the visually selective neurons, 76% preferred the contralateral visual hemifield, whereas 24% preferred the ipsilateral hemifield. The angular width of visual and movement-related fields scaled positively with increasing eccentricity. Moreover, responses of neurons with visual receptive fields were modulated by target contrast exhibiting sigmoid tuning curves that resemble those of visual neurons in upstream areas such as MT and V4. Finally, we found that neurons with receptive fields at similar spatial locations were clustered within the area; however, this organization did not appear retinotopic.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Common trends observed in many visual and oculomotor-related cortical areas include retinotopically organized receptive and movement fields exhibiting a Gaussian shape and increasing size with eccentricity. These trends are demonstrated in the frontal eye fields (FEF), many visual areas, and the superior colliculus (SC), but have not been thoroughly characterized in prearcuate area 8Ar of the prefrontal cortex. This is important since area 8Ar, located anterior to the FEF, is more cytoarchitectonically similar to prefrontal areas than premotor areas. Here we recorded the responses of 166 neurons in area 8Ar of two male macaques while the animals made visually guided saccades to a peripheral sine-wave grating stimulus positioned at one of 40 possible locations (8 angles along 5 eccentricities). To characterize the neurons' receptive and movement fields, we fit a bivariate Gaussian model to the baseline-subtracted average firing rate during stimulus presentation (early and late visual epoch) and prior to saccade onset (presaccadic epoch). 121/166 neurons showed spatially selective visual and presaccadic responses. Of the visually selective neurons, 76% preferred the contralateral visual hemifield, whereas 24% preferred the ipsilateral hemifield. The angular width of visual and movement-related fields scaled positively with increasing eccentricity. Moreover, responses of neurons with visual receptive fields were modulated by target contrast exhibiting sigmoid tuning curves that resemble those of visual neurons in upstream areas such as MT and V4. Finally, we found that neurons with receptive fields at similar spatial locations were clustered within the area; however, this organization did not appear retinotopic. |
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 Neuron, 76 (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},
url = {http://dx.doi.org/10.1016/j.neuron.2012.09.029},
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}
}
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. |
Brittany N Bushnell; Philip J Harding; Yoshito Kosai; Wyeth Bair; Anitha Pasupathy Equiluminance cells in visual cortical area V4 Journal Article Journal of Neuroscience, 31 (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},
url = {http://www.jneurosci.org/cgi/doi/10.1523/JNEUROSCI.1890-11.2011},
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}
}
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. |
Brittany N Bushnell; Philip J Harding; Yoshito Kosai; Anitha Pasupathy Partial occlusion modulates contour-based shape encoding in primate area V4 Journal Article Journal of Neuroscience, 31 (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},
url = {http://www.jneurosci.org/cgi/doi/10.1523/JNEUROSCI.4766-10.2011},
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}
}
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. |
Brittany N Bushnell; Anitha Pasupathy Shape encoding consistency across colors in primate V4 Journal Article Journal of Neurophysiology, 108 (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},
url = {http://jn.physiology.org/cgi/doi/10.1152/jn.01063.2011},
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}
}
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. |
Charles F Cadieu; Ha Hong; Daniel L K Yamins; Nicolas Pinto; Diego Ardila; Ethan A Solomon; Najib J Majaj; James J DiCarlo Deep neural networks rival the representation of primate IT cortex for core visual object recognition Journal Article PLoS Computational Biology, 10 (12), pp. 1–18, 2014. Abstract | Links | BibTeX @article{Cadieu2014,
title = {Deep neural networks rival the representation of primate IT cortex for core visual object recognition},
author = {Charles F Cadieu and Ha Hong and Daniel L K Yamins and Nicolas Pinto and Diego Ardila and Ethan A Solomon and Najib J Majaj and James J DiCarlo},
doi = {10.1016/j.apergo.2010.02.001},
year = {2014},
date = {2014-01-01},
journal = {PLoS Computational Biology},
volume = {10},
number = {12},
pages = {1--18},
abstract = {The primate visual system achieves remarkable visual object recognition performance even in brief presentations, and under changes to object exemplar, geometric transformations, and background variation (a.k.a. core visual object recognition). This remarkable performance is mediated by the representation formed in inferior temporal (IT) cortex. In parallel, recent advances in machine learning have led to ever higher performing models of object recognition using artificial deep neural networks (DNNs). It remains unclear, however, whether the representational performance of DNNs rivals that of the brain. To accurately produce such a comparison, a major difficulty has been a unifying metric that accounts for experimental limitations, such as the amount of noise, the number of neural recording sites, and the number of trials, and computational limitations, such as the complexity of the decoding classifier and the number of classifier training examples. In this work, we perform a direct comparison that corrects for these experimental limitations and computational considerations. As part of our methodology, we propose an extension of ‘‘kernel analysis'' that measures the generalization accuracy as a function of representational complexity. Our evaluations show that, unlike previous bio-inspired models, the latest DNNs rival the representational performance of IT cortex on this visual object recognition task. Furthermore, we show that models that perform well on measures of representational performance also perform well on measures of representational similarity to IT, and on measures of predicting individual IT multi-unit responses. Whether these DNNs rely on computational mechanisms similar to the primate visual system is yet to be determined, but, unlike all previous bio- inspired models, that possibility cannot be ruled out merely on representational performance grounds.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
The primate visual system achieves remarkable visual object recognition performance even in brief presentations, and under changes to object exemplar, geometric transformations, and background variation (a.k.a. core visual object recognition). This remarkable performance is mediated by the representation formed in inferior temporal (IT) cortex. In parallel, recent advances in machine learning have led to ever higher performing models of object recognition using artificial deep neural networks (DNNs). It remains unclear, however, whether the representational performance of DNNs rivals that of the brain. To accurately produce such a comparison, a major difficulty has been a unifying metric that accounts for experimental limitations, such as the amount of noise, the number of neural recording sites, and the number of trials, and computational limitations, such as the complexity of the decoding classifier and the number of classifier training examples. In this work, we perform a direct comparison that corrects for these experimental limitations and computational considerations. As part of our methodology, we propose an extension of ‘‘kernel analysis'' that measures the generalization accuracy as a function of representational complexity. Our evaluations show that, unlike previous bio-inspired models, the latest DNNs rival the representational performance of IT cortex on this visual object recognition task. Furthermore, we show that models that perform well on measures of representational performance also perform well on measures of representational similarity to IT, and on measures of predicting individual IT multi-unit responses. Whether these DNNs rely on computational mechanisms similar to the primate visual system is yet to be determined, but, unlike all previous bio- inspired models, that possibility cannot be ruled out merely on representational performance grounds. |
X Cai; Camillo Padoa-Schioppa Neuronal encoding of subjective value in dorsal and ventral anterior cingulate cortex Journal Article Journal of Neuroscience, 32 (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},
url = {http://www.jneurosci.org/cgi/doi/10.1523/JNEUROSCI.3864-11.2012},
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}
}
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. |
Xinying Cai; Camillo Padoa-Schioppa Contributions of orbitofrontal and lateral prefrontal cortices to economic choice and the good-to-action transformation Journal Article Neuron, 81 (5), pp. 1140–1151, 2014. Abstract | Links | BibTeX @article{Cai2014,
title = {Contributions of orbitofrontal and lateral prefrontal cortices to economic choice and the good-to-action transformation},
author = {Xinying Cai and Camillo Padoa-Schioppa},
url = {http://dx.doi.org/10.1016/j.neuron.2014.01.008},
doi = {10.1016/j.neuron.2014.01.008},
year = {2014},
date = {2014-01-01},
journal = {Neuron},
volume = {81},
number = {5},
pages = {1140--1151},
publisher = {Elsevier Inc.},
abstract = {Previous work indicates that economic decisions can be made independently of the visuomotor contingencies of the choice task (space of goods). However, the neuronal mechanisms through which the choice outcome (the chosen good) is transformed into a suitable action plan remain poorly understood. Here we show that neurons in lateral prefrontal cortex reflect the early stages of this good-to-action transformation. Monkeys chose between different juices. The experimental design dissociated in space and time the presentation of the offers and the saccade targets associated with them. We recorded from the orbital, ventrolateral, and dorsolateral prefrontal cortices (OFC, LPFCv, and LPFCd, respectively). Prior to target presentation, neurons in both LPFCv and LPFCd encoded the choice outcome in goods space. After target presentation, they gradually came to encode the location of the targets and the upcoming action plan. Consistent with the anatomical connectivity, all spatial and action-related signals emerged in LPFCv before LPFCd.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Previous work indicates that economic decisions can be made independently of the visuomotor contingencies of the choice task (space of goods). However, the neuronal mechanisms through which the choice outcome (the chosen good) is transformed into a suitable action plan remain poorly understood. Here we show that neurons in lateral prefrontal cortex reflect the early stages of this good-to-action transformation. Monkeys chose between different juices. The experimental design dissociated in space and time the presentation of the offers and the saccade targets associated with them. We recorded from the orbital, ventrolateral, and dorsolateral prefrontal cortices (OFC, LPFCv, and LPFCd, respectively). Prior to target presentation, neurons in both LPFCv and LPFCd encoded the choice outcome in goods space. After target presentation, they gradually came to encode the location of the targets and the upcoming action plan. Consistent with the anatomical connectivity, all spatial and action-related signals emerged in LPFCv before LPFCd. |
Valeria C Caruso; Daniel S Pages; Marc A Sommer; Jennifer M Groh Similar prevalence and magnitude of auditory-evoked and visually evoked activity in the frontal eye fields: Implications for multisensory motor control Journal Article Journal of Neurophysiology, 115 (6), pp. 3162–3173, 2016. Abstract | Links | BibTeX @article{Caruso2016,
title = {Similar prevalence and magnitude of auditory-evoked and visually evoked activity in the frontal eye fields: Implications for multisensory motor control},
author = {Valeria C Caruso and Daniel S Pages and Marc A Sommer and Jennifer M Groh},
url = {http://jn.physiology.org/lookup/doi/10.1152/jn.00935.2015},
doi = {10.1152/jn.00935.2015},
year = {2016},
date = {2016-01-01},
journal = {Journal of Neurophysiology},
volume = {115},
number = {6},
pages = {3162--3173},
abstract = {Saccadic eye movements can be elic- ited by more than one type of sensory stimulus. This implies substantial transformations of signals originating in different sense organs as they reach a common motor output pathway. In this study, we compared the prevalence and magnitude of auditory- and visually evoked activity in a structure implicated in oculomotor processing, the primate frontal eye fields (FEF). We recorded from 324 single neurons while 2 monkeys performed delayed saccades to visual or auditory targets. We found that 64% of FEF neurons were active on presenta- tion of auditory targets and 87% were active during auditory-guided saccades, compared with 75 and 84% for visual targets and saccades. As saccade onset approached, the average level of population activity in the FEF became indistinguishable on visual and auditory trials. FEF activity was better correlated with the movement vector than with the target location for both modalities. In summary, the large proportion of auditory-responsive neurons in the FEF, the similarity between visual and auditory activity levels at the time of the saccade, and the strong correlation between the activity and the saccade vector suggest that auditory signals undergo tailoring to match roughly the strength of visual signals present in the FEF, facilitating accessing of a common motor output pathway.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Saccadic eye movements can be elic- ited by more than one type of sensory stimulus. This implies substantial transformations of signals originating in different sense organs as they reach a common motor output pathway. In this study, we compared the prevalence and magnitude of auditory- and visually evoked activity in a structure implicated in oculomotor processing, the primate frontal eye fields (FEF). We recorded from 324 single neurons while 2 monkeys performed delayed saccades to visual or auditory targets. We found that 64% of FEF neurons were active on presenta- tion of auditory targets and 87% were active during auditory-guided saccades, compared with 75 and 84% for visual targets and saccades. As saccade onset approached, the average level of population activity in the FEF became indistinguishable on visual and auditory trials. FEF activity was better correlated with the movement vector than with the target location for both modalities. In summary, the large proportion of auditory-responsive neurons in the FEF, the similarity between visual and auditory activity levels at the time of the saccade, and the strong correlation between the activity and the saccade vector suggest that auditory signals undergo tailoring to match roughly the strength of visual signals present in the FEF, facilitating accessing of a common motor output pathway. |
Aaron L Cecala; Ivan Smalianchuk; Sanjeev B Khanna; Matthew A Smith; Neeraj J Gandhi Context cue-dependent saccadic adaptation in rhesus macaques cannot be elicited using color Journal Article Journal of Neurophysiology, 114 (1), pp. 570–584, 2015. Abstract | Links | BibTeX @article{Cecala2015,
title = {Context cue-dependent saccadic adaptation in rhesus macaques cannot be elicited using color},
author = {Aaron L Cecala and Ivan Smalianchuk and Sanjeev B Khanna and Matthew A Smith and Neeraj J Gandhi},
url = {http://www.physiology.org/doi/10.1152/jn.00666.2014},
doi = {10.1152/jn.00666.2014},
year = {2015},
date = {2015-01-01},
journal = {Journal of Neurophysiology},
volume = {114},
number = {1},
pages = {570--584},
abstract = {When the head does not move, rapid movements of the eyes called saccades are used to redirect the line of sight. Saccades are defined by a series of metrical and kinematic (evolution of a movement as a function of time) relationships. For example, the amplitude of a saccade made from one visual target to another is roughly 90% of the distance between the initial fixation point (T0) and the peripheral target (T1). However, this stereotypical relationship between saccade amplitude and initial retinal error (T1-T0) may be altered, either increased or decreased, by surreptitiously displacing a visual target during an ongoing saccade. This form of motor learning (called saccadic adaptation) has been described in both humans and monkeys. Recent experiments in humans and monkeys have suggested that internal (proprioceptive) and external (target shape, color, and/or motion) cues may be used to produce context-dependent adaptation. We tested the hypothesis that an external contextual cue (target color) could be used to evoke differential gain (actual saccade/initial retinal error) states in rhesus monkeys. We did not observe differential gain states correlated with target color regardless of whether targets were displaced along the same vector as the primary saccade or perpendicular to it. Furthermore, this observation held true regardless of whether adaptation trials using various colors and intrasaccade target displacements were randomly intermixed or presented in short or long blocks of trials. These results are consistent with hypotheses that state that color cannot be used as a contextual cue and are interpreted in light of previous studies of saccadic adaptation in both humans and monkeys.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
When the head does not move, rapid movements of the eyes called saccades are used to redirect the line of sight. Saccades are defined by a series of metrical and kinematic (evolution of a movement as a function of time) relationships. For example, the amplitude of a saccade made from one visual target to another is roughly 90% of the distance between the initial fixation point (T0) and the peripheral target (T1). However, this stereotypical relationship between saccade amplitude and initial retinal error (T1-T0) may be altered, either increased or decreased, by surreptitiously displacing a visual target during an ongoing saccade. This form of motor learning (called saccadic adaptation) has been described in both humans and monkeys. Recent experiments in humans and monkeys have suggested that internal (proprioceptive) and external (target shape, color, and/or motion) cues may be used to produce context-dependent adaptation. We tested the hypothesis that an external contextual cue (target color) could be used to evoke differential gain (actual saccade/initial retinal error) states in rhesus monkeys. We did not observe differential gain states correlated with target color regardless of whether targets were displaced along the same vector as the primary saccade or perpendicular to it. Furthermore, this observation held true regardless of whether adaptation trials using various colors and intrasaccade target displacements were randomly intermixed or presented in short or long blocks of trials. These results are consistent with hypotheses that state that color cannot be used as a contextual cue and are interpreted in light of previous studies of saccadic adaptation in both humans and monkeys. |
Jason L Chan; Michael J Koval; Thilo Womelsdorf; Stephen G Lomber; Stefan Everling Dorsolateral prefrontal cortex deactivation in monkeys reduces preparatory beta and gamma power in the superior colliculus Journal Article Cerebral Cortex, 25 (12), pp. 4704–4714, 2015. Abstract | Links | BibTeX @article{Chan2015,
title = {Dorsolateral prefrontal cortex deactivation in monkeys reduces preparatory beta and gamma power in the superior colliculus},
author = {Jason L Chan and Michael J Koval and Thilo Womelsdorf and Stephen G Lomber and Stefan Everling},
doi = {10.1093/cercor/bhu154},
year = {2015},
date = {2015-01-01},
journal = {Cerebral Cortex},
volume = {25},
number = {12},
pages = {4704--4714},
abstract = {Cognitive control requires the selection and maintenance of task-relevant stimulus-response associations, or rules. The dorsolateral prefrontal cortex (DLPFC) has been implicated by lesion, functional imaging, and neurophysiological studies to be involved in encoding rules, but the mechanisms by which it modulates other brain areas are poorly understood. Here, the functional relationship of the DLPFC with the superior colliculus (SC) was investigated by bilaterally deactivating the DLPFC while recording local field potentials (LFPs) in the SC in monkeys performing an interleaved pro- and antisaccade task. Event-related LFPs showed differences between pro- and antisaccades and responded prominently to stimulus presentation. LFP power after stimulus onset was higher for correct saccades than erroneous saccades. Deactivation of the DLPFC did not affect stimulus onset related LFP activity, but reduced high beta (20-30 Hz) and high gamma (60-150 Hz) power during the preparatory period for both pro- and antisaccades. Spike rate during the preparatory period was positively correlated with gamma power and this relationship was attenuated by DLPFC deactivation. These results suggest that top-down control of the SC by the DLPFC may be mediated by beta oscillations.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Cognitive control requires the selection and maintenance of task-relevant stimulus-response associations, or rules. The dorsolateral prefrontal cortex (DLPFC) has been implicated by lesion, functional imaging, and neurophysiological studies to be involved in encoding rules, but the mechanisms by which it modulates other brain areas are poorly understood. Here, the functional relationship of the DLPFC with the superior colliculus (SC) was investigated by bilaterally deactivating the DLPFC while recording local field potentials (LFPs) in the SC in monkeys performing an interleaved pro- and antisaccade task. Event-related LFPs showed differences between pro- and antisaccades and responded prominently to stimulus presentation. LFP power after stimulus onset was higher for correct saccades than erroneous saccades. Deactivation of the DLPFC did not affect stimulus onset related LFP activity, but reduced high beta (20-30 Hz) and high gamma (60-150 Hz) power during the preparatory period for both pro- and antisaccades. Spike rate during the preparatory period was positively correlated with gamma power and this relationship was attenuated by DLPFC deactivation. These results suggest that top-down control of the SC by the DLPFC may be mediated by beta oscillations. |
