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.
2014 |
Mari Anzai; Soich Nagao Motor learning in common marmosets: Vestibulo-ocular reflex adaptation and its sensitivity to inhibitors of Purkinje cell long-term depression Journal Article Neuroscience Research, 83 , pp. 33–42, 2014. @article{Anzai2014, title = {Motor learning in common marmosets: Vestibulo-ocular reflex adaptation and its sensitivity to inhibitors of Purkinje cell long-term depression}, author = {Mari Anzai and Soich Nagao}, doi = {10.1016/j.neures.2014.04.002}, year = {2014}, date = {2014-01-01}, journal = {Neuroscience Research}, volume = {83}, pages = {33--42}, publisher = {83}, abstract = {Adaptation of the horizontal vestibulo-ocular reflex (HVOR) provides an experimental model for cerebellum-dependent motor learning. We developed an eye movement measuring system and a paradigm for induction of HVOR adaptation for the common marmoset. The HVOR gain in dark measured by 10° (peak-to-peak amplitude) and 0.11-0.5. Hz turntable oscillation was around unity. The gain-up and gain-down HVOR adaptation was induced by 1. h of sustained out-of-phase and in-phase 10°-0.33. Hz combined turntable-screen oscillation in the light, respectively. To examine the role of long-term depression (LTD) of parallel fiber-Purkinje cell synapses, we intraperitonially applied T-588 or nimesulide, which block the induction of LTD in vitro or in vivo preparations, 1. h before the test of HVOR adaptation. T-588 (3 and 5. mg/kg body weight) did not affect nonadapted HVOR gains, and impaired both gain-up and gain-down HVOR adaptation. Nimesulide (3 and 6. mg/kg) did not affect nonadapted HVOR gains, and impaired gain-up HVOR adaptation dose-dependently; however, it very little affected gain-down HVOR adaptation. These findings are consistent with the results of our study of nimesulide on the adaptation of horizontal optokinetic response in mice (. Le et al., 2010), and support the view that LTD underlies HVOR adaptation.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Adaptation of the horizontal vestibulo-ocular reflex (HVOR) provides an experimental model for cerebellum-dependent motor learning. We developed an eye movement measuring system and a paradigm for induction of HVOR adaptation for the common marmoset. The HVOR gain in dark measured by 10° (peak-to-peak amplitude) and 0.11-0.5. Hz turntable oscillation was around unity. The gain-up and gain-down HVOR adaptation was induced by 1. h of sustained out-of-phase and in-phase 10°-0.33. Hz combined turntable-screen oscillation in the light, respectively. To examine the role of long-term depression (LTD) of parallel fiber-Purkinje cell synapses, we intraperitonially applied T-588 or nimesulide, which block the induction of LTD in vitro or in vivo preparations, 1. h before the test of HVOR adaptation. T-588 (3 and 5. mg/kg body weight) did not affect nonadapted HVOR gains, and impaired both gain-up and gain-down HVOR adaptation. Nimesulide (3 and 6. mg/kg) did not affect nonadapted HVOR gains, and impaired gain-up HVOR adaptation dose-dependently; however, it very little affected gain-down HVOR adaptation. These findings are consistent with the results of our study of nimesulide on the adaptation of horizontal optokinetic response in mice (. Le et al., 2010), and support the view that LTD underlies HVOR adaptation. |
Dong Hyun Baek; Jeyeon Lee; Hang Jin Byeon; Hoseok Choi; In Young Kim; Kyoung-Min Lee; James Jungho Pak; Dong Pyo Jang; Sang Hoon Lee A thin film polyimide mesh microelectrode for chronic epidural electrocorticography recording with enhanced contactability Journal Article Journal of Neural Engineering, 11 (4), pp. 1–10, 2014. @article{Baek2014, title = {A thin film polyimide mesh microelectrode for chronic epidural electrocorticography recording with enhanced contactability}, author = {Dong Hyun Baek and Jeyeon Lee and Hang Jin Byeon and Hoseok Choi and In Young Kim and Kyoung-Min Lee and James Jungho Pak and Dong Pyo Jang and Sang Hoon Lee}, doi = {10.1088/1741-2560/11/4/046023}, year = {2014}, date = {2014-01-01}, journal = {Journal of Neural Engineering}, volume = {11}, number = {4}, pages = {1--10}, publisher = {IOP Publishing}, abstract = {Objective. Epidural electrocorticography (ECoG) activity may be more reliable and stable than single-unit-activity or local field potential. Invasive brain computer interface (BCI) devices are limited by mechanical mismatching and cellular reactive responses due to differences in the elastic modulus and the motion of stiff electrodes. We propose a mesh-shaped electrode to enhance the contactability between surface of dura and electrode. Approach. We designed a polyimide (PI) electrode with a mesh pattern for more conformal contact with a curved surface. We compared the contact capability of mesh PI electrodes with conventionally used sheet PI electrode. The electrical properties of the mesh PI electrode were evaluated for four weeks. We recorded the epidural ECoG (eECoG) activity on the surface of rhesus monkey brains while they performed a saccadic task for four months. Main results. The mesh PI electrode showed good contact with the agarose brain surface, as evaluated by visual inspection and signal measurement. It was about 87% accurate in predicting the direction of saccade eye movement. Significance. Our results indicate that the mesh PI electrode was flexible and good contact on the curved surface and can record eECoG activity maintaining close contact to dura, which was proved by in vivo and in vitro test.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Objective. Epidural electrocorticography (ECoG) activity may be more reliable and stable than single-unit-activity or local field potential. Invasive brain computer interface (BCI) devices are limited by mechanical mismatching and cellular reactive responses due to differences in the elastic modulus and the motion of stiff electrodes. We propose a mesh-shaped electrode to enhance the contactability between surface of dura and electrode. Approach. We designed a polyimide (PI) electrode with a mesh pattern for more conformal contact with a curved surface. We compared the contact capability of mesh PI electrodes with conventionally used sheet PI electrode. The electrical properties of the mesh PI electrode were evaluated for four weeks. We recorded the epidural ECoG (eECoG) activity on the surface of rhesus monkey brains while they performed a saccadic task for four months. Main results. The mesh PI electrode showed good contact with the agarose brain surface, as evaluated by visual inspection and signal measurement. It was about 87% accurate in predicting the direction of saccade eye movement. Significance. Our results indicate that the mesh PI electrode was flexible and good contact on the curved surface and can record eECoG activity maintaining close contact to dura, which was proved by in vivo and in vitro test. |
T C Blanchard; B Y Hayden Neurons in dorsal anterior cingulate cortex signal postdecisional variables in a foraging task Journal Article The Journal of Neuroscience, 34 (2), pp. 646–655, 2014. @article{Blanchard2014, title = {Neurons in dorsal anterior cingulate cortex signal postdecisional variables in a foraging task}, author = {T C Blanchard and B Y Hayden}, doi = {10.1523/JNEUROSCI.3151-13.2014}, year = {2014}, date = {2014-01-01}, journal = {The Journal of Neuroscience}, volume = {34}, number = {2}, pages = {646--655}, abstract = {The dorsal anterior cingulate cortex (dACC) is a key hub of the brain's executive control system. Although a great deal is known about its role in outcome monitoring and behavioral adjustment, whether and how it contributes to the decision process remain unclear. Some theories suggest that dACC neurons track decision variables (e.g., option values) that feed into choice processes and is thus "predecisional." Other theories suggest that dACC activity patterns differ qualitatively depending on the choice that is made and is thus "postdecisional." To compare these hypotheses, we examined responses of 124 dACC neurons in a simple foraging task in which monkeys accepted or rejected offers of delayed rewards. In this task, options that vary in benefit (reward size) and cost (delay) appear for 1 s; accepting the option provides the cued reward after the cued delay. To get at dACC neurons' contributions to decisions, we focused on responses around the time of choice, several seconds before the reward and the end of the trial. We found that dACC neurons signal the foregone value of the rejected option, a postdecisional variable. Neurons also signal the profitability (that is, the relative value) of the offer, but even these signals are qualitatively different on accept and reject decisions, meaning that they are also postdecisional. These results suggest that dACC can be placed late in the decision process and also support models that give it a regulatory role in decision, rather than serving as a site of comparison.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The dorsal anterior cingulate cortex (dACC) is a key hub of the brain's executive control system. Although a great deal is known about its role in outcome monitoring and behavioral adjustment, whether and how it contributes to the decision process remain unclear. Some theories suggest that dACC neurons track decision variables (e.g., option values) that feed into choice processes and is thus "predecisional." Other theories suggest that dACC activity patterns differ qualitatively depending on the choice that is made and is thus "postdecisional." To compare these hypotheses, we examined responses of 124 dACC neurons in a simple foraging task in which monkeys accepted or rejected offers of delayed rewards. In this task, options that vary in benefit (reward size) and cost (delay) appear for 1 s; accepting the option provides the cued reward after the cued delay. To get at dACC neurons' contributions to decisions, we focused on responses around the time of choice, several seconds before the reward and the end of the trial. We found that dACC neurons signal the foregone value of the rejected option, a postdecisional variable. Neurons also signal the profitability (that is, the relative value) of the offer, but even these signals are qualitatively different on accept and reject decisions, meaning that they are also postdecisional. These results suggest that dACC can be placed late in the decision process and also support models that give it a regulatory role in decision, rather than serving as a site of comparison. |
Tommy C Blanchard; Andreas Wilke; Benjamin Y Hayden Hot-hand bias in rhesus monkeys Journal Article Journal of Experimental Psychology: Animal Behavior Processes, 40 (3), pp. 280–286, 2014. @article{Blanchard2014a, title = {Hot-hand bias in rhesus monkeys}, author = {Tommy C Blanchard and Andreas Wilke and Benjamin Y Hayden}, doi = {10.1037/xan0000033}, year = {2014}, date = {2014-01-01}, journal = {Journal of Experimental Psychology: Animal Behavior Processes}, volume = {40}, number = {3}, pages = {280--286}, abstract = {Human decision-makers often exhibit the hot-hand phenomenon, a tendency to perceive positive serial autocorrelations in independent sequential events. The term is named after the observation that basketball fans and players tend to perceive streaks of high accuracy shooting when they are demonstrably absent. That is, both observing fans and participating players tend to hold the belief that a player's chance of hitting a shot are greater following a hit than following a miss. We hypothesize that this bias reflects a strong and stable tendency among primates (including humans) to perceive positive autocorrelations in temporal sequences, that this bias is an adaptation to clumpy foraging environments, and that it may even be ecologically rational. Several studies support this idea in humans, but a stronger test would be to determine whether nonhuman primates also exhibit a hot-hand bias. Here we report behavior of 3 monkeys performing a novel gambling task in which correlation between sequential gambles (i.e., temporal clumpiness) is systematically manipulated. We find that monkeys have better performance (meaning, more optimal behavior) for clumped (positively correlated) than for dispersed (negatively correlated) distributions. These results identify and quantify a new bias in monkeys' risky decisions, support accounts that specifically incorporate cognitive biases into risky choice, and support the suggestion that the hot-hand phenomenon is an evolutionary ancient bias.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Human decision-makers often exhibit the hot-hand phenomenon, a tendency to perceive positive serial autocorrelations in independent sequential events. The term is named after the observation that basketball fans and players tend to perceive streaks of high accuracy shooting when they are demonstrably absent. That is, both observing fans and participating players tend to hold the belief that a player's chance of hitting a shot are greater following a hit than following a miss. We hypothesize that this bias reflects a strong and stable tendency among primates (including humans) to perceive positive autocorrelations in temporal sequences, that this bias is an adaptation to clumpy foraging environments, and that it may even be ecologically rational. Several studies support this idea in humans, but a stronger test would be to determine whether nonhuman primates also exhibit a hot-hand bias. Here we report behavior of 3 monkeys performing a novel gambling task in which correlation between sequential gambles (i.e., temporal clumpiness) is systematically manipulated. We find that monkeys have better performance (meaning, more optimal behavior) for clumped (positively correlated) than for dispersed (negatively correlated) distributions. These results identify and quantify a new bias in monkeys' risky decisions, support accounts that specifically incorporate cognitive biases into risky choice, and support the suggestion that the hot-hand phenomenon is an evolutionary ancient bias. |
Tommy C Blanchard; Lauren S Wolfe; Ivo Vlaev; Joel S Winston; Benjamin Y Hayden Biases in preferences for sequences of outcomes in monkeys Journal Article Cognition, 130 (3), pp. 289–299, 2014. @article{Blanchard2014b, title = {Biases in preferences for sequences of outcomes in monkeys}, author = {Tommy C Blanchard and Lauren S Wolfe and Ivo Vlaev and Joel S Winston and Benjamin Y Hayden}, doi = {10.1016/j.cognition.2013.11.012}, year = {2014}, date = {2014-01-01}, journal = {Cognition}, volume = {130}, number = {3}, pages = {289--299}, publisher = {Elsevier B.V.}, abstract = {Movies, vacations, and meals are all examples of events composed of a sequence of smaller events. How do we go from our evaluations of each scene in a movie to an evaluation of the sequence as a whole$alpha$ In theory, we should simply average the values of the individual events. In practice, however, we are biased towards sequences where each element tends to be better than the previous, where the last value is large, and we overweight the best (or worst) part of the sequence. To study how general these biases are we examined monkeys' preferences for sequences of rewards in a novel reward repeat task. Monkeys were first given a sequence of rewards and then chose between repeating the sequence or receiving a standard comparator sequence. We found that, like humans, monkeys overweight events that happen later in a sequence, so much so that adding a small reward to the end of a sequence can paradoxically reduce its value. Monkeys were also biased towards sequences with large peak values (the highest value in the sequence), but only following a working memory challenge, suggesting that this preference may be driven by memory limitations. These results demonstrate the cross-species nature of biases in preferences for sequences of outcomes. In addition, monkeys' consistent preference for sequences in which large values occur later challenges the generality of discounting models of intertemporal choice in animals.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Movies, vacations, and meals are all examples of events composed of a sequence of smaller events. How do we go from our evaluations of each scene in a movie to an evaluation of the sequence as a whole$alpha$ In theory, we should simply average the values of the individual events. In practice, however, we are biased towards sequences where each element tends to be better than the previous, where the last value is large, and we overweight the best (or worst) part of the sequence. To study how general these biases are we examined monkeys' preferences for sequences of rewards in a novel reward repeat task. Monkeys were first given a sequence of rewards and then chose between repeating the sequence or receiving a standard comparator sequence. We found that, like humans, monkeys overweight events that happen later in a sequence, so much so that adding a small reward to the end of a sequence can paradoxically reduce its value. Monkeys were also biased towards sequences with large peak values (the highest value in the sequence), but only following a working memory challenge, suggesting that this preference may be driven by memory limitations. These results demonstrate the cross-species nature of biases in preferences for sequences of outcomes. In addition, monkeys' consistent preference for sequences in which large values occur later challenges the generality of discounting models of intertemporal choice in animals. |
Charles F Cadieu; Ha Hong; Daniel L K Yamins; Nicolas Pinto; Diego Ardila; Ethan A Solomon; Najib J Majaj; James J DiCarlo Deep neural networks rival the representation of primate IT cortex for core visual object recognition Journal Article PLoS Computational Biology, 10 (12), pp. 1–18, 2014. @article{Cadieu2014, title = {Deep neural networks rival the representation of primate IT cortex for core visual object recognition}, author = {Charles F Cadieu and Ha Hong and Daniel L K Yamins and Nicolas Pinto and Diego Ardila and Ethan A Solomon and Najib J Majaj and James J DiCarlo}, doi = {10.1016/j.apergo.2010.02.001}, year = {2014}, date = {2014-01-01}, journal = {PLoS Computational Biology}, volume = {10}, number = {12}, pages = {1--18}, abstract = {The primate visual system achieves remarkable visual object recognition performance even in brief presentations, and under changes to object exemplar, geometric transformations, and background variation (a.k.a. core visual object recognition). This remarkable performance is mediated by the representation formed in inferior temporal (IT) cortex. In parallel, recent advances in machine learning have led to ever higher performing models of object recognition using artificial deep neural networks (DNNs). It remains unclear, however, whether the representational performance of DNNs rivals that of the brain. To accurately produce such a comparison, a major difficulty has been a unifying metric that accounts for experimental limitations, such as the amount of noise, the number of neural recording sites, and the number of trials, and computational limitations, such as the complexity of the decoding classifier and the number of classifier training examples. In this work, we perform a direct comparison that corrects for these experimental limitations and computational considerations. As part of our methodology, we propose an extension of ‘‘kernel analysis'' that measures the generalization accuracy as a function of representational complexity. Our evaluations show that, unlike previous bio-inspired models, the latest DNNs rival the representational performance of IT cortex on this visual object recognition task. Furthermore, we show that models that perform well on measures of representational performance also perform well on measures of representational similarity to IT, and on measures of predicting individual IT multi-unit responses. Whether these DNNs rely on computational mechanisms similar to the primate visual system is yet to be determined, but, unlike all previous bio- inspired models, that possibility cannot be ruled out merely on representational performance grounds.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The primate visual system achieves remarkable visual object recognition performance even in brief presentations, and under changes to object exemplar, geometric transformations, and background variation (a.k.a. core visual object recognition). This remarkable performance is mediated by the representation formed in inferior temporal (IT) cortex. In parallel, recent advances in machine learning have led to ever higher performing models of object recognition using artificial deep neural networks (DNNs). It remains unclear, however, whether the representational performance of DNNs rivals that of the brain. To accurately produce such a comparison, a major difficulty has been a unifying metric that accounts for experimental limitations, such as the amount of noise, the number of neural recording sites, and the number of trials, and computational limitations, such as the complexity of the decoding classifier and the number of classifier training examples. In this work, we perform a direct comparison that corrects for these experimental limitations and computational considerations. As part of our methodology, we propose an extension of ‘‘kernel analysis'' that measures the generalization accuracy as a function of representational complexity. Our evaluations show that, unlike previous bio-inspired models, the latest DNNs rival the representational performance of IT cortex on this visual object recognition task. Furthermore, we show that models that perform well on measures of representational performance also perform well on measures of representational similarity to IT, and on measures of predicting individual IT multi-unit responses. Whether these DNNs rely on computational mechanisms similar to the primate visual system is yet to be determined, but, unlike all previous bio- inspired models, that possibility cannot be ruled out merely on representational performance grounds. |
Xinying Cai; Camillo Padoa-Schioppa Contributions of orbitofrontal and lateral prefrontal cortices to economic choice and the good-to-action transformation Journal Article Neuron, 81 (5), pp. 1140–1151, 2014. @article{Cai2014, title = {Contributions of orbitofrontal and lateral prefrontal cortices to economic choice and the good-to-action transformation}, author = {Xinying Cai and Camillo Padoa-Schioppa}, doi = {10.1016/j.neuron.2014.01.008}, year = {2014}, date = {2014-01-01}, journal = {Neuron}, volume = {81}, number = {5}, pages = {1140--1151}, publisher = {Elsevier Inc.}, abstract = {Previous work indicates that economic decisions can be made independently of the visuomotor contingencies of the choice task (space of goods). However, the neuronal mechanisms through which the choice outcome (the chosen good) is transformed into a suitable action plan remain poorly understood. Here we show that neurons in lateral prefrontal cortex reflect the early stages of this good-to-action transformation. Monkeys chose between different juices. The experimental design dissociated in space and time the presentation of the offers and the saccade targets associated with them. We recorded from the orbital, ventrolateral, and dorsolateral prefrontal cortices (OFC, LPFCv, and LPFCd, respectively). Prior to target presentation, neurons in both LPFCv and LPFCd encoded the choice outcome in goods space. After target presentation, they gradually came to encode the location of the targets and the upcoming action plan. Consistent with the anatomical connectivity, all spatial and action-related signals emerged in LPFCv before LPFCd.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Previous work indicates that economic decisions can be made independently of the visuomotor contingencies of the choice task (space of goods). However, the neuronal mechanisms through which the choice outcome (the chosen good) is transformed into a suitable action plan remain poorly understood. Here we show that neurons in lateral prefrontal cortex reflect the early stages of this good-to-action transformation. Monkeys chose between different juices. The experimental design dissociated in space and time the presentation of the offers and the saccade targets associated with them. We recorded from the orbital, ventrolateral, and dorsolateral prefrontal cortices (OFC, LPFCv, and LPFCd, respectively). Prior to target presentation, neurons in both LPFCv and LPFCd encoded the choice outcome in goods space. After target presentation, they gradually came to encode the location of the targets and the upcoming action plan. Consistent with the anatomical connectivity, all spatial and action-related signals emerged in LPFCv before LPFCd. |
Michael Colombo; James S Magnuson Eye movements reveal planning in humans: A comparison with Scarf and Colombo's (2009) monkeys Journal Article Journal of Experimental Psychology: Animal Learning and Cognition, 40 (2), pp. 178–184, 2014. @article{Colombo2014, title = {Eye movements reveal planning in humans: A comparison with Scarf and Colombo's (2009) monkeys}, author = {Michael Colombo and James S Magnuson}, doi = {10.1037/xan0000008}, year = {2014}, date = {2014-01-01}, journal = {Journal of Experimental Psychology: Animal Learning and Cognition}, volume = {40}, number = {2}, pages = {178--184}, abstract = {On sequential response tasks, a long pause preceding the first response is thought to reflect participants taking time to plan a sequence of responses. By tracking the eye movements of two monkeys (Macaca fascicularis), Scarf and Colombo (2009, Eye Movements During List Execution Reveal No Planning in Monkeys [Macaca fascicularis], Journal of Experimental Psychology: Animal Behavior Processes, Vol. 35, pp. 587–592) demonstrated that, at least with respect to monkeys, the long pause preceding the first response is not necessarily the product of planning. In the present experiment, we tracked the eye movements of adult humans using the paradigm employed by Scarf and Colombo and found that, in contrast to monkeys, the pause preceding the first item is indicative of planning in humans. These findings highlight the fact that similar response time profiles, displayed by human and nonhuman animals, do not necessarily reflect similar underlying cognitive operations.}, keywords = {}, pubstate = {published}, tppubtype = {article} } On sequential response tasks, a long pause preceding the first response is thought to reflect participants taking time to plan a sequence of responses. By tracking the eye movements of two monkeys (Macaca fascicularis), Scarf and Colombo (2009, Eye Movements During List Execution Reveal No Planning in Monkeys [Macaca fascicularis], Journal of Experimental Psychology: Animal Behavior Processes, Vol. 35, pp. 587–592) demonstrated that, at least with respect to monkeys, the long pause preceding the first response is not necessarily the product of planning. In the present experiment, we tracked the eye movements of adult humans using the paradigm employed by Scarf and Colombo and found that, in contrast to monkeys, the pause preceding the first item is indicative of planning in humans. These findings highlight the fact that similar response time profiles, displayed by human and nonhuman animals, do not necessarily reflect similar underlying cognitive operations. |
Becket R Ebitz; John M Pearson; Michael L Platt Pupil size and social vigilance in rhesus macaques Journal Article Frontiers in Neuroscience, 8 (8 MAY), pp. 1–13, 2014. @article{Ebitz2014, title = {Pupil size and social vigilance in rhesus macaques}, author = {Becket R Ebitz and John M Pearson and Michael L Platt}, doi = {10.3389/fnins.2014.00100}, year = {2014}, date = {2014-01-01}, journal = {Frontiers in Neuroscience}, volume = {8}, number = {8 MAY}, pages = {1--13}, abstract = {Complex natural environments favor the dynamic alignment of neural processing between goal-relevant stimuli and conflicting but biologically salient stimuli like social competitors or predators. The biological mechanisms that regulate dynamic changes in vigilance have not been fully elucidated. Arousal systems that ready the body to respond adaptively to threat may contribute to dynamic regulation of vigilance. Under conditions of constant luminance, pupil diameter provides a peripheral index of arousal state. Although pupil size varies with the processing of goal-relevant stimuli, it remains unclear whether pupil size also predicts attention to biologically salient objects and events like social competitors, whose presence interferes with current goals. Here we show that pupil size in rhesus macaques both reflects the biological salience of task-irrelevant social distractors and predicts vigilance for these stimuli. We measured pupil size in monkeys performing a visual orienting task in which distractors-monkey faces and phase-scrambled versions of the same images-could appear in a congruent, incongruent, or neutral position relative to a rewarded target. Baseline pupil size under constant illumination predicted distractor interference, consistent with the hypothesis that pupil-linked arousal mechanisms regulate task engagement and distractibility. Notably, pupil size also predicted enhanced vigilance for social distractors, suggesting that pupil-linked arousal may adjust the balance of processing resources between goal-relevant and biologically important stimuli. The magnitude of pupil constriction in response to distractors closely tracked distractor interference, saccade planning and the social relevance of distractors, endorsing the idea that the pupillary light response is modulated by attention. These findings indicate that pupil size indexes dynamic changes in attention evoked by both the social environment and arousal.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Complex natural environments favor the dynamic alignment of neural processing between goal-relevant stimuli and conflicting but biologically salient stimuli like social competitors or predators. The biological mechanisms that regulate dynamic changes in vigilance have not been fully elucidated. Arousal systems that ready the body to respond adaptively to threat may contribute to dynamic regulation of vigilance. Under conditions of constant luminance, pupil diameter provides a peripheral index of arousal state. Although pupil size varies with the processing of goal-relevant stimuli, it remains unclear whether pupil size also predicts attention to biologically salient objects and events like social competitors, whose presence interferes with current goals. Here we show that pupil size in rhesus macaques both reflects the biological salience of task-irrelevant social distractors and predicts vigilance for these stimuli. We measured pupil size in monkeys performing a visual orienting task in which distractors-monkey faces and phase-scrambled versions of the same images-could appear in a congruent, incongruent, or neutral position relative to a rewarded target. Baseline pupil size under constant illumination predicted distractor interference, consistent with the hypothesis that pupil-linked arousal mechanisms regulate task engagement and distractibility. Notably, pupil size also predicted enhanced vigilance for social distractors, suggesting that pupil-linked arousal may adjust the balance of processing resources between goal-relevant and biologically important stimuli. The magnitude of pupil constriction in response to distractors closely tracked distractor interference, saccade planning and the social relevance of distractors, endorsing the idea that the pupillary light response is modulated by attention. These findings indicate that pupil size indexes dynamic changes in attention evoked by both the social environment and arousal. |
David C Godlove; Alexander Maier; Geoffrey F Woodman; Jeffrey D Schall Microcircuitry of agranular frontal cortex: Testing the generality of the canonical cortical microcircuit Journal Article The Journal of Neuroscience, 34 (15), pp. 5355–5369, 2014. @article{Godlove2014, title = {Microcircuitry of agranular frontal cortex: Testing the generality of the canonical cortical microcircuit}, author = {David C Godlove and Alexander Maier and Geoffrey F Woodman and Jeffrey D Schall}, doi = {10.1523/JNEUROSCI.5127-13.2014}, year = {2014}, date = {2014-01-01}, journal = {The Journal of Neuroscience}, volume = {34}, number = {15}, pages = {5355--5369}, abstract = {We investigated whether a frontal area that lacks granular layer IV, supplementary eye field, exhibits features of laminar circuitry similar to those observed in primary sensory areas. We report, for the first time, visually evoked local field potentials (LFPs) and spiking activity recorded simultaneously across all layers of agranular frontal cortex using linear electrode arrays. We calculated current source density from the LFPs and compared the laminar organization of evolving sinks to those reported in sensory areas. Simultaneous, transient synaptic current sinks appeared first in layers III and V followed by more prolonged current sinks in layers I/II and VI. We also found no variation of single- or multi-unit visual response latency across layers, and putative pyramidal neurons and interneurons displayed similar response latencies. Many units exhibited pronounced discharge suppression that was strongest in superficial relative to deep layers. Maximum discharge suppression also occurred later in superficial than in deep layers. These results are discussed in the context of the canonical cortical microcircuit model originally formulated to describe early sensory cortex. The data indicate that agranular cortex resembles sensory areas in certain respects, but the cortical microcircuit is modified in nontrivial ways.}, keywords = {}, pubstate = {published}, tppubtype = {article} } We investigated whether a frontal area that lacks granular layer IV, supplementary eye field, exhibits features of laminar circuitry similar to those observed in primary sensory areas. We report, for the first time, visually evoked local field potentials (LFPs) and spiking activity recorded simultaneously across all layers of agranular frontal cortex using linear electrode arrays. We calculated current source density from the LFPs and compared the laminar organization of evolving sinks to those reported in sensory areas. Simultaneous, transient synaptic current sinks appeared first in layers III and V followed by more prolonged current sinks in layers I/II and VI. We also found no variation of single- or multi-unit visual response latency across layers, and putative pyramidal neurons and interneurons displayed similar response latencies. Many units exhibited pronounced discharge suppression that was strongest in superficial relative to deep layers. Maximum discharge suppression also occurred later in superficial than in deep layers. These results are discussed in the context of the canonical cortical microcircuit model originally formulated to describe early sensory cortex. The data indicate that agranular cortex resembles sensory areas in certain respects, but the cortical microcircuit is modified in nontrivial ways. |
Arnulf B A Graf; Richard A Andersen Inferring eye position from populations of lateral intraparietal neurons Journal Article eLife, 2014 (3), pp. 1–13, 2014. @article{Graf2014, title = {Inferring eye position from populations of lateral intraparietal neurons}, author = {Arnulf B A Graf and Richard A Andersen}, doi = {10.7554/eLife.02813}, year = {2014}, date = {2014-01-01}, journal = {eLife}, volume = {2014}, number = {3}, pages = {1--13}, abstract = {Understanding how the brain computes eye position is essential to unraveling high- level visual functions such as eye movement planning, coordinate transformations and stability of spatial awareness. The lateral intraparietal area (LIP) is essential for this process. However, despite decades of research, its contribution to the eye position signal remains controversial. LIP neurons have recently been reported to inaccurately represent eye position during a saccadic eye movement, and to be too slow to support a role in high-level visual functions. We addressed this issue by predicting eye position and saccade direction from the responses of populations of LIP neurons. We found that both signals were accurately predicted before, during and after a saccade. Also, the dynamics of these signals support their contribution to visual functions. These findings provide a principled understanding of the coding of information in populations of neurons within an important node of the cortical network for visual-motor behaviors.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Understanding how the brain computes eye position is essential to unraveling high- level visual functions such as eye movement planning, coordinate transformations and stability of spatial awareness. The lateral intraparietal area (LIP) is essential for this process. However, despite decades of research, its contribution to the eye position signal remains controversial. LIP neurons have recently been reported to inaccurately represent eye position during a saccadic eye movement, and to be too slow to support a role in high-level visual functions. We addressed this issue by predicting eye position and saccade direction from the responses of populations of LIP neurons. We found that both signals were accurately predicted before, during and after a saccade. Also, the dynamics of these signals support their contribution to visual functions. These findings provide a principled understanding of the coding of information in populations of neurons within an important node of the cortical network for visual-motor behaviors. |
Jianbo Xiao; Yu-Qiong Niu; Steven Wiesner; Xin Huang Normalization of neuronal responses in cortical area MT across signal strengths and motion directions Journal Article Journal of Neurophysiology, 112 (6), pp. 1291–1306, 2014. @article{Xiao2014, title = {Normalization of neuronal responses in cortical area MT across signal strengths and motion directions}, author = {Jianbo Xiao and Yu-Qiong Niu and Steven Wiesner and Xin Huang}, doi = {10.1152/jn.00700.2013}, year = {2014}, date = {2014-01-01}, journal = {Journal of Neurophysiology}, volume = {112}, number = {6}, pages = {1291--1306}, abstract = {Multiple visual stimuli are common in natural scenes, yet it remains unclear how multiple stimuli interact to influence neuronal responses. We investigated this question by manipulating relative signal strengths of two stimuli moving simultaneously within the receptive fields (RFs) of neurons in the extrastriate middle temporal (MT) cortex. Visual stimuli were overlapping random-dot patterns moving in two directions separated by 90°. We first varied the motion coherence of each random-dot pattern and characterized, across the direction tuning curve, the relationship between neuronal responses elicited by bidirectional stimuli and by the constituent motion components. The tuning curve for bidirectional stimuli showed response normalization and can be accounted for by a weighted sum of the responses to the motion components. Allowing nonlinear, multiplicative interaction between the two component responses significantly improved the data fit for some neurons, and the interaction mainly had a suppressive effect on the neuronal response. The weighting of the component responses was not fixed but dependent on relative signal strengths. When two stimulus components moved at different coherence levels, the response weight for the higher-coherence component was significantly greater than that for the lower-coherence component. We also varied relative luminance levels of two coherently moving stimuli and found that MT response weight for the higher-luminance component was also greater. These results suggest that competition between multiple stimuli within a neuron's RF depends on relative signal strengths of the stimuli and that multiplicative nonlinearity may play an important role in shaping the response tuning for multiple stimuli.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Multiple visual stimuli are common in natural scenes, yet it remains unclear how multiple stimuli interact to influence neuronal responses. We investigated this question by manipulating relative signal strengths of two stimuli moving simultaneously within the receptive fields (RFs) of neurons in the extrastriate middle temporal (MT) cortex. Visual stimuli were overlapping random-dot patterns moving in two directions separated by 90°. We first varied the motion coherence of each random-dot pattern and characterized, across the direction tuning curve, the relationship between neuronal responses elicited by bidirectional stimuli and by the constituent motion components. The tuning curve for bidirectional stimuli showed response normalization and can be accounted for by a weighted sum of the responses to the motion components. Allowing nonlinear, multiplicative interaction between the two component responses significantly improved the data fit for some neurons, and the interaction mainly had a suppressive effect on the neuronal response. The weighting of the component responses was not fixed but dependent on relative signal strengths. When two stimulus components moved at different coherence levels, the response weight for the higher-coherence component was significantly greater than that for the lower-coherence component. We also varied relative luminance levels of two coherently moving stimuli and found that MT response weight for the higher-luminance component was also greater. These results suggest that competition between multiple stimuli within a neuron's RF depends on relative signal strengths of the stimuli and that multiplicative nonlinearity may play an important role in shaping the response tuning for multiple stimuli. |
