EyeLink Non-Human Primate Publications
All EyeLink non-human primate research publications up until 2019 (with some early 2020s) are listed below by year. You can search the publications using key words such as Temporal Cortex, Macaque, Antisaccade, etc. You can also search for individual author names. If we missed any EyeLink non-human primate article, please email us!
All EyeLink non-human primatee publications are also available for download / import into reference management software as a single Bibtex (.bib) file.
2018 |
Kevin D Johnston; Kevin Barker; David Schaeffer; Lauren Schaeffer; Stefan Everling Methods for chair restraint and training of the common marmoset on oculomotor tasks Journal Article Journal of Neurophysiology, 119 (5), pp. 1636–1646, 2018. @article{Johnston2018, title = {Methods for chair restraint and training of the common marmoset on oculomotor tasks}, author = {Kevin D Johnston and Kevin Barker and David Schaeffer and Lauren Schaeffer and Stefan Everling}, doi = {10.1152/jn.00866.2017}, year = {2018}, date = {2018-01-01}, journal = {Journal of Neurophysiology}, volume = {119}, number = {5}, pages = {1636--1646}, abstract = {The oculomotor system is the most thoroughly understood sensorimotor system in the brain, due in large part to electrophysiological studies carried out in macaque monkeys trained to perform oculomotor tasks. A disadvantage of the macaque model is that many cortical oculomotor areas of interest lie within sulci, making high-density array and laminar recordings impractical. Many techniques of molecular biology developed in rodents, such as optogenetic manipulation of neuronal subtypes, are also limited in this species. The common marmoset (Callithrix jacchus) possesses a smooth cortex, allowing easy access to frontoparietal oculomotor areas, and may bridge the gap between systems neuroscience in macaques and molecular techniques. Techniques for restraint, training, and neural recording in these animals have been well developed in auditory neuroscience. Those for oculomotor neuroscience, however, remain at a relatively early stage. In this article we provide details of a custom-designed restraint chair for marmosets, a combination head restraint/recording chamber allowing access to cortical oculomotor areas and providing stability suitable for eye movement and neural recordings, as well as a training protocol for oculomotor tasks. We additionally report the results of a psychophysical study in marmosets trained to perform a saccade task using these methods, showing that, as in rhesus and humans, marmosets exhibit a “gap effect,” a decrease in reaction time when the fixation stimulus is removed before the onset of a visual saccade target. These results are the first evidence of this effect in marmosets and support the common marmoset model for neurophysiological investigations of oculomotor control.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The oculomotor system is the most thoroughly understood sensorimotor system in the brain, due in large part to electrophysiological studies carried out in macaque monkeys trained to perform oculomotor tasks. A disadvantage of the macaque model is that many cortical oculomotor areas of interest lie within sulci, making high-density array and laminar recordings impractical. Many techniques of molecular biology developed in rodents, such as optogenetic manipulation of neuronal subtypes, are also limited in this species. The common marmoset (Callithrix jacchus) possesses a smooth cortex, allowing easy access to frontoparietal oculomotor areas, and may bridge the gap between systems neuroscience in macaques and molecular techniques. Techniques for restraint, training, and neural recording in these animals have been well developed in auditory neuroscience. Those for oculomotor neuroscience, however, remain at a relatively early stage. In this article we provide details of a custom-designed restraint chair for marmosets, a combination head restraint/recording chamber allowing access to cortical oculomotor areas and providing stability suitable for eye movement and neural recordings, as well as a training protocol for oculomotor tasks. We additionally report the results of a psychophysical study in marmosets trained to perform a saccade task using these methods, showing that, as in rhesus and humans, marmosets exhibit a “gap effect,” a decrease in reaction time when the fixation stimulus is removed before the onset of a visual saccade target. These results are the first evidence of this effect in marmosets and support the common marmoset model for neurophysiological investigations of oculomotor control. |
Peter Kaposvari; Susheel Kumar; Rufin Vogels Statistical learning signals in macaque inferior temporal cortex Journal Article Cerebral Cortex, 28 (1), pp. 250–266, 2018. @article{Kaposvari2018, title = {Statistical learning signals in macaque inferior temporal cortex}, author = {Peter Kaposvari and Susheel Kumar and Rufin Vogels}, doi = {10.1093/cercor/bhw374}, year = {2018}, date = {2018-01-01}, journal = {Cerebral Cortex}, volume = {28}, number = {1}, pages = {250--266}, abstract = {Humans are sensitive to statistical regularities in their visual environment, but the nature of the underlying neural statistical learning signals still remains to be clarified. As in human behavioral and neuroimaging studies of statistical learning, we exposed rhesus monkeys to a continuous stream of images, presented without interstimulus interval or reward association. The stimulus set consisted of 3 groups of 5 images each (quintets). The stimulus order within each quintet was fixed, but the quintets were presented repeatedly in a random order without interruption. Thus, only transitional probabilities defined quintets of images. Postexposure recordings in inferior temporal (IT) cortex showed an enhanced response to stimuli that violated the exposed sequence. This enhancement was found only for stimuli that were not predicted by the just preceding stimulus, reflecting a temporally adjacent stimulus relationship, and was sensitive to stimulus order. By comparing IT responses with sequences with and without statistical regularities, we observed a short latency, transient response suppression for stimuli of the sequence with regularities, in addition to a later sustained response enhancement to stimuli that violated the sequence with regularities. These findings constrain models of mechanisms underlying neural responses in predictable temporal sequences, such as predictive coding.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Humans are sensitive to statistical regularities in their visual environment, but the nature of the underlying neural statistical learning signals still remains to be clarified. As in human behavioral and neuroimaging studies of statistical learning, we exposed rhesus monkeys to a continuous stream of images, presented without interstimulus interval or reward association. The stimulus set consisted of 3 groups of 5 images each (quintets). The stimulus order within each quintet was fixed, but the quintets were presented repeatedly in a random order without interruption. Thus, only transitional probabilities defined quintets of images. Postexposure recordings in inferior temporal (IT) cortex showed an enhanced response to stimuli that violated the exposed sequence. This enhancement was found only for stimuli that were not predicted by the just preceding stimulus, reflecting a temporally adjacent stimulus relationship, and was sensitive to stimulus order. By comparing IT responses with sequences with and without statistical regularities, we observed a short latency, transient response suppression for stimuli of the sequence with regularities, in addition to a later sustained response enhancement to stimuli that violated the sequence with regularities. These findings constrain models of mechanisms underlying neural responses in predictable temporal sequences, such as predictive coding. |
Katsuhisa Kawaguchi; Stephane Clery; Paria Pourriahi; Lenka Seillier; Ralf M Haefner; Hendrikje Nienborg Differentiating between models of perceptual decision making using pupil size inferred confidence Journal Article The Journal of Neuroscience, 38 (41), pp. 8874–8888, 2018. @article{Kawaguchi2018, title = {Differentiating between models of perceptual decision making using pupil size inferred confidence}, author = {Katsuhisa Kawaguchi and Stephane Clery and Paria Pourriahi and Lenka Seillier and Ralf M Haefner and Hendrikje Nienborg}, doi = {10.1523/jneurosci.0735-18.2018}, year = {2018}, date = {2018-01-01}, journal = {The Journal of Neuroscience}, volume = {38}, number = {41}, pages = {8874--8888}, abstract = {During perceptual decisions, subjects often rely more strongly on early, rather than late, sensory evidence, even in tasks when both are equally informative about the correct decision. This early psychophysical weighting has been explained by an integration-to-bound decision process, in which the stimulus is ignored after the accumulated evidence reaches a certain bound, or confidence level. Here, we derive predictions about how the average temporal weighting of the evidence depends on a subject's decision confidence in this model. To test these predictions empirically, we devised a method to infer decision confidence from pupil size in 2 male monkeys performing a disparity discrimination task. Our animals' data confirmed the integration-to-bound predictions, with different internal decision bounds and different levels of correlation between pupil size and decision confidence accounting for differences between animals. However, the data were less compatible with two alternative accounts for early psychophysical weighting: attractor dynamics either within the decision area or due to feedback to sensory areas, or a feedforward account due to neuronal response adaptation. This approach also opens the door to using confidence more broadly when studying the neural basis of decision making.}, keywords = {}, pubstate = {published}, tppubtype = {article} } During perceptual decisions, subjects often rely more strongly on early, rather than late, sensory evidence, even in tasks when both are equally informative about the correct decision. This early psychophysical weighting has been explained by an integration-to-bound decision process, in which the stimulus is ignored after the accumulated evidence reaches a certain bound, or confidence level. Here, we derive predictions about how the average temporal weighting of the evidence depends on a subject's decision confidence in this model. To test these predictions empirically, we devised a method to infer decision confidence from pupil size in 2 male monkeys performing a disparity discrimination task. Our animals' data confirmed the integration-to-bound predictions, with different internal decision bounds and different levels of correlation between pupil size and decision confidence accounting for differences between animals. However, the data were less compatible with two alternative accounts for early psychophysical weighting: attractor dynamics either within the decision area or due to feedback to sensory areas, or a feedforward account due to neuronal response adaptation. This approach also opens the door to using confidence more broadly when studying the neural basis of decision making. |
Jonas Knöll; Jonathan W Pillow; Alexander C Huk Lawful tracking of visual motion in humans, macaques, and marmosets in a naturalistic, continuous, and untrained behavioral context Journal Article Proceedings of the National Academy of Sciences, 115 (44), pp. E10486–E10494, 2018. @article{Knoell2018, title = {Lawful tracking of visual motion in humans, macaques, and marmosets in a naturalistic, continuous, and untrained behavioral context}, author = {Jonas Knöll and Jonathan W Pillow and Alexander C Huk}, doi = {10.1073/pnas.1807192115}, year = {2018}, date = {2018-01-01}, journal = {Proceedings of the National Academy of Sciences}, volume = {115}, number = {44}, pages = {E10486--E10494}, abstract = {Much study of the visual system has focused on how humans and monkeys integrate moving stimuli over space and time. Such assessments of spatiotemporal integration provide fundamental grounding for the interpretation of neurophysiological data, as well as how the resulting neural signals support perceptual deci- sions and behavior. However, the insights supported by classical characterizations of integration performed in humans and rhesus monkeys are potentially limited with respect to both generality and detail: Standard tasks require extensive amounts of training, involve abstract stimulus–response mappings, and depend on combining data across many trials and/or sessions. It is thus of concern that the integration observed in classical tasks involves the recruitment of brain circuits that might not normally subsume natural behaviors, and that quantitative analyses have limited power for characterizing single-trial or single-session processes. Here we bridge these gaps by showing that three primate species (humans, macaques, and marmosets) track the focus of expansion of an optic flow field continuously and without substantial training. This flow-tracking behavior was volitional and reflected substantial temporal integration. Most strikingly, gaze patterns exhibited lawful and nuanced dependencies on random perturbations in the stimulus, such that repetitions of identical flow movies elicited remarkably similar eye movements over long and continuous time periods. These results demonstrate the generality of spatiotemporal integration in natural vision, and offer a means for studying integration outside of artificial tasks while maintaining lawful and highly reliable behavior.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Much study of the visual system has focused on how humans and monkeys integrate moving stimuli over space and time. Such assessments of spatiotemporal integration provide fundamental grounding for the interpretation of neurophysiological data, as well as how the resulting neural signals support perceptual deci- sions and behavior. However, the insights supported by classical characterizations of integration performed in humans and rhesus monkeys are potentially limited with respect to both generality and detail: Standard tasks require extensive amounts of training, involve abstract stimulus–response mappings, and depend on combining data across many trials and/or sessions. It is thus of concern that the integration observed in classical tasks involves the recruitment of brain circuits that might not normally subsume natural behaviors, and that quantitative analyses have limited power for characterizing single-trial or single-session processes. Here we bridge these gaps by showing that three primate species (humans, macaques, and marmosets) track the focus of expansion of an optic flow field continuously and without substantial training. This flow-tracking behavior was volitional and reflected substantial temporal integration. Most strikingly, gaze patterns exhibited lawful and nuanced dependencies on random perturbations in the stimulus, such that repetitions of identical flow movies elicited remarkably similar eye movements over long and continuous time periods. These results demonstrate the generality of spatiotemporal integration in natural vision, and offer a means for studying integration outside of artificial tasks while maintaining lawful and highly reliable behavior. |
Matthew L Leavitt; Florian Pieper; Adam J Sachs; Julio C Martinez-Trujillo A quadrantic bias in prefrontal representation of visual-mnemonic space Journal Article Cerebral Cortex, 28 , pp. 2405–2421, 2018. @article{Leavitt2018, title = {A quadrantic bias in prefrontal representation of visual-mnemonic space}, author = {Matthew L Leavitt and Florian Pieper and Adam J Sachs and Julio C Martinez-Trujillo}, doi = {10.1093/cercor/bhx142}, year = {2018}, date = {2018-01-01}, journal = {Cerebral Cortex}, volume = {28}, pages = {2405--2421}, abstract = {Single neurons in primate dorsolateral prefrontal cortex (dLPFC) are known to encode working memory (WM) representations of visual space. Psychophysical studies have shown that the horizontal and vertical meridians of the visual field can bias spatial information maintained in WM. However, most studies and models have tacitly assumed that dLPFC neurons represent mnemonic space homogenously. The anatomical organization of these representations has also eluded clear parametric description. We investigated these issues by recording from neuronal ensembles in macaque dLPFC with microelectrode arrays while subjects performed an oculomotor delayed-response task. We found that spatial WM representations in macaque dLPFC are biased by the vertical and horizontal meridians of the visual field, dividing mnemonic space into quadrants. This bias is reflected in single neuron firing rates, neuronal ensemble representations, the spike count correlation structure, and eye movement patterns. We also found that dLPFC representations of mnemonic space cluster anatomically in a nonretinotopic manner that partially reflects the organization of visual space. These results provide an explanation for known WM biases, and reveal novel principles of WM representation in prefrontal neuronal ensembles and across the cortical surface, as well as the need to reconceptualize models of WM to accommodate the observed representational biases.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Single neurons in primate dorsolateral prefrontal cortex (dLPFC) are known to encode working memory (WM) representations of visual space. Psychophysical studies have shown that the horizontal and vertical meridians of the visual field can bias spatial information maintained in WM. However, most studies and models have tacitly assumed that dLPFC neurons represent mnemonic space homogenously. The anatomical organization of these representations has also eluded clear parametric description. We investigated these issues by recording from neuronal ensembles in macaque dLPFC with microelectrode arrays while subjects performed an oculomotor delayed-response task. We found that spatial WM representations in macaque dLPFC are biased by the vertical and horizontal meridians of the visual field, dividing mnemonic space into quadrants. This bias is reflected in single neuron firing rates, neuronal ensemble representations, the spike count correlation structure, and eye movement patterns. We also found that dLPFC representations of mnemonic space cluster anatomically in a nonretinotopic manner that partially reflects the organization of visual space. These results provide an explanation for known WM biases, and reveal novel principles of WM representation in prefrontal neuronal ensembles and across the cortical surface, as well as the need to reconceptualize models of WM to accommodate the observed representational biases. |
Aaron J Levi; Jacob L Yates; Alexander C Huk; Leor N Katz Strategic and dynamic temporal weighting for perceptual decisions in humans and macaques Journal Article Eneuro, 5 (5), pp. 1–15, 2018. @article{Levi2018, title = {Strategic and dynamic temporal weighting for perceptual decisions in humans and macaques}, author = {Aaron J Levi and Jacob L Yates and Alexander C Huk and Leor N Katz}, doi = {10.1523/eneuro.0169-18.2018}, year = {2018}, date = {2018-01-01}, journal = {Eneuro}, volume = {5}, number = {5}, pages = {1--15}, abstract = {Perceptual decision-making is often modeled as the accumulation of sensory evidence over time. Recent studies using psychophysical reverse correlation have shown that even though the sensory evidence is stationary over time, subjects may exhibit a time-varying weighting strategy, weighting some stimulus epochs more heavily than others. While previous work has explained time-varying weighting as a consequence of static decision mechanisms (e.g., decision bound or leak), here we show that time-varying weighting can reflect strategic adaptation to stimulus statistics, and thus can readily take a number of forms. We characterized the temporal weighting strategies of humans and macaques performing a motion discrimination task in which the amount of information carried by the motion stimulus was manipulated over time. Both species could adapt their temporal weighting strategy to match the time-varying statistics of the sensory stimulus. When early stimulus epochs had higher mean motion strength than late, subjects adopted a pronounced early weighting strategy, where early information was weighted more heavily in guiding perceptual decisions. When the mean motion strength was greater in later stimulus epochs, in contrast, subjects shifted to a marked late weighting strategy. These results demonstrate that perceptual decisions involve a temporally flexible weighting process in both humans and monkeys, and introduce a paradigm with which to manipulate sensory weighting in decision-making tasks.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Perceptual decision-making is often modeled as the accumulation of sensory evidence over time. Recent studies using psychophysical reverse correlation have shown that even though the sensory evidence is stationary over time, subjects may exhibit a time-varying weighting strategy, weighting some stimulus epochs more heavily than others. While previous work has explained time-varying weighting as a consequence of static decision mechanisms (e.g., decision bound or leak), here we show that time-varying weighting can reflect strategic adaptation to stimulus statistics, and thus can readily take a number of forms. We characterized the temporal weighting strategies of humans and macaques performing a motion discrimination task in which the amount of information carried by the motion stimulus was manipulated over time. Both species could adapt their temporal weighting strategy to match the time-varying statistics of the sensory stimulus. When early stimulus epochs had higher mean motion strength than late, subjects adopted a pronounced early weighting strategy, where early information was weighted more heavily in guiding perceptual decisions. When the mean motion strength was greater in later stimulus epochs, in contrast, subjects shifted to a marked late weighting strategy. These results demonstrate that perceptual decisions involve a temporally flexible weighting process in both humans and monkeys, and introduce a paradigm with which to manipulate sensory weighting in decision-making tasks. |
Liu D Liu; Kenneth D Miller; Christopher C Pack A unifying motif for spatial and directional surround suppression Journal Article The Journal of Neuroscience, 38 (4), pp. 989–999, 2018. @article{Liu2018c, title = {A unifying motif for spatial and directional surround suppression}, author = {Liu D Liu and Kenneth D Miller and Christopher C Pack}, doi = {10.1523/jneurosci.2386-17.2017}, year = {2018}, date = {2018-01-01}, journal = {The Journal of Neuroscience}, volume = {38}, number = {4}, pages = {989--999}, abstract = {In the visual system, the response to a stimulus in a neuron's receptive field can be modulated by stimulus context, and the strength of these contextual influences vary with stimulus intensity. Recent work has shown how a theoretical model, the stabilized supralinear network (SSN), can account for such modulatory influences, using a small set of computational mechanisms. While the predictions of the SSN have been confirmed in primary visual cortex (V1), its computational principles apply with equal validity to any cortical structure. We have therefore tested the generality of the SSN by examining modulatory influences in the middle temporal area (MT) of the macaque visual cortex, using electrophysiological recordings and pharmacological manipulations. We developed a novel stimulus that can be adjusted parametrically to be larger or smaller in the space of all possible motion directions. We found, as predicted by the SSN, that MT neurons integrate across motion directions for low-contrast stimuli, but that they exhibit suppression by the same stimuli when they are high in contrast. These results are analogous to those found in visual cortex when stimulus size is varied in the space domain. We further tested the mechanisms of inhibition using pharmacologically manipulations of inhibitory efficacy. As predicted by the SSN, local manipulation of inhibitory strength altered firing rates, but did not change the strength of surround suppression. These results are consistent with the idea that the SSN can account for modulatory influences along different stimulus dimensions and in different cortical areas.}, keywords = {}, pubstate = {published}, tppubtype = {article} } In the visual system, the response to a stimulus in a neuron's receptive field can be modulated by stimulus context, and the strength of these contextual influences vary with stimulus intensity. Recent work has shown how a theoretical model, the stabilized supralinear network (SSN), can account for such modulatory influences, using a small set of computational mechanisms. While the predictions of the SSN have been confirmed in primary visual cortex (V1), its computational principles apply with equal validity to any cortical structure. We have therefore tested the generality of the SSN by examining modulatory influences in the middle temporal area (MT) of the macaque visual cortex, using electrophysiological recordings and pharmacological manipulations. We developed a novel stimulus that can be adjusted parametrically to be larger or smaller in the space of all possible motion directions. We found, as predicted by the SSN, that MT neurons integrate across motion directions for low-contrast stimuli, but that they exhibit suppression by the same stimuli when they are high in contrast. These results are analogous to those found in visual cortex when stimulus size is varied in the space domain. We further tested the mechanisms of inhibition using pharmacologically manipulations of inhibitory efficacy. As predicted by the SSN, local manipulation of inhibitory strength altered firing rates, but did not change the strength of surround suppression. These results are consistent with the idea that the SSN can account for modulatory influences along different stimulus dimensions and in different cortical areas. |
Kaleb A Lowe; Jeffrey D Schall Functional categories of visuomotor neurons in macaque frontal eye field Journal Article Eneuro, 5 (5), pp. 1–21, 2018. @article{Lowe2018, title = {Functional categories of visuomotor neurons in macaque frontal eye field}, author = {Kaleb A Lowe and Jeffrey D Schall}, doi = {10.1523/eneuro.0131-18.2018}, year = {2018}, date = {2018-01-01}, journal = {Eneuro}, volume = {5}, number = {5}, pages = {1--21}, abstract = {Frontal eye field (FEF) in macaque monkeys contributes to visual attention, visual-motor transformations and production of eye movements. Traditionally, neurons in FEF have been classified by the magnitude of increased discharge rates following visual stimulus presentation, during a waiting period, and associated with eye movement production. However, considerable heterogeneity remains within the traditional visual, visuomovement and movement categories. Cluster analysis is a data-driven method of identifying self-segregating groups within a dataset. Because many cluster analysis techniques exist and outcomes vary with analysis assumptions, consensus clustering aggregates over multiple analyses, identifying robust groups. To describe more comprehensively the neuronal composition of FEF, we applied a consensus clustering technique for unsupervised categorization of patterns of spike rate modulation measured during a memory-guided saccade task. We report ten functional categories, expanding on the traditional three. Categories were distinguished by latency, magnitude, and sign of visual response, presence of sustained activity, and dynamics, magnitude and sign of saccade-related modulation. Consensus clustering can include other metrics and can be applied to datasets from other brain regions to provide better information guiding microcircuit models of cortical function.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Frontal eye field (FEF) in macaque monkeys contributes to visual attention, visual-motor transformations and production of eye movements. Traditionally, neurons in FEF have been classified by the magnitude of increased discharge rates following visual stimulus presentation, during a waiting period, and associated with eye movement production. However, considerable heterogeneity remains within the traditional visual, visuomovement and movement categories. Cluster analysis is a data-driven method of identifying self-segregating groups within a dataset. Because many cluster analysis techniques exist and outcomes vary with analysis assumptions, consensus clustering aggregates over multiple analyses, identifying robust groups. To describe more comprehensively the neuronal composition of FEF, we applied a consensus clustering technique for unsupervised categorization of patterns of spike rate modulation measured during a memory-guided saccade task. We report ten functional categories, expanding on the traditional three. Categories were distinguished by latency, magnitude, and sign of visual response, presence of sustained activity, and dynamics, magnitude and sign of saccade-related modulation. Consensus clustering can include other metrics and can be applied to datasets from other brain regions to provide better information guiding microcircuit models of cortical function. |
Eric Lowet; Bruno Gomes; Karthik Srinivasan; Huihui Zhou; Robert John Schafer; Robert Desimone Enhanced neural processing by covert attention only during microsaccades directed toward the attended stimulus Journal Article Neuron, 99 (1), pp. 207–214, 2018. @article{Lowet2018, title = {Enhanced neural processing by covert attention only during microsaccades directed toward the attended stimulus}, author = {Eric Lowet and Bruno Gomes and Karthik Srinivasan and Huihui Zhou and Robert John Schafer and Robert Desimone}, doi = {10.1016/j.neuron.2018.05.041}, year = {2018}, date = {2018-01-01}, journal = {Neuron}, volume = {99}, number = {1}, pages = {207--214}, publisher = {Elsevier Inc.}, abstract = {Attention can be “covertly” directed without eye movements; yet, even during fixation, there are continuous microsaccades (MSs). In areas V4 and IT of macaques, we found that firing rates and stimulus representations were enhanced by attention but only following a MS toward the attended stimulus. The onset of neural attentional modulations was tightly coupled to the MS onset. The results reveal a major link between the effects of covert attention on cortical visual processing and the overt movement of the eyes.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Attention can be “covertly” directed without eye movements; yet, even during fixation, there are continuous microsaccades (MSs). In areas V4 and IT of macaques, we found that firing rates and stimulus representations were enhanced by attention but only following a MS toward the attended stimulus. The onset of neural attentional modulations was tightly coupled to the MS onset. The results reveal a major link between the effects of covert attention on cortical visual processing and the overt movement of the eyes. |