Jason Lloyd Chan; Michael J Koval; Kevin Johnston; Stefan Everling Neural correlates for task switching in the macaque superior colliculus Journal Article Journal of Neurophysiology, 118 , pp. 2156–2170, 2017. Abstract | Links | BibTeX @article{Chan2017,
title = {Neural correlates for task switching in the macaque superior colliculus},
author = {Jason Lloyd Chan and Michael J Koval and Kevin Johnston and Stefan Everling},
url = {http://jn.physiology.org/lookup/doi/10.1152/jn.00139.2017},
doi = {10.1152/jn.00139.2017},
year = {2017},
date = {2017-01-01},
journal = {Journal of Neurophysiology},
volume = {118},
pages = {2156--2170},
abstract = {Successful task switching requires a network of brain areas to select, maintain, implement, and execute the appropriate task. Although frontoparietal brain areas are thought to play a critical role in task switching by selecting and encoding task rules and exerting top-down control, how brain areas closer to the execution of tasks participate in task switching is unclear. The superior colliculus (SC) integrates information from various brain areas to generate saccades and is likely influenced by task switching. Here, we investigated switch costs in nonhuman primates and their neural correlates in the activity of SC saccade-related neurons in monkeys performing cued, randomly interleaved pro- and anti-saccade trials. We predicted that behavioral switch costs would be associated with differential modulations of SC activity in trials on which the task was switched vs. repeated, with activity on the current trial resembling that associated with the task set of the previous trial when a switch occurred. We observed both error rate and reaction time switch costs and changes in the discharge rate and timing of activity in SC neurons between switch and repeat trials. These changes were present later in the task only after fixation on the cue stimuli but before saccade onset. These results further establish switch costs in macaque monkeys and suggest that SC activity is modulated by task-switching processes in a manner inconsistent with the concept of task set inertia.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Successful task switching requires a network of brain areas to select, maintain, implement, and execute the appropriate task. Although frontoparietal brain areas are thought to play a critical role in task switching by selecting and encoding task rules and exerting top-down control, how brain areas closer to the execution of tasks participate in task switching is unclear. The superior colliculus (SC) integrates information from various brain areas to generate saccades and is likely influenced by task switching. Here, we investigated switch costs in nonhuman primates and their neural correlates in the activity of SC saccade-related neurons in monkeys performing cued, randomly interleaved pro- and anti-saccade trials. We predicted that behavioral switch costs would be associated with differential modulations of SC activity in trials on which the task was switched vs. repeated, with activity on the current trial resembling that associated with the task set of the previous trial when a switch occurred. We observed both error rate and reaction time switch costs and changes in the discharge rate and timing of activity in SC neurons between switch and repeat trials. These changes were present later in the task only after fixation on the cue stimuli but before saccade onset. These results further establish switch costs in macaque monkeys and suggest that SC activity is modulated by task-switching processes in a manner inconsistent with the concept of task set inertia. |
Steve W C Chang; Amy A Winecoff; Michael L Platt Vicarious reinforcement in rhesus macaques (Macaca mulatta) Journal Article Frontiers in Neuroscience, 5 , pp. 1–10, 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 = {1--10},
publisher = {10},
address = {doi},
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}
}
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. |
Steve W C Chang; Joseph W Barter; Becket R Ebitz; Karli K Watson; Michael L Platt Inhaled oxytocin amplifies both vicarious reinforcement and self reinforcement in rhesus macaques (Macaca mulatta) Journal Article Proceedings of the National Academy of Sciences, 109 (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 Becket R Ebitz and Karli K Watson and Michael L Platt},
url = {http://www.pnas.org/cgi/doi/10.1073/pnas.1114621109},
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}
}
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. |
Steve W C Chang; Jean François Gariépy; Michael L Platt Neuronal reference frames for social decisions in primate frontal cortex Journal Article Nature Neuroscience, 16 (2), pp. 243–250, 2013. Abstract | Links | BibTeX @article{Chang2013,
title = {Neuronal reference frames for social decisions in primate frontal cortex},
author = {Steve W C Chang and Jean Fran{ç}ois Gariépy and Michael L Platt},
doi = {10.1007/s10914-012-9194-1},
year = {2013},
date = {2013-01-01},
journal = {Nature Neuroscience},
volume = {16},
number = {2},
pages = {243--250},
publisher = {Nature Neuroscience 16},
abstract = {Social decisions are crucial for the success of individuals and the groups that they comprise. Group members respond vicariously to benefits obtained by others, and impairments in this capacity contribute to neuropsychiatric disorders such as autism and sociopathy. We examined the manner in which neurons in three frontal cortical areas encoded the outcomes of social decisions as monkeys performed a reward-allocation task. Neurons in the orbitofrontal cortex (OFC) predominantly encoded rewards that were delivered to oneself. Neurons in the anterior cingulate gyrus (ACCg) encoded reward allocations to the other monkey, to oneself or to both. Neurons in the anterior cingulate sulcus (ACCs) signaled reward allocations to the other monkey or to no one. In this network of received (OFC) and foregone (ACCs) reward signaling, ACCg emerged as an important nexus for the computation of shared experience and social reward. Individual and species-specific variations in social decision-making might result from the relative activation and influence of these areas.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Social decisions are crucial for the success of individuals and the groups that they comprise. Group members respond vicariously to benefits obtained by others, and impairments in this capacity contribute to neuropsychiatric disorders such as autism and sociopathy. We examined the manner in which neurons in three frontal cortical areas encoded the outcomes of social decisions as monkeys performed a reward-allocation task. Neurons in the orbitofrontal cortex (OFC) predominantly encoded rewards that were delivered to oneself. Neurons in the anterior cingulate gyrus (ACCg) encoded reward allocations to the other monkey, to oneself or to both. Neurons in the anterior cingulate sulcus (ACCs) signaled reward allocations to the other monkey or to no one. In this network of received (OFC) and foregone (ACCs) reward signaling, ACCg emerged as an important nexus for the computation of shared experience and social reward. Individual and species-specific variations in social decision-making might result from the relative activation and influence of these areas. |
Steve W C Chang; Nicholas A Fagan; Koji Toda; Amanda V Utevsky; John M Pearson; Michael L Platt Neural mechanisms of social decision-making in the primate amygdala Journal Article Proceedings of the National Academy of Sciences, 112 (52), pp. 16012–16017, 2015. Abstract | Links | BibTeX @article{Chang2015,
title = {Neural mechanisms of social decision-making in the primate amygdala},
author = {Steve W C Chang and Nicholas A Fagan and Koji Toda and Amanda V Utevsky and John M Pearson and Michael L Platt},
url = {http://www.pnas.org/lookup/doi/10.1073/pnas.1514761112},
doi = {10.1073/pnas.1514761112},
year = {2015},
date = {2015-01-01},
journal = {Proceedings of the National Academy of Sciences},
volume = {112},
number = {52},
pages = {16012--16017},
abstract = {SignificanceMaking social decisions requires evaluation of benefits and costs to self and others. Long associated with emotion and vigilance, neurons in primate amygdala also signal reward and punishment as well as information about the faces and eyes of others. Here we show that neurons in the basolateral amygdala signal the value of rewards for self and others when monkeys make social decisions. These value-mirroring neurons reflected monkeys tendency to make prosocial decisions on a momentary as well as long-term basis. We also found that delivering the social peptide oxytocin into basolateral amygdala enhances both prosocial tendencies and attention to the recipients of prosocial decisions. Our findings endorse the amygdala as a critical neural nexus regulating social decisions. Social decisions require evaluation of costs and benefits to oneself and others. Long associated with emotion and vigilance, the amygdala has recently been implicated in both decision-making and social behavior. The amygdala signals reward and punishment, as well as facial expressions and the gaze of others. Amygdala damage impairs social interactions, and the social neuropeptide oxytocin (OT) influences human social decisions, in part, by altering amygdala function. Here we show in monkeys playing a modified dictator game, in which one individual can donate or withhold rewards from another, that basolateral amygdala (BLA) neurons signaled social preferences both across trials and across days. BLA neurons mirrored the value of rewards delivered to self and others when monkeys were free to choose but not when the computer made choices for them. We also found that focal infusion of OT unilaterally into BLA weakly but significantly increased both the frequency of prosocial decisions and attention to recipients for context-specific prosocial decisions, endorsing the hypothesis that OT regulates social behavior, in part, via amygdala neuromodulation. Our findings demonstrate both neurophysiological and neuroendocrinological connections between primate amygdala and social decisions.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
SignificanceMaking social decisions requires evaluation of benefits and costs to self and others. Long associated with emotion and vigilance, neurons in primate amygdala also signal reward and punishment as well as information about the faces and eyes of others. Here we show that neurons in the basolateral amygdala signal the value of rewards for self and others when monkeys make social decisions. These value-mirroring neurons reflected monkeys tendency to make prosocial decisions on a momentary as well as long-term basis. We also found that delivering the social peptide oxytocin into basolateral amygdala enhances both prosocial tendencies and attention to the recipients of prosocial decisions. Our findings endorse the amygdala as a critical neural nexus regulating social decisions. Social decisions require evaluation of costs and benefits to oneself and others. Long associated with emotion and vigilance, the amygdala has recently been implicated in both decision-making and social behavior. The amygdala signals reward and punishment, as well as facial expressions and the gaze of others. Amygdala damage impairs social interactions, and the social neuropeptide oxytocin (OT) influences human social decisions, in part, by altering amygdala function. Here we show in monkeys playing a modified dictator game, in which one individual can donate or withhold rewards from another, that basolateral amygdala (BLA) neurons signaled social preferences both across trials and across days. BLA neurons mirrored the value of rewards delivered to self and others when monkeys were free to choose but not when the computer made choices for them. We also found that focal infusion of OT unilaterally into BLA weakly but significantly increased both the frequency of prosocial decisions and attention to recipients for context-specific prosocial decisions, endorsing the hypothesis that OT regulates social behavior, in part, via amygdala neuromodulation. Our findings demonstrate both neurophysiological and neuroendocrinological connections between primate amygdala and social decisions. |
Mircea I Chelaru; Valentin Dragoi Negative correlations in visual cortical networks Journal Article Cerebral Cortex, 26 (1), pp. 246–256, 2016. Abstract | Links | BibTeX @article{Chelaru2016,
title = {Negative correlations in visual cortical networks},
author = {Mircea I Chelaru and Valentin Dragoi},
doi = {10.1093/cercor/bhu207},
year = {2016},
date = {2016-01-01},
journal = {Cerebral Cortex},
volume = {26},
number = {1},
pages = {246--256},
abstract = {The amount of information encoded by cortical circuits depends critically on the capacity of nearby neurons to exhibit trial-to-trial (noise) correlations in their responses. Depending on their sign and relationship to signal correlations, noise correlations can either increase or decrease the population code accuracy relative to uncorrelated neuronal firing. Whereas positive noise correlations have been extensively studied using experimental and theoretical tools, the functional role of negative correlations in cortical circuits has remained elusive. We addressed this issue by performing multiple-electrode recording in the superficial layers of the primary visual cortex (V1) of alert monkey. Despite the fact that positive noise correlations decayed exponentially with the difference in the orientation preference between cells, negative correlations were uniformly distributed across the population. Using a statistical model for Fisher Information estimation, we found that a mild increase in negative correlations causes a sharp increase in network accuracy even when mean correlations were held constant. To examine the variables controlling the strength of negative correlations, we implemented a recurrent spiking network model of V1. We found that increasing local inhibition and reducing excitation causes a decrease in the firing rates of neurons while increasing the negative noise correlations, which in turn increase the population signal-to-noise ratio and network accuracy. Altogether, these results contribute to our understanding of the neuronal mechanism involved in the generation of negative correlations and their beneficial impact on cortical circuit function.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
The amount of information encoded by cortical circuits depends critically on the capacity of nearby neurons to exhibit trial-to-trial (noise) correlations in their responses. Depending on their sign and relationship to signal correlations, noise correlations can either increase or decrease the population code accuracy relative to uncorrelated neuronal firing. Whereas positive noise correlations have been extensively studied using experimental and theoretical tools, the functional role of negative correlations in cortical circuits has remained elusive. We addressed this issue by performing multiple-electrode recording in the superficial layers of the primary visual cortex (V1) of alert monkey. Despite the fact that positive noise correlations decayed exponentially with the difference in the orientation preference between cells, negative correlations were uniformly distributed across the population. Using a statistical model for Fisher Information estimation, we found that a mild increase in negative correlations causes a sharp increase in network accuracy even when mean correlations were held constant. To examine the variables controlling the strength of negative correlations, we implemented a recurrent spiking network model of V1. We found that increasing local inhibition and reducing excitation causes a decrease in the firing rates of neurons while increasing the negative noise correlations, which in turn increase the population signal-to-noise ratio and network accuracy. Altogether, these results contribute to our understanding of the neuronal mechanism involved in the generation of negative correlations and their beneficial impact on cortical circuit function. |
Xiaodong Chen; Feng Han; Mu-ming Poo; Yang Dan Excitatory and suppressive receptive field subunits in awake monkey primary visual cortex (V1) Journal Article Proceedings of the National Academy of Sciences, 104 (48), pp. 19120–19125, 2007. Abstract | Links | BibTeX @article{Chen2007a,
title = {Excitatory and suppressive receptive field subunits in awake monkey primary visual cortex (V1)},
author = {Xiaodong Chen and Feng Han and Mu-ming Poo and Yang Dan},
url = {http://www.pnas.org/cgi/doi/10.1073/pnas.0706938104},
doi = {10.1073/pnas.0706938104},
year = {2007},
date = {2007-01-01},
journal = {Proceedings of the National Academy of Sciences},
volume = {104},
number = {48},
pages = {19120--19125},
abstract = {An essential step in understanding visual processing is to characterize the neuronal receptive fields (RFs) at each stage of the visual pathway. However, RF characterization beyond simple cells in the primary visual cortex (V1) remains a major challenge. Recent application of spike-triggered covariance (STC) analysis has greatly facilitated characterization of complex cell RFs in anesthetized animals. Here we apply STC to RF characterization in awake monkey V1. We found up to nine subunits for each cell, including one or two dominant excitatory subunits as described by the standard model, along with additional excitatory and suppressive subunits with weaker contributions. Compared with the dominant subunits, the nondominant excitatory subunits prefer similar orientations and spatial frequencies but have larger spatial envelopes. They contribute to response invariance to small changes in stimulus orientation, position, and spatial frequency. In contrast, the suppressive subunits are tuned to orientations 45 degrees -90 degrees different from the excitatory subunits, which may underlie cross-orientation suppression. Together, the excitatory and suppressive subunits form a compact description of RFs in awake monkey V1, allowing prediction of the responses to arbitrary visual stimuli.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
An essential step in understanding visual processing is to characterize the neuronal receptive fields (RFs) at each stage of the visual pathway. However, RF characterization beyond simple cells in the primary visual cortex (V1) remains a major challenge. Recent application of spike-triggered covariance (STC) analysis has greatly facilitated characterization of complex cell RFs in anesthetized animals. Here we apply STC to RF characterization in awake monkey V1. We found up to nine subunits for each cell, including one or two dominant excitatory subunits as described by the standard model, along with additional excitatory and suppressive subunits with weaker contributions. Compared with the dominant subunits, the nondominant excitatory subunits prefer similar orientations and spatial frequencies but have larger spatial envelopes. They contribute to response invariance to small changes in stimulus orientation, position, and spatial frequency. In contrast, the suppressive subunits are tuned to orientations 45 degrees -90 degrees different from the excitatory subunits, which may underlie cross-orientation suppression. Together, the excitatory and suppressive subunits form a compact description of RFs in awake monkey V1, allowing prediction of the responses to arbitrary visual stimuli. |
Xiaomo Chen; Katherine Wilson Scangos; Veit Stuphorn Supplementary motor area exerts proactive and reactive control of arm movements Journal Article Journal of Neuroscience, 30 (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},
url = {http://www.jneurosci.org/cgi/doi/10.1523/JNEUROSCI.2669-10.2010},
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}
}
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. |
Chih Yang Chen; Ziad M Hafed Postmicrosaccadic enhancement of slow eye movements Journal Article Journal of Neuroscience, 33 (12), pp. 5375–5386, 2013. Abstract | Links | BibTeX @article{Chen2013,
title = {Postmicrosaccadic enhancement of slow eye movements},
author = {Chih Yang Chen and Ziad M Hafed},
doi = {10.1523/JNEUROSCI.3703-12.2013},
year = {2013},
date = {2013-01-01},
journal = {Journal of Neuroscience},
volume = {33},
number = {12},
pages = {5375--5386},