Daniel L K Yamins; Ha Hong; Charles F Cadieu; Ethan A Solomon; Darren Seibert; James J DiCarlo Estimating international migration on the base of small area techniques Journal Article Proceedings of the National Academy of Sciences, 111 (23), pp. 8619–8624, 2014. @article{Yamins2014, title = {Estimating international migration on the base of small area techniques}, author = {Daniel L K Yamins and Ha Hong and Charles F Cadieu and Ethan A Solomon and Darren Seibert and James J DiCarlo}, doi = {10.1073/pnas.1403112111}, year = {2014}, date = {2014-01-01}, journal = {Proceedings of the National Academy of Sciences}, volume = {111}, number = {23}, pages = {8619--8624}, abstract = {The ventral visual stream underlies key human visual object recognition abilities. However, neural encoding in the higher areas of the ventral stream remains poorly understood. Here, we describe a modeling approach that yields a quantitatively accurate model of inferior temporal (IT) cortex, the highest ventral cortical area. Using high-throughput computational techniques, we discovered that, within a class of biologically plausible hierarchical neural network models, there is a strong correlation between a model's categorization performance and its ability to predict individual IT neural unit response data. To pursue this idea, we then identified a high-performing neural network that matches human performance on a range of recognition tasks. Critically, even though we did not constrain this model to match neural data, its top output layer turns out to be highly predictive of IT spiking responses to complex naturalistic images at both the single site and population levels. Moreover, the model's intermediate layers are highly predictive of neural responses in the V4 cortex, a midlevel visual area that provides the dominant cortical input to IT. These results show that performance optimization--applied in a biologically appropriate model class--can be used to build quantitative predictive models of neural processing.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The ventral visual stream underlies key human visual object recognition abilities. However, neural encoding in the higher areas of the ventral stream remains poorly understood. Here, we describe a modeling approach that yields a quantitatively accurate model of inferior temporal (IT) cortex, the highest ventral cortical area. Using high-throughput computational techniques, we discovered that, within a class of biologically plausible hierarchical neural network models, there is a strong correlation between a model's categorization performance and its ability to predict individual IT neural unit response data. To pursue this idea, we then identified a high-performing neural network that matches human performance on a range of recognition tasks. Critically, even though we did not constrain this model to match neural data, its top output layer turns out to be highly predictive of IT spiking responses to complex naturalistic images at both the single site and population levels. Moreover, the model's intermediate layers are highly predictive of neural responses in the V4 cortex, a midlevel visual area that provides the dominant cortical input to IT. These results show that performance optimization--applied in a biologically appropriate model class--can be used to build quantitative predictive models of neural processing. |
Chin-An Wang; Douglas P Munoz Modulation of stimulus contrast on the human pupil orienting response Journal Article European Journal of Neuroscience, 40 (5), pp. 2822–2832, 2014. @article{Wang2014g, title = {Modulation of stimulus contrast on the human pupil orienting response}, author = {Chin-An Wang and Douglas P Munoz}, doi = {10.1111/ejn.12641}, year = {2014}, date = {2014-01-01}, journal = {European Journal of Neuroscience}, volume = {40}, number = {5}, pages = {2822--2832}, abstract = {The sudden appearance of a novel stimulus initiates a series of responses to orient the body for appropriate actions, including not only shifts of gaze and attention, but also transient pupil dilation. Modulation of pupil dynamics by stimulus properties is less understood, although its effects on other components of orienting have been extensively explored. Microstimulation of the superior colliculus evoked transient pupil dilation, and the initial component of pupil dilation evoked by microstimulation was similar to that elicited by the presentation of salient sensory stimuli, suggesting a coordinated role of the superior colliculus on this behavior, although evidence in humans is yet to be established. To examine pupil orienting responses in humans, we presented visual stimuli while participants fixated on a central visual spot. Transient pupil dilation in humans was elicited after presentation of a visual stimulus in the periphery. The evoked pupil responses were modulated systematically by stimulus contrast, with faster and larger pupil responses triggered by higher contrast stimuli. The pupil response onset latencies for high contrast stimuli were similar to those produced by the light reflex and significantly faster than the darkness reflex, suggesting that the initial component of pupil dilation is probably mediated by inhibition of the parasympathetic pathway. The contrast modulation was pronounced under different levels of baseline pupil size. Together, our results demonstrate visual contrast modulation on the orienting pupil response in humans.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The sudden appearance of a novel stimulus initiates a series of responses to orient the body for appropriate actions, including not only shifts of gaze and attention, but also transient pupil dilation. Modulation of pupil dynamics by stimulus properties is less understood, although its effects on other components of orienting have been extensively explored. Microstimulation of the superior colliculus evoked transient pupil dilation, and the initial component of pupil dilation evoked by microstimulation was similar to that elicited by the presentation of salient sensory stimuli, suggesting a coordinated role of the superior colliculus on this behavior, although evidence in humans is yet to be established. To examine pupil orienting responses in humans, we presented visual stimuli while participants fixated on a central visual spot. Transient pupil dilation in humans was elicited after presentation of a visual stimulus in the periphery. The evoked pupil responses were modulated systematically by stimulus contrast, with faster and larger pupil responses triggered by higher contrast stimuli. The pupil response onset latencies for high contrast stimuli were similar to those produced by the light reflex and significantly faster than the darkness reflex, suggesting that the initial component of pupil dilation is probably mediated by inhibition of the parasympathetic pathway. The contrast modulation was pronounced under different levels of baseline pupil size. Together, our results demonstrate visual contrast modulation on the orienting pupil response in humans. |
Guilhem Ibos; David J Freedman Dynamic integration of task-relevant visual features in posterior parietal cortex Journal Article Neuron, 83 (6), pp. 1468–1480, 2014. @article{Ibos2014, title = {Dynamic integration of task-relevant visual features in posterior parietal cortex}, author = {Guilhem Ibos and David J Freedman}, doi = {10.1016/j.neuron.2014.08.020}, year = {2014}, date = {2014-01-01}, journal = {Neuron}, volume = {83}, number = {6}, pages = {1468--1480}, publisher = {83}, abstract = {The primate visual system consists of multiple hierarchically organized cortical areas, each specialized for processing distinct aspects of the visual scene. For example, color and form are encoded in ventralpathway areas such as V4 and inferior temporal cortex, while motion is preferentially processed in dorsal pathway areas such as the middletemporal area. Such representations often need to be integrated perceptually to solve tasks that depend on multiple features. We tested the hypothesis that the lateral intraparietal area (LIP) integrates disparate task-relevant visual features by recording from LIP neurons in monkeys trained to identify target stimuli composed of conjunctionsof color and motion features. We show that LIP neurons exhibit integrative representations of both color and motion features when they are taskrelevant and task-dependent shifts of both direction and color tuning. This suggests that LIP plays a role in flexibly integrating task-relevant sensory signals.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The primate visual system consists of multiple hierarchically organized cortical areas, each specialized for processing distinct aspects of the visual scene. For example, color and form are encoded in ventralpathway areas such as V4 and inferior temporal cortex, while motion is preferentially processed in dorsal pathway areas such as the middletemporal area. Such representations often need to be integrated perceptually to solve tasks that depend on multiple features. We tested the hypothesis that the lateral intraparietal area (LIP) integrates disparate task-relevant visual features by recording from LIP neurons in monkeys trained to identify target stimuli composed of conjunctionsof color and motion features. We show that LIP neurons exhibit integrative representations of both color and motion features when they are taskrelevant and task-dependent shifts of both direction and color tuning. This suggests that LIP plays a role in flexibly integrating task-relevant sensory signals. |
Kevin Johnston; Michael J Koval; Stephen G Lomber; Stefan Everling Macaque dorsolateral prefrontal cortex does not suppress saccade-related activity in the superior colliculus Journal Article Cerebral Cortex, 24 (5), pp. 1373–1388, 2014. @article{Johnston2014, title = {Macaque dorsolateral prefrontal cortex does not suppress saccade-related activity in the superior colliculus}, author = {Kevin Johnston and Michael J Koval and Stephen G Lomber and Stefan Everling}, doi = {10.1093/cercor/bhs424}, year = {2014}, date = {2014-01-01}, journal = {Cerebral Cortex}, volume = {24}, number = {5}, pages = {1373--1388}, abstract = {Of the many functions ascribed to the dorsolateral prefrontal cortex (DLPFC), the ability to override automatic stimulus-driven behavior is one of the most prominent. This ability has been investigated extensively with the antisaccade task, which requires suppression of saccades toward suddenly appearing visual stimuli. Convergent lines of evidence have supported a model in which the DLPFC suppresses unwanted saccades by inhibiting saccade-related activity in the ipsilateral superior colliculus (SC), a midbrain oculomotor structure. Here, we carried out a direct test of this inhibitory model using unilateral cryogenic deactivation of the DLPFC within the caudal principal sulcus (cPS) and simultaneous single-neuron recording of SC saccade-related neurons in monkeys performing saccades and antisaccades. Contrary to the inhibition model, which predicts that attenuation of inhibition effected by unilateral cPS deactivation should result in activity increases in ipsilateral and decreases in contralateral SC, we observed a delayed onset of saccade-related activity in the ipsilateral SC, and activity increases in the contralateral SC. These effects were mirrored by increased error rates of ipsiversive antisaccades, and reaction times of contraversive saccades. These data challenge the inhibitory model and suggest instead that the primary influence of the DLPFC on the SC is excitatory.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Of the many functions ascribed to the dorsolateral prefrontal cortex (DLPFC), the ability to override automatic stimulus-driven behavior is one of the most prominent. This ability has been investigated extensively with the antisaccade task, which requires suppression of saccades toward suddenly appearing visual stimuli. Convergent lines of evidence have supported a model in which the DLPFC suppresses unwanted saccades by inhibiting saccade-related activity in the ipsilateral superior colliculus (SC), a midbrain oculomotor structure. Here, we carried out a direct test of this inhibitory model using unilateral cryogenic deactivation of the DLPFC within the caudal principal sulcus (cPS) and simultaneous single-neuron recording of SC saccade-related neurons in monkeys performing saccades and antisaccades. Contrary to the inhibition model, which predicts that attenuation of inhibition effected by unilateral cPS deactivation should result in activity increases in ipsilateral and decreases in contralateral SC, we observed a delayed onset of saccade-related activity in the ipsilateral SC, and activity increases in the contralateral SC. These effects were mirrored by increased error rates of ipsiversive antisaccades, and reaction times of contraversive saccades. These data challenge the inhibitory model and suggest instead that the primary influence of the DLPFC on the SC is excitatory. |
R M Kalwani; S Joshi; J I Gold Phasic activation of individual neurons in the locus ceruleus/subceruleus complex of monkeys reflects rewarded decisions to go but not stop Journal Article The Journal of Neuroscience, 34 (41), pp. 13656–13669, 2014. @article{Kalwani2014, title = {Phasic activation of individual neurons in the locus ceruleus/subceruleus complex of monkeys reflects rewarded decisions to go but not stop}, author = {R M Kalwani and S Joshi and J I Gold}, doi = {10.1523/JNEUROSCI.2566-14.2014}, year = {2014}, date = {2014-01-01}, journal = {The Journal of Neuroscience}, volume = {34}, number = {41}, pages = {13656--13669}, abstract = {Neurons in the brainstem nucleus locus ceruleus (LC) often exhibit phasic activation in the context of simple sensory-motor tasks. The functional role of this activation, which leads to the release of norepinephrine throughout the brain, is not yet understood in part because the conditions under which it occurs remain in question. Early studies focused on the relationship of LC phasic activation to salient sensory events, whereas more recent work has emphasized its timing relative to goal-directed behavioral responses, possibly representing the end of a sensory-motor decision process. To better understand the relationship between LC phasic activation and sensory, motor, and decision processing, we recorded spiking activity of neurons in the LC+ (LC and the adjacent, norepinephrine-containing subceruleus nucleus) of monkeys performing a countermanding task. The task required the monkeys to occasionally withhold planned, saccadic eye movements to a visual target. We found that many well isolated LC+ units responded to both the onset of the visual cue instructing the monkey to initiate the saccade and again after saccade onset, even when it was initiated erroneously in the presence of a stop signal. Many of these neurons did not respond to saccades made outside of the task context. In contrast, neither the appearance of the stop signal nor the successful withholding of the saccade elicited an LC+ response. Therefore, LC+ phasic activation encodes sensory and motor events related to decisions to execute, but not withhold, movements, implying a functional role in goal-directed actions, but not necessarily more covert forms of processing.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Neurons in the brainstem nucleus locus ceruleus (LC) often exhibit phasic activation in the context of simple sensory-motor tasks. The functional role of this activation, which leads to the release of norepinephrine throughout the brain, is not yet understood in part because the conditions under which it occurs remain in question. Early studies focused on the relationship of LC phasic activation to salient sensory events, whereas more recent work has emphasized its timing relative to goal-directed behavioral responses, possibly representing the end of a sensory-motor decision process. To better understand the relationship between LC phasic activation and sensory, motor, and decision processing, we recorded spiking activity of neurons in the LC+ (LC and the adjacent, norepinephrine-containing subceruleus nucleus) of monkeys performing a countermanding task. The task required the monkeys to occasionally withhold planned, saccadic eye movements to a visual target. We found that many well isolated LC+ units responded to both the onset of the visual cue instructing the monkey to initiate the saccade and again after saccade onset, even when it was initiated erroneously in the presence of a stop signal. Many of these neurons did not respond to saccades made outside of the task context. In contrast, neither the appearance of the stop signal nor the successful withholding of the saccade elicited an LC+ response. Therefore, LC+ phasic activation encodes sensory and motor events related to decisions to execute, but not withhold, movements, implying a functional role in goal-directed actions, but not necessarily more covert forms of processing. |
Yoshito Kosai; Yasmine El-shamayleh; Amber M Fyall; Anitha Pasupathy The role of visual area V4 in the discrimination of partially occluded shapes Journal Article The Journal of Neuroscience, 34 (25), pp. 8570–8584, 2014. @article{Kosai2014, title = {The role of visual area V4 in the discrimination of partially occluded shapes}, author = {Yoshito Kosai and Yasmine El-shamayleh and Amber M Fyall and Anitha Pasupathy}, doi = {10.1523/JNEUROSCI.1375-14.2014}, year = {2014}, date = {2014-01-01}, journal = {The Journal of Neuroscience}, volume = {34}, number = {25}, pages = {8570--8584}, abstract = {The primate brain successfully recognizes objects, even when they are partially occluded. To begin to elucidate the neural substrates of this perceptual capacity, we measured the responses of shape-selective neurons in visual area V4 while monkeys discriminated pairs of shapes under varying degrees of occlusion. We found that neuronal shape selectivity always decreased with increasing occlusion level, with some neurons being notably more robust to occlusion than others. The responses of neurons that maintained their selectivity across a wider range of occlusion levels were often sufficiently sensitive to support behavioral performance. Many of these same neurons were distinctively selective for the curvature of local boundary features and their shape tuning was well fit by a model of boundary curvature (curvature-tuned neurons). A significant subset of V4 neurons also signaled the animal's upcoming behavioral choices; these decision signals had short onset latencies that emerged progressively later for higher occlusion levels. The time course of the decision signals in V4 paralleled that of shape selectivity in curvature-tuned neurons: shape selectivity in curvature-tuned neurons, but not others, emerged earlier than the decision signals. These findings provide evidence for the involvement of contour-based mechanisms in the segmentation and recognition of partially occluded objects, consistent with psychophysical theory. Furthermore, they suggest that area V4 participates in the representation of the relevant sensory signals and the generation of decision signals underlying discrimination.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The primate brain successfully recognizes objects, even when they are partially occluded. To begin to elucidate the neural substrates of this perceptual capacity, we measured the responses of shape-selective neurons in visual area V4 while monkeys discriminated pairs of shapes under varying degrees of occlusion. We found that neuronal shape selectivity always decreased with increasing occlusion level, with some neurons being notably more robust to occlusion than others. The responses of neurons that maintained their selectivity across a wider range of occlusion levels were often sufficiently sensitive to support behavioral performance. Many of these same neurons were distinctively selective for the curvature of local boundary features and their shape tuning was well fit by a model of boundary curvature (curvature-tuned neurons). A significant subset of V4 neurons also signaled the animal's upcoming behavioral choices; these decision signals had short onset latencies that emerged progressively later for higher occlusion levels. The time course of the decision signals in V4 paralleled that of shape selectivity in curvature-tuned neurons: shape selectivity in curvature-tuned neurons, but not others, emerged earlier than the decision signals. These findings provide evidence for the involvement of contour-based mechanisms in the segmentation and recognition of partially occluded objects, consistent with psychophysical theory. Furthermore, they suggest that area V4 participates in the representation of the relevant sensory signals and the generation of decision signals underlying discrimination. |
Michael J Koval; Matthew R Hutchison; Stephen G Lomber; Stefan Everling Effects of unilateral deactivations of dorsolateral prefrontal cortex and anterior cingulate cortex on saccadic eye movements Journal Article Journal of Neurophysiology, 111 (4), pp. 787–803, 2014. @article{Koval2014, title = {Effects of unilateral deactivations of dorsolateral prefrontal cortex and anterior cingulate cortex on saccadic eye movements}, author = {Michael J Koval and Matthew R Hutchison and Stephen G Lomber and Stefan Everling}, doi = {10.1152/jn.00626.2013}, year = {2014}, date = {2014-01-01}, journal = {Journal of Neurophysiology}, volume = {111}, number = {4}, pages = {787--803}, abstract = {The dorsolateral prefrontal cortex (dlPFC) and anterior cingulate cortex (ACC) have both been implicated in the cognitive control of saccadic eye movements by single neuron recording studies in nonhuman primates and functional imaging studies in humans, but their relative roles remain unclear. Here, we reversibly deactivated either dlPFC or ACC subregions in macaque monkeys while the animals performed randomly interleaved pro- and antisaccades. In addition, we explored the whole-brain functional connectivity of these two regions by applying a seed-based resting-state functional MRI analysis in a separate cohort of monkeys. We found that unilateral dlPFC deactivation had stronger behavioral effects on saccades than unilateral ACC deactivation, and that the dlPFC displayed stronger functional connectivity with frontoparietal areas than the ACC. We suggest that the dlPFC plays a more prominent role in the preparation of pro- and antisaccades than the ACC.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The dorsolateral prefrontal cortex (dlPFC) and anterior cingulate cortex (ACC) have both been implicated in the cognitive control of saccadic eye movements by single neuron recording studies in nonhuman primates and functional imaging studies in humans, but their relative roles remain unclear. Here, we reversibly deactivated either dlPFC or ACC subregions in macaque monkeys while the animals performed randomly interleaved pro- and antisaccades. In addition, we explored the whole-brain functional connectivity of these two regions by applying a seed-based resting-state functional MRI analysis in a separate cohort of monkeys. We found that unilateral dlPFC deactivation had stronger behavioral effects on saccades than unilateral ACC deactivation, and that the dlPFC displayed stronger functional connectivity with frontoparietal areas than the ACC. We suggest that the dlPFC plays a more prominent role in the preparation of pro- and antisaccades than the ACC. |
Jens Kremkow; Jianzhong Jin; Stanley J Komban; Yushi Wang; Reza Lashgari; Xiaobing Li; Michael Jansen; Qasim Zaidi; Jose-Manuel Alonso Neuronal nonlinearity explains greater visual spatial resolution for darks than lights Journal Article Proceedings of the National Academy of Sciences, 111 (8), pp. 3170–3175, 2014. @article{Kremkow2014, title = {Neuronal nonlinearity explains greater visual spatial resolution for darks than lights}, author = {Jens Kremkow and Jianzhong Jin and Stanley J Komban and Yushi Wang and Reza Lashgari and Xiaobing Li and Michael Jansen and Qasim Zaidi and Jose-Manuel Alonso}, doi = {10.1073/pnas.1310442111}, year = {2014}, date = {2014-01-01}, journal = {Proceedings of the National Academy of Sciences}, volume = {111}, number = {8}, pages = {3170--3175}, abstract = {Astronomers and physicists noticed centuries ago that visual spatial resolution is higher for dark than light stimuli, but the neuronal mechanisms for this perceptual asymmetry remain unknown. Here we demonstrate that the asymmetry is caused by a neuronal nonlinearity in the early visual pathway. We show that neurons driven by darks (OFF neurons) increase their responses roughly linearly with luminance decrements, independent of the background luminance. However, neurons driven by lights (ON neurons) saturate their responses with small increases in luminance and need bright backgrounds to approach the linearity of OFF neurons. We show that, as a consequence of this difference in linearity, receptive fields are larger in ON than OFF thalamic neurons, and cortical neurons are more strongly driven by darks than lights at low spatial frequencies. This ON/OFF asymmetry in linearity could be demonstrated in the visual cortex of cats, monkeys, and humans and in the cat visual thalamus. Furthermore, in the cat visual thalamus, we show that the neuronal nonlinearity is present at the ON receptive field center of ON-center neurons and ON receptive field surround of OFF-center neurons, suggesting an origin at the level of the photoreceptor. These results demonstrate a fundamental difference in visual processing between ON and OFF channels and reveal a competitive advantage for OFF neurons over ON neurons at low spatial frequencies, which could be important during cortical development when retinal images are blurred by immature optics in infant eyes.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Astronomers and physicists noticed centuries ago that visual spatial resolution is higher for dark than light stimuli, but the neuronal mechanisms for this perceptual asymmetry remain unknown. Here we demonstrate that the asymmetry is caused by a neuronal nonlinearity in the early visual pathway. We show that neurons driven by darks (OFF neurons) increase their responses roughly linearly with luminance decrements, independent of the background luminance. However, neurons driven by lights (ON neurons) saturate their responses with small increases in luminance and need bright backgrounds to approach the linearity of OFF neurons. We show that, as a consequence of this difference in linearity, receptive fields are larger in ON than OFF thalamic neurons, and cortical neurons are more strongly driven by darks than lights at low spatial frequencies. This ON/OFF asymmetry in linearity could be demonstrated in the visual cortex of cats, monkeys, and humans and in the cat visual thalamus. Furthermore, in the cat visual thalamus, we show that the neuronal nonlinearity is present at the ON receptive field center of ON-center neurons and ON receptive field surround of OFF-center neurons, suggesting an origin at the level of the photoreceptor. These results demonstrate a fundamental difference in visual processing between ON and OFF channels and reveal a competitive advantage for OFF neurons over ON neurons at low spatial frequencies, which could be important during cortical development when retinal images are blurred by immature optics in infant eyes. |
Rogier Landman; Jitendra Sharma; Mriganka Sur; Robert Desimone Effect of distracting faces on visual selective attention in the monkey Journal Article Proceedings of the National Academy of Sciences, 111 (50), pp. 18037–18042, 2014. @article{Landman2014, title = {Effect of distracting faces on visual selective attention in the monkey}, author = {Rogier Landman and Jitendra Sharma and Mriganka Sur and Robert Desimone}, doi = {10.1073/pnas.1420167111}, year = {2014}, date = {2014-01-01}, journal = {Proceedings of the National Academy of Sciences}, volume = {111}, number = {50}, pages = {18037--18042}, abstract = {In primates, visual stimuli with social and emotional content tend to attract attention. Attention might be captured through rapid, automatic, subcortical processing or guided by slower, more voluntary cortical processing. Here we examined whether irrelevant faces with varied emotional expressions interfere with a covert attention task in macaque monkeys. In the task, the monkeys monitored a target grating in the periphery for a subtle color change while ignoring distracters that included faces appearing elsewhere on the screen. The onset time of distracter faces before the target change, as well as their spatial proximity to the target, was varied from trial to trial. The presence of faces, especially faces with emotional expressions interfered with the task, indicating a competition for attentional resources between the task and the face stimuli. However, this interference was significant only when faces were presented for greater than 200 ms. Emotional faces also affected saccade velocity and reduced pupillary reflex. Our results indicate that the attraction of attention by emotional faces in the monkey takes a considerable amount of processing time, possibly involving cortical–subcortical interactions. Intranasal application of the hormone oxytocin ameliorated the interfering effects of faces. Together these results provide evidence for slow modulation of attention by emotional distracters, which likely involves oxytocinergic brain circuits.}, keywords = {}, pubstate = {published}, tppubtype = {article} } In primates, visual stimuli with social and emotional content tend to attract attention. Attention might be captured through rapid, automatic, subcortical processing or guided by slower, more voluntary cortical processing. Here we examined whether irrelevant faces with varied emotional expressions interfere with a covert attention task in macaque monkeys. In the task, the monkeys monitored a target grating in the periphery for a subtle color change while ignoring distracters that included faces appearing elsewhere on the screen. The onset time of distracter faces before the target change, as well as their spatial proximity to the target, was varied from trial to trial. The presence of faces, especially faces with emotional expressions interfered with the task, indicating a competition for attentional resources between the task and the face stimuli. However, this interference was significant only when faces were presented for greater than 200 ms. Emotional faces also affected saccade velocity and reduced pupillary reflex. Our results indicate that the attraction of attention by emotional faces in the monkey takes a considerable amount of processing time, possibly involving cortical–subcortical interactions. Intranasal application of the hormone oxytocin ameliorated the interfering effects of faces. Together these results provide evidence for slow modulation of attention by emotional distracters, which likely involves oxytocinergic brain circuits. |
David B T McMahon; Igor V Bondar; Olusoji A T Afuwape; David C Ide; David A Leopold One month in the life of a neuron: longitudinal single-unit electrophysiology in the monkey visual system Journal Article Journal of Neurophysiology, 112 (7), pp. 1748–1762, 2014. @article{McMahon2014, title = {One month in the life of a neuron: longitudinal single-unit electrophysiology in the monkey visual system}, author = {David B T McMahon and Igor V Bondar and Olusoji A T Afuwape and David C Ide and David A Leopold}, doi = {10.1152/jn.00052.2014}, year = {2014}, date = {2014-01-01}, journal = {Journal of Neurophysiology}, volume = {112}, number = {7}, pages = {1748--1762}, abstract = {Conventional recording methods generally preclude following the activity of the same neurons in awake animals across days. This limits our ability to systematically investigate the principles of neuronal specialization, or to study phenomena that evolve over multiple days such as experience-dependent plasticity. To redress this shortcoming, we developed a drivable, chronically implanted microwire recording preparation that allowed us to follow visual responses in inferotemporal (IT) cortex in awake behaving monkeys across multiple days, and in many cases across months. The microwire bundle and other implanted components were MRI compatible and thus permitted in the same animals both functional imaging and long-term recording from multiple neurons in deep structures within a region the approximate size of one voxel (textless1 mm). The distinct patterns of stimulus selectivity observed in IT neurons, together with stable features in spike waveforms and interspike interval distributions, allowed us to track individual neurons across weeks and sometimes months. The long-term consistency of visual responses shown here permits large-scale mappings of neuronal properties using massive image libraries presented over the course of days. We demonstrate this possibility by screening the visual responses of single neurons to a set of 10,000 stimuli.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Conventional recording methods generally preclude following the activity of the same neurons in awake animals across days. This limits our ability to systematically investigate the principles of neuronal specialization, or to study phenomena that evolve over multiple days such as experience-dependent plasticity. To redress this shortcoming, we developed a drivable, chronically implanted microwire recording preparation that allowed us to follow visual responses in inferotemporal (IT) cortex in awake behaving monkeys across multiple days, and in many cases across months. The microwire bundle and other implanted components were MRI compatible and thus permitted in the same animals both functional imaging and long-term recording from multiple neurons in deep structures within a region the approximate size of one voxel (textless1 mm). The distinct patterns of stimulus selectivity observed in IT neurons, together with stable features in spike waveforms and interspike interval distributions, allowed us to track individual neurons across weeks and sometimes months. The long-term consistency of visual responses shown here permits large-scale mappings of neuronal properties using massive image libraries presented over the course of days. We demonstrate this possibility by screening the visual responses of single neurons to a set of 10,000 stimuli. |
David B T McMahon; Adam P Jones; Igor V Bondar; David A Leopold Face-selective neurons maintain consistent visual responses across months Journal Article Proceedings of the National Academy of Sciences, 111 (22), pp. 8251–8256, 2014. @article{McMahon2014a, title = {Face-selective neurons maintain consistent visual responses across months}, author = {David B T McMahon and Adam P Jones and Igor V Bondar and David A Leopold}, doi = {10.1073/pnas.1318331111}, year = {2014}, date = {2014-01-01}, journal = {Proceedings of the National Academy of Sciences}, volume = {111}, number = {22}, pages = {8251--8256}, abstract = {Face perception in both humans and monkeys is thought to depend on neurons clustered in discrete, specialized brain regions. Because primates are frequently called upon to recognize and remember new individuals, the neuronal representation of faces in the brain might be expected to change over time. The functional properties of neurons in behaving animals are typically assessed over time periods ranging from minutes to hours, which amounts to a snapshot compared to a lifespan of a neuron. It therefore remains unclear how neuronal properties observed on a given day predict that same neuron's activity months or years later. Here we show that the macaque inferotemporal cortex contains face-selective cells that show virtually no change in their patterns of visual responses over time periods as long as one year. Using chronically implanted microwire electrodes guided by functional MRI targeting, we obtained distinct profiles of selectivity for face and nonface stimuli that served as fingerprints for individual neurons in the anterior fundus (AF) face patch within the superior temporal sulcus. Longitudinal tracking over a series of daily recording sessions revealed that face-selective neurons maintain consistent visual response profiles across months-long time spans despite the influence of ongoing daily experience. We propose that neurons in the AF face patch are specialized for aspects of face perception that demand stability as opposed to plasticity.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Face perception in both humans and monkeys is thought to depend on neurons clustered in discrete, specialized brain regions. Because primates are frequently called upon to recognize and remember new individuals, the neuronal representation of faces in the brain might be expected to change over time. The functional properties of neurons in behaving animals are typically assessed over time periods ranging from minutes to hours, which amounts to a snapshot compared to a lifespan of a neuron. It therefore remains unclear how neuronal properties observed on a given day predict that same neuron's activity months or years later. Here we show that the macaque inferotemporal cortex contains face-selective cells that show virtually no change in their patterns of visual responses over time periods as long as one year. Using chronically implanted microwire electrodes guided by functional MRI targeting, we obtained distinct profiles of selectivity for face and nonface stimuli that served as fingerprints for individual neurons in the anterior fundus (AF) face patch within the superior temporal sulcus. Longitudinal tracking over a series of daily recording sessions revealed that face-selective neurons maintain consistent visual response profiles across months-long time spans despite the influence of ongoing daily experience. We propose that neurons in the AF face patch are specialized for aspects of face perception that demand stability as opposed to plasticity. |
David Méary; Zhihan Li; Wu Li; Kun Guo; Olivier Pascalis Seeing two faces together: Preference formation in humans and rhesus macaques Journal Article Animal Cognition, 17 (5), pp. 1107–1119, 2014. @article{Meary2014, title = {Seeing two faces together: Preference formation in humans and rhesus macaques}, author = {David Méary and Zhihan Li and Wu Li and Kun Guo and Olivier Pascalis}, doi = {10.1007/s10071-014-0742-3}, year = {2014}, date = {2014-01-01}, journal = {Animal Cognition}, volume = {17}, number = {5}, pages = {1107--1119}, abstract = {Humans, great apes and old world monkeys show selective attention to faces depending on conspecificity, familiarity, and social status supporting the view that primates share similar face processing mechanisms. Although many studies have been done on face scanning strategy in monkeys and humans, the mechanisms influencing viewing preference have received little attention. To determine how face categories influence viewing preference in humans and rhesus macaques (Macaca mulatta), we performed two eye-tracking experiments using a visual preference task whereby pairs of faces from different species were presented simultaneously. The results indicated that viewing time was significantly influenced by the pairing of the face categories. Humans showed a strong bias towards an own-race face in an Asian-Caucasian condition. Rhesus macaques directed more attention towards non-human primate faces when they were paired with human faces, regardless of the species. When rhesus faces were paired with faces from Barbary macaques (Macaca sylvanus) or chimpanzees (Pan troglodytes), the novel species' faces attracted more attention. These results indicate that monkeys' viewing preferences, as assessed by a visual preference task, are modulated by several factors, species and dominance being the most influential.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Humans, great apes and old world monkeys show selective attention to faces depending on conspecificity, familiarity, and social status supporting the view that primates share similar face processing mechanisms. Although many studies have been done on face scanning strategy in monkeys and humans, the mechanisms influencing viewing preference have received little attention. To determine how face categories influence viewing preference in humans and rhesus macaques (Macaca mulatta), we performed two eye-tracking experiments using a visual preference task whereby pairs of faces from different species were presented simultaneously. The results indicated that viewing time was significantly influenced by the pairing of the face categories. Humans showed a strong bias towards an own-race face in an Asian-Caucasian condition. Rhesus macaques directed more attention towards non-human primate faces when they were paired with human faces, regardless of the species. When rhesus faces were paired with faces from Barbary macaques (Macaca sylvanus) or chimpanzees (Pan troglodytes), the novel species' faces attracted more attention. These results indicate that monkeys' viewing preferences, as assessed by a visual preference task, are modulated by several factors, species and dominance being the most influential. |