Yiliang Lu; Jiapeng Yin; Zheyuan Chen; Hongliang Gong; Ye Liu; Liling Qian; Xiaohong Li; Rui Liu; Ian Max Andolina; Wei Wang Revealing detail along the visual hierarchy: Neural clustering preserves acuity from V1 to V4 Journal Article Neuron, 98 (2), pp. 417–428, 2018. @article{Lu2018a, title = {Revealing detail along the visual hierarchy: Neural clustering preserves acuity from V1 to V4}, author = {Yiliang Lu and Jiapeng Yin and Zheyuan Chen and Hongliang Gong and Ye Liu and Liling Qian and Xiaohong Li and Rui Liu and Ian Max Andolina and Wei Wang}, doi = {10.1016/j.neuron.2018.03.009}, year = {2018}, date = {2018-01-01}, journal = {Neuron}, volume = {98}, number = {2}, pages = {417--428}, publisher = {Elsevier Inc.}, abstract = {How primates perceive objects along with their detailed features remains a mystery. This ability to make fine visual discriminations depends upon a high-acuity analysis of spatial frequency (SF) along the visual hierarchy from V1 to inferotemporal cortex. By studying the transformation of SF across macaque parafoveal V1, V2, and V4, we discovered SF-selective functional domains in V4 encoding higher SFs up to 12 cycles/°. These intermittent higher-SF-selective domains, surrounded by domains encoding lower SFs, violate the inverse relationship between SF preference and retinal eccentricity. The neural activities of higher- and lower-SF domains correspond to local and global features, respectively, of the same stimuli. Neural response latencies in high-SF domains are around 10 ms later than in low-SF domains, consistent with the coarse-to-fine nature of perception. Thus, our finding of preserved resolution from V1 into V4, separated both spatially and temporally, may serve as a connecting link for detailed object representation.}, keywords = {}, pubstate = {published}, tppubtype = {article} } How primates perceive objects along with their detailed features remains a mystery. This ability to make fine visual discriminations depends upon a high-acuity analysis of spatial frequency (SF) along the visual hierarchy from V1 to inferotemporal cortex. By studying the transformation of SF across macaque parafoveal V1, V2, and V4, we discovered SF-selective functional domains in V4 encoding higher SFs up to 12 cycles/°. These intermittent higher-SF-selective domains, surrounded by domains encoding lower SFs, violate the inverse relationship between SF preference and retinal eccentricity. The neural activities of higher- and lower-SF domains correspond to local and global features, respectively, of the same stimuli. Neural response latencies in high-SF domains are around 10 ms later than in low-SF domains, consistent with the coarse-to-fine nature of perception. Thus, our finding of preserved resolution from V1 into V4, separated both spatially and temporally, may serve as a connecting link for detailed object representation. |
Thomas Zhihao Luo; John H R Maunsell Attentional changes in either criterion or sensitivity are associated with robust modulations in lateral prefrontal cortex Journal Article Neuron, 97 (6), pp. 1382–1393, 2018. @article{Luo2018a, title = {Attentional changes in either criterion or sensitivity are associated with robust modulations in lateral prefrontal cortex}, author = {Thomas Zhihao Luo and John H R Maunsell}, doi = {10.1016/j.neuron.2018.02.007}, year = {2018}, date = {2018-01-01}, journal = {Neuron}, volume = {97}, number = {6}, pages = {1382--1393}, publisher = {Elsevier Inc.}, abstract = {Visual attention is associated with neuronal changes across the brain, and these widespread signals are generally assumed to underlie a unitary mechanism of attention. However, using signal detection theory, attention-related effects on performance can be partitioned into changes in either the subject's criterion or sensitivity. Neuronal modulations associated with only sensitivity changes were previously observed in visual cortex, raising questions about which structures mediate attention-related changes in criterion and whether individual neurons are involved in multiple components of attention. Here, we recorded from monkey lateral prefrontal cortex (LPFC) and found that, in contrast to visual cortex, neurons in LPFC changed their firing rates, pairwise correlation, and Fano factor when subjects changed either their criterion or their sensitivity. These results indicate that attention-related neuronal modulations in separate brain regions are not a monolithic signal and instead can be linked to distinct behavioral changes.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Visual attention is associated with neuronal changes across the brain, and these widespread signals are generally assumed to underlie a unitary mechanism of attention. However, using signal detection theory, attention-related effects on performance can be partitioned into changes in either the subject's criterion or sensitivity. Neuronal modulations associated with only sensitivity changes were previously observed in visual cortex, raising questions about which structures mediate attention-related changes in criterion and whether individual neurons are involved in multiple components of attention. Here, we recorded from monkey lateral prefrontal cortex (LPFC) and found that, in contrast to visual cortex, neurons in LPFC changed their firing rates, pairwise correlation, and Fano factor when subjects changed either their criterion or their sensitivity. These results indicate that attention-related neuronal modulations in separate brain regions are not a monolithic signal and instead can be linked to distinct behavioral changes. |
Liya Ma; Kevin Skoblenick; Kevin Johnston; Stefan Everling Ketamine alters lateral prefrontal oscillations in a rule-based working memory gask Journal Article The Journal of Neuroscience, 38 (10), pp. 2482–2494, 2018. @article{Ma2018a, title = {Ketamine alters lateral prefrontal oscillations in a rule-based working memory gask}, author = {Liya Ma and Kevin Skoblenick and Kevin Johnston and Stefan Everling}, doi = {10.1523/jneurosci.2659-17.2018}, year = {2018}, date = {2018-01-01}, journal = {The Journal of Neuroscience}, volume = {38}, number = {10}, pages = {2482--2494}, abstract = {Acute administration of N-methyl-D-aspartate receptor (NMDAR) antagonists in healthy humans and animals produces working memory deficits similar to those observed in schizophrenia. However, it is unclear whether they also lead to altered low-frequency (textless=60Hz) neural oscillatory activities similar to those associated with schizophrenia during working memory processes. Here we recorded local field potentials (LFPs) and single unit activity from the lateral prefrontal cortex (LPFC) of three male rhesus macaque monkeys while they performed a rule-based prosaccade and antisaccade working memory task, both before and after systemic injections of a subanesthetic dose (textless=0.7mg/kg) of ketamine. Accompanying working-memory impairment, ketamine enhanced the low gamma band (30-60Hz) and dampened the beta band (13-30Hz) oscillatory activities in the LPFC during both delay periods and inter-trial intervals. It also increased task-related alpha-band activities, likely reflecting compromised attention. Beta-band oscillations may be especially relevant to working memory processes, as stronger beta power weakly but significantly predicted shorter saccadic reaction time. Also in beta band, ketamine reduced the performance-related oscillation as well as the rule information encoded in the spectral power. Ketamine also reduced rule information in the spike-field phase consistency in almost all frequencies up to 60Hz. Our findings support NMDAR antagonists in non-human primates as a meaningful model for altered neural oscillations and synchrony, which reflect a disorganized network underlying the working memory deficits in schizophrenia.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Acute administration of N-methyl-D-aspartate receptor (NMDAR) antagonists in healthy humans and animals produces working memory deficits similar to those observed in schizophrenia. However, it is unclear whether they also lead to altered low-frequency (textless=60Hz) neural oscillatory activities similar to those associated with schizophrenia during working memory processes. Here we recorded local field potentials (LFPs) and single unit activity from the lateral prefrontal cortex (LPFC) of three male rhesus macaque monkeys while they performed a rule-based prosaccade and antisaccade working memory task, both before and after systemic injections of a subanesthetic dose (textless=0.7mg/kg) of ketamine. Accompanying working-memory impairment, ketamine enhanced the low gamma band (30-60Hz) and dampened the beta band (13-30Hz) oscillatory activities in the LPFC during both delay periods and inter-trial intervals. It also increased task-related alpha-band activities, likely reflecting compromised attention. Beta-band oscillations may be especially relevant to working memory processes, as stronger beta power weakly but significantly predicted shorter saccadic reaction time. Also in beta band, ketamine reduced the performance-related oscillation as well as the rule information encoded in the spectral power. Ketamine also reduced rule information in the spike-field phase consistency in almost all frequencies up to 60Hz. Our findings support NMDAR antagonists in non-human primates as a meaningful model for altered neural oscillations and synchrony, which reflect a disorganized network underlying the working memory deficits in schizophrenia. |
Kazutaka Maeda; Jun Kunimatsu; Okihide Hikosaka Amygdala activity for the modulation of goal-directed behavior in emotional contexts Journal Article PLoS Biology, 16 (6), pp. 1–29, 2018. @article{Maeda2018, title = {Amygdala activity for the modulation of goal-directed behavior in emotional contexts}, author = {Kazutaka Maeda and Jun Kunimatsu and Okihide Hikosaka}, doi = {10.1371/journal.pbio.2005339}, year = {2018}, date = {2018-01-01}, journal = {PLoS Biology}, volume = {16}, number = {6}, pages = {1--29}, abstract = {Choosing valuable objects and rewarding actions is critical for survival. While such choices must be made in a way that suits the animal's circumstances, the neural mechanisms underlying such context-appropriate behavior are unclear. To address this question, we devised a context-dependent reward-seeking task for macaque monkeys. Each trial started with the appearance of one of many visual scenes containing two or more objects, and the monkey had to choose the good object by saccade to get a reward. These scenes were categorized into two dimensions of emotional context: dangerous versus safe and rich versus poor. We found that many amygdala neurons were more strongly activated by dangerous scenes, by rich scenes, or by both. Furthermore, saccades to target objects occurred more quickly in dangerous than in safe scenes and were also quicker in rich than in poor scenes. Thus, amygdala neuronal activity and saccadic reaction times were negatively correlated in each monkey. These results suggest that amygdala neurons facilitate targeting saccades predictably based on aspects of emotional context, as is necessary for goal-directed and social behavior.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Choosing valuable objects and rewarding actions is critical for survival. While such choices must be made in a way that suits the animal's circumstances, the neural mechanisms underlying such context-appropriate behavior are unclear. To address this question, we devised a context-dependent reward-seeking task for macaque monkeys. Each trial started with the appearance of one of many visual scenes containing two or more objects, and the monkey had to choose the good object by saccade to get a reward. These scenes were categorized into two dimensions of emotional context: dangerous versus safe and rich versus poor. We found that many amygdala neurons were more strongly activated by dangerous scenes, by rich scenes, or by both. Furthermore, saccades to target objects occurred more quickly in dangerous than in safe scenes and were also quicker in rich than in poor scenes. Thus, amygdala neuronal activity and saccadic reaction times were negatively correlated in each monkey. These results suggest that amygdala neurons facilitate targeting saccades predictably based on aspects of emotional context, as is necessary for goal-directed and social behavior. |
Alexandria C Marino; James A Mazer Saccades trigger predictive updating of attentional topography in area V4 Journal Article Neuron, 98 (2), pp. 429–438, 2018. @article{Marino2018, title = {Saccades trigger predictive updating of attentional topography in area V4}, author = {Alexandria C Marino and James A Mazer}, doi = {10.1016/j.neuron.2018.03.020}, year = {2018}, date = {2018-01-01}, journal = {Neuron}, volume = {98}, number = {2}, pages = {429--438}, publisher = {Elsevier Inc.}, abstract = {During natural behavior, saccades and attention act together to allocate limited neural resources. Attention is generally mediated by retinotopic visual neurons; therefore, specific neurons representing attended features change with each saccade. We investigated the neural mechanisms that allow attentional targeting in the face of saccades. Specifically, we looked for predictive changes in attentional modulation state or receptive field position that could stabilize attentional representations across saccades in area V4, known to be necessary for attention-dependent behavior. We recorded from neurons in monkeys performing a novel spatiotopic attention task, in which performance depended on accurate saccade compensation. Measurements of attentional modulation revealed a predictive attentional “hand-off” corresponding to a presaccadic transfer of attentional state from neurons inside the attentional focus before the saccade to those that will be inside the focus after the saccade. The predictive nature of the hand-off ensures that attentional brain maps are properly configured immediately after each saccade.}, keywords = {}, pubstate = {published}, tppubtype = {article} } During natural behavior, saccades and attention act together to allocate limited neural resources. Attention is generally mediated by retinotopic visual neurons; therefore, specific neurons representing attended features change with each saccade. We investigated the neural mechanisms that allow attentional targeting in the face of saccades. Specifically, we looked for predictive changes in attentional modulation state or receptive field position that could stabilize attentional representations across saccades in area V4, known to be necessary for attention-dependent behavior. We recorded from neurons in monkeys performing a novel spatiotopic attention task, in which performance depended on accurate saccade compensation. Measurements of attentional modulation revealed a predictive attentional “hand-off” corresponding to a presaccadic transfer of attentional state from neurons inside the attentional focus before the saccade to those that will be inside the focus after the saccade. The predictive nature of the hand-off ensures that attentional brain maps are properly configured immediately after each saccade. |
Yaser Merrikhi; Kelsey Clark; Behrad Noudoost Concurrent influence of top-down and bottom-up inputs on correlated activity of Macaque extrastriate neurons Journal Article Nature Communications, 9 (1), 2018. @article{Merrikhi2018, title = {Concurrent influence of top-down and bottom-up inputs on correlated activity of Macaque extrastriate neurons}, author = {Yaser Merrikhi and Kelsey Clark and Behrad Noudoost}, doi = {10.1038/s41467-018-07816-4}, year = {2018}, date = {2018-01-01}, journal = {Nature Communications}, volume = {9}, number = {1}, publisher = {Springer US}, abstract = {Correlations between neurons can profoundly impact the information encoding capacity of a neural population. We studied how maintenance of visuospatial information affects correlated activity in visual areas by recording the activity of neurons in visual area MT of rhesus macaques during a spatial working memory task. Correlations between MT neurons depended upon the spatial overlap between neurons' receptive fields. These correlations were influenced by the content of working memory, but the effect of a top-down memory signal differed in the presence or absence of bottom-up visual input. Neurons representing the same area of space showed increased correlations when remembering a location in their receptive fields in the absence of visual input, but decreased correlations in the presence of a visual stimulus. This set of results reveals the correlating nature of top-down signals influencing visual areas and uncovers how such a correlating signal, in interaction with bottom-up information, could enhance sensory representations.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Correlations between neurons can profoundly impact the information encoding capacity of a neural population. We studied how maintenance of visuospatial information affects correlated activity in visual areas by recording the activity of neurons in visual area MT of rhesus macaques during a spatial working memory task. Correlations between MT neurons depended upon the spatial overlap between neurons' receptive fields. These correlations were influenced by the content of working memory, but the effect of a top-down memory signal differed in the presence or absence of bottom-up visual input. Neurons representing the same area of space showed increased correlations when remembering a location in their receptive fields in the absence of visual input, but decreased correlations in the presence of a visual stimulus. This set of results reveals the correlating nature of top-down signals influencing visual areas and uncovers how such a correlating signal, in interaction with bottom-up information, could enhance sensory representations. |
Jérôme Munuera; Mattia Rigotti; Daniel C Salzman Shared neural coding for social hierarchy and reward value in primate amygdala Journal Article Nature Neuroscience, 21 (3), pp. 415–423, 2018. @article{Munuera2018, title = {Shared neural coding for social hierarchy and reward value in primate amygdala}, author = {Jér{ô}me Munuera and Mattia Rigotti and Daniel C Salzman}, doi = {10.1038/s41593-018-0082-8}, year = {2018}, date = {2018-01-01}, journal = {Nature Neuroscience}, volume = {21}, number = {3}, pages = {415--423}, publisher = {Springer US}, abstract = {The social brain hypothesis posits that dedicated neural systems process social information. In support of this, neurophysiological data have shown that some brain regions are specialized for representing faces. It remains unknown, however, whether distinct anatomical substrates also represent more complex social variables, such as the hierarchical rank of individuals within a social group. Here we show that the primate amygdala encodes the hierarchical rank of individuals in the same neuronal ensembles that encode the rewards associated with nonsocial stimuli. By contrast, orbitofrontal and anterior cingulate cortices lack strong representations of hierarchical rank while still representing reward values. These results challenge the conventional view that dedicated neural systems process social information. Instead, information about hierarchical rank—which contributes to the assessment of the social value of individuals within a group—is linked in the amygdala to representations of rewards associated with nonsocial stimuli.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The social brain hypothesis posits that dedicated neural systems process social information. In support of this, neurophysiological data have shown that some brain regions are specialized for representing faces. It remains unknown, however, whether distinct anatomical substrates also represent more complex social variables, such as the hierarchical rank of individuals within a social group. Here we show that the primate amygdala encodes the hierarchical rank of individuals in the same neuronal ensembles that encode the rewards associated with nonsocial stimuli. By contrast, orbitofrontal and anterior cingulate cortices lack strong representations of hierarchical rank while still representing reward values. These results challenge the conventional view that dedicated neural systems process social information. Instead, information about hierarchical rank—which contributes to the assessment of the social value of individuals within a group—is linked in the amygdala to representations of rewards associated with nonsocial stimuli. |
James E Niemeyer; Michael A Paradiso Saccade-based termination responses in macaque V1 and visual perception Journal Article Visual Neuroscience, 35 , pp. 1–7, 2018. @article{Niemeyer2018, title = {Saccade-based termination responses in macaque V1 and visual perception}, author = {James E Niemeyer and Michael A Paradiso}, doi = {10.1017/s0952523818000032}, year = {2018}, date = {2018-01-01}, journal = {Visual Neuroscience}, volume = {35}, pages = {1--7}, abstract = {Neurons in visual areas of the brain are generally characterized by the increase in firing rate that occurs when a stimulus is flashed on in the receptive field (RF). However, neurons also increase their firing rate when a stimulus is turned off. These “termination responses” or “after-discharges” that occur with flashed stimuli have been observed in area V1 and they may be important for vision as stimulus terminations have been shown to influence visual perception. The goal of the present study was to determine the strength of termination responses in the more natural situation in which eye movements move a stimulus out of an RF. We find that termination responses do occur in macaque V1 when termination results from a saccadic eye movement, but they are smaller in amplitude compared to flashed-off stimuli. Furthermore, there are termination responses even in the absence of visual stimulation. These findings demonstrate that termination responses are a component of naturalistic vision. They appear to be based on both visual and nonvisual signals in visual cortex. We speculate that the weakening of termination responses might be a neural correlate of saccadic suppression, the loss of perceptual sensitivity around the time of saccades.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Neurons in visual areas of the brain are generally characterized by the increase in firing rate that occurs when a stimulus is flashed on in the receptive field (RF). However, neurons also increase their firing rate when a stimulus is turned off. These “termination responses” or “after-discharges” that occur with flashed stimuli have been observed in area V1 and they may be important for vision as stimulus terminations have been shown to influence visual perception. The goal of the present study was to determine the strength of termination responses in the more natural situation in which eye movements move a stimulus out of an RF. We find that termination responses do occur in macaque V1 when termination results from a saccadic eye movement, but they are smaller in amplitude compared to flashed-off stimuli. Furthermore, there are termination responses even in the absence of visual stimulation. These findings demonstrate that termination responses are a component of naturalistic vision. They appear to be based on both visual and nonvisual signals in visual cortex. We speculate that the weakening of termination responses might be a neural correlate of saccadic suppression, the loss of perceptual sensitivity around the time of saccades. |
Atsushi Noritake; Taihei Ninomiya; Masaki Isoda Social reward monitoring and valuation in the macaque brain Journal Article Nature Neuroscience, 21 (10), pp. 1452–1462, 2018. @article{Noritake2018, title = {Social reward monitoring and valuation in the macaque brain}, author = {Atsushi Noritake and Taihei Ninomiya and Masaki Isoda}, doi = {10.1038/s41593-018-0229-7}, year = {2018}, date = {2018-01-01}, journal = {Nature Neuroscience}, volume = {21}, number = {10}, pages = {1452--1462}, publisher = {Springer US}, abstract = {Behaviors are influenced by rewards to both oneself and others, but the neurons and neural connections that monitor and evaluate rewards in social contexts are unknown. To address this issue, we devised a social Pavlovian conditioning procedure for pairs of monkeys. Despite being constant in amount and probability, the subjective value of forthcoming self-rewards, as indexed by licking and choice behaviors, decreased as partner-reward probability increased. This value modulation was absent when the conspecific partner was replaced by a physical object. Medial prefrontal cortex neurons selectively monitored self-reward and partner-reward information, whereas midbrain dopaminergic neurons integrated this information into a subjective value. Recordings of local field potentials revealed that responses to reward-predictive stimuli in medial prefrontal cortex started before those in dopaminergic midbrain nuclei and that neural information flowed predominantly in a medial prefrontal cortex-to-midbrain direction. These findings delineate a dedicated pathway for subjective reward evaluation in social environments.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Behaviors are influenced by rewards to both oneself and others, but the neurons and neural connections that monitor and evaluate rewards in social contexts are unknown. To address this issue, we devised a social Pavlovian conditioning procedure for pairs of monkeys. Despite being constant in amount and probability, the subjective value of forthcoming self-rewards, as indexed by licking and choice behaviors, decreased as partner-reward probability increased. This value modulation was absent when the conspecific partner was replaced by a physical object. Medial prefrontal cortex neurons selectively monitored self-reward and partner-reward information, whereas midbrain dopaminergic neurons integrated this information into a subjective value. Recordings of local field potentials revealed that responses to reward-predictive stimuli in medial prefrontal cortex started before those in dopaminergic midbrain nuclei and that neural information flowed predominantly in a medial prefrontal cortex-to-midbrain direction. These findings delineate a dedicated pathway for subjective reward evaluation in social environments. |
Takaya Ogasawara; Masafumi Nejime; Masahiko Takada; Masayuki Matsumoto Primate nigrostriatal dopamine system regulates saccadic response inhibition Journal Article Neuron, 100 (6), pp. 1513–1526, 2018. @article{Ogasawara2018, title = {Primate nigrostriatal dopamine system regulates saccadic response inhibition}, author = {Takaya Ogasawara and Masafumi Nejime and Masahiko Takada and Masayuki Matsumoto}, doi = {10.1016/j.neuron.2018.10.025}, year = {2018}, date = {2018-01-01}, journal = {Neuron}, volume = {100}, number = {6}, pages = {1513--1526}, publisher = {Elsevier Inc.}, abstract = {Animals need to inhibit inappropriate actions that would lead to unwanted outcomes. Although this ability, called response inhibition, is impaired in neurological/psychiatric disorders with dopaminergic dysfunctions, how dopamine regulates response inhibition remains unclear. Here we investigated neuronal signals of the nigrostriatal dopamine system in monkeys performing a saccadic countermanding task. Subsets of dopamine neurons in the substantia nigra and striatal neurons receiving the dopaminergic input were activated when the monkey was required to cancel a planned saccadic eye movement. These activations were stronger when canceling the eye movements was successful compared with failed and were enhanced in demanding trials. The activated dopamine neurons were distributed mainly in the dorsolateral, but not in the ventromedial, part of the nigra. Furthermore, pharmacological blockade of dopaminergic neurotransmission in the striatum dampened the performance of canceling saccadic eye movements. The present findings indicate that disruption of nigrostriatal dopamine signaling causes impairments in response inhibition.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Animals need to inhibit inappropriate actions that would lead to unwanted outcomes. Although this ability, called response inhibition, is impaired in neurological/psychiatric disorders with dopaminergic dysfunctions, how dopamine regulates response inhibition remains unclear. Here we investigated neuronal signals of the nigrostriatal dopamine system in monkeys performing a saccadic countermanding task. Subsets of dopamine neurons in the substantia nigra and striatal neurons receiving the dopaminergic input were activated when the monkey was required to cancel a planned saccadic eye movement. These activations were stronger when canceling the eye movements was successful compared with failed and were enhanced in demanding trials. The activated dopamine neurons were distributed mainly in the dorsolateral, but not in the ventromedial, part of the nigra. Furthermore, pharmacological blockade of dopaminergic neurotransmission in the striatum dampened the performance of canceling saccadic eye movements. The present findings indicate that disruption of nigrostriatal dopamine signaling causes impairments in response inhibition. |
Timothy D Oleskiw; Amy Nowack; Anitha Pasupathy Joint coding of shape and blur in area V4 Journal Article Nature Communications, 9 (1), pp. 1–13, 2018. @article{Oleskiw2018, title = {Joint coding of shape and blur in area V4}, author = {Timothy D Oleskiw and Amy Nowack and Anitha Pasupathy}, doi = {10.1038/s41467-017-02438-8}, year = {2018}, date = {2018-01-01}, journal = {Nature Communications}, volume = {9}, number = {1}, pages = {1--13}, publisher = {Springer US}, abstract = {Edge blur, a prevalent feature of natural images, is believed to facilitate multiple visual processes including segmentation and depth perception. Furthermore, image descriptions that explicitly combine blur and shape information provide complete representations of naturalistic scenes. Here we report the first demonstration of blur encoding in primate visual cortex: neurons in macaque V4 exhibit tuning for both object shape and boundary blur, with observed blur tuning not explained by potential confounds including stimulus size, intensity, or curvature. A descriptive model wherein blur selectivity is cast as a distinct neural process that modulates the gain of shape-selective V4 neurons explains observed data, supporting the hypothesis that shape and blur are fundamental features of a sufficient neural code for natural image representation in V4.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Edge blur, a prevalent feature of natural images, is believed to facilitate multiple visual processes including segmentation and depth perception. Furthermore, image descriptions that explicitly combine blur and shape information provide complete representations of naturalistic scenes. Here we report the first demonstration of blur encoding in primate visual cortex: neurons in macaque V4 exhibit tuning for both object shape and boundary blur, with observed blur tuning not explained by potential confounds including stimulus size, intensity, or curvature. A descriptive model wherein blur selectivity is cast as a distinct neural process that modulates the gain of shape-selective V4 neurons explains observed data, supporting the hypothesis that shape and blur are fundamental features of a sufficient neural code for natural image representation in V4. |