abstract = {Active sensation poses unique challenges to sensory systems because moving the sensor necessarily alters the input sensory stream. Sensory input quality is additionally compromised if the sensor moves rapidly, as during rapid eye movements, making the period immediately after the movement critical for recovering reliable sensation. Here, we studied this immediate postmovement interval for the case of microsaccades during fixation, which rapidly jitter the "sensor" exactly when it is being voluntarily stabilized to maintain clear vision. We characterized retinal-image slip in monkeys immediately after microsaccades by analyzing postmovement ocular drifts. We observed enhanced ocular drifts by up to ~28% relative to premicrosaccade levels, and for up to ~50 ms after movement end. Moreover, we used a technique to trigger full-field image motion contingent on real-time microsaccade detection, and we used the initial ocular following response to this motion as a proxy for changes in early visual motion processing caused by microsaccades. When the full-field image motion started during microsaccades, ocular following was strongly suppressed, consistent with detrimental retinal effects of the movements. However, when the motion started after microsaccades, there was up to ~73% increase in ocular following speed, suggesting an enhanced motion sensitivity. These results suggest that the interface between even the smallest possible saccades and "fixation" includes a period of faster than usual image slip, as well as an enhanced responsiveness to image motion, and that both of these phenomena need to be considered when interpreting the pervasive neural and perceptual modulations frequently observed around the time of microsaccades.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Active sensation poses unique challenges to sensory systems because moving the sensor necessarily alters the input sensory stream. Sensory input quality is additionally compromised if the sensor moves rapidly, as during rapid eye movements, making the period immediately after the movement critical for recovering reliable sensation. Here, we studied this immediate postmovement interval for the case of microsaccades during fixation, which rapidly jitter the "sensor" exactly when it is being voluntarily stabilized to maintain clear vision. We characterized retinal-image slip in monkeys immediately after microsaccades by analyzing postmovement ocular drifts. We observed enhanced ocular drifts by up to ~28% relative to premicrosaccade levels, and for up to ~50 ms after movement end. Moreover, we used a technique to trigger full-field image motion contingent on real-time microsaccade detection, and we used the initial ocular following response to this motion as a proxy for changes in early visual motion processing caused by microsaccades. When the full-field image motion started during microsaccades, ocular following was strongly suppressed, consistent with detrimental retinal effects of the movements. However, when the motion started after microsaccades, there was up to ~73% increase in ocular following speed, suggesting an enhanced motion sensitivity. These results suggest that the interface between even the smallest possible saccades and "fixation" includes a period of faster than usual image slip, as well as an enhanced responsiveness to image motion, and that both of these phenomena need to be considered when interpreting the pervasive neural and perceptual modulations frequently observed around the time of microsaccades. |
Ming Chen; Peichao Li; Shude Zhu; Chao Han; Haoran Xu; Yang Fang; Jiaming Hu; Anna W Roe; Lu HD; Haidong D Lu An orientation map for motion boundaries in macaque V2 Journal Article Cerebral Cortex, 26 (1), pp. 279–287, 2016. Abstract | Links | BibTeX @article{Chen2016c,
title = {An orientation map for motion boundaries in macaque V2},
author = {Ming Chen and Peichao Li and Shude Zhu and Chao Han and Haoran Xu and Yang Fang and Jiaming Hu and Anna W Roe and Lu HD and Haidong D Lu},
doi = {10.1093/cercor/bhu235},
year = {2016},
date = {2016-01-01},
journal = {Cerebral Cortex},
volume = {26},
number = {1},
pages = {279--287},
abstract = {The ability to extract the shape of moving objects is fundamental to visual perception. However, where such computations are processed in the visual system is unknown. To address this question, we used intrinsic signal optical imaging in awake monkeys to examine cortical response to perceptual contours defined by motion contrast (motion boundaries, MBs). We found that MB stimuli elicit a robust orientation response in area V2. Orientation maps derived from subtraction of orthogonal MB stimuli aligned well with the orientation maps obtained with luminance gratings (LGs). In contrast, area V1 responded well to LGs, but exhibited a much weaker orientation response to MBs. We further show that V2 direction domains respond to motion contrast, which is required in the detection of MB in V2. These results suggest that V2 represents MB information, an important prerequisite for shape recognition and figure-ground segregation.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
The ability to extract the shape of moving objects is fundamental to visual perception. However, where such computations are processed in the visual system is unknown. To address this question, we used intrinsic signal optical imaging in awake monkeys to examine cortical response to perceptual contours defined by motion contrast (motion boundaries, MBs). We found that MB stimuli elicit a robust orientation response in area V2. Orientation maps derived from subtraction of orthogonal MB stimuli aligned well with the orientation maps obtained with luminance gratings (LGs). In contrast, area V1 responded well to LGs, but exhibited a much weaker orientation response to MBs. We further show that V2 direction domains respond to motion contrast, which is required in the detection of MB in V2. These results suggest that V2 represents MB information, an important prerequisite for shape recognition and figure-ground segregation. |
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 Current Biology, 18 (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}
}
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. |
Jan Churan; Daniel Guitton; Christopher C Pack Context dependence of receptive field remapping in superior colliculus Journal Article Journal of Neurophysiology, 106 (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},
url = {http://www.physiology.org/doi/10.1152/jn.00288.2011},
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}
}
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. |
Jan Churan; Daniel Guitton; Christopher C Pack Perisaccadic remapping and rescaling of visual responses in macaque superior colliculus Journal Article PLoS ONE, 7 (12), pp. 1–10, 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 = {1--10},
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}
}
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. |
Evy Cleeren; Cindy Casteels; Karolien Goffin; Peter Janssen; Wim Van Paesschen Ictal perfusion changes associated with seizure progression in the amygdala kindling model in the rhesus monkey Journal Article Epilepsia, 56 (9), pp. 1366–1375, 2015. Abstract | Links | BibTeX @article{Cleeren2015,
title = {Ictal perfusion changes associated with seizure progression in the amygdala kindling model in the rhesus monkey},
author = {Evy Cleeren and Cindy Casteels and Karolien Goffin and Peter Janssen and Wim {Van Paesschen}},
doi = {10.1111/epi.13077},
year = {2015},
date = {2015-01-01},
journal = {Epilepsia},
volume = {56},
number = {9},
pages = {1366--1375},
abstract = {OBJECTIVE: Amygdala kindling is a widely used animal model for studying mesial temporal lobe epileptogenesis. In the macaque monkey, electrical amygdala kindling develops slowly and provides an opportunity for investigating ictal perfusion changes during epileptogenesis. METHODS: Two rhesus monkeys were electrically kindled through chronically implanted electrodes in the right amygdala over a period of 16 and 17 months. Ictal perfusion single photon emission computed tomography (SPECT) imaging was performed during each of the four predefined clinical stages. RESULTS: Afterdischarge duration increased slowly over 477 days for monkey K and 515 days for monkey S (18 ± 8 s in stage I; 52 ± 13 s in stage IV). During this time, the animals progressed through four clinical stages ranging from interrupting ongoing behavior to bilateral convulsions. Ictal SPECT perfusion imaging showed well-localized but widely distributed regions of hyperperfusion and hypoperfusion, in both cortical and subcortical structures, at every seizure stage. A large portion of the ictal network was involved in the early stages of epileptogenesis and subsequently expanded over time as seizure severity evolved. SIGNIFICANCE: Our data indicate that the different mesial temporal lobe seizure types occur within a common network affecting several parts of the brain, and that seizure severity may be determined by seizure-induced epileptogenesis within a bihemispheric network that is implicated from the start of the process.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
OBJECTIVE: Amygdala kindling is a widely used animal model for studying mesial temporal lobe epileptogenesis. In the macaque monkey, electrical amygdala kindling develops slowly and provides an opportunity for investigating ictal perfusion changes during epileptogenesis. METHODS: Two rhesus monkeys were electrically kindled through chronically implanted electrodes in the right amygdala over a period of 16 and 17 months. Ictal perfusion single photon emission computed tomography (SPECT) imaging was performed during each of the four predefined clinical stages. RESULTS: Afterdischarge duration increased slowly over 477 days for monkey K and 515 days for monkey S (18 ± 8 s in stage I; 52 ± 13 s in stage IV). During this time, the animals progressed through four clinical stages ranging from interrupting ongoing behavior to bilateral convulsions. Ictal SPECT perfusion imaging showed well-localized but widely distributed regions of hyperperfusion and hypoperfusion, in both cortical and subcortical structures, at every seizure stage. A large portion of the ictal network was involved in the early stages of epileptogenesis and subsequently expanded over time as seizure severity evolved. SIGNIFICANCE: Our data indicate that the different mesial temporal lobe seizure types occur within a common network affecting several parts of the brain, and that seizure severity may be determined by seizure-induced epileptogenesis within a bihemispheric network that is implicated from the start of the process. |
Michael Colombo; James S Magnuson Eye movements reveal planning in humans: A comparison with Scarf and Colombo's (2009) monkeys Journal Article Journal of Experimental Psychology: Animal Learning and Cognition, 40 (2), pp. 178–184, 2014. Abstract | Links | BibTeX @article{Colombo2014,
title = {Eye movements reveal planning in humans: A comparison with Scarf and Colombo's (2009) monkeys},
author = {Michael Colombo and James S Magnuson},
doi = {10.1037/xan0000008},
year = {2014},
date = {2014-01-01},
journal = {Journal of Experimental Psychology: Animal Learning and Cognition},
volume = {40},
number = {2},
pages = {178--184},
abstract = {On sequential response tasks, a long pause preceding the first response is thought to reflect participants taking time to plan a sequence of responses. By tracking the eye movements of two monkeys (Macaca fascicularis), Scarf and Colombo (2009, Eye Movements During List Execution Reveal No Planning in Monkeys [Macaca fascicularis], Journal of Experimental Psychology: Animal Behavior Processes, Vol. 35, pp. 587–592) demonstrated that, at least with respect to monkeys, the long pause preceding the first response is not necessarily the product of planning. In the present experiment, we tracked the eye movements of adult humans using the paradigm employed by Scarf and Colombo and found that, in contrast to monkeys, the pause preceding the first item is indicative of planning in humans. These findings highlight the fact that similar response time profiles, displayed by human and nonhuman animals, do not necessarily reflect similar underlying cognitive operations.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
On sequential response tasks, a long pause preceding the first response is thought to reflect participants taking time to plan a sequence of responses. By tracking the eye movements of two monkeys (Macaca fascicularis), Scarf and Colombo (2009, Eye Movements During List Execution Reveal No Planning in Monkeys [Macaca fascicularis], Journal of Experimental Psychology: Animal Behavior Processes, Vol. 35, pp. 587–592) demonstrated that, at least with respect to monkeys, the long pause preceding the first response is not necessarily the product of planning. In the present experiment, we tracked the eye movements of adult humans using the paradigm employed by Scarf and Colombo and found that, in contrast to monkeys, the pause preceding the first item is indicative of planning in humans. These findings highlight the fact that similar response time profiles, displayed by human and nonhuman animals, do not necessarily reflect similar underlying cognitive operations. |
Benjamin W Corrigan; Roberto A Gulli; Guillaume Doucet; Julio C Martinez-Trujillo Characterizing eye movement behaviors and kinematics of non-human primates during virtual navigation tasks Journal Article Journal of Vision, 17 (12), pp. 1–22, 2017. Abstract | Links | BibTeX @article{Corrigan2017,
title = {Characterizing eye movement behaviors and kinematics of non-human primates during virtual navigation tasks},
author = {Benjamin W Corrigan and Roberto A Gulli and Guillaume Doucet and Julio C Martinez-Trujillo},
url = {http://jov.arvojournals.org/article.aspx?doi=10.1167/17.12.15},
doi = {10.1167/17.12.15},
year = {2017},
date = {2017-01-01},
journal = {Journal of Vision},
volume = {17},
number = {12},
pages = {1--22},
abstract = {Virtual environments (VE) allow testing complex behaviors in naturalistic settings by combining highly controlled visual stimuli with spatial navigation and other cognitive tasks. They also allow for the recording of eye movements using high-precision eye tracking techniques, which is important in electrophysiological studies examining the response properties of neurons in visual areas of nonhuman primates. However, during virtual navigation, the pattern of retinal stimulation can be highly dynamic which may influence eye movements. Here we examine whether and how eye movement patterns change as a function of dynamic visual stimulation during virtual navigation tasks, relative to standard oculomotor tasks. We trained two rhesus macaques to use a joystick to navigate in a VE to complete two tasks. To contrast VE behavior with classic measurements, the monkeys also performed a simple Cued Saccade task. We used a robust algorithm for rapid classification of saccades, fixations, and smooth pursuits. We then analyzed the kinematics of saccades during all tasks, and specifically during different phases of the VE tasks. We found that fixation to smooth pursuit ratios were smaller in VE tasks (4:5) compared to the Cued Saccade task (7:1), reflecting a more intensive use of smooth pursuit to foveate targets in VE than in a standard visually guided saccade task or during spontaneous fixations. Saccades made to rewarded targets (exploitation) tended to have increased peak velocities compared to saccades made to unrewarded objects (exploration). VE exploitation saccades were 6% slower than saccades to discrete targets in the Cued Saccade task. Virtual environments represent a technological advance in experimental design for nonhuman primates. Here we provide a framework to study the ways that eye movements change between and within static and dynamic displays.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Virtual environments (VE) allow testing complex behaviors in naturalistic settings by combining highly controlled visual stimuli with spatial navigation and other cognitive tasks. They also allow for the recording of eye movements using high-precision eye tracking techniques, which is important in electrophysiological studies examining the response properties of neurons in visual areas of nonhuman primates. However, during virtual navigation, the pattern of retinal stimulation can be highly dynamic which may influence eye movements. Here we examine whether and how eye movement patterns change as a function of dynamic visual stimulation during virtual navigation tasks, relative to standard oculomotor tasks. We trained two rhesus macaques to use a joystick to navigate in a VE to complete two tasks. To contrast VE behavior with classic measurements, the monkeys also performed a simple Cued Saccade task. We used a robust algorithm for rapid classification of saccades, fixations, and smooth pursuits. We then analyzed the kinematics of saccades during all tasks, and specifically during different phases of the VE tasks. We found that fixation to smooth pursuit ratios were smaller in VE tasks (4:5) compared to the Cued Saccade task (7:1), reflecting a more intensive use of smooth pursuit to foveate targets in VE than in a standard visually guided saccade task or during spontaneous fixations. Saccades made to rewarded targets (exploitation) tended to have increased peak velocities compared to saccades made to unrewarded objects (exploration). VE exploitation saccades were 6% slower than saccades to discrete targets in the Cued Saccade task. Virtual environments represent a technological advance in experimental design for nonhuman primates. Here we provide a framework to study the ways that eye movements change between and within static and dynamic displays. |
Gabriela M Costello; Dantong Zhu; Emilio Salinas; Terrence R Stanford Perceptual modulation of motor-but not visual-responses in the frontal eye field during an urgent-decision task Journal Article Journal of Neuroscience, 33 (41), pp. 16394–16408, 2013. Abstract | Links | BibTeX @article{Costello2013,
title = {Perceptual modulation of motor-but not visual-responses in the frontal eye field during an urgent-decision task},
author = {Gabriela M Costello and Dantong Zhu and Emilio Salinas and Terrence R Stanford},
url = {http://www.jneurosci.org/cgi/doi/10.1523/JNEUROSCI.1899-13.2013},
doi = {10.1523/JNEUROSCI.1899-13.2013},
year = {2013},
date = {2013-01-01},
journal = {Journal of Neuroscience},
volume = {33},
number = {41},
pages = {16394--16408},
abstract = {Neuronal activity in the frontal eye field (FEF) ranges from purely motor (related to saccade production) to purely visual (related to stimulus presence). According to numerous studies, visual responses correlate strongly with early perceptual analysis of the visual scene, including the deployment of spatial attention, whereas motor responses do not. Thus, functionally, the consensus is that visually responsive FEF neurons select a target among visible objects, whereas motor-related neurons plan specific eye movements based on such earlier target selection. However, these conclusions are based on behavioral tasks that themselves promote a serial arrangement of perceptual analysis followed by motor planning. So, is the presumed functional hierarchy in FEF an intrinsic property of its circuitry or does it reflect just one possible mode of operation? We investigate this in monkeys performing a rapid-choice task in which, crucially, motor planning always starts ahead of task-critical perceptual analysis, and the two relevant spatial locations are equally informative and equally likely to be target or distracter. We find that the choice is instantiated in FEF as a competition between oculomotor plans, in agreement with model predictions. Notably, although perception strongly influences the motor neurons, it has little if any measurable impact on the visual cells; more generally, the more dominant the visual response, the weaker the perceptual modulation. The results indicate that, contrary to expectations, during rapid saccadic choices perceptual information may directly modulate ongoing saccadic plans, and this process is not contingent on prior selection of the saccadic goal by visually driven FEF responses.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Neuronal activity in the frontal eye field (FEF) ranges from purely motor (related to saccade production) to purely visual (related to stimulus presence). According to numerous studies, visual responses correlate strongly with early perceptual analysis of the visual scene, including the deployment of spatial attention, whereas motor responses do not. Thus, functionally, the consensus is that visually responsive FEF neurons select a target among visible objects, whereas motor-related neurons plan specific eye movements based on such earlier target selection. However, these conclusions are based on behavioral tasks that themselves promote a serial arrangement of perceptual analysis followed by motor planning. So, is the presumed functional hierarchy in FEF an intrinsic property of its circuitry or does it reflect just one possible mode of operation? We investigate this in monkeys performing a rapid-choice task in which, crucially, motor planning always starts ahead of task-critical perceptual analysis, and the two relevant spatial locations are equally informative and equally likely to be target or distracter. We find that the choice is instantiated in FEF as a competition between oculomotor plans, in agreement with model predictions. Notably, although perception strongly influences the motor neurons, it has little if any measurable impact on the visual cells; more generally, the more dominant the visual response, the weaker the perceptual modulation. The results indicate that, contrary to expectations, during rapid saccadic choices perceptual information may directly modulate ongoing saccadic plans, and this process is not contingent on prior selection of the saccadic goal by visually driven FEF responses. |
Gabriela M Costello; Dantong Zhu; Paul J May; Emilio Salinas; Terrence R Stanford Task dependence of decision- and choice-related activity in monkey oculomotor thalamus Journal Article Journal of Neurophysiology, 115 (1), pp. 581–601, 2016. Abstract | Links | BibTeX @article{Costello2016,
title = {Task dependence of decision- and choice-related activity in monkey oculomotor thalamus},
author = {Gabriela M Costello and Dantong Zhu and Paul J May and Emilio Salinas and Terrence R Stanford},
url = {http://jn.physiology.org/lookup/doi/10.1152/jn.00592.2015},
doi = {10.1152/jn.00592.2015},
year = {2016},
date = {2016-01-01},
journal = {Journal of Neurophysiology},
volume = {115},
number = {1},
pages = {581--601},