Diego Mendoza-Halliday; Santiago Torres; Julio C Martinez-Trujillo Sharp emergence of feature-selective sustained activity along the dorsal visual pathway Journal Article Nature Neuroscience, 17 (9), pp. 1255–1262, 2014. @article{Mendoza-Halliday2014, title = {Sharp emergence of feature-selective sustained activity along the dorsal visual pathway}, author = {Diego Mendoza-Halliday and Santiago Torres and Julio C Martinez-Trujillo}, doi = {10.1038/nn.3785}, year = {2014}, date = {2014-01-01}, journal = {Nature Neuroscience}, volume = {17}, number = {9}, pages = {1255--1262}, publisher = {Nature Publishing Group}, abstract = {Sustained activity encoding visual working memory representations has been observed in several cortical areas of primates. Where along the visual pathways this activity emerges remains unknown. Here we show in macaques that sustained spiking activity encoding memorized visual motion directions is absent in direction-selective neurons in early visual area middle temporal (MT). However, it is robustly present immediately downstream, in multimodal association area medial superior temporal (MST), as well as and in the lateral prefrontal cortex (LPFC). This sharp emergence of sustained activity along the dorsal visual pathway suggests a functional boundary between early visual areas, which encode sensory inputs, and downstream association areas, which additionally encode mnemonic representations. Moreover, local field potential oscillations in MT encoded the memorized directions and, in the low frequencies, were phase-coherent with LPFC spikes. This suggests that LPFC sustained activity modulates synaptic activity in MT, a putative top-down mechanism by which memory signals influence stimulus processing in early visual cortex.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Sustained activity encoding visual working memory representations has been observed in several cortical areas of primates. Where along the visual pathways this activity emerges remains unknown. Here we show in macaques that sustained spiking activity encoding memorized visual motion directions is absent in direction-selective neurons in early visual area middle temporal (MT). However, it is robustly present immediately downstream, in multimodal association area medial superior temporal (MST), as well as and in the lateral prefrontal cortex (LPFC). This sharp emergence of sustained activity along the dorsal visual pathway suggests a functional boundary between early visual areas, which encode sensory inputs, and downstream association areas, which additionally encode mnemonic representations. Moreover, local field potential oscillations in MT encoded the memorized directions and, in the low frequencies, were phase-coherent with LPFC spikes. This suggests that LPFC sustained activity modulates synaptic activity in MT, a putative top-down mechanism by which memory signals influence stimulus processing in early visual cortex. |
Paul G Middlebrooks; Jeffrey D Schall Response inhibition during perceptual decision making in humans and macaques Journal Article Attention, Perception, & Psychophysics, 76 (2), pp. 353–366, 2014. @article{Middlebrooks2014, title = {Response inhibition during perceptual decision making in humans and macaques}, author = {Paul G Middlebrooks and Jeffrey D Schall}, doi = {10.3758/s13414-013-0599-6}, year = {2014}, date = {2014-01-01}, journal = {Attention, Perception, & Psychophysics}, volume = {76}, number = {2}, pages = {353--366}, abstract = {Response inhibition in stop signal tasks has been explained as the outcome of a race between GO and STOP processes (e.g., Logan, 1981). Response choice in two-alternative perceptual categorization tasks has been explained as the outcome of an accumulation of evidence for the alternative responses. To begin unifying these two powerful investigation frameworks, we obtained data from humans and macaque monkeys performing a stop signal task with responses guided by perceptual categorization and variable degrees of difficulty, ranging from low to high accuracy. Comparable results across species reinforced the validity of this animal model. Response times and errors increased with categorization difficulty. The probability of failing to inhibit responses on stop signal trials increased with stop signal delay, and the response times for failed stop signal trials were shorter than those for trials with no stop signal. Thus, the Logan race model could be applied to estimate the duration of the stopping process. We found that the duration of the STOP process did not vary across a wide range of discrimination accuracies. This is consistent with the functional, and possibly mechanistic, independence of choice and inhibition mechanisms.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Response inhibition in stop signal tasks has been explained as the outcome of a race between GO and STOP processes (e.g., Logan, 1981). Response choice in two-alternative perceptual categorization tasks has been explained as the outcome of an accumulation of evidence for the alternative responses. To begin unifying these two powerful investigation frameworks, we obtained data from humans and macaque monkeys performing a stop signal task with responses guided by perceptual categorization and variable degrees of difficulty, ranging from low to high accuracy. Comparable results across species reinforced the validity of this animal model. Response times and errors increased with categorization difficulty. The probability of failing to inhibit responses on stop signal trials increased with stop signal delay, and the response times for failed stop signal trials were shorter than those for trials with no stop signal. Thus, the Logan race model could be applied to estimate the duration of the stopping process. We found that the duration of the STOP process did not vary across a wide range of discrimination accuracies. This is consistent with the functional, and possibly mechanistic, independence of choice and inhibition mechanisms. |
Tania Ortuno; Kenneth L Grieve; Ricardo Cao; Javier Cudeiro; Casto Rivadulla Bursting thalamic responses in awake monkey contribute to visual detection and are modulated by corticofugal feedback Journal Article Frontiers in Behavioral Neuroscience, 8 , pp. 1–10, 2014. @article{Ortuno2014, title = {Bursting thalamic responses in awake monkey contribute to visual detection and are modulated by corticofugal feedback}, author = {Tania Ortuno and Kenneth L Grieve and Ricardo Cao and Javier Cudeiro and Casto Rivadulla}, doi = {10.3389/fnbeh.2014.00198}, year = {2014}, date = {2014-01-01}, journal = {Frontiers in Behavioral Neuroscience}, volume = {8}, pages = {1--10}, abstract = {The lateral geniculate nucleus is the gateway for visual information en route to the visual cortex. Neural activity is characterized by the existence of two firing modes: burst and tonic. Originally associated with sleep, bursts have now been postulated to be a part of the normal visual response, structured to increase the probability of cortical activation, able to act as a "wake-up" call to the cortex. We investigated a potential role for burst in the detection of novel stimuli by recording neuronal activity in the lateral geniculate nucleus (LGN) of behaving monkeys during a visual detection task. Our results show that bursts are often the neuron's first response, and are more numerous in the response to attended target stimuli than to unattended distractor stimuli. Bursts are indicators of the task novelty, as repetition decreased bursting. Because the primary visual cortex is the major modulatory input to the LGN, we compared the results obtained in control conditions with those observed when cortical activity was reduced by TMS. This cortical deactivation reduced visual response related bursting by 90%. These results highlight a novel role for the thalamus, able to code higher order image attributes as important as novelty early in the thalamo-cortical conversation.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The lateral geniculate nucleus is the gateway for visual information en route to the visual cortex. Neural activity is characterized by the existence of two firing modes: burst and tonic. Originally associated with sleep, bursts have now been postulated to be a part of the normal visual response, structured to increase the probability of cortical activation, able to act as a "wake-up" call to the cortex. We investigated a potential role for burst in the detection of novel stimuli by recording neuronal activity in the lateral geniculate nucleus (LGN) of behaving monkeys during a visual detection task. Our results show that bursts are often the neuron's first response, and are more numerous in the response to attended target stimuli than to unattended distractor stimuli. Bursts are indicators of the task novelty, as repetition decreased bursting. Because the primary visual cortex is the major modulatory input to the LGN, we compared the results obtained in control conditions with those observed when cortical activity was reduced by TMS. This cortical deactivation reduced visual response related bursting by 90%. These results highlight a novel role for the thalamus, able to code higher order image attributes as important as novelty early in the thalamo-cortical conversation. |
Xiaochuan Pan; Hongwei Fan; Kosuke Sawa; Ichiro Tsuda; Minoru Tsukada; Masamichi Sakagami Reward inference by primate prefrontal and striatal neurons Journal Article The Journal of Neuroscience, 34 (4), pp. 1380–1396, 2014. @article{Pan2014b, title = {Reward inference by primate prefrontal and striatal neurons}, author = {Xiaochuan Pan and Hongwei Fan and Kosuke Sawa and Ichiro Tsuda and Minoru Tsukada and Masamichi Sakagami}, doi = {10.1523/JNEUROSCI.2263-13.2014}, year = {2014}, date = {2014-01-01}, journal = {The Journal of Neuroscience}, volume = {34}, number = {4}, pages = {1380--1396}, publisher = {34}, abstract = {The brain contains multiple yet distinct systems involved in reward prediction. To understand the nature of these processes, we recorded single-unit activity from the lateral prefrontal cortex (LPFC) and the striatum in monkeys performing a reward inference task using an asymmetric reward schedule. We found that neurons both in the LPFC and in the striatum predicted reward values for stimuli that had been previously well experienced with set reward quantities in the asymmetric reward task. Importantly, these LPFC neurons could predict the reward value of a stimulus using transitive inference even when the monkeys had not yet learned the stimulus–reward association directly; whereas these striatal neurons did not show such an ability. Nevertheless, because there were two set amounts of reward (large and small), the selected striatal neurons were able to exclusively infer the reward value (e.g., large) of one novel stimulus from a pair after directly experiencing the alternative stimulus with the other reward value (e.g., small). Our results suggest that although neurons that predict reward value for old stimuli in the LPFC could also do so for new stimuli via transitive inference, those in the striatum could only predict reward for new stimuli via exclusive inference. Moreover, the striatum showed more complex functions than was surmised previously for model-free learning.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The brain contains multiple yet distinct systems involved in reward prediction. To understand the nature of these processes, we recorded single-unit activity from the lateral prefrontal cortex (LPFC) and the striatum in monkeys performing a reward inference task using an asymmetric reward schedule. We found that neurons both in the LPFC and in the striatum predicted reward values for stimuli that had been previously well experienced with set reward quantities in the asymmetric reward task. Importantly, these LPFC neurons could predict the reward value of a stimulus using transitive inference even when the monkeys had not yet learned the stimulus–reward association directly; whereas these striatal neurons did not show such an ability. Nevertheless, because there were two set amounts of reward (large and small), the selected striatal neurons were able to exclusively infer the reward value (e.g., large) of one novel stimulus from a pair after directly experiencing the alternative stimulus with the other reward value (e.g., small). Our results suggest that although neurons that predict reward value for old stimuli in the LPFC could also do so for new stimuli via transitive inference, those in the striatum could only predict reward for new stimuli via exclusive inference. Moreover, the striatum showed more complex functions than was surmised previously for model-free learning. |
Pierpaolo Pani; Tom Theys; Maria C Romero; Peter Janssen Grasping execution and grasping observation activity of single neurons in the macaque anterior intraparietal area Journal Article Journal of Cognitive Neuroscience, 26 (10), pp. 2342–2355, 2014. @article{Pani2014, title = {Grasping execution and grasping observation activity of single neurons in the macaque anterior intraparietal area}, author = {Pierpaolo Pani and Tom Theys and Maria C Romero and Peter Janssen}, doi = {10.1162/jocn_a_00647}, year = {2014}, date = {2014-01-01}, journal = {Journal of Cognitive Neuroscience}, volume = {26}, number = {10}, pages = {2342--2355}, abstract = {Primates use vision to guide their actions in everyday life. Visually guided object grasping is known to rely on a network of cortical areas located in the parietal and premotor cortex. We recorded in the anterior intraparietal area (AIP), an area in the dorsal visual stream that is critical for object grasping and densely connected with the premotor cortex, while monkeys were grasping objects under visual guidance and during passive fixation of videos of grasping actions from the first-person perspective. All AIP neurons in this study responded during grasping execution in the light, that is, became more active after the hand had started to move toward the object and during grasping in the dark. More than half of these AIP neurons responded during the observation of a video of the same grasping actions on a display. Furthermore, these AIP neurons responded as strongly during passive fixation of movements of a hand on a scrambled background and to a lesser extent to a shape appearing within the visual field near the object. Therefore, AIP neurons responding during grasping execution also respond during passive observation of grasping actions and most of them even during passive observation of movements of a simple shape in the visual field.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Primates use vision to guide their actions in everyday life. Visually guided object grasping is known to rely on a network of cortical areas located in the parietal and premotor cortex. We recorded in the anterior intraparietal area (AIP), an area in the dorsal visual stream that is critical for object grasping and densely connected with the premotor cortex, while monkeys were grasping objects under visual guidance and during passive fixation of videos of grasping actions from the first-person perspective. All AIP neurons in this study responded during grasping execution in the light, that is, became more active after the hand had started to move toward the object and during grasping in the dark. More than half of these AIP neurons responded during the observation of a video of the same grasping actions on a display. Furthermore, these AIP neurons responded as strongly during passive fixation of movements of a hand on a scrambled background and to a lesser extent to a shape appearing within the visual field near the object. Therefore, AIP neurons responding during grasping execution also respond during passive observation of grasping actions and most of them even during passive observation of movements of a simple shape in the visual field. |
C A Patterson; J Duijnhouwer; S C Wissig; B Krekelberg; A Kohn Similar adaptation effects in primary visual cortex and area MT of the macaque monkey under matched stimulus conditions Journal Article Journal of Neurophysiology, 111 (6), pp. 1203–1213, 2014. @article{Patterson2014, title = {Similar adaptation effects in primary visual cortex and area MT of the macaque monkey under matched stimulus conditions}, author = {C A Patterson and J Duijnhouwer and S C Wissig and B Krekelberg and A Kohn}, doi = {10.1152/jn.00030.2013}, year = {2014}, date = {2014-01-01}, journal = {Journal of Neurophysiology}, volume = {111}, number = {6}, pages = {1203--1213}, abstract = {Recent stimulus history, or adaptation, can alter neuronal response properties. Adaptation effects have been characterized in a number of visually responsive structures, from the retina to higher visual cortex. However, it remains unclear whether adaptation effects across stages of the visual system take a similar form in response to a particular sensory event. This is because studies typically probe a single structure or cortical area, using a stimulus ensemble chosen to provide potent drive to the cells of interest. Here we adopt an alternative approach and compare adaptation effects in primary visual cortex (V1) and area MT using identical stimulus ensembles. Previous work has suggested these areas adjust to recent stimulus drive in distinct ways. We show that this is not the case: adaptation effects in V1 and MT can involve weak or strong loss of responsivity and shifts in neuronal preference toward or away from the adapter, depending on stimulus size and adaptation duration. For a particular stimulus size and adaptation duration, however, effects are similar in nature and magnitude in V1 and MT. We also show that adaptation effects in MT of awake animals depend strongly on stimulus size. Our results suggest that the strategies for adjusting to recent stimulus history depend more strongly on adaptation duration and stimulus size than on the cortical area. Moreover, they indicate that different levels of the visual system adapt similarly to recent sensory experience.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Recent stimulus history, or adaptation, can alter neuronal response properties. Adaptation effects have been characterized in a number of visually responsive structures, from the retina to higher visual cortex. However, it remains unclear whether adaptation effects across stages of the visual system take a similar form in response to a particular sensory event. This is because studies typically probe a single structure or cortical area, using a stimulus ensemble chosen to provide potent drive to the cells of interest. Here we adopt an alternative approach and compare adaptation effects in primary visual cortex (V1) and area MT using identical stimulus ensembles. Previous work has suggested these areas adjust to recent stimulus drive in distinct ways. We show that this is not the case: adaptation effects in V1 and MT can involve weak or strong loss of responsivity and shifts in neuronal preference toward or away from the adapter, depending on stimulus size and adaptation duration. For a particular stimulus size and adaptation duration, however, effects are similar in nature and magnitude in V1 and MT. We also show that adaptation effects in MT of awake animals depend strongly on stimulus size. Our results suggest that the strategies for adjusting to recent stimulus history depend more strongly on adaptation duration and stimulus size than on the cortical area. Moreover, they indicate that different levels of the visual system adapt similarly to recent sensory experience. |
Ivo D Popivanov; Jan Jastorff; Wim Vanduffel; Rufin Vogels Heterogeneous single-unit selectivity in an fMRI-defined body-selective patch Journal Article The Journal of Neuroscience, 34 (1), pp. 95–111, 2014. @article{Popivanov2014, title = {Heterogeneous single-unit selectivity in an fMRI-defined body-selective patch}, author = {Ivo D Popivanov and Jan Jastorff and Wim Vanduffel and Rufin Vogels}, doi = {10.1523/JNEUROSCI.2748-13.2014}, year = {2014}, date = {2014-01-01}, journal = {The Journal of Neuroscience}, volume = {34}, number = {1}, pages = {95--111}, abstract = {Although the visual representation of bodies is essential for reproduction, survival, and social communication, little is known about the mechanisms of body recognition at the single neuron level. Imaging studies showed body-category selective regions in the primate occipitotemporal cortex, but it is difficult to infer the stimulus selectivities of the neurons from the population activity measured in these fMRI studies. To overcome this, we recorded single unit activity and local field potentials (LFPs) in the middle superior temporal sulcus body patch, defined by fMRI in the same rhesus monkeys. Both the spiking activity, averaged across single neurons, and LFP gamma power in this body patch was greater for bodies (including monkey bodies, human bodies, mammals, and birds) compared with other objects, which fits the fMRI activation. Single neurons responded to a small proportion of body images. Thus, the category selectivity at the population level resulted from averaging responses of a heterogeneous population of single units. Despite such strong within-category selectivity at the single unit level, two distinct clusters, bodies and nonbodies, were present when analyzing the responses at the population level, and a classifier that was trained using the responses to a subset of images was able to classify novel images of bodies with high accuracy. The body-patch neurons showed strong selectivity for individual body parts at different orientations. Overall, these data suggest that single units in the fMRI-defined body patch are biased to prefer bodies over nonbody objects, including faces, with a strong selectivity for individual body images.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Although the visual representation of bodies is essential for reproduction, survival, and social communication, little is known about the mechanisms of body recognition at the single neuron level. Imaging studies showed body-category selective regions in the primate occipitotemporal cortex, but it is difficult to infer the stimulus selectivities of the neurons from the population activity measured in these fMRI studies. To overcome this, we recorded single unit activity and local field potentials (LFPs) in the middle superior temporal sulcus body patch, defined by fMRI in the same rhesus monkeys. Both the spiking activity, averaged across single neurons, and LFP gamma power in this body patch was greater for bodies (including monkey bodies, human bodies, mammals, and birds) compared with other objects, which fits the fMRI activation. Single neurons responded to a small proportion of body images. Thus, the category selectivity at the population level resulted from averaging responses of a heterogeneous population of single units. Despite such strong within-category selectivity at the single unit level, two distinct clusters, bodies and nonbodies, were present when analyzing the responses at the population level, and a classifier that was trained using the responses to a subset of images was able to classify novel images of bodies with high accuracy. The body-patch neurons showed strong selectivity for individual body parts at different orientations. Overall, these data suggest that single units in the fMRI-defined body patch are biased to prefer bodies over nonbody objects, including faces, with a strong selectivity for individual body images. |
Elsie Premereur; Wim Vanduffel; Peter Janssen The effect of FEF microstimulation on the responses of neurons in the lateral intraparietal area Journal Article Journal of Cognitive Neuroscience, 26 (8), pp. 1672–1684, 2014. @article{Premereur2014, title = {The effect of FEF microstimulation on the responses of neurons in the lateral intraparietal area}, author = {Elsie Premereur and Wim Vanduffel and Peter Janssen}, doi = {10.1162/jocn_a_00591}, year = {2014}, date = {2014-01-01}, journal = {Journal of Cognitive Neuroscience}, volume = {26}, number = {8}, pages = {1672--1684}, abstract = {The macaque FEFs and the lateral intraparietal area (LIP) are high-level cortical areas involved in both spatial attention and oculomotor behavior. Stimulating FEF at a level below the threshold for evoking saccades increases fMRI activity and gamma power in area LIP, but the precise effect exerted by the FEF on LIP neurons is unknown. In our study, we recorded LIP single-unit activity during a visually guided saccade task with a peripherally presented go signal during microstimulation of FEF. We found that FEF microstimulation increased the LIP spike rate imme- diately after the highly salient go signal inside the LIP receptive field when both target and go signal were presented inside the receptive field, and no other possible go cues were present on the screen. The effect of FEF microstimulation on the LIP response was positive until at least 800msec aftermicrostimulation had ceased, but reversed for longer trial durations. Therefore, FEF microstimulation can modulate the LIP spike rate only when attention is selectively directed toward the stimulated location. These results provide the first direct evidence for LIP spike rate modulations caused by FEF microstimulation, thus showing that FEF activity can be the source of top–down control ofarea LIP.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The macaque FEFs and the lateral intraparietal area (LIP) are high-level cortical areas involved in both spatial attention and oculomotor behavior. Stimulating FEF at a level below the threshold for evoking saccades increases fMRI activity and gamma power in area LIP, but the precise effect exerted by the FEF on LIP neurons is unknown. In our study, we recorded LIP single-unit activity during a visually guided saccade task with a peripherally presented go signal during microstimulation of FEF. We found that FEF microstimulation increased the LIP spike rate imme- diately after the highly salient go signal inside the LIP receptive field when both target and go signal were presented inside the receptive field, and no other possible go cues were present on the screen. The effect of FEF microstimulation on the LIP response was positive until at least 800msec aftermicrostimulation had ceased, but reversed for longer trial durations. Therefore, FEF microstimulation can modulate the LIP spike rate only when attention is selectively directed toward the stimulated location. These results provide the first direct evidence for LIP spike rate modulations caused by FEF microstimulation, thus showing that FEF activity can be the source of top–down control ofarea LIP. |
A P Raghuraman; Camillo Padoa-Schioppa Integration of multiple determinants in the neuronal computation of economic values Journal Article The Journal of Neuroscience, 34 (35), pp. 11583–11603, 2014. @article{Raghuraman2014, title = {Integration of multiple determinants in the neuronal computation of economic values}, author = {A P Raghuraman and Camillo Padoa-Schioppa}, doi = {10.1523/JNEUROSCI.1235-14.2014}, year = {2014}, date = {2014-01-01}, journal = {The Journal of Neuroscience}, volume = {34}, number = {35}, pages = {11583--11603}, abstract = {Economic goods may vary on multiple dimensions (determinants). A central conjecture in decision neuroscience is that choices between goods are made by comparing subjective values computed through the integration of all relevant determinants. Previous work identified three groups of neurons in the orbitofrontal cortex (OFC) of monkeys engaged in economic choices: (1) offer value cells, which encode the value of individual offers; (2) chosen value cells, which encode the value of the chosen good; and (3) chosen juice cells, which encode the identity of the chosen good. In principle, these populations could be sufficient to generate a decision. Critically, previous work did not assess whether offer value cells (the putative input to the decision) indeed encode subjective values as opposed to physical properties of the goods, and/or whether offer value cells integrate multiple determinants. To address these issues, we recorded from the OFC while monkeys chose between risky outcomes. Confirming previous observations, three populations of neurons encoded the value of individual offers, the value of the chosen option, and the value-independent choice outcome. The activity of both offer value cells and chosen value cells encoded values defined by the integration of juice quantity and probability. Furthermore, both populations reflected the subjective risk attitude of the animals. We also found additional groups of neurons encoding the risk associated with a particular option, the risky nature of the chosen option, and whether the trial outcome was positive or negative. These results provide substantial support for the conjecture described above and for the involvement of OFC in good-based decisions.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Economic goods may vary on multiple dimensions (determinants). A central conjecture in decision neuroscience is that choices between goods are made by comparing subjective values computed through the integration of all relevant determinants. Previous work identified three groups of neurons in the orbitofrontal cortex (OFC) of monkeys engaged in economic choices: (1) offer value cells, which encode the value of individual offers; (2) chosen value cells, which encode the value of the chosen good; and (3) chosen juice cells, which encode the identity of the chosen good. In principle, these populations could be sufficient to generate a decision. Critically, previous work did not assess whether offer value cells (the putative input to the decision) indeed encode subjective values as opposed to physical properties of the goods, and/or whether offer value cells integrate multiple determinants. To address these issues, we recorded from the OFC while monkeys chose between risky outcomes. Confirming previous observations, three populations of neurons encoded the value of individual offers, the value of the chosen option, and the value-independent choice outcome. The activity of both offer value cells and chosen value cells encoded values defined by the integration of juice quantity and probability. Furthermore, both populations reflected the subjective risk attitude of the animals. We also found additional groups of neurons encoding the risk associated with a particular option, the risky nature of the chosen option, and whether the trial outcome was positive or negative. These results provide substantial support for the conjecture described above and for the involvement of OFC in good-based decisions. |
Maria C Romero; Pierpaolo Pani; Peter Janssen Coding of shape features in the macaque anterior intraparietal area Journal Article The Journal of Neuroscience, 34 (11), pp. 4006–4021, 2014. @article{Romero2014, title = {Coding of shape features in the macaque anterior intraparietal area}, author = {Maria C Romero and Pierpaolo Pani and Peter Janssen}, doi = {10.1523/JNEUROSCI.4095-13.2014}, year = {2014}, date = {2014-01-01}, journal = {The Journal of Neuroscience}, volume = {34}, number = {11}, pages = {4006--4021}, abstract = {The exquisite ability of primates to grasp and manipulate objects relies on the transformation of visual information into motor com- mands. To this end, the visual system extracts object affordances that can be used to program and execute the appropriate grip. The macaque anterior intraparietal (AIP) area hasbeen implicated in the extraction ofaffordances for the purpose ofgrasping. Neurons in the AIP area respond during visually guided grasping and to the visual presentation ofobjects. A subset ofAIP neurons is also activated by two-dimensional images ofobjects and even by outline contours defining the object shape, but it is unknown how AIP neurons actually represent object shape. In this study, we used a stimulus reduction approach to determine the minimum effective shape feature evoking AIP responses. AIP neurons responding to outline shapes also responded selectively to very small fragment stimuli measuring only 1–2°. This fragment selectivity could not be explained bydifferences in eyemovementsor simple orientation selectivity, but proved to be highly dependent on the relative position ofthe stimulus in the receptive field. Our findings challenge the current understanding ofthe AIP area as a critical stage in the dorsal stream for the extraction ofobject affordances.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The exquisite ability of primates to grasp and manipulate objects relies on the transformation of visual information into motor com- mands. To this end, the visual system extracts object affordances that can be used to program and execute the appropriate grip. The macaque anterior intraparietal (AIP) area hasbeen implicated in the extraction ofaffordances for the purpose ofgrasping. Neurons in the AIP area respond during visually guided grasping and to the visual presentation ofobjects. A subset ofAIP neurons is also activated by two-dimensional images ofobjects and even by outline contours defining the object shape, but it is unknown how AIP neurons actually represent object shape. In this study, we used a stimulus reduction approach to determine the minimum effective shape feature evoking AIP responses. AIP neurons responding to outline shapes also responded selectively to very small fragment stimuli measuring only 1–2°. This fragment selectivity could not be explained bydifferences in eyemovementsor simple orientation selectivity, but proved to be highly dependent on the relative position ofthe stimulus in the receptive field. Our findings challenge the current understanding ofthe AIP area as a critical stage in the dorsal stream for the extraction ofobject affordances. |
Arani Roy; Stephen V Shepherd; Michael L Platt Reversible inactivation of pSTS suppresses social gaze following in the macaque (Macaca mulatta) Journal Article Social Cognitive and Affective Neuroscience, 9 (2), pp. 209–217, 2014. @article{Roy2014, title = {Reversible inactivation of pSTS suppresses social gaze following in the macaque (Macaca mulatta)}, author = {Arani Roy and Stephen V Shepherd and Michael L Platt}, doi = {10.1093/scan/nss123}, year = {2014}, date = {2014-01-01}, journal = {Social Cognitive and Affective Neuroscience}, volume = {9}, number = {2}, pages = {209--217}, abstract = {Humans and other primates shift their attention to follow the gaze of others [gaze following (GF)]. This behavior is a foundational component of joint attention, which is severely disrupted in neurodevelopmental disorders such as autism and schizophrenia. Both cortical and subcortical pathways have been implicated in GF, but their contributions remain largely untested. While the proposed subcortical pathway hinges crucially on the amygdala, the cortical pathway is thought to require perceptual processing by a region in the posterior superior temporal sulcus (pSTS). To determine whether pSTS is necessary for typical GF behavior, we engaged rhesus macaques in a reward discrimination task confounded by leftward- and rightward-facing social distractors following saline or muscimol injections into left pSTS. We found that reversible inactivation of left pSTS with muscimol strongly suppressed GF, as assessed by reduced influence of observed gaze on target choices and saccadic reaction times. These findings demonstrate that activity in pSTS is required for normal GF by primates.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Humans and other primates shift their attention to follow the gaze of others [gaze following (GF)]. This behavior is a foundational component of joint attention, which is severely disrupted in neurodevelopmental disorders such as autism and schizophrenia. Both cortical and subcortical pathways have been implicated in GF, but their contributions remain largely untested. While the proposed subcortical pathway hinges crucially on the amygdala, the cortical pathway is thought to require perceptual processing by a region in the posterior superior temporal sulcus (pSTS). To determine whether pSTS is necessary for typical GF behavior, we engaged rhesus macaques in a reward discrimination task confounded by leftward- and rightward-facing social distractors following saline or muscimol injections into left pSTS. We found that reversible inactivation of left pSTS with muscimol strongly suppressed GF, as assessed by reduced influence of observed gaze on target choices and saccadic reaction times. These findings demonstrate that activity in pSTS is required for normal GF by primates. |
Douglas A Ruff; Marlene R Cohen Attention can either increase or decrease spike count correlations in visual cortex Journal Article Nature Neuroscience, 17 (11), pp. 1591–1597, 2014. @article{Ruff2014, title = {Attention can either increase or decrease spike count correlations in visual cortex}, author = {Douglas A Ruff and Marlene R Cohen}, doi = {10.1038/nn.3835}, year = {2014}, date = {2014-01-01}, journal = {Nature Neuroscience}, volume = {17}, number = {11}, pages = {1591--1597}, abstract = {Visual attention enhances the responses of visual neurons that encode the attended location. Several recent studies have shown that attention also decreases correlations between fluctuations in the responses of pairs of neurons (termed spike count correlation or r(SC)). These results are consistent with two hypotheses. First, attention-related changes in rate and r(SC) might be linked (perhaps through a common mechanism), with attention always decreasing r(SC). Second, attention might either increase or decrease r(SC), possibly depending on the role of the neurons in the behavioral task. We recorded simultaneously from dozens of neurons in area V4 while monkeys performed a discrimination task. We found strong evidence in favor of the second hypothesis, showing that attention can flexibly increase or decrease correlations depending on whether the neurons provide evidence for the same or opposite choices. These results place important constraints on models of the neuronal mechanisms underlying cognitive factors.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Visual attention enhances the responses of visual neurons that encode the attended location. Several recent studies have shown that attention also decreases correlations between fluctuations in the responses of pairs of neurons (termed spike count correlation or r(SC)). These results are consistent with two hypotheses. First, attention-related changes in rate and r(SC) might be linked (perhaps through a common mechanism), with attention always decreasing r(SC). Second, attention might either increase or decrease r(SC), possibly depending on the role of the neurons in the behavioral task. We recorded simultaneously from dozens of neurons in area V4 while monkeys performed a discrimination task. We found strong evidence in favor of the second hypothesis, showing that attention can flexibly increase or decrease correlations depending on whether the neurons provide evidence for the same or opposite choices. These results place important constraints on models of the neuronal mechanisms underlying cognitive factors. |
Douglas A Ruff; Marlene R Cohen Attention can increase or decrease spike count correlations between pairs of neurons depending on their role in a task Journal Article Nature Neuroscience, 17 (11), pp. 1591–1597, 2014. @article{Ruff2014a, title = {Attention can increase or decrease spike count correlations between pairs of neurons depending on their role in a task}, author = {Douglas A Ruff and Marlene R Cohen}, doi = {10.1038/nn.3835.Attention}, year = {2014}, date = {2014-01-01}, journal = {Nature Neuroscience}, volume = {17}, number = {11}, pages = {1591--1597}, abstract = {Visual attention enhances the responses of visual neurons that encode the attended location. Several recent studies showed that attention also decreases correlations between fluctuations in the responses of pairs of neurons (termed spike count correlation or rSC). The previous results are consistent with two hypotheses. Attention–related changes in rate and rSC might be linked (perhaps through a common mechanism), so that attention always decreases rSC. Alternately, attention might either increase or decrease rSC, possibly depending on the role the neurons play in the behavioral task. We recorded simultaneously from dozens of neurons in area V4 while monkeys performed a discrimination task. We found strong evidence in favor of the second hypothesis, showing that attention can flexibly increase or decrease correlations, depending on whether the neurons provide evidence for the same or opposite perceptual decisions. These results place important constraints on models of the neuronal mechanisms underlying cognitive factors.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Visual attention enhances the responses of visual neurons that encode the attended location. Several recent studies showed that attention also decreases correlations between fluctuations in the responses of pairs of neurons (termed spike count correlation or rSC). The previous results are consistent with two hypotheses. Attention–related changes in rate and rSC might be linked (perhaps through a common mechanism), so that attention always decreases rSC. Alternately, attention might either increase or decrease rSC, possibly depending on the role the neurons play in the behavioral task. We recorded simultaneously from dozens of neurons in area V4 while monkeys performed a discrimination task. We found strong evidence in favor of the second hypothesis, showing that attention can flexibly increase or decrease correlations, depending on whether the neurons provide evidence for the same or opposite perceptual decisions. These results place important constraints on models of the neuronal mechanisms underlying cognitive factors. |