Adam Pallus; Mark M G Walton; Michael Mustari Activity of near-response cells during disconjugate saccades in strabismic monkeys Journal Article Journal of Neurophysiology, 120 (5), pp. 2282–2295, 2018. @article{Pallus2018, title = {Activity of near-response cells during disconjugate saccades in strabismic monkeys}, author = {Adam Pallus and Mark M G Walton and Michael Mustari}, doi = {10.1152/jn.00219.2018}, year = {2018}, date = {2018-01-01}, journal = {Journal of Neurophysiology}, volume = {120}, number = {5}, pages = {2282--2295}, abstract = {Infantile strabismus is a common disorder characterized by a chronic misalignment of the eyes, impairment of binocular vision, and oculomotor abnormalities. Nonhuman primates with strabismus, induced in infancy, show a pattern of abnormalities similar to those of strabismic children. This allows strabismic nonhuman primates to serve as an ideal animal model to examine neural mechanisms associated with aberrant oculomotor behavior. Here, we test the hypothesis that impairment of disparity vergence and horizontal saccade disconjugacy in exotropia and esotropia are associated with disrupted tuning of near- and far-response neurons in the supraoculomotor area (SOA). In normal animals, these neurons carry signals related to vergence position and/or velocity. We hypothesized that, in strabismus, these neurons modulate inappropriately in associ- ation with saccades between equidistant targets. We recorded from 62 SOA neurons from 4 strabismic animals (2 esotropes and 2 exotropes) during visually guided saccades to a target that stepped to different locations on a tangent screen. Under these same conditions, SOA neurons in normal animals show no detectable modulation. In our strabismic subjects, we found that a subset of SOA neurons carry weak vergence velocity signals during saccades. In addition, a subset of SOA neurons showed clear modulation associated with slow fluctuations of horizontal strabismus angle in the absence of a saccade. We suggest that abnormal SOA activity contributes to fixation instability but plays only a minor role in the horizontal disconjugacy of saccades that do not switch fixation from one eye to the other.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Infantile strabismus is a common disorder characterized by a chronic misalignment of the eyes, impairment of binocular vision, and oculomotor abnormalities. Nonhuman primates with strabismus, induced in infancy, show a pattern of abnormalities similar to those of strabismic children. This allows strabismic nonhuman primates to serve as an ideal animal model to examine neural mechanisms associated with aberrant oculomotor behavior. Here, we test the hypothesis that impairment of disparity vergence and horizontal saccade disconjugacy in exotropia and esotropia are associated with disrupted tuning of near- and far-response neurons in the supraoculomotor area (SOA). In normal animals, these neurons carry signals related to vergence position and/or velocity. We hypothesized that, in strabismus, these neurons modulate inappropriately in associ- ation with saccades between equidistant targets. We recorded from 62 SOA neurons from 4 strabismic animals (2 esotropes and 2 exotropes) during visually guided saccades to a target that stepped to different locations on a tangent screen. Under these same conditions, SOA neurons in normal animals show no detectable modulation. In our strabismic subjects, we found that a subset of SOA neurons carry weak vergence velocity signals during saccades. In addition, a subset of SOA neurons showed clear modulation associated with slow fluctuations of horizontal strabismus angle in the absence of a saccade. We suggest that abnormal SOA activity contributes to fixation instability but plays only a minor role in the horizontal disconjugacy of saccades that do not switch fixation from one eye to the other. |
Angelo Pirrone; Habiba Azab; Benjamin Y Hayden; Tom Stafford; James A R Marshall Evidence for the speed–value trade-Off: Human and monkey decision making Is magnitude sensitive Journal Article Decision, 5 (2), pp. 129–142, 2018. @article{Pirrone2018, title = {Evidence for the speed–value trade-Off: Human and monkey decision making Is magnitude sensitive}, author = {Angelo Pirrone and Habiba Azab and Benjamin Y Hayden and Tom Stafford and James A R Marshall}, doi = {10.1037/dec0000075.Evidence}, year = {2018}, date = {2018-01-01}, journal = {Decision}, volume = {5}, number = {2}, pages = {129--142}, abstract = {Complex natural systems from brains to bee swarms have evolved to make adaptive multifactorial decisions. Recent theoretical and empirical work suggests that many evolved systems may take advantage of common motifs across multiple domains. We are particularly interested in value sensitivity (i.e., sensitivity to the magnitude or intensity of the stimuli or reward under consideration) as a mechanism to resolve deadlocks adaptively. This mechanism favors long-term reward maximization over accuracy in a simple manner, because it avoids costly delays associated with ambivalence between similar options; speed–value trade-offs have been proposed to be evolutionarily advantageous for many kinds of decision. A key prediction of the value-sensitivity hypothesis is that choices between equally valued options will proceed faster when the options have a high value than when they have a low value. However, value sensitivity is not part of idealized choice models such as diffusion to bound. Here, we examine 2 different choice behaviors in 2 different species, perceptual decisions in humans and economic choices in rhesus monkeys, to test this hypothesis. We observe the same value sensitivity in both human perceptual decisions and monkey value-based decisions. These results endorse the idea that neural decision systems make use of the same basic principle of value sensitivity in order to resolve costly deadlocks and thus improve long-term reward intake.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Complex natural systems from brains to bee swarms have evolved to make adaptive multifactorial decisions. Recent theoretical and empirical work suggests that many evolved systems may take advantage of common motifs across multiple domains. We are particularly interested in value sensitivity (i.e., sensitivity to the magnitude or intensity of the stimuli or reward under consideration) as a mechanism to resolve deadlocks adaptively. This mechanism favors long-term reward maximization over accuracy in a simple manner, because it avoids costly delays associated with ambivalence between similar options; speed–value trade-offs have been proposed to be evolutionarily advantageous for many kinds of decision. A key prediction of the value-sensitivity hypothesis is that choices between equally valued options will proceed faster when the options have a high value than when they have a low value. However, value sensitivity is not part of idealized choice models such as diffusion to bound. Here, we examine 2 different choice behaviors in 2 different species, perceptual decisions in humans and economic choices in rhesus monkeys, to test this hypothesis. We observe the same value sensitivity in both human perceptual decisions and monkey value-based decisions. These results endorse the idea that neural decision systems make use of the same basic principle of value sensitivity in order to resolve costly deadlocks and thus improve long-term reward intake. |
Evan D Remington; Devika Narain; Eghbal A Hosseini; Mehrdad Jazayeri Flexible sensorimotor computations through rapid reconfiguration of cortical dynamics Journal Article Neuron, 98 , pp. 1005–1019, 2018. @article{Remington2018a, title = {Flexible sensorimotor computations through rapid reconfiguration of cortical dynamics}, author = {Evan D Remington and Devika Narain and Eghbal A Hosseini and Mehrdad Jazayeri}, doi = {10.1016/j.neuron.2018.05.020}, year = {2018}, date = {2018-01-01}, journal = {Neuron}, volume = {98}, pages = {1005--1019}, publisher = {Elsevier Inc.}, abstract = {Neural mechanisms that support flexible sensorimotor computations are not well understood. In a dynamical system whose state is determined by interactions among neurons, computations can be rapidly reconfigured by controlling the system's inputs and initial conditions. To investigate whether the brain employs such control mechanisms, we recorded from the dorsomedial frontal cortex of monkeys trained to measure and produce time intervals in two sensorimotor contexts. The geometry of neural trajectories during the production epoch was consistent with a mechanism wherein the measured interval and sensorimotor context exerted control over cortical dynamics by adjusting the system's initial condition and input, respectively. These adjustments, in turn, set the speed at which activity evolved in the production epoch, allowing the animal to flexibly produce different time intervals. These results provide evidence that the language of dynamical systems can be used to parsimoniously link brain activity to sensorimotor computations.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Neural mechanisms that support flexible sensorimotor computations are not well understood. In a dynamical system whose state is determined by interactions among neurons, computations can be rapidly reconfigured by controlling the system's inputs and initial conditions. To investigate whether the brain employs such control mechanisms, we recorded from the dorsomedial frontal cortex of monkeys trained to measure and produce time intervals in two sensorimotor contexts. The geometry of neural trajectories during the production epoch was consistent with a mechanism wherein the measured interval and sensorimotor context exerted control over cortical dynamics by adjusting the system's initial condition and input, respectively. These adjustments, in turn, set the speed at which activity evolved in the production epoch, allowing the animal to flexibly produce different time intervals. These results provide evidence that the language of dynamical systems can be used to parsimoniously link brain activity to sensorimotor computations. |
Thomas R Reppert; Mathieu Servant; Richard P Heitz; Jeffrey D Schall Journal of Neurophysiology, 120 (1), pp. 372–384, 2018. @article{Reppert2018b, title = {Neural mechanisms of speed-accuracy tradeoff of visual search: Saccade vigor, the origin of targeting errors, and comparison of the superior colliculus and frontal eye field}, author = {Thomas R Reppert and Mathieu Servant and Richard P Heitz and Jeffrey D Schall}, doi = {10.1152/jn.00887.2017}, year = {2018}, date = {2018-01-01}, journal = {Journal of Neurophysiology}, volume = {120}, number = {1}, pages = {372--384}, abstract = {Balancing the speed-accuracy tradeoff (SAT) is necessary for successful behavior. Using a visual search task with interleaved cues emphasizing speed or accuracy, we recently reported diverse contributions of frontal eye field (FEF) neurons instantiating salience evidence and response preparation. Here, we report replication of visual search SAT performance in two macaque monkeys, new information about variation of saccade dynamics with SAT, extension of the neurophysiological investigation to describe processes in the superior colliculus (SC), and a description of the origin of search errors in this task. Saccade vigor varied idiosyncratically across SAT conditions and monkeys but tended to decrease with response time. As observed in the FEF, speed-accuracy tradeoff was accomplished through several distinct adjustments in the superior colliculus. In “Accurate” relative to “Fast” trials, visually responsive neurons in SC as in FEF had lower baseline firing rates and later target selection. The magnitude of these adjustments in SC was indistinguishable from that in FEF. Search errors occurred when visual salience neurons in the FEF and the SC treated distractors as targets, even in the Accurate condition. Unlike FEF, the magnitude of visual responses in the SC did not vary across SAT conditions. Also unlike FEF, the activity of SC movement neurons when saccades were initiated was equivalent in Fast and Accurate trials. Saccade-related neural activity in SC, but not FEF, varied with saccade peak velocity. These results extend our understanding of the cortical and subcortical contributions to SAT.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Balancing the speed-accuracy tradeoff (SAT) is necessary for successful behavior. Using a visual search task with interleaved cues emphasizing speed or accuracy, we recently reported diverse contributions of frontal eye field (FEF) neurons instantiating salience evidence and response preparation. Here, we report replication of visual search SAT performance in two macaque monkeys, new information about variation of saccade dynamics with SAT, extension of the neurophysiological investigation to describe processes in the superior colliculus (SC), and a description of the origin of search errors in this task. Saccade vigor varied idiosyncratically across SAT conditions and monkeys but tended to decrease with response time. As observed in the FEF, speed-accuracy tradeoff was accomplished through several distinct adjustments in the superior colliculus. In “Accurate” relative to “Fast” trials, visually responsive neurons in SC as in FEF had lower baseline firing rates and later target selection. The magnitude of these adjustments in SC was indistinguishable from that in FEF. Search errors occurred when visual salience neurons in the FEF and the SC treated distractors as targets, even in the Accurate condition. Unlike FEF, the magnitude of visual responses in the SC did not vary across SAT conditions. Also unlike FEF, the activity of SC movement neurons when saccades were initiated was equivalent in Fast and Accurate trials. Saccade-related neural activity in SC, but not FEF, varied with saccade peak velocity. These results extend our understanding of the cortical and subcortical contributions to SAT. |
Douglas A Ruff; David H Brainard; Marlene R Cohen Neuronal population mechanisms of lightness perception Journal Article Journal of Neurophysiology, 120 (5), pp. 2296–2310, 2018. @article{Ruff2018, title = {Neuronal population mechanisms of lightness perception}, author = {Douglas A Ruff and David H Brainard and Marlene R Cohen}, doi = {10.1152/jn.00906.2017}, year = {2018}, date = {2018-01-01}, journal = {Journal of Neurophysiology}, volume = {120}, number = {5}, pages = {2296--2310}, abstract = {The way that humans and animals perceive the lightness of an object depends on its physical luminance as well as its surrounding context. While neuronal responses throughout the visual pathway are modulated by context, the relationship between neuronal responses and lightness perception is poorly understood. We searched for a neuronal mechanism of lightness by recording responses of neuronal populations in monkey primary visual cortex (V1) and area V4 to stimuli that produce a lightness illusion in humans, in which the lightness of a disk depends on the context in which it is embedded. We found that the way individual units encode the luminance (or equivalently for our stimuli, contrast) of the disk and its context is extremely heterogeneous. This motivated us to ask whether the population representation in either V1 or V4 satisfies three criteria: 1) disk luminance is represented with high fidelity, 2) the context surrounding the disk is also represented, and 3) the representations of disk luminance and context interact to create a representation of lightness that depends on these factors in a manner consistent with human psychophysical judgments of disk lightness. We found that populations of units in both V1 and V4 fulfill the first two criteria, but that we cannot conclude that the two types of information in either area interact in a manner that clearly predicts human psychophysical measurements: the interpretation of our population measurements depends on how subsequent areas read out lightness from the population responses.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The way that humans and animals perceive the lightness of an object depends on its physical luminance as well as its surrounding context. While neuronal responses throughout the visual pathway are modulated by context, the relationship between neuronal responses and lightness perception is poorly understood. We searched for a neuronal mechanism of lightness by recording responses of neuronal populations in monkey primary visual cortex (V1) and area V4 to stimuli that produce a lightness illusion in humans, in which the lightness of a disk depends on the context in which it is embedded. We found that the way individual units encode the luminance (or equivalently for our stimuli, contrast) of the disk and its context is extremely heterogeneous. This motivated us to ask whether the population representation in either V1 or V4 satisfies three criteria: 1) disk luminance is represented with high fidelity, 2) the context surrounding the disk is also represented, and 3) the representations of disk luminance and context interact to create a representation of lightness that depends on these factors in a manner consistent with human psychophysical judgments of disk lightness. We found that populations of units in both V1 and V4 fulfill the first two criteria, but that we cannot conclude that the two types of information in either area interact in a manner that clearly predicts human psychophysical measurements: the interpretation of our population measurements depends on how subsequent areas read out lightness from the population responses. |
Jason M Samonds; Wilson S Geisler; Nicholas J Priebe Natural image and receptive field statistics predict saccade sizes Journal Article Nature Neuroscience, 21 (11), pp. 1591–1599, 2018. @article{Samonds2018, title = {Natural image and receptive field statistics predict saccade sizes}, author = {Jason M Samonds and Wilson S Geisler and Nicholas J Priebe}, doi = {10.1038/s41593-018-0255-5}, year = {2018}, date = {2018-01-01}, journal = {Nature Neuroscience}, volume = {21}, number = {11}, pages = {1591--1599}, publisher = {Springer US}, abstract = {Humans and other primates sample the visual environment using saccadic eye movements that shift a high-resolution fovea toward regions of interest to create a clear perception of a scene across fixations. Many mammals, however, like mice, lack a fovea, which raises the question of why they make saccades. Here we describe and test the hypothesis that saccades are matched to natural scene statistics and to the receptive field sizes and adaptive properties of neural populations. Specifically, we determined the minimum amplitude of saccades in natural scenes necessary to provide uncorrelated inputs to model neural populations. This analysis predicts the distributions of observed saccade sizes during passive viewing for nonhuman primates, cats, and mice. Furthermore, disrupting the development of receptive field properties by monocular deprivation changed saccade sizes consistent with this hypothesis. Therefore, natural-scene statistics and the neural representation of natural images appear to be critical factors guiding saccadic eye movements.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Humans and other primates sample the visual environment using saccadic eye movements that shift a high-resolution fovea toward regions of interest to create a clear perception of a scene across fixations. Many mammals, however, like mice, lack a fovea, which raises the question of why they make saccades. Here we describe and test the hypothesis that saccades are matched to natural scene statistics and to the receptive field sizes and adaptive properties of neural populations. Specifically, we determined the minimum amplitude of saccades in natural scenes necessary to provide uncorrelated inputs to model neural populations. This analysis predicts the distributions of observed saccade sizes during passive viewing for nonhuman primates, cats, and mice. Furthermore, disrupting the development of receptive field properties by monocular deprivation changed saccade sizes consistent with this hypothesis. Therefore, natural-scene statistics and the neural representation of natural images appear to be critical factors guiding saccadic eye movements. |
Joshua A Seideman; Terrence R Stanford; Emilio Salinas Saccade metrics reflect decision-making dynamics during urgent choices Journal Article Nature Communications, 9 (1), pp. 1–11, 2018. @article{Seideman2018, title = {Saccade metrics reflect decision-making dynamics during urgent choices}, author = {Joshua A Seideman and Terrence R Stanford and Emilio Salinas}, doi = {10.1038/s41467-018-05319-w}, year = {2018}, date = {2018-01-01}, journal = {Nature Communications}, volume = {9}, number = {1}, pages = {1--11}, abstract = {A perceptual judgment is typically characterized by constructing psychometric and chronometric functions, i.e., by mapping the accuracies and reaction times of motor choices as functions of a sensory stimulus feature dimension. Here, we show that various saccade metrics (e.g., peak velocity) are similarly modulated as functions of sensory cue viewing time during performance of an urgent-decision task. Each of the newly discovered functions reveals the dynamics of the perceptual evaluation process inherent to the underlying judgment. Remarkably, saccade peak velocity correlates with statistical decision confidence, suggesting that saccade kinematics reflect the degree of certainty with which an urgent perceptual decision is made. The data were explained by a race-to-threshold model that also replicates standard performance measures and cortical oculomotor neuronal activity in the task. The results indicate that, although largely stereotyped, saccade metrics carry subtle but reliable traces of the underlying cognitive processes that give rise to each oculomotor choice.}, keywords = {}, pubstate = {published}, tppubtype = {article} } A perceptual judgment is typically characterized by constructing psychometric and chronometric functions, i.e., by mapping the accuracies and reaction times of motor choices as functions of a sensory stimulus feature dimension. Here, we show that various saccade metrics (e.g., peak velocity) are similarly modulated as functions of sensory cue viewing time during performance of an urgent-decision task. Each of the newly discovered functions reveals the dynamics of the perceptual evaluation process inherent to the underlying judgment. Remarkably, saccade peak velocity correlates with statistical decision confidence, suggesting that saccade kinematics reflect the degree of certainty with which an urgent perceptual decision is made. The data were explained by a race-to-threshold model that also replicates standard performance measures and cortical oculomotor neuronal activity in the task. The results indicate that, although largely stereotyped, saccade metrics carry subtle but reliable traces of the underlying cognitive processes that give rise to each oculomotor choice. |
Adam C Snyder; Deepa Issar; Matthew A Smith What does scalp electroencephalogram coherence tell us about long-range cortical networks? Journal Article European Journal of Neuroscience, pp. 1–16, 2018. @article{Snyder2018, title = {What does scalp electroencephalogram coherence tell us about long-range cortical networks?}, author = {Adam C Snyder and Deepa Issar and Matthew A Smith}, doi = {10.1111/ejn.13840}, year = {2018}, date = {2018-01-01}, journal = {European Journal of Neuroscience}, pages = {1--16}, abstract = {Long-range interactions between cortical areas are undoubtedly a key to the computational power of the brain. For healthy human subjects, the premier method for measuring brain activity on fast timescales is electroencephalography (EEG), and coherence between EEG signals is often used to assay functional connectivity between different brain regions. However, the nature of the underlying brain activity that is reflected in EEG coherence is currently the realm of speculation, because seldom have EEG signals been recorded simultaneously with intracranial recordings near cell bodies in multiple brain areas. Here, we take the early steps towards narrowing this gap in our understanding of EEG coherence by measuring local field potentials with microelectrode arrays in two brain areas (extrastriate visual area V4 and dorsolateral prefrontal cortex) simultaneously with EEG at the nearby scalp in rhesus macaque monkeys. Although we found inter-area coherence at both scales of measurement, we did not find that scalp-level coherence was reliably related to coherence between brain areas measured intracranially on a trial-to-trial basis, despite that scalp-level EEG was related to other important features of neural oscillations, such as trial-to-trial variability in overall amplitudes. This suggests that caution must be exercised when interpreting EEG coherence effects, and new theories devised about what aspects of neural activity long-range coherence in the EEG reflects.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Long-range interactions between cortical areas are undoubtedly a key to the computational power of the brain. For healthy human subjects, the premier method for measuring brain activity on fast timescales is electroencephalography (EEG), and coherence between EEG signals is often used to assay functional connectivity between different brain regions. However, the nature of the underlying brain activity that is reflected in EEG coherence is currently the realm of speculation, because seldom have EEG signals been recorded simultaneously with intracranial recordings near cell bodies in multiple brain areas. Here, we take the early steps towards narrowing this gap in our understanding of EEG coherence by measuring local field potentials with microelectrode arrays in two brain areas (extrastriate visual area V4 and dorsolateral prefrontal cortex) simultaneously with EEG at the nearby scalp in rhesus macaque monkeys. Although we found inter-area coherence at both scales of measurement, we did not find that scalp-level coherence was reliably related to coherence between brain areas measured intracranially on a trial-to-trial basis, despite that scalp-level EEG was related to other important features of neural oscillations, such as trial-to-trial variability in overall amplitudes. This suggests that caution must be exercised when interpreting EEG coherence effects, and new theories devised about what aspects of neural activity long-range coherence in the EEG reflects. |
Adam C Snyder; Byron M Yu; Matthew A Smith Distinct population codes for attention in the absence and presence of visual stimulation Journal Article Nature Communications, 9 (1), pp. 1–14, 2018. @article{Snyder2018a, title = {Distinct population codes for attention in the absence and presence of visual stimulation}, author = {Adam C Snyder and Byron M Yu and Matthew A Smith}, doi = {10.1038/s41467-018-06754-5}, year = {2018}, date = {2018-01-01}, journal = {Nature Communications}, volume = {9}, number = {1}, pages = {1--14}, publisher = {Springer US}, abstract = {Visual neurons respond more vigorously to an attended stimulus than an unattended one. How the brain prepares for response gain in anticipation of that stimulus is not well understood. One prominent proposal is that anticipation is characterized by gain-like modulations of spontaneous activity similar to gains in stimulus responses. Here we test an alternative idea: anticipation is characterized by a mixture of both increases and decreases of spontaneous firing rates. Such a strategy would be adaptive as it supports a simple linear scheme for disentangling internal, modulatory signals from external, sensory inputs. We recorded populations of V4 neurons in monkeys performing an attention task, and found that attention states are signaled by different mixtures of neurons across the population in the presence or absence of a stimulus. Our findings support a move from a stimulation-invariant account of anticipation towards a richer view of attentional modulation in a diverse neuronal population.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Visual neurons respond more vigorously to an attended stimulus than an unattended one. How the brain prepares for response gain in anticipation of that stimulus is not well understood. One prominent proposal is that anticipation is characterized by gain-like modulations of spontaneous activity similar to gains in stimulus responses. Here we test an alternative idea: anticipation is characterized by a mixture of both increases and decreases of spontaneous firing rates. Such a strategy would be adaptive as it supports a simple linear scheme for disentangling internal, modulatory signals from external, sensory inputs. We recorded populations of V4 neurons in monkeys performing an attention task, and found that attention states are signaled by different mixtures of neurons across the population in the presence or absence of a stimulus. Our findings support a move from a stimulation-invariant account of anticipation towards a richer view of attentional modulation in a diverse neuronal population. |
Jessica Taubert; Goedele Van Belle; Rufin Vogels; Bruno Rossion The impact of stimulus size and orientation on individual face coding in monkey face-selective cortex Journal Article Scientific Reports, 8 (1), pp. 1–9, 2018. @article{Taubert2018, title = {The impact of stimulus size and orientation on individual face coding in monkey face-selective cortex}, author = {Jessica Taubert and Goedele {Van Belle} and Rufin Vogels and Bruno Rossion}, doi = {10.1038/s41598-018-28144-z}, year = {2018}, date = {2018-01-01}, journal = {Scientific Reports}, volume = {8}, number = {1}, pages = {1--9}, publisher = {Springer US}, abstract = {Face-selective neurons in the monkey temporal cortex discharge at different rates in response to pictures of different individual faces. Here we tested whether this pattern of response across single neurons in the face-selective area ML (located in the middle Superior Temporal Sulcus) tolerates two affine transformations; picture-plane inversion, known to decrease the average response of face- selective neurons and the other, stimulus size. We recorded the response of 57 ML neurons in two awake and fixating monkeys. Face stimuli were presented at two sizes (10 and 5 degrees of visual angle) and two orientations (upright and inverted). Different faces elicited distinct patterns of activity across ML neurons that were reliable (i.e., predictable with a classifier) within a specific size and orientation condition. Despite observing a reduction in the average response magnitude of face-selective neurons to inverted faces, compared to upright faces, classifier performance was above chance for both upright and inverted faces. While decoding was largely preserved across changes in stimulus size, a classifier trained with one orientation condition and tested on the other did not lead to performance above chance level. We conclude that different individual faces can be decoded from patterns of responses in the monkey area ML regardless of orientation or size, but with qualitatively different patterns of responses for upright and inverted faces.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Face-selective neurons in the monkey temporal cortex discharge at different rates in response to pictures of different individual faces. Here we tested whether this pattern of response across single neurons in the face-selective area ML (located in the middle Superior Temporal Sulcus) tolerates two affine transformations; picture-plane inversion, known to decrease the average response of face- selective neurons and the other, stimulus size. We recorded the response of 57 ML neurons in two awake and fixating monkeys. Face stimuli were presented at two sizes (10 and 5 degrees of visual angle) and two orientations (upright and inverted). Different faces elicited distinct patterns of activity across ML neurons that were reliable (i.e., predictable with a classifier) within a specific size and orientation condition. Despite observing a reduction in the average response magnitude of face-selective neurons to inverted faces, compared to upright faces, classifier performance was above chance for both upright and inverted faces. While decoding was largely preserved across changes in stimulus size, a classifier trained with one orientation condition and tested on the other did not lead to performance above chance level. We conclude that different individual faces can be decoded from patterns of responses in the monkey area ML regardless of orientation or size, but with qualitatively different patterns of responses for upright and inverted faces. |