abstract = {Oculomotor signals circulate within putative recurrent feedback loops that include the frontal eye field (FEF) and the oculomotor thalamus (OcTh). To examine how OcTh contributes to visuomotor control, and perceptually informed saccadic choices in particular, neural correlates of perceptual judgment and motor selection in OcTh were evaluated and compared with those previously reported for FEF in the same subjects. Monkeys performed three tasks: a choice task in which perceptual decisions are urgent, a choice task in which identical decisions are made without time pressure, and a single-target, delayed saccade task. The OcTh yielded far fewer task-responsive neurons than the FEF, but across responsive pools, similar neuron types were found, ranging from purely visual to purely saccade related. Across such types, the impact of the perceptual information relevant to saccadic choices was qualitatively the same in FEF and OcTh. However, distinct from that in FEF, activity in OcTh was strongly task dependent, typically being most vigorous in the urgent task, less so in the easier choice task, and least in the single-target task. This was true for responsive and nonresponsive cells alike. Neurons with exclusively motor-related activity showed strong task dependence, fired less, and differed most patently from their FEF counterparts, whereas those that combined visual and motor activity fired most similarly to their FEF counterparts. The results suggest that OcTh activity is more distantly related to saccade production per se, because its degree of commitment to a motor choice varies markedly as a function of ongoing cognitive or behavioral demands.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Oculomotor signals circulate within putative recurrent feedback loops that include the frontal eye field (FEF) and the oculomotor thalamus (OcTh). To examine how OcTh contributes to visuomotor control, and perceptually informed saccadic choices in particular, neural correlates of perceptual judgment and motor selection in OcTh were evaluated and compared with those previously reported for FEF in the same subjects. Monkeys performed three tasks: a choice task in which perceptual decisions are urgent, a choice task in which identical decisions are made without time pressure, and a single-target, delayed saccade task. The OcTh yielded far fewer task-responsive neurons than the FEF, but across responsive pools, similar neuron types were found, ranging from purely visual to purely saccade related. Across such types, the impact of the perceptual information relevant to saccadic choices was qualitatively the same in FEF and OcTh. However, distinct from that in FEF, activity in OcTh was strongly task dependent, typically being most vigorous in the urgent task, less so in the easier choice task, and least in the single-target task. This was true for responsive and nonresponsive cells alike. Neurons with exclusively motor-related activity showed strong task dependence, fired less, and differed most patently from their FEF counterparts, whereas those that combined visual and motor activity fired most similarly to their FEF counterparts. The results suggest that OcTh activity is more distantly related to saccade production per se, because its degree of commitment to a motor choice varies markedly as a function of ongoing cognitive or behavioral demands. |
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 Journal of Neurophysiology, 100 (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},
url = {http://jn.physiology.org/cgi/doi/10.1152/jn.90672.2008},
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 textless150 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}
}
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 textless150 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. |
Michele A Cox; Michael C Schmid; Andrew J Peters; Richards C Saunders; David A Leopold; Alexander Maier Receptive field focus of visual area V4 neurons determines responses to illusory surfaces Journal Article Proceedings of the National Academy of Sciences, 110 (42), pp. 17095–17100, 2013. Abstract | Links | BibTeX @article{Cox2013,
title = {Receptive field focus of visual area V4 neurons determines responses to illusory surfaces},
author = {Michele A Cox and Michael C Schmid and Andrew J Peters and Richards C Saunders and David A Leopold and Alexander Maier},
url = {http://www.pnas.org/cgi/doi/10.1073/pnas.1310806110},
doi = {10.1073/pnas.1310806110},
year = {2013},
date = {2013-01-01},
journal = {Proceedings of the National Academy of Sciences},
volume = {110},
number = {42},
pages = {17095--17100},
abstract = {Illusory figures demonstrate the visual system's ability to infer surfaces under conditions of fragmented sensory input. To investigate the role of midlevel visual area V4 in visual surface completion, we used multielectrode arrays to measure spiking responses to two types of visual stimuli: Kanizsa patterns that induce the perception of an illusory surface and physically similar control stimuli that do not. Neurons in V4 exhibited stronger and sometimes rhythmic spiking responses for the illusion-promoting configurations compared with controls. Moreover, this elevated response depended on the precise alignment of the neuron's peak visual field sensitivity (receptive field focus) with the illusory surface itself. Neurons whose receptive field focus was over adjacent inducing elements, less than 1.5° away, did not show response enhancement to the illusion. Neither receptive field sizes nor fixational eye movements could account for this effect, which was present in both single-unit signals and multiunit activity. These results suggest that the active perceptual completion of surfaces and shapes, which is a fundamental problem in natural visual experience, draws upon the selective enhancement of activity within a distinct subpopulation of neurons in cortical area V4.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Illusory figures demonstrate the visual system's ability to infer surfaces under conditions of fragmented sensory input. To investigate the role of midlevel visual area V4 in visual surface completion, we used multielectrode arrays to measure spiking responses to two types of visual stimuli: Kanizsa patterns that induce the perception of an illusory surface and physically similar control stimuli that do not. Neurons in V4 exhibited stronger and sometimes rhythmic spiking responses for the illusion-promoting configurations compared with controls. Moreover, this elevated response depended on the precise alignment of the neuron's peak visual field sensitivity (receptive field focus) with the illusory surface itself. Neurons whose receptive field focus was over adjacent inducing elements, less than 1.5° away, did not show response enhancement to the illusion. Neither receptive field sizes nor fixational eye movements could account for this effect, which was present in both single-unit signals and multiunit activity. These results suggest that the active perceptual completion of surfaces and shapes, which is a fundamental problem in natural visual experience, draws upon the selective enhancement of activity within a distinct subpopulation of neurons in cortical area V4. |
Michele A Cox; Kacie Dougherty; Geoffrey K Adams; Eric A Reavis; Jacob A Westerberg; Brandon S Moore; David A Leopold; Alexander Maier Spiking suppression precedes cued attentional enhancement of neural responses in primary visual Cortex Journal Article Cerebral Cortex, 29 (1), pp. 77–90, 2017. Abstract | Links | BibTeX @article{Cox2017,
title = {Spiking suppression precedes cued attentional enhancement of neural responses in primary visual Cortex},
author = {Michele A Cox and Kacie Dougherty and Geoffrey K Adams and Eric A Reavis and Jacob A Westerberg and Brandon S Moore and David A Leopold and Alexander Maier},
url = {http://academic.oup.com/cercor/advance-article/doi/10.1093/cercor/bhx305/4653733},
doi = {10.1093/cercor/bhx305},
year = {2017},
date = {2017-01-01},
journal = {Cerebral Cortex},
volume = {29},
number = {1},
pages = {77--90},
abstract = {Attending to a visual stimulus increases its detectability, even if gaze is directed elsewhere. This covert attentional selection is known to enhance spiking across many brain areas, including the primary visual cortex (V1). Here we investigate the temporal dynamics of attention-related spiking changes in V1 of macaques performing a task that separates attentional selection from the onset of visual stimulation. We found that preceding attentional enhancement there was a sharp, transient decline in spiking following presentation of an attention-guiding cue. This disruption of V1 spiking was not observed in a task-naïve subject that passively observed the same stimulus sequence, suggesting that sensory activation is insufficient to cause suppression. Following this suppression, attended stimuli evoked more spiking than unattended stimuli, matching previous reports of attention-related activity in V1. Laminar analyses revealed a distinct pattern of activation in feedback-associated layers during both the cue-induced suppression and subsequent attentional enhancement. These findings suggest that top-down modulation of V1 spiking can be bidirectional and result in either suppression or enhancement of spiking responses.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Attending to a visual stimulus increases its detectability, even if gaze is directed elsewhere. This covert attentional selection is known to enhance spiking across many brain areas, including the primary visual cortex (V1). Here we investigate the temporal dynamics of attention-related spiking changes in V1 of macaques performing a task that separates attentional selection from the onset of visual stimulation. We found that preceding attentional enhancement there was a sharp, transient decline in spiking following presentation of an attention-guiding cue. This disruption of V1 spiking was not observed in a task-naïve subject that passively observed the same stimulus sequence, suggesting that sensory activation is insufficient to cause suppression. Following this suppression, attended stimuli evoked more spiking than unattended stimuli, matching previous reports of attention-related activity in V1. Laminar analyses revealed a distinct pattern of activation in feedback-associated layers during both the cue-induced suppression and subsequent attentional enhancement. These findings suggest that top-down modulation of V1 spiking can be bidirectional and result in either suppression or enhancement of spiking responses. |
Yuwei Cui; Liu D Liu; Farhan A Khawaja; Christopher C Pack; Daniel A Butts Diverse suppressive Iinfluences in area MT and selectivity to complex motion features Journal Article Journal of Neuroscience, 33 (42), pp. 16715–16728, 2013. Abstract | Links | BibTeX @article{Cui2013c,
title = {Diverse suppressive Iinfluences in area MT and selectivity to complex motion features},
author = {Yuwei Cui and Liu D Liu and Farhan A Khawaja and Christopher C Pack and Daniel A Butts},
url = {http://www.jneurosci.org/cgi/doi/10.1523/JNEUROSCI.0203-13.2013},
doi = {10.1523/JNEUROSCI.0203-13.2013},
year = {2013},
date = {2013-01-01},
journal = {Journal of Neuroscience},
volume = {33},
number = {42},
pages = {16715--16728},
abstract = {Neuronal selectivity results from both excitatory and suppressive inputs to a given neuron. Suppressive influences can often significantly modulate neuronal responses and impart novel selectivity in the context of behaviorally relevant stimuli. In this work, we use a naturalistic optic flow stimulus to explore the responses of neurons in the middle temporal area (MT) of the alert macaque monkey; these responses are interpreted using a hierarchical model that incorporates relevant nonlinear properties of upstream processing in the primary visual cortex (V1). In this stimulus context, MT neuron responses can be predicted from distinct excitatory and suppressive components. Excitation is spatially localized and matches the measured preferred direction of each neuron. Suppression is typically composed of two distinct components: (1) a directionally untuned component, which appears to play the role of surround suppression and normalization; and (2) a direction-selective component, with comparable tuning width as excitation and a distinct spatial footprint that is usually partially overlapping with excitation. The direction preference of this direction-tuned suppression varies widely across MT neurons: approximately one-third have overlapping suppression in the opposite direction as excitation, and many other neurons have suppression with similar direction preferences to excitation. There is also a population of MT neurons with orthogonally oriented suppression. We demonstrate that direction-selective suppression can impart selectivity of MT neurons to more complex velocity fields and that it can be used for improved estimation of the three-dimensional velocity of moving objects. Thus, considering MT neurons in a complex stimulus context reveals a diverse set of computations likely relevant for visual processing in natural visual contexts.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Neuronal selectivity results from both excitatory and suppressive inputs to a given neuron. Suppressive influences can often significantly modulate neuronal responses and impart novel selectivity in the context of behaviorally relevant stimuli. In this work, we use a naturalistic optic flow stimulus to explore the responses of neurons in the middle temporal area (MT) of the alert macaque monkey; these responses are interpreted using a hierarchical model that incorporates relevant nonlinear properties of upstream processing in the primary visual cortex (V1). In this stimulus context, MT neuron responses can be predicted from distinct excitatory and suppressive components. Excitation is spatially localized and matches the measured preferred direction of each neuron. Suppression is typically composed of two distinct components: (1) a directionally untuned component, which appears to play the role of surround suppression and normalization; and (2) a direction-selective component, with comparable tuning width as excitation and a distinct spatial footprint that is usually partially overlapping with excitation. The direction preference of this direction-tuned suppression varies widely across MT neurons: approximately one-third have overlapping suppression in the opposite direction as excitation, and many other neurons have suppression with similar direction preferences to excitation. There is also a population of MT neurons with orthogonally oriented suppression. We demonstrate that direction-selective suppression can impart selectivity of MT neurons to more complex velocity fields and that it can be used for improved estimation of the three-dimensional velocity of moving objects. Thus, considering MT neurons in a complex stimulus context reveals a diverse set of computations likely relevant for visual processing in natural visual contexts. |
Yuwei Cui; Liu D Liu; James M McFarland; Christopher C Pack; Daniel A Butts Inferring cortical variability from local field potentials Journal Article Journal of Neuroscience, 36 (14), pp. 4121–4135, 2016. Abstract | Links | BibTeX @article{Cui2016,
title = {Inferring cortical variability from local field potentials},
author = {Yuwei Cui and Liu D Liu and James M McFarland and Christopher C Pack and Daniel A Butts},
url = {http://www.jneurosci.org/cgi/doi/10.1523/JNEUROSCI.2502-15.2016},
doi = {10.1523/JNEUROSCI.2502-15.2016},
year = {2016},
date = {2016-01-01},
journal = {Journal of Neuroscience},
volume = {36},
number = {14},
pages = {4121--4135},
abstract = {The responses of sensory neurons can be quite different to repeated presentations of the same stimulus. Here, we demonstrate a direct link between the trial-to-trial variability of cortical neuron responses and network activity that is reflected in local field potentials (LFPs). Spikes and LFPs were recorded with a multielectrode array from the middle temporal (MT) area of the visual cortex of macaques during the presentation of continuous optic flow stimuli. A maximum likelihood-based modeling framework was used to predict single-neuron spiking responses using the stimulus, the LFPs, and the activity of other recorded neurons. MT neuron responses were strongly linked to gamma oscillations (maximum at 40 Hz) as well as to lower-frequency delta oscillations (1-4 Hz), with consistent phase preferences across neurons. The predicted modulation associated with the LFP was largely complementary to that driven by visual stimulation, as well as the activity of other neurons, and accounted for nearly half of the trial-to-trial variability in the spiking responses. Moreover, the LFP model predictions accurately captured the temporal structure of noise correlations between pairs of simultaneously recorded neurons, and explained the variation in correlation magnitudes observed across the population. These results therefore identify signatures of network activity related to the variability of cortical neuron responses, and suggest their central role in sensory cortical function.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
The responses of sensory neurons can be quite different to repeated presentations of the same stimulus. Here, we demonstrate a direct link between the trial-to-trial variability of cortical neuron responses and network activity that is reflected in local field potentials (LFPs). Spikes and LFPs were recorded with a multielectrode array from the middle temporal (MT) area of the visual cortex of macaques during the presentation of continuous optic flow stimuli. A maximum likelihood-based modeling framework was used to predict single-neuron spiking responses using the stimulus, the LFPs, and the activity of other recorded neurons. MT neuron responses were strongly linked to gamma oscillations (maximum at 40 Hz) as well as to lower-frequency delta oscillations (1-4 Hz), with consistent phase preferences across neurons. The predicted modulation associated with the LFP was largely complementary to that driven by visual stimulation, as well as the activity of other neurons, and accounted for nearly half of the trial-to-trial variability in the spiking responses. Moreover, the LFP model predictions accurately captured the temporal structure of noise correlations between pairs of simultaneously recorded neurons, and explained the variation in correlation magnitudes observed across the population. These results therefore identify signatures of network activity related to the variability of cortical neuron responses, and suggest their central role in sensory cortical function. |
Olga Dal Monte; Matthew Piva; Jason A Morris; Steve W C Chang Live interaction distinctively shapes social gaze dynamics in rhesus macaques Journal Article Journal of Neurophysiology, 116 (4), pp. 1626–1643, 2016. Abstract | Links | BibTeX @article{DalMonte2016,
title = {Live interaction distinctively shapes social gaze dynamics in rhesus macaques},
author = {Olga {Dal Monte} and Matthew Piva and Jason A Morris and Steve W C Chang},
url = {http://jn.physiology.org/lookup/doi/10.1152/jn.00442.2016},
doi = {10.1152/jn.00442.2016},
year = {2016},
date = {2016-01-01},
journal = {Journal of Neurophysiology},
volume = {116},
number = {4},
pages = {1626--1643},
abstract = {The dynamic interaction of gaze between individuals is a hallmark of social cognition. However, very few studies have examined social gaze dynamics after mutual eye contact during real-time interactions. We used a highly quantifiable paradigm to assess social gaze dynamics between pairs of monkeys and modeled these dynamics using an exponential decay function to investigate sustained attention after mutual eye contact. When mon- keys were interacting with real partners compared with static images and movies of the same monkeys, we found a significant increase in the proportion of fixations to the eyes and a smaller dispersion of fixations around the eyes, indicating enhanced focal attention to the eye region. Notably, dominance and familiarity between the interact- ing pairs induced separable components of gaze dynamics that were unique to live interactions. Gaze dynamics of dominant monkeys after mutual eye contact were associated with a greater number of fixations to the eyes, whereas those of familiar pairs were associated with a faster rate of decrease in this eye-directed attention. Our findings endorse the notion that certain key aspects of social cognition are only captured during interactive social contexts and dependent on the elapsed time relative to socially meaningful events.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
The dynamic interaction of gaze between individuals is a hallmark of social cognition. However, very few studies have examined social gaze dynamics after mutual eye contact during real-time interactions. We used a highly quantifiable paradigm to assess social gaze dynamics between pairs of monkeys and modeled these dynamics using an exponential decay function to investigate sustained attention after mutual eye contact. When mon- keys were interacting with real partners compared with static images and movies of the same monkeys, we found a significant increase in the proportion of fixations to the eyes and a smaller dispersion of fixations around the eyes, indicating enhanced focal attention to the eye region. Notably, dominance and familiarity between the interact- ing pairs induced separable components of gaze dynamics that were unique to live interactions. Gaze dynamics of dominant monkeys after mutual eye contact were associated with a greater number of fixations to the eyes, whereas those of familiar pairs were associated with a faster rate of decrease in this eye-directed attention. Our findings endorse the notion that certain key aspects of social cognition are only captured during interactive social contexts and dependent on the elapsed time relative to socially meaningful events. |
Olga Dal Monte; Matthew Piva; Kevin M Anderson; Marios Tringides; Avram J Holmes; Steve W C Chang Oxytocin under opioid antagonism leads to supralinear enhancement of social attention Journal Article Proceedings of the National Academy of Sciences, 114 (20), pp. 5247–5252, 2017. Abstract | Links | BibTeX @article{DalMonte2017,
title = {Oxytocin under opioid antagonism leads to supralinear enhancement of social attention},
