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2018 |
Jan Churan; Doris I. Braun; Karl R. Gegenfurtner; Frank Bremmer Comparison of the precision of smooth pursuit in humans and head unrestrained monkeys Journal Article In: Journal of Eye Movement Research, vol. 11, no. 4, pp. 1–15, 2018. @article{Churan2018,Direct comparison of results of humans and monkeys is often complicated by differences in experimental conditions. We replicated in head unrestrained macaques experiments of a recent study comparing human directional precision during smooth pursuit eye movements (SPEM) and saccades to moving targets (Braun & Gegenfurtner, 2016). Directional precision of human SPEM follows an exponential decay function reaching optimal values of 1.5°-3° within 300 ms after target motion onset, whereas precision of initial saccades to moving targets is slightly better. As in humans, we found general agreement in the development of directional precision of SPEM over time and in the differences between directional precision of initial saccades and SPEM initiation. However, monkeys showed overall lower precision in SPEM compared to humans. This was most likely due to differences in experimental conditions, such as in the stabilization of the head, which was by a chin and a head rest in human subjects and unrestrained in monkeys. |
Suryadeep Dash; Tyler R. Peel; Stephen G. Lomber; Brian D. Corneil In: eNeuro, vol. 5, no. 2, pp. 1–16, 2018. @article{Dash2018,A neural correlate for saccadic reaction times (SRTs) in the gap saccade task is the level of low-frequency activity in the intermediate layers of the superior colliculus (iSC) just before visual target onset: greater levels of such preparatory iSC low-frequency activity precede shorter SRTs. The frontal eye fields (FEFs) are one likely source of iSC preparatory activity, since FEF preparatory activity is also inversely related to SRT. To better understand the FEF's role in saccade preparation, and the way in which such preparation relates to SRT, in two male rhesus monkeys, we compared iSC preparatory activity across unilateral reversible cryogenic inactivation of the FEF. FEF inactivation increased contralesional SRTs, and lowered ipsilesional iSC preparatory activity. FEF inactivation also reduced rostral iSC activity during the gap period. Importantly, the distributions of SRTs generated with or without FEF inactivation overlapped, enabling us to conduct a novel population-level analyses examining iSC preparatory activity just before generation of SRT-matched saccades. When matched for SRTs, we observed no change during FEF inactivation in the relationship between iSC preparatory activity and SRT-matched saccades across a range of SRTs, even for the occasional express saccade. Thus, while our results emphasize that the FEF has an overall excitatory influence on preparatory activity in the iSC, the communication between the iSC and downstream oculomotor brainstem is unaltered for SRT-matched saccades. |
Mohammad-Reza A. Dehaqani; Abdol-Hossein Vahabie; Mohammadbagher Parsa; Behrad Noudoost; Alireza Soltani Selective changes in noise correlations contribute to an enhanced representation of saccadic targets in prefrontal neuronal ensembles Journal Article In: Cerebral Cortex, vol. 28, no. 8, pp. 3046–3063, 2018. @article{Dehaqani2018,An ensemble of neurons can provide a dynamic representation of external stimuli, ongoing processes, or upcoming actions. This dynamic representation could be achieved by changes in the activity of individual neurons and/or their interactions. To investigate these possibilities, we simultaneously recorded from ensembles of prefrontal neurons in non-human primates during a memory-guided saccade task. Using both decoding and encoding methods, we examined changes in the information content of individual neurons and that of ensembles between visual encoding and saccadic target selection. We found that individual neurons maintained their limited spatial sensitivity between these cognitive states, whereas the ensemble selectively improved its encoding of spatial locations far from the neurons' preferred locations. This population- level “encoding expansion” was not due to the ceiling effect at the preferred locations and was accompanied by selective changes in noise correlations for non-preferred locations. Moreover, the encoding expansion was observed for ensembles of different types of neurons and could not be explained by shifts in the preferred location of individual neurons. Our results demonstrate that the representation of space by neuronal ensembles is dynamically enhanced prior to saccades, and this enhancement occurs alongside changes in noise correlations more than changes in the activity of individual neurons. |
R. Becket Ebitz; Eddy Albarran; Tirin Moore Exploration disrupts choice-predictive signals and alters dynamics in prefrontal cortex Journal Article In: Neuron, vol. 97, no. 2, pp. 450–461.e9, 2018. @article{Ebitz2018,In uncertain environments, decision-makers must balance two goals: they must “exploit” rewarding options but also “explore” in order to discover rewarding alternatives. Exploring and exploiting necessarily change how the brain responds to identical stimuli, but little is known about how these states, and transitions between them, change how the brain transforms sensory information into action. To address this question, we recorded neural activity in a prefrontal sensorimotor area while monkeys naturally switched between exploring and exploiting rewarding options. We found that exploration profoundly reduced spatially selective, choice-predictive activity in single neurons and delayed choice-predictive population dynamics. At the same time, reward learning was increased in brain and behavior. These results indicate that exploration is related to sudden disruptions in prefrontal sensorimotor control and rapid, reward-dependent reorganization of control dynamics. This may facilitate discovery through trial and error. Exploratory choices permit the discovery of new rewarding options. Ebitz et al. report that spatially selective, choice-predictive neurons in the prefrontal cortex do not predict choice before exploratory decisions. Reduced prefrontal control may underlie flexible decision-making and trial-and-error discovery. |