Kasper Vinken; Hans P Op de Beeck; Rufin Vogels Face repetition probability does not affect repetition suppression in macaque inferotemporal cortex Journal Article The Journal of Neuroscience, 38 (34), pp. 7492–7504, 2018. @article{Vinken2018, title = {Face repetition probability does not affect repetition suppression in macaque inferotemporal cortex}, author = {Kasper Vinken and Hans P {Op de Beeck} and Rufin Vogels}, doi = {10.1523/jneurosci.0462-18.2018}, year = {2018}, date = {2018-01-01}, journal = {The Journal of Neuroscience}, volume = {38}, number = {34}, pages = {7492--7504}, abstract = {Repetition suppression, which refers to reduced neural activity for repeated stimuli, is typically explained by bottom-up or local adaptation mechanisms. However, recent theories have emphasized the role of top-down processes, suggesting that this response reduction reflects the fulfillment of perceptual expectations. To support this, an influential human functional magnetic resonance imaging (fMRI) study showed that the magnitude of suppression is modulated by the probability of a repetition. No such repetition probability effect was found in macaque inferior temporal (IT) cortex for spiking activity, despite the presence of repetition suppression. Contrary to the human fMRI studies that showed an effect of repetition probability, the macaque single unit study employed a large variety of unfamiliar stimuli and the monkeys were not required to attend the stimuli. Here, as in the human fMRI studies, we employed faces as stimuli and made the monkeys attend to the stimulus content. We simultaneously recorded spiking activity and local field potentials (LFPs) in the middle lateral face patch (ML) of one monkey (male), and a face-responsive region of another (female). While we observed significant repetition suppression of spiking activity and high gamma band LFPs in both animals, there were no effects of repetition probability, even when repetitions were task-relevant and repetition probability affected behavioral decisions. In conclusion, despite the use of face stimuli and a stimulus-related task, no neural signature of repetition probability was present for faces in a face responsive patch of macaque IT. This further challenges a general perceptual expectation account of repetition suppression.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Repetition suppression, which refers to reduced neural activity for repeated stimuli, is typically explained by bottom-up or local adaptation mechanisms. However, recent theories have emphasized the role of top-down processes, suggesting that this response reduction reflects the fulfillment of perceptual expectations. To support this, an influential human functional magnetic resonance imaging (fMRI) study showed that the magnitude of suppression is modulated by the probability of a repetition. No such repetition probability effect was found in macaque inferior temporal (IT) cortex for spiking activity, despite the presence of repetition suppression. Contrary to the human fMRI studies that showed an effect of repetition probability, the macaque single unit study employed a large variety of unfamiliar stimuli and the monkeys were not required to attend the stimuli. Here, as in the human fMRI studies, we employed faces as stimuli and made the monkeys attend to the stimulus content. We simultaneously recorded spiking activity and local field potentials (LFPs) in the middle lateral face patch (ML) of one monkey (male), and a face-responsive region of another (female). While we observed significant repetition suppression of spiking activity and high gamma band LFPs in both animals, there were no effects of repetition probability, even when repetitions were task-relevant and repetition probability affected behavioral decisions. In conclusion, despite the use of face stimuli and a stimulus-related task, no neural signature of repetition probability was present for faces in a face responsive patch of macaque IT. This further challenges a general perceptual expectation account of repetition suppression. |
Jing Wang; Devika Narain; Eghbal A Hosseini; Mehrdad Jazayeri Flexible timing by temporal scaling of cortical responses Journal Article Nature Neuroscience, 21 (1), pp. 102–112, 2018. @article{Wang2018h, title = {Flexible timing by temporal scaling of cortical responses}, author = {Jing Wang and Devika Narain and Eghbal A Hosseini and Mehrdad Jazayeri}, doi = {10.1038/s41593-017-0028-6}, year = {2018}, date = {2018-01-01}, journal = {Nature Neuroscience}, volume = {21}, number = {1}, pages = {102--112}, publisher = {Springer US}, abstract = {Musicians can perform at different tempos, speakers can control the cadence of their speech, and children can flexibly vary their temporal expectations of events. To understand the neural basis of such flexibility, we recorded from the medial frontal cortex of nonhuman primates trained to produce different time intervals with different effectors. Neural responses were heterogeneous, nonlinear, and complex, and they exhibited a remarkable form of temporal invariance: firing rate profiles were temporally scaled to match the produced intervals. Recording from downstream neurons in the caudate and from thalamic neurons projecting to the medial frontal cortex indicated that this phenomenon originates within cortical networks. Recurrent neural network models trained to perform the task revealed that temporal scaling emerges from nonlinearities in the network and that the degree of scaling is controlled by the strength of external input. These findings demonstrate a simple and general mechanism for conferring temporal flexibility upon sensorimotor and cognitive functions.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Musicians can perform at different tempos, speakers can control the cadence of their speech, and children can flexibly vary their temporal expectations of events. To understand the neural basis of such flexibility, we recorded from the medial frontal cortex of nonhuman primates trained to produce different time intervals with different effectors. Neural responses were heterogeneous, nonlinear, and complex, and they exhibited a remarkable form of temporal invariance: firing rate profiles were temporally scaled to match the produced intervals. Recording from downstream neurons in the caudate and from thalamic neurons projecting to the medial frontal cortex indicated that this phenomenon originates within cortical networks. Recurrent neural network models trained to perform the task revealed that temporal scaling emerges from nonlinearities in the network and that the degree of scaling is controlled by the strength of external input. These findings demonstrate a simple and general mechanism for conferring temporal flexibility upon sensorimotor and cognitive functions. |
Andreas Wutz; Roman Loonis; Jefferson E Roy; Jacob A Donoghue; Earl K Miller Different levels of category abstraction by different dynamics in different prefrontal areas Journal Article Neuron, 97 (3), pp. 716–726, 2018. @article{Wutz2018, title = {Different levels of category abstraction by different dynamics in different prefrontal areas}, author = {Andreas Wutz and Roman Loonis and Jefferson E Roy and Jacob A Donoghue and Earl K Miller}, doi = {10.1016/j.neuron.2018.01.009}, year = {2018}, date = {2018-01-01}, journal = {Neuron}, volume = {97}, number = {3}, pages = {716--726}, publisher = {Elsevier Inc.}, abstract = {Categories can be grouped by shared sensory attributes (i.e., cats) or a more abstract rule (i.e., animals). We explored the neural basis of abstraction by recording from multi-electrode arrays in prefrontal cortex (PFC) while monkeys performed a dot-pattern categorization task. Category abstraction was varied by the degree of exemplar distortion from the prototype pattern. Different dynamics in different PFC regions processed different levels of category abstraction. Bottom-up dynamics (stimulus-locked gamma power and spiking) in the ventral PFC processed more low-level abstractions, whereas top-down dynamics (beta power and beta spike-LFP coherence) in the dorsal PFC processed more high-level abstractions. Our results suggest a two-stage, rhythm-based model for abstracting categories.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Categories can be grouped by shared sensory attributes (i.e., cats) or a more abstract rule (i.e., animals). We explored the neural basis of abstraction by recording from multi-electrode arrays in prefrontal cortex (PFC) while monkeys performed a dot-pattern categorization task. Category abstraction was varied by the degree of exemplar distortion from the prototype pattern. Different dynamics in different PFC regions processed different levels of category abstraction. Bottom-up dynamics (stimulus-locked gamma power and spiking) in the ventral PFC processed more low-level abstractions, whereas top-down dynamics (beta power and beta spike-LFP coherence) in the dorsal PFC processed more high-level abstractions. Our results suggest a two-stage, rhythm-based model for abstracting categories. |
Yang Xie; Chechang Nie; Tianming Yang Covert shift of attention modulates the value encoding in the orbitofrontal cortex Journal Article eLife, 7 , pp. 1–21, 2018. @article{Xie2018b, title = {Covert shift of attention modulates the value encoding in the orbitofrontal cortex}, author = {Yang Xie and Chechang Nie and Tianming Yang}, doi = {10.7554/elife.31507}, year = {2018}, date = {2018-01-01}, journal = {eLife}, volume = {7}, pages = {1--21}, abstract = {During value-based decision making, we often evaluate the value of each option sequentially by shifting our attention, even when the options are presented simultaneously. The orbitofrontal cortex (OFC) has been suggested to encode value during value-based decision making. Yet it is not known how its activity is modulated by attention shifts. We investigated this question by employing a passive viewing task that allowed us to disentangle effects of attention, value, choice and eye movement. We found that the attention modulated OFC activity through a winner-take-all mechanism. When we attracted the monkeys' attention covertly, the OFC neuronal activity reflected the reward value of the newly attended cue. The shift of attention could be explained by a normalization model. Our results strongly argue for the hypothesis that the OFC neuronal activity represents the value of the attended item. They provide important insights toward understanding the OFC's role in value-based decision making.}, keywords = {}, pubstate = {published}, tppubtype = {article} } During value-based decision making, we often evaluate the value of each option sequentially by shifting our attention, even when the options are presented simultaneously. The orbitofrontal cortex (OFC) has been suggested to encode value during value-based decision making. Yet it is not known how its activity is modulated by attention shifts. We investigated this question by employing a passive viewing task that allowed us to disentangle effects of attention, value, choice and eye movement. We found that the attention modulated OFC activity through a winner-take-all mechanism. When we attracted the monkeys' attention covertly, the OFC neuronal activity reflected the reward value of the newly attended cue. The shift of attention could be explained by a normalization model. Our results strongly argue for the hypothesis that the OFC neuronal activity represents the value of the attended item. They provide important insights toward understanding the OFC's role in value-based decision making. |
Yin Yan; Li Zhaoping; Wu Li Bottom-up saliency and top-down learning in the primary visual cortex of monkeys Journal Article Proceedings of the National Academy of Sciences, 115 (41), pp. 10499–10504, 2018. @article{Yan2018a, title = {Bottom-up saliency and top-down learning in the primary visual cortex of monkeys}, author = {Yin Yan and Li Zhaoping and Wu Li}, doi = {10.1073/pnas.1803854115}, year = {2018}, date = {2018-01-01}, journal = {Proceedings of the National Academy of Sciences}, volume = {115}, number = {41}, pages = {10499--10504}, abstract = {Early sensory cortex is better known for representing sensory inputs but less for the effect of its responses on behavior. Here we explore the behavioral correlates of neuronal responses in primary visual cortex (V1) in a task to detect a uniquely oriented bar-the orientation singleton-in a background of uniformly oriented bars. This singleton is salient or inconspicuous when the orientation contrast between the singleton and background bars is sufficiently large or small, respectively. Using implanted microelectrodes, we measured V1 activities while monkeys were trained to quickly saccade to the singleton. A neuron's responses to the singleton within its receptive field had an early and a late component, both increased with the orientation contrast. The early component started from the outset of neuronal responses; it remained unchanged before and after training on the singleton detection. The late component started ∼40 ms after the early one; it emerged and evolved with practicing the detection task. Training increased the behavioral accuracy and speed of singleton detection and increased the amount of information in the late response component about a singleton's presence or absence. Furthermore, for a given singleton, faster detection performance was associated with higher V1 responses; training increased this be-havioral-neural correlate in the early V1 responses but decreased it in the late V1 responses. Therefore, V1's early responses are directly linked with behavior and represent the bottom-up saliency signals. Learning strengthens this link, likely serving as the basis for making the detection task more reflexive and less top-down driven.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Early sensory cortex is better known for representing sensory inputs but less for the effect of its responses on behavior. Here we explore the behavioral correlates of neuronal responses in primary visual cortex (V1) in a task to detect a uniquely oriented bar-the orientation singleton-in a background of uniformly oriented bars. This singleton is salient or inconspicuous when the orientation contrast between the singleton and background bars is sufficiently large or small, respectively. Using implanted microelectrodes, we measured V1 activities while monkeys were trained to quickly saccade to the singleton. A neuron's responses to the singleton within its receptive field had an early and a late component, both increased with the orientation contrast. The early component started from the outset of neuronal responses; it remained unchanged before and after training on the singleton detection. The late component started ∼40 ms after the early one; it emerged and evolved with practicing the detection task. Training increased the behavioral accuracy and speed of singleton detection and increased the amount of information in the late response component about a singleton's presence or absence. Furthermore, for a given singleton, faster detection performance was associated with higher V1 responses; training increased this be-havioral-neural correlate in the early V1 responses but decreased it in the late V1 responses. Therefore, V1's early responses are directly linked with behavior and represent the bottom-up saliency signals. Learning strengthens this link, likely serving as the basis for making the detection task more reflexive and less top-down driven. |
Sheng-Tao Yang; Min Wang; Constantinos D Paspalas; Johanna L Crimins; Marcus T Altman; James A Mazer; Amy F T Arnsten Core differences in synaptic signaling between primary visual and dorsolateral prefrontal cortex Journal Article Cerebral Cortex, 28 (4), pp. 1458–1471, 2018. @article{Yang2018, title = {Core differences in synaptic signaling between primary visual and dorsolateral prefrontal cortex}, author = {Sheng-Tao Yang and Min Wang and Constantinos D Paspalas and Johanna L Crimins and Marcus T Altman and James A Mazer and Amy F T Arnsten}, doi = {10.1093/cercor/bhx357}, year = {2018}, date = {2018-01-01}, journal = {Cerebral Cortex}, volume = {28}, number = {4}, pages = {1458--1471}, abstract = {Neurons in primary visual cortex (V1) are more resilient than those in dorsolateral prefrontal cortex (dlPFC) in aging, schizophrenia and Alzheimer's disease. The current study compared glutamate and neuromodulatory actions in macaque V1 to those in dlPFC, and found striking regional differences. V1 neuronal firing to visual stimuli depended on AMPA receptors, with subtle NMDA receptor contributions, while dlPFC depends primarily on NMDA receptors. Neuromodulatory actions also differed between regions. In V1, cAMP signaling increased neuronal firing, and the phosphodiesterase PDE4A was positioned to regulate cAMP effects on glutamate release from axons. HCN channels in V1 were classically located on distal dendrites, and enhanced cell firing. These data contrast with dlPFC, where PDE4A and HCN channels are concentrated in thin spines, and cAMP-HCN signaling gates inputs and weakens firing. These regional differences may explain why V1 neurons are more resilient than dlPFC neurons to the challenges of age and disease.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Neurons in primary visual cortex (V1) are more resilient than those in dorsolateral prefrontal cortex (dlPFC) in aging, schizophrenia and Alzheimer's disease. The current study compared glutamate and neuromodulatory actions in macaque V1 to those in dlPFC, and found striking regional differences. V1 neuronal firing to visual stimuli depended on AMPA receptors, with subtle NMDA receptor contributions, while dlPFC depends primarily on NMDA receptors. Neuromodulatory actions also differed between regions. In V1, cAMP signaling increased neuronal firing, and the phosphodiesterase PDE4A was positioned to regulate cAMP effects on glutamate release from axons. HCN channels in V1 were classically located on distal dendrites, and enhanced cell firing. These data contrast with dlPFC, where PDE4A and HCN channels are concentrated in thin spines, and cAMP-HCN signaling gates inputs and weakens firing. These regional differences may explain why V1 neurons are more resilient than dlPFC neurons to the challenges of age and disease. |
Tao Yao; Stefan Treue; Suresh B Krishna Saccade-synchronized rapid attention shifts in macaque visual cortical area MT Journal Article Nature Communications, 9 (1), pp. 1–9, 2018. @article{Yao2018, title = {Saccade-synchronized rapid attention shifts in macaque visual cortical area MT}, author = {Tao Yao and Stefan Treue and Suresh B Krishna}, doi = {10.1038/s41467-018-03398-3}, year = {2018}, date = {2018-01-01}, journal = {Nature Communications}, volume = {9}, number = {1}, pages = {1--9}, publisher = {Springer US}, abstract = {While making saccadic eye-movements to scan a visual scene, humans and monkeys are able to keep track of relevant visual stimuli by maintaining spatial attention on them. This ability requires a shift of attentional modulation from the neuronal population representing the relevant stimulus pre-saccadically to the one representing it post-saccadically. For optimal performance, this trans-saccadic attention shift should be rapid and saccade-synchronized. Whether this is so is not known. We trained two rhesus monkeys to make saccades while maintaining covert attention at a fixed spatial location. We show that the trans-saccadic attention shift in cortical visual medial temporal (MT) area is well synchronized to saccades. Attentional modulation crosses over from the pre-saccadic to the post-saccadic neuronal representation by about 50 ms after a saccade. Taking response latency into account, the trans-saccadic attention shift is well timed to maintain spatial attention on relevant stimuli, so that they can be optimally tracked and processed across saccades.}, keywords = {}, pubstate = {published}, tppubtype = {article} } While making saccadic eye-movements to scan a visual scene, humans and monkeys are able to keep track of relevant visual stimuli by maintaining spatial attention on them. This ability requires a shift of attentional modulation from the neuronal population representing the relevant stimulus pre-saccadically to the one representing it post-saccadically. For optimal performance, this trans-saccadic attention shift should be rapid and saccade-synchronized. Whether this is so is not known. We trained two rhesus monkeys to make saccades while maintaining covert attention at a fixed spatial location. We show that the trans-saccadic attention shift in cortical visual medial temporal (MT) area is well synchronized to saccades. Attentional modulation crosses over from the pre-saccadic to the post-saccadic neuronal representation by about 50 ms after a saccade. Taking response latency into account, the trans-saccadic attention shift is well timed to maintain spatial attention on relevant stimuli, so that they can be optimally tracked and processed across saccades. |
Seng Bum Michael Yoo; Brianna J Sleezer; Benjamin Y Hayden Robust encoding of spatial information in orbitofrontal cortex and striatum Journal Article Journal of Cognitive Neuroscience, 30 (6), pp. 898–913, 2018. @article{Yoo2018c, title = {Robust encoding of spatial information in orbitofrontal cortex and striatum}, author = {Seng Bum Michael Yoo and Brianna J Sleezer and Benjamin Y Hayden}, doi = {10.1162/jocn}, year = {2018}, date = {2018-01-01}, journal = {Journal of Cognitive Neuroscience}, volume = {30}, number = {6}, pages = {898--913}, abstract = {Knowing whether core reward regions carry information about the positions of relevant objects is crucial for adjudicating between choice models. One limitation of previous studies, including our own, is that spatial positions can be consistently differentially associated with rewards, and thus position can be confounded with attention, motor plans, or target identity. We circumvented these problems by using a task in which value— and thus choices—was determined solely by a frequently changing rule, which was randomized relative to spatial position on each trial. We presented offers asynchronously, which allowed us to control for reward expectation, spatial attention, and motor plans in our analyses. We find robust encoding of the spatial position of both offers and choices in two core reward regions, orbitofrontal Area 13 and ventral striatum, as well as in dorsal striatum of macaques. The trial-by-trial correlation in noise in encoding of position was associated with variation in choice, an effect known as choice probability correlation, suggesting that the spatial encoding is associated with choice and is not incidental to it. Spatial information and reward information are not carried by separate sets of neurons, although the two forms of information are temporally dissociable. These results highlight the ubiquity of multiplexed information in association cortex and argue against the idea that these ostensible reward regions serve as part of a pure value domain.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Knowing whether core reward regions carry information about the positions of relevant objects is crucial for adjudicating between choice models. One limitation of previous studies, including our own, is that spatial positions can be consistently differentially associated with rewards, and thus position can be confounded with attention, motor plans, or target identity. We circumvented these problems by using a task in which value— and thus choices—was determined solely by a frequently changing rule, which was randomized relative to spatial position on each trial. We presented offers asynchronously, which allowed us to control for reward expectation, spatial attention, and motor plans in our analyses. We find robust encoding of the spatial position of both offers and choices in two core reward regions, orbitofrontal Area 13 and ventral striatum, as well as in dorsal striatum of macaques. The trial-by-trial correlation in noise in encoding of position was associated with variation in choice, an effect known as choice probability correlation, suggesting that the spatial encoding is associated with choice and is not incidental to it. Spatial information and reward information are not carried by separate sets of neurons, although the two forms of information are temporally dissociable. These results highlight the ubiquity of multiplexed information in association cortex and argue against the idea that these ostensible reward regions serve as part of a pure value domain. |
2017 |
Jordi Aguila; Javier F Cudeiro; Casto Rivadulla Cerebral Cortex, 27 (6), pp. 3331–3345, 2017. @article{Aguila2017, title = {Suppression of V1 feedback produces a shift in the topographic representation of receptive fields of LGN cells by unmasking latent retinal drives}, author = {Jordi Aguila and Javier F Cudeiro and Casto Rivadulla}, doi = {10.1093/cercor/bhx071}, year = {2017}, date = {2017-01-01}, journal = {Cerebral Cortex}, volume = {27}, number = {6}, pages = {3331--3345}, abstract = {In awake monkeys, we used repetitive transcranial magnetic stimulation (rTMS) to focally inactivate visual cortex while measuring the responsiveness of parvocellular lateral geniculate nucleus (LGN) neurons. Effects were noted in 64/75 neurons, and could be divided into 2 main groups: (1) for 39 neurons, visual responsiveness decreased and visual latency increased without apparent shift in receptive field (RF) position and (2) a second group (n = 25, 33% of the recorded cells) whose excitability was not compromised, but whose RF position shifted an average of 4.5°. This change is related to the retinotopic correspondence observed between the recorded thalamic area and the affected cortical zone. The effect of inactivation for this group of neurons was compatible with silencing the original retinal drive and unmasking a second latent retinal drive onto the studied neuron. These results indicate novel and remarkable dynamics in thalamocortical circuitry that force us to reassess constraints on retinogeniculate transmission.}, keywords = {}, pubstate = {published}, tppubtype = {article} } In awake monkeys, we used repetitive transcranial magnetic stimulation (rTMS) to focally inactivate visual cortex while measuring the responsiveness of parvocellular lateral geniculate nucleus (LGN) neurons. Effects were noted in 64/75 neurons, and could be divided into 2 main groups: (1) for 39 neurons, visual responsiveness decreased and visual latency increased without apparent shift in receptive field (RF) position and (2) a second group (n = 25, 33% of the recorded cells) whose excitability was not compromised, but whose RF position shifted an average of 4.5°. This change is related to the retinotopic correspondence observed between the recorded thalamic area and the affected cortical zone. The effect of inactivation for this group of neurons was compatible with silencing the original retinal drive and unmasking a second latent retinal drive onto the studied neuron. These results indicate novel and remarkable dynamics in thalamocortical circuitry that force us to reassess constraints on retinogeniculate transmission. |
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. @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. @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}, 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. |
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. @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}, 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. |
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. @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}, 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. @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}, 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. |
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. @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}, 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. |
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. @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}, 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. |
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. @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}, 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. |
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. @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}, 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. |
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. @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. @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. |
Becket R Ebitz; Tirin Moore Selective modulation of the pupil light reflex by microstimulation of prefrontal cortex Journal Article The Journal of Neuroscience, 37 (19), pp. 5008–5018, 2017. @article{Ebitz2017, title = {Selective modulation of the pupil light reflex by microstimulation of prefrontal cortex}, author = {Becket R Ebitz and Tirin Moore}, doi = {10.1523/JNEUROSCI.2433-16.2017}, year = {2017}, date = {2017-01-01}, journal = {The 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. |
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. @article{Fan2017a, 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. |
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. @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}, 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. |
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. @article{Gutnisky2017, 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. |
Diego A Gutnisky; Charles Beaman; Sergio E Lew; Valentin Dragoi Cortical response states for enhanced sensory discrimination Journal Article eLife, 6 , pp. 1–23, 2017. @article{Gutnisky2017a, title = {Cortical response states for enhanced sensory discrimination}, author = {Diego A Gutnisky and Charles Beaman and Sergio E Lew and Valentin Dragoi}, doi = {10.7554/eLife.29226}, year = {2017}, date = {2017-01-01}, journal = {eLife}, volume = {6}, pages = {1--23}, abstract = {Brain activity during wakefulness is characterized by rapid fluctuations in neuronal responses. Whether these fluctuations play any role in modulating the accuracy of behavioral responses is poorly understood. Here, we investigated whether and how trial changes in the population response impact sensory coding in monkey V1 and perceptual performance. Although the responses of individual neurons varied widely across trials, many cells tended to covary with the local population. When population activity was in a 'low' state, neurons had lower evoked responses and correlated variability, yet higher probability to predict perceptual accuracy. The impact of firing rate fluctuations on network and perceptual accuracy was strongest 200-ms before stimulus presentation, and it greatly diminished when the number of cells used to measure the state of the population was decreased. These findings indicate that enhanced perceptual discrimination occurs when population activity is in a 'silent' response mode in which neurons increase information extraction.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Brain activity during wakefulness is characterized by rapid fluctuations in neuronal responses. Whether these fluctuations play any role in modulating the accuracy of behavioral responses is poorly understood. Here, we investigated whether and how trial changes in the population response impact sensory coding in monkey V1 and perceptual performance. Although the responses of individual neurons varied widely across trials, many cells tended to covary with the local population. When population activity was in a 'low' state, neurons had lower evoked responses and correlated variability, yet higher probability to predict perceptual accuracy. The impact of firing rate fluctuations on network and perceptual accuracy was strongest 200-ms before stimulus presentation, and it greatly diminished when the number of cells used to measure the state of the population was decreased. These findings indicate that enhanced perceptual discrimination occurs when population activity is in a 'silent' response mode in which neurons increase information extraction. |