Patrick T Sadtler; Kristin M Quick; Matthew D Golub; Steven M Chase; Stephen I Ryu; Elizabeth C Tyler-Kabara; Byron M Yu; Aaron P Batista Neural constraints on learning Journal Article Nature, 512 , pp. 423–426, 2014. @article{Sadtler2014, title = {Neural constraints on learning}, author = {Patrick T Sadtler and Kristin M Quick and Matthew D Golub and Steven M Chase and Stephen I Ryu and Elizabeth C Tyler-Kabara and Byron M Yu and Aaron P Batista}, doi = {http://dx.doi.org/10.1038/nature13665}, year = {2014}, date = {2014-01-01}, journal = {Nature}, volume = {512}, pages = {423--426}, publisher = {Nature Publishing Group}, abstract = {Learning, whether motor, sensory or cognitive, requires networks of neurons to generate new activity patterns. As some behaviours are easier to learn than others, we asked if some neural activity patterns are easier to generate than others. Here we investigate whether an existing network constrains the patterns that a subset of its neurons is capable of exhibiting, and if so, what principles define this constraint. We employed a closed-loop intracortical brain-computer interface learning paradigm in which Rhesus macaques (Macaca mulatta) controlled a computer cursor by modulating neural activity patterns in the primary motor cortex. Using the brain-computer interface paradigm, we could specify and alter how neural activity mapped to cursor velocity. At the start of each session, we observed the characteristic activity patterns of the recorded neural population. The activity of a neural population can be represented in a high-dimensional space (termed the neural space), wherein each dimension corresponds to the activity of one neuron. These characteristic activity patterns comprise a low-dimensional subspace (termed the intrinsic manifold) within the neural space. The intrinsic manifold presumably reflects constraints imposed by the underlying neural circuitry. Here we show that the animals could readily learn to proficiently control the cursor using neural activity patterns that were within the intrinsic manifold. However, animals were less able to learn to proficiently control the cursor using activity patterns that were outside of the intrinsic manifold. These results suggest that the existing structure of a network can shape learning. On a timescale of hours, it seems to be difficult to learn to generate neural activity patterns that are not consistent with the existing network structure. These findings offer a network-level explanation for the observation that we are more readily able to learn new skills when they are related to the skills that we already possess.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Learning, whether motor, sensory or cognitive, requires networks of neurons to generate new activity patterns. As some behaviours are easier to learn than others, we asked if some neural activity patterns are easier to generate than others. Here we investigate whether an existing network constrains the patterns that a subset of its neurons is capable of exhibiting, and if so, what principles define this constraint. We employed a closed-loop intracortical brain-computer interface learning paradigm in which Rhesus macaques (Macaca mulatta) controlled a computer cursor by modulating neural activity patterns in the primary motor cortex. Using the brain-computer interface paradigm, we could specify and alter how neural activity mapped to cursor velocity. At the start of each session, we observed the characteristic activity patterns of the recorded neural population. The activity of a neural population can be represented in a high-dimensional space (termed the neural space), wherein each dimension corresponds to the activity of one neuron. These characteristic activity patterns comprise a low-dimensional subspace (termed the intrinsic manifold) within the neural space. The intrinsic manifold presumably reflects constraints imposed by the underlying neural circuitry. Here we show that the animals could readily learn to proficiently control the cursor using neural activity patterns that were within the intrinsic manifold. However, animals were less able to learn to proficiently control the cursor using activity patterns that were outside of the intrinsic manifold. These results suggest that the existing structure of a network can shape learning. On a timescale of hours, it seems to be difficult to learn to generate neural activity patterns that are not consistent with the existing network structure. These findings offer a network-level explanation for the observation that we are more readily able to learn new skills when they are related to the skills that we already possess. |
Nicholas A Steinmetz; Tirin Moore Eye movement preparation modulates neuronal responses in area V4 when dissociated from attentional demands Journal Article Neuron, 83 (2), pp. 496–506, 2014. @article{Steinmetz2014, title = {Eye movement preparation modulates neuronal responses in area V4 when dissociated from attentional demands}, author = {Nicholas A Steinmetz and Tirin Moore}, doi = {10.1016/j.neuron.2014.06.014}, year = {2014}, date = {2014-01-01}, journal = {Neuron}, volume = {83}, number = {2}, pages = {496--506}, publisher = {83}, abstract = {We examined whether the preparation of saccadic eye movements, when behaviorally dissociated from covert attention, modulates activity within visual cortex. We measured single-neuron and local field potential (LFP) responses to visual stimuli in area V4 while monkeys covertly attended a stimulus at one location and prepared saccades to a potential target at another. In spite of the irrelevance of visual information at the saccade target, visual activity at that location was modulated at least as much as, and often more than, activity at the covertly attended location. Modulations of activity at the attended and saccade target locations were qualitatively similar and included increased response magnitude, stimulus selectivity, and spiking reliability, as well as increased gamma and decreased low-frequency power of LFPs. These results demonstrate that saccade preparation is sufficient to modulate visual cortical representations and suggest that the interrelationship of oculomotor and attention-related mechanisms extends to posterior visual cortex.}, keywords = {}, pubstate = {published}, tppubtype = {article} } We examined whether the preparation of saccadic eye movements, when behaviorally dissociated from covert attention, modulates activity within visual cortex. We measured single-neuron and local field potential (LFP) responses to visual stimuli in area V4 while monkeys covertly attended a stimulus at one location and prepared saccades to a potential target at another. In spite of the irrelevance of visual information at the saccade target, visual activity at that location was modulated at least as much as, and often more than, activity at the covertly attended location. Modulations of activity at the attended and saccade target locations were qualitatively similar and included increased response magnitude, stimulus selectivity, and spiking reliability, as well as increased gamma and decreased low-frequency power of LFPs. These results demonstrate that saccade preparation is sufficient to modulate visual cortical representations and suggest that the interrelationship of oculomotor and attention-related mechanisms extends to posterior visual cortex. |
Chess Stetson; Richard A Andersen The parietal reach region selectively anti-synchronizes with dorsal premotor cortex during planning Journal Article The Journal of Neuroscience, 34 (36), pp. 11948–11958, 2014. @article{Stetson2014, title = {The parietal reach region selectively anti-synchronizes with dorsal premotor cortex during planning}, author = {Chess Stetson and Richard A Andersen}, doi = {10.1523/JNEUROSCI.0097-14.2014}, year = {2014}, date = {2014-01-01}, journal = {The Journal of Neuroscience}, volume = {34}, number = {36}, pages = {11948--11958}, abstract = {Recent reports have indicated that oscillations shared across distant cortical regions can enhance their connectivity, but do coherent oscillations ever diminish connectivity? We investigated oscillatory activity in two distinct reach-related regions in the awake behaving monkey (Macaca mulatta): the parietal reach region (PRR) and the dorsal premotor cortex (PMd). PRR and PMd were found to oscillate at similar frequencies (beta, 15–30 Hz) during periods of fixation and movement planning. At first glance, the stronger oscillator of the two, PRR, would seem to drive the weaker, PMd. However, a more fine-grained measure, the partial spike-field coherence, revealed a different relationship. Relative to global beta-band activity in the brain, action potentials in PRR anti-synchronize with PMd oscillations. These data suggest that, rather than driving PMd during planning, PRR neurons fire in such a way that they are less likely to communicate information to PMd.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Recent reports have indicated that oscillations shared across distant cortical regions can enhance their connectivity, but do coherent oscillations ever diminish connectivity? We investigated oscillatory activity in two distinct reach-related regions in the awake behaving monkey (Macaca mulatta): the parietal reach region (PRR) and the dorsal premotor cortex (PMd). PRR and PMd were found to oscillate at similar frequencies (beta, 15–30 Hz) during periods of fixation and movement planning. At first glance, the stronger oscillator of the two, PRR, would seem to drive the weaker, PMd. However, a more fine-grained measure, the partial spike-field coherence, revealed a different relationship. Relative to global beta-band activity in the brain, action potentials in PRR anti-synchronize with PMd oscillations. These data suggest that, rather than driving PMd during planning, PRR neurons fire in such a way that they are less likely to communicate information to PMd. |
Caleb E Strait; Tommy C Blanchard; Benjamin Y Hayden Reward value comparison via mutual inhibition in ventromedial prefrontal cortex Journal Article Neuron, 82 (6), pp. 1357–1366, 2014. @article{Strait2014, title = {Reward value comparison via mutual inhibition in ventromedial prefrontal cortex}, author = {Caleb E Strait and Tommy C Blanchard and Benjamin Y Hayden}, doi = {10.1016/j.neuron.2014.04.032}, year = {2014}, date = {2014-01-01}, journal = {Neuron}, volume = {82}, number = {6}, pages = {1357--1366}, publisher = {Elsevier Inc.}, abstract = {Recent theories suggest that reward-based choice reflects competition between value signals in the ventromedial prefrontal cortex (vmPFC). We tested this idea by recording vmPFC neurons while macaques performed a gambling task with asynchronous offer presentation. We found that neuronal activity shows four patterns consistent with selection via mutual inhibition: (1) correlated tuning for probability and reward size, suggesting that vmPFC carries an integrated value signal; (2) anti-correlated tuning curves for the two options, suggesting mutual inhibition; (3) neurons rapidly come to signal the value of the chosen offer, suggesting the circuit serves to produce a choice; and (4) after regressing out the effects of option values, firing rates still could predict choice-a choice probability signal. In addition, neurons signaled gamble outcomes, suggesting that vmPFC contributes to both monitoring and choice processes. These data suggest a possible mechanism for reward-based choice and endorse the centrality of vmPFC in that process.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Recent theories suggest that reward-based choice reflects competition between value signals in the ventromedial prefrontal cortex (vmPFC). We tested this idea by recording vmPFC neurons while macaques performed a gambling task with asynchronous offer presentation. We found that neuronal activity shows four patterns consistent with selection via mutual inhibition: (1) correlated tuning for probability and reward size, suggesting that vmPFC carries an integrated value signal; (2) anti-correlated tuning curves for the two options, suggesting mutual inhibition; (3) neurons rapidly come to signal the value of the chosen offer, suggesting the circuit serves to produce a choice; and (4) after regressing out the effects of option values, firing rates still could predict choice-a choice probability signal. In addition, neurons signaled gamble outcomes, suggesting that vmPFC contributes to both monitoring and choice processes. These data suggest a possible mechanism for reward-based choice and endorse the centrality of vmPFC in that process. |
Siavash Vaziri; Eric T Carlson; Zhihong Wang; Charles E Connor A channel for 3D environmental shape in anterior inferotemporal cortex Journal Article Neuron, 84 (1), pp. 55–62, 2014. @article{Vaziri2014, title = {A channel for 3D environmental shape in anterior inferotemporal cortex}, author = {Siavash Vaziri and Eric T Carlson and Zhihong Wang and Charles E Connor}, doi = {10.1016/j.neuron.2014.08.043}, year = {2014}, date = {2014-01-01}, journal = {Neuron}, volume = {84}, number = {1}, pages = {55--62}, publisher = {Elsevier Inc.}, abstract = {Inferotemporal cortex (IT) has long been studied as asingle pathway dedicated to object vision, but connectivity analysis reveals anatomically distinct channels, through ventral superior temporal sulcus (STSv) and dorsal/ventral inferotemporal gyrus (TEd, TEv). Here, we report a major functional distinction between channels. We studied individual IT neurons in monkeys viewing stereoscopic 3D images projected on a large screen. We used adaptive stimuli to explore neural tuning for 3D abstract shapes ranging in scale and topology from small, closed, bounded objects to large, open, unbounded environments (landscape-like surfaces and cave-like interiors). In STSv, most neurons were more responsive to objects, as expected. In TEd, surprisingly, most neurons were more responsive to 3D environmental shape. Previous studies have localized environmental information to posterior cortical modules. Our results show it is also channeled through anterior IT, where extensive cross-connections between STSv and TEd could integrate object and environmental shape information.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Inferotemporal cortex (IT) has long been studied as asingle pathway dedicated to object vision, but connectivity analysis reveals anatomically distinct channels, through ventral superior temporal sulcus (STSv) and dorsal/ventral inferotemporal gyrus (TEd, TEv). Here, we report a major functional distinction between channels. We studied individual IT neurons in monkeys viewing stereoscopic 3D images projected on a large screen. We used adaptive stimuli to explore neural tuning for 3D abstract shapes ranging in scale and topology from small, closed, bounded objects to large, open, unbounded environments (landscape-like surfaces and cave-like interiors). In STSv, most neurons were more responsive to objects, as expected. In TEd, surprisingly, most neurons were more responsive to 3D environmental shape. Previous studies have localized environmental information to posterior cortical modules. Our results show it is also channeled through anterior IT, where extensive cross-connections between STSv and TEd could integrate object and environmental shape information. |
2013 |
Daniel S Pages; Jennifer M Groh Looking at the ventriloquist: Visual outcome of eye movements calibrates sound localization Journal Article PLoS ONE, 8 (8), pp. 1–7, 2013. @article{Pages2013, title = {Looking at the ventriloquist: Visual outcome of eye movements calibrates sound localization}, author = {Daniel S Pages and Jennifer M Groh}, doi = {10.1371/journal.pone.0072562}, year = {2013}, date = {2013-01-01}, journal = {PLoS ONE}, volume = {8}, number = {8}, pages = {1--7}, publisher = {10. 1371/journal.pone.0072562}, address = {e72562. doi}, abstract = {A general problem in learning is how the brain determines what lesson to learn (and what lessons not to learn). For example, sound localization is a behavior that is partially learned with the aid of vision. This process requires correctly matching a visual location to that of a sound. This is an intrinsically circular problem when sound location is itself uncertain and the visual scene is rife with possible visual matches. Here, we develop a simple paradigm using visual guidance of sound localization to gain insight into how the brain confronts this type of circularity. We tested two competing hypotheses. 1: The brain guides sound location learning based on the synchrony or simultaneity of auditory-visual stimuli, potentially involving a Hebbian associative mechanism. 2: The brain uses a 'guess and check' heuristic in which visual feedback that is obtained after an eye movement to a sound alters future performance, perhaps by recruiting the brain's reward-related circuitry. We assessed the effects of exposure to visual stimuli spatially mismatched from sounds on performance of an interleaved auditory-only saccade task. We found that when humans and monkeys were provided the visual stimulus asynchronously with the sound but as feedback to an auditory-guided saccade, they shifted their subsequent auditory-only performance toward the direction of the visual cue by 1.3-1.7 degrees, or 22-28% of the original 6 degree visual-auditory mismatch. In contrast when the visual stimulus was presented synchronously with the sound but extinguished too quickly to provide this feedback, there was little change in subsequent auditory-only performance. Our results suggest that the outcome of our own actions is vital to localizing sounds correctly. Contrary to previous expectations, visual calibration of auditory space does not appear to require visual-auditory associations based on synchrony/simultaneity.}, keywords = {}, pubstate = {published}, tppubtype = {article} } A general problem in learning is how the brain determines what lesson to learn (and what lessons not to learn). For example, sound localization is a behavior that is partially learned with the aid of vision. This process requires correctly matching a visual location to that of a sound. This is an intrinsically circular problem when sound location is itself uncertain and the visual scene is rife with possible visual matches. Here, we develop a simple paradigm using visual guidance of sound localization to gain insight into how the brain confronts this type of circularity. We tested two competing hypotheses. 1: The brain guides sound location learning based on the synchrony or simultaneity of auditory-visual stimuli, potentially involving a Hebbian associative mechanism. 2: The brain uses a 'guess and check' heuristic in which visual feedback that is obtained after an eye movement to a sound alters future performance, perhaps by recruiting the brain's reward-related circuitry. We assessed the effects of exposure to visual stimuli spatially mismatched from sounds on performance of an interleaved auditory-only saccade task. We found that when humans and monkeys were provided the visual stimulus asynchronously with the sound but as feedback to an auditory-guided saccade, they shifted their subsequent auditory-only performance toward the direction of the visual cue by 1.3-1.7 degrees, or 22-28% of the original 6 degree visual-auditory mismatch. In contrast when the visual stimulus was presented synchronously with the sound but extinguished too quickly to provide this feedback, there was little change in subsequent auditory-only performance. Our results suggest that the outcome of our own actions is vital to localizing sounds correctly. Contrary to previous expectations, visual calibration of auditory space does not appear to require visual-auditory associations based on synchrony/simultaneity. |
Christopher J Peck; Brian Lau; Daniel C Salzman The primate amygdala combines information about space and value Journal Article Nature Neuroscience, 16 (3), pp. 340–348, 2013. @article{Peck2013, title = {The primate amygdala combines information about space and value}, author = {Christopher J Peck and Brian Lau and Daniel C Salzman}, doi = {10.1038/nn.3328}, year = {2013}, date = {2013-01-01}, journal = {Nature Neuroscience}, volume = {16}, number = {3}, pages = {340--348}, publisher = {Nature Neuroscience 16}, abstract = {A stimulus predicting reinforcement can trigger emotional responses, such as arousal, and cognitive ones, such as increased attention toward the stimulus. Neuroscientists have long appreciated that the amygdala mediates spatially nonspecific emotional responses, but it remains unclear whether the amygdala links motivational and spatial representations. To test whether amygdala neurons encode spatial and motivational information, we presented reward-predictive cues in different spatial configurations to monkeys and assessed how these cues influenced spatial attention. Cue configuration and predicted reward magnitude modulated amygdala neural activity in a coordinated fashion. Moreover, fluctuations in activity were correlated with trial-to-trial variability in spatial attention. Thus, the amygdala integrates spatial and motivational information, which may influence the spatial allocation of cognitive resources. These results suggest that amygdala dysfunction may contribute to deficits in cognitive processes normally coordinated with emotional responses, such as the directing of attention toward the location of emotionally relevant stimuli.}, keywords = {}, pubstate = {published}, tppubtype = {article} } A stimulus predicting reinforcement can trigger emotional responses, such as arousal, and cognitive ones, such as increased attention toward the stimulus. Neuroscientists have long appreciated that the amygdala mediates spatially nonspecific emotional responses, but it remains unclear whether the amygdala links motivational and spatial representations. To test whether amygdala neurons encode spatial and motivational information, we presented reward-predictive cues in different spatial configurations to monkeys and assessed how these cues influenced spatial attention. Cue configuration and predicted reward magnitude modulated amygdala neural activity in a coordinated fashion. Moreover, fluctuations in activity were correlated with trial-to-trial variability in spatial attention. Thus, the amygdala integrates spatial and motivational information, which may influence the spatial allocation of cognitive resources. These results suggest that amygdala dysfunction may contribute to deficits in cognitive processes normally coordinated with emotional responses, such as the directing of attention toward the location of emotionally relevant stimuli. |
Chris A Rishel; Gang Huang; David J Freedman Independent category and spatial encoding in parietal cortex Journal Article Neuron, 77 (5), pp. 969–979, 2013. @article{Rishel2013, title = {Independent category and spatial encoding in parietal cortex}, author = {Chris A Rishel and Gang Huang and David J Freedman}, doi = {10.1016/j.neuron.2013.01.007}, year = {2013}, date = {2013-01-01}, journal = {Neuron}, volume = {77}, number = {5}, pages = {969--979}, publisher = {Elsevier Inc.}, abstract = {The posterior parietal cortex plays a central role in spatial functions, such as spatial attention and saccadic eye movements. However, recent work has increasingly focused on the role of parietal cortex in encoding nonspatial cognitive factors such as visual categories, learned stimulus associations, and task rules. The relationship between spatial encoding and nonspatial cognitive signals in parietal cortex, and whether cognitive signals are robustly encoded in the presence of strong spatial neuronal responses, is unknown. We directly compared nonspatial cognitive and spatial encoding in the lateral intraparietal (LIP) area by training monkeys to perform a visual categorization task during which they made saccades toward or away from LIP response fields (RFs). Here we show that strong saccade-related responses minimally influence robustly encoded category signals in LIP. This suggests that cognitive and spatial signals are encoded independently in LIP and underscores the role of parietal cortex in nonspatial cognitive functions.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The posterior parietal cortex plays a central role in spatial functions, such as spatial attention and saccadic eye movements. However, recent work has increasingly focused on the role of parietal cortex in encoding nonspatial cognitive factors such as visual categories, learned stimulus associations, and task rules. The relationship between spatial encoding and nonspatial cognitive signals in parietal cortex, and whether cognitive signals are robustly encoded in the presence of strong spatial neuronal responses, is unknown. We directly compared nonspatial cognitive and spatial encoding in the lateral intraparietal (LIP) area by training monkeys to perform a visual categorization task during which they made saccades toward or away from LIP response fields (RFs). Here we show that strong saccade-related responses minimally influence robustly encoded category signals in LIP. This suggests that cognitive and spatial signals are encoded independently in LIP and underscores the role of parietal cortex in nonspatial cognitive functions. |
Maria C Romero; Ilse C L Van Dromme; Peter Janssen The role of binocular disparity in stereoscopic images of objects in the macaque anterior intraparietal area Journal Article PLoS ONE, 8 (2), pp. 1–12, 2013. @article{Romero2013, title = {The role of binocular disparity in stereoscopic images of objects in the macaque anterior intraparietal area}, author = {Maria C Romero and Ilse C L {Van Dromme} and Peter Janssen}, doi = {10.1371/journal.pone.0055340}, year = {2013}, date = {2013-01-01}, journal = {PLoS ONE}, volume = {8}, number = {2}, pages = {1--12}, publisher = {10. 1371/journal.pone.0055340}, address = {e55340. doi}, abstract = {Neurons in the macaque Anterior Intraparietal area (AIP) encode depth structure in random-dot stimuli defined by gradients of binocular disparity, but the importance of binocular disparity in real-world objects for AIP neurons is unknown. We investigated the effect of binocular disparity on the responses of AIP neurons to images of real-world objects during passive fixation. We presented stereoscopic images of natural and man-made objects in which the disparity information was congruent or incongruent with disparity gradients present in the real-world objects, and images of the same objects where such gradients were absent. Although more than half of the AIP neurons were significantly affected by binocular disparity, the great majority of AIP neurons remained image selective even in the absence of binocular disparity. AIP neurons tended to prefer stimuli in which the depth information derived from binocular disparity was congruent with the depth information signaled by monocular depth cues, indicating that these monocular depth cues have an influence upon AIP neurons. Finally, in contrast to neurons in the inferior temporal cortex, AIP neurons do not represent images of objects in terms of categories such as animate-inanimate, but utilize representations based upon simple shape features including aspect ratio.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Neurons in the macaque Anterior Intraparietal area (AIP) encode depth structure in random-dot stimuli defined by gradients of binocular disparity, but the importance of binocular disparity in real-world objects for AIP neurons is unknown. We investigated the effect of binocular disparity on the responses of AIP neurons to images of real-world objects during passive fixation. We presented stereoscopic images of natural and man-made objects in which the disparity information was congruent or incongruent with disparity gradients present in the real-world objects, and images of the same objects where such gradients were absent. Although more than half of the AIP neurons were significantly affected by binocular disparity, the great majority of AIP neurons remained image selective even in the absence of binocular disparity. AIP neurons tended to prefer stimuli in which the depth information derived from binocular disparity was congruent with the depth information signaled by monocular depth cues, indicating that these monocular depth cues have an influence upon AIP neurons. Finally, in contrast to neurons in the inferior temporal cortex, AIP neurons do not represent images of objects in terms of categories such as animate-inanimate, but utilize representations based upon simple shape features including aspect ratio. |
Adam C Snyder; Michael J Morais; Matthew A Smith Variance in population firing rate as a measure of slow time-scale correlation Journal Article Frontiers in Computational Neuroscience, 7 , pp. 1–10, 2013. @article{Snyder2013, title = {Variance in population firing rate as a measure of slow time-scale correlation}, author = {Adam C Snyder and Michael J Morais and Matthew A Smith}, doi = {10.3389/fncom.2013.00176}, year = {2013}, date = {2013-01-01}, journal = {Frontiers in Computational Neuroscience}, volume = {7}, pages = {1--10}, abstract = {Correlated variability in the spiking responses of pairs of neurons, also known as spike count correlation, is a key indicator of functional connectivity and a critical factor in population coding. Underscoring the importance of correlation as a measure for cognitive neuroscience research is the observation that spike count correlations are not fixed, but are rather modulated by perceptual and cognitive context. Yet while this context fluctuates from moment to moment, correlation must be calculated over multiple trials. This property undermines its utility as a dependent measure for investigations of cognitive processes which fluctuate on a trial-to-trial basis, such as selective attention. A measure of functional connectivity that can be assayed on a moment-to-moment basis is needed to investigate the single-trial dynamics of populations of spiking neurons. Here, we introduce the measure of population variance in normalized firing rate for this goal. We show using mathematical analysis, computer simulations and in vivo data how population variance in normalized firing rate is inversely related to the latent correlation in the population, and how this measure can be used to reliably classify trials from different typical correlation conditions, even when firing rate is held constant. We discuss the potential advantages for using population variance in normalized firing rate as a dependent measure for both basic and applied neuroscience research.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Correlated variability in the spiking responses of pairs of neurons, also known as spike count correlation, is a key indicator of functional connectivity and a critical factor in population coding. Underscoring the importance of correlation as a measure for cognitive neuroscience research is the observation that spike count correlations are not fixed, but are rather modulated by perceptual and cognitive context. Yet while this context fluctuates from moment to moment, correlation must be calculated over multiple trials. This property undermines its utility as a dependent measure for investigations of cognitive processes which fluctuate on a trial-to-trial basis, such as selective attention. A measure of functional connectivity that can be assayed on a moment-to-moment basis is needed to investigate the single-trial dynamics of populations of spiking neurons. Here, we introduce the measure of population variance in normalized firing rate for this goal. We show using mathematical analysis, computer simulations and in vivo data how population variance in normalized firing rate is inversely related to the latent correlation in the population, and how this measure can be used to reliably classify trials from different typical correlation conditions, even when firing rate is held constant. We discuss the potential advantages for using population variance in normalized firing rate as a dependent measure for both basic and applied neuroscience research. |
Sruthi K Swaminathan; Nicolas Y Masse; David J Freedman A comparison of lateral and medial intraparietal areas during a visual categorization task Journal Article The Journal of Neuroscience, 33 (32), pp. 13157–13170, 2013. @article{Swaminathan2013, title = {A comparison of lateral and medial intraparietal areas during a visual categorization task}, author = {Sruthi K Swaminathan and Nicolas Y Masse and David J Freedman}, doi = {10.1523/JNEUROSCI.5723-12.2013}, year = {2013}, date = {2013-01-01}, journal = {The Journal of Neuroscience}, volume = {33}, number = {32}, pages = {13157--13170}, abstract = {Categorization is essential for interpreting sensory stimuli and guiding our actions. Recent studies have revealed robust neuronal category representations in the lateral intraparietal area (LIP). Here, we examine the specialization of LIP for categorization and the roles of other parietal areas by comparing LIP and the medial intraparietal area (MIP) during a visual categorization task. MIP is involved in goal-directed arm movements and visuomotor coordination but has not been implicated in non-motor cognitive functions, such as categorization. As expected, we found strong category encoding in LIP. Interestingly, we also observed category signals in MIP. However, category signals were stronger and appeared with a shorter latency in LIP than MIP. In this task, monkeys indicated whether a test stimulus was a category match to a previous sample with a manual response. Test-period activity in LIP showed category encoding and distinguished between matches and non-matches. In contrast, MIP primarily reflected the match/non-match status of test stimuli, with a strong preference for matches (which required a motor response). This suggests that, although category representations are distributed across parietal cortex, LIP and MIP play distinct roles: LIP appears more involved in the categorization process itself, whereas MIP is more closely tied to decision-related motor actions.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Categorization is essential for interpreting sensory stimuli and guiding our actions. Recent studies have revealed robust neuronal category representations in the lateral intraparietal area (LIP). Here, we examine the specialization of LIP for categorization and the roles of other parietal areas by comparing LIP and the medial intraparietal area (MIP) during a visual categorization task. MIP is involved in goal-directed arm movements and visuomotor coordination but has not been implicated in non-motor cognitive functions, such as categorization. As expected, we found strong category encoding in LIP. Interestingly, we also observed category signals in MIP. However, category signals were stronger and appeared with a shorter latency in LIP than MIP. In this task, monkeys indicated whether a test stimulus was a category match to a previous sample with a manual response. Test-period activity in LIP showed category encoding and distinguished between matches and non-matches. In contrast, MIP primarily reflected the match/non-match status of test stimuli, with a strong preference for matches (which required a motor response). This suggests that, although category representations are distributed across parietal cortex, LIP and MIP play distinct roles: LIP appears more involved in the categorization process itself, whereas MIP is more closely tied to decision-related motor actions. |
Tom Theys; Pierpaolo Pani; Johannes van Loon; Jan Goffin; Peter Janssen Three-dimensional shape coding in grasping circuits: A comparison between the anterior intraparietal area and ventral premotor area F5a Journal Article Journal of Cognitive Neuroscience, 25 (3), pp. 352–364, 2013. @article{Theys2013, title = {Three-dimensional shape coding in grasping circuits: A comparison between the anterior intraparietal area and ventral premotor area F5a}, author = {Tom Theys and Pierpaolo Pani and Johannes van Loon and Jan Goffin and Peter Janssen}, doi = {10.1162/jocn_a_00332}, year = {2013}, date = {2013-01-01}, journal = {Journal of Cognitive Neuroscience}, volume = {25}, number = {3}, pages = {352--364}, abstract = {Depth information is necessary for adjusting the hand to the three-dimensional (3-D) shape of an object to grasp it. The transformation of visual information into appropriate distal motor commands is critically dependent on the anterior intraparietal area (AIP) and the ventral premotor cortex (area F5), particularly the F5p sector. Recent studies have demonstrated that both AIP and the F5a sector of the ventral premotor cortex contain neurons that respond selectively to disparity-defined 3-D shape. To investigate the neural coding of 3-D shape and the behavioral role of 3-D shape-selective neurons in these two areas, we recorded single-cell activity in AIP and F5a during passive fixation of curved surfaces and during grasping of real-world objects. Similar to those in AIP, F5a neurons were either first- or second-order disparity selective, frequently showed selectivity for discrete approximations of smoothly curved surfaces that contained disparity discontinuities, and exhibited mostly monotonic tuning for the degree of disparity variation. Furthermore, in both areas, 3-D shape-selective neurons were colocalized with neurons that were active during grasping of real-world objects. Thus, area AIP and F5a contain highly similar representations of 3-D shape, which is consistent with the proposed transfer of object information from AIP to the motor system through the ventral premotor cortex.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Depth information is necessary for adjusting the hand to the three-dimensional (3-D) shape of an object to grasp it. The transformation of visual information into appropriate distal motor commands is critically dependent on the anterior intraparietal area (AIP) and the ventral premotor cortex (area F5), particularly the F5p sector. Recent studies have demonstrated that both AIP and the F5a sector of the ventral premotor cortex contain neurons that respond selectively to disparity-defined 3-D shape. To investigate the neural coding of 3-D shape and the behavioral role of 3-D shape-selective neurons in these two areas, we recorded single-cell activity in AIP and F5a during passive fixation of curved surfaces and during grasping of real-world objects. Similar to those in AIP, F5a neurons were either first- or second-order disparity selective, frequently showed selectivity for discrete approximations of smoothly curved surfaces that contained disparity discontinuities, and exhibited mostly monotonic tuning for the degree of disparity variation. Furthermore, in both areas, 3-D shape-selective neurons were colocalized with neurons that were active during grasping of real-world objects. Thus, area AIP and F5a contain highly similar representations of 3-D shape, which is consistent with the proposed transfer of object information from AIP to the motor system through the ventral premotor cortex. |
Mark M G Walton; Seiji Ono; Michael J Mustari Stimulation of pontine reticular formation in monkeys with strabismus Journal Article Investigative Ophthalmology & Visual Science, 54 (10), pp. 7125–7136, 2013. @article{Walton2013, title = {Stimulation of pontine reticular formation in monkeys with strabismus}, author = {Mark M G Walton and Seiji Ono and Michael J Mustari}, doi = {10.1167/iovs.13-12924}, year = {2013}, date = {2013-01-01}, journal = {Investigative Ophthalmology & Visual Science}, volume = {54}, number = {10}, pages = {7125--7136}, abstract = {PURPOSE: Saccade disconjugacy in strabismus could result from any of a number of factors, including abnormalities of eye muscles, the plant, motoneurons, near response cells, or atypical tuning of neurons in saccade-related areas of the brain. This study was designed to investigate the possibility that saccade disconjugacy in strabismus is associated with abnormalities in paramedian pontine reticular formation (PPRF). METHODS: We applied microstimulation to 22 sites in PPRF and 20 sites in abducens nucleus in three rhesus macaque monkeys (one normal, one esotrope, and one exotrope). RESULTS: When mean velocity was compared between the two eyes, a slight difference was found for 1/5 sites in the normal animal. Significant differences were found for 5/6 sites in an esotrope and 10/11 sites in an exotrope. For five sites in the strabismic monkeys, the directions of evoked movements differed by more than 40° between the two eyes. When stimulation was applied to abducens nucleus (20 sites), the ipsilateral eye moved faster for 4/6 sites in the normal animal and all nine sites in the esotrope. For the exotrope, however, the left eye always moved faster, even for three sites on the right side. For the strabismic animals, stimulation of abducens nucleus often caused a different eye to move faster than stimulation of PPRF. CONCLUSIONS: These data suggest that PPRF is organized at least partly monocularly in strabismus and that disconjugate saccades are at least partly a consequence of unbalanced saccadic commands being sent to the two eyes.}, keywords = {}, pubstate = {published}, tppubtype = {article} } PURPOSE: Saccade disconjugacy in strabismus could result from any of a number of factors, including abnormalities of eye muscles, the plant, motoneurons, near response cells, or atypical tuning of neurons in saccade-related areas of the brain. This study was designed to investigate the possibility that saccade disconjugacy in strabismus is associated with abnormalities in paramedian pontine reticular formation (PPRF). METHODS: We applied microstimulation to 22 sites in PPRF and 20 sites in abducens nucleus in three rhesus macaque monkeys (one normal, one esotrope, and one exotrope). RESULTS: When mean velocity was compared between the two eyes, a slight difference was found for 1/5 sites in the normal animal. Significant differences were found for 5/6 sites in an esotrope and 10/11 sites in an exotrope. For five sites in the strabismic monkeys, the directions of evoked movements differed by more than 40° between the two eyes. When stimulation was applied to abducens nucleus (20 sites), the ipsilateral eye moved faster for 4/6 sites in the normal animal and all nine sites in the esotrope. For the exotrope, however, the left eye always moved faster, even for three sites on the right side. For the strabismic animals, stimulation of abducens nucleus often caused a different eye to move faster than stimulation of PPRF. CONCLUSIONS: These data suggest that PPRF is organized at least partly monocularly in strabismus and that disconjugate saccades are at least partly a consequence of unbalanced saccadic commands being sent to the two eyes. |