Shiva Farashahi; Habiba Azab; Benjamin Y. Hayden; Alireza Soltani On the flexibility of basic risk attitudes in monkeys Journal Article In: Journal of Neuroscience, vol. 38, no. 18, pp. 4383–4398, 2018. @article{Farashahi2018,Monkeys and other animals appear to share with humans two risk attitudes predicted by prospect theory: an inverse-S-shaped probability weighting function and a steeper utility curve for losses than for gains. These findings suggest that such preferences are stable traits with common neural substrates. We hypothesized instead that animals tailor their preferences to subtle changes in task contexts, making risk attitudes flexible. Previous studies used a limited number of outcomes, trial types, and contexts. To gain a broader perspective, we examined two large datasets of male macaques' risky choices: one from a task with real (juice) gains and another from a token task with gains and losses. In contrast to previous findings, monkeys were risk-seeking for both gains and losses (i.e. lacked a reflection effect) and showed steeper gain than loss curves (loss-seeking). Utility curves for gains were substantially different in the two tasks. Monkeys showed nearly linear probability weightings in one task and S-shaped ones in the other; neither task produced a consistent inverse-S-shaped curve. To account for these observations, we developed and tested various computational models of the processes involved in the construction of reward value. We found that adaptive differential weighting of prospective gamble outcomes could partially account for the observed differences in the utility functions across the two experiments and thus, provide a plausible mechanism underlying flexible risk attitudes. Together, our results support the idea that risky choices are constructed flexibly at the time of elicitation and place important constraints on neural models of economic choice. |
Jose A. Fernandez-Leon; Bryan J. Hansen; Valentin Dragoi Representation of rapid image sequences in V4 Networks Journal Article In: Cerebral Cortex, vol. 28, no. 8, pp. 2675–2684, 2018. @article{FernandezLeon2018,Natural viewing often consists of sequences of brief fixations to image patches of different structure. Whether and how briefly presented sequential stimuli are encoded in a temporal-position manner is poorly understood. Here, we performed multiple-electrode recordings in the visual cortex (area V4) of nonhuman primates (Macaca mulatta) viewing a sequence of 7 briefly flashed natural images, and measured correlations between the cue-triggered population response in the presence and absence of the stimulus. Surprisingly, we found significant correlations for images occurring at the beginning and the end of a sequence, but not for those in the middle. The correlation strength increased with stimulus exposure and favored the image position in the sequence rather than image identity. These results challenge the commonly held view that images are represented in visual cortex exclusively based on their informational content, and indicate that, in the absence of sensory information, neuronal populations exhibit reactivation of stimulus-evoked responses in a way that reflects temporal position within a stimulus sequence. |
Ian C. Fiebelkorn; Mark A. Pinsk; Sabine Kastner A dynamic interplay within the frontoparietal network underlies rhythmic spatial attention Journal Article In: Neuron, vol. 99, no. 4, pp. 842–853.e8, 2018. @article{Fiebelkorn2018,Classic studies of spatial attention assumed that its neural and behavioral effects were continuous over time. Recent behavioral studies have instead revealed that spatial attention leads to alternating periods of heightened or diminished perceptual sensitivity. Yet, the neural basis of these rhythmic fluctuations has remained largely unknown. We show that a dynamic interplay within the macaque frontoparietal network accounts for the rhythmic properties of spatial attention. Neural oscillations characterize functional interactions between the frontal eye fields (FEF) and the lateral intraparietal area (LIP), with theta phase (3–8 Hz) coordinating two rhythmically alternating states. The first is defined by FEF-dominated beta-band activity, associated with suppressed attentional shifts, and LIP-dominated gamma-band activity, associated with enhanced visual processing and better behavioral performance. The second is defined by LIP-specific alpha-band activity, associated with attenuated visual processing and worse behavioral performance. Our findings reveal how network-level interactions organize environmental sampling into rhythmic cycles. Fiebelkorn et al. use simultaneous recordings in two hubs of the macaque frontoparietal network to demonstrate a neural basis of rhythmic sampling during spatial attention. Theta-organized, alternating attentional states, characterized by different spatiotemporal dynamics, shape environmental sampling. |