author = {Olga {Dal Monte} and Matthew Piva and Kevin M Anderson and Marios Tringides and Avram J Holmes and Steve W C Chang},
url = {http://www.pnas.org/lookup/doi/10.1073/pnas.1702725114},
doi = {10.1073/pnas.1702725114},
year = {2017},
date = {2017-01-01},
journal = {Proceedings of the National Academy of Sciences},
volume = {114},
number = {20},
pages = {5247--5252},
abstract = {To provide new preclinical evidence toward improving the efficacy of oxytocin (OT) in treating social dysfunction, we tested the benefit of administering OT under simultaneously induced opioid antagonism during dyadic gaze interactions in monkeys. OT coadministered with a $mu$-opioid receptor antagonist, naloxone, invoked a supralinear enhancement of prolonged and selective social attention, producing a stronger effect than the summed effects of each administered separately. These effects were consistently observed when averaging over entire sessions, as well as specifically following events of particular social importance, including mutual eye contact and mutual reward receipt. Furthermore, attention to various facial regions was differentially modulated depending on social context. Using the Allen Institute's transcriptional atlas, we further established the colocalization of $mu$-opioid and $kappa$-opioid receptor genes and OT genes at the OT-releasing sites in the human brain. These data across monkeys and humans support a regulatory relationship between the OT and opioid systems and suggest that administering OT under opioid antagonism may boost the therapeutic efficacy of OT for enhancing social cognition.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
To provide new preclinical evidence toward improving the efficacy of oxytocin (OT) in treating social dysfunction, we tested the benefit of administering OT under simultaneously induced opioid antagonism during dyadic gaze interactions in monkeys. OT coadministered with a $mu$-opioid receptor antagonist, naloxone, invoked a supralinear enhancement of prolonged and selective social attention, producing a stronger effect than the summed effects of each administered separately. These effects were consistently observed when averaging over entire sessions, as well as specifically following events of particular social importance, including mutual eye contact and mutual reward receipt. Furthermore, attention to various facial regions was differentially modulated depending on social context. Using the Allen Institute's transcriptional atlas, we further established the colocalization of $mu$-opioid and $kappa$-opioid receptor genes and OT genes at the OT-releasing sites in the human brain. These data across monkeys and humans support a regulatory relationship between the OT and opioid systems and suggest that administering OT under opioid antagonism may boost the therapeutic efficacy of OT for enhancing social cognition. |
S V David; B Y Hayden; J L Gallant Spectral receptive field properties explain shape selectivity in area V4 Journal Article Journal of Neurophysiology, 96 (6), pp. 3492–3505, 2006. Abstract | Links | BibTeX @article{David2006,
title = {Spectral receptive field properties explain shape selectivity in area V4},
author = {S V David and B Y Hayden and J L Gallant},
url = {http://jn.physiology.org/cgi/doi/10.1152/jn.00575.2006},
doi = {10.1152/jn.00575.2006},
year = {2006},
date = {2006-01-01},
journal = {Journal of Neurophysiology},
volume = {96},
number = {6},
pages = {3492--3505},
abstract = {Neurons in cortical area V4 respond selectively to complex visual patterns such as curved contours and non-Cartesian gratings. Most previous experiments in V4 have measured responses to small, idiosyncratic stimulus sets and no single functional model yet accounts for all of the disparate results. We propose that one model, the spectral receptive field (SRF), can explain many observations of selectivity in V4. The SRF describes tuning in terms of the orientation and spatial frequency spectrum and can, in principle, predict the response to any visual stimulus. We estimated SRFs for neurons in V4 of awake primates by linearized reverse correlation of responses to a large set of natural images. We find that V4 neurons have large orientation and spatial frequency bandwidth and often bimodal orientation tuning. For comparison, we estimated SRFs for neurons in primary visual cortex (V1). Consistent with previous observations, we find that V1 neurons have narrower bandwidth than that of V4. To determine whether estimated SRFs can account for previous observations of selectivity, we used them to predict responses to Cartesian gratings, non-Cartesian gratings, natural images, and curved contours. Based on these predictions, we find that the majority of neurons in V1 are selective for Cartesian gratings, whereas the majority of V4 neurons are selective for non-Cartesian gratings or natural images. The SRF describes visual tuning properties with a second-order nonlinear model. These results support the hypothesis that a second-order model is sufficient to describe the general mechanisms mediating shape selectivity in area V4.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Neurons in cortical area V4 respond selectively to complex visual patterns such as curved contours and non-Cartesian gratings. Most previous experiments in V4 have measured responses to small, idiosyncratic stimulus sets and no single functional model yet accounts for all of the disparate results. We propose that one model, the spectral receptive field (SRF), can explain many observations of selectivity in V4. The SRF describes tuning in terms of the orientation and spatial frequency spectrum and can, in principle, predict the response to any visual stimulus. We estimated SRFs for neurons in V4 of awake primates by linearized reverse correlation of responses to a large set of natural images. We find that V4 neurons have large orientation and spatial frequency bandwidth and often bimodal orientation tuning. For comparison, we estimated SRFs for neurons in primary visual cortex (V1). Consistent with previous observations, we find that V1 neurons have narrower bandwidth than that of V4. To determine whether estimated SRFs can account for previous observations of selectivity, we used them to predict responses to Cartesian gratings, non-Cartesian gratings, natural images, and curved contours. Based on these predictions, we find that the majority of neurons in V1 are selective for Cartesian gratings, whereas the majority of V4 neurons are selective for non-Cartesian gratings or natural images. The SRF describes visual tuning properties with a second-order nonlinear model. These results support the hypothesis that a second-order model is sufficient to describe the general mechanisms mediating shape selectivity in area V4. |
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 Neuron, 59 (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}
}
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. |
T S Davis; K Torab; P House; B Greger A minimally invasive approach to long-term head fixation in behaving nonhuman primates Journal Article Journal of Neuroscience Methods, 181 (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 P House and B 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}
}
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. |
T S Davis; R A Parker; P A House; E Bagley; S Wendelken; R A Normann; B Greger Spatial and temporal characteristics of V1 microstimulation during chronic implantation of a microelectrode array in a behaving macaque Journal Article Journal of Neural Engineering, 9 (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 P A House and E Bagley and S Wendelken and R A Normann and B 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}
}
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. |
Thomas Deffieux; Youliana Younan; Nicolas Wattiez; Mickael Tanter; Pierre Pouget; Jean François Aubry Low-intensity focused ultrasound modulates monkey visuomotor behavior Journal Article Current Biology, 23 , pp. 2430–2433, 2013. Abstract | Links | BibTeX @article{Deffieux2013,
title = {Low-intensity focused ultrasound modulates monkey visuomotor behavior},
author = {Thomas Deffieux and Youliana Younan and Nicolas Wattiez and Mickael Tanter and Pierre Pouget and Jean Fran{ç}ois Aubry},
url = {http://dx.doi.org/10.1016/j.cub.2013.10.029},
doi = {10.1016/j.cub.2013.10.029},
year = {2013},
date = {2013-01-01},
journal = {Current Biology},
volume = {23},
pages = {2430--2433},
abstract = {In vivo feasibility of using low-intensity focused ultrasound (FUS) to transiently modulate the function of regional brain tissue has been recently tested in anesthetized lagomorphs [1] and rodents [2-4]. Hypothetically, ultrasonic stimulation of the brain possesses several advantages [5]: it does not necessitate surgery or genetic alteration but could ultimately confer spatial resolutions superior to other noninvasive methods. Here, we gauged the ability of noninvasive FUS to causally modulate high-level cognitive behavior. Therefore, we examined how FUS might interfere with prefrontal activity in two awake macaque rhesus monkeys that had been trained to perform an antisaccade (AS) task. We show that ultrasound significantly modulated AS latencies. Such effects proved to be dependent on FUS hemifield of stimulation (relative latency increases most for ipsilateral AS). These results are interpreted in terms of a modulation of saccade inhibition to the contralateral visual field due to the disruption of processing across the frontal eye fields. Our study demonstrates for the first time the feasibility of using FUS stimulation to causally modulate behavior in the awake nonhuman primate brain. This result supports the use of this approach to study brain function. Neurostimulation with ultrasound could be used for exploratory and therapeutic purposes noninvasively, with potentially unprecedented spatial resolution.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
In vivo feasibility of using low-intensity focused ultrasound (FUS) to transiently modulate the function of regional brain tissue has been recently tested in anesthetized lagomorphs [1] and rodents [2-4]. Hypothetically, ultrasonic stimulation of the brain possesses several advantages [5]: it does not necessitate surgery or genetic alteration but could ultimately confer spatial resolutions superior to other noninvasive methods. Here, we gauged the ability of noninvasive FUS to causally modulate high-level cognitive behavior. Therefore, we examined how FUS might interfere with prefrontal activity in two awake macaque rhesus monkeys that had been trained to perform an antisaccade (AS) task. We show that ultrasound significantly modulated AS latencies. Such effects proved to be dependent on FUS hemifield of stimulation (relative latency increases most for ipsilateral AS). These results are interpreted in terms of a modulation of saccade inhibition to the contralateral visual field due to the disruption of processing across the frontal eye fields. Our study demonstrates for the first time the feasibility of using FUS stimulation to causally modulate behavior in the awake nonhuman primate brain. This result supports the use of this approach to study brain function. Neurostimulation with ultrasound could be used for exploratory and therapeutic purposes noninvasively, with potentially unprecedented spatial resolution. |
T M Desrochers; D Z Jin; N D Goodman; A M Graybiel Optimal habits can develop spontaneously through sensitivity to local cost Journal Article Proceedings of the National Academy of Sciences, 107 (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 A M Graybiel},
url = {http://www.pnas.org/cgi/doi/10.1073/pnas.1013470107},
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}
}
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. |
Nicholas K DeWind; Jiyun Peng; Andrew Luo; Elizabeth M Brannon; Michael L Platt Pharmacological inactivation does not support a unique causal role for intraparietal sulcus in the discrimination of visual number Journal Article PLoS ONE, 12 (12), pp. 1–23, 2017. Abstract | Links | BibTeX @article{DeWind2017,
title = {Pharmacological inactivation does not support a unique causal role for intraparietal sulcus in the discrimination of visual number},
author = {Nicholas K DeWind and Jiyun Peng and Andrew Luo and Elizabeth M Brannon and Michael L Platt},
doi = {10.1371/journal.pone.0188820},
year = {2017},
date = {2017-01-01},
journal = {PLoS ONE},
volume = {12},
number = {12},
pages = {1--23},
abstract = {The "number sense" describes the intuitive ability to quantify without counting. Single neu-ron recordings in non-human primates and functional imaging in humans suggest the intra-parietal sulcus is an important neuroanatomical locus of numerical estimation. Other lines of inquiry implicate the IPS in numerous other functions, including attention and decision mak-ing. Here we provide a direct test of whether IPS has functional specificity for numerosity judgments. We used muscimol to reversibly and independently inactivate the ventral and lat-eral intraparietal areas in two monkeys performing a numerical discrimination task and a color discrimination task, roughly equilibrated for difficulty. Inactivation of either area caused parallel impairments in both tasks and no evidence of a selective deficit in numerical pro-cessing. These findings do not support a causal role for the IPS in numerical discrimination, except insofar as it also has a role in the discrimination of color. We discuss our findings in light of several alternative hypotheses of IPS function, including a role in orienting responses, a general cognitive role in attention and decision making processes and a more specific role in ordinal comparison that encompasses both number and color judgments.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
The "number sense" describes the intuitive ability to quantify without counting. Single neu-ron recordings in non-human primates and functional imaging in humans suggest the intra-parietal sulcus is an important neuroanatomical locus of numerical estimation. Other lines of inquiry implicate the IPS in numerous other functions, including attention and decision mak-ing. Here we provide a direct test of whether IPS has functional specificity for numerosity judgments. We used muscimol to reversibly and independently inactivate the ventral and lat-eral intraparietal areas in two monkeys performing a numerical discrimination task and a color discrimination task, roughly equilibrated for difficulty. Inactivation of either area caused parallel impairments in both tasks and no evidence of a selective deficit in numerical pro-cessing. These findings do not support a causal role for the IPS in numerical discrimination, except insofar as it also has a role in the discrimination of color. We discuss our findings in light of several alternative hypotheses of IPS function, including a role in orienting responses, a general cognitive role in attention and decision making processes and a more specific role in ordinal comparison that encompasses both number and color judgments. |
Kacie Dougherty; Michele A Cox; Taihei Ninomiya; David A Leopold; Alexander Maier Ongoing alpha activity in V1 regulates visually driven spiking responses Journal Article Cerebral Cortex, 27 (2), pp. 1113–1124, 2017. Abstract | Links | BibTeX @article{Dougherty2017,
title = {Ongoing alpha activity in V1 regulates visually driven spiking responses},
author = {Kacie Dougherty and Michele A Cox and Taihei Ninomiya and David A Leopold and Alexander Maier},
doi = {10.1093/cercor/bhv304},
year = {2017},
date = {2017-01-01},
journal = {Cerebral Cortex},
volume = {27},
number = {2},
pages = {1113--1124},
abstract = {The interlaminar connections in the primate primary visual cortex (V1) are well described, as is the presence of ongoing alpha-range (7-14 Hz) fluctuations in this area. Less well understood is how these interlaminar connections and ongoing fluctuations contribute to the regulation of visual spiking responses. Here, we investigate the relationship between alpha fluctuations and spiking responses to visual stimuli across cortical layers. Using laminar probes in macaque V1, we show that neural firing couples with the phase of alpha fluctuations, and that magnitude of this coupling is particularly pronounced during visual stimulation. The strongest modulation of spiking activity was observed in layers 2/3. Alpha-spike coupling and current source density analysis pointed to an infragranular origin of the alpha fluctuations. Taken together, these results indicate that ongoing infragranular alpha-range fluctuations in V1 play a role in regulating columnar visual activity.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
The interlaminar connections in the primate primary visual cortex (V1) are well described, as is the presence of ongoing alpha-range (7-14 Hz) fluctuations in this area. Less well understood is how these interlaminar connections and ongoing fluctuations contribute to the regulation of visual spiking responses. Here, we investigate the relationship between alpha fluctuations and spiking responses to visual stimuli across cortical layers. Using laminar probes in macaque V1, we show that neural firing couples with the phase of alpha fluctuations, and that magnitude of this coupling is particularly pronounced during visual stimulation. The strongest modulation of spiking activity was observed in layers 2/3. Alpha-spike coupling and current source density analysis pointed to an infragranular origin of the alpha fluctuations. Taken together, these results indicate that ongoing infragranular alpha-range fluctuations in V1 play a role in regulating columnar visual activity. |
Ilse Van C Dromme; Elsie Premereur; Bram-Ernst Verhoef; Wim Vanduffel Posterior parietal cortex drives inferotemporal activations during three- dimensional object vision Journal Article PloS Biology, 14 (4), pp. 1–26, 2016. Abstract | Links | BibTeX @article{Dromme2016,
title = {Posterior parietal cortex drives inferotemporal activations during three- dimensional object vision},
author = {Ilse Van C Dromme and Elsie Premereur and Bram-Ernst Verhoef and Wim Vanduffel},
doi = {10.1371/journal.pbio.1002445},
year = {2016},
date = {2016-01-01},
journal = {PloS Biology},
volume = {14},
number = {4},
pages = {1--26},
abstract = {The primate visual system consists of a ventral stream, specialized for object recognition, and a dorsal visual stream, which is crucial for spatial vision and actions. However, little is known about the interactions and information flow between these two streams. We investigated these interactions within the network processing three-dimensional (3D) object information, comprising both the dorsal and ventral stream. Reversible inactivation of the macaque caudal intraparietal area (CIP) during functional magnetic resonance imaging (fMRI) reduced fMRI activations in posterior parietal cortex in the dorsal stream and, surprisingly, also in the inferotemporal cortex (ITC) in the ventral visual stream. Moreover, CIP inactivation caused a perceptual deficit in a depth-structure categorization task. CIP-micro-stimulation during fMRI further suggests that CIP projects via posterior parietal areas to the ITC in the ventral stream. To our knowledge, these results provide the first causal evidence for the flow of visual 3D information from the dorsal stream to the ventral stream, and identify CIP as a key area for depth-structure processing. Thus, combining reversible inactivation and electrical microstimulation during fMRI provides a detailed view of the functional interactions between the two visual processing streams.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
The primate visual system consists of a ventral stream, specialized for object recognition, and a dorsal visual stream, which is crucial for spatial vision and actions. However, little is known about the interactions and information flow between these two streams. We investigated these interactions within the network processing three-dimensional (3D) object information, comprising both the dorsal and ventral stream. Reversible inactivation of the macaque caudal intraparietal area (CIP) during functional magnetic resonance imaging (fMRI) reduced fMRI activations in posterior parietal cortex in the dorsal stream and, surprisingly, also in the inferotemporal cortex (ITC) in the ventral visual stream. Moreover, CIP inactivation caused a perceptual deficit in a depth-structure categorization task. CIP-micro-stimulation during fMRI further suggests that CIP projects via posterior parietal areas to the ITC in the ventral stream. To our knowledge, these results provide the first causal evidence for the flow of visual 3D information from the dorsal stream to the ventral stream, and identify CIP as a key area for depth-structure processing. Thus, combining reversible inactivation and electrical microstimulation during fMRI provides a detailed view of the functional interactions between the two visual processing streams. |
Caroline B Drucker; Monica L Carlson; Koji Toda; Nicholas K DeWind; Michael L Platt Non-invasive primate head restraint using thermoplastic masks. Journal Article Journal of Neuroscience Methods, 253 , pp. 90–100, 2015. Abstract | Links | BibTeX @article{Drucker2015,
title = {Non-invasive primate head restraint using thermoplastic masks.},
author = {Caroline B Drucker and Monica L Carlson and Koji Toda and Nicholas K DeWind and Michael L Platt},
url = {http://www.sciencedirect.com/science/article/pii/S0165027015002307},
doi = {10.1016/j.jneumeth.2015.06.013},
year = {2015},
date = {2015-01-01},
journal = {Journal of Neuroscience Methods},
volume = {253},
pages = {90--100},
publisher = {Elsevier B.V.},