Gerald Hahn; Adrian Ponce-Alvarez; Cyril Monier; Giacomo Benvenuti; Arvind Kumar; Frédéric Chavane; Gustavo Deco; Yves Frégnac Spontaneous cortical activity is transiently poised close to criticality Journal Article PLoS Computational Biology, 13 (5), pp. 1–29, 2017. @article{Hahn2017, title = {Spontaneous cortical activity is transiently poised close to criticality}, author = {Gerald Hahn and Adrian Ponce-Alvarez and Cyril Monier and Giacomo Benvenuti and Arvind Kumar and Frédéric Chavane and Gustavo Deco and Yves Frégnac}, doi = {10.1371/journal.pcbi.1005543}, year = {2017}, date = {2017-01-01}, journal = {PLoS Computational Biology}, volume = {13}, number = {5}, pages = {1--29}, abstract = {Brain activity displays a large repertoire of dynamics across the sleep-wake cycle and even during anesthesia. It was suggested that criticality could serve as a unifying principle underlying the diversity of dynamics. This view has been supported by the observation of spontaneous bursts of cortical activity with scale-invariant sizes and durations, known as neuronal avalanches, in recordings of mesoscopic cortical signals. However, the existence of neuronal avalanches in spiking activity has been equivocal with studies reporting both its presence and absence. Here, we show that signs of criticality in spiking activity can change between synchronized and desynchronized cortical states. We analyzed the spontaneous activity in the primary visual cortex of the anesthetized cat and the awake monkey, and found that neuronal avalanches and thermodynamic indicators of criticality strongly depend on collective synchrony among neurons, LFP fluctuations, and behavioral state. We found that synchronized states are associated to criticality, large dynamical repertoire and prolonged epochs of eye closure, while desynchronized states are associated to sub-criticality, reduced dynamical repertoire, and eyes open conditions. Our results show that criticality in cortical dynamics is not stationary, but fluctuates during anesthesia and between different vigilance states.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Brain activity displays a large repertoire of dynamics across the sleep-wake cycle and even during anesthesia. It was suggested that criticality could serve as a unifying principle underlying the diversity of dynamics. This view has been supported by the observation of spontaneous bursts of cortical activity with scale-invariant sizes and durations, known as neuronal avalanches, in recordings of mesoscopic cortical signals. However, the existence of neuronal avalanches in spiking activity has been equivocal with studies reporting both its presence and absence. Here, we show that signs of criticality in spiking activity can change between synchronized and desynchronized cortical states. We analyzed the spontaneous activity in the primary visual cortex of the anesthetized cat and the awake monkey, and found that neuronal avalanches and thermodynamic indicators of criticality strongly depend on collective synchrony among neurons, LFP fluctuations, and behavioral state. We found that synchronized states are associated to criticality, large dynamical repertoire and prolonged epochs of eye closure, while desynchronized states are associated to sub-criticality, reduced dynamical repertoire, and eyes open conditions. Our results show that criticality in cortical dynamics is not stationary, but fluctuates during anesthesia and between different vigilance states. |
S A Hassani; M Oemisch; M Balcarras; S Westendorff; S Ardid; M A van der Meer; P Tiesinga; T Womelsdorf Scientific Reports, 7 , pp. 1–19, 2017. @article{Hassani2017, title = {A computational psychiatry approach identifies how alpha-2A noradrenergic agonist Guanfacine affects feature-based reinforcement learning in the macaque}, author = {S A Hassani and M Oemisch and M Balcarras and S Westendorff and S Ardid and M A van der Meer and P Tiesinga and T Womelsdorf}, doi = {10.1038/srep40606}, year = {2017}, date = {2017-01-01}, journal = {Scientific Reports}, volume = {7}, pages = {1--19}, publisher = {Nature Publishing Group}, abstract = {Noradrenaline is believed to support cognitive flexibility through the alpha 2A noradrenergic receptor (a2A-NAR) acting in prefrontal cortex. Enhanced flexibility has been inferred from improved working memory with the a2A-NA agonist Guanfacine. But it has been unclear whether Guanfacine improves specific attention and learning mechanisms beyond working memory, and whether the drug effects can be formalized computationally to allow single subject predictions. We tested and confirmed these suggestions in a case study with a healthy nonhuman primate performing a feature-based reversal learning task evaluating performance using Bayesian and Reinforcement learning models. In an initial dose-testing phase we found a Guanfacine dose that increased performance accuracy, decreased distractibility and improved learning. In a second experimental phase using only that dose we examined the faster feature-based reversal learning with Guanfacine with single-subject computational modeling. Parameter estimation suggested that improved learning is not accounted for by varying a single reinforcement learning mechanism, but by changing the set of parameter values to higher learning rates and stronger suppression of non-chosen over chosen feature information. These findings provide an important starting point for developing nonhuman primate models to discern the synaptic mechanisms of attention and learning functions within the context of a computational neuropsychiatry framework.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Noradrenaline is believed to support cognitive flexibility through the alpha 2A noradrenergic receptor (a2A-NAR) acting in prefrontal cortex. Enhanced flexibility has been inferred from improved working memory with the a2A-NA agonist Guanfacine. But it has been unclear whether Guanfacine improves specific attention and learning mechanisms beyond working memory, and whether the drug effects can be formalized computationally to allow single subject predictions. We tested and confirmed these suggestions in a case study with a healthy nonhuman primate performing a feature-based reversal learning task evaluating performance using Bayesian and Reinforcement learning models. In an initial dose-testing phase we found a Guanfacine dose that increased performance accuracy, decreased distractibility and improved learning. In a second experimental phase using only that dose we examined the faster feature-based reversal learning with Guanfacine with single-subject computational modeling. Parameter estimation suggested that improved learning is not accounted for by varying a single reinforcement learning mechanism, but by changing the set of parameter values to higher learning rates and stronger suppression of non-chosen over chosen feature information. These findings provide an important starting point for developing nonhuman primate models to discern the synaptic mechanisms of attention and learning functions within the context of a computational neuropsychiatry framework. |
James P Herman; Richard J Krauzlis Color-change detection activity in the primate superior colliculus Journal Article eNeuro, 4 (2), pp. 1–16, 2017. @article{Herman2017, title = {Color-change detection activity in the primate superior colliculus}, author = {James P Herman and Richard J Krauzlis}, doi = {10.1523/ENEURO.0046-17.2017}, year = {2017}, date = {2017-01-01}, journal = {eNeuro}, volume = {4}, number = {2}, pages = {1--16}, abstract = {The primate superior colliculus (SC) is a midbrain structure that participates in the control of spatial attention. Previous studies examining the role of the SC in attention have mostly used luminance-based visual features (e.g., motion, contrast) as the stimuli and saccadic eye movements as the behavioral response, both of which are known to modulate the activity of SC neurons. To explore the limits of the SC's involvement in the control of spatial attention, we recorded SC neuronal activity during a task using color, a visual feature dimension not traditionally associated with the SC, and required monkeys to detect threshold-level changes in the saturation of a cued stimulus by releasing a joystick during maintained fixation. Using this color-based spatial attention task, we found substantial cue-related modulation in all categories of visually responsive neurons in the intermediate layers of the SC. Notably, near-threshold changes in color saturation, both increases and decreases, evoked phasic bursts of activity with magnitudes as large as those evoked by stimulus onset. This change-detection activity had two distinctive features: activity for hits was larger than for misses, and the timing of change-detection activity accounted for 67% of joystick release latency, even though it preceded the release by at least 200 ms. We conclude that during attention tasks, SC activity denotes the behavioral relevance of the stimulus regardless of feature dimension and that phasic event-related SC activity is suitable to guide the selection of manual responses as well as saccadic eye movements.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The primate superior colliculus (SC) is a midbrain structure that participates in the control of spatial attention. Previous studies examining the role of the SC in attention have mostly used luminance-based visual features (e.g., motion, contrast) as the stimuli and saccadic eye movements as the behavioral response, both of which are known to modulate the activity of SC neurons. To explore the limits of the SC's involvement in the control of spatial attention, we recorded SC neuronal activity during a task using color, a visual feature dimension not traditionally associated with the SC, and required monkeys to detect threshold-level changes in the saturation of a cued stimulus by releasing a joystick during maintained fixation. Using this color-based spatial attention task, we found substantial cue-related modulation in all categories of visually responsive neurons in the intermediate layers of the SC. Notably, near-threshold changes in color saturation, both increases and decreases, evoked phasic bursts of activity with magnitudes as large as those evoked by stimulus onset. This change-detection activity had two distinctive features: activity for hits was larger than for misses, and the timing of change-detection activity accounted for 67% of joystick release latency, even though it preceded the release by at least 200 ms. We conclude that during attention tasks, SC activity denotes the behavioral relevance of the stimulus regardless of feature dimension and that phasic event-related SC activity is suitable to guide the selection of manual responses as well as saccadic eye movements. |
Markus A Hietanen; Nicholas S C Price; Shaun L Cloherty; Kostas Hadjidimitrakis; Michael R Ibbotson Long-term sensorimotor adaptation in the ocular following system of primates Journal Article PLoS ONE, 12 (12), pp. 1–15, 2017. @article{Hietanen2017, title = {Long-term sensorimotor adaptation in the ocular following system of primates}, author = {Markus A Hietanen and Nicholas S C Price and Shaun L Cloherty and Kostas Hadjidimitrakis and Michael R Ibbotson}, doi = {10.1371/journal.pone.0189030}, year = {2017}, date = {2017-01-01}, journal = {PLoS ONE}, volume = {12}, number = {12}, pages = {1--15}, abstract = {The sudden movement of a wide-field image leads to a reflexive eye tracking response referred to as short-latency ocular following. If the image motion occurs soon after a saccade the initial speed of the ocular following is enhanced, a phenomenon known as post-saccadic enhancement. We show in macaque monkeys that repeated exposure to the same stimulus regime over a period of months leads to progressive increases in the initial speeds of ocular following. The improvement in tracking speed occurs for ocular following with and without a prior saccade. As a result of the improvement in ocular following speeds, the influence of post-saccadic enhancement wanes with increasing levels of training. The improvement in ocular following speed following repeated exposure to the same oculomotor task represents a novel form of sensori-motor learning in the context of a reflexive movement.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The sudden movement of a wide-field image leads to a reflexive eye tracking response referred to as short-latency ocular following. If the image motion occurs soon after a saccade the initial speed of the ocular following is enhanced, a phenomenon known as post-saccadic enhancement. We show in macaque monkeys that repeated exposure to the same stimulus regime over a period of months leads to progressive increases in the initial speeds of ocular following. The improvement in tracking speed occurs for ocular following with and without a prior saccade. As a result of the improvement in ocular following speeds, the influence of post-saccadic enhancement wanes with increasing levels of training. The improvement in ocular following speed following repeated exposure to the same oculomotor task represents a novel form of sensori-motor learning in the context of a reflexive movement. |
Guilhem Ibos; David J Freedman Sequential sensory and decision processing in posterior parietal cortex Journal Article eLife, 6 , pp. 1–19, 2017. @article{Ibos2017, title = {Sequential sensory and decision processing in posterior parietal cortex}, author = {Guilhem Ibos and David J Freedman}, doi = {10.7554/eLife.23743}, year = {2017}, date = {2017-01-01}, journal = {eLife}, volume = {6}, pages = {1--19}, abstract = {textlessptextgreaterDecisions about the behavioral significance of sensory stimuli often require comparing sensory inference of what we are looking at to internal models of what we are looking for. Here, we test how neuronal selectivity for visual features is transformed into decision-related signals in posterior parietal cortex (area LIP). Monkeys performed a visual matching task that required them to detect target stimuli composed of conjunctions of color and motion-direction. Neuronal recordings from area LIP revealed two main findings. First, the sequential processing of visual features and the selection of target-stimuli suggest that LIP is involved in transforming sensory information into decision-related signals. Second, the patterns of color and motion selectivity and their impact on decision-related encoding suggest that LIP plays a role in detecting target stimuli by comparing bottom-up sensory inputs (what the monkeys were looking at) and top-down cognitive encoding inputs (what the monkeys were looking for).textless/ptextgreater}, keywords = {}, pubstate = {published}, tppubtype = {article} } textlessptextgreaterDecisions about the behavioral significance of sensory stimuli often require comparing sensory inference of what we are looking at to internal models of what we are looking for. Here, we test how neuronal selectivity for visual features is transformed into decision-related signals in posterior parietal cortex (area LIP). Monkeys performed a visual matching task that required them to detect target stimuli composed of conjunctions of color and motion-direction. Neuronal recordings from area LIP revealed two main findings. First, the sequential processing of visual features and the selection of target-stimuli suggest that LIP is involved in transforming sensory information into decision-related signals. Second, the patterns of color and motion selectivity and their impact on decision-related encoding suggest that LIP plays a role in detecting target stimuli by comparing bottom-up sensory inputs (what the monkeys were looking at) and top-down cognitive encoding inputs (what the monkeys were looking for).textless/ptextgreater |
Nan Jia; Scott L Brincat; Andrés F Salazar-Gómez; Mikhail Panko; Frank H Guenther; Earl K Miller Decoding of intended saccade direction in an oculomotor brain-computer interface Journal Article Journal of Neural Engineering, 14 (4), pp. 1–13, 2017. @article{Jia2017a, title = {Decoding of intended saccade direction in an oculomotor brain-computer interface}, author = {Nan Jia and Scott L Brincat and Andrés F Salazar-Gómez and Mikhail Panko and Frank H Guenther and Earl K Miller}, doi = {10.1088/1741-2552/aa5a3e}, year = {2017}, date = {2017-01-01}, journal = {Journal of Neural Engineering}, volume = {14}, number = {4}, pages = {1--13}, abstract = {OBJECTIVE: To date, invasive brain-computer interface (BCI) research has largely focused on replacing lost limb functions using signals from of hand/arm areas of motor cortex. However, the oculomotor system may be better suited to BCI applications involving rapid serial selection from spatial targets, such as choosing from a set of possible words displayed on a computer screen in an augmentative and alternative communication (AAC) application. Here we aimed to demonstrate the feasibility of a BCI utilizing the oculomotor system. APPROACH: We developed a chronic intracortical BCI in monkeys to decode intended saccadic eye movement direction using activity from multiple frontal cortical areas. MAIN RESULTS: Intended saccade direction could be decoded in real time with high accuracy, particularly at contralateral locations. Accurate decoding was evident even at the beginning of the BCI session; no extensive BCI experience was necessary. High-frequency (80-500 Hz) local field potential magnitude provided the best performance, even over spiking activity, thus simplifying future BCI applications. Most of the information came from the frontal and supplementary eye fields, with relatively little contribution from dorsolateral prefrontal cortex. SIGNIFICANCE: Our results support the feasibility of high-accuracy intracortical oculomotor BCIs that require little or no practice to operate and may be ideally suited for 'point and click' computer operation as used in most current AAC systems.}, keywords = {}, pubstate = {published}, tppubtype = {article} } OBJECTIVE: To date, invasive brain-computer interface (BCI) research has largely focused on replacing lost limb functions using signals from of hand/arm areas of motor cortex. However, the oculomotor system may be better suited to BCI applications involving rapid serial selection from spatial targets, such as choosing from a set of possible words displayed on a computer screen in an augmentative and alternative communication (AAC) application. Here we aimed to demonstrate the feasibility of a BCI utilizing the oculomotor system. APPROACH: We developed a chronic intracortical BCI in monkeys to decode intended saccadic eye movement direction using activity from multiple frontal cortical areas. MAIN RESULTS: Intended saccade direction could be decoded in real time with high accuracy, particularly at contralateral locations. Accurate decoding was evident even at the beginning of the BCI session; no extensive BCI experience was necessary. High-frequency (80-500 Hz) local field potential magnitude provided the best performance, even over spiking activity, thus simplifying future BCI applications. Most of the information came from the frontal and supplementary eye fields, with relatively little contribution from dorsolateral prefrontal cortex. SIGNIFICANCE: Our results support the feasibility of high-accuracy intracortical oculomotor BCIs that require little or no practice to operate and may be ideally suited for 'point and click' computer operation as used in most current AAC systems. |
Yoshinao Kajikawa; John F Smiley; Charles E Schroeder Primary generators of visually evoked field potentials recorded in the macaque auditory cortex Journal Article The Journal of Neuroscience, 37 (42), pp. 10139–10153, 2017. @article{Kajikawa2017, title = {Primary generators of visually evoked field potentials recorded in the macaque auditory cortex}, author = {Yoshinao Kajikawa and John F Smiley and Charles E Schroeder}, doi = {10.1523/JNEUROSCI.3800-16.2017}, year = {2017}, date = {2017-01-01}, journal = {The Journal of Neuroscience}, volume = {37}, number = {42}, pages = {10139--10153}, abstract = {Prior studies have reported “local” field potential (LFP) responses to faces in the macaque auditory cortex and have suggested that such face-LFPs may be substrates of audiovisual integration. However, although field potentials (FPs) may reflect the synaptic currents of neurons near the recording electrode, due to the use of a distant reference electrode, they often reflect those of synaptic activity occurring in distant sites as well. Thus, FP recordings within a given brain region (e.g., auditory cortex) may be “contaminated” by activity generated elsewhere in the brain. To determine whether face responses are indeed generated within macaque auditory cortex, we recorded FPs and concomitant multiunit activity with linear array multielectrodes across auditory cortex in three macaques (one female), and applied current source density (CSD) analysis to the laminar FP profile. CSD analysis revealed no appreciable local generator contribution to the visual FP in auditory cortex, although we did note an increase in the amplitude of visual FP with cortical depth, suggesting that their generators are located below auditory cortex. In the underlying inferotemporal cortex, we found polarity inversions of the main visual FP components accompanied by robust CSD responses and large-amplitude multiunit activity. These results indicate that face-evoked FP responses in auditory cortex are not generated locally but are volume-conducted from other face-responsive regions. In broader terms, our results underscore the caution that, unless far-field contamination is removed, LFPs in general may reflect such “far-field” activity, in addition to, or in absence of, local synaptic responses.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Prior studies have reported “local” field potential (LFP) responses to faces in the macaque auditory cortex and have suggested that such face-LFPs may be substrates of audiovisual integration. However, although field potentials (FPs) may reflect the synaptic currents of neurons near the recording electrode, due to the use of a distant reference electrode, they often reflect those of synaptic activity occurring in distant sites as well. Thus, FP recordings within a given brain region (e.g., auditory cortex) may be “contaminated” by activity generated elsewhere in the brain. To determine whether face responses are indeed generated within macaque auditory cortex, we recorded FPs and concomitant multiunit activity with linear array multielectrodes across auditory cortex in three macaques (one female), and applied current source density (CSD) analysis to the laminar FP profile. CSD analysis revealed no appreciable local generator contribution to the visual FP in auditory cortex, although we did note an increase in the amplitude of visual FP with cortical depth, suggesting that their generators are located below auditory cortex. In the underlying inferotemporal cortex, we found polarity inversions of the main visual FP components accompanied by robust CSD responses and large-amplitude multiunit activity. These results indicate that face-evoked FP responses in auditory cortex are not generated locally but are volume-conducted from other face-responsive regions. In broader terms, our results underscore the caution that, unless far-field contamination is removed, LFPs in general may reflect such “far-field” activity, in addition to, or in absence of, local synaptic responses. |
Kohitij Kar; Jacob Duijnhouwer; Bart Krekelberg Transcranial alternating current stimulation attenuates neuronal adaptation Journal Article The Journal of Neuroscience, 37 (9), pp. 2325–2335, 2017. @article{Kar2017, title = {Transcranial alternating current stimulation attenuates neuronal adaptation}, author = {Kohitij Kar and Jacob Duijnhouwer and Bart Krekelberg}, doi = {10.1523/JNEUROSCI.2266-16.2016}, year = {2017}, date = {2017-01-01}, journal = {The Journal of Neuroscience}, volume = {37}, number = {9}, pages = {2325--2335}, abstract = {We previously showed that brief application of 2 mA (peak-to-peak) transcranial currents alternating at 10 Hz significantly reduces motion adaptation in humans. This is but one of many behavioral studies showing that weak currents applied to the scalp modulate neural processing. Transcranial stimulation has been shown to improve perception, learning, and a range of clinical symptoms. Few studies, however, have measured the neural consequences of transcranial current stimulation. We capitalized on the strong link between motion perception and neural activity in the middle temporal (MT) area of the macaque monkey to study the neural mechanisms that underlie the behavioral consequences of transcranial alternating current stimulation. First, we observed that 2 mA currents generated substantial intracranial fields, which were much stronger in the stimulated hemisphere (0.12 V/m) than on the opposite side of the brain (0.03 V/m). Second, we found that brief application of transcranial alternating current stimulation at 10 Hz reduced spike-frequency adaptation of MT neurons and led to a broadband increase in the power spectrum of local field potentials. Together, these findings provide a direct demonstration that weak electric fields applied to the scalp significantly affect neural processing in the primate brain and that this includes a hitherto unknown mechanism that attenuates sensory adaptation.}, keywords = {}, pubstate = {published}, tppubtype = {article} } We previously showed that brief application of 2 mA (peak-to-peak) transcranial currents alternating at 10 Hz significantly reduces motion adaptation in humans. This is but one of many behavioral studies showing that weak currents applied to the scalp modulate neural processing. Transcranial stimulation has been shown to improve perception, learning, and a range of clinical symptoms. Few studies, however, have measured the neural consequences of transcranial current stimulation. We capitalized on the strong link between motion perception and neural activity in the middle temporal (MT) area of the macaque monkey to study the neural mechanisms that underlie the behavioral consequences of transcranial alternating current stimulation. First, we observed that 2 mA currents generated substantial intracranial fields, which were much stronger in the stimulated hemisphere (0.12 V/m) than on the opposite side of the brain (0.03 V/m). Second, we found that brief application of transcranial alternating current stimulation at 10 Hz reduced spike-frequency adaptation of MT neurons and led to a broadband increase in the power spectrum of local field potentials. Together, these findings provide a direct demonstration that weak electric fields applied to the scalp significantly affect neural processing in the primate brain and that this includes a hitherto unknown mechanism that attenuates sensory adaptation. |
Steffen Klingenhoefer; Bart Krekelberg Perisaccadic visual perception Journal Article Journal of Vision, 17 (9), pp. 1–14, 2017. @article{Klingenhoefer2017, title = {Perisaccadic visual perception}, author = {Steffen Klingenhoefer and Bart Krekelberg}, doi = {10.1167/17.9.16}, year = {2017}, date = {2017-01-01}, journal = {Journal of Vision}, volume = {17}, number = {9}, pages = {1--14}, abstract = {Primates use frequent, rapid eye movements to sample their visual environment. This is a fruitful strategy to make the best use of the highly sensitive foveal part of the retina, but it requires neural mechanisms to bind the rapidly changing visual input into a single, stable percept. Studies investigating these neural mechanisms have typically assumed that perisaccadic perception in nonhuman primates matches that of humans. We tested this assumption by performing identical experiments in human and nonhuman primates. Our data confirm that perisaccadic visual perception of macaques and humans is qualitatively similar. Specifically, we found a reduction in detectability and mislocalization of targets presented at the time of saccades. We also found substantial differences between human and nonhuman primates. Notably, in nonhuman primates, localization that requires knowledge of eye position was less precise, nonhuman primates detected fewer perisaccadic stimuli, and perisaccadic compression was not towards the saccade target. The qualitative similarities between species support the view that the nonhuman primate is ideally suited to study aspects of brain function-such as those relying on foveal vision-that are uniquely developed in primates. The quantitative differences, however, demonstrate the need for a reassessment of the models purportedly linking neural response changes at the time of saccades with the behavioral phenomena of perisaccadic reduction of detectability and mislocalization.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Primates use frequent, rapid eye movements to sample their visual environment. This is a fruitful strategy to make the best use of the highly sensitive foveal part of the retina, but it requires neural mechanisms to bind the rapidly changing visual input into a single, stable percept. Studies investigating these neural mechanisms have typically assumed that perisaccadic perception in nonhuman primates matches that of humans. We tested this assumption by performing identical experiments in human and nonhuman primates. Our data confirm that perisaccadic visual perception of macaques and humans is qualitatively similar. Specifically, we found a reduction in detectability and mislocalization of targets presented at the time of saccades. We also found substantial differences between human and nonhuman primates. Notably, in nonhuman primates, localization that requires knowledge of eye position was less precise, nonhuman primates detected fewer perisaccadic stimuli, and perisaccadic compression was not towards the saccade target. The qualitative similarities between species support the view that the nonhuman primate is ideally suited to study aspects of brain function-such as those relying on foveal vision-that are uniquely developed in primates. The quantitative differences, however, demonstrate the need for a reassessment of the models purportedly linking neural response changes at the time of saccades with the behavioral phenomena of perisaccadic reduction of detectability and mislocalization. |
Matthew R Krause; Theodoros P Zanos; Bennett A Csorba; Praveen K Pilly; Jaehoon Choe; Matthew E Phillips; Abhishek Datta; Christopher C Pack Transcranial direct current stimulation facilitates associative learning and alters functional connectivity in the primate brain Journal Article Current Biology, 27 (20), pp. 3086–3096, 2017. @article{Krause2017, title = {Transcranial direct current stimulation facilitates associative learning and alters functional connectivity in the primate brain}, author = {Matthew R Krause and Theodoros P Zanos and Bennett A Csorba and Praveen K Pilly and Jaehoon Choe and Matthew E Phillips and Abhishek Datta and Christopher C Pack}, doi = {10.1016/j.cub.2017.09.020}, year = {2017}, date = {2017-01-01}, journal = {Current Biology}, volume = {27}, number = {20}, pages = {3086--3096}, publisher = {Elsevier Ltd.}, abstract = {There has been growing interest in transcranial direct current stimulation (tDCS), a non-invasive technique purported to modulate neural activity via weak, externally applied electric fields. Although some promising preliminary data have been reported for applications ranging from stroke rehabilitation to cognitive enhancement, little is known about how tDCS affects the human brain, and some studies have concluded that it may have no effect at all. Here, we describe a macaque model of tDCS that allows us to simultaneously examine the effects of tDCS on brain activity and behavior. We find that applying tDCS to right prefrontal cortex improves monkeys' performance on an associative learning task. While firing rates do not change within the targeted area, tDCS does induce large low-frequency oscillations in the underlying tissue. These oscillations alter functional connectivity, both locally and between distant brain areas, and these long-range changes correlate with tDCS's effects on behavior. Together, these results are consistent with the idea that tDCS leads to widespread changes in brain activity and suggest that it may be a valuable method for cheaply and non-invasively altering functional connectivity in humans. Krause et al. test transcranial direct current stimulation (tDCS) in a realistic non-human primate model. Stimulation of prefrontal cortex (PFC) improved animals' associative learning while altering coherence between PFC and sensory areas. Their data suggest that tDCS may act by altering long-range connectivity between PFC and other brain areas.}, keywords = {}, pubstate = {published}, tppubtype = {article} } There has been growing interest in transcranial direct current stimulation (tDCS), a non-invasive technique purported to modulate neural activity via weak, externally applied electric fields. Although some promising preliminary data have been reported for applications ranging from stroke rehabilitation to cognitive enhancement, little is known about how tDCS affects the human brain, and some studies have concluded that it may have no effect at all. Here, we describe a macaque model of tDCS that allows us to simultaneously examine the effects of tDCS on brain activity and behavior. We find that applying tDCS to right prefrontal cortex improves monkeys' performance on an associative learning task. While firing rates do not change within the targeted area, tDCS does induce large low-frequency oscillations in the underlying tissue. These oscillations alter functional connectivity, both locally and between distant brain areas, and these long-range changes correlate with tDCS's effects on behavior. Together, these results are consistent with the idea that tDCS leads to widespread changes in brain activity and suggest that it may be a valuable method for cheaply and non-invasively altering functional connectivity in humans. Krause et al. test transcranial direct current stimulation (tDCS) in a realistic non-human primate model. Stimulation of prefrontal cortex (PFC) improved animals' associative learning while altering coherence between PFC and sensory areas. Their data suggest that tDCS may act by altering long-range connectivity between PFC and other brain areas. |