Wael F Asaad; Navaneethan Santhanam; Steven McClellan; David J Freedman High-performance execution of psychophysical tasks with complex visual stimuli in MATLAB Journal Article Journal of Neurophysiology, 109 (1), pp. 249–260, 2013. @article{Asaad2013, title = {High-performance execution of psychophysical tasks with complex visual stimuli in MATLAB}, author = {Wael F Asaad and Navaneethan Santhanam and Steven McClellan and David J Freedman}, doi = {10.1152/jn.00527.2012}, year = {2013}, date = {2013-01-01}, journal = {Journal of Neurophysiology}, volume = {109}, number = {1}, pages = {249--260}, abstract = {Behavioral, psychological, and physiological experiments often require the ability to present sensory stimuli, monitor and record subjects' responses, interface with a wide range of devices, and precisely control the timing of events within a behavioral task. Here, we describe our recent progress developing an accessible and full-featured software system for controlling such studies using the MATLAB environment. Compared with earlier reports on this software, key new features have been implemented to allow the presentation of more complex visual stimuli, increase temporal precision, and enhance user interaction. These features greatly improve the performance of the system and broaden its applicability to a wider range of possible experiments. This report describes these new features and improvements, current limitations, and quantifies the performance of the system in a real-world experimental setting.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Behavioral, psychological, and physiological experiments often require the ability to present sensory stimuli, monitor and record subjects' responses, interface with a wide range of devices, and precisely control the timing of events within a behavioral task. Here, we describe our recent progress developing an accessible and full-featured software system for controlling such studies using the MATLAB environment. Compared with earlier reports on this software, key new features have been implemented to allow the presentation of more complex visual stimuli, increase temporal precision, and enhance user interaction. These features greatly improve the performance of the system and broaden its applicability to a wider range of possible experiments. This report describes these new features and improvements, current limitations, and quantifies the performance of the system in a real-world experimental setting. |
T C Blanchard; J M Pearson; B Y Hayden Postreward delays and systematic biases in measures of animal temporal discounting Journal Article Proceedings of the National Academy of Sciences, 110 (38), pp. 15491–15496, 2013. @article{Blanchard2013, title = {Postreward delays and systematic biases in measures of animal temporal discounting}, author = {T C Blanchard and J M Pearson and B Y Hayden}, doi = {10.1073/pnas.1310446110}, year = {2013}, date = {2013-01-01}, journal = {Proceedings of the National Academy of Sciences}, volume = {110}, number = {38}, pages = {15491--15496}, abstract = {Intertemporal choice tasks, which pit smaller/sooner rewards against larger/later ones, are frequently used to study time preferences and, by extension, impulsivity and self-control. When used in animals, many trials are strung together in sequence and an adjusting buffer is added after the smaller/sooner option to hold the total duration of each trial constant. Choices of the smaller/sooner option are not reward maximizing and so are taken to indicate that the animal is discounting future rewards. However, if animals fail to correctly factor in the duration of the postreward buffers, putative discounting behavior may instead reflect constrained reward maximization. Here, we report three results consistent with this discounting-free hypothesis. We find that (i) monkeys are insensitive to the association between the duration of postreward delays and their choices; (ii) they are sensitive to the length of postreward delays, although they greatly underestimate them; and (iii) increasing the salience of the postreward delay biases monkeys toward the larger/later option, reducing measured discounting rates. These results are incompatible with standard discounting-based accounts but are compatible with an alternative heuristic model. Our data suggest that measured intertemporal preferences in animals may not reflect impulsivity, or even mental discounting of future options, and that standard human and animal intertemporal choice tasks measure unrelated mental processes.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Intertemporal choice tasks, which pit smaller/sooner rewards against larger/later ones, are frequently used to study time preferences and, by extension, impulsivity and self-control. When used in animals, many trials are strung together in sequence and an adjusting buffer is added after the smaller/sooner option to hold the total duration of each trial constant. Choices of the smaller/sooner option are not reward maximizing and so are taken to indicate that the animal is discounting future rewards. However, if animals fail to correctly factor in the duration of the postreward buffers, putative discounting behavior may instead reflect constrained reward maximization. Here, we report three results consistent with this discounting-free hypothesis. We find that (i) monkeys are insensitive to the association between the duration of postreward delays and their choices; (ii) they are sensitive to the length of postreward delays, although they greatly underestimate them; and (iii) increasing the salience of the postreward delay biases monkeys toward the larger/later option, reducing measured discounting rates. These results are incompatible with standard discounting-based accounts but are compatible with an alternative heuristic model. Our data suggest that measured intertemporal preferences in animals may not reflect impulsivity, or even mental discounting of future options, and that standard human and animal intertemporal choice tasks measure unrelated mental processes. |
Steve W C Chang; Jean-François Gariépy; Michael L Platt Neuronal reference frames for social decisions in primate frontal cortex Journal Article Nature Neuroscience, 16 (2), pp. 243–250, 2013. @article{Chang2013, title = {Neuronal reference frames for social decisions in primate frontal cortex}, author = {Steve W C Chang and Jean-Fran{ç}ois Gariépy and Michael L Platt}, doi = {10.1007/s10914-012-9194-1}, year = {2013}, date = {2013-01-01}, journal = {Nature Neuroscience}, volume = {16}, number = {2}, pages = {243--250}, publisher = {Nature Neuroscience 16}, abstract = {Social decisions are crucial for the success of individuals and the groups that they comprise. Group members respond vicariously to benefits obtained by others, and impairments in this capacity contribute to neuropsychiatric disorders such as autism and sociopathy. We examined the manner in which neurons in three frontal cortical areas encoded the outcomes of social decisions as monkeys performed a reward-allocation task. Neurons in the orbitofrontal cortex (OFC) predominantly encoded rewards that were delivered to oneself. Neurons in the anterior cingulate gyrus (ACCg) encoded reward allocations to the other monkey, to oneself or to both. Neurons in the anterior cingulate sulcus (ACCs) signaled reward allocations to the other monkey or to no one. In this network of received (OFC) and foregone (ACCs) reward signaling, ACCg emerged as an important nexus for the computation of shared experience and social reward. Individual and species-specific variations in social decision-making might result from the relative activation and influence of these areas.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Social decisions are crucial for the success of individuals and the groups that they comprise. Group members respond vicariously to benefits obtained by others, and impairments in this capacity contribute to neuropsychiatric disorders such as autism and sociopathy. We examined the manner in which neurons in three frontal cortical areas encoded the outcomes of social decisions as monkeys performed a reward-allocation task. Neurons in the orbitofrontal cortex (OFC) predominantly encoded rewards that were delivered to oneself. Neurons in the anterior cingulate gyrus (ACCg) encoded reward allocations to the other monkey, to oneself or to both. Neurons in the anterior cingulate sulcus (ACCs) signaled reward allocations to the other monkey or to no one. In this network of received (OFC) and foregone (ACCs) reward signaling, ACCg emerged as an important nexus for the computation of shared experience and social reward. Individual and species-specific variations in social decision-making might result from the relative activation and influence of these areas. |
Chih Yang Chen; Ziad M Hafed Postmicrosaccadic enhancement of slow eye movements Journal Article The Journal of Neuroscience, 33 (12), pp. 5375–5386, 2013. @article{Chen2013, title = {Postmicrosaccadic enhancement of slow eye movements}, author = {Chih Yang Chen and Ziad M Hafed}, doi = {10.1523/JNEUROSCI.3703-12.2013}, year = {2013}, date = {2013-01-01}, journal = {The Journal of Neuroscience}, volume = {33}, number = {12}, pages = {5375--5386}, abstract = {Active sensation poses unique challenges to sensory systems because moving the sensor necessarily alters the input sensory stream. Sensory input quality is additionally compromised if the sensor moves rapidly, as during rapid eye movements, making the period immediately after the movement critical for recovering reliable sensation. Here, we studied this immediate postmovement interval for the case of microsaccades during fixation, which rapidly jitter the "sensor" exactly when it is being voluntarily stabilized to maintain clear vision. We characterized retinal-image slip in monkeys immediately after microsaccades by analyzing postmovement ocular drifts. We observed enhanced ocular drifts by up to ~28% relative to premicrosaccade levels, and for up to ~50 ms after movement end. Moreover, we used a technique to trigger full-field image motion contingent on real-time microsaccade detection, and we used the initial ocular following response to this motion as a proxy for changes in early visual motion processing caused by microsaccades. When the full-field image motion started during microsaccades, ocular following was strongly suppressed, consistent with detrimental retinal effects of the movements. However, when the motion started after microsaccades, there was up to ~73% increase in ocular following speed, suggesting an enhanced motion sensitivity. These results suggest that the interface between even the smallest possible saccades and "fixation" includes a period of faster than usual image slip, as well as an enhanced responsiveness to image motion, and that both of these phenomena need to be considered when interpreting the pervasive neural and perceptual modulations frequently observed around the time of microsaccades.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Active sensation poses unique challenges to sensory systems because moving the sensor necessarily alters the input sensory stream. Sensory input quality is additionally compromised if the sensor moves rapidly, as during rapid eye movements, making the period immediately after the movement critical for recovering reliable sensation. Here, we studied this immediate postmovement interval for the case of microsaccades during fixation, which rapidly jitter the "sensor" exactly when it is being voluntarily stabilized to maintain clear vision. We characterized retinal-image slip in monkeys immediately after microsaccades by analyzing postmovement ocular drifts. We observed enhanced ocular drifts by up to ~28% relative to premicrosaccade levels, and for up to ~50 ms after movement end. Moreover, we used a technique to trigger full-field image motion contingent on real-time microsaccade detection, and we used the initial ocular following response to this motion as a proxy for changes in early visual motion processing caused by microsaccades. When the full-field image motion started during microsaccades, ocular following was strongly suppressed, consistent with detrimental retinal effects of the movements. However, when the motion started after microsaccades, there was up to ~73% increase in ocular following speed, suggesting an enhanced motion sensitivity. These results suggest that the interface between even the smallest possible saccades and "fixation" includes a period of faster than usual image slip, as well as an enhanced responsiveness to image motion, and that both of these phenomena need to be considered when interpreting the pervasive neural and perceptual modulations frequently observed around the time of microsaccades. |
Gabriela M Costello; Dantong Zhu; Emilio Salinas; Terrence R Stanford Perceptual modulation of motor-but not visual-responses in the frontal eye field during an urgent-decision task Journal Article The Journal of Neuroscience, 33 (41), pp. 16394–16408, 2013. @article{Costello2013, title = {Perceptual modulation of motor-but not visual-responses in the frontal eye field during an urgent-decision task}, author = {Gabriela M Costello and Dantong Zhu and Emilio Salinas and Terrence R Stanford}, doi = {10.1523/JNEUROSCI.1899-13.2013}, year = {2013}, date = {2013-01-01}, journal = {The Journal of Neuroscience}, volume = {33}, number = {41}, pages = {16394--16408}, abstract = {Neuronal activity in the frontal eye field (FEF) ranges from purely motor (related to saccade production) to purely visual (related to stimulus presence). According to numerous studies, visual responses correlate strongly with early perceptual analysis of the visual scene, including the deployment of spatial attention, whereas motor responses do not. Thus, functionally, the consensus is that visually responsive FEF neurons select a target among visible objects, whereas motor-related neurons plan specific eye movements based on such earlier target selection. However, these conclusions are based on behavioral tasks that themselves promote a serial arrangement of perceptual analysis followed by motor planning. So, is the presumed functional hierarchy in FEF an intrinsic property of its circuitry or does it reflect just one possible mode of operation? We investigate this in monkeys performing a rapid-choice task in which, crucially, motor planning always starts ahead of task-critical perceptual analysis, and the two relevant spatial locations are equally informative and equally likely to be target or distracter. We find that the choice is instantiated in FEF as a competition between oculomotor plans, in agreement with model predictions. Notably, although perception strongly influences the motor neurons, it has little if any measurable impact on the visual cells; more generally, the more dominant the visual response, the weaker the perceptual modulation. The results indicate that, contrary to expectations, during rapid saccadic choices perceptual information may directly modulate ongoing saccadic plans, and this process is not contingent on prior selection of the saccadic goal by visually driven FEF responses.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Neuronal activity in the frontal eye field (FEF) ranges from purely motor (related to saccade production) to purely visual (related to stimulus presence). According to numerous studies, visual responses correlate strongly with early perceptual analysis of the visual scene, including the deployment of spatial attention, whereas motor responses do not. Thus, functionally, the consensus is that visually responsive FEF neurons select a target among visible objects, whereas motor-related neurons plan specific eye movements based on such earlier target selection. However, these conclusions are based on behavioral tasks that themselves promote a serial arrangement of perceptual analysis followed by motor planning. So, is the presumed functional hierarchy in FEF an intrinsic property of its circuitry or does it reflect just one possible mode of operation? We investigate this in monkeys performing a rapid-choice task in which, crucially, motor planning always starts ahead of task-critical perceptual analysis, and the two relevant spatial locations are equally informative and equally likely to be target or distracter. We find that the choice is instantiated in FEF as a competition between oculomotor plans, in agreement with model predictions. Notably, although perception strongly influences the motor neurons, it has little if any measurable impact on the visual cells; more generally, the more dominant the visual response, the weaker the perceptual modulation. The results indicate that, contrary to expectations, during rapid saccadic choices perceptual information may directly modulate ongoing saccadic plans, and this process is not contingent on prior selection of the saccadic goal by visually driven FEF responses. |
Michele A Cox; Michael C Schmid; Andrew J Peters; Richard C Saunders; David A Leopold; Alexander Maier Receptive field focus of visual area V4 neurons determines responses to illusory surfaces Journal Article Proceedings of the National Academy of Sciences, 110 (42), pp. 17095–17100, 2013. @article{Cox2013, title = {Receptive field focus of visual area V4 neurons determines responses to illusory surfaces}, author = {Michele A Cox and Michael C Schmid and Andrew J Peters and Richard C Saunders and David A Leopold and Alexander Maier}, doi = {10.1073/pnas.1310806110}, year = {2013}, date = {2013-01-01}, journal = {Proceedings of the National Academy of Sciences}, volume = {110}, number = {42}, pages = {17095--17100}, abstract = {Illusory figures demonstrate the visual system's ability to infer surfaces under conditions of fragmented sensory input. To investigate the role of midlevel visual area V4 in visual surface completion, we used multielectrode arrays to measure spiking responses to two types of visual stimuli: Kanizsa patterns that induce the perception of an illusory surface and physically similar control stimuli that do not. Neurons in V4 exhibited stronger and sometimes rhythmic spiking responses for the illusion-promoting configurations compared with controls. Moreover, this elevated response depended on the precise alignment of the neuron's peak visual field sensitivity (receptive field focus) with the illusory surface itself. Neurons whose receptive field focus was over adjacent inducing elements, less than 1.5° away, did not show response enhancement to the illusion. Neither receptive field sizes nor fixational eye movements could account for this effect, which was present in both single-unit signals and multiunit activity. These results suggest that the active perceptual completion of surfaces and shapes, which is a fundamental problem in natural visual experience, draws upon the selective enhancement of activity within a distinct subpopulation of neurons in cortical area V4.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Illusory figures demonstrate the visual system's ability to infer surfaces under conditions of fragmented sensory input. To investigate the role of midlevel visual area V4 in visual surface completion, we used multielectrode arrays to measure spiking responses to two types of visual stimuli: Kanizsa patterns that induce the perception of an illusory surface and physically similar control stimuli that do not. Neurons in V4 exhibited stronger and sometimes rhythmic spiking responses for the illusion-promoting configurations compared with controls. Moreover, this elevated response depended on the precise alignment of the neuron's peak visual field sensitivity (receptive field focus) with the illusory surface itself. Neurons whose receptive field focus was over adjacent inducing elements, less than 1.5° away, did not show response enhancement to the illusion. Neither receptive field sizes nor fixational eye movements could account for this effect, which was present in both single-unit signals and multiunit activity. These results suggest that the active perceptual completion of surfaces and shapes, which is a fundamental problem in natural visual experience, draws upon the selective enhancement of activity within a distinct subpopulation of neurons in cortical area V4. |
Yuwei Cui; Liu D Liu; Farhan A Khawaja; Christopher C Pack; Daniel A Butts Diverse suppressive Iinfluences in area MT and selectivity to complex motion features Journal Article The Journal of Neuroscience, 33 (42), pp. 16715–16728, 2013. @article{Cui2013c, title = {Diverse suppressive Iinfluences in area MT and selectivity to complex motion features}, author = {Yuwei Cui and Liu D Liu and Farhan A Khawaja and Christopher C Pack and Daniel A Butts}, doi = {10.1523/JNEUROSCI.0203-13.2013}, year = {2013}, date = {2013-01-01}, journal = {The Journal of Neuroscience}, volume = {33}, number = {42}, pages = {16715--16728}, abstract = {Neuronal selectivity results from both excitatory and suppressive inputs to a given neuron. Suppressive influences can often significantly modulate neuronal responses and impart novel selectivity in the context of behaviorally relevant stimuli. In this work, we use a naturalistic optic flow stimulus to explore the responses of neurons in the middle temporal area (MT) of the alert macaque monkey; these responses are interpreted using a hierarchical model that incorporates relevant nonlinear properties of upstream processing in the primary visual cortex (V1). In this stimulus context, MT neuron responses can be predicted from distinct excitatory and suppressive components. Excitation is spatially localized and matches the measured preferred direction of each neuron. Suppression is typically composed of two distinct components: (1) a directionally untuned component, which appears to play the role of surround suppression and normalization; and (2) a direction-selective component, with comparable tuning width as excitation and a distinct spatial footprint that is usually partially overlapping with excitation. The direction preference of this direction-tuned suppression varies widely across MT neurons: approximately one-third have overlapping suppression in the opposite direction as excitation, and many other neurons have suppression with similar direction preferences to excitation. There is also a population of MT neurons with orthogonally oriented suppression. We demonstrate that direction-selective suppression can impart selectivity of MT neurons to more complex velocity fields and that it can be used for improved estimation of the three-dimensional velocity of moving objects. Thus, considering MT neurons in a complex stimulus context reveals a diverse set of computations likely relevant for visual processing in natural visual contexts.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Neuronal selectivity results from both excitatory and suppressive inputs to a given neuron. Suppressive influences can often significantly modulate neuronal responses and impart novel selectivity in the context of behaviorally relevant stimuli. In this work, we use a naturalistic optic flow stimulus to explore the responses of neurons in the middle temporal area (MT) of the alert macaque monkey; these responses are interpreted using a hierarchical model that incorporates relevant nonlinear properties of upstream processing in the primary visual cortex (V1). In this stimulus context, MT neuron responses can be predicted from distinct excitatory and suppressive components. Excitation is spatially localized and matches the measured preferred direction of each neuron. Suppression is typically composed of two distinct components: (1) a directionally untuned component, which appears to play the role of surround suppression and normalization; and (2) a direction-selective component, with comparable tuning width as excitation and a distinct spatial footprint that is usually partially overlapping with excitation. The direction preference of this direction-tuned suppression varies widely across MT neurons: approximately one-third have overlapping suppression in the opposite direction as excitation, and many other neurons have suppression with similar direction preferences to excitation. There is also a population of MT neurons with orthogonally oriented suppression. We demonstrate that direction-selective suppression can impart selectivity of MT neurons to more complex velocity fields and that it can be used for improved estimation of the three-dimensional velocity of moving objects. Thus, considering MT neurons in a complex stimulus context reveals a diverse set of computations likely relevant for visual processing in natural visual contexts. |
Thomas Deffieux; Youliana Younan; Nicolas Wattiez; Mickael Tanter; Pierre Pouget; Jean François Aubry Low-intensity focused ultrasound modulates monkey visuomotor behavior Journal Article Current Biology, 23 , pp. 2430–2433, 2013. @article{Deffieux2013, title = {Low-intensity focused ultrasound modulates monkey visuomotor behavior}, author = {Thomas Deffieux and Youliana Younan and Nicolas Wattiez and Mickael Tanter and Pierre Pouget and Jean Fran{ç}ois Aubry}, doi = {10.1016/j.cub.2013.10.029}, year = {2013}, date = {2013-01-01}, journal = {Current Biology}, volume = {23}, pages = {2430--2433}, abstract = {In vivo feasibility of using low-intensity focused ultrasound (FUS) to transiently modulate the function of regional brain tissue has been recently tested in anesthetized lagomorphs [1] and rodents [2-4]. Hypothetically, ultrasonic stimulation of the brain possesses several advantages [5]: it does not necessitate surgery or genetic alteration but could ultimately confer spatial resolutions superior to other noninvasive methods. Here, we gauged the ability of noninvasive FUS to causally modulate high-level cognitive behavior. Therefore, we examined how FUS might interfere with prefrontal activity in two awake macaque rhesus monkeys that had been trained to perform an antisaccade (AS) task. We show that ultrasound significantly modulated AS latencies. Such effects proved to be dependent on FUS hemifield of stimulation (relative latency increases most for ipsilateral AS). These results are interpreted in terms of a modulation of saccade inhibition to the contralateral visual field due to the disruption of processing across the frontal eye fields. Our study demonstrates for the first time the feasibility of using FUS stimulation to causally modulate behavior in the awake nonhuman primate brain. This result supports the use of this approach to study brain function. Neurostimulation with ultrasound could be used for exploratory and therapeutic purposes noninvasively, with potentially unprecedented spatial resolution.}, keywords = {}, pubstate = {published}, tppubtype = {article} } In vivo feasibility of using low-intensity focused ultrasound (FUS) to transiently modulate the function of regional brain tissue has been recently tested in anesthetized lagomorphs [1] and rodents [2-4]. Hypothetically, ultrasonic stimulation of the brain possesses several advantages [5]: it does not necessitate surgery or genetic alteration but could ultimately confer spatial resolutions superior to other noninvasive methods. Here, we gauged the ability of noninvasive FUS to causally modulate high-level cognitive behavior. Therefore, we examined how FUS might interfere with prefrontal activity in two awake macaque rhesus monkeys that had been trained to perform an antisaccade (AS) task. We show that ultrasound significantly modulated AS latencies. Such effects proved to be dependent on FUS hemifield of stimulation (relative latency increases most for ipsilateral AS). These results are interpreted in terms of a modulation of saccade inhibition to the contralateral visual field due to the disruption of processing across the frontal eye fields. Our study demonstrates for the first time the feasibility of using FUS stimulation to causally modulate behavior in the awake nonhuman primate brain. This result supports the use of this approach to study brain function. Neurostimulation with ultrasound could be used for exploratory and therapeutic purposes noninvasively, with potentially unprecedented spatial resolution. |
Becket R Ebitz; Karli K Watson; Michael L Platt Oxytocin blunts social vigilance in the rhesus macaque Journal Article Proceedings of the National Academy of Sciences, 110 (28), pp. 11630–11635, 2013. @article{Ebitz2013, title = {Oxytocin blunts social vigilance in the rhesus macaque}, author = {Becket R Ebitz and Karli K Watson and Michael L Platt}, doi = {10.1073/pnas.1305230110}, year = {2013}, date = {2013-01-01}, journal = {Proceedings of the National Academy of Sciences}, volume = {110}, number = {28}, pages = {11630--11635}, abstract = {Exogenous application of the neuromodulatory hormone oxytocin (OT) promotes prosocial behavior and can improve social function. It is unclear, however, whether OT promotes prosocial behavior per se, or whether it facilitates social interaction by reducing a state of vigilance toward potential social threats. To disambiguate these two possibilities, we exogenously delivered OT to male rhesus macaques, which have a characteristic pattern of species-typical social vigilance, and examined their performance in three social attention tasks. We first determined that, in the absence of competing task demands or goals, OT increased attention to faces and eyes, as in humans. By contrast, OT reduced species typical social vigilance for unfamiliar, dominant, and emotional faces in two additional tasks. OT eliminated the emergence of a typical state of vigilance when dominant face images were available during a social image choice task. Moreover, OT improved performance on a reward-guided saccade task, despite salient social distractors: OT reduced the interference of unfamiliar faces, particularly emotional ones, when these faces were task irrelevant. Together, these results demonstrate that OT suppresses vigilance toward potential social threats in the rhesus macaque. We hypothesize that a basic role for OT in regulating social vigilance may have facilitated the evolution of prosocial behaviors in humans.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Exogenous application of the neuromodulatory hormone oxytocin (OT) promotes prosocial behavior and can improve social function. It is unclear, however, whether OT promotes prosocial behavior per se, or whether it facilitates social interaction by reducing a state of vigilance toward potential social threats. To disambiguate these two possibilities, we exogenously delivered OT to male rhesus macaques, which have a characteristic pattern of species-typical social vigilance, and examined their performance in three social attention tasks. We first determined that, in the absence of competing task demands or goals, OT increased attention to faces and eyes, as in humans. By contrast, OT reduced species typical social vigilance for unfamiliar, dominant, and emotional faces in two additional tasks. OT eliminated the emergence of a typical state of vigilance when dominant face images were available during a social image choice task. Moreover, OT improved performance on a reward-guided saccade task, despite salient social distractors: OT reduced the interference of unfamiliar faces, particularly emotional ones, when these faces were task irrelevant. Together, these results demonstrate that OT suppresses vigilance toward potential social threats in the rhesus macaque. We hypothesize that a basic role for OT in regulating social vigilance may have facilitated the evolution of prosocial behaviors in humans. |
Christopher D Fiorillo; Minryung R Song; Sora R Yun Multiphasic temporal dynamics in responses of midbrain dopamine neurons to appetitive and aversive stimuli Journal Article The Journal of Neuroscience, 33 (11), pp. 4710–4725, 2013. @article{Fiorillo2013, title = {Multiphasic temporal dynamics in responses of midbrain dopamine neurons to appetitive and aversive stimuli}, author = {Christopher D Fiorillo and Minryung R Song and Sora R Yun}, doi = {10.1523/JNEUROSCI.3883-12.2013}, year = {2013}, date = {2013-01-01}, journal = {The Journal of Neuroscience}, volume = {33}, number = {11}, pages = {4710--4725}, abstract = {The transient response of dopamine neurons has been described as reward prediction error (RPE), with activation or suppression by events that are better or worse than expected, respectively. However, at least a minority of neurons are activated by aversive or high-intensity stimuli, casting doubt on the generality of RPE in describing the dopamine signal. To overcome limitations of previous studies, we studied neuronal responses to a wider variety of high-intensity and aversive stimuli, and we quantified and controlled aversiveness through a choice task in which macaques sacrificed juice to avoid aversive stimuli. Whereas most previous work has portrayed the RPE as a single impulse or "phase," here we demonstrate its multiphasic temporal dynamics. Aversive or high-intensity stimuli evoked a triphasic sequence of activation-suppression-activation extending over a period of 40-700 ms. The initial activation at short latencies (40-120 ms) reflected sensory intensity. The influence of motivational value became dominant between 150 and 250 ms, with activation in the case of appetitive stimuli, and suppression in the case of aversive and neutral stimuli. The previously unreported late activation appeared to be a modest "rebound" after strong suppression. Similarly, strong activation by reward was often followed by suppression. We suggest that these "rebounds" may result from overcompensation by homeostatic mechanisms in some cells. Our results are consistent with a realistic RPE, which evolves over time through a dynamic balance of excitation and inhibition.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The transient response of dopamine neurons has been described as reward prediction error (RPE), with activation or suppression by events that are better or worse than expected, respectively. However, at least a minority of neurons are activated by aversive or high-intensity stimuli, casting doubt on the generality of RPE in describing the dopamine signal. To overcome limitations of previous studies, we studied neuronal responses to a wider variety of high-intensity and aversive stimuli, and we quantified and controlled aversiveness through a choice task in which macaques sacrificed juice to avoid aversive stimuli. Whereas most previous work has portrayed the RPE as a single impulse or "phase," here we demonstrate its multiphasic temporal dynamics. Aversive or high-intensity stimuli evoked a triphasic sequence of activation-suppression-activation extending over a period of 40-700 ms. The initial activation at short latencies (40-120 ms) reflected sensory intensity. The influence of motivational value became dominant between 150 and 250 ms, with activation in the case of appetitive stimuli, and suppression in the case of aversive and neutral stimuli. The previously unreported late activation appeared to be a modest "rebound" after strong suppression. Similarly, strong activation by reward was often followed by suppression. We suggest that these "rebounds" may result from overcompensation by homeostatic mechanisms in some cells. Our results are consistent with a realistic RPE, which evolves over time through a dynamic balance of excitation and inhibition. |
Christopher D Fiorillo; Sora R Yun; Minryung R Song Diversity and homogeneity in responses of midbrain dopamine neurons Journal Article The Journal of Neuroscience, 33 (11), pp. 4693–4709, 2013. @article{Fiorillo2013a, title = {Diversity and homogeneity in responses of midbrain dopamine neurons}, author = {Christopher D Fiorillo and Sora R Yun and Minryung R Song}, doi = {10.1523/JNEUROSCI.3886-12.2013}, year = {2013}, date = {2013-01-01}, journal = {The Journal of Neuroscience}, volume = {33}, number = {11}, pages = {4693--4709}, abstract = {Dopamine neurons of the ventral midbrain have been found to signal a reward prediction error that can mediate positive reinforcement. Despite the demonstration of modest diversity at the cellular and molecular levels, there has been little analysis of response diversity in behaving animals. Here we examine response diversity in rhesus macaques to appetitive, aversive, and neutral stimuli having relative motivational values that were measured and controlled through a choice task. First, consistent with previous studies, we observed a continuum of response variability and an apparent absence of distinct clusters in scatter plots, suggesting a lack of statistically discrete subpopulations of neurons. Second, we found that a group of " sensitive " neurons tend to be more strongly suppressed by a variety of stimuli and to be more strongly activated by juice. Third, neurons in the " ventral tier " of substantia nigra were found to have greater suppression, and a subset of these had higher baseline firing rates and late " rebound " activation after suppression. These neurons could belong to a previously identified subgroup of dopamine neurons that express high levels of H-type cation channels but lack calbindin. Fourth, neurons further rostral exhibited greater suppression. Fifth, although we observed weak activation of some neurons by aversive stimuli, this was not associated with their aversiveness. In conclusion, we find a diversity of response properties, distributed along a continuum, within what may be a single functional population of neurons signaling reward prediction error.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Dopamine neurons of the ventral midbrain have been found to signal a reward prediction error that can mediate positive reinforcement. Despite the demonstration of modest diversity at the cellular and molecular levels, there has been little analysis of response diversity in behaving animals. Here we examine response diversity in rhesus macaques to appetitive, aversive, and neutral stimuli having relative motivational values that were measured and controlled through a choice task. First, consistent with previous studies, we observed a continuum of response variability and an apparent absence of distinct clusters in scatter plots, suggesting a lack of statistically discrete subpopulations of neurons. Second, we found that a group of " sensitive " neurons tend to be more strongly suppressed by a variety of stimuli and to be more strongly activated by juice. Third, neurons in the " ventral tier " of substantia nigra were found to have greater suppression, and a subset of these had higher baseline firing rates and late " rebound " activation after suppression. These neurons could belong to a previously identified subgroup of dopamine neurons that express high levels of H-type cation channels but lack calbindin. Fourth, neurons further rostral exhibited greater suppression. Fifth, although we observed weak activation of some neurons by aversive stimuli, this was not associated with their aversiveness. In conclusion, we find a diversity of response properties, distributed along a continuum, within what may be a single functional population of neurons signaling reward prediction error. |
Benjamin Y Hayden; Jack L Gallant Working memory and decision processes in visual area V4 Journal Article Frontiers in Neuroscience, 7 , pp. 1–10, 2013. @article{Hayden2013, title = {Working memory and decision processes in visual area V4}, author = {Benjamin Y Hayden and Jack L Gallant}, doi = {10.3389/fnins.2013.00018}, year = {2013}, date = {2013-01-01}, journal = {Frontiers in Neuroscience}, volume = {7}, pages = {1--10}, publisher = {10}, address = {doi}, abstract = {Recognizing and responding to a remembered stimulus requires the coordination of perception, working memory and decision-making. To investigate the role of visual cortex in these processes, we recorded responses of single V4 neurons during performance of a delayed match-to-sample task that incorporates rapid serial visual presentation of natural images. We found that neuronal activity during the delay period after the cue but before the images depends on the identity of the remembered image and that this change persists while distractors appear. This persistent response modulation has been identified as a diagnostic criterion for putative working memory signals; our data thus suggest that working memory may involve reactivation of sensory neurons. When the remembered image reappears in the neuron's receptive field, visually evoked responses are enhanced; this match enhancement is a diagnostic criterion for decision. One model that predicts these data is the matched filter hypothesis, which holds that during search V4 neurons change their tuning so as to match the remembered cue, and thus become detectors for that image. More generally, these results suggest that V4 neurons participate in the perceptual, working memory and decision processes that are needed to perform memory-guided decision-making.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Recognizing and responding to a remembered stimulus requires the coordination of perception, working memory and decision-making. To investigate the role of visual cortex in these processes, we recorded responses of single V4 neurons during performance of a delayed match-to-sample task that incorporates rapid serial visual presentation of natural images. We found that neuronal activity during the delay period after the cue but before the images depends on the identity of the remembered image and that this change persists while distractors appear. This persistent response modulation has been identified as a diagnostic criterion for putative working memory signals; our data thus suggest that working memory may involve reactivation of sensory neurons. When the remembered image reappears in the neuron's receptive field, visually evoked responses are enhanced; this match enhancement is a diagnostic criterion for decision. One model that predicts these data is the matched filter hypothesis, which holds that during search V4 neurons change their tuning so as to match the remembered cue, and thus become detectors for that image. More generally, these results suggest that V4 neurons participate in the perceptual, working memory and decision processes that are needed to perform memory-guided decision-making. |