abstract = {Background: The success of many neuroscientific studies depends upon adequate head fixation of awake, behaving animals. Typically, this is achieved by surgically affixing a head-restraint prosthesis to the skull. New Method: Here we report the use of thermoplastic masks to non-invasively restrain monkeys' heads. Mesh thermoplastic sheets become pliable when heated and can then be molded to an individual monkey's head. After cooling, the custom mask retains this shape indefinitely for day-to-day use. Results: We successfully trained rhesus macaques (Macaca mulatta) to perform cognitive tasks while wearing thermoplastic masks. Using these masks, we achieved a level of head stability sufficient for high-resolution eye-tracking and intracranial electrophysiology. Comparison with Existing Method: Compared with traditional head-posts, we find that thermoplastic masks perform at least as well during infrared eye-tracking and single-neuron recordings, allow for clearer magnetic resonance image acquisition, enable freer placement of a transcranial magnetic stimulation coil, and impose lower financial and time costs on the lab.Conclusions: We conclude that thermoplastic masks are a viable non-invasive form of primate head restraint that enable a wide range of neuroscientific experiments.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Background: The success of many neuroscientific studies depends upon adequate head fixation of awake, behaving animals. Typically, this is achieved by surgically affixing a head-restraint prosthesis to the skull. New Method: Here we report the use of thermoplastic masks to non-invasively restrain monkeys' heads. Mesh thermoplastic sheets become pliable when heated and can then be molded to an individual monkey's head. After cooling, the custom mask retains this shape indefinitely for day-to-day use. Results: We successfully trained rhesus macaques (Macaca mulatta) to perform cognitive tasks while wearing thermoplastic masks. Using these masks, we achieved a level of head stability sufficient for high-resolution eye-tracking and intracranial electrophysiology. Comparison with Existing Method: Compared with traditional head-posts, we find that thermoplastic masks perform at least as well during infrared eye-tracking and single-neuron recordings, allow for clearer magnetic resonance image acquisition, enable freer placement of a transcranial magnetic stimulation coil, and impose lower financial and time costs on the lab.Conclusions: We conclude that thermoplastic masks are a viable non-invasive form of primate head restraint that enable a wide range of neuroscientific experiments. |
Jacob Duijnhouwer; Bart Krekelberg Evidence and counterevidence in motion perception Journal Article Cerebral Cortex, 26 , pp. 4602–4612, 2016. Abstract | Links | BibTeX @article{Duijnhouwer2016,
title = {Evidence and counterevidence in motion perception},
author = {Jacob Duijnhouwer and Bart Krekelberg},
doi = {10.1093/cercor/bhw221},
year = {2016},
date = {2016-01-01},
journal = {Cerebral Cortex},
volume = {26},
pages = {4602--4612},
abstract = {Sensory neurons gather evidence in favor ofthe specific stimuli to which they are tuned, but they could improve their sensitivity by also taking counterevidence into account. The Bours–Lankheet model for motion detection uses counterevidence that relies on a specific combination ofthe ON and OFF channels in the early visual system. Specifically, the model detects pairs offlashes that occur separated in space and time. Ifthe flashes have the same contrast polarity, they are interpreted as evidence in favorof the corresponding motion. But if they have opposite contrasts, they are interpreted as evidence against it. This mechanism provides an explanation for reverse-phi (the perceived reversal of an apparent motion stimulus due to periodic contrast-inversions) that is a conceptual departure from the standard explanations of the effect. Here, we investigate this counterevidence mechanism by measuring directional tuning curves of neurons in the primary visual and middle temporal cortex areas of awake, behaving macaques using constant-contrast and inverting-contrast moving dot stimuli. Our electrophysiological data support the Bours–Lankheet model and suggest that the counterevidence computation occurs at an early stage of neural processing not captured by the standard models.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Sensory neurons gather evidence in favor ofthe specific stimuli to which they are tuned, but they could improve their sensitivity by also taking counterevidence into account. The Bours–Lankheet model for motion detection uses counterevidence that relies on a specific combination ofthe ON and OFF channels in the early visual system. Specifically, the model detects pairs offlashes that occur separated in space and time. Ifthe flashes have the same contrast polarity, they are interpreted as evidence in favorof the corresponding motion. But if they have opposite contrasts, they are interpreted as evidence against it. This mechanism provides an explanation for reverse-phi (the perceived reversal of an apparent motion stimulus due to periodic contrast-inversions) that is a conceptual departure from the standard explanations of the effect. Here, we investigate this counterevidence mechanism by measuring directional tuning curves of neurons in the primary visual and middle temporal cortex areas of awake, behaving macaques using constant-contrast and inverting-contrast moving dot stimuli. Our electrophysiological data support the Bours–Lankheet model and suggest that the counterevidence computation occurs at an early stage of neural processing not captured by the standard models. |
S L Eagleman; V Dragoi Image sequence reactivation in awake V4 networks Journal Article Proceedings of the National Academy of Sciences, 109 (47), pp. 19450–19455, 2012. Abstract | Links | BibTeX @article{Eagleman2012,
title = {Image sequence reactivation in awake V4 networks},
author = {S L Eagleman and V Dragoi},
url = {http://www.pnas.org/cgi/doi/10.1073/pnas.1212059109},
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}
}
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. |
Becket R Ebitz; Karli K Watson; Michael L Platt Oxytocin blunts social vigilance in the rhesus macaque Journal Article Proceedings of the National Academy of Sciences, 110 (28), pp. 11630–11635, 2013. Abstract | Links | BibTeX @article{Ebitz2013,
title = {Oxytocin blunts social vigilance in the rhesus macaque},
author = {Becket R Ebitz and Karli K Watson and Michael L Platt},
url = {http://www.pnas.org/cgi/doi/10.1073/pnas.1305230110},
doi = {10.1073/pnas.1305230110},
year = {2013},
date = {2013-01-01},
journal = {Proceedings of the National Academy of Sciences},
volume = {110},
number = {28},
pages = {11630--11635},
abstract = {Exogenous application of the neuromodulatory hormone oxytocin (OT) promotes prosocial behavior and can improve social function. It is unclear, however, whether OT promotes prosocial behavior per se, or whether it facilitates social interaction by reducing a state of vigilance toward potential social threats. To disambiguate these two possibilities, we exogenously delivered OT to male rhesus macaques, which have a characteristic pattern of species-typical social vigilance, and examined their performance in three social attention tasks. We first determined that, in the absence of competing task demands or goals, OT increased attention to faces and eyes, as in humans. By contrast, OT reduced species typical social vigilance for unfamiliar, dominant, and emotional faces in two additional tasks. OT eliminated the emergence of a typical state of vigilance when dominant face images were available during a social image choice task. Moreover, OT improved performance on a reward-guided saccade task, despite salient social distractors: OT reduced the interference of unfamiliar faces, particularly emotional ones, when these faces were task irrelevant. Together, these results demonstrate that OT suppresses vigilance toward potential social threats in the rhesus macaque. We hypothesize that a basic role for OT in regulating social vigilance may have facilitated the evolution of prosocial behaviors in humans.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Exogenous application of the neuromodulatory hormone oxytocin (OT) promotes prosocial behavior and can improve social function. It is unclear, however, whether OT promotes prosocial behavior per se, or whether it facilitates social interaction by reducing a state of vigilance toward potential social threats. To disambiguate these two possibilities, we exogenously delivered OT to male rhesus macaques, which have a characteristic pattern of species-typical social vigilance, and examined their performance in three social attention tasks. We first determined that, in the absence of competing task demands or goals, OT increased attention to faces and eyes, as in humans. By contrast, OT reduced species typical social vigilance for unfamiliar, dominant, and emotional faces in two additional tasks. OT eliminated the emergence of a typical state of vigilance when dominant face images were available during a social image choice task. Moreover, OT improved performance on a reward-guided saccade task, despite salient social distractors: OT reduced the interference of unfamiliar faces, particularly emotional ones, when these faces were task irrelevant. Together, these results demonstrate that OT suppresses vigilance toward potential social threats in the rhesus macaque. We hypothesize that a basic role for OT in regulating social vigilance may have facilitated the evolution of prosocial behaviors in humans. |
Becket R Ebitz; John M Pearson; Michael L Platt Pupil size and social vigilance in rhesus macaques Journal Article Frontiers in Neuroscience, 8 (8 MAY), pp. 1–13, 2014. Abstract | Links | BibTeX @article{Ebitz2014,
title = {Pupil size and social vigilance in rhesus macaques},
author = {Becket R Ebitz and John M Pearson and Michael L Platt},
doi = {10.3389/fnins.2014.00100},
year = {2014},
date = {2014-01-01},
journal = {Frontiers in Neuroscience},
volume = {8},
number = {8 MAY},
pages = {1--13},
abstract = {Complex natural environments favor the dynamic alignment of neural processing between goal-relevant stimuli and conflicting but biologically salient stimuli like social competitors or predators. The biological mechanisms that regulate dynamic changes in vigilance have not been fully elucidated. Arousal systems that ready the body to respond adaptively to threat may contribute to dynamic regulation of vigilance. Under conditions of constant luminance, pupil diameter provides a peripheral index of arousal state. Although pupil size varies with the processing of goal-relevant stimuli, it remains unclear whether pupil size also predicts attention to biologically salient objects and events like social competitors, whose presence interferes with current goals. Here we show that pupil size in rhesus macaques both reflects the biological salience of task-irrelevant social distractors and predicts vigilance for these stimuli. We measured pupil size in monkeys performing a visual orienting task in which distractors-monkey faces and phase-scrambled versions of the same images-could appear in a congruent, incongruent, or neutral position relative to a rewarded target. Baseline pupil size under constant illumination predicted distractor interference, consistent with the hypothesis that pupil-linked arousal mechanisms regulate task engagement and distractibility. Notably, pupil size also predicted enhanced vigilance for social distractors, suggesting that pupil-linked arousal may adjust the balance of processing resources between goal-relevant and biologically important stimuli. The magnitude of pupil constriction in response to distractors closely tracked distractor interference, saccade planning and the social relevance of distractors, endorsing the idea that the pupillary light response is modulated by attention. These findings indicate that pupil size indexes dynamic changes in attention evoked by both the social environment and arousal.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Complex natural environments favor the dynamic alignment of neural processing between goal-relevant stimuli and conflicting but biologically salient stimuli like social competitors or predators. The biological mechanisms that regulate dynamic changes in vigilance have not been fully elucidated. Arousal systems that ready the body to respond adaptively to threat may contribute to dynamic regulation of vigilance. Under conditions of constant luminance, pupil diameter provides a peripheral index of arousal state. Although pupil size varies with the processing of goal-relevant stimuli, it remains unclear whether pupil size also predicts attention to biologically salient objects and events like social competitors, whose presence interferes with current goals. Here we show that pupil size in rhesus macaques both reflects the biological salience of task-irrelevant social distractors and predicts vigilance for these stimuli. We measured pupil size in monkeys performing a visual orienting task in which distractors-monkey faces and phase-scrambled versions of the same images-could appear in a congruent, incongruent, or neutral position relative to a rewarded target. Baseline pupil size under constant illumination predicted distractor interference, consistent with the hypothesis that pupil-linked arousal mechanisms regulate task engagement and distractibility. Notably, pupil size also predicted enhanced vigilance for social distractors, suggesting that pupil-linked arousal may adjust the balance of processing resources between goal-relevant and biologically important stimuli. The magnitude of pupil constriction in response to distractors closely tracked distractor interference, saccade planning and the social relevance of distractors, endorsing the idea that the pupillary light response is modulated by attention. These findings indicate that pupil size indexes dynamic changes in attention evoked by both the social environment and arousal. |
Becket R Ebitz; Michael L Platt Neuronal activity in primate dorsal anterior cingulate cortex signals Task conflict and predicts adjustments in pupil-linked arousal Journal Article Neuron, 85 (3), pp. 628–640, 2015. Abstract | Links | BibTeX @article{Ebitz2015,
title = {Neuronal activity in primate dorsal anterior cingulate cortex signals Task conflict and predicts adjustments in pupil-linked arousal},
author = {Becket R Ebitz and Michael L Platt},
url = {http://dx.doi.org/10.1016/j.neuron.2014.12.053},
doi = {10.1016/j.neuron.2014.12.053},
year = {2015},
date = {2015-01-01},
journal = {Neuron},
volume = {85},
number = {3},
pages = {628--640},
publisher = {Elsevier Inc.},
abstract = {Whether driving a car, shopping for food, or paying attention in a classroom of boisterous teenagers, it's often hard to maintain focus on goals in theface of distraction. Brain imaging studies in humans implicate the dorsal anterior cingulate cortex (dACC) in regulating the conflict between goals and distractors. Here we show that single dACC neurons signal conflict between task goals and distractors in the rhesus macaque, particularly for biologically relevant social stimuli. For some neurons, task conflict signals predicted subsequent changes in pupil size-a peripheral index of arousal linked to noradrenergic tone-associated with reduced distractor interference. dACC neurons also responded to errors, and these signals predicted adjustments in pupil size. These findings provide the first neurophysiological endorsement of the hypothesis that dACC regulates conflict, in part, via modulation of pupil-linked processes such as arousal.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Whether driving a car, shopping for food, or paying attention in a classroom of boisterous teenagers, it's often hard to maintain focus on goals in theface of distraction. Brain imaging studies in humans implicate the dorsal anterior cingulate cortex (dACC) in regulating the conflict between goals and distractors. Here we show that single dACC neurons signal conflict between task goals and distractors in the rhesus macaque, particularly for biologically relevant social stimuli. For some neurons, task conflict signals predicted subsequent changes in pupil size-a peripheral index of arousal linked to noradrenergic tone-associated with reduced distractor interference. dACC neurons also responded to errors, and these signals predicted adjustments in pupil size. These findings provide the first neurophysiological endorsement of the hypothesis that dACC regulates conflict, in part, via modulation of pupil-linked processes such as arousal. |
Becket R Ebitz; Tirin Moore Selective modulation of the pupil light reflex by microstimulation of prefrontal cortex Journal Article Journal of Neuroscience, 37 (19), pp. 5008–5018, 2017. Abstract | Links | BibTeX @article{Ebitz2017,
title = {Selective modulation of the pupil light reflex by microstimulation of prefrontal cortex},
author = {Becket R Ebitz and Tirin Moore},
url = {http://www.jneurosci.org/lookup/doi/10.1523/JNEUROSCI.2433-16.2017},
doi = {10.1523/JNEUROSCI.2433-16.2017},
year = {2017},
date = {2017-01-01},
journal = {Journal of Neuroscience},
volume = {37},
number = {19},
pages = {5008--5018},
abstract = {The prefrontal cortex (PFC) is thought to flexibly regulate sensorimotor responses, perhaps through modulating activity in other circuits. However, the scope of that control remains unknown: it remains unclear whether the PFC can modulate basic reflexes. One canonical example of a central reflex is the pupil light reflex (PLR): the automatic constriction of the pupil in response to luminance increments. Unlike pupil size, which depends on the interaction of multiple physiological and neuromodulatory influences, the PLR reflects the action of a simple brainstem circuit. However, emerging behavioral evidence suggests that the PLR may be modulated by cognitive processes. Although the neural basis of these modulations remains unknown, one possible source is the PFC, particularly the frontal eye field (FEF), an area of the PFC implicated in the control of attention. We show that microstimulation of the rhesus macaque FEF alters the magnitude of the PLR in a spatially specific manner. FEF microstimulation enhanced the PLR to probes presented within the stimulated visual field, but suppressed the PLR to probes at nonoverlapping locations. The spatial specificity of this effect parallels the effect of FEF stimulation on attention and suggests that FEF is capable of modulating visuomotor transformations performed at a lower level than was previously known. These results provide evidence of the selective regulation of a basic brainstem reflex by the PFC.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
The prefrontal cortex (PFC) is thought to flexibly regulate sensorimotor responses, perhaps through modulating activity in other circuits. However, the scope of that control remains unknown: it remains unclear whether the PFC can modulate basic reflexes. One canonical example of a central reflex is the pupil light reflex (PLR): the automatic constriction of the pupil in response to luminance increments. Unlike pupil size, which depends on the interaction of multiple physiological and neuromodulatory influences, the PLR reflects the action of a simple brainstem circuit. However, emerging behavioral evidence suggests that the PLR may be modulated by cognitive processes. Although the neural basis of these modulations remains unknown, one possible source is the PFC, particularly the frontal eye field (FEF), an area of the PFC implicated in the control of attention. We show that microstimulation of the rhesus macaque FEF alters the magnitude of the PLR in a spatially specific manner. FEF microstimulation enhanced the PLR to probes presented within the stimulated visual field, but suppressed the PLR to probes at nonoverlapping locations. The spatial specificity of this effect parallels the effect of FEF stimulation on attention and suggests that FEF is capable of modulating visuomotor transformations performed at a lower level than was previously known. These results provide evidence of the selective regulation of a basic brainstem reflex by the PFC. |
Yasmine El-Shamayleh; Anitha Pasupathy Contour curvature as an invariant code for objects in visual area V4 Journal Article Journal of Neuroscience, 36 (20), pp. 5532–5543, 2016. Abstract | Links | BibTeX @article{El-Shamayleh2016,
title = {Contour curvature as an invariant code for objects in visual area V4},
author = {Yasmine El-Shamayleh and Anitha Pasupathy},
url = {http://www.jneurosci.org/cgi/doi/10.1523/JNEUROSCI.4139-15.2016},
doi = {10.1523/JNEUROSCI.4139-15.2016},
year = {2016},
date = {2016-01-01},
journal = {Journal of Neuroscience},
volume = {36},
number = {20},
pages = {5532--5543},
abstract = {Size-invariant object recognition-the ability to recognize objects across transformations of scale-is a fundamental feature of biological and artificial vision. To investigate its basis in the primate cerebral cortex, we measured single neuron responses to stimuli of varying size in visual area V4, a cornerstone of the object-processing pathway, in rhesus monkeys (Macaca mulatta). Leveraging two competing models for how neuronal selectivity for the bounding contours of objects may depend on stimulus size, we show that most V4 neurons (∼70%) encode objects in a size-invariant manner, consistent with selectivity for a size-independent parameter of boundary form: for these neurons, "normalized" curvature, rather than "absolute" curvature, provided a better account of responses. Our results demonstrate the suitability of contour curvature as a basis for size-invariant object representation in the visual cortex, and posit V4 as a foundation for behaviorally relevant object codes.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Size-invariant object recognition-the ability to recognize objects across transformations of scale-is a fundamental feature of biological and artificial vision. To investigate its basis in the primate cerebral cortex, we measured single neuron responses to stimuli of varying size in visual area V4, a cornerstone of the object-processing pathway, in rhesus monkeys (Macaca mulatta). Leveraging two competing models for how neuronal selectivity for the bounding contours of objects may depend on stimulus size, we show that most V4 neurons (∼70%) encode objects in a size-invariant manner, consistent with selectivity for a size-independent parameter of boundary form: for these neurons, "normalized" curvature, rather than "absolute" curvature, provided a better account of responses. Our results demonstrate the suitability of contour curvature as a basis for size-invariant object representation in the visual cortex, and posit V4 as a foundation for behaviorally relevant object codes. |