Matthew L Leavitt; Florian Pieper; Adam J Sachs; Julio C Martinez-Trujillo Correlated variability modifies working memory fidelity in primate prefrontal neuronal ensembles Journal Article Proceedings of the National Academy of Sciences, 114 (12), pp. E2494–E2503, 2017. @article{Leavitt2017, title = {Correlated variability modifies working memory fidelity in primate prefrontal neuronal ensembles}, author = {Matthew L Leavitt and Florian Pieper and Adam J Sachs and Julio C Martinez-Trujillo}, doi = {10.1073/pnas.1619949114}, year = {2017}, date = {2017-01-01}, journal = {Proceedings of the National Academy of Sciences}, volume = {114}, number = {12}, pages = {E2494--E2503}, abstract = {Neurons in the primate lateral prefrontal cortex (LPFC) encode working memory (WM) representations via sustained firing, a phenomenon hypothesized to arise from recurrent dynamics within ensembles of interconnected neurons. Here, we tested this hypothesis by using microelectrode arrays to examine spike count correlations (rsc) in LPFC neuronal ensembles during a spatial WM task. We found a pattern of pairwise rsc during WM maintenance indicative of stronger coupling between similarly tuned neurons and increased inhibition between dissimilarly tuned neurons. We then used a linear decoder to quantify the effects of the high-dimensional rsc structure on information coding in the neuronal ensembles. We found that the rsc structure could facilitate or impair coding, depending on the size of the ensemble and tuning properties of its constituent neurons. A simple optimization procedure demonstrated that near-maximum decoding performance could be achieved using a relatively small number of neurons. These WM- optimized subensembles were more signal correlation (rsignal)- diverse and anatomically dispersed than predicted by the statistics of the full recorded population of neurons, and they often con- tained neurons that were poorly WM-selective, yet enhanced cod- ing fidelity by shaping the ensemble's rsc structure. We observed a pattern of rsc between LPFC neurons indicative of recurrent dynamics as a mechanism for WM-related activity and that the rsc structure can increase the fidelity ofWM representations. Thus, WM coding in LPFC neuronal ensembles arises from a complex synergy between single neuron coding properties and multidimensional, ensemble-level phenomena.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Neurons in the primate lateral prefrontal cortex (LPFC) encode working memory (WM) representations via sustained firing, a phenomenon hypothesized to arise from recurrent dynamics within ensembles of interconnected neurons. Here, we tested this hypothesis by using microelectrode arrays to examine spike count correlations (rsc) in LPFC neuronal ensembles during a spatial WM task. We found a pattern of pairwise rsc during WM maintenance indicative of stronger coupling between similarly tuned neurons and increased inhibition between dissimilarly tuned neurons. We then used a linear decoder to quantify the effects of the high-dimensional rsc structure on information coding in the neuronal ensembles. We found that the rsc structure could facilitate or impair coding, depending on the size of the ensemble and tuning properties of its constituent neurons. A simple optimization procedure demonstrated that near-maximum decoding performance could be achieved using a relatively small number of neurons. These WM- optimized subensembles were more signal correlation (rsignal)- diverse and anatomically dispersed than predicted by the statistics of the full recorded population of neurons, and they often con- tained neurons that were poorly WM-selective, yet enhanced cod- ing fidelity by shaping the ensemble's rsc structure. We observed a pattern of rsc between LPFC neurons indicative of recurrent dynamics as a mechanism for WM-related activity and that the rsc structure can increase the fidelity ofWM representations. Thus, WM coding in LPFC neuronal ensembles arises from a complex synergy between single neuron coding properties and multidimensional, ensemble-level phenomena. |
Jeyeon Lee; Hoseok Choi; Seho Lee; Baek Hwan Cho; Kyoung-Ha Ahn; In Young Kim; Kyoung-Min Lee; Dong-Pyo Jang Decoding saccadic directions using epidural ECoG in non-human primates Journal Article Journal of Korean Medical Science, 32 (8), pp. 1243–1250, 2017. @article{Lee2017b, title = {Decoding saccadic directions using epidural ECoG in non-human primates}, author = {Jeyeon Lee and Hoseok Choi and Seho Lee and Baek Hwan Cho and Kyoung-Ha Ahn and In Young Kim and Kyoung-Min Lee and Dong-Pyo Jang}, doi = {10.3346/jkms.2017.32.8.1243}, year = {2017}, date = {2017-01-01}, journal = {Journal of Korean Medical Science}, volume = {32}, number = {8}, pages = {1243--1250}, abstract = {A brain-computer interface (BCI) can be used to restore some communication as an alternative interface for patients suffering from locked-in syndrome. However, most BCI systems are based on SSVEP, P300, or motor imagery, and a diversity of BCI protocols would be needed for various types of patients. In this paper, we trained the choice saccade (CS) task in 2 non-human primate monkeys and recorded the brain signal using an epidural electrocorticogram (eECoG) to predict eye movement direction. We successfully predicted the direction of the upcoming eye movement using a support vector machine (SVM) with the brain signals after the directional cue onset and before the saccade execution. The mean accuracies were 80% for 2 directions and 43% for 4 directions. We also quantified the spatial-spectro-temporal contribution ratio using SVM recursive feature elimination (RFE). The channels over the frontal eye field (FEF), supplementary eye field (SEF), and superior parietal lobule (SPL) area were dominantly used for classification. The $alpha$-band in the spectral domain and the time bins just after the directional cue onset and just before the saccadic execution were mainly useful for prediction. A saccade based BCI paradigm can be projected in the 2D space, and will hopefully provide an intuitive and convenient communication platform for users.}, keywords = {}, pubstate = {published}, tppubtype = {article} } A brain-computer interface (BCI) can be used to restore some communication as an alternative interface for patients suffering from locked-in syndrome. However, most BCI systems are based on SSVEP, P300, or motor imagery, and a diversity of BCI protocols would be needed for various types of patients. In this paper, we trained the choice saccade (CS) task in 2 non-human primate monkeys and recorded the brain signal using an epidural electrocorticogram (eECoG) to predict eye movement direction. We successfully predicted the direction of the upcoming eye movement using a support vector machine (SVM) with the brain signals after the directional cue onset and before the saccade execution. The mean accuracies were 80% for 2 directions and 43% for 4 directions. We also quantified the spatial-spectro-temporal contribution ratio using SVM recursive feature elimination (RFE). The channels over the frontal eye field (FEF), supplementary eye field (SEF), and superior parietal lobule (SPL) area were dominantly used for classification. The $alpha$-band in the spectral domain and the time bins just after the directional cue onset and just before the saccadic execution were mainly useful for prediction. A saccade based BCI paradigm can be projected in the 2D space, and will hopefully provide an intuitive and convenient communication platform for users. |
Roman F Loonis; Scott L Brincat; Evan G Antzoulatos; Earl K Miller A meta-analysis suggests different neural correlates for implicit and explicit learning Journal Article Neuron, 96 (2), pp. 521–534., 2017. @article{Loonis2017, title = {A meta-analysis suggests different neural correlates for implicit and explicit learning}, author = {Roman F Loonis and Scott L Brincat and Evan G Antzoulatos and Earl K Miller}, doi = {10.1016/j.neuron.2017.09.032}, year = {2017}, date = {2017-01-01}, journal = {Neuron}, volume = {96}, number = {2}, pages = {521--534.}, publisher = {Elsevier Inc.}, abstract = {A meta-analysis of non-human primates performing three different tasks (Object-Match, Category-Match, and Category-Saccade associations) revealed signatures of explicit and implicit learning. Performance improved equally following correct and error trials in the Match (explicit) tasks, but it improved more after correct trials in the Saccade (implicit) task, a signature of explicit versus implicit learning. Likewise, error-related negativity, a marker for error processing, was greater in the Match (explicit) tasks. All tasks showed an increase in alpha/beta (10–30 Hz) synchrony after correct choices. However, only the implicit task showed an increase in theta (3–7 Hz) synchrony after correct choices that decreased with learning. In contrast, in the explicit tasks, alpha/beta synchrony increased with learning and decreased thereafter. Our results suggest that explicit versus implicit learning engages different neural mechanisms that rely on different patterns of oscillatory synchrony. Loonis et al. find that explicit and implicit learning use feedback about correct choices versus errors differently. Implicit learning relies more on theta synchrony (3–7 Hz) while explicit learning relies on alpha/beta synchrony (10–30 Hz).}, keywords = {}, pubstate = {published}, tppubtype = {article} } A meta-analysis of non-human primates performing three different tasks (Object-Match, Category-Match, and Category-Saccade associations) revealed signatures of explicit and implicit learning. Performance improved equally following correct and error trials in the Match (explicit) tasks, but it improved more after correct trials in the Saccade (implicit) task, a signature of explicit versus implicit learning. Likewise, error-related negativity, a marker for error processing, was greater in the Match (explicit) tasks. All tasks showed an increase in alpha/beta (10–30 Hz) synchrony after correct choices. However, only the implicit task showed an increase in theta (3–7 Hz) synchrony after correct choices that decreased with learning. In contrast, in the explicit tasks, alpha/beta synchrony increased with learning and decreased thereafter. Our results suggest that explicit versus implicit learning engages different neural mechanisms that rely on different patterns of oscillatory synchrony. Loonis et al. find that explicit and implicit learning use feedback about correct choices versus errors differently. Implicit learning relies more on theta synchrony (3–7 Hz) while explicit learning relies on alpha/beta synchrony (10–30 Hz). |
Nicolas Y Masse; Jonathan M Hodnefield; David J Freedman Mnemonic encoding and cortical organization in parietal and prefrontal cortices Journal Article The Journal of Neuroscience, 37 (25), pp. 6098–6112, 2017. @article{Masse2017, title = {Mnemonic encoding and cortical organization in parietal and prefrontal cortices}, author = {Nicolas Y Masse and Jonathan M Hodnefield and David J Freedman}, doi = {10.1523/JNEUROSCI.3903-16.2017}, year = {2017}, date = {2017-01-01}, journal = {The Journal of Neuroscience}, volume = {37}, number = {25}, pages = {6098--6112}, abstract = {Persistent activity within the frontoparietal network is consistently observed during tasks that require working memory. However, the neural circuit mechanisms underlying persistent neuronal encoding within this network remain unresolved. Here, we ask how neural circuits support persistent activity by examining population recordings from posterior parietal (PPC) and prefrontal (PFC) cortices in two male monkeys that performed spatial and motion direction-based tasks that required working memory. While spatially selective persistent activity was observed in both areas, robust selective persistent activity for motion direction was only observed in PFC. Crucially, we find that this difference between mnemonic encoding in PPC and PFC is associated with the presence offunctional clustering: PPC and PFC neurons up to ~700 $mu$m apart preferred similar spatial locations, and PFC neurons up to ~700 $mu$m apart preferred similar motion directions. In contrast, motion-direction tuning similarity between nearby PPC neurons was much weaker and decayed rapidly beyond ~200 $mu$m. We also observed a similar association between persistent activity and functional clustering in trained recurrent neural network models embedded with a columnar topology. These results suggest that functional clustering facilitates mnemonic encoding of sensory information.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Persistent activity within the frontoparietal network is consistently observed during tasks that require working memory. However, the neural circuit mechanisms underlying persistent neuronal encoding within this network remain unresolved. Here, we ask how neural circuits support persistent activity by examining population recordings from posterior parietal (PPC) and prefrontal (PFC) cortices in two male monkeys that performed spatial and motion direction-based tasks that required working memory. While spatially selective persistent activity was observed in both areas, robust selective persistent activity for motion direction was only observed in PFC. Crucially, we find that this difference between mnemonic encoding in PPC and PFC is associated with the presence offunctional clustering: PPC and PFC neurons up to ~700 $mu$m apart preferred similar spatial locations, and PFC neurons up to ~700 $mu$m apart preferred similar motion directions. In contrast, motion-direction tuning similarity between nearby PPC neurons was much weaker and decayed rapidly beyond ~200 $mu$m. We also observed a similar association between persistent activity and functional clustering in trained recurrent neural network models embedded with a columnar topology. These results suggest that functional clustering facilitates mnemonic encoding of sensory information. |
Diego Mendoza-Halliday; Julio C Martinez-Trujillo Neuronal population coding of perceived and memorized visual features in the lateral prefrontal cortex Journal Article Nature Communications, 8 , pp. 1–13, 2017. @article{Mendoza-Halliday2017, title = {Neuronal population coding of perceived and memorized visual features in the lateral prefrontal cortex}, author = {Diego Mendoza-Halliday and Julio C Martinez-Trujillo}, doi = {10.1038/ncomms15471}, year = {2017}, date = {2017-01-01}, journal = {Nature Communications}, volume = {8}, pages = {1--13}, publisher = {Nature Publishing Group}, abstract = {The primate lateral prefrontal cortex (LPFC) encodes visual stimulus features while they are perceived and while they are maintained in working memory. However, it remains unclear whether perceived and memorized features are encoded by the same or different neurons and population activity patterns. Here we record LPFC neuronal activity while monkeys perceive the motion direction of a stimulus that remains visually available, or memorize the direction if the stimulus disappears. We find neurons with a wide variety of combinations of coding strength for perceived and memorized directions: some neurons encode both to similar degrees while others preferentially or exclusively encode either one. Reading out the combined activity of all neurons, a machine-learning algorithm reliably decode the motion direction and determine whether it is perceived or memorized. Our results indicate that a functionally diverse population of LPFC neurons provides a substrate for discriminating between perceptual and mnemonic representations of visual features.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The primate lateral prefrontal cortex (LPFC) encodes visual stimulus features while they are perceived and while they are maintained in working memory. However, it remains unclear whether perceived and memorized features are encoded by the same or different neurons and population activity patterns. Here we record LPFC neuronal activity while monkeys perceive the motion direction of a stimulus that remains visually available, or memorize the direction if the stimulus disappears. We find neurons with a wide variety of combinations of coding strength for perceived and memorized directions: some neurons encode both to similar degrees while others preferentially or exclusively encode either one. Reading out the combined activity of all neurons, a machine-learning algorithm reliably decode the motion direction and determine whether it is perceived or memorized. Our results indicate that a functionally diverse population of LPFC neurons provides a substrate for discriminating between perceptual and mnemonic representations of visual features. |
Yaser Merrikhi; Kelsey Clark; Eddy Albarran; Mohammadbagher Parsa; Marc Zirnsak; Tirin Moore; Behrad Noudoost Spatial working memory alters the efficacy of input to visual cortex Journal Article Nature Communications, 8 , pp. 1–10, 2017. @article{Merrikhi2017, title = {Spatial working memory alters the efficacy of input to visual cortex}, author = {Yaser Merrikhi and Kelsey Clark and Eddy Albarran and Mohammadbagher Parsa and Marc Zirnsak and Tirin Moore and Behrad Noudoost}, doi = {10.1038/ncomms15041}, year = {2017}, date = {2017-01-01}, journal = {Nature Communications}, volume = {8}, pages = {1--10}, publisher = {Nature Publishing Group}, abstract = {Prefrontal cortex modulates sensory signals in extrastriate visual cortex, in part via its direct projections from the frontal eye field (FEF), an area involved in selective attention. We find that working memory-related activity is a dominant signal within FEF input to visual cortex. Although this signal alone does not evoke spiking responses in areas V4 and MT during memory, the gain of visual responses in these areas increases, and neuronal receptive fields expand and shift towards the remembered location, improving the stimulus representation by neuronal populations. These results provide a basis for enhancing the representation of working memory targets and implicate persistent FEF activity as a basis for the interdependence of working memory and selective attention.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Prefrontal cortex modulates sensory signals in extrastriate visual cortex, in part via its direct projections from the frontal eye field (FEF), an area involved in selective attention. We find that working memory-related activity is a dominant signal within FEF input to visual cortex. Although this signal alone does not evoke spiking responses in areas V4 and MT during memory, the gain of visual responses in these areas increases, and neuronal receptive fields expand and shift towards the remembered location, improving the stimulus representation by neuronal populations. These results provide a basis for enhancing the representation of working memory targets and implicate persistent FEF activity as a basis for the interdependence of working memory and selective attention. |
Juri Minxha; Clayton Mosher; Jeremiah K Morrow; Adam N Mamelak; Ralph Adolphs; Katalin M Gothard; Ueli Rutishauser Fixations gate species-specific responses to free viewing of faces in the human and macaque amygdala Journal Article Cell Reports, 18 (4), pp. 878–891, 2017. @article{Minxha2017, title = {Fixations gate species-specific responses to free viewing of faces in the human and macaque amygdala}, author = {Juri Minxha and Clayton Mosher and Jeremiah K Morrow and Adam N Mamelak and Ralph Adolphs and Katalin M Gothard and Ueli Rutishauser}, doi = {10.1016/j.celrep.2016.12.083}, year = {2017}, date = {2017-01-01}, journal = {Cell Reports}, volume = {18}, number = {4}, pages = {878--891}, publisher = {ElsevierCompany.}, abstract = {Neurons in the primate amygdala respond prominently to faces. This implicates the amygdala in the processing of socially significant stimuli, yet its contribution to social perception remains poorly understood. We evaluated the representation of faces in the primate amygdala during naturalistic conditions by recording from both human and macaque amygdala neurons during free viewing of identical arrays of images with concurrent eye tracking. Neurons responded to faces only when they were fixated, suggesting that neuronal activity was gated by visual attention. Further experiments in humans utilizing covert attention confirmed this hypothesis. In both species, the majority of face-selective neurons preferred faces of conspecifics, a bias also seen behaviorally in first fixation preferences. Response latencies, relative to fixation onset, were shortest for conspecific-selective neurons and were ∼100 ms shorter in monkeys compared to humans. This argues that attention to faces gates amygdala responses, which in turn prioritize species-typical information for further processing.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Neurons in the primate amygdala respond prominently to faces. This implicates the amygdala in the processing of socially significant stimuli, yet its contribution to social perception remains poorly understood. We evaluated the representation of faces in the primate amygdala during naturalistic conditions by recording from both human and macaque amygdala neurons during free viewing of identical arrays of images with concurrent eye tracking. Neurons responded to faces only when they were fixated, suggesting that neuronal activity was gated by visual attention. Further experiments in humans utilizing covert attention confirmed this hypothesis. In both species, the majority of face-selective neurons preferred faces of conspecifics, a bias also seen behaviorally in first fixation preferences. Response latencies, relative to fixation onset, were shortest for conspecific-selective neurons and were ∼100 ms shorter in monkeys compared to humans. This argues that attention to faces gates amygdala responses, which in turn prioritize species-typical information for further processing. |
Ilya E Monosov Anterior cingulate is a source of valence-specific information about value and uncertainty Journal Article Nature Communications, 8 , pp. 1–12, 2017. @article{Monosov2017, title = {Anterior cingulate is a source of valence-specific information about value and uncertainty}, author = {Ilya E Monosov}, doi = {10.1038/s41467-017-00072-y}, year = {2017}, date = {2017-01-01}, journal = {Nature Communications}, volume = {8}, pages = {1--12}, publisher = {Springer US}, abstract = {Anterior cingulate cortex (ACC) is thought to control a wide range of reward, punishment, and uncertainty-related behaviors. However, how it does so is unclear. Here, in a Pavlovian procedure in which monkeys displayed a diverse repertoire of reward-related, punishment-related, and uncertainty-related behaviors, we show that many ACC-neurons represent expected value and uncertainty in a valence-specific manner, signaling value or uncertainty predictions about either rewards or punishments. Other ACC-neurons signal prediction information about rewards and punishments by displaying excitation to both (rather than excitation to one and inhibition to the other). This diversity in valence representations may support the role of ACC in many behavioral states that are either enhanced by reward and punishment (e.g., vigilance) or specific to either reward or punishment (e.g., approach and avoidance). Also, this first demonstration of punishment-uncertainty signals in the brain suggests that ACC could be a target for the treatment of uncertainty-related disorders of mood.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Anterior cingulate cortex (ACC) is thought to control a wide range of reward, punishment, and uncertainty-related behaviors. However, how it does so is unclear. Here, in a Pavlovian procedure in which monkeys displayed a diverse repertoire of reward-related, punishment-related, and uncertainty-related behaviors, we show that many ACC-neurons represent expected value and uncertainty in a valence-specific manner, signaling value or uncertainty predictions about either rewards or punishments. Other ACC-neurons signal prediction information about rewards and punishments by displaying excitation to both (rather than excitation to one and inhibition to the other). This diversity in valence representations may support the role of ACC in many behavioral states that are either enhanced by reward and punishment (e.g., vigilance) or specific to either reward or punishment (e.g., approach and avoidance). Also, this first demonstration of punishment-uncertainty signals in the brain suggests that ACC could be a target for the treatment of uncertainty-related disorders of mood. |
Sujaya Neupane; Daniel Guitton; Christopher C Pack Coherent alpha oscillations link current and future receptive fields during saccades Journal Article Proceedings of the National Academy of Sciences, 114 (29), pp. E5979–E5985, 2017. @article{Neupane2017, title = {Coherent alpha oscillations link current and future receptive fields during saccades}, author = {Sujaya Neupane and Daniel Guitton and Christopher C Pack}, doi = {10.1073/pnas.1701672114}, year = {2017}, date = {2017-01-01}, journal = {Proceedings of the National Academy of Sciences}, volume = {114}, number = {29}, pages = {E5979--E5985}, abstract = {Oscillations are ubiquitous in the brain, and they can powerfully influence neural coding. In particular, when oscillations at distinct sites are coherent, they provide a means of gating the flow of neural signals between different cortical regions. Coherent oscillations also occur within individual brain regions, although the purpose of this coherence is not well understood. Here, we report that within a single brain region, coherent alpha oscillations link stimulus representations as they change in space and time. Specifically, in primate cortical area V4, alpha coherence links sites that encode the retinal location of a visual stimulus before and after a saccade. These coherence changes exhibit properties similar to those of receptive field remapping, a phenomenon in which individual neurons change their receptive fields according to the metrics of each saccade. In particular, alpha coherence, like remapping, is highly dependent on the saccade vector and the spatial arrangement of current and future receptive fields. Moreover, although visual stimulation plays a modulatory role, it is neither necessary nor sufficient to elicit alpha coherence. Indeed, a similar pattern of coherence is observed even when saccades are made in darkness. Together, these results show that the pattern of alpha coherence across the retinotopic map in V4 matches many of the properties of receptive field remapping. Thus, oscillatory coherence might play a role in constructing the stable representation of visual space that is an essential aspect of conscious perception.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Oscillations are ubiquitous in the brain, and they can powerfully influence neural coding. In particular, when oscillations at distinct sites are coherent, they provide a means of gating the flow of neural signals between different cortical regions. Coherent oscillations also occur within individual brain regions, although the purpose of this coherence is not well understood. Here, we report that within a single brain region, coherent alpha oscillations link stimulus representations as they change in space and time. Specifically, in primate cortical area V4, alpha coherence links sites that encode the retinal location of a visual stimulus before and after a saccade. These coherence changes exhibit properties similar to those of receptive field remapping, a phenomenon in which individual neurons change their receptive fields according to the metrics of each saccade. In particular, alpha coherence, like remapping, is highly dependent on the saccade vector and the spatial arrangement of current and future receptive fields. Moreover, although visual stimulation plays a modulatory role, it is neither necessary nor sufficient to elicit alpha coherence. Indeed, a similar pattern of coherence is observed even when saccades are made in darkness. Together, these results show that the pattern of alpha coherence across the retinotopic map in V4 matches many of the properties of receptive field remapping. Thus, oscillatory coherence might play a role in constructing the stable representation of visual space that is an essential aspect of conscious perception. |
Soo Hyun Park; Brian E Russ; David B T McMahon; Kenji W Koyano; Rebecca A Berman; David A Leopold Functional subpopulations of neurons in a macaque face patch revealed by single-unit fMRI mapping Journal Article Neuron, 95 (4), pp. 1–11, 2017. @article{Park2017, title = {Functional subpopulations of neurons in a macaque face patch revealed by single-unit fMRI mapping}, author = {Soo Hyun Park and Brian E Russ and David B T McMahon and Kenji W Koyano and Rebecca A Berman and David A Leopold}, doi = {10.1016/j.neuron.2017.07.014}, year = {2017}, date = {2017-01-01}, journal = {Neuron}, volume = {95}, number = {4}, pages = {1--11}, publisher = {Elsevier Inc.}, abstract = {Neurons within fMRI-defined face patches of the macaque brain exhibit shared categorical responses to flashed images but diverge in their responses under more natural viewing conditions. Here we investigate functional diversity among neurons in the anterior fundus (AF) face patch, combining whole-brain fMRI with longitudinal single-unit recordings in a local population (textless1 mm3). For each cell, we computed a whole-brain correlation map based on its shared time course with voxels throughout the brain during naturalistic movie viewing. Based on this mapping, neighboring neurons showed markedly different affiliation with distant visually responsive areas and fell coarsely into subpopulations. Of these, only one subpopulation (∼16% of neurons) yielded similar correlation maps to the local fMRI signal. The results employ the readout of large-scale fMRI networks and, by indicating multiple functional domains within a single voxel, present a new view of functional diversity within a local neural population.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Neurons within fMRI-defined face patches of the macaque brain exhibit shared categorical responses to flashed images but diverge in their responses under more natural viewing conditions. Here we investigate functional diversity among neurons in the anterior fundus (AF) face patch, combining whole-brain fMRI with longitudinal single-unit recordings in a local population (textless1 mm3). For each cell, we computed a whole-brain correlation map based on its shared time course with voxels throughout the brain during naturalistic movie viewing. Based on this mapping, neighboring neurons showed markedly different affiliation with distant visually responsive areas and fell coarsely into subpopulations. Of these, only one subpopulation (∼16% of neurons) yielded similar correlation maps to the local fMRI signal. The results employ the readout of large-scale fMRI networks and, by indicating multiple functional domains within a single voxel, present a new view of functional diversity within a local neural population. |