Sarah R Heilbronner; Michael L Platt Causal evidence of performance monitoring by neurons in posterior cingulate cortex during learning Journal Article Neuron, 80 (6), pp. 1384–1391, 2013. @article{Heilbronner2013, title = {Causal evidence of performance monitoring by neurons in posterior cingulate cortex during learning}, author = {Sarah R Heilbronner and Michael L Platt}, doi = {10.1016/j.neuron.2013.09.028}, year = {2013}, date = {2013-01-01}, journal = {Neuron}, volume = {80}, number = {6}, pages = {1384--1391}, publisher = {Elsevier Inc.}, abstract = {The posterior cingulate cortex (CGp) is a major hub of the default mode network (DMN), a set of cortical areas with high resting activity that declines during task performance. This relationship suggests that DMN activity contributes to mental processes that are antagonistic to performance. Alternatively, DMN may detect conditions under which performance is poor and marshal cognitive resources for improvement. To test this idea, we recorded activity of CGp neurons in monkeys performing a learning task while varying reward size and novelty. We found that CGp neurons responded to errors, and this activity was magnified by small reward and novel stimuli. Inactivating CGp with muscimol impaired new learning when rewards were small but had no effect when rewards were large; inactivation did not affect performance on well-learned associations. Thus, CGp, and by extension the DMN, may support learning, and possibly other cognitive processes, by monitoring performance and motivating exploration.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The posterior cingulate cortex (CGp) is a major hub of the default mode network (DMN), a set of cortical areas with high resting activity that declines during task performance. This relationship suggests that DMN activity contributes to mental processes that are antagonistic to performance. Alternatively, DMN may detect conditions under which performance is poor and marshal cognitive resources for improvement. To test this idea, we recorded activity of CGp neurons in monkeys performing a learning task while varying reward size and novelty. We found that CGp neurons responded to errors, and this activity was magnified by small reward and novel stimuli. Inactivating CGp with muscimol impaired new learning when rewards were small but had no effect when rewards were large; inactivation did not affect performance on well-learned associations. Thus, CGp, and by extension the DMN, may support learning, and possibly other cognitive processes, by monitoring performance and motivating exploration. |
Farhan A Khawaja; Liu D Liu; Christopher C Pack Responses of MST neurons to plaid stimuli Journal Article Journal of Neurophysiology, 110 (1), pp. 63–74, 2013. @article{Khawaja2013, title = {Responses of MST neurons to plaid stimuli}, author = {Farhan A Khawaja and Liu D Liu and Christopher C Pack}, doi = {10.1152/jn.00338.2012}, year = {2013}, date = {2013-01-01}, journal = {Journal of Neurophysiology}, volume = {110}, number = {1}, pages = {63--74}, abstract = {The estimation of motion information from retinal input is a fundamental function of the primate dorsal visual pathway. Previous work has shown that this function involves multiple cortical areas, with each area integrating information from its predecessors. Compared with neurons in the primary visual cortex (V1), neurons in the middle temporal (MT) area more faithfully represent the velocity of plaid stimuli, and the observation of this pattern selectivity has led to two-stage models in which MT neurons integrate the outputs of component-selective V1 neurons. Motion integration in these models is generally complemented by motion opponency, which refines velocity selectivity. Area MT projects to a third stage of motion processing, the medial superior temporal (MST) area, but surprisingly little is known about MST responses to plaid stimuli. Here we show that increased pattern selectivity in MST is associated with greater prevalence of the mechanisms implemented by two-stage MT models: Compared with MT neurons, MST neurons integrate motion components to a greater degree and exhibit evidence of stronger motion opponency. Moreover, when tested with more challenging unikinetic plaid stimuli, an appreciable percentage of MST neurons are pattern selective, while such selectivity is rare in MT. Surprisingly, increased motion integration is found in MST even for transparent plaid stimuli, which are not typically integrated perceptually. Thus the relationship between MST and MT is qualitatively similar to that between MT and V1, as repeated application of basic motion mechanisms leads to novel selectivities at each stage along the pathway.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The estimation of motion information from retinal input is a fundamental function of the primate dorsal visual pathway. Previous work has shown that this function involves multiple cortical areas, with each area integrating information from its predecessors. Compared with neurons in the primary visual cortex (V1), neurons in the middle temporal (MT) area more faithfully represent the velocity of plaid stimuli, and the observation of this pattern selectivity has led to two-stage models in which MT neurons integrate the outputs of component-selective V1 neurons. Motion integration in these models is generally complemented by motion opponency, which refines velocity selectivity. Area MT projects to a third stage of motion processing, the medial superior temporal (MST) area, but surprisingly little is known about MST responses to plaid stimuli. Here we show that increased pattern selectivity in MST is associated with greater prevalence of the mechanisms implemented by two-stage MT models: Compared with MT neurons, MST neurons integrate motion components to a greater degree and exhibit evidence of stronger motion opponency. Moreover, when tested with more challenging unikinetic plaid stimuli, an appreciable percentage of MST neurons are pattern selective, while such selectivity is rare in MT. Surprisingly, increased motion integration is found in MST even for transparent plaid stimuli, which are not typically integrated perceptually. Thus the relationship between MST and MT is qualitatively similar to that between MT and V1, as repeated application of basic motion mechanisms leads to novel selectivities at each stage along the pathway. |
Jeffrey T Klein; Michael L Platt Social information signaling by neurons in primate striatum Journal Article Current Biology, 23 , pp. 691–696, 2013. @article{Klein2013, title = {Social information signaling by neurons in primate striatum}, author = {Jeffrey T Klein and Michael L Platt}, doi = {10.1016/j.cub.2013.03.022}, year = {2013}, date = {2013-01-01}, journal = {Current Biology}, volume = {23}, pages = {691--696}, publisher = {Elsevier Ltd}, abstract = {Social decisions depend on reliable information about others. Consequently, social primates are motivated to acquire information about the identity, social status, and reproductive quality of others [1]. Neurophysiological [2] and neuroimaging [3, 4] studies implicate the striatum in the motivational control of behavior. Neuroimaging studies specifically implicate the ventromedial striatum in signaling motivational aspects of social interaction [5]. Despite this evidence, precisely how striatal neurons encode social information remains unknown. Therefore, we probed the activity of single striatal neurons in monkeys choosing between visual social information at the potential expense of fluid reward. We show for the first time that a population of neurons located primarily in medial striatum selectively signals social information. Surprisingly, representation of social information was unrelated to simultaneously expressed social preferences. A largely nonoverlapping population of neurons that was not restricted to the medial striatum signaled information about fluid reward. Our findings demonstrate that information about social context and nutritive reward are maintained largely independently in striatum, even when both influence decisions to execute a single action.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Social decisions depend on reliable information about others. Consequently, social primates are motivated to acquire information about the identity, social status, and reproductive quality of others [1]. Neurophysiological [2] and neuroimaging [3, 4] studies implicate the striatum in the motivational control of behavior. Neuroimaging studies specifically implicate the ventromedial striatum in signaling motivational aspects of social interaction [5]. Despite this evidence, precisely how striatal neurons encode social information remains unknown. Therefore, we probed the activity of single striatal neurons in monkeys choosing between visual social information at the potential expense of fluid reward. We show for the first time that a population of neurons located primarily in medial striatum selectively signals social information. Surprisingly, representation of social information was unrelated to simultaneously expressed social preferences. A largely nonoverlapping population of neurons that was not restricted to the medial striatum signaled information about fluid reward. Our findings demonstrate that information about social context and nutritive reward are maintained largely independently in striatum, even when both influence decisions to execute a single action. |
Matthew L Leavitt; Florian Pieper; Adam Sachs; Ridha Joober; Julio C Martinez-Trujillo PLoS ONE, 8 (4), pp. 1–11, 2013. @article{Leavitt2013, title = {Structure of spike count correlations reveals functional interactions between neurons in dorsolateral prefrontal cortex area 8a of behaving primates}, author = {Matthew L Leavitt and Florian Pieper and Adam Sachs and Ridha Joober and Julio C Martinez-Trujillo}, doi = {10.1371/journal.pone.0061503}, year = {2013}, date = {2013-01-01}, journal = {PLoS ONE}, volume = {8}, number = {4}, pages = {1--11}, publisher = {10. 1371/journal.pone.0061503}, address = {e61503. doi}, abstract = {Neurons within the primate dorsolateral prefrontal cortex (dlPFC) are clustered in microcolumns according to their visuospatial tuning. One issue that remains poorly investigated is how this anatomical arrangement influences functional interactions between neurons during behavior. To investigate this question we implanted 4 mm×4 mm multielectrode arrays in two macaques' dlPFC area 8a and measured spike count correlations (rsc ) between responses of simultaneously recorded neurons when animals maintained stationary gaze. Positive and negative rsc were significantly higher than predicted by chance across a wide range of inter-neuron distances (from 0.4 to 4 mm). Positive rsc were stronger between neurons with receptive fields (RFs) separated by ≤90° of angular distance and progressively decreased as a function of inter-neuron physical distance. Negative rsc were stronger between neurons with RFs separated by textgreater90° and increased as a function of inter-neuron distance. Our results show that short- and long-range functional interactions between dlPFC neurons depend on the physical distance between them and the relationship between their visuospatial tuning preferences. Neurons with similar visuospatial tuning show positive rsc that decay with inter-neuron distance, suggestive of excitatory interactions within and between adjacent microcolumns. Neurons with dissimilar tuning from spatially segregated microcolumns show negative rsc that increase with inter-neuron distance, suggestive of inhibitory interactions. This pattern of results shows that functional interactions between prefrontal neurons closely follow the pattern of connectivity reported in anatomical studies. Such interactions may be important for the role of the prefrontal cortex in the allocation of attention to targets in the presence of competing distracters.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Neurons within the primate dorsolateral prefrontal cortex (dlPFC) are clustered in microcolumns according to their visuospatial tuning. One issue that remains poorly investigated is how this anatomical arrangement influences functional interactions between neurons during behavior. To investigate this question we implanted 4 mm×4 mm multielectrode arrays in two macaques' dlPFC area 8a and measured spike count correlations (rsc ) between responses of simultaneously recorded neurons when animals maintained stationary gaze. Positive and negative rsc were significantly higher than predicted by chance across a wide range of inter-neuron distances (from 0.4 to 4 mm). Positive rsc were stronger between neurons with receptive fields (RFs) separated by ≤90° of angular distance and progressively decreased as a function of inter-neuron physical distance. Negative rsc were stronger between neurons with RFs separated by textgreater90° and increased as a function of inter-neuron distance. Our results show that short- and long-range functional interactions between dlPFC neurons depend on the physical distance between them and the relationship between their visuospatial tuning preferences. Neurons with similar visuospatial tuning show positive rsc that decay with inter-neuron distance, suggestive of excitatory interactions within and between adjacent microcolumns. Neurons with dissimilar tuning from spatially segregated microcolumns show negative rsc that increase with inter-neuron distance, suggestive of inhibitory interactions. This pattern of results shows that functional interactions between prefrontal neurons closely follow the pattern of connectivity reported in anatomical studies. Such interactions may be important for the role of the prefrontal cortex in the allocation of attention to targets in the presence of competing distracters. |
Kyoung-Min Lee; Kyung-Ha Ahn The frontal eye fields limit the capacity of visual short-term memory in rhesus monkeys Journal Article PLoS ONE, 8 (3), pp. 1–11, 2013. @article{Lee2013bb, title = {The frontal eye fields limit the capacity of visual short-term memory in rhesus monkeys}, author = {Kyoung-Min Lee and Kyung-Ha Ahn}, doi = {10.1371/journal.pone.0059606}, year = {2013}, date = {2013-01-01}, journal = {PLoS ONE}, volume = {8}, number = {3}, pages = {1--11}, publisher = {10. 1371/journal.pone.0059606}, address = {e59606. doi}, abstract = {The frontal eye fields (FEF) in rhesus monkeys have been implicated in visual short-term memory (VSTM) as well as control of visual attention. Here we examined the importance of the area in the VSTM capacity and the relationship between VSTM and attention, using the chemical inactivation technique and multi-target saccade tasks with or without the need of target-location memory. During FEF inactivation, serial saccades to targets defined by color contrast were unaffected, but saccades relying on short-term memory were impaired when the target count was at the capacity limit of VSTM. The memory impairment was specific to the FEF-coded retinotopic locations, and subject to competition among targets distributed across visual fields. These results together suggest that the FEF plays a crucial role during the entry of information into VSTM, by enabling attention deployment on targets to be remembered. In this view, the memory capacity results from the limited availability of attentional resources provided by FEF: The FEF can concurrently maintain only a limited number of activations to register the targets into memory. When lesions render part of the area unavailable for activation, the number would decrease, further reducing the capacity of VSTM.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The frontal eye fields (FEF) in rhesus monkeys have been implicated in visual short-term memory (VSTM) as well as control of visual attention. Here we examined the importance of the area in the VSTM capacity and the relationship between VSTM and attention, using the chemical inactivation technique and multi-target saccade tasks with or without the need of target-location memory. During FEF inactivation, serial saccades to targets defined by color contrast were unaffected, but saccades relying on short-term memory were impaired when the target count was at the capacity limit of VSTM. The memory impairment was specific to the FEF-coded retinotopic locations, and subject to competition among targets distributed across visual fields. These results together suggest that the FEF plays a crucial role during the entry of information into VSTM, by enabling attention deployment on targets to be remembered. In this view, the memory capacity results from the limited availability of attentional resources provided by FEF: The FEF can concurrently maintain only a limited number of activations to register the targets into memory. When lesions render part of the area unavailable for activation, the number would decrease, further reducing the capacity of VSTM. |
Masayuki Matsumoto; Masahiko Takada Distinct representations of cognitive and motivational signals in midbrain dopamine neurons Journal Article Neuron, 79 (5), pp. 1011–1024, 2013. @article{Matsumoto2013, title = {Distinct representations of cognitive and motivational signals in midbrain dopamine neurons}, author = {Masayuki Matsumoto and Masahiko Takada}, doi = {10.1016/j.neuron.2013.07.002}, year = {2013}, date = {2013-01-01}, journal = {Neuron}, volume = {79}, number = {5}, pages = {1011--1024}, publisher = {Elsevier Inc.}, abstract = {Dopamine is essential to cognitive functions. However, despite abundant studies demonstrating that dopamine neuron activity is related to reinforcement and motivation, little is known about what signals dopamine neurons convey to promote cognitive processing. We therefore examined dopamine neuron activity in monkeys performing a delayed matching-to-sample task that required working memory and visual search. We found that dopamine neurons responded to task events associated with cognitive operations. A subset of dopamine neurons were activated by visual stimuli if the monkey had to store the stimuli in working memory. These neurons were located dorsolaterally in the substantia nigra pars compacta, whereas ventromedial dopamine neurons, some in the ventral tegmental area, represented reward prediction signals. Furthermore, dopamine neurons monitored visual search performance, becoming active when the monkey made an internal judgment that the search was successfully completed. Our findings suggest an anatomical gradient of dopamine signals along the dorsolateral-ventromedial axis of the ventral midbrain.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Dopamine is essential to cognitive functions. However, despite abundant studies demonstrating that dopamine neuron activity is related to reinforcement and motivation, little is known about what signals dopamine neurons convey to promote cognitive processing. We therefore examined dopamine neuron activity in monkeys performing a delayed matching-to-sample task that required working memory and visual search. We found that dopamine neurons responded to task events associated with cognitive operations. A subset of dopamine neurons were activated by visual stimuli if the monkey had to store the stimuli in working memory. These neurons were located dorsolaterally in the substantia nigra pars compacta, whereas ventromedial dopamine neurons, some in the ventral tegmental area, represented reward prediction signals. Furthermore, dopamine neurons monitored visual search performance, becoming active when the monkey made an internal judgment that the search was successfully completed. Our findings suggest an anatomical gradient of dopamine signals along the dorsolateral-ventromedial axis of the ventral midbrain. |
Richard McFarland; Hettie Roebuck; Yin Yan; Bonaventura Majolo; Wu Li; Kun Guo Social interactions through the eyes of macaques and humans Journal Article PLoS ONE, 8 (2), pp. 1–11, 2013. @article{McFarland2013, title = {Social interactions through the eyes of macaques and humans}, author = {Richard McFarland and Hettie Roebuck and Yin Yan and Bonaventura Majolo and Wu Li and Kun Guo}, doi = {10.1371/journal.pone.0056437}, year = {2013}, date = {2013-01-01}, journal = {PLoS ONE}, volume = {8}, number = {2}, pages = {1--11}, publisher = {10. 1371/journal.pone.0056437}, address = {e56437. doi}, abstract = {Group-living primates frequently interact with each other to maintain social bonds as well as to compete for valuable resources. Observing such social interactions between group members provides individuals with essential information (e.g. on the fighting ability or altruistic attitude of group companions) to guide their social tactics and choice of social partners. This process requires individuals to selectively attend to the most informative content within a social scene. It is unclear how non-human primates allocate attention to social interactions in different contexts, and whether they share similar patterns of social attention to humans. Here we compared the gaze behaviour of rhesus macaques and humans when free-viewing the same set of naturalistic images. The images contained positive or negative social interactions between two conspecifics of different phylogenetic distance from the observer; i.e. affiliation or aggression exchanged by two humans, rhesus macaques, Barbary macaques, baboons or lions. Monkeys directed a variable amount of gaze at the two conspecific individuals in the images according to their roles in the interaction (i.e. giver or receiver of affiliation/aggression). Their gaze distribution to non-conspecific individuals was systematically varied according to the viewed species and the nature of interactions, suggesting a contribution of both prior experience and innate bias in guiding social attention. Furthermore, the monkeys' gaze behavior was qualitatively similar to that of humans, especially when viewing negative interactions. Detailed analysis revealed that both species directed more gaze at the face than the body region when inspecting individuals, and attended more to the body region in negative than in positive social interactions. Our study suggests that monkeys and humans share a similar pattern of role-sensitive, species- and context-dependent social attention, implying a homologous cognitive mechanism of social attention between rhesus macaques and humans.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Group-living primates frequently interact with each other to maintain social bonds as well as to compete for valuable resources. Observing such social interactions between group members provides individuals with essential information (e.g. on the fighting ability or altruistic attitude of group companions) to guide their social tactics and choice of social partners. This process requires individuals to selectively attend to the most informative content within a social scene. It is unclear how non-human primates allocate attention to social interactions in different contexts, and whether they share similar patterns of social attention to humans. Here we compared the gaze behaviour of rhesus macaques and humans when free-viewing the same set of naturalistic images. The images contained positive or negative social interactions between two conspecifics of different phylogenetic distance from the observer; i.e. affiliation or aggression exchanged by two humans, rhesus macaques, Barbary macaques, baboons or lions. Monkeys directed a variable amount of gaze at the two conspecific individuals in the images according to their roles in the interaction (i.e. giver or receiver of affiliation/aggression). Their gaze distribution to non-conspecific individuals was systematically varied according to the viewed species and the nature of interactions, suggesting a contribution of both prior experience and innate bias in guiding social attention. Furthermore, the monkeys' gaze behavior was qualitatively similar to that of humans, especially when viewing negative interactions. Detailed analysis revealed that both species directed more gaze at the face than the body region when inspecting individuals, and attended more to the body region in negative than in positive social interactions. Our study suggests that monkeys and humans share a similar pattern of role-sensitive, species- and context-dependent social attention, implying a homologous cognitive mechanism of social attention between rhesus macaques and humans. |
Patrick J Mineault; Theodoros P Zanos; Christopher C Pack Local field potentials reflect multiple spatial scales in V4 Journal Article Frontiers in Computational Neuroscience, 7 , pp. 1–15, 2013. @article{Mineault2013, title = {Local field potentials reflect multiple spatial scales in V4}, author = {Patrick J Mineault and Theodoros P Zanos and Christopher C Pack}, doi = {10.3389/fncom.2013.00021}, year = {2013}, date = {2013-01-01}, journal = {Frontiers in Computational Neuroscience}, volume = {7}, pages = {1--15}, publisher = {10}, address = {doi}, abstract = {Local field potentials (LFP) reflect the properties of neuronal circuits or columns recorded in a volume around a microelectrode (Buzsáki et al., 2012). The extent of this integration volume has been a subject of some debate, with estimates ranging from a few hundred microns (Katzner et al., 2009; Xing et al., 2009) to several millimeters (Kreiman et al., 2006). We estimated receptive fields (RFs) of multi-unit activity (MUA) and LFPs at an intermediate level of visual processing, in area V4 of two macaques. The spatial structure of LFP receptive fields varied greatly as a function of time lag following stimulus onset, with the retinotopy of LFPs matching that of MUAs at a restricted set of time lags. A model-based analysis of the LFPs allowed us to recover two distinct stimulus-triggered components: an MUA-like retinotopic component that originated in a small volume around the microelectrodes (~350 $mu$m), and a second component that was shared across the entire V4 region; this second component had tuning properties unrelated to those of the MUAs. Our results suggest that the LFP reflects neural activity across multiple spatial scales, which both complicates its interpretation and offers new opportunities for investigating the large-scale structure of network processing.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Local field potentials (LFP) reflect the properties of neuronal circuits or columns recorded in a volume around a microelectrode (Buzsáki et al., 2012). The extent of this integration volume has been a subject of some debate, with estimates ranging from a few hundred microns (Katzner et al., 2009; Xing et al., 2009) to several millimeters (Kreiman et al., 2006). We estimated receptive fields (RFs) of multi-unit activity (MUA) and LFPs at an intermediate level of visual processing, in area V4 of two macaques. The spatial structure of LFP receptive fields varied greatly as a function of time lag following stimulus onset, with the retinotopy of LFPs matching that of MUAs at a restricted set of time lags. A model-based analysis of the LFPs allowed us to recover two distinct stimulus-triggered components: an MUA-like retinotopic component that originated in a small volume around the microelectrodes (~350 $mu$m), and a second component that was shared across the entire V4 region; this second component had tuning properties unrelated to those of the MUAs. Our results suggest that the LFP reflects neural activity across multiple spatial scales, which both complicates its interpretation and offers new opportunities for investigating the large-scale structure of network processing. |
2012 |
Bryan J Hansen; Mircea I Chelaru; Valentin Dragoi Correlated variability in laminar cortical circuits Journal Article Neuron, 76 (3), pp. 590–602, 2012. @article{Hansen2012, title = {Correlated variability in laminar cortical circuits}, author = {Bryan J Hansen and Mircea I Chelaru and Valentin Dragoi}, doi = {10.1016/j.neuron.2012.08.029}, year = {2012}, date = {2012-01-01}, journal = {Neuron}, volume = {76}, number = {3}, pages = {590--602}, publisher = {Elsevier Inc.}, abstract = {Despite the fact that strong trial-to-trial correlated variability in responses has been reported in many cortical areas, recent evidence suggests that neuronal correlations are much lower than previously thought. Here, we used multicontact laminar probes to revisit the issue of correlated variability in primary visual (V1) cortical circuits. We found that correlations between neurons depend strongly on local network context-whereas neurons in the input (granular) layers showed virtually no correlated variability, neurons in the output layers (supragranular and infragranular) exhibited strong correlations. The laminar dependence of noise correlations is consistent with recurrent models in which neurons in the granular layer receive intracortical inputs from nearby cells, whereas supragranular and infragranular layer neurons receive inputs over larger distances. Contrary to expectation that the output cortical layers encode stimulus information most accurately, we found that the input network offers superior discrimination performance compared to the output networks.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Despite the fact that strong trial-to-trial correlated variability in responses has been reported in many cortical areas, recent evidence suggests that neuronal correlations are much lower than previously thought. Here, we used multicontact laminar probes to revisit the issue of correlated variability in primary visual (V1) cortical circuits. We found that correlations between neurons depend strongly on local network context-whereas neurons in the input (granular) layers showed virtually no correlated variability, neurons in the output layers (supragranular and infragranular) exhibited strong correlations. The laminar dependence of noise correlations is consistent with recurrent models in which neurons in the granular layer receive intracortical inputs from nearby cells, whereas supragranular and infragranular layer neurons receive inputs over larger distances. Contrary to expectation that the output cortical layers encode stimulus information most accurately, we found that the input network offers superior discrimination performance compared to the output networks. |
E B Issa; J J DiCarlo Precedence of the eye region in neural processing of faces Journal Article The Journal of Neuroscience, 32 (47), pp. 16666–16682, 2012. @article{Issa2012, title = {Precedence of the eye region in neural processing of faces}, author = {E B Issa and J J DiCarlo}, doi = {10.1523/JNEUROSCI.2391-12.2012}, year = {2012}, date = {2012-01-01}, journal = {The Journal of Neuroscience}, volume = {32}, number = {47}, pages = {16666--16682}, abstract = {Functional magnetic resonance imaging (fMRI) has revealed multiple subregions in monkey inferior temporal cortex (IT) that are selective for images of faces over other objects. The earliest of these subregions, the posterior lateral face patch (PL), has not been studied previously at the neurophysiological level. Perhaps not surprisingly, we found that PL contains a high concentration of "face-selective" cells when tested with standard image sets comparable to those used previously to define the region at the level of fMRI. However, we here report that several different image sets and analytical approaches converge to show that nearly all face-selective PL cells are driven by the presence of a single eye in the context of a face outline. Most strikingly, images containing only an eye, even when incorrectly positioned in an outline, drove neurons nearly as well as full-face images, and face images lacking only this feature led to longer latency responses. Thus, bottom-up face processing is relatively local and linearly integrates features-consistent with parts-based models-grounding investigation of how the presence of a face is first inferred in the IT face processing hierarchy.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Functional magnetic resonance imaging (fMRI) has revealed multiple subregions in monkey inferior temporal cortex (IT) that are selective for images of faces over other objects. The earliest of these subregions, the posterior lateral face patch (PL), has not been studied previously at the neurophysiological level. Perhaps not surprisingly, we found that PL contains a high concentration of "face-selective" cells when tested with standard image sets comparable to those used previously to define the region at the level of fMRI. However, we here report that several different image sets and analytical approaches converge to show that nearly all face-selective PL cells are driven by the presence of a single eye in the context of a face outline. Most strikingly, images containing only an eye, even when incorrectly positioned in an outline, drove neurons nearly as well as full-face images, and face images lacking only this feature led to longer latency responses. Thus, bottom-up face processing is relatively local and linearly integrates features-consistent with parts-based models-grounding investigation of how the presence of a face is first inferred in the IT face processing hierarchy. |
Daniel L Kimmel; Dagem Mammo; William T Newsome Tracking the eye non-invasively: Simultaneous comparison of the scleral search coil and optical tracking techniques in the macaque monkey Journal Article Frontiers in Behavioral Neuroscience, 6 , pp. 1–17, 2012. @article{Kimmel2012, title = {Tracking the eye non-invasively: Simultaneous comparison of the scleral search coil and optical tracking techniques in the macaque monkey}, author = {Daniel L Kimmel and Dagem Mammo and William T Newsome}, doi = {10.3389/fnbeh.2012.00049}, year = {2012}, date = {2012-01-01}, journal = {Frontiers in Behavioral Neuroscience}, volume = {6}, pages = {1--17}, publisher = {10}, address = {doi}, abstract = {From human perception to primate neurophysiology, monitoring eye position is critical to the study of vision, attention, oculomotor control, and behavior. Two principal techniques for the precise measurement of eye position-the long-standing sclera-embedded search coil and more recent optical tracking techniques-are in use in various laboratories, but no published study compares the performance of the two methods simultaneously in the same primates. Here we compare two popular systems-a sclera-embedded search coil from C-N-C Engineering and the EyeLink 1000 optical system from SR Research-by recording simultaneously from the same eye in the macaque monkey while the animal performed a simple oculomotor task. We found broad agreement between the two systems, particularly in positional accuracy during fixation, measurement of saccade amplitude, detection of fixational saccades, and sensitivity to subtle changes in eye position from trial to trial. Nonetheless, certain discrepancies persist, particularly elevated saccade peak velocities, post-saccadic ringing, influence of luminance change on reported position, and greater sample-to-sample variation in the optical system. Our study shows that optical performance now rivals that of the search coil, rendering optical systems appropriate for many if not most applications. This finding is consequential, especially for animal subjects, because the optical systems do not require invasive surgery for implantation and repair of search coils around the eye. Our data also allow laboratories using the optical system in human subjects to assess the strengths and limitations of the technique for their own applications.}, keywords = {}, pubstate = {published}, tppubtype = {article} } From human perception to primate neurophysiology, monitoring eye position is critical to the study of vision, attention, oculomotor control, and behavior. Two principal techniques for the precise measurement of eye position-the long-standing sclera-embedded search coil and more recent optical tracking techniques-are in use in various laboratories, but no published study compares the performance of the two methods simultaneously in the same primates. Here we compare two popular systems-a sclera-embedded search coil from C-N-C Engineering and the EyeLink 1000 optical system from SR Research-by recording simultaneously from the same eye in the macaque monkey while the animal performed a simple oculomotor task. We found broad agreement between the two systems, particularly in positional accuracy during fixation, measurement of saccade amplitude, detection of fixational saccades, and sensitivity to subtle changes in eye position from trial to trial. Nonetheless, certain discrepancies persist, particularly elevated saccade peak velocities, post-saccadic ringing, influence of luminance change on reported position, and greater sample-to-sample variation in the optical system. Our study shows that optical performance now rivals that of the search coil, rendering optical systems appropriate for many if not most applications. This finding is consequential, especially for animal subjects, because the optical systems do not require invasive surgery for implantation and repair of search coils around the eye. Our data also allow laboratories using the optical system in human subjects to assess the strengths and limitations of the technique for their own applications. |
Christiaan P Klink; Anna Oleksiak; Martin J M Lankheet; Richard J A van Wezel Intermittent stimulus presentation stabilizes neuronal responses in macaque area MT Journal Article Journal of Neurophysiology, 108 (8), pp. 2101–2114, 2012. @article{Klink2012, title = {Intermittent stimulus presentation stabilizes neuronal responses in macaque area MT}, author = {Christiaan P Klink and Anna Oleksiak and Martin J M Lankheet and Richard J A van Wezel}, doi = {10.1152/jn.00252.2012}, year = {2012}, date = {2012-01-01}, journal = {Journal of Neurophysiology}, volume = {108}, number = {8}, pages = {2101--2114}, abstract = {Repeated stimulation impacts neuronal responses. Here we show how response characteristics of sensory neurons in macaque visual cortex are influenced by the duration of the interruptions during intermittent stimulus presentation. Besides effects on response magnitude consistent with neuronal ad- aptation, the response variability was also systematically influenced. Spike rate variability in motion-sensitive area MT decreased when interruption durations were systematically increased from 250 to 2,000 ms. Activity fluctuations between subsequent trials and Fano factors over full response sequences were both lower with longer interruptions, while spike timing patterns became more regular. These variability changes partially depended on the response magnitude, but another significant effect that was uncorrelated with adaptation-in- duced changes in response magnitude was also present. Reduced response variability was furthermore accompanied by changes in spike-field coherence, pointing to the possibility that reduced spiking variability results from interactions in the local cortical network. While neuronal response stabilization may be a general effect of repeated sensory stimulation, we discuss its potential link with the phenomenon of perceptual stabilization of ambiguous stimuli as a result of interrupted presentation.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Repeated stimulation impacts neuronal responses. Here we show how response characteristics of sensory neurons in macaque visual cortex are influenced by the duration of the interruptions during intermittent stimulus presentation. Besides effects on response magnitude consistent with neuronal ad- aptation, the response variability was also systematically influenced. Spike rate variability in motion-sensitive area MT decreased when interruption durations were systematically increased from 250 to 2,000 ms. Activity fluctuations between subsequent trials and Fano factors over full response sequences were both lower with longer interruptions, while spike timing patterns became more regular. These variability changes partially depended on the response magnitude, but another significant effect that was uncorrelated with adaptation-in- duced changes in response magnitude was also present. Reduced response variability was furthermore accompanied by changes in spike-field coherence, pointing to the possibility that reduced spiking variability results from interactions in the local cortical network. While neuronal response stabilization may be a general effect of repeated sensory stimulation, we discuss its potential link with the phenomenon of perceptual stabilization of ambiguous stimuli as a result of interrupted presentation. |
Anders Ledberg; Anna Montagnini; Richard Coppola; Steven L Bressler Reduced variability of ongoing and evoked cortical activity leads to improved behavioral performance Journal Article PLoS ONE, 7 (8), pp. 1–10, 2012. @article{Ledberg2012, title = {Reduced variability of ongoing and evoked cortical activity leads to improved behavioral performance}, author = {Anders Ledberg and Anna Montagnini and Richard Coppola and Steven L Bressler}, doi = {10.1371/journal.pone.0043166}, year = {2012}, date = {2012-01-01}, journal = {PLoS ONE}, volume = {7}, number = {8}, pages = {1--10}, publisher = {10. 1371/journal.pone.0043166}, address = {e43166. doi}, abstract = {Sensory responses of the brain are known to be highly variable, but the origin and functional relevance of this variability have long remained enigmatic. Using the variable foreperiod of a visual discrimination task to assess variability in the primate cerebral cortex, we report that visual evoked response variability is not only tied to variability in ongoing cortical activity, but also predicts mean response time. We used cortical local field potentials, simultaneously recorded from widespread cortical areas, to gauge both ongoing and visually evoked activity. Trial-to-trial variability of sensory evoked responses was strongly modulated by foreperiod duration and correlated both with the cortical variability before stimulus onset as well as with response times. In a separate set of experiments we probed the relation between small saccadic eye movements, foreperiod duration and manual response times. The rate of eye movements was modulated by foreperiod duration and eye position variability was positively correlated with response times. Our results indicate that when the time of a sensory stimulus is predictable, reduction in cortical variability before the stimulus can improve normal behavioral function that depends on the stimulus.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Sensory responses of the brain are known to be highly variable, but the origin and functional relevance of this variability have long remained enigmatic. Using the variable foreperiod of a visual discrimination task to assess variability in the primate cerebral cortex, we report that visual evoked response variability is not only tied to variability in ongoing cortical activity, but also predicts mean response time. We used cortical local field potentials, simultaneously recorded from widespread cortical areas, to gauge both ongoing and visually evoked activity. Trial-to-trial variability of sensory evoked responses was strongly modulated by foreperiod duration and correlated both with the cortical variability before stimulus onset as well as with response times. In a separate set of experiments we probed the relation between small saccadic eye movements, foreperiod duration and manual response times. The rate of eye movements was modulated by foreperiod duration and eye position variability was positively correlated with response times. Our results indicate that when the time of a sensory stimulus is predictable, reduction in cortical variability before the stimulus can improve normal behavioral function that depends on the stimulus. |