Sarah J Fairhall; Carol A Dickson; Leah Scott; Peter C Pearce A non-invasive method for studying an index of pupil diameter and visual performance in the rhesus monkey Journal Article Journal of Medical Primatology, 35 (2), pp. 67–77, 2006. Abstract | Links | BibTeX @article{Fairhall2006,
title = {A non-invasive method for studying an index of pupil diameter and visual performance in the rhesus monkey},
author = {Sarah J Fairhall and Carol A Dickson and Leah Scott and Peter C Pearce},
doi = {10.1111/j.1600-0684.2005.00135.x},
year = {2006},
date = {2006-01-01},
journal = {Journal of Medical Primatology},
volume = {35},
number = {2},
pages = {67--77},
abstract = {BACKGROUND: A non-invasive model has been developed to estimate gaze direction and relative pupil diameter, in minimally restrained rhesus monkeys, to investigate the effects of low doses of ocularly administered cholinergic compounds on visual performance. METHODS: Animals were trained to co-operate with a novel device, which enabled eye movements to be recorded using modified human eye-tracking equipment, and to perform a task which determined visual threshold contrast. Responses were made by gaze transfer under twilight conditions. 4% w/v pilocarpine nitrate was studied to demonstrate the suitability of the model. RESULTS: Pilocarpine induced marked miosis for textgreater3 h which was accompanied by a decrement in task performance. CONCLUSIONS: The method obviates the need for invasive surgery and, as the position of point of gaze can be approximately defined, the approach may have utility in other areas of research involving non-human primates.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
BACKGROUND: A non-invasive model has been developed to estimate gaze direction and relative pupil diameter, in minimally restrained rhesus monkeys, to investigate the effects of low doses of ocularly administered cholinergic compounds on visual performance. METHODS: Animals were trained to co-operate with a novel device, which enabled eye movements to be recorded using modified human eye-tracking equipment, and to perform a task which determined visual threshold contrast. Responses were made by gaze transfer under twilight conditions. 4% w/v pilocarpine nitrate was studied to demonstrate the suitability of the model. RESULTS: Pilocarpine induced marked miosis for textgreater3 h which was accompanied by a decrement in task performance. CONCLUSIONS: The method obviates the need for invasive surgery and, as the position of point of gaze can be approximately defined, the approach may have utility in other areas of research involving non-human primates. |
Hongwei Fan; Xiaochuan Pan; Rubin Wang; Masamichi Sakagami Differences in reward processing between putative cell types in primate prefrontal cortex Journal Article PLoS ONE, 12 (12), pp. 1–27, 2017. Abstract | Links | BibTeX @article{Fan2017,
title = {Differences in reward processing between putative cell types in primate prefrontal cortex},
author = {Hongwei Fan and Xiaochuan Pan and Rubin Wang and Masamichi Sakagami},
doi = {10.1371/journal.pone.0189771},
year = {2017},
date = {2017-01-01},
journal = {PLoS ONE},
volume = {12},
number = {12},
pages = {1--27},
abstract = {Single-unit studies in monkeys have demonstrated that neurons in the prefrontal cortex predict the reward type, reward amount or reward availability associated with a stimulus. To examine contributions of pyramidal cells and interneurons in reward processing, single-unit activity was extracellularly recorded in prefrontal cortices of four monkeys performing a reward prediction task. Based on their shapes of spike waveforms, prefrontal neurons were classified into broad-spike and narrow-spike units that represented putative pyramidal cells and interneurons, respectively. We mainly observed that narrow-spike neurons showed higher firing rates but less bursty discharges than did broad-spike neurons. Both narrow-spike and broad-spike cells selectively responded to the stimulus, reward and their interaction, and the proportions of each type of selective neurons were similar between the two cell classes. Moreover, the two types of cells displayed equal reliability of reward or stimulus discrimination. Furthermore, we found that broad-spike and narrow-spike cells showed distinct mechanisms for encoding reward or stimulus information. Broad-spike neurons raised their firing rate relative to the baseline rate to represent the preferred reward or stimulus information, whereas narrow-spike neurons inhibited their firing rate lower than the baseline rate to encode the non-preferred reward or stimulus information. Our results suggest that narrow-spike and broad-spike cells were equally involved in reward and stimulus processing in the prefrontal cortex. They utilized a binary strategy to complementarily represent reward or stimulus information, which was consistent with the task structure in which the monkeys were required to remember two reward conditions and two visual stimuli.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Single-unit studies in monkeys have demonstrated that neurons in the prefrontal cortex predict the reward type, reward amount or reward availability associated with a stimulus. To examine contributions of pyramidal cells and interneurons in reward processing, single-unit activity was extracellularly recorded in prefrontal cortices of four monkeys performing a reward prediction task. Based on their shapes of spike waveforms, prefrontal neurons were classified into broad-spike and narrow-spike units that represented putative pyramidal cells and interneurons, respectively. We mainly observed that narrow-spike neurons showed higher firing rates but less bursty discharges than did broad-spike neurons. Both narrow-spike and broad-spike cells selectively responded to the stimulus, reward and their interaction, and the proportions of each type of selective neurons were similar between the two cell classes. Moreover, the two types of cells displayed equal reliability of reward or stimulus discrimination. Furthermore, we found that broad-spike and narrow-spike cells showed distinct mechanisms for encoding reward or stimulus information. Broad-spike neurons raised their firing rate relative to the baseline rate to represent the preferred reward or stimulus information, whereas narrow-spike neurons inhibited their firing rate lower than the baseline rate to encode the non-preferred reward or stimulus information. Our results suggest that narrow-spike and broad-spike cells were equally involved in reward and stimulus processing in the prefrontal cortex. They utilized a binary strategy to complementarily represent reward or stimulus information, which was consistent with the task structure in which the monkeys were required to remember two reward conditions and two visual stimuli. |
Jose A Fernandez-Leon; Bryan J Hansen; Valentin Dragoi Representation of rapid image sequences in V4 Networks Journal Article Cerebral Cortex, 28 (8), pp. 2675–2684, 2018. Abstract | Links | BibTeX @article{Fernandez-Leon2018,
title = {Representation of rapid image sequences in V4 Networks},
author = {Jose A Fernandez-Leon and Bryan J Hansen and Valentin Dragoi},
doi = {10.1093/cercor/bhx146},
year = {2018},
date = {2018-01-01},
journal = {Cerebral Cortex},
volume = {28},
number = {8},
pages = {2675--2684},
abstract = {Natural viewing often consists of sequences of brief fixations to image patches of different structure. Whether and how briefly presented sequential stimuli are encoded in a temporal-position manner is poorly understood. Here, we performed multiple-electrode recordings in the visual cortex (area V4) of nonhuman primates (Macaca mulatta) viewing a sequence of 7 briefly flashed natural images, and measured correlations between the cue-triggered population response in the presence and absence of the stimulus. Surprisingly, we found significant correlations for images occurring at the beginning and the end of a sequence, but not for those in the middle. The correlation strength increased with stimulus exposure and favored the image position in the sequence rather than image identity. These results challenge the commonly held view that images are represented in visual cortex exclusively based on their informational content, and indicate that, in the absence of sensory information, neuronal populations exhibit reactivation of stimulus-evoked responses in a way that reflects temporal position within a stimulus sequence.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Natural viewing often consists of sequences of brief fixations to image patches of different structure. Whether and how briefly presented sequential stimuli are encoded in a temporal-position manner is poorly understood. Here, we performed multiple-electrode recordings in the visual cortex (area V4) of nonhuman primates (Macaca mulatta) viewing a sequence of 7 briefly flashed natural images, and measured correlations between the cue-triggered population response in the presence and absence of the stimulus. Surprisingly, we found significant correlations for images occurring at the beginning and the end of a sequence, but not for those in the middle. The correlation strength increased with stimulus exposure and favored the image position in the sequence rather than image identity. These results challenge the commonly held view that images are represented in visual cortex exclusively based on their informational content, and indicate that, in the absence of sensory information, neuronal populations exhibit reactivation of stimulus-evoked responses in a way that reflects temporal position within a stimulus sequence. |
C D Fiorillo Transient activation of midbrain dopamine neurons by reward risk Journal Article Neuroscience, 197 , pp. 162–171, 2011. Abstract | Links | BibTeX @article{Fiorillo2011,
title = {Transient activation of midbrain dopamine neurons by reward risk},
author = {C D Fiorillo},
url = {http://dx.doi.org/10.1016/j.neuroscience.2011.09.037},
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}
}
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. |
Christopher D Fiorillo; Minryung R Song; Sora R Yun Multiphasic temporal dynamics in responses of midbrain dopamine neurons to appetitive and aversive stimuli Journal Article Journal of Neuroscience, 33 (11), pp. 4710–4725, 2013. Abstract | Links | BibTeX @article{Fiorillo2013,
title = {Multiphasic temporal dynamics in responses of midbrain dopamine neurons to appetitive and aversive stimuli},
author = {Christopher D Fiorillo and Minryung R Song and Sora R Yun},
url = {http://www.jneurosci.org/cgi/doi/10.1523/JNEUROSCI.3883-12.2013},
doi = {10.1523/JNEUROSCI.3883-12.2013},
year = {2013},
date = {2013-01-01},
journal = {Journal of Neuroscience},
volume = {33},
number = {11},
pages = {4710--4725},
abstract = {The transient response of dopamine neurons has been described as reward prediction error (RPE), with activation or suppression by events that are better or worse than expected, respectively. However, at least a minority of neurons are activated by aversive or high-intensity stimuli, casting doubt on the generality of RPE in describing the dopamine signal. To overcome limitations of previous studies, we studied neuronal responses to a wider variety of high-intensity and aversive stimuli, and we quantified and controlled aversiveness through a choice task in which macaques sacrificed juice to avoid aversive stimuli. Whereas most previous work has portrayed the RPE as a single impulse or "phase," here we demonstrate its multiphasic temporal dynamics. Aversive or high-intensity stimuli evoked a triphasic sequence of activation-suppression-activation extending over a period of 40-700 ms. The initial activation at short latencies (40-120 ms) reflected sensory intensity. The influence of motivational value became dominant between 150 and 250 ms, with activation in the case of appetitive stimuli, and suppression in the case of aversive and neutral stimuli. The previously unreported late activation appeared to be a modest "rebound" after strong suppression. Similarly, strong activation by reward was often followed by suppression. We suggest that these "rebounds" may result from overcompensation by homeostatic mechanisms in some cells. Our results are consistent with a realistic RPE, which evolves over time through a dynamic balance of excitation and inhibition.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
The transient response of dopamine neurons has been described as reward prediction error (RPE), with activation or suppression by events that are better or worse than expected, respectively. However, at least a minority of neurons are activated by aversive or high-intensity stimuli, casting doubt on the generality of RPE in describing the dopamine signal. To overcome limitations of previous studies, we studied neuronal responses to a wider variety of high-intensity and aversive stimuli, and we quantified and controlled aversiveness through a choice task in which macaques sacrificed juice to avoid aversive stimuli. Whereas most previous work has portrayed the RPE as a single impulse or "phase," here we demonstrate its multiphasic temporal dynamics. Aversive or high-intensity stimuli evoked a triphasic sequence of activation-suppression-activation extending over a period of 40-700 ms. The initial activation at short latencies (40-120 ms) reflected sensory intensity. The influence of motivational value became dominant between 150 and 250 ms, with activation in the case of appetitive stimuli, and suppression in the case of aversive and neutral stimuli. The previously unreported late activation appeared to be a modest "rebound" after strong suppression. Similarly, strong activation by reward was often followed by suppression. We suggest that these "rebounds" may result from overcompensation by homeostatic mechanisms in some cells. Our results are consistent with a realistic RPE, which evolves over time through a dynamic balance of excitation and inhibition. |
Christopher D Fiorillo; Sora R Yun; Minryung R Song Diversity and homogeneity in responses of midbrain dopamine neurons Journal Article Journal of Neuroscience, 33 (11), pp. 4693–4709, 2013. Abstract | Links | BibTeX @article{Fiorillo2013a,
title = {Diversity and homogeneity in responses of midbrain dopamine neurons},
author = {Christopher D Fiorillo and Sora R Yun and Minryung R Song},
url = {http://www.jneurosci.org/cgi/doi/10.1523/JNEUROSCI.3886-12.2013},
doi = {10.1523/JNEUROSCI.3886-12.2013},
year = {2013},
date = {2013-01-01},
journal = {Journal of Neuroscience},
volume = {33},
number = {11},
pages = {4693--4709},
abstract = {Dopamine neurons of the ventral midbrain have been found to signal a reward prediction error that can mediate positive reinforcement. Despite the demonstration of modest diversity at the cellular and molecular levels, there has been little analysis of response diversity in behaving animals. Here we examine response diversity in rhesus macaques to appetitive, aversive, and neutral stimuli having relative motivational values that were measured and controlled through a choice task. First, consistent with previous studies, we observed a continuum of response variability and an apparent absence of distinct clusters in scatter plots, suggesting a lack of statistically discrete subpopulations of neurons. Second, we found that a group of " sensitive " neurons tend to be more strongly suppressed by a variety of stimuli and to be more strongly activated by juice. Third, neurons in the " ventral tier " of substantia nigra were found to have greater suppression, and a subset of these had higher baseline firing rates and late " rebound " activation after suppression. These neurons could belong to a previously identified subgroup of dopamine neurons that express high levels of H-type cation channels but lack calbindin. Fourth, neurons further rostral exhibited greater suppression. Fifth, although we observed weak activation of some neurons by aversive stimuli, this was not associated with their aversiveness. In conclusion, we find a diversity of response properties, distributed along a continuum, within what may be a single functional population of neurons signaling reward prediction error.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Dopamine neurons of the ventral midbrain have been found to signal a reward prediction error that can mediate positive reinforcement. Despite the demonstration of modest diversity at the cellular and molecular levels, there has been little analysis of response diversity in behaving animals. Here we examine response diversity in rhesus macaques to appetitive, aversive, and neutral stimuli having relative motivational values that were measured and controlled through a choice task. First, consistent with previous studies, we observed a continuum of response variability and an apparent absence of distinct clusters in scatter plots, suggesting a lack of statistically discrete subpopulations of neurons. Second, we found that a group of " sensitive " neurons tend to be more strongly suppressed by a variety of stimuli and to be more strongly activated by juice. Third, neurons in the " ventral tier " of substantia nigra were found to have greater suppression, and a subset of these had higher baseline firing rates and late " rebound " activation after suppression. These neurons could belong to a previously identified subgroup of dopamine neurons that express high levels of H-type cation channels but lack calbindin. Fourth, neurons further rostral exhibited greater suppression. Fifth, although we observed weak activation of some neurons by aversive stimuli, this was not associated with their aversiveness. In conclusion, we find a diversity of response properties, distributed along a continuum, within what may be a single functional population of neurons signaling reward prediction error. |
K A Ford; S Everling Neural activity in primate caudate nucleus associated with pro- and antisaccades Journal Article Journal of Neurophysiology, 102 (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 S Everling},
url = {http://jn.physiology.org/cgi/doi/10.1152/jn.00125.2009},
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}
}
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. |
Amber M Fyall; Yasmine El-Shamayleh; Hannah Choi; Eric Shea-Brown; Anitha Pasupathy Dynamic representation of partially occluded objects in primate prefrontal and visual cortex Journal Article eLife, 6 , pp. 1–25, 2017. Abstract | Links | BibTeX @article{Fyall2017,
title = {Dynamic representation of partially occluded objects in primate prefrontal and visual cortex},
author = {Amber M Fyall and Yasmine El-Shamayleh and Hannah Choi and Eric Shea-Brown and Anitha Pasupathy},
url = {https://doi.org/10.7554/eLife.25784.001},
doi = {10.7554/eLife.25784},
year = {2017},
date = {2017-01-01},
journal = {eLife},
volume = {6},
pages = {1--25},
abstract = {Successful recognition of partially occluded objects is presumed to involve dynamic interactions between brain areas responsible for vision and cognition, but neurophysiological evidence for the involvement of feedback signals is lacking. Here, we demonstrate that neurons in the ventrolateral prefrontal cortex (vlPFC) of monkeys performing a shape discrimination task respond more strongly to occluded than unoccluded stimuli. In contrast, neurons in visual area V4 respond more strongly to unoccluded stimuli. Analyses of V4 response dynamics reveal that many neurons exhibit two transient response peaks, the second of which emerges after vlPFC response onset and displays stronger selectivity for occluded shapes. We replicate these findings using a model of V4/vlPFC interactions in which occlusion-sensitive vlPFC neurons feed back to shape- selective V4 neurons, thereby enhancing V4 responses and selectivity to occluded shapes. These results reveal how signals from frontal and visual cortex could interact to facilitate object recognition under occlusion.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Successful recognition of partially occluded objects is presumed to involve dynamic interactions between brain areas responsible for vision and cognition, but neurophysiological evidence for the involvement of feedback signals is lacking. Here, we demonstrate that neurons in the ventrolateral prefrontal cortex (vlPFC) of monkeys performing a shape discrimination task respond more strongly to occluded than unoccluded stimuli. In contrast, neurons in visual area V4 respond more strongly to unoccluded stimuli. Analyses of V4 response dynamics reveal that many neurons exhibit two transient response peaks, the second of which emerges after vlPFC response onset and displays stronger selectivity for occluded shapes. We replicate these findings using a model of V4/vlPFC interactions in which occlusion-sensitive vlPFC neurons feed back to shape- selective V4 neurons, thereby enhancing V4 responses and selectivity to occluded shapes. These results reveal how signals from frontal and visual cortex could interact to facilitate object recognition under occlusion. |
Ali Ghazizadeh; Whitney Griggs; Okihide Hikosaka Ecological origins of object salience: Reward, uncertainty, aversiveness, and novelty Journal Article Frontiers in Neuroscience, 10 , pp. 1–16, 2016. Abstract | Links | BibTeX @article{Ghazizadeh2016,
title = {Ecological origins of object salience: Reward, uncertainty, aversiveness, and novelty},
author = {Ali Ghazizadeh and Whitney Griggs and Okihide Hikosaka},
doi = {10.3389/fnins.2016.00378},
year = {2016},
date = {2016-01-01},
journal = {Frontiers in Neuroscience},