Aishwarya Parthasarathy; Roger Herikstad; Jit Hon Bong; Felipe Salvador Medina; Camilo Libedinsky; Shih Cheng Yen Mixed selectivity morphs population codes in prefrontal cortex Journal Article Nature Neuroscience, 20 (12), pp. 1770–1779, 2017. @article{Parthasarathy2017, title = {Mixed selectivity morphs population codes in prefrontal cortex}, author = {Aishwarya Parthasarathy and Roger Herikstad and Jit Hon Bong and Felipe Salvador Medina and Camilo Libedinsky and Shih Cheng Yen}, doi = {10.1038/s41593-017-0003-2}, year = {2017}, date = {2017-01-01}, journal = {Nature Neuroscience}, volume = {20}, number = {12}, pages = {1770--1779}, publisher = {Springer US}, abstract = {The prefrontal cortex plays an important role in the maintenance of working memory, as evidenced by studies using microelectrode recordings 1, lesions 2, inactivation 3, micro-stimulation 4, 5, and functional neuroimaging 6. Furthermore, the pre-frontal cortex suppresses task-irrelevant stimuli, or distractors 3, 7, 8. This has led to the notion that the prefrontal cortex plays a central role in the maintenance of working memory and the suppression of distractors, which are cornerstones of executive processing. Individual neurons in the lateral prefrontal cortex (LPFC; Brodmann area 46) show selective, sustained activity during the delay period of working memory and only as long as the memory is maintained 1,9,10. Populations of LPFC neurons form a stable memory code during the delay period of a working memory task 11. Distractors are thought to be suppressed in the LPFC, since it responds less to distractors than to task-relevant stimuli 3, 7, 8. Notably, sustained activity of LPFC neurons persists even after distractors are presented 3, 10. Thus, it is reasonable to hypothesize that the stable code observed during the delay period persists after a distractor is presented, forming a persistent code throughout the memory period. Recent studies have shown that the LPFC hosts an abundance of neurons with mixed selectivity 12-19. These cells encode multiple parameters of the task simultaneously, such as sensory stimuli, task rule, or motor response. In particular, neurons with nonlinear mixed selectivity (NMS) are thought to play a key role in the encoding of information 18, 20. In the context of a working memory task with interfering distractors, mixed selectivity could lead to a change in code after the distractor is presented. Thus, it is also reasonable to hypothesize that the code does not persist throughout the memory period but rather that it is flexible, with the ability to adapt to new task contingencies, such as the presentation of a distractor. Here we found that the LPFC morphs its code, as the latter hypothesis predicts , while the frontal eye fields (FEF) maintain a stable code, in agreement with the former hypothesis. Results Two monkeys were trained to perform a delayed saccade task (Fig. 1a). Overall performance of both animals was higher than 75% correct (Fig. 1b). We recorded a total of 256 neurons from the LPFC (144 from Monkey A and 112 from Monkey B; the positions of the implanted electrode arrays are shown in red in Fig. 1c) and 137 neurons from the FEF (125 from Monkey A and 12 from Monkey B; electrode arrays are shown in blue in Fig. 1c) while the animals performed the task. Of the neurons recorded, more than 40% displayed selectiv-ity to target location in at least one stage during the trial (Fig. 1d). Examples of the responses of an LPFC and an FEF neuron are shown in Supplementary Fig. 1a,b. To quantify the magnitude of this selec-tivity, we computed the percentage of explained variance (PEV) for spatial selectivity in each neuron. The average PEVs across significant neurons (Methods) are shown in Fig. 1d. In the LPFC, we observed that target information in selective cells (n = 107, 42% of the LPFC population) increased during the target presentation period and remained stable throughout the rest of the trial (Fig. 1d). In addition, in Supplementary Fig. 1c, we show that the distractor information was much lower in these same neurons during the Delay 2 period (P textless 0.001, Hedges' g = 23.99). A previous study found a sharp decrease in target information following distractor presentation , together with an increase of distractor information 21. Our results, however, did not replicate these observations. Rather, we found that target information remained stable, and distractor information stayed close to baseline throughout the trial (Supplementary Fig. 1c). This difference may reflect the simpler nature of our task and the comparatively lower behavioral saliency of the distractor we used. It may also reflect differences in the ways different types of information are encoded; perhaps the working memory code for numerosity in LPFC is more susceptible to distractors than the code for spatial locations. In contrast, in the FEF we observed The prefrontal cortex maintains working memory information in the presence of distracting stimuli. It has long been thought that sustained activity in individual neurons or groups of neurons was responsible for maintaining information in the form of a persistent, stable code. Here we show that, upon the presentation of a distractor, information in the lateral prefrontal cortex was reorganized into a different pattern of activity to create a morphed stable code without losing information. In contrast, the code in the frontal eye fields persisted across different delay periods but exhibited substantial instability and information loss after the presentation of a distractor. We found that neurons with mixed-selective responses were necessary and sufficient for the morphing of code and that these neurons were more abundant in the lateral prefrontal cortex than the frontal eye fields. This suggests that mixed selectivity provides populations with code-morphing capability, a property that may underlie cognitive flexibility.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The prefrontal cortex plays an important role in the maintenance of working memory, as evidenced by studies using microelectrode recordings 1, lesions 2, inactivation 3, micro-stimulation 4, 5, and functional neuroimaging 6. Furthermore, the pre-frontal cortex suppresses task-irrelevant stimuli, or distractors 3, 7, 8. This has led to the notion that the prefrontal cortex plays a central role in the maintenance of working memory and the suppression of distractors, which are cornerstones of executive processing. Individual neurons in the lateral prefrontal cortex (LPFC; Brodmann area 46) show selective, sustained activity during the delay period of working memory and only as long as the memory is maintained 1,9,10. Populations of LPFC neurons form a stable memory code during the delay period of a working memory task 11. Distractors are thought to be suppressed in the LPFC, since it responds less to distractors than to task-relevant stimuli 3, 7, 8. Notably, sustained activity of LPFC neurons persists even after distractors are presented 3, 10. Thus, it is reasonable to hypothesize that the stable code observed during the delay period persists after a distractor is presented, forming a persistent code throughout the memory period. Recent studies have shown that the LPFC hosts an abundance of neurons with mixed selectivity 12-19. These cells encode multiple parameters of the task simultaneously, such as sensory stimuli, task rule, or motor response. In particular, neurons with nonlinear mixed selectivity (NMS) are thought to play a key role in the encoding of information 18, 20. In the context of a working memory task with interfering distractors, mixed selectivity could lead to a change in code after the distractor is presented. Thus, it is also reasonable to hypothesize that the code does not persist throughout the memory period but rather that it is flexible, with the ability to adapt to new task contingencies, such as the presentation of a distractor. Here we found that the LPFC morphs its code, as the latter hypothesis predicts , while the frontal eye fields (FEF) maintain a stable code, in agreement with the former hypothesis. Results Two monkeys were trained to perform a delayed saccade task (Fig. 1a). Overall performance of both animals was higher than 75% correct (Fig. 1b). We recorded a total of 256 neurons from the LPFC (144 from Monkey A and 112 from Monkey B; the positions of the implanted electrode arrays are shown in red in Fig. 1c) and 137 neurons from the FEF (125 from Monkey A and 12 from Monkey B; electrode arrays are shown in blue in Fig. 1c) while the animals performed the task. Of the neurons recorded, more than 40% displayed selectiv-ity to target location in at least one stage during the trial (Fig. 1d). Examples of the responses of an LPFC and an FEF neuron are shown in Supplementary Fig. 1a,b. To quantify the magnitude of this selec-tivity, we computed the percentage of explained variance (PEV) for spatial selectivity in each neuron. The average PEVs across significant neurons (Methods) are shown in Fig. 1d. In the LPFC, we observed that target information in selective cells (n = 107, 42% of the LPFC population) increased during the target presentation period and remained stable throughout the rest of the trial (Fig. 1d). In addition, in Supplementary Fig. 1c, we show that the distractor information was much lower in these same neurons during the Delay 2 period (P textless 0.001, Hedges' g = 23.99). A previous study found a sharp decrease in target information following distractor presentation , together with an increase of distractor information 21. Our results, however, did not replicate these observations. Rather, we found that target information remained stable, and distractor information stayed close to baseline throughout the trial (Supplementary Fig. 1c). This difference may reflect the simpler nature of our task and the comparatively lower behavioral saliency of the distractor we used. It may also reflect differences in the ways different types of information are encoded; perhaps the working memory code for numerosity in LPFC is more susceptible to distractors than the code for spatial locations. In contrast, in the FEF we observed The prefrontal cortex maintains working memory information in the presence of distracting stimuli. It has long been thought that sustained activity in individual neurons or groups of neurons was responsible for maintaining information in the form of a persistent, stable code. Here we show that, upon the presentation of a distractor, information in the lateral prefrontal cortex was reorganized into a different pattern of activity to create a morphed stable code without losing information. In contrast, the code in the frontal eye fields persisted across different delay periods but exhibited substantial instability and information loss after the presentation of a distractor. We found that neurons with mixed-selective responses were necessary and sufficient for the morphing of code and that these neurons were more abundant in the lateral prefrontal cortex than the frontal eye fields. This suggests that mixed selectivity provides populations with code-morphing capability, a property that may underlie cognitive flexibility. |
Tyler R Peel; Suryadeep Dash; Stephen G Lomber; Brian D Corneil Frontal eye field inactivation diminishes superior colliculus activity, but delayed saccadic accumulation governs reaction time increases Journal Article The Journal of Neuroscience, 37 (48), pp. 11715–11730, 2017. @article{Peel2017, title = {Frontal eye field inactivation diminishes superior colliculus activity, but delayed saccadic accumulation governs reaction time increases}, author = {Tyler R Peel and Suryadeep Dash and Stephen G Lomber and Brian D Corneil}, doi = {10.1523/JNEUROSCI.2664-17.2017}, year = {2017}, date = {2017-01-01}, journal = {The Journal of Neuroscience}, volume = {37}, number = {48}, pages = {11715--11730}, abstract = {Stochastic accumulator models provide a comprehensive framework for how neural activity could produce behavior. Neural activity within the frontal eye fields (FEFs) and intermediate layers of the superior colliculus (iSC) support such models for saccade initiation by relating variations in saccade reaction time (SRT) to variations in such parameters as baseline, rate of accumulation of activity, and threshold. Here, by recording iSC activity during reversible cryogenic inactivation of the FEF in four male nonhuman primates, we causally tested which parameter(s) best explains concomitant increases in SRT. While FEF inactivation decreased all aspects of ipsilesional iSC activity, decreases in accumulation rate and threshold poorly predicted accompanying increases in SRT. Instead, SRT increases best correlated with delays in the onset of saccade-related accumulation. We conclude that FEF signals govern the onset of saccade-related accumulation within the iSC, and that the onset of accumulation is a relevant parameter for stochastic accumulation models of saccade initiation.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Stochastic accumulator models provide a comprehensive framework for how neural activity could produce behavior. Neural activity within the frontal eye fields (FEFs) and intermediate layers of the superior colliculus (iSC) support such models for saccade initiation by relating variations in saccade reaction time (SRT) to variations in such parameters as baseline, rate of accumulation of activity, and threshold. Here, by recording iSC activity during reversible cryogenic inactivation of the FEF in four male nonhuman primates, we causally tested which parameter(s) best explains concomitant increases in SRT. While FEF inactivation decreased all aspects of ipsilesional iSC activity, decreases in accumulation rate and threshold poorly predicted accompanying increases in SRT. Instead, SRT increases best correlated with delays in the onset of saccade-related accumulation. We conclude that FEF signals govern the onset of saccade-related accumulation within the iSC, and that the onset of accumulation is a relevant parameter for stochastic accumulation models of saccade initiation. |
Joel Reithler; Judith C Peters; Rainer Goebel NeuroImage, 152 , pp. 551–562, 2017. @article{Reithler2017, title = {Characterizing object- and position-dependent response profiles to uni- and bilateral stimulus configurations in human higher visual cortex: A 7T fMRI study}, author = {Joel Reithler and Judith C Peters and Rainer Goebel}, doi = {10.1016/j.neuroimage.2017.03.038}, year = {2017}, date = {2017-01-01}, journal = {NeuroImage}, volume = {152}, pages = {551--562}, abstract = {Visual scenes are initially processed via segregated neural pathways dedicated to either of the two visual hemifields. Although higher-order visual areas are generally believed to utilize invariant object representations (abstracted away from features such as stimulus position), recent findings suggest they retain more spatial information than previously thought. Here, we assessed the nature of such higher-order object representations in human cortex using high-resolution fMRI at 7T, supported by corroborative 3T data. We show that multi-voxel activation patterns in both the contra- and ipsilateral hemisphere can be exploited to successfully classify the object category of unilaterally presented stimuli. Moreover, robustly identified rank order-based response profiles demonstrated a strong contralateral bias which frequently outweighed object category preferences. Finally, we contrasted different combinatorial operations to predict the responses during bilateral stimulation conditions based on responses to their constituent unilateral elements. Results favored a max operation predominantly reflecting the contralateral stimuli. The current findings extend previous work by showing that configuration-dependent modulations in higher-order visual cortex responses as observed in single unit activity have a counterpart in human neural population coding. They furthermore corroborate the emerging view that position coding is a fundamental functional characteristic of ventral visual stream processing.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Visual scenes are initially processed via segregated neural pathways dedicated to either of the two visual hemifields. Although higher-order visual areas are generally believed to utilize invariant object representations (abstracted away from features such as stimulus position), recent findings suggest they retain more spatial information than previously thought. Here, we assessed the nature of such higher-order object representations in human cortex using high-resolution fMRI at 7T, supported by corroborative 3T data. We show that multi-voxel activation patterns in both the contra- and ipsilateral hemisphere can be exploited to successfully classify the object category of unilaterally presented stimuli. Moreover, robustly identified rank order-based response profiles demonstrated a strong contralateral bias which frequently outweighed object category preferences. Finally, we contrasted different combinatorial operations to predict the responses during bilateral stimulation conditions based on responses to their constituent unilateral elements. Results favored a max operation predominantly reflecting the contralateral stimuli. The current findings extend previous work by showing that configuration-dependent modulations in higher-order visual cortex responses as observed in single unit activity have a counterpart in human neural population coding. They furthermore corroborate the emerging view that position coding is a fundamental functional characteristic of ventral visual stream processing. |
Douglas A Ruff; Marlene R Cohen A normalization model suggests that attention changes the weighting of inputs between visual areas Journal Article Proceedings of the National Academy of Sciences, 114 (20), pp. E4085–E4094, 2017. @article{Ruff2017, title = {A normalization model suggests that attention changes the weighting of inputs between visual areas}, author = {Douglas A Ruff and Marlene R Cohen}, doi = {10.1073/pnas.1619857114}, year = {2017}, date = {2017-01-01}, journal = {Proceedings of the National Academy of Sciences}, volume = {114}, number = {20}, pages = {E4085--E4094}, abstract = {Models of divisive normalization can explain the trial-averaged responses of neurons in sensory, association, and motor areas under a wide range of conditions, including how visual attention changes the gains of neurons in visual cortex. Attention, like other modulatory processes, is also associated with changes in the extent to which pairs of neurons share trial-to-trial variability. We showed recently that in addition to decreasing correlations between similarly tuned neurons within the same visual area, attention increases correlations between neurons in primary visual cortex (V1) and the middle temporal area (MT) and that an extension of a classic normalization model can account for this correlation increase. One of the benefits of having a descriptive model that can account for many physiological observations is that it can be used to probe the mechanisms underlying processes such as attention. Here, we use electrical microstimulation in V1 paired with recording in MT to provide causal evidence that the relationship between V1 and MT activity is nonlinear and is well described by divisive normalization. We then use the normalization model and recording and microstimulation experiments to show that the attention dependence of V1-MT correlations is better explained by a mechanism in which attention changes the weights of connections between V1 and MT than by a mechanism that modulates responses in either area. Our study shows that normalization can explain interactions between neurons in different areas and provides a framework for using multiarea recording and stimulation to probe the neural mechanisms underlying neuronal computations.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Models of divisive normalization can explain the trial-averaged responses of neurons in sensory, association, and motor areas under a wide range of conditions, including how visual attention changes the gains of neurons in visual cortex. Attention, like other modulatory processes, is also associated with changes in the extent to which pairs of neurons share trial-to-trial variability. We showed recently that in addition to decreasing correlations between similarly tuned neurons within the same visual area, attention increases correlations between neurons in primary visual cortex (V1) and the middle temporal area (MT) and that an extension of a classic normalization model can account for this correlation increase. One of the benefits of having a descriptive model that can account for many physiological observations is that it can be used to probe the mechanisms underlying processes such as attention. Here, we use electrical microstimulation in V1 paired with recording in MT to provide causal evidence that the relationship between V1 and MT activity is nonlinear and is well described by divisive normalization. We then use the normalization model and recording and microstimulation experiments to show that the attention dependence of V1-MT correlations is better explained by a mechanism in which attention changes the weights of connections between V1 and MT than by a mechanism that modulates responses in either area. Our study shows that normalization can explain interactions between neurons in different areas and provides a framework for using multiarea recording and stimulation to probe the neural mechanisms underlying neuronal computations. |
Aldo Rustichini; Katherine E Conen; Xinying Cai; Camillo Padoa-Schioppa Optimal coding and neuronal adaptation in economic decisions Journal Article Nature Communications, 8 (1), pp. 1–14, 2017. @article{Rustichini2017, title = {Optimal coding and neuronal adaptation in economic decisions}, author = {Aldo Rustichini and Katherine E Conen and Xinying Cai and Camillo Padoa-Schioppa}, doi = {10.1038/s41467-017-01373-y}, year = {2017}, date = {2017-01-01}, journal = {Nature Communications}, volume = {8}, number = {1}, pages = {1--14}, publisher = {Springer US}, abstract = {During economic decisions, offer value cells in orbitofrontal cortex (OFC) encode the values of offered goods. Furthermore, their tuning functions adapt to the range of values available in any given context. A fundamental and open question is whether range adaptation is behaviorally advantageous. Here we present a theory of optimal coding for economic decisions. We propose that the representation of offer values is optimal if it ensures maximal expected payoff. In this framework, we examine offer value cells in non-human primates. We show that their responses are quasi-linear even when optimal tuning functions are highly non-linear. Most importantly, we demonstrate that for linear tuning functions range adaptation maximizes the expected payoff. Thus value coding in OFC is functionally rigid (linear tuning) but parametrically plastic (range adaptation with optimal gain). Importantly, the benefit of range adaptation outweighs the cost of functional rigidity. While generally suboptimal, linear tuning may facilitate transitive choices.}, keywords = {}, pubstate = {published}, tppubtype = {article} } During economic decisions, offer value cells in orbitofrontal cortex (OFC) encode the values of offered goods. Furthermore, their tuning functions adapt to the range of values available in any given context. A fundamental and open question is whether range adaptation is behaviorally advantageous. Here we present a theory of optimal coding for economic decisions. We propose that the representation of offer values is optimal if it ensures maximal expected payoff. In this framework, we examine offer value cells in non-human primates. We show that their responses are quasi-linear even when optimal tuning functions are highly non-linear. Most importantly, we demonstrate that for linear tuning functions range adaptation maximizes the expected payoff. Thus value coding in OFC is functionally rigid (linear tuning) but parametrically plastic (range adaptation with optimal gain). Importantly, the benefit of range adaptation outweighs the cost of functional rigidity. While generally suboptimal, linear tuning may facilitate transitive choices. |
Philipp Schwedhelm; Daniel Baldauf; Stefan Treue Electrical stimulation of macaque lateral prefrontal cortex modulates oculomotor behavior indicative of a disruption of top-down attention Journal Article Scientific Reports, 7 , pp. 1–10, 2017. @article{Schwedhelm2017, title = {Electrical stimulation of macaque lateral prefrontal cortex modulates oculomotor behavior indicative of a disruption of top-down attention}, author = {Philipp Schwedhelm and Daniel Baldauf and Stefan Treue}, doi = {10.1038/s41598-017-18153-9}, year = {2017}, date = {2017-01-01}, journal = {Scientific Reports}, volume = {7}, pages = {1--10}, publisher = {Springer US}, abstract = {The lateral prefrontal cortex (lPFC) of primates is hypothesized to be heavily involved in decision-making and selective visual attention. Recent neurophysiological evidence suggests that information necessary for an orchestration of those high-level cognitive factors are indeed represented in the lPFC. However, we know little about the specific contribution of sub-networks within lPFC to the deployment of top-down influences that can be measured in extrastriate visual cortex. Here, we systematically applied electrical stimulations to areas 8Av and 45 of two macaque monkeys performing a concurrent goal-directed saccade task. Despite using currents well above saccadic thresholds of the directly adjacent Frontal Eye Fields (FEF), saccades were only rarely evoked by the stimulation. Instead, two types of behavioral effects were observed: Stimulations of caudal sites in 8Av (close to FEF) shortened or prolonged saccadic reaction times, depending on the task-instructed saccade, while rostral stimulations of 8Av/45 seem to affect the relative attentional weighting of saccade targets as well as saccadic reaction times. These results illuminate important differences in the causal involvement of different sub-networks within the lPFC and are most compatible with a stimulation-induced biasing of stimulus processing that accelerates the detection of saccade targets presented ipsilateral to stimulation through a disruption of contralaterally deployed top-down attention.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The lateral prefrontal cortex (lPFC) of primates is hypothesized to be heavily involved in decision-making and selective visual attention. Recent neurophysiological evidence suggests that information necessary for an orchestration of those high-level cognitive factors are indeed represented in the lPFC. However, we know little about the specific contribution of sub-networks within lPFC to the deployment of top-down influences that can be measured in extrastriate visual cortex. Here, we systematically applied electrical stimulations to areas 8Av and 45 of two macaque monkeys performing a concurrent goal-directed saccade task. Despite using currents well above saccadic thresholds of the directly adjacent Frontal Eye Fields (FEF), saccades were only rarely evoked by the stimulation. Instead, two types of behavioral effects were observed: Stimulations of caudal sites in 8Av (close to FEF) shortened or prolonged saccadic reaction times, depending on the task-instructed saccade, while rostral stimulations of 8Av/45 seem to affect the relative attentional weighting of saccade targets as well as saccadic reaction times. These results illuminate important differences in the causal involvement of different sub-networks within the lPFC and are most compatible with a stimulation-induced biasing of stimulus processing that accelerates the detection of saccade targets presented ipsilateral to stimulation through a disruption of contralaterally deployed top-down attention. |
Lenka Seillier; Corinna Lorenz; Katsuhisa Kawaguchi; Torben Ott; Andreas Nieder; Paria Pourriahi; Hendrikje Nienborg Serotonin decreases the gain of visual responses in awake macaque V1 Journal Article The Journal of Neuroscience, 37 (47), pp. 11390 –11405 Systems/Circuits, 2017. @article{Seillier2017, title = {Serotonin decreases the gain of visual responses in awake macaque V1}, author = {Lenka Seillier and Corinna Lorenz and Katsuhisa Kawaguchi and Torben Ott and Andreas Nieder and Paria Pourriahi and Hendrikje Nienborg}, doi = {10.1523/JNEUROSCI.1339-17.2017}, year = {2017}, date = {2017-01-01}, journal = {The Journal of Neuroscience}, volume = {37}, number = {47}, pages = {11390 --11405 Systems/Circuits}, abstract = {Serotonin, an important neuromodulator in the brain, is implicated in affective and cognitive functions. However, its role even for basic cortical processes is controversial. For example, in the mammalian primary visual cortex (V1), heterogenous serotonergic modulation has been observed in anesthetized animals. Here, we combined extracellular single-unit recordings with iontophoresis in awake animals. We examined the role of serotonin on well-defined tuning properties (orientation, spatial frequency, contrast, and size) in V1 of two male macaque monkeys. We find that in the awake macaque the modulatory effect of serotonin is surprisingly uniform: it causes a mainly multiplicative decrease of the visual responses and a slight increase in the stimulus-selective response latency. Moreover, serotonin neither systematically changes the selectivity or variability of the response, nor the interneuronal correlation unexplained by the stimulus ("noise-correlation"). The modulation by serotonin has qualitative similarities with that for a decrease in stimulus contrast, but differs quantitatively from decreasing contrast. It can be captured by a simple additive change to a threshold-linear spiking nonlinearity. Together, our results show that serotonin is well suited to control the response gain of neurons in V1 depending on the animal's behavioral or motivational context, complementing other known state-dependent gain-control mechanisms.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Serotonin, an important neuromodulator in the brain, is implicated in affective and cognitive functions. However, its role even for basic cortical processes is controversial. For example, in the mammalian primary visual cortex (V1), heterogenous serotonergic modulation has been observed in anesthetized animals. Here, we combined extracellular single-unit recordings with iontophoresis in awake animals. We examined the role of serotonin on well-defined tuning properties (orientation, spatial frequency, contrast, and size) in V1 of two male macaque monkeys. We find that in the awake macaque the modulatory effect of serotonin is surprisingly uniform: it causes a mainly multiplicative decrease of the visual responses and a slight increase in the stimulus-selective response latency. Moreover, serotonin neither systematically changes the selectivity or variability of the response, nor the interneuronal correlation unexplained by the stimulus ("noise-correlation"). The modulation by serotonin has qualitative similarities with that for a decrease in stimulus contrast, but differs quantitatively from decreasing contrast. It can be captured by a simple additive change to a threshold-linear spiking nonlinearity. Together, our results show that serotonin is well suited to control the response gain of neurons in V1 depending on the animal's behavioral or motivational context, complementing other known state-dependent gain-control mechanisms. |