Kyoung-Min Lee; Kyung-Ha Ahn; Edward L Keller Saccade generation by the frontal eye fields in Rhesus monkeys is separable from visual detection and bottom-up attention shift Journal Article PLoS ONE, 7 (6), pp. 1–8, 2012. @article{Lee2012a, title = {Saccade generation by the frontal eye fields in Rhesus monkeys is separable from visual detection and bottom-up attention shift}, author = {Kyoung-Min Lee and Kyung-Ha Ahn and Edward L Keller}, doi = {10.1371/journal.pone.0039886}, year = {2012}, date = {2012-01-01}, journal = {PLoS ONE}, volume = {7}, number = {6}, pages = {1--8}, publisher = {10. 1371/journal.pone.0039886}, address = {e39886. doi}, abstract = {The frontal eye fields (FEF), originally identified as an oculomotor cortex, have also been implicated in perceptual functions, such as constructing a visual saliency map and shifting visual attention. Further dissecting the area's role in the transformation from visual input to oculomotor command has been difficult because of spatial confounding between stimuli and responses and consequently between intermediate cognitive processes, such as attention shift and saccade preparation. Here we developed two tasks in which the visual stimulus and the saccade response were dissociated in space (the extended memory-guided saccade task), and bottom-up attention shift and saccade target selection were independent (the four-alternative delayed saccade task). Reversible inactivation of the FEF in rhesus monkeys disrupted, as expected, contralateral memory-guided saccades, but visual detection was demonstrated to be intact at the same field. Moreover, saccade behavior was impaired when a bottom-up shift of attention was not a prerequisite for saccade target selection, indicating that the inactivation effect was independent of the previously reported dysfunctions in bottom-up attention control. These findings underscore the motor aspect of the area's functions, especially in situations where saccades are generated by internal cognitive processes, including visual short-term memory and long-term associative memory.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The frontal eye fields (FEF), originally identified as an oculomotor cortex, have also been implicated in perceptual functions, such as constructing a visual saliency map and shifting visual attention. Further dissecting the area's role in the transformation from visual input to oculomotor command has been difficult because of spatial confounding between stimuli and responses and consequently between intermediate cognitive processes, such as attention shift and saccade preparation. Here we developed two tasks in which the visual stimulus and the saccade response were dissociated in space (the extended memory-guided saccade task), and bottom-up attention shift and saccade target selection were independent (the four-alternative delayed saccade task). Reversible inactivation of the FEF in rhesus monkeys disrupted, as expected, contralateral memory-guided saccades, but visual detection was demonstrated to be intact at the same field. Moreover, saccade behavior was impaired when a bottom-up shift of attention was not a prerequisite for saccade target selection, indicating that the inactivation effect was independent of the previously reported dysfunctions in bottom-up attention control. These findings underscore the motor aspect of the area's functions, especially in situations where saccades are generated by internal cognitive processes, including visual short-term memory and long-term associative memory. |
Patrick J Mineault; Farhan A Khawaja; Daniel A Butts; Christopher C Pack Hierarchical processing of complex motion along the primate dorsal visual pathway Journal Article Proceedings of the National Academy of Sciences, 109 (16), pp. E972–E980, 2012. @article{Mineault2012, title = {Hierarchical processing of complex motion along the primate dorsal visual pathway}, author = {Patrick J Mineault and Farhan A Khawaja and Daniel A Butts and Christopher C Pack}, doi = {10.1073/pnas.1115685109}, year = {2012}, date = {2012-01-01}, journal = {Proceedings of the National Academy of Sciences}, volume = {109}, number = {16}, pages = {E972--E980}, publisher = {109, E972-E980}, abstract = {Neurons in the medial superior temporal (MST) area of the primate visual cortex respond selectively to complex motion patterns defined by expansion, rotation, and deformation. Consequently they are often hypothesized to be involved in important behavioral functions, such as encoding the velocities of moving objects and surfaces relative to the observer. However, the computations underlying such selectivity are unknown. In this work we have developed a unique, naturalistic motion stimulus and used it to probe the complex selectivity of MST neurons. The resulting data were then used to estimate the properties of the feed-forward inputs to each neuron. This analysis yielded models that successfully accounted for much of the observed stimulus selectivity, provided that the inputs were combined via a nonlinear integration mechanism that approximates a multiplicative interaction among MST inputs. In simulations we found that this type of integration has the functional role of improving estimates of the 3D velocity of moving objects. As this computation is of general utility for detecting complex stimulus features, we suggest that it may represent a fundamental aspect of hierarchical sensory processing.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Neurons in the medial superior temporal (MST) area of the primate visual cortex respond selectively to complex motion patterns defined by expansion, rotation, and deformation. Consequently they are often hypothesized to be involved in important behavioral functions, such as encoding the velocities of moving objects and surfaces relative to the observer. However, the computations underlying such selectivity are unknown. In this work we have developed a unique, naturalistic motion stimulus and used it to probe the complex selectivity of MST neurons. The resulting data were then used to estimate the properties of the feed-forward inputs to each neuron. This analysis yielded models that successfully accounted for much of the observed stimulus selectivity, provided that the inputs were combined via a nonlinear integration mechanism that approximates a multiplicative interaction among MST inputs. In simulations we found that this type of integration has the functional role of improving estimates of the 3D velocity of moving objects. As this computation is of general utility for detecting complex stimulus features, we suggest that it may represent a fundamental aspect of hierarchical sensory processing. |
Ryan E B Mruczek; David L Sheinberg Stimulus selectivity and response latency in putative inhibitory and excitatory neurons of the primate inferior temporal cortex Journal Article Journal of Neurophysiology, 108 (10), pp. 2725–2736, 2012. @article{Mruczek2012, title = {Stimulus selectivity and response latency in putative inhibitory and excitatory neurons of the primate inferior temporal cortex}, author = {Ryan E B Mruczek and David L Sheinberg}, doi = {10.1152/jn.00618.2012}, year = {2012}, date = {2012-01-01}, journal = {Journal of Neurophysiology}, volume = {108}, number = {10}, pages = {2725--2736}, abstract = {The cerebral cortex is composed of many distinct classes of neurons. Numerous studies have demonstrated corresponding differences in neuronal properties across cell types, but these comparisons have largely been limited to conditions outside of awake, behaving animals. Thus the functional role of the various cell types is not well understood. Here, we investigate differences in the functional properties of two widespread and broad classes of cells in inferior temporal cortex of macaque monkeys: inhibitory interneurons and excitatory projection cells. Cells were classified as putative inhibitory or putative excitatory neurons on the basis of their extracellular waveform characteristics (e.g., spike duration). Consistent with previous intracellular recordings in cortical slices, putative inhibitory neurons had higher spontaneous firing rates and higher stimulus-evoked firing rates than putative excitatory neurons. Additionally, putative excitatory neurons were more susceptible to spike waveform adaptation following very short interspike intervals. Finally, we compared two functional properties of each neuron's stimulus-evoked response: stimulus selectivity and response latency. First, putative excitatory neurons showed stronger stimulus selectivity compared with putative inhibitory neurons. Second, putative inhibitory neurons had shorter response latencies compared with putative excitatory neurons. Selectivity differences were maintained and latency differences were enhanced during a visual search task emulating more natural viewing conditions. Our results suggest that short-latency inhibitory responses are likely to sculpt visual processing in excitatory neurons, yielding a sparser visual representation.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The cerebral cortex is composed of many distinct classes of neurons. Numerous studies have demonstrated corresponding differences in neuronal properties across cell types, but these comparisons have largely been limited to conditions outside of awake, behaving animals. Thus the functional role of the various cell types is not well understood. Here, we investigate differences in the functional properties of two widespread and broad classes of cells in inferior temporal cortex of macaque monkeys: inhibitory interneurons and excitatory projection cells. Cells were classified as putative inhibitory or putative excitatory neurons on the basis of their extracellular waveform characteristics (e.g., spike duration). Consistent with previous intracellular recordings in cortical slices, putative inhibitory neurons had higher spontaneous firing rates and higher stimulus-evoked firing rates than putative excitatory neurons. Additionally, putative excitatory neurons were more susceptible to spike waveform adaptation following very short interspike intervals. Finally, we compared two functional properties of each neuron's stimulus-evoked response: stimulus selectivity and response latency. First, putative excitatory neurons showed stronger stimulus selectivity compared with putative inhibitory neurons. Second, putative inhibitory neurons had shorter response latencies compared with putative excitatory neurons. Selectivity differences were maintained and latency differences were enhanced during a visual search task emulating more natural viewing conditions. Our results suggest that short-latency inhibitory responses are likely to sculpt visual processing in excitatory neurons, yielding a sparser visual representation. |
Kyoko Yoshida; Nobuhito Saito; Atsushi Iriki; Masaki Isoda Social error monitoring in macaque frontal cortex Journal Article Nature Neuroscience, 15 (9), pp. 1307–1312, 2012. @article{Yoshida2012, title = {Social error monitoring in macaque frontal cortex}, author = {Kyoko Yoshida and Nobuhito Saito and Atsushi Iriki and Masaki Isoda}, doi = {10.1038/nn.3180}, year = {2012}, date = {2012-01-01}, journal = {Nature Neuroscience}, volume = {15}, number = {9}, pages = {1307--1312}, publisher = {Nature Publishing Group}, abstract = {Although much learning occurs through direct experience of errors, humans and other animals can learn from the errors of other individuals. The medial frontal cortex (MFC) processes self-generated errors, but the neuronal architecture and mechanisms underlying the monitoring of others' errors are poorly understood. Exploring such mechanisms is important, as they underlie observational learning and allow adaptive behavior in uncertain social environments. Using two paired monkeys that monitored each other's action for their own action selection, we identified a group of neurons in the MFC that exhibited a substantial activity increase that was associated with another's errors. Nearly half of these neurons showed activity changes consistent with general reward-omission signals, whereas the remaining neurons specifically responded to another's erroneous actions. These findings indicate that the MFC contains a dedicated circuit for monitoring others' mistakes during social interactions.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Although much learning occurs through direct experience of errors, humans and other animals can learn from the errors of other individuals. The medial frontal cortex (MFC) processes self-generated errors, but the neuronal architecture and mechanisms underlying the monitoring of others' errors are poorly understood. Exploring such mechanisms is important, as they underlie observational learning and allow adaptive behavior in uncertain social environments. Using two paired monkeys that monitored each other's action for their own action selection, we identified a group of neurons in the MFC that exhibited a substantial activity increase that was associated with another's errors. Nearly half of these neurons showed activity changes consistent with general reward-omission signals, whereas the remaining neurons specifically responded to another's erroneous actions. These findings indicate that the MFC contains a dedicated circuit for monitoring others' mistakes during social interactions. |
Bram-Ernst Verhoef; Rufin Vogels; Peter Janssen Inferotemporal cortex subserves three-dimensional structure categorization Journal Article Neuron, 73 (1), pp. 171–182, 2012. @article{Verhoef2012, title = {Inferotemporal cortex subserves three-dimensional structure categorization}, author = {Bram-Ernst Verhoef and Rufin Vogels and Peter Janssen}, doi = {10.1016/j.neuron.2011.10.031}, year = {2012}, date = {2012-01-01}, journal = {Neuron}, volume = {73}, number = {1}, pages = {171--182}, publisher = {Elsevier Inc.}, abstract = {We perceive real-world objects as three-dimensional (3D), yet it is unknown which brain area underlies our ability to perceive objects in this way. The macaque inferotemporal (IT) cortex contains neurons that respond selectively to 3D structures defined by binocular disparity. To examine the causal role of IT in the categorization of 3D structures, we electrically stimulated clusters of IT neurons with a similar 3D-structure preference while monkeys performed a 3D-structure categorization task. Microstimulation of 3D-structure-selective IT clusters caused monkeys to choose the preferred structure of the 3D-structure-selective neurons considerably more often. Microstimulation in IT also accelerated the monkeys' choice for the preferred structure, while delaying choices corresponding to the nonpreferred structure of a given site. These findings reveal that 3D-structure-selective neurons in IT contribute to the categorization of 3D objects. How and where 3D shape perception arises from neuronal activity of neurons remains an unanswered question. Verhoef etal. find that manipulating the activity of neurons in the temporal lobe can influence the performance of monkeys performing a 3D shape categorization task.}, keywords = {}, pubstate = {published}, tppubtype = {article} } We perceive real-world objects as three-dimensional (3D), yet it is unknown which brain area underlies our ability to perceive objects in this way. The macaque inferotemporal (IT) cortex contains neurons that respond selectively to 3D structures defined by binocular disparity. To examine the causal role of IT in the categorization of 3D structures, we electrically stimulated clusters of IT neurons with a similar 3D-structure preference while monkeys performed a 3D-structure categorization task. Microstimulation of 3D-structure-selective IT clusters caused monkeys to choose the preferred structure of the 3D-structure-selective neurons considerably more often. Microstimulation in IT also accelerated the monkeys' choice for the preferred structure, while delaying choices corresponding to the nonpreferred structure of a given site. These findings reveal that 3D-structure-selective neurons in IT contribute to the categorization of 3D objects. How and where 3D shape perception arises from neuronal activity of neurons remains an unanswered question. Verhoef etal. find that manipulating the activity of neurons in the temporal lobe can influence the performance of monkeys performing a 3D shape categorization task. |
Heng Zou; Hermann J Muller; Zhuanghua Shi Non-spatial sounds regulate eye movements and enhance visual search Journal Article Journal of Vision, 12 (5), pp. 2–2, 2012. @article{Zou2012, title = {Non-spatial sounds regulate eye movements and enhance visual search}, author = {Heng Zou and Hermann J Muller and Zhuanghua Shi}, doi = {10.1167/12.5.2}, year = {2012}, date = {2012-01-01}, journal = {Journal of Vision}, volume = {12}, number = {5}, pages = {2--2}, abstract = {Spatially uninformative sounds can enhance visual search when the sounds are synchronized with color changes of the visual target, a phenomenon referred to as "pip-and-pop" effect (van der Burg, Olivers, Bronkhorst, & Theeuwes, 2008). The present study investigated the relationship of this effect to changes in oculomotor scanning behavior induced by the sounds. The results revealed sound events to increase fixation durations upon their occurrence and to decrease the mean number of saccades. More specifically, spatially uninformative sounds facilitated the orientation of ocular scanning away from already scanned display regions not containing a target (Experiment 1) and enhanced search performance even on target-absent trials (Experiment 2). Facilitation was also observed when the sounds were presented 100 ms prior to the target or at random (Experiment 3). These findings suggest that non-spatial sounds cause a general freezing effect on oculomotor scanning behavior, an effect which in turn benefits visual search performance by temporally and spatially extended information sampling.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Spatially uninformative sounds can enhance visual search when the sounds are synchronized with color changes of the visual target, a phenomenon referred to as "pip-and-pop" effect (van der Burg, Olivers, Bronkhorst, & Theeuwes, 2008). The present study investigated the relationship of this effect to changes in oculomotor scanning behavior induced by the sounds. The results revealed sound events to increase fixation durations upon their occurrence and to decrease the mean number of saccades. More specifically, spatially uninformative sounds facilitated the orientation of ocular scanning away from already scanned display regions not containing a target (Experiment 1) and enhanced search performance even on target-absent trials (Experiment 2). Facilitation was also observed when the sounds were presented 100 ms prior to the target or at random (Experiment 3). These findings suggest that non-spatial sounds cause a general freezing effect on oculomotor scanning behavior, an effect which in turn benefits visual search performance by temporally and spatially extended information sampling. |
Luke Woloszyn; David L Sheinberg Effects of long-term visual experience on responses of distinct classes of single units in inferior temporal cortex Journal Article Neuron, 74 (1), pp. 193–205, 2012. @article{Woloszyn2012, title = {Effects of long-term visual experience on responses of distinct classes of single units in inferior temporal cortex}, author = {Luke Woloszyn and David L Sheinberg}, doi = {10.1016/j.neuron.2012.01.032}, year = {2012}, date = {2012-01-01}, journal = {Neuron}, volume = {74}, number = {1}, pages = {193--205}, publisher = {Elsevier Inc.}, abstract = {Primates can learn to recognize a virtually limitless number of visual objects. A candidate neural substrate for this adult plasticity is the inferior temporal cortex (ITC). Using a large stimulus set, we explored the impact that long-term experience has on the response properties of two classes of neurons in ITC: broad-spiking (putative excitatory) cells and narrow-spiking (putative inhibitory) cells. We found that experience increased maximum responses of putative excitatory neurons but had the opposite effect on maximum responses of putative inhibitory neurons, an observation that helps to reconcile contradictory reports regarding the presence and direction of this effect. In addition, we found that experience reduced the average stimulus-evoked response in both cell classes, but this decrease was much more pronounced in putative inhibitory units. This latter finding supports a potentially critical role of inhibitory neurons in detecting and initiating the cascade of events underlying adult neural plasticity in ITC. Woloszyn and Sheinberg show that long-term visual experience enhances activity of putative excitatory neurons in inferior temporal cortex but decreases global activity of putative inhibitory neurons. These findings help reconcile conflicting views of the influence of visual experience on activity in IT cortex.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Primates can learn to recognize a virtually limitless number of visual objects. A candidate neural substrate for this adult plasticity is the inferior temporal cortex (ITC). Using a large stimulus set, we explored the impact that long-term experience has on the response properties of two classes of neurons in ITC: broad-spiking (putative excitatory) cells and narrow-spiking (putative inhibitory) cells. We found that experience increased maximum responses of putative excitatory neurons but had the opposite effect on maximum responses of putative inhibitory neurons, an observation that helps to reconcile contradictory reports regarding the presence and direction of this effect. In addition, we found that experience reduced the average stimulus-evoked response in both cell classes, but this decrease was much more pronounced in putative inhibitory units. This latter finding supports a potentially critical role of inhibitory neurons in detecting and initiating the cascade of events underlying adult neural plasticity in ITC. Woloszyn and Sheinberg show that long-term visual experience enhances activity of putative excitatory neurons in inferior temporal cortex but decreases global activity of putative inhibitory neurons. These findings help reconcile conflicting views of the influence of visual experience on activity in IT cortex. |
Karli K Watson; Michael L Platt Social signals in primate orbitofrontal cortex Journal Article Current Biology, 22 (23), pp. 2268–2273, 2012. @article{Watson2012, title = {Social signals in primate orbitofrontal cortex}, author = {Karli K Watson and Michael L Platt}, doi = {10.1016/j.cub.2012.10.016}, year = {2012}, date = {2012-01-01}, journal = {Current Biology}, volume = {22}, number = {23}, pages = {2268--2273}, publisher = {Elsevier Ltd}, abstract = {Primate evolution produced an increased capacity to respond flexibly to varying social contexts as well as expansion of the prefrontal cortex [1, 2]. Despite this association, how prefrontal neurons respond to social information remains virtually unknown. People with damage to their orbitofrontal cortex (OFC) struggle to recognize facial expressions [3, 4], make poor social judgments [5, 6], and frequently make social faux pas [7, 8]. Here we test explicitly whether neurons in primate OFC signal social information and, if so, how such signals compare with responses to primary fluid rewards. We find that OFC neurons distinguish images that belong to socially defined categories, such as female perinea and faces, as well as the social dominance of those faces. These modulations signaled both how much monkeys valued these pictures and their interest in continuing to view them. Far more neurons signaled social category than signaled fluid value, despite the stronger impact of fluid reward on monkeys' choices. These findings indicate that OFC represents both the motivational value and attentional priority of other individuals, thus contributing to both the acquisition of information about others and subsequent social decisions. Our results betray a fundamental disconnect between preferences expressed through overt choice, which were primarily driven by the desire for more fluid, and preferential neuronal processing, which favored social computations.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Primate evolution produced an increased capacity to respond flexibly to varying social contexts as well as expansion of the prefrontal cortex [1, 2]. Despite this association, how prefrontal neurons respond to social information remains virtually unknown. People with damage to their orbitofrontal cortex (OFC) struggle to recognize facial expressions [3, 4], make poor social judgments [5, 6], and frequently make social faux pas [7, 8]. Here we test explicitly whether neurons in primate OFC signal social information and, if so, how such signals compare with responses to primary fluid rewards. We find that OFC neurons distinguish images that belong to socially defined categories, such as female perinea and faces, as well as the social dominance of those faces. These modulations signaled both how much monkeys valued these pictures and their interest in continuing to view them. Far more neurons signaled social category than signaled fluid value, despite the stronger impact of fluid reward on monkeys' choices. These findings indicate that OFC represents both the motivational value and attentional priority of other individuals, thus contributing to both the acquisition of information about others and subsequent social decisions. Our results betray a fundamental disconnect between preferences expressed through overt choice, which were primarily driven by the desire for more fluid, and preferential neuronal processing, which favored social computations. |
Chin-An Wang; Susan E Boehnke; Brian J White; Douglas P Munoz Microstimulation of the monkey superior colliculus induces pupil dilation without evoking saccades Journal Article The Journal of Neuroscience, 32 (11), pp. 3629–3636, 2012. @article{Wang2012, title = {Microstimulation of the monkey superior colliculus induces pupil dilation without evoking saccades}, author = {Chin-An Wang and Susan E Boehnke and Brian J White and Douglas P Munoz}, doi = {10.1523/JNEUROSCI.5512-11.2012}, year = {2012}, date = {2012-01-01}, journal = {The Journal of Neuroscience}, volume = {32}, number = {11}, pages = {3629--3636}, abstract = {The orienting reflex is initiated by a salient stimulus and facilitates quick, appropriate action. It involves a rapid shift of the eyes, head, and attention and other physiological responses such as changes in heart rate and transient pupil dilation. The SC is a critical structure in the midbrain that selects incoming stimuli based on saliency and relevance to coordinate orienting behaviors, particularly gaze shifts, but its causal role in pupil dilation remains poorly understood in mammals. Here, we examined the role of the primate SC in the control of pupil dynamics. While requiring monkeys to keep their gaze fixed, we delivered weak electrical microstimulation to the SC, so that saccadic eye movements were not evoked. Pupil size increased transiently after microstimulation of the intermediate SC layers (SCi) and the size of evoked pupil dilation was larger on a dim versus bright background. In contrast, microstimulation of the superficial SC layers did not cause pupil dilation. Thus, the SCi is directly involved not only in shifts of gaze and attention, but also in pupil dilation as part of the orienting reflex, and the function of pupil dilation may be related to increasing visual sensitivity. The shared neural mechanisms suggest that pupil dilation may be associated with covert attention.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The orienting reflex is initiated by a salient stimulus and facilitates quick, appropriate action. It involves a rapid shift of the eyes, head, and attention and other physiological responses such as changes in heart rate and transient pupil dilation. The SC is a critical structure in the midbrain that selects incoming stimuli based on saliency and relevance to coordinate orienting behaviors, particularly gaze shifts, but its causal role in pupil dilation remains poorly understood in mammals. Here, we examined the role of the primate SC in the control of pupil dynamics. While requiring monkeys to keep their gaze fixed, we delivered weak electrical microstimulation to the SC, so that saccadic eye movements were not evoked. Pupil size increased transiently after microstimulation of the intermediate SC layers (SCi) and the size of evoked pupil dilation was larger on a dim versus bright background. In contrast, microstimulation of the superficial SC layers did not cause pupil dilation. Thus, the SCi is directly involved not only in shifts of gaze and attention, but also in pupil dilation as part of the orienting reflex, and the function of pupil dilation may be related to increasing visual sensitivity. The shared neural mechanisms suggest that pupil dilation may be associated with covert attention. |
Ioan Opris; Robert E Hampson; Greg A Gerhardt; Theodore W Berger; Sam A Deadwyler Columnar processing in primate pFC: Evidence for executive control microcircuits Journal Article Journal of Cognitive Neuroscience, 24 (12), pp. 2334–2347, 2012. @article{Opris2012, title = {Columnar processing in primate pFC: Evidence for executive control microcircuits}, author = {Ioan Opris and Robert E Hampson and Greg A Gerhardt and Theodore W Berger and Sam A Deadwyler}, doi = {10.1162/jocn_a_00307}, year = {2012}, date = {2012-01-01}, journal = {Journal of Cognitive Neuroscience}, volume = {24}, number = {12}, pages = {2334--2347}, abstract = {A common denominator for many cognitive disorders of human brain is the disruption of neural activity within pFC, whose structural basis is primarily interlaminar (columnar) microcircuits or "minicolumns." The importance of this brain region for executive decision-making has been well documented; however, because of technological constraints, the minicolumnar basis is not well understood. Here, via implementation of a unique conformal multielectrode recording array, the role of interlaminar pFC minicolumns in the executive control of task-related target selection is demonstrated in nonhuman primates performing a visuomotor DMS task. The results reveal target-specific, interlaminar correlated firing during the decision phase of the trial between multielectrode recording array-isolated minicolumnar pairs of neurons located in parallel in layers 2/3 and layer 5 of pFC. The functional significance of individual pFC minicolumns (separated by 40 $mu$m) was shown by reduced correlated firing between cell pairs within single minicolumns on error trials with inappropriate target selection. To further demonstrate dependence on performance, a task-disrupting drug (cocaine) was administered in the middle of the session, which also reduced interlaminar firing in minicolumns that fired appropriately in the early (nondrug) portion of the session. The results provide a direct demonstration of task-specific, real-time columnar processing in pFC indicating the role of this type of microcircuit in executive control of decision-making in primate brain.}, keywords = {}, pubstate = {published}, tppubtype = {article} } A common denominator for many cognitive disorders of human brain is the disruption of neural activity within pFC, whose structural basis is primarily interlaminar (columnar) microcircuits or "minicolumns." The importance of this brain region for executive decision-making has been well documented; however, because of technological constraints, the minicolumnar basis is not well understood. Here, via implementation of a unique conformal multielectrode recording array, the role of interlaminar pFC minicolumns in the executive control of task-related target selection is demonstrated in nonhuman primates performing a visuomotor DMS task. The results reveal target-specific, interlaminar correlated firing during the decision phase of the trial between multielectrode recording array-isolated minicolumnar pairs of neurons located in parallel in layers 2/3 and layer 5 of pFC. The functional significance of individual pFC minicolumns (separated by 40 $mu$m) was shown by reduced correlated firing between cell pairs within single minicolumns on error trials with inappropriate target selection. To further demonstrate dependence on performance, a task-disrupting drug (cocaine) was administered in the middle of the session, which also reduced interlaminar firing in minicolumns that fired appropriately in the early (nondrug) portion of the session. The results provide a direct demonstration of task-specific, real-time columnar processing in pFC indicating the role of this type of microcircuit in executive control of decision-making in primate brain. |
Jessica M Phillips; Stefan Everling Neural activity in the macaque putamen associated with saccades and behavioral uutcome Journal Article PLoS ONE, 7 (12), pp. 1–19, 2012. @article{Phillips2012a, title = {Neural activity in the macaque putamen associated with saccades and behavioral uutcome}, author = {Jessica M Phillips and Stefan Everling}, doi = {10.1371/journal.pone.0051596}, year = {2012}, date = {2012-01-01}, journal = {PLoS ONE}, volume = {7}, number = {12}, pages = {1--19}, publisher = {10. 1371/journal.pone.0051596}, address = {e51596. doi}, abstract = {It is now widely accepted that the basal ganglia nuclei form segregated, parallel loops with neocortical areas. The prevalent view is that the putamen is part of the motor loop, which receives inputs from sensorimotor areas, whereas the caudate, which receives inputs from frontal cortical eye fields and projects via the substantia nigra pars reticulata to the superior colliculus, belongs to the oculomotor loop. Tracer studies in monkeys and functional neuroimaging studies in human subjects, however, also suggest a potential role for the putamen in oculomotor control. To investigate the role of the putamen in saccadic eye movements, we recorded single neuron activity in the caudal putamen of two rhesus monkeys while they alternated between short blocks of pro- and anti-saccades. In each trial, the instruction cue was provided after the onset of the peripheral stimulus, thus the monkeys could either generate an immediate response to the stimulus based on the internal representation of the rule from the previous trial, or alternatively, could await the visual rule-instruction cue to guide their saccadic response. We found that a subset of putamen neurons showed saccade-related activity, that the preparatory mode (internally- versus externally-cued) influenced the expression of task-selectivity in roughly one third of the task-modulated neurons, and further that a large proportion of neurons encoded the outcome of the saccade. These results suggest that the caudal putamen may be part of the neural network for goal-directed saccades, wherein the monitoring of saccadic eye movements, context and performance feedback may be processed together to ensure optimal behavioural performance and outcomes are achieved during ongoing behaviour.}, keywords = {}, pubstate = {published}, tppubtype = {article} } It is now widely accepted that the basal ganglia nuclei form segregated, parallel loops with neocortical areas. The prevalent view is that the putamen is part of the motor loop, which receives inputs from sensorimotor areas, whereas the caudate, which receives inputs from frontal cortical eye fields and projects via the substantia nigra pars reticulata to the superior colliculus, belongs to the oculomotor loop. Tracer studies in monkeys and functional neuroimaging studies in human subjects, however, also suggest a potential role for the putamen in oculomotor control. To investigate the role of the putamen in saccadic eye movements, we recorded single neuron activity in the caudal putamen of two rhesus monkeys while they alternated between short blocks of pro- and anti-saccades. In each trial, the instruction cue was provided after the onset of the peripheral stimulus, thus the monkeys could either generate an immediate response to the stimulus based on the internal representation of the rule from the previous trial, or alternatively, could await the visual rule-instruction cue to guide their saccadic response. We found that a subset of putamen neurons showed saccade-related activity, that the preparatory mode (internally- versus externally-cued) influenced the expression of task-selectivity in roughly one third of the task-modulated neurons, and further that a large proportion of neurons encoded the outcome of the saccade. These results suggest that the caudal putamen may be part of the neural network for goal-directed saccades, wherein the monitoring of saccadic eye movements, context and performance feedback may be processed together to ensure optimal behavioural performance and outcomes are achieved during ongoing behaviour. |
Elsie Premereur; Wim Vanduffel; Peter Janssen Local field potential activity associated with temporal expectations in the macaque lateral intraparietal area Journal Article Journal of Cognitive Neuroscience, 24 (6), pp. 1314–1330, 2012. @article{Premereur2012, title = {Local field potential activity associated with temporal expectations in the macaque lateral intraparietal area}, author = {Elsie Premereur and Wim Vanduffel and Peter Janssen}, doi = {10.1162/jocn_a_00221}, year = {2012}, date = {2012-01-01}, journal = {Journal of Cognitive Neuroscience}, volume = {24}, number = {6}, pages = {1314--1330}, abstract = {Oscillatory brain activity is attracting increasing interest in cognitive neuroscience. Numerous EEG (magnetoencephalography) and local field potential (LFP) measurements have related cognitive functions to different types of brain oscillations, but the functional significance of these rhythms remains poorly understood. Despite its proven value, LFP activity has not been extensively tested in the macaque lateral intraparietal area (LIP), which has been implicated in a wide variety of cognitive control processes. We recorded action potentials and LFPs in area LIP during delayed eye movement tasks and during a passive fixation task, in which the time schedule was fixed so that temporal expectations about task-relevant cues could be formed. LFP responses in the gamma band discriminated reliably between saccade targets and distractors inside the receptive field (RF). Alpha and beta responses were much less strongly affected by the presence of a saccade target, however, but rose sharply in the waiting period before the go signal. Surprisingly, conditions without visual stimulation of the LIP-RF-evoked robust LFP responses in every frequency band—most prominently in those below 50 Hz—precisely time-locked to the expected time of stimulus onset in the RF. These results indicate that in area LIP, oscillations in the LFP, which reflect synaptic input and local network activity, are tightly coupled to the temporal expectation of task-relevant cues.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Oscillatory brain activity is attracting increasing interest in cognitive neuroscience. Numerous EEG (magnetoencephalography) and local field potential (LFP) measurements have related cognitive functions to different types of brain oscillations, but the functional significance of these rhythms remains poorly understood. Despite its proven value, LFP activity has not been extensively tested in the macaque lateral intraparietal area (LIP), which has been implicated in a wide variety of cognitive control processes. We recorded action potentials and LFPs in area LIP during delayed eye movement tasks and during a passive fixation task, in which the time schedule was fixed so that temporal expectations about task-relevant cues could be formed. LFP responses in the gamma band discriminated reliably between saccade targets and distractors inside the receptive field (RF). Alpha and beta responses were much less strongly affected by the presence of a saccade target, however, but rose sharply in the waiting period before the go signal. Surprisingly, conditions without visual stimulation of the LIP-RF-evoked robust LFP responses in every frequency band—most prominently in those below 50 Hz—precisely time-locked to the expected time of stimulus onset in the RF. These results indicate that in area LIP, oscillations in the LFP, which reflect synaptic input and local network activity, are tightly coupled to the temporal expectation of task-relevant cues. |