volume = {10},
pages = {1--16},
abstract = {Among many objects around us, some of them are more salient than others (i.e., attract our attention automatically). Some objects may be inherently salient (e.g., brighter), but others may become salient by virtue of their ecological relevance through experience. However, the importance of ecological experience in guiding attention has not been studied systematically. To address this question, we let subjects (macaque monkeys) view a large number of complex objects (textgreater300), each experienced repeatedly (textgreater5 days) with rewarding, aversive or no outcome association (mere-perceptual exposure). Test of salience was done on separate days using free viewing with no outcome. We found that gaze was biased among the objects from the outset, affecting saccades to objects or fixations within objects. When the outcome was rewarding, gaze preference was stronger (i.e. positive) for objects with larger or equal but uncertain rewards. The effects of aversive outcomes were variable. Gaze preference was positive for some outcome associations (e.g. airpuff), but negative for others (e.g. time-out), possibly due to differences in threat levels. Finally, novel objects attracted gaze, but mere perceptual exposure of objects reduced their salience (learned negative salience). Our results show that, in primates, object salience is strongly influenced by previous ecological experience and is supported by a large memory capacity. Owing to such learned salience, the capacity to rapidly choose important objects can grow during the entire life to promote biological fitness.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Among many objects around us, some of them are more salient than others (i.e., attract our attention automatically). Some objects may be inherently salient (e.g., brighter), but others may become salient by virtue of their ecological relevance through experience. However, the importance of ecological experience in guiding attention has not been studied systematically. To address this question, we let subjects (macaque monkeys) view a large number of complex objects (textgreater300), each experienced repeatedly (textgreater5 days) with rewarding, aversive or no outcome association (mere-perceptual exposure). Test of salience was done on separate days using free viewing with no outcome. We found that gaze was biased among the objects from the outset, affecting saccades to objects or fixations within objects. When the outcome was rewarding, gaze preference was stronger (i.e. positive) for objects with larger or equal but uncertain rewards. The effects of aversive outcomes were variable. Gaze preference was positive for some outcome associations (e.g. airpuff), but negative for others (e.g. time-out), possibly due to differences in threat levels. Finally, novel objects attracted gaze, but mere perceptual exposure of objects reduced their salience (learned negative salience). Our results show that, in primates, object salience is strongly influenced by previous ecological experience and is supported by a large memory capacity. Owing to such learned salience, the capacity to rapidly choose important objects can grow during the entire life to promote biological fitness. |
D M Glasser; James M G Tsui; Christopher C Pack; D Tadin Perceptual and neural consequences of rapid motion adaptation Journal Article Proceedings of the National Academy of Sciences, 108 (45), pp. E1080–E1088, 2011. Abstract | Links | BibTeX @article{Glasser2011,
title = {Perceptual and neural consequences of rapid motion adaptation},
author = {D M Glasser and James M G Tsui and Christopher C Pack and D Tadin},
url = {http://www.pnas.org/cgi/doi/10.1073/pnas.1101141108},
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}
}
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. |
David C Godlove; Alexander Maier; Geoffrey F Woodman; Jeffrey D Schall Microcircuitry of agranular frontal cortex: Testing the generality of the canonical cortical microcircuit Journal Article Journal of Neuroscience, 34 (15), pp. 5355–5369, 2014. Abstract | Links | BibTeX @article{Godlove2014,
title = {Microcircuitry of agranular frontal cortex: Testing the generality of the canonical cortical microcircuit},
author = {David C Godlove and Alexander Maier and Geoffrey F Woodman and Jeffrey D Schall},
url = {http://www.jneurosci.org/cgi/doi/10.1523/JNEUROSCI.5127-13.2014},
doi = {10.1523/JNEUROSCI.5127-13.2014},
year = {2014},
date = {2014-01-01},
journal = {Journal of Neuroscience},
volume = {34},
number = {15},
pages = {5355--5369},
abstract = {We investigated whether a frontal area that lacks granular layer IV, supplementary eye field, exhibits features of laminar circuitry similar to those observed in primary sensory areas. We report, for the first time, visually evoked local field potentials (LFPs) and spiking activity recorded simultaneously across all layers of agranular frontal cortex using linear electrode arrays. We calculated current source density from the LFPs and compared the laminar organization of evolving sinks to those reported in sensory areas. Simultaneous, transient synaptic current sinks appeared first in layers III and V followed by more prolonged current sinks in layers I/II and VI. We also found no variation of single- or multi-unit visual response latency across layers, and putative pyramidal neurons and interneurons displayed similar response latencies. Many units exhibited pronounced discharge suppression that was strongest in superficial relative to deep layers. Maximum discharge suppression also occurred later in superficial than in deep layers. These results are discussed in the context of the canonical cortical microcircuit model originally formulated to describe early sensory cortex. The data indicate that agranular cortex resembles sensory areas in certain respects, but the cortical microcircuit is modified in nontrivial ways.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
We investigated whether a frontal area that lacks granular layer IV, supplementary eye field, exhibits features of laminar circuitry similar to those observed in primary sensory areas. We report, for the first time, visually evoked local field potentials (LFPs) and spiking activity recorded simultaneously across all layers of agranular frontal cortex using linear electrode arrays. We calculated current source density from the LFPs and compared the laminar organization of evolving sinks to those reported in sensory areas. Simultaneous, transient synaptic current sinks appeared first in layers III and V followed by more prolonged current sinks in layers I/II and VI. We also found no variation of single- or multi-unit visual response latency across layers, and putative pyramidal neurons and interneurons displayed similar response latencies. Many units exhibited pronounced discharge suppression that was strongest in superficial relative to deep layers. Maximum discharge suppression also occurred later in superficial than in deep layers. These results are discussed in the context of the canonical cortical microcircuit model originally formulated to describe early sensory cortex. The data indicate that agranular cortex resembles sensory areas in certain respects, but the cortical microcircuit is modified in nontrivial ways. |
David C Godlove; Jeffrey D Schall Microsaccade production during saccade cancelation in a stop-signal task Journal Article Vision Research, 118 , pp. 5–16, 2016. Abstract | Links | BibTeX @article{Godlove2016,
title = {Microsaccade production during saccade cancelation in a stop-signal task},
author = {David C Godlove and Jeffrey D Schall},
url = {http://dx.doi.org/10.1016/j.visres.2014.10.025},
doi = {10.1016/j.visres.2014.10.025},
year = {2016},
date = {2016-01-01},
journal = {Vision Research},
volume = {118},
pages = {5--16},
publisher = {Elsevier Ltd},
abstract = {We obtained behavioral data to evaluate two alternative hypotheses about the neural mechanisms of gaze control. The "fixation" hypothesis states that neurons in rostral superior colliculus (SC) enforce fixation of gaze. The "microsaccade" hypothesis states that neurons in rostral SC encode microsaccades rather than fixation per se. Previously reported neuronal activity in monkey SC during the saccade stop-signal task leads to specific, dissociable behavioral predictions of these two hypotheses. When subjects are required to cancel partially-prepared saccades, imbalanced activity spreads across rostral and caudal SC with a reliable temporal profile. The microsaccade hypothesis predicts that this imbalance will lead to elevated microsaccade production biased toward the target location, while the fixation hypothesis predicts reduced microsaccade production. We tested these predictions by analyzing the microsaccades produced by 4 monkeys while they voluntarily canceled partially prepared eye movements in response to explicit stop signals. Consistent with the fixation hypothesis and contradicting the microsaccade hypothesis, we found that each subject produced significantly fewer microsaccades when normal saccades were successfully canceled. The few microsaccades escaping this inhibition tended to be directed toward the target location. We additionally investigated interactions between initiating microsaccades and inhibiting normal saccades. Reaction times were longer when microsaccades immediately preceded target presentation. However, pre-target microsaccade production did not affect stop-signal reaction time or alter the probability of canceling saccades following stop signals. These findings demonstrate that imbalanced activity within SC does not necessarily produce microsaccades and add to evidence that saccade preparation and cancelation are separate processes.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
We obtained behavioral data to evaluate two alternative hypotheses about the neural mechanisms of gaze control. The "fixation" hypothesis states that neurons in rostral superior colliculus (SC) enforce fixation of gaze. The "microsaccade" hypothesis states that neurons in rostral SC encode microsaccades rather than fixation per se. Previously reported neuronal activity in monkey SC during the saccade stop-signal task leads to specific, dissociable behavioral predictions of these two hypotheses. When subjects are required to cancel partially-prepared saccades, imbalanced activity spreads across rostral and caudal SC with a reliable temporal profile. The microsaccade hypothesis predicts that this imbalance will lead to elevated microsaccade production biased toward the target location, while the fixation hypothesis predicts reduced microsaccade production. We tested these predictions by analyzing the microsaccades produced by 4 monkeys while they voluntarily canceled partially prepared eye movements in response to explicit stop signals. Consistent with the fixation hypothesis and contradicting the microsaccade hypothesis, we found that each subject produced significantly fewer microsaccades when normal saccades were successfully canceled. The few microsaccades escaping this inhibition tended to be directed toward the target location. We additionally investigated interactions between initiating microsaccades and inhibiting normal saccades. Reaction times were longer when microsaccades immediately preceded target presentation. However, pre-target microsaccade production did not affect stop-signal reaction time or alter the probability of canceling saccades following stop signals. These findings demonstrate that imbalanced activity within SC does not necessarily produce microsaccades and add to evidence that saccade preparation and cancelation are separate processes. |
Samanthi C Goonetilleke; Leor Katz; Daniel K Wood; Chao Gu; Alexander C Huk; Brian D Corneil Cross-species comparison of anticipatory and stimulus-driven neck muscle activity well before saccadic gaze shifts in humans and nonhuman primates Journal Article Journal of Neurophysiology, 114 (2), pp. 902–913, 2015. Abstract | Links | BibTeX @article{Goonetilleke2015,
title = {Cross-species comparison of anticipatory and stimulus-driven neck muscle activity well before saccadic gaze shifts in humans and nonhuman primates},
author = {Samanthi C Goonetilleke and Leor Katz and Daniel K Wood and Chao Gu and Alexander C Huk and Brian D Corneil},
url = {http://jn.physiology.org/lookup/doi/10.1152/jn.00230.2015},
doi = {10.1152/jn.00230.2015},
year = {2015},
date = {2015-01-01},
journal = {Journal of Neurophysiology},
volume = {114},
number = {2},
pages = {902--913},
abstract = {Recent studies have described a phenomenon wherein the onset of a peripheral visual stimulus elicits short-latency (textless100 ms) stimulus-locked recruitment (SLR) of neck muscles in nonhuman primates (NHPs), well before any saccadic gaze shift. The SLR is thought to arise from visual responses within the intermediate layers of the superior colliculus (SCi), hence neck muscle recordings may reflect presaccadic activity within the SCi, even in humans. We obtained bilateral intramuscular recordings from splenius capitis (SPL, an ipsilateral head-turning muscle) from 28 human subjects performing leftward or rightward visually guided eye-head gaze shifts. Evidence of an SLR was obtained in 16/55 (29%) of samples; we also observed examples where the SLR was present only unilaterally. We compared these human results with those recorded from a sample of eight NHPs from which recordings of both SPL and deeper suboccipital muscles were available. Using the same criteria, evidence of an SLR was obtained in 8/14 (57%) of SPL recordings, but in 26/29 (90%) of recordings from suboccipital muscles. Thus, both species-specific and muscle- specific factors contribute to the low SLR prevalence in human SPL. Regardless of the presence of the SLR, neck muscle activity in both human SPL and in NHPs became predictive of the reaction time of the ensuing saccade gaze shift ~70 ms after target appearance; such pregaze recruitment likely reflects developing SCi activity, even if the tectoreticulospinal pathway does not reliably relay visually related activity to SPL in humans.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Recent studies have described a phenomenon wherein the onset of a peripheral visual stimulus elicits short-latency (textless100 ms) stimulus-locked recruitment (SLR) of neck muscles in nonhuman primates (NHPs), well before any saccadic gaze shift. The SLR is thought to arise from visual responses within the intermediate layers of the superior colliculus (SCi), hence neck muscle recordings may reflect presaccadic activity within the SCi, even in humans. We obtained bilateral intramuscular recordings from splenius capitis (SPL, an ipsilateral head-turning muscle) from 28 human subjects performing leftward or rightward visually guided eye-head gaze shifts. Evidence of an SLR was obtained in 16/55 (29%) of samples; we also observed examples where the SLR was present only unilaterally. We compared these human results with those recorded from a sample of eight NHPs from which recordings of both SPL and deeper suboccipital muscles were available. Using the same criteria, evidence of an SLR was obtained in 8/14 (57%) of SPL recordings, but in 26/29 (90%) of recordings from suboccipital muscles. Thus, both species-specific and muscle- specific factors contribute to the low SLR prevalence in human SPL. Regardless of the presence of the SLR, neck muscle activity in both human SPL and in NHPs became predictive of the reaction time of the ensuing saccade gaze shift ~70 ms after target appearance; such pregaze recruitment likely reflects developing SCi activity, even if the tectoreticulospinal pathway does not reliably relay visually related activity to SPL in humans. |
Arnulf B A Graf; Richard A Andersen Inferring eye position from populations of lateral intraparietal neurons Journal Article eLife, 2014 (3), pp. 1–13, 2014. Abstract | Links | BibTeX @article{Graf2014,
title = {Inferring eye position from populations of lateral intraparietal neurons},
author = {Arnulf B A Graf and Richard A Andersen},
doi = {10.7554/eLife.02813},
year = {2014},
date = {2014-01-01},
journal = {eLife},
volume = {2014},
number = {3},
pages = {1--13},
abstract = {Understanding how the brain computes eye position is essential to unraveling high- level visual functions such as eye movement planning, coordinate transformations and stability of spatial awareness. The lateral intraparietal area (LIP) is essential for this process. However, despite decades of research, its contribution to the eye position signal remains controversial. LIP neurons have recently been reported to inaccurately represent eye position during a saccadic eye movement, and to be too slow to support a role in high-level visual functions. We addressed this issue by predicting eye position and saccade direction from the responses of populations of LIP neurons. We found that both signals were accurately predicted before, during and after a saccade. Also, the dynamics of these signals support their contribution to visual functions. These findings provide a principled understanding of the coding of information in populations of neurons within an important node of the cortical network for visual-motor behaviors.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Understanding how the brain computes eye position is essential to unraveling high- level visual functions such as eye movement planning, coordinate transformations and stability of spatial awareness. The lateral intraparietal area (LIP) is essential for this process. However, despite decades of research, its contribution to the eye position signal remains controversial. LIP neurons have recently been reported to inaccurately represent eye position during a saccadic eye movement, and to be too slow to support a role in high-level visual functions. We addressed this issue by predicting eye position and saccade direction from the responses of populations of LIP neurons. We found that both signals were accurately predicted before, during and after a saccade. Also, the dynamics of these signals support their contribution to visual functions. These findings provide a principled understanding of the coding of information in populations of neurons within an important node of the cortical network for visual-motor behaviors. |
Diego A Gutnisky; Charles B Beaman; Sergio E Lew; Valentin Dragoi Spontaneous fluctuations in visual cortical responses influence population coding accuracy Journal Article Cerebral Cortex, 27 (2), pp. 1409–1427, 2017. Abstract | Links | BibTeX @article{Gutnisky2017a,
title = {Spontaneous fluctuations in visual cortical responses influence population coding accuracy},
author = {Diego A Gutnisky and Charles B Beaman and Sergio E Lew and Valentin Dragoi},
doi = {10.1093/cercor/bhv312},
year = {2017},
date = {2017-01-01},
journal = {Cerebral Cortex},
volume = {27},
number = {2},
pages = {1409--1427},
abstract = {Information processing in the cerebral cortex depends not only on the nature of incoming stimuli, but also on the state of neuronal networks at the time of stimulation. That is, the same stimulus will be processed differently depending on the neuronal context in which it is received. A major factor that could influence neuronal context is the background, or ongoing neuronal activity before stimulation. In visual cortex, ongoing activity is known to play a critical role in the development of local circuits, yet whether it influences the coding of visual features in adult cortex is unclear. Here, we investigate whether and how the information encoded by individual neurons and populations in primary visual cortex (V1) depends on the ongoing activity before stimulus presentation. We report that when individual neurons are in a "low" prestimulus state, they have a higher capacity to discriminate stimulus features, such as orientation, despite their reduction in evoked responses. By measuring the distribution of prestimulus activity across a population of neurons, we found that network discrimination accuracy is improved in the low prestimulus state. Thus, the distribution of ongoing activity states across the network creates an "internal context" that dynamically filters incoming stimuli to modulate the accuracy of sensory coding. The modulation of stimulus coding by ongoing activity state is consistent with recurrent network models in which ongoing activity dynamically controls the balanced background excitation and inhibition to individual neurons.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}
Information processing in the cerebral cortex depends not only on the nature of incoming stimuli, but also on the state of neuronal networks at the time of stimulation. That is, the same stimulus will be processed differently depending on the neuronal context in which it is received. A major factor that could influence neuronal context is the background, or ongoing neuronal activity before stimulation. In visual cortex, ongoing activity is known to play a critical role in the development of local circuits, yet whether it influences the coding of visual features in adult cortex is unclear. Here, we investigate whether and how the information encoded by individual neurons and populations in primary visual cortex (V1) depends on the ongoing activity before stimulus presentation. We report that when individual neurons are in a "low" prestimulus state, they have a higher capacity to discriminate stimulus features, such as orientation, despite their reduction in evoked responses. By measuring the distribution of prestimulus activity across a population of neurons, we found that network discrimination accuracy is improved in the low prestimulus state. Thus, the distribution of ongoing activity states across the network creates an "internal context" that dynamically filters incoming stimuli to modulate the accuracy of sensory coding. The modulation of stimulus coding by ongoing activity state is consistent with recurrent network models in which ongoing activity dynamically controls the balanced background excitation and inhibition to individual neurons. |