Brianna J Sleezer; Giuliana LoConte; Meghan D Castagno; Benjamin Y Hayden Neuronal responses support a role for orbitofrontal cortex in cognitive set reconfiguration Journal Article European Journal of Neuroscience, 45 , pp. 940–951, 2017. @article{Sleezer2017, title = {Neuronal responses support a role for orbitofrontal cortex in cognitive set reconfiguration}, author = {Brianna J Sleezer and Giuliana LoConte and Meghan D Castagno and Benjamin Y Hayden}, year = {2017}, date = {2017-01-01}, journal = {European Journal of Neuroscience}, volume = {45}, pages = {940--951}, abstract = {We are often faced with the need to abandon no-longer beneficial rules and adopt new ones. This process, known as cognitive set reconfiguration, is a hallmark of executive control. Although cognitive functions like reconfiguration are most often associated with dorsal prefrontal structures, recent evidence suggests that the orbitofrontal cortex (OFC) may play an important role as well. We recorded the activity of OFC neurons while rhesus macaques performed an analogue of the Wisconsin Card Sorting Task that involved a trial and error stage. The OFC neurons demonstrated two types of switch-related activity, an early (switch-away) signal and a late (switch-to) signal, when the new task set was established. We also found a pattern of match modulation: a sig- nificant change in activity for the stimulus that matched the current perceptual rule (and would therefore be selected). These results extend our understanding of the executive functions of the OFC. They also allow us to directly compare the OFC with the complementary datasets we previously collected in the ventral (VS) and dorsal (DS) striatum. Although both effects are observed in all three areas, the timing of responses aligns the OFC more closely with DS than with VS.}, keywords = {}, pubstate = {published}, tppubtype = {article} } We are often faced with the need to abandon no-longer beneficial rules and adopt new ones. This process, known as cognitive set reconfiguration, is a hallmark of executive control. Although cognitive functions like reconfiguration are most often associated with dorsal prefrontal structures, recent evidence suggests that the orbitofrontal cortex (OFC) may play an important role as well. We recorded the activity of OFC neurons while rhesus macaques performed an analogue of the Wisconsin Card Sorting Task that involved a trial and error stage. The OFC neurons demonstrated two types of switch-related activity, an early (switch-away) signal and a late (switch-to) signal, when the new task set was established. We also found a pattern of match modulation: a sig- nificant change in activity for the stimulus that matched the current perceptual rule (and would therefore be selected). These results extend our understanding of the executive functions of the OFC. They also allow us to directly compare the OFC with the complementary datasets we previously collected in the ventral (VS) and dorsal (DS) striatum. Although both effects are observed in all three areas, the timing of responses aligns the OFC more closely with DS than with VS. |
Courtney Turrin; Nicholas A Fagan; Olga Dal Monte; Steve W C Chang Social resource foraging is guided by the principles of the Marginal Value Theorem Journal Article Scientific Reports, 7 (1), pp. 1–13, 2017. @article{Turrin2017, title = {Social resource foraging is guided by the principles of the Marginal Value Theorem}, author = {Courtney Turrin and Nicholas A Fagan and Olga Dal Monte and Steve W C Chang}, doi = {10.1038/s41598-017-11763-3}, year = {2017}, date = {2017-01-01}, journal = {Scientific Reports}, volume = {7}, number = {1}, pages = {1--13}, publisher = {Springer US}, abstract = {Optimality principles guide how animals adapt to changing environments. During foraging for nonsocial resources such as food and water, species across taxa obey a strategy that maximizes resource harvest rate. However, it remains unknown whether foraging for social resources also obeys such a strategic principle. We investigated how primates forage for social information conveyed by conspecific facial expressions using the framework of optimal foraging theory. We found that the canonical principle of Marginal Value Theorem (MVT) also applies to social resources. Consistent with MVT, rhesus macaques (Macaca mulatta) spent more time foraging for social information when alternative sources of information were farther away compared to when they were closer by. A comparison of four models of patch-leaving behavior confirmed that the MVT framework provided the best fit to the observed foraging behavior. This analysis further demonstrated that patch-leaving decisions were not driven simply by the declining value of the images in the patch, but instead were dependent upon both the instantaneous social value intake rate and current time in the patch.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Optimality principles guide how animals adapt to changing environments. During foraging for nonsocial resources such as food and water, species across taxa obey a strategy that maximizes resource harvest rate. However, it remains unknown whether foraging for social resources also obeys such a strategic principle. We investigated how primates forage for social information conveyed by conspecific facial expressions using the framework of optimal foraging theory. We found that the canonical principle of Marginal Value Theorem (MVT) also applies to social resources. Consistent with MVT, rhesus macaques (Macaca mulatta) spent more time foraging for social information when alternative sources of information were farther away compared to when they were closer by. A comparison of four models of patch-leaving behavior confirmed that the MVT framework provided the best fit to the observed foraging behavior. This analysis further demonstrated that patch-leaving decisions were not driven simply by the declining value of the images in the patch, but instead were dependent upon both the instantaneous social value intake rate and current time in the patch. |
Bram-Ernst Verhoef; John H R Maunsell Attention-related changes in correlated neuronal activity arise from normalization mechanisms Journal Article Nature Neuroscience, 20 (7), pp. 969–977, 2017. @article{Verhoef2017, title = {Attention-related changes in correlated neuronal activity arise from normalization mechanisms}, author = {Bram-Ernst Verhoef and John H R Maunsell}, doi = {10.1038/nn.4572}, year = {2017}, date = {2017-01-01}, journal = {Nature Neuroscience}, volume = {20}, number = {7}, pages = {969--977}, publisher = {Nature Publishing Group}, abstract = {Attention is believed to enhance perception by altering the activity-level correlations between pairs of neurons. How attention changes neuronal activity correlations is unknown. Using multielectrodes in monkey visual cortex, we measured spike-count correlations when single or multiple stimuli were presented and when stimuli were attended or unattended. When stimuli were unattended, adding a suppressive, nonpreferred stimulus beside a preferred stimulus increased spike-count correlations between pairs of similarly tuned neurons but decreased spike-count correlations between pairs of oppositely tuned neurons. A stochastic normalization model containing populations of oppositely tuned, mutually suppressive neurons explains these changes and also explains why attention decreased or increased correlations: as an indirect consequence of attention-related changes in the inputs to normalization mechanisms. Our findings link normalization mechanisms to correlated neuronal activity and attention, showing that normalization mechanisms shape response correlations and that these correlations change when attention biases normalization mechanisms.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Attention is believed to enhance perception by altering the activity-level correlations between pairs of neurons. How attention changes neuronal activity correlations is unknown. Using multielectrodes in monkey visual cortex, we measured spike-count correlations when single or multiple stimuli were presented and when stimuli were attended or unattended. When stimuli were unattended, adding a suppressive, nonpreferred stimulus beside a preferred stimulus increased spike-count correlations between pairs of similarly tuned neurons but decreased spike-count correlations between pairs of oppositely tuned neurons. A stochastic normalization model containing populations of oppositely tuned, mutually suppressive neurons explains these changes and also explains why attention decreased or increased correlations: as an indirect consequence of attention-related changes in the inputs to normalization mechanisms. Our findings link normalization mechanisms to correlated neuronal activity and attention, showing that normalization mechanisms shape response correlations and that these correlations change when attention biases normalization mechanisms. |
Maya Zhe Wang; Benjamin Y Hayden Reactivation of associative structure specific outcome responses during prospective evaluation in reward-based choices Journal Article Nature communications, 8 , pp. 1–13, 2017. @article{Wang2017e, title = {Reactivation of associative structure specific outcome responses during prospective evaluation in reward-based choices}, author = {Maya Zhe Wang and Benjamin Y Hayden}, doi = {10.1038/ncomms15821}, year = {2017}, date = {2017-01-01}, journal = {Nature communications}, volume = {8}, pages = {1--13}, publisher = {Nature Publishing Group}, abstract = {Before making a reward-based choice, we must evaluate each option. Some theories propose that prospective evaluation involves a reactivation of the neural response to the outcome. Others propose that it calls upon a response pattern that is specific to each underlying associative structure. We hypothesize that these views are reconcilable: during prospective evaluation, offers reactivate neural responses to outcomes that are unique to each associative structure; when the outcome occurs, this pattern is activated, simultaneously, with a general response to the reward. We recorded single-units from macaque orbitofrontal cortex (Area 13) in a riskless choice task with interleaved described and experienced offer trials. Here we report that neural activations to offers and their outcomes overlap, as do neural activations to the outcomes on the two trial types. Neural activations to experienced and described offers are unrelated even though they predict the same outcomes. Our reactivation theory parsimoniously explains these results.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Before making a reward-based choice, we must evaluate each option. Some theories propose that prospective evaluation involves a reactivation of the neural response to the outcome. Others propose that it calls upon a response pattern that is specific to each underlying associative structure. We hypothesize that these views are reconcilable: during prospective evaluation, offers reactivate neural responses to outcomes that are unique to each associative structure; when the outcome occurs, this pattern is activated, simultaneously, with a general response to the reward. We recorded single-units from macaque orbitofrontal cortex (Area 13) in a riskless choice task with interleaved described and experienced offer trials. Here we report that neural activations to offers and their outcomes overlap, as do neural activations to the outcomes on the two trial types. Neural activations to experienced and described offers are unrelated even though they predict the same outcomes. Our reactivation theory parsimoniously explains these results. |
Brian J White; David J Berg; Janis Y Kan; Robert A Marino; Laurent Itti; Douglas P Munoz Superior colliculus neurons encode a visual saliency map during free viewing of natural dynamic video Journal Article Nature Communications, 8 , pp. 1–9, 2017. @article{White2017b, title = {Superior colliculus neurons encode a visual saliency map during free viewing of natural dynamic video}, author = {Brian J White and David J Berg and Janis Y Kan and Robert A Marino and Laurent Itti and Douglas P Munoz}, doi = {10.1038/ncomms14263}, year = {2017}, date = {2017-01-01}, journal = {Nature Communications}, volume = {8}, pages = {1--9}, publisher = {Nature Publishing Group}, abstract = {Models of visual attention postulate the existence of a saliency map whose function is to guide attention and gaze to the most conspicuous regions in a visual scene. Although cortical representations of saliency have been reported, there is mounting evidence for a subcortical saliency mechanism, which pre-dates the evolution of neocortex. Here, we conduct a strong test of the saliency hypothesis by comparing the output of a well-established computational saliency model with the activation of neurons in the primate superior colliculus (SC), a midbrain structure associated with attention and gaze, while monkeys watched video of natural scenes. We find that the activity of SC superficial visual-layer neurons (SCs), specifically, is well-predicted by the model. This saliency representation is unlikely to be inherited from fronto-parietal cortices, which do not project to SCs, but may be computed in SCs and relayed to other areas via tectothalamic pathways.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Models of visual attention postulate the existence of a saliency map whose function is to guide attention and gaze to the most conspicuous regions in a visual scene. Although cortical representations of saliency have been reported, there is mounting evidence for a subcortical saliency mechanism, which pre-dates the evolution of neocortex. Here, we conduct a strong test of the saliency hypothesis by comparing the output of a well-established computational saliency model with the activation of neurons in the primate superior colliculus (SC), a midbrain structure associated with attention and gaze, while monkeys watched video of natural scenes. We find that the activity of SC superficial visual-layer neurons (SCs), specifically, is well-predicted by the model. This saliency representation is unlikely to be inherited from fronto-parietal cortices, which do not project to SCs, but may be computed in SCs and relayed to other areas via tectothalamic pathways. |
Brian J White; Janis Y Kan; Ron Levy; Laurent Itti; Douglas P Munoz Superior colliculus encodes visual saliency before the primary visual cortex Journal Article Proceedings of the National Academy of Sciences, 114 (35), pp. 9451–9456, 2017. @article{White2017c, title = {Superior colliculus encodes visual saliency before the primary visual cortex}, author = {Brian J White and Janis Y Kan and Ron Levy and Laurent Itti and Douglas P Munoz}, doi = {10.1073/pnas.1701003114}, year = {2017}, date = {2017-01-01}, journal = {Proceedings of the National Academy of Sciences}, volume = {114}, number = {35}, pages = {9451--9456}, abstract = {Models of visual attention postulate the existence of a bottom-up saliency map that is formed early in the visual processing stream. Although studies have reported evidence of a saliency map in various cortical brain areas, determining the contribution of phylogenetically older pathways is crucial to understanding its origin. Here, we compared saliency coding from neurons in two early gateways into the visual system: the primary visual cortex (V1) and the evolutionarily older superior colliculus (SC). We found that, while the response latency to visual stimulus onset was earlier for V1 neurons than superior colliculus superficial visual-layer neurons (SCs), the saliency representation emerged earlier in SCs than in V1. Because the dominant input to the SCs arises from V1, these relative timings are consistent with the hypothesis that SCs neurons pool the inputs from multiple V1 neurons to form a feature-agnostic saliency map, which may then be relayed to other brain areas.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Models of visual attention postulate the existence of a bottom-up saliency map that is formed early in the visual processing stream. Although studies have reported evidence of a saliency map in various cortical brain areas, determining the contribution of phylogenetically older pathways is crucial to understanding its origin. Here, we compared saliency coding from neurons in two early gateways into the visual system: the primary visual cortex (V1) and the evolutionarily older superior colliculus (SC). We found that, while the response latency to visual stimulus onset was earlier for V1 neurons than superior colliculus superficial visual-layer neurons (SCs), the saliency representation emerged earlier in SCs than in V1. Because the dominant input to the SCs arises from V1, these relative timings are consistent with the hypothesis that SCs neurons pool the inputs from multiple V1 neurons to form a feature-agnostic saliency map, which may then be relayed to other brain areas. |
Niklas Wilming; Tim C Kietzmann; Megan Jutras; Cheng Xue; Stefan Treue; Elizabeth A Buffalo; Peter König Differential contribution of low- and high-level image content to eye movements in monkeys and humans Journal Article Cerebral Cortex, 27 (1), pp. 279–293, 2017. @article{Wilming2017, title = {Differential contribution of low- and high-level image content to eye movements in monkeys and humans}, author = {Niklas Wilming and Tim C Kietzmann and Megan Jutras and Cheng Xue and Stefan Treue and Elizabeth A Buffalo and Peter König}, doi = {10.1093/cercor/bhw399}, year = {2017}, date = {2017-01-01}, journal = {Cerebral Cortex}, volume = {27}, number = {1}, pages = {279--293}, abstract = {Oculomotor selection exerts a fundamental impact on our experience of the environment. To better understand the underlying principles, researchers typically rely on behavioral data from humans, and electrophysiological recordings in macaque monkeys. This approach rests on the assumption that the same selection processes are at play in both species. To test this assumption, we compared the viewing behavior of 106 humans and 11 macaques in an unconstrained free-viewing task. Our data-driven clustering analyses revealed distinct human and macaque clusters, indicating species-specific selection strategies. Yet, cross-species predictions were found to be above chance, indicating some level of shared behavior. Analyses relying on computational models of visual saliency indicate that such cross-species commonalities in free viewing are largely due to similar low-level selection mechanisms, with only a small contribution by shared higher level selection mechanisms and with consistent viewing behavior of monkeys being a subset of the consistent viewing behavior of humans.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Oculomotor selection exerts a fundamental impact on our experience of the environment. To better understand the underlying principles, researchers typically rely on behavioral data from humans, and electrophysiological recordings in macaque monkeys. This approach rests on the assumption that the same selection processes are at play in both species. To test this assumption, we compared the viewing behavior of 106 humans and 11 macaques in an unconstrained free-viewing task. Our data-driven clustering analyses revealed distinct human and macaque clusters, indicating species-specific selection strategies. Yet, cross-species predictions were found to be above chance, indicating some level of shared behavior. Analyses relying on computational models of visual saliency indicate that such cross-species commonalities in free viewing are largely due to similar low-level selection mechanisms, with only a small contribution by shared higher level selection mechanisms and with consistent viewing behavior of monkeys being a subset of the consistent viewing behavior of humans. |
Kitty Z Xu; Brian A Anderson; Erik E Emeric; Anthony W Sali; Veit Stuphorn; Steven Yantis; Susan M Courtney Neural basis of cognitive control over movement inhibition: Human fMRI and primate electrophysiology evidence Journal Article Neuron, 96 (6), pp. 1447–1458, 2017. @article{Xu2017, title = {Neural basis of cognitive control over movement inhibition: Human fMRI and primate electrophysiology evidence}, author = {Kitty Z Xu and Brian A Anderson and Erik E Emeric and Anthony W Sali and Veit Stuphorn and Steven Yantis and Susan M Courtney}, doi = {10.1016/j.neuron.2017.11.010}, year = {2017}, date = {2017-01-01}, journal = {Neuron}, volume = {96}, number = {6}, pages = {1447--1458}, publisher = {Elsevier Inc.}, abstract = {Executive control involves the ability to flexibly inhibit or change an action when it is contextually inappropriate. Using the complimentary techniques of human fMRI and monkey electrophysiology in a context-dependent stop signal task, we found a functional double dissociation between the right ventrolateral prefrontal cortex (rVLPFC) and the bi-lateral frontal eye field (FEF). Different regions of rVLPFC were associated with context-based signal meaning versus intention to inhibit a response, while FEF activity corresponded to success or failure of the response inhibition regardless of the stimulus response mapping or the context. These results were validated by electrophysiological recordings in rVLPFC and FEF from one monkey. Inhibition of a planned behavior is therefore likely not governed by a single brain system as had been previously proposed, but instead depends on two distinct neural processes involving different sub-regions of the rVLPFC and their interactions with other motor-related brain regions. Xu et al. present a rare combination of complementary evidence from human fMRI and primate neurophysiology, demonstrating that response inhibition is not directly accomplished by the rVLPFC, but instead requires multiple, distinct rVLPFC networks involving attention and contextual stimulus interpretation.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Executive control involves the ability to flexibly inhibit or change an action when it is contextually inappropriate. Using the complimentary techniques of human fMRI and monkey electrophysiology in a context-dependent stop signal task, we found a functional double dissociation between the right ventrolateral prefrontal cortex (rVLPFC) and the bi-lateral frontal eye field (FEF). Different regions of rVLPFC were associated with context-based signal meaning versus intention to inhibit a response, while FEF activity corresponded to success or failure of the response inhibition regardless of the stimulus response mapping or the context. These results were validated by electrophysiological recordings in rVLPFC and FEF from one monkey. Inhibition of a planned behavior is therefore likely not governed by a single brain system as had been previously proposed, but instead depends on two distinct neural processes involving different sub-regions of the rVLPFC and their interactions with other motor-related brain regions. Xu et al. present a rare combination of complementary evidence from human fMRI and primate neurophysiology, demonstrating that response inhibition is not directly accomplished by the rVLPFC, but instead requires multiple, distinct rVLPFC networks involving attention and contextual stimulus interpretation. |
Jacob L Yates; Il Memming Park; Leor N Katz; Jonathan W Pillow; Alexander C Huk Functional dissection of signal and noise in MT and LIP during decision-making Journal Article Nature Neuroscience, 20 (9), pp. 1285–1292, 2017. @article{Yates2017, title = {Functional dissection of signal and noise in MT and LIP during decision-making}, author = {Jacob L Yates and Il Memming Park and Leor N Katz and Jonathan W Pillow and Alexander C Huk}, doi = {10.1038/nn.4611}, year = {2017}, date = {2017-01-01}, journal = {Nature Neuroscience}, volume = {20}, number = {9}, pages = {1285--1292}, publisher = {Nature Publishing Group}, abstract = {During perceptual decision-making, responses in the middle temporal (MT) and lateral intraparietal (LIP) areas appear to map onto theoretically defined quantities, with MT representing instantaneous motion evidence and LIP reflecting the accumulated evidence. However, several aspects of the transformation between the two areas have not been empirically tested. We therefore performed multistage systems identification analyses of the simultaneous activity of MT and LIP during individual decisions. We found that monkeys based their choices on evidence presented in early epochs of the motion stimulus and that substantial early weighting of motion was present in MT responses. LIP responses recapitulated MT early weighting and contained a choice-dependent buildup that was distinguishable from motion integration. Furthermore, trial-by-trial variability in LIP did not depend on MT activity. These results identify important deviations from idealizations of MT and LIP and motivate inquiry into sensorimotor computations that may intervene between MT and LIP.}, keywords = {}, pubstate = {published}, tppubtype = {article} } During perceptual decision-making, responses in the middle temporal (MT) and lateral intraparietal (LIP) areas appear to map onto theoretically defined quantities, with MT representing instantaneous motion evidence and LIP reflecting the accumulated evidence. However, several aspects of the transformation between the two areas have not been empirically tested. We therefore performed multistage systems identification analyses of the simultaneous activity of MT and LIP during individual decisions. We found that monkeys based their choices on evidence presented in early epochs of the motion stimulus and that substantial early weighting of motion was present in MT responses. LIP responses recapitulated MT early weighting and contained a choice-dependent buildup that was distinguishable from motion integration. Furthermore, trial-by-trial variability in LIP did not depend on MT activity. These results identify important deviations from idealizations of MT and LIP and motivate inquiry into sensorimotor computations that may intervene between MT and LIP. |
2016 |
Sujaya Neupane; Daniel Guitton; Christopher C Pack Two distinct types of remapping in primate cortical area V4 Journal Article Nature Communications, 7 , pp. 1–11, 2016. @article{Neupane2016a, title = {Two distinct types of remapping in primate cortical area V4}, author = {Sujaya Neupane and Daniel Guitton and Christopher C Pack}, doi = {10.1038/ncomms10402}, year = {2016}, date = {2016-12-01}, journal = {Nature Communications}, volume = {7}, pages = {1--11}, publisher = {Nature Publishing Group}, abstract = {Visual neurons typically receive information from a limited portion of the retina, and such receptive fields are a key organizing principle for much of visual cortex. At the same time, there is strong evidence that receptive fields transiently shift around the time of saccades. The nature of the shift is controversial: Previous studies have found shifts consistent with a role for perceptual constancy; other studies suggest a role in the allocation of spatial attention. Here we present evidence that both the previously documented functions exist in individual neurons in primate cortical area V4. Remapping associated with perceptual constancy occurs for saccades in all directions, while attentional shifts mainly occur for neurons with receptive fields in the same hemifield as the saccade end point. The latter are relatively sluggish and can be observed even during saccade planning. Overall these results suggest a complex interplay of visual and extraretinal influences during the execution of saccades.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Visual neurons typically receive information from a limited portion of the retina, and such receptive fields are a key organizing principle for much of visual cortex. At the same time, there is strong evidence that receptive fields transiently shift around the time of saccades. The nature of the shift is controversial: Previous studies have found shifts consistent with a role for perceptual constancy; other studies suggest a role in the allocation of spatial attention. Here we present evidence that both the previously documented functions exist in individual neurons in primate cortical area V4. Remapping associated with perceptual constancy occurs for saccades in all directions, while attentional shifts mainly occur for neurons with receptive fields in the same hemifield as the saccade end point. The latter are relatively sluggish and can be observed even during saccade planning. Overall these results suggest a complex interplay of visual and extraretinal influences during the execution of saccades. |
Nayoung So; Veit Stuphorn Supplementary eye field encodes confidence in decisions under risk Journal Article Cerebral Cortex, 26 (2), pp. 764–782, 2016. @article{So2016h, title = {Supplementary eye field encodes confidence in decisions under risk}, author = {Nayoung So and Veit Stuphorn}, doi = {10.1093/cercor/bhv025}, year = {2016}, date = {2016-03-01}, journal = {Cerebral Cortex}, volume = {26}, number = {2}, pages = {764--782}, publisher = {Oxford University Press}, abstract = {Choices are made with varying degrees of confidence, a cognitive signal representing the subjective belief in the optimality of the choice. Confidence has been mostly studied in the context of perceptual judgments, in which choice accuracy can be measured using objective criteria. Here, we study confidence in subjective value-based decisions. We recorded in the supplementary eye field (SEF) of monkeys performing a gambling task, where they had to use subjective criteria for placing bets. We found neural signals in the SEF that explicitly represent choice confidence independent from reward expectation. This confidence signal appeared after the choice and diminished before the choice outcome. Most of this neuronal activity was negatively correlated with confidence, and was strongest in trials on which the monkey spontaneously withdrew his choice. Such confidence-related activity indicates that the SEF not only guides saccade selection, but also evaluates the likelihood that the choice was optimal. This internal evaluation influences decisions concerning the willingness to bear later costs that follow from the choice or to avoid them. More generally, our findings indicate that choice confidence is an integral component of all forms of decision-making, whether they are based on perceptual evidence or on value estimations.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Choices are made with varying degrees of confidence, a cognitive signal representing the subjective belief in the optimality of the choice. Confidence has been mostly studied in the context of perceptual judgments, in which choice accuracy can be measured using objective criteria. Here, we study confidence in subjective value-based decisions. We recorded in the supplementary eye field (SEF) of monkeys performing a gambling task, where they had to use subjective criteria for placing bets. We found neural signals in the SEF that explicitly represent choice confidence independent from reward expectation. This confidence signal appeared after the choice and diminished before the choice outcome. Most of this neuronal activity was negatively correlated with confidence, and was strongest in trials on which the monkey spontaneously withdrew his choice. Such confidence-related activity indicates that the SEF not only guides saccade selection, but also evaluates the likelihood that the choice was optimal. This internal evaluation influences decisions concerning the willingness to bear later costs that follow from the choice or to avoid them. More generally, our findings indicate that choice confidence is an integral component of all forms of decision-making, whether they are based on perceptual evidence or on value estimations. |
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. @article{Acker2016, title = {FEF inactivation with improved optogenetic methods}, author = {Leah Acker and Erica N Pino and Edward S Boyden and Robert Desimone}, 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; Rufin Vogels Perturbation of posterior inferior temporal cortical activity impairs coarse orientation discrimination Journal Article Cerebral Cortex, 26 (9), pp. 3814–3827, 2016. @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. @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. |
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. @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. |
Paul L Aparicio; Elias B Issa; James J DiCarlo Neurophysiological organization of the middle face patch in macaque inferior temporal cortex Journal Article The Journal of Neuroscience, 36 (50), pp. 12729–12745, 2016. @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}, doi = {10.1523/JNEUROSCI.0237-16.2016}, year = {2016}, date = {2016-01-01}, journal = {The 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. @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. |
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. @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}, 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. |