Elsie Premereur; Wim Vanduffel; Pieter R Roelfsema; Peter Janssen Frontal eye field microstimulation induces task-dependent gamma oscillations in the lateral intraparietal area Journal Article Journal of Neurophysiology, 108 (5), pp. 1392–1402, 2012. @article{Premereur2012a, title = {Frontal eye field microstimulation induces task-dependent gamma oscillations in the lateral intraparietal area}, author = {Elsie Premereur and Wim Vanduffel and Pieter R Roelfsema and Peter Janssen}, doi = {10.1152/jn.00323.2012}, year = {2012}, date = {2012-01-01}, journal = {Journal of Neurophysiology}, volume = {108}, number = {5}, pages = {1392--1402}, abstract = {Macaque frontal eye fields (FEF) and the lateral intraparietal area (LIP) are high-level oculomotor control centers that have been implicated in the allocation of spatial attention. Electrical microstimulation of macaque FEF elicits functional magnetic resonance imaging (fMRI) activations in area LIP, but no study has yet investigated the effect of FEF microstimulation on LIP at the single-cell or local field potential (LFP) level. We recorded spiking and LFP activity in area LIP during weak, subthreshold microstimulation of the FEF in a delayed-saccade task. FEF microstimulation caused a highly time- and frequency-specific, task-dependent increase in gamma power in retinotopically corresponding sites in LIP: FEF microstimulation produced a significant increase in LIP gamma power when a saccade target appeared and remained present in the LIP receptive field (RF), whereas less specific increases in alpha power were evoked by FEF microstimulation for saccades directed away from the RF. Stimulating FEF with weak currents had no effect on LIP spike rates or on the gamma power during memory saccades or passive fixation. These results provide the first evidence for task-dependent modulations of LFPs in LIP caused by top-down stimulation of FEF. Since the allocation and disengagement of spatial attention in visual cortex have been associated with increases in gamma and alpha power, respectively, the effects of FEF microstimulation on LIP are consistent with the known effects of spatial attention.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Macaque frontal eye fields (FEF) and the lateral intraparietal area (LIP) are high-level oculomotor control centers that have been implicated in the allocation of spatial attention. Electrical microstimulation of macaque FEF elicits functional magnetic resonance imaging (fMRI) activations in area LIP, but no study has yet investigated the effect of FEF microstimulation on LIP at the single-cell or local field potential (LFP) level. We recorded spiking and LFP activity in area LIP during weak, subthreshold microstimulation of the FEF in a delayed-saccade task. FEF microstimulation caused a highly time- and frequency-specific, task-dependent increase in gamma power in retinotopically corresponding sites in LIP: FEF microstimulation produced a significant increase in LIP gamma power when a saccade target appeared and remained present in the LIP receptive field (RF), whereas less specific increases in alpha power were evoked by FEF microstimulation for saccades directed away from the RF. Stimulating FEF with weak currents had no effect on LIP spike rates or on the gamma power during memory saccades or passive fixation. These results provide the first evidence for task-dependent modulations of LFPs in LIP caused by top-down stimulation of FEF. Since the allocation and disengagement of spatial attention in visual cortex have been associated with increases in gamma and alpha power, respectively, the effects of FEF microstimulation on LIP are consistent with the known effects of spatial attention. |
Victoria M Puig; Earl K Miller The role of prefrontal dopamine D1 receptors in the neural mechanisms of associative learning Journal Article Neuron, 74 (5), pp. 874–886, 2012. @article{Puig2012, title = {The role of prefrontal dopamine D1 receptors in the neural mechanisms of associative learning}, author = {Victoria M Puig and Earl K Miller}, doi = {10.1016/j.neuron.2012.04.018}, year = {2012}, date = {2012-01-01}, journal = {Neuron}, volume = {74}, number = {5}, pages = {874--886}, publisher = {Elsevier Inc.}, abstract = {Dopamine is thought to play a major role in learning. However, while dopamine D1 receptors (D1Rs) in the prefrontal cortex (PFC) have been shown to modulate working memory-related neural activity, their role in the cellular basis of learning is unknown. We recorded activity from multiple electrodes while injecting the D1R antagonist SCH23390 in the lateral PFC as monkeys learned visuomotor associations. Blocking D1Rs impaired learning of novel associations and decreased cognitive flexibility but spared performance of already familiar associations. This suggests a greater role for prefrontal D1Rs in learning new, rather than performing familiar, associations. There was a corresponding greater decrease in neural selectivity and increase in alpha and beta oscillations in local field potentials for novel than for familiar associations. Our results suggest that weak stimulation of D1Rs observed in aging and psychiatric disorders may impair learning and PFC function by reducing neural selectivity and exacerbating neural oscillations associated with inattention and cognitive deficits.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Dopamine is thought to play a major role in learning. However, while dopamine D1 receptors (D1Rs) in the prefrontal cortex (PFC) have been shown to modulate working memory-related neural activity, their role in the cellular basis of learning is unknown. We recorded activity from multiple electrodes while injecting the D1R antagonist SCH23390 in the lateral PFC as monkeys learned visuomotor associations. Blocking D1Rs impaired learning of novel associations and decreased cognitive flexibility but spared performance of already familiar associations. This suggests a greater role for prefrontal D1Rs in learning new, rather than performing familiar, associations. There was a corresponding greater decrease in neural selectivity and increase in alpha and beta oscillations in local field potentials for novel than for familiar associations. Our results suggest that weak stimulation of D1Rs observed in aging and psychiatric disorders may impair learning and PFC function by reducing neural selectivity and exacerbating neural oscillations associated with inattention and cognitive deficits. |
Braden A Purcell; Pauline K Weigand; Jeffrey D Schall Supplementary eye field during visual search: Salience, cognitive control, and performance monitoring Journal Article The Journal of Neuroscience, 32 (30), pp. 10273–10285, 2012. @article{Purcell2012, title = {Supplementary eye field during visual search: Salience, cognitive control, and performance monitoring}, author = {Braden A Purcell and Pauline K Weigand and Jeffrey D Schall}, doi = {10.1523/JNEUROSCI.6386-11.2012}, year = {2012}, date = {2012-01-01}, journal = {The Journal of Neuroscience}, volume = {32}, number = {30}, pages = {10273--10285}, abstract = {How supplementary eye field (SEF) contributes to visual search is unknown. Inputs from cortical and subcortical structures known to represent visual salience suggest that SEF may serve as an additional node in this network. This hypothesis was tested by recording action potentials and local field potentials (LFPs) in two monkeys performing an efficient pop-out visual search task. Target selection modulation, tuning width, and response magnitude of spikes and LFP in SEF were compared with those in frontal eye field. Surprisingly, only ~2% of SEF neurons and ~8% of SEF LFP sites selected the location of the search target. The absence of salience in SEF may be due to an absence of appropriate visual afferents, which suggests that these inputs are a necessary anatomical feature of areas representing salience. We also tested whether SEF contributes to overcoming the automatic tendency to respond to a primed color when the target identity switches during priming of pop-out. Very few SEF neurons or LFP sites modulated in association with performance deficits following target switches. However, a subset of SEF neurons and LFPs exhibited strong modulation following erroneous saccades to a distractor. Altogether, these results suggest that SEF plays a limited role in controlling ongoing visual search behavior, but may play a larger role in monitoring search performance.}, keywords = {}, pubstate = {published}, tppubtype = {article} } How supplementary eye field (SEF) contributes to visual search is unknown. Inputs from cortical and subcortical structures known to represent visual salience suggest that SEF may serve as an additional node in this network. This hypothesis was tested by recording action potentials and local field potentials (LFPs) in two monkeys performing an efficient pop-out visual search task. Target selection modulation, tuning width, and response magnitude of spikes and LFP in SEF were compared with those in frontal eye field. Surprisingly, only ~2% of SEF neurons and ~8% of SEF LFP sites selected the location of the search target. The absence of salience in SEF may be due to an absence of appropriate visual afferents, which suggests that these inputs are a necessary anatomical feature of areas representing salience. We also tested whether SEF contributes to overcoming the automatic tendency to respond to a primed color when the target identity switches during priming of pop-out. Very few SEF neurons or LFP sites modulated in association with performance deficits following target switches. However, a subset of SEF neurons and LFPs exhibited strong modulation following erroneous saccades to a distractor. Altogether, these results suggest that SEF plays a limited role in controlling ongoing visual search behavior, but may play a larger role in monitoring search performance. |
Robert M G Reinhart; Richard P Heitz; Braden A Purcell; Pauline K Weigand; Jeffrey D Schall; Geoffrey F Woodman Homologous mechanisms of visuospatial working memory maintenance in macaque and human: Properties and sources Journal Article The Journal of Neuroscience, 32 (22), pp. 7711–7722, 2012. @article{Reinhart2012, title = {Homologous mechanisms of visuospatial working memory maintenance in macaque and human: Properties and sources}, author = {Robert M G Reinhart and Richard P Heitz and Braden A Purcell and Pauline K Weigand and Jeffrey D Schall and Geoffrey F Woodman}, doi = {10.1523/JNEUROSCI.0215-12.2012}, year = {2012}, date = {2012-01-01}, journal = {The Journal of Neuroscience}, volume = {32}, number = {22}, pages = {7711--7722}, abstract = {Although areas of frontal cortex are thought to be critical for maintaining information in visuospatial working memory, the event-related potential (ERP) index of maintenance is found over posterior cortex in humans. In the present study, we reconcile these seemingly contradictory findings. Here, we show that macaque monkeys and humans exhibit the same posterior ERP signature of working memory maintenance that predicts the precision of the memory-based behavioral responses. In addition, we show that the specific pattern of rhythmic oscillations in the alpha band, recently demonstrated to underlie the human visual working memory ERP component, is also present in monkeys. Next, we concurrently recorded intracranial local field potentials from two prefrontal and another frontal cortical area to determine their contribution to the surface potential indexing maintenance. The local fields in the two prefrontal areas, but not the cortex immediately posterior, exhibited amplitude modulations, timing, and relationships to behavior indicating that they contribute to the generation of the surface ERP component measured from the distal posterior electrodes. Rhythmic neural activity in the theta and gamma bands during maintenance provided converging support for the engagement of the same brain regions. These findings demonstrate that nonhuman primates have homologous electrophysiological signatures of visuospatial working memory to those of humans and that a distributed neural network, including frontal areas, underlies the posterior ERP index of visuospatial working memory maintenance.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Although areas of frontal cortex are thought to be critical for maintaining information in visuospatial working memory, the event-related potential (ERP) index of maintenance is found over posterior cortex in humans. In the present study, we reconcile these seemingly contradictory findings. Here, we show that macaque monkeys and humans exhibit the same posterior ERP signature of working memory maintenance that predicts the precision of the memory-based behavioral responses. In addition, we show that the specific pattern of rhythmic oscillations in the alpha band, recently demonstrated to underlie the human visual working memory ERP component, is also present in monkeys. Next, we concurrently recorded intracranial local field potentials from two prefrontal and another frontal cortical area to determine their contribution to the surface potential indexing maintenance. The local fields in the two prefrontal areas, but not the cortex immediately posterior, exhibited amplitude modulations, timing, and relationships to behavior indicating that they contribute to the generation of the surface ERP component measured from the distal posterior electrodes. Rhythmic neural activity in the theta and gamma bands during maintenance provided converging support for the engagement of the same brain regions. These findings demonstrate that nonhuman primates have homologous electrophysiological signatures of visuospatial working memory to those of humans and that a distributed neural network, including frontal areas, underlies the posterior ERP index of visuospatial working memory maintenance. |
Maria C Romero; Ilse Van Dromme; Peter Janssen Responses to two-dimensional shapes in the macaque anterior intraparietal area Journal Article European Journal of Neuroscience, 36 (3), pp. 2324–2334, 2012. @article{Romero2012, title = {Responses to two-dimensional shapes in the macaque anterior intraparietal area}, author = {Maria C Romero and Ilse {Van Dromme} and Peter Janssen}, doi = {10.1111/j.1460-9568.2012.08135.x}, year = {2012}, date = {2012-01-01}, journal = {European Journal of Neuroscience}, volume = {36}, number = {3}, pages = {2324--2334}, abstract = {Neurons in the macaque dorsal visual stream respond to the visual presentation of objects in the context of a grasping task and to three-dimensional (3D) surfaces defined by binocular disparity, but little is known about the neural representation of two-dimensional (2D) shape in the dorsal stream. We recorded the activity of single neurons in the macaque anterior intraparietal area (AIP), which is known to be crucial for grasping, during the presentation of images of objects and silhouette, outline and line-drawing versions of these images (contour stimuli). The vast majority of AIP neurons responding selectively to 2D images were also selective for at least one of the contour stimuli with the same boundary shape, suggesting that the boundary is sufficient for the image selectivity of most AIP neurons. Furthermore, a subset of these neurons with foveal receptive fields generally preserved the shape preference across positions, whereas for more than half of the AIP population the center of the receptive field was at a parafoveal location with less tolerance to changes in stimulus position. AIP neurons frequently exhibited shape selectivity across different stimulus sizes. These results demonstrate that AIP neurons encode not only 3D but also 2D shape features.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Neurons in the macaque dorsal visual stream respond to the visual presentation of objects in the context of a grasping task and to three-dimensional (3D) surfaces defined by binocular disparity, but little is known about the neural representation of two-dimensional (2D) shape in the dorsal stream. We recorded the activity of single neurons in the macaque anterior intraparietal area (AIP), which is known to be crucial for grasping, during the presentation of images of objects and silhouette, outline and line-drawing versions of these images (contour stimuli). The vast majority of AIP neurons responding selectively to 2D images were also selective for at least one of the contour stimuli with the same boundary shape, suggesting that the boundary is sufficient for the image selectivity of most AIP neurons. Furthermore, a subset of these neurons with foveal receptive fields generally preserved the shape preference across positions, whereas for more than half of the AIP population the center of the receptive field was at a parafoveal location with less tolerance to changes in stimulus position. AIP neurons frequently exhibited shape selectivity across different stimulus sizes. These results demonstrate that AIP neurons encode not only 3D but also 2D shape features. |
Octavio Ruiz; Michael A Paradiso Macaque V1 representations in natural and reduced visual contexts: Spatial and temporal properties and influence of saccadic eye movements Journal Article Journal of Neurophysiology, 108 (1), pp. 324–333, 2012. @article{Ruiz2012, title = {Macaque V1 representations in natural and reduced visual contexts: Spatial and temporal properties and influence of saccadic eye movements}, author = {Octavio Ruiz and Michael A Paradiso}, doi = {10.1152/jn.00733.2011}, year = {2012}, date = {2012-01-01}, journal = {Journal of Neurophysiology}, volume = {108}, number = {1}, pages = {324--333}, abstract = {Vision in natural situations is different from the paradigms generally used to study vision in the laboratory. In natural vision, stimuli usually appear in a receptive field as the result of saccadic eye movements rather than suddenly flashing into view. The stimuli themselves are rich with meaningful and recognizable objects rather than simple abstract patterns. In this study we examined the sensitivity of neurons in macaque area V1 to saccades and to complex background contexts. Using a variety of visual conditions, we find that natural visual response patterns are unique. Compared with standard laboratory situations, in more natural vision V1 responses have longer latency, slower time course, delayed orientation selectivity, higher peak selectivity, and lower amplitude. Furthermore, the influences of saccades and background type (complex picture vs. uniform gray) interact to give a distinctive, and presumably more natural, response pattern. While in most of the experiments natural images were used as background, we find that similar synthetic unnatural background stimuli produce nearly identical responses (i.e., complexity matters more than "naturalness"). These findings have important implications for our understanding of vision in more natural situations. They suggest that with the saccades used to explore complex images, visual context ("surround effects") would have a far greater effect on perception than in standard experiments with stimuli flashed on a uniform background. Perceptual thresholds for contrast and orientation should also be significantly different in more natural situations.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Vision in natural situations is different from the paradigms generally used to study vision in the laboratory. In natural vision, stimuli usually appear in a receptive field as the result of saccadic eye movements rather than suddenly flashing into view. The stimuli themselves are rich with meaningful and recognizable objects rather than simple abstract patterns. In this study we examined the sensitivity of neurons in macaque area V1 to saccades and to complex background contexts. Using a variety of visual conditions, we find that natural visual response patterns are unique. Compared with standard laboratory situations, in more natural vision V1 responses have longer latency, slower time course, delayed orientation selectivity, higher peak selectivity, and lower amplitude. Furthermore, the influences of saccades and background type (complex picture vs. uniform gray) interact to give a distinctive, and presumably more natural, response pattern. While in most of the experiments natural images were used as background, we find that similar synthetic unnatural background stimuli produce nearly identical responses (i.e., complexity matters more than "naturalness"). These findings have important implications for our understanding of vision in more natural situations. They suggest that with the saccades used to explore complex images, visual context ("surround effects") would have a far greater effect on perception than in standard experiments with stimuli flashed on a uniform background. Perceptual thresholds for contrast and orientation should also be significantly different in more natural situations. |
NaYoung So; Veit Stuphorn Supplementary eye field encodes reward prediction error Journal Article The Journal of Neuroscience, 32 (9), pp. 2950–2963, 2012. @article{So2012, title = {Supplementary eye field encodes reward prediction error}, author = {NaYoung So and Veit Stuphorn}, doi = {10.1523/JNEUROSCI.4419-11.2012}, year = {2012}, date = {2012-01-01}, journal = {The Journal of Neuroscience}, volume = {32}, number = {9}, pages = {2950--2963}, abstract = {The outcomes of many decisions are uncertain and therefore need to be evaluated. We studied this evaluation process by recording neuronal activity in the supplementary eye field (SEF) during an oculomotor gambling task. While the monkeys awaited the outcome, SEF neurons represented attributes of the chosen option, namely, its expected value and the uncertainty of this value signal. After the gamble result was revealed, a number of neurons reflected the actual reward outcome. Other neurons evaluated the outcome by encoding the difference between the reward expectation represented during the delay period and the actual reward amount (i.e., the reward prediction error). Thus, SEF encodes not only reward prediction error but also all the components necessary for its computation: the expected and the actual outcome. This suggests that SEF might actively evaluate value-based decisions in the oculomotor domain, independent of other brain regions.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The outcomes of many decisions are uncertain and therefore need to be evaluated. We studied this evaluation process by recording neuronal activity in the supplementary eye field (SEF) during an oculomotor gambling task. While the monkeys awaited the outcome, SEF neurons represented attributes of the chosen option, namely, its expected value and the uncertainty of this value signal. After the gamble result was revealed, a number of neurons reflected the actual reward outcome. Other neurons evaluated the outcome by encoding the difference between the reward expectation represented during the delay period and the actual reward amount (i.e., the reward prediction error). Thus, SEF encodes not only reward prediction error but also all the components necessary for its computation: the expected and the actual outcome. This suggests that SEF might actively evaluate value-based decisions in the oculomotor domain, independent of other brain regions. |
Sruthi K Swaminathan; David J Freedman Preferential encoding of visual categories in parietal cortex compared with prefrontal cortex Journal Article Nature Neuroscience, 15 (2), pp. 315–320, 2012. @article{Swaminathan2012, title = {Preferential encoding of visual categories in parietal cortex compared with prefrontal cortex}, author = {Sruthi K Swaminathan and David J Freedman}, doi = {10.1038/nn.3016}, year = {2012}, date = {2012-01-01}, journal = {Nature Neuroscience}, volume = {15}, number = {2}, pages = {315--320}, publisher = {Nature Publishing Group}, abstract = {The ability to recognize the behavioral relevance, or category membership, of sensory stimuli is critical for interpreting the meaning of events in our environment. Neurophysiological studies of visual categorization have found categorical representations of stimuli in prefrontal cortex (PFC), an area that is closely associated with cognitive and executive functions. Recent studies have also identified neuronal category signals in parietal areas that are typically associated with visual-spatial processing. It has been proposed that category-related signals in parietal cortex and other visual areas may result from 'top-down' feedback from PFC. We directly compared neuronal activity in the lateral intraparietal (LIP) area and PFC in monkeys performing a visual motion categorization task. We found that LIP showed stronger, more reliable and shorter latency category signals than PFC. These findings suggest that LIP is strongly involved in visual categorization and argue against the idea that parietal category signals arise as a result of feedback from PFC during this task.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The ability to recognize the behavioral relevance, or category membership, of sensory stimuli is critical for interpreting the meaning of events in our environment. Neurophysiological studies of visual categorization have found categorical representations of stimuli in prefrontal cortex (PFC), an area that is closely associated with cognitive and executive functions. Recent studies have also identified neuronal category signals in parietal areas that are typically associated with visual-spatial processing. It has been proposed that category-related signals in parietal cortex and other visual areas may result from 'top-down' feedback from PFC. We directly compared neuronal activity in the lateral intraparietal (LIP) area and PFC in monkeys performing a visual motion categorization task. We found that LIP showed stronger, more reliable and shorter latency category signals than PFC. These findings suggest that LIP is strongly involved in visual categorization and argue against the idea that parietal category signals arise as a result of feedback from PFC during this task. |
T Theys; S Srivastava; J van Loon; J Goffin; P Janssen Selectivity for three-dimensional contours and surfaces in the anterior intraparietal area Journal Article Journal of Neurophysiology, 107 (3), pp. 995–1008, 2012. @article{Theys2012, title = {Selectivity for three-dimensional contours and surfaces in the anterior intraparietal area}, author = {T Theys and S Srivastava and J van Loon and J Goffin and P Janssen}, doi = {10.1152/jn.00248.2011}, year = {2012}, date = {2012-01-01}, journal = {Journal of Neurophysiology}, volume = {107}, number = {3}, pages = {995--1008}, abstract = {The macaque anterior intraparietal area (AIP) is crucial for visually guided grasping. AIP neurons respond during the visual presentation of real-world objects and encode the depth profile of disparity-defined curved surfaces. We investigated the neural representation of curved surfaces in AIP using a stimulus-reduction approach. The stimuli consisted of three-dimensional (3-D) shapes curved along the horizontal axis, the vertical axis, or both the horizontal and the vertical axes of the shape. The depth profile was defined solely by binocular disparity that varied along either the boundary or the surface of the shape or along both the boundary and the surface of the shape. The majority of AIP neurons were selective for curved boundaries along the horizontal or the vertical axis, and neural selectivity emerged at short latencies. Stimuli in which disparity varied only along the surface of the shape (with zero disparity on the boundaries) evoked selectivity in a smaller proportion of AIP neurons and at considerably longer latencies. AIP neurons were not selective for 3-D surfaces composed of anticorrelated disparities. Thus the neural selectivity for object depth profile in AIP is present when only the boundary is curved in depth, but not for disparity in anticorrelated stereograms.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The macaque anterior intraparietal area (AIP) is crucial for visually guided grasping. AIP neurons respond during the visual presentation of real-world objects and encode the depth profile of disparity-defined curved surfaces. We investigated the neural representation of curved surfaces in AIP using a stimulus-reduction approach. The stimuli consisted of three-dimensional (3-D) shapes curved along the horizontal axis, the vertical axis, or both the horizontal and the vertical axes of the shape. The depth profile was defined solely by binocular disparity that varied along either the boundary or the surface of the shape or along both the boundary and the surface of the shape. The majority of AIP neurons were selective for curved boundaries along the horizontal or the vertical axis, and neural selectivity emerged at short latencies. Stimuli in which disparity varied only along the surface of the shape (with zero disparity on the boundaries) evoked selectivity in a smaller proportion of AIP neurons and at considerably longer latencies. AIP neurons were not selective for 3-D surfaces composed of anticorrelated disparities. Thus the neural selectivity for object depth profile in AIP is present when only the boundary is curved in depth, but not for disparity in anticorrelated stereograms. |
Ken Ichi Amemori; Ann M Graybiel Localized microstimulation of primate pregenual cingulate cortex induces negative decision-making Journal Article Nature Neuroscience, 15 (5), pp. 776–785, 2012. @article{Amemori2012, title = {Localized microstimulation of primate pregenual cingulate cortex induces negative decision-making}, author = {Ken Ichi Amemori and Ann M Graybiel}, doi = {10.1038/nn.3088}, year = {2012}, date = {2012-01-01}, journal = {Nature Neuroscience}, volume = {15}, number = {5}, pages = {776--785}, abstract = {The pregenual anterior cingulate cortex (pACC) has been implicated in human anxiety disorders and depression, but the circuit-level mechanisms underlying these disorders are unclear. In healthy individuals, the pACC is involved in cost-benefit evaluation. We developed a macaque version of an approach-avoidance decision task used to evaluate anxiety and depression in humans and, with multi-electrode recording and cortical microstimulation, we probed pACC function as monkeys performed this task. We found that the macaque pACC has an opponent process-like organization of neurons representing motivationally positive and negative subjective value. Spatial distribution of these two neuronal populations overlapped in the pACC, except in one subzone, where neurons with negative coding were more numerous. Notably, microstimulation in this subzone, but not elsewhere in the pACC, increased negative decision-making, and this negative biasing was blocked by anti-anxiety drug treatment. This cortical zone could be critical for regulating negative emotional valence and anxiety in decision-making.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The pregenual anterior cingulate cortex (pACC) has been implicated in human anxiety disorders and depression, but the circuit-level mechanisms underlying these disorders are unclear. In healthy individuals, the pACC is involved in cost-benefit evaluation. We developed a macaque version of an approach-avoidance decision task used to evaluate anxiety and depression in humans and, with multi-electrode recording and cortical microstimulation, we probed pACC function as monkeys performed this task. We found that the macaque pACC has an opponent process-like organization of neurons representing motivationally positive and negative subjective value. Spatial distribution of these two neuronal populations overlapped in the pACC, except in one subzone, where neurons with negative coding were more numerous. Notably, microstimulation in this subzone, but not elsewhere in the pACC, increased negative decision-making, and this negative biasing was blocked by anti-anxiety drug treatment. This cortical zone could be critical for regulating negative emotional valence and anxiety in decision-making. |
Timothy J Buschman; Eric L Denovellis; Cinira Diogo; Daniel Bullock; Earl K Miller Synchronous oscillatory neural ensembles for rules in the prefrontal cortex Journal Article Neuron, 76 (4), pp. 838–846, 2012. @article{Buschman2012, title = {Synchronous oscillatory neural ensembles for rules in the prefrontal cortex}, author = {Timothy J Buschman and Eric L Denovellis and Cinira Diogo and Daniel Bullock and Earl K Miller}, doi = {10.1016/j.neuron.2012.09.029}, year = {2012}, date = {2012-01-01}, journal = {Neuron}, volume = {76}, number = {4}, pages = {838--846}, publisher = {Elsevier Inc.}, abstract = {Intelligent behavior requires acquiring and following rules. Rules define how our behavior should fit different situations. To understand its neural mechanisms, we simultaneously recorded from multiple electrodes in dorsolateral prefrontal cortex (PFC) while monkeys switched between two rules (respond to color versus orientation). We found evidence that oscillatory synchronization of local field potentials (LFPs) formed neural ensembles representing the rules: there were rule-specific increases in synchrony at " beta" (19-40 Hz) frequencies between electrodes. In addition, individual PFC neurons synchronized to the LFP ensemble corresponding to the current rule (color versus orientation). Furthermore, the ensemble encoding the behaviorally dominant orientation rule showed increased " alpha" (6-16 Hz) synchrony when preparing to apply the alternative (weaker) color rule. This suggests that beta-frequency synchrony selects the relevant rule ensemble, while alpha-frequency synchrony deselects a stronger, but currently irrelevant, ensemble. Synchrony may act to dynamically shape task-relevant neural ensembles out of larger, overlapping circuits.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Intelligent behavior requires acquiring and following rules. Rules define how our behavior should fit different situations. To understand its neural mechanisms, we simultaneously recorded from multiple electrodes in dorsolateral prefrontal cortex (PFC) while monkeys switched between two rules (respond to color versus orientation). We found evidence that oscillatory synchronization of local field potentials (LFPs) formed neural ensembles representing the rules: there were rule-specific increases in synchrony at " beta" (19-40 Hz) frequencies between electrodes. In addition, individual PFC neurons synchronized to the LFP ensemble corresponding to the current rule (color versus orientation). Furthermore, the ensemble encoding the behaviorally dominant orientation rule showed increased " alpha" (6-16 Hz) synchrony when preparing to apply the alternative (weaker) color rule. This suggests that beta-frequency synchrony selects the relevant rule ensemble, while alpha-frequency synchrony deselects a stronger, but currently irrelevant, ensemble. Synchrony may act to dynamically shape task-relevant neural ensembles out of larger, overlapping circuits. |
Brittany N Bushnell; Anitha Pasupathy Shape encoding consistency across colors in primate V4 Journal Article Journal of Neurophysiology, 108 (5), pp. 1299–1308, 2012. @article{Bushnell2012, title = {Shape encoding consistency across colors in primate V4}, author = {Brittany N Bushnell and Anitha Pasupathy}, doi = {10.1152/jn.01063.2011}, year = {2012}, date = {2012-01-01}, journal = {Journal of Neurophysiology}, volume = {108}, number = {5}, pages = {1299--1308}, abstract = {Neurons in primate cortical area V4 are sensitive to the form and color of visual stimuli. To determine whether form selectivity remains consistent across colors, we studied the responses of single V4 neurons in awake monkeys to a set of two-dimensional shapes presented in two different colors. For each neuron, we chose two colors that were visually distinct and that evoked reliable and different responses. Across neurons, the correlation coefficient between responses in the two colors ranged from -0.03 to 0.93 (median 0.54). Neurons with highly consistent shape responses, i.e., high correlation coefficients, showed greater dispersion in their responses to the different shapes, i.e., greater shape selectivity, and also tended to have less eccentric receptive field locations; among shape-selective neurons, shape consistency ranged from 0.16 to 0.93 (median 0.63). Consistency of shape responses was independent of the physical difference between the stimulus colors used and the strength of neuronal color tuning. Finally, we found that our measurement of shape response consistency was strongly influenced by the number of stimulus repeats: consistency estimates based on fewer than 10 repeats were substantially underestimated. In conclusion, our results suggest that neurons that are likely to contribute to shape perception and discrimination exhibit shape responses that are largely consistent across colors, facilitating the use of simpler algorithms for decoding shape information from V4 neuronal populations.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Neurons in primate cortical area V4 are sensitive to the form and color of visual stimuli. To determine whether form selectivity remains consistent across colors, we studied the responses of single V4 neurons in awake monkeys to a set of two-dimensional shapes presented in two different colors. For each neuron, we chose two colors that were visually distinct and that evoked reliable and different responses. Across neurons, the correlation coefficient between responses in the two colors ranged from -0.03 to 0.93 (median 0.54). Neurons with highly consistent shape responses, i.e., high correlation coefficients, showed greater dispersion in their responses to the different shapes, i.e., greater shape selectivity, and also tended to have less eccentric receptive field locations; among shape-selective neurons, shape consistency ranged from 0.16 to 0.93 (median 0.63). Consistency of shape responses was independent of the physical difference between the stimulus colors used and the strength of neuronal color tuning. Finally, we found that our measurement of shape response consistency was strongly influenced by the number of stimulus repeats: consistency estimates based on fewer than 10 repeats were substantially underestimated. In conclusion, our results suggest that neurons that are likely to contribute to shape perception and discrimination exhibit shape responses that are largely consistent across colors, facilitating the use of simpler algorithms for decoding shape information from V4 neuronal populations. |
X Cai; Camillo Padoa-Schioppa Neuronal encoding of subjective value in dorsal and ventral anterior cingulate cortex Journal Article The Journal of Neuroscience, 32 (11), pp. 3791–3808, 2012. @article{Cai2012, title = {Neuronal encoding of subjective value in dorsal and ventral anterior cingulate cortex}, author = {X Cai and Camillo Padoa-Schioppa}, doi = {10.1523/JNEUROSCI.3864-11.2012}, year = {2012}, date = {2012-01-01}, journal = {The Journal of Neuroscience}, volume = {32}, number = {11}, pages = {3791--3808}, abstract = {We examined the activity of individual cells in the primate anterior cingulate cortex during an economic choice task. In the experiments, monkeys chose between different juices offered in variables amounts and subjective values were inferred from the animals' choices. We analyzed neuronal firing rates in relation to a large number of behaviorally relevant variables. We report three main results. First, there were robust differences between the dorsal bank (ACCd) and the ventral bank (ACCv) of the cingulate sulcus. Specifically, neurons in ACCd but not in ACCv were modulated by the movement direction. Furthermore, neurons in ACCd were most active before movement initiation, whereas neurons in ACCv were most active after juice delivery. Second, neurons in both areas encoded the identity and the subjective value of the juice chosen by the animal. In contrast, neither region encoded the value of individual offers. Third, the population of value-encoding neurons in both ACCd and ACCv underwent range adaptation. With respect to economic choice, it is interesting to compare these areas with the orbitofrontal cortex (OFC), previously examined. While neurons in OFC encoded both pre-decision and post-decision variables, neurons in ACCd and ACCv only encoded post-decision variables. Moreover, the encoding of the choice outcome (chosen value and chosen juice) in ACCd and ACCv trailed that found in OFC. These observations indicate that economic decisions (i.e., value comparisons) take place upstream of ACCd and ACCv. The coexistence of choice outcome and movement signals in ACCd suggests that this area constitutes a gateway through which the choice system informs motor systems.}, keywords = {}, pubstate = {published}, tppubtype = {article} } We examined the activity of individual cells in the primate anterior cingulate cortex during an economic choice task. In the experiments, monkeys chose between different juices offered in variables amounts and subjective values were inferred from the animals' choices. We analyzed neuronal firing rates in relation to a large number of behaviorally relevant variables. We report three main results. First, there were robust differences between the dorsal bank (ACCd) and the ventral bank (ACCv) of the cingulate sulcus. Specifically, neurons in ACCd but not in ACCv were modulated by the movement direction. Furthermore, neurons in ACCd were most active before movement initiation, whereas neurons in ACCv were most active after juice delivery. Second, neurons in both areas encoded the identity and the subjective value of the juice chosen by the animal. In contrast, neither region encoded the value of individual offers. Third, the population of value-encoding neurons in both ACCd and ACCv underwent range adaptation. With respect to economic choice, it is interesting to compare these areas with the orbitofrontal cortex (OFC), previously examined. While neurons in OFC encoded both pre-decision and post-decision variables, neurons in ACCd and ACCv only encoded post-decision variables. Moreover, the encoding of the choice outcome (chosen value and chosen juice) in ACCd and ACCv trailed that found in OFC. These observations indicate that economic decisions (i.e., value comparisons) take place upstream of ACCd and ACCv. The coexistence of choice outcome and movement signals in ACCd suggests that this area constitutes a gateway through which the choice system informs motor systems. |