Whitney S. Griggs; Hidetoshi Amita; Atul Gopal; Okihide Hikosaka Visual neurons in the superior colliculus discriminate many objects by their historical values Journal Article In: Frontiers in Neuroscience, vol. 12, pp. 396, 2018. @article{Griggs2018,The superior colliculus (SC) is an important structure in the mammalian brain that orients the animal towards distinct visual events. Visually-responsive neurons in SC are modulated by visual object features, including size, motion, and color. However, it remains unclear whether SC activity is modulated by non-visual object features, such as the reward value associated with the object. To address this question, three monkeys were trained (>10 days) to saccade to multiple fractal objects, half of which were consistently associated with large reward while other half were associated with small reward. This created historically high-valued (‘good') and low-valued (‘bad') objects. During the neuronal recordings from the SC, the monkeys maintained fixation at the center while the objects were flashed in the receptive field of the neuron without any reward. We found that approximately half of the visual neurons responded more strongly to the good than bad objects. In some neurons, this value-coding remained intact for a long time (>1 year) after the last object-reward association learning. Notably, the neuronal discrimination of reward values started about 100 ms after the appearance of visual objects and lasted for more than 100 ms. These results provide evidence that SC neurons can discriminate objects by their historical (long-term) values. This object value information may be provided by the basal ganglia, especially the circuit originating from the tail of the caudate nucleus. The information may be used by the neural circuits inside SC for motor (saccade) output or may be sent to the circuits outside SC for future behavior. |
Marcel Jan Haan; Thomas Brochier; Sonja Grün; Alexa Riehle; Frédéric V. Barthélemy Real-time visuomotor behavior and electrophysiology recording setup for use with humans and monkeys Journal Article In: Journal of Neurophysiology, vol. 120, no. 2, pp. 539–552, 2018. @article{Haan2018a,Large-scale network dynamics in multiple visuomotor areas is of great interest in the study of eye-hand coordination in both human and monkey. To explore this, it is essential to develop a setup that allows for precise tracking of eye and hand movements. It is desirable that it is able to generate mechanical or visual perturbations of hand trajec- tories so that eye-hand coordination can be studied in a variety of conditions. There are simple solutions that satisfy these requirements for hand movements performed in the horizontal plane while visual stimuli and hand feedback are presented in the vertical plane. How- ever, this spatial dissociation requires cognitive rules for eye-hand coordination different from eye-hand movements performed in the same space, as is the case in most natural conditions. Here we present an innovative solution for the precise tracking of eye and hand movements in a single reference frame. Importantly, our solution allows behavioral explorations under normal and perturbed conditions in both humans and monkeys. It is based on the integration of two noninvasive commercially available systems to achieve online control and synchronous recording of eye (EyeLink) and hand (KINARM) positions during interactive visuomotor tasks. We also present an eye calibration method compatible with different eye trackers that com- pensates for nonlinearities caused by the system's geometry. Our setup monitors the two effectors in real time with high spatial and temporal resolution and simultaneously outputs behavioral and neu- ronal data to an external data acquisition system using a common data format. |
Christopher K. Hauser; Dantong Zhu; Terrence R. Stanford; Emilio Salinas Motor selection dynamics in FEF explain the reaction time variance of saccades to single targets Journal Article In: eLife, vol. 7, pp. 1–32, 2018. @article{Hauser2018,In studies of voluntary movement, a most elemental quantity is the reaction time (RT) between the onset of a visual stimulus and a saccade toward it. However, this RT demonstrates extremely high variability which, in spite of extensive research, remains unexplained. It is well established that, when a visual target appears, oculomotor activity gradually builds up until a critical level is reached, at which point a saccade is triggered. Here, based on computational work and single-neuron recordings from monkey frontal eye field (FEF), we show that this rise-to-threshold process starts from a dynamic initial state that already contains other incipient, internally driven motor plans, which compete with the target-driven activity to varying degrees. The ensuing conflict resolution process, which manifests in subtle covariations between baseline activity, build-up rate, and threshold, consists of fundamentally deterministic interactions, and explains the observed RT distributions while invoking only a small amount of intrinsic randomness.As we examine the space around us our eyes move in short steps, looking toward a new location about four times a second. Neurons in a region of the brain called the frontal eye field help initiate these eye movements, which are known as saccades. Each neuron contributes to a saccade with a specific direction and size. Before a saccade, the relevant neurons in the frontal eye field steadily increase their activity. When this activity reaches a critical threshold, the visual system issues a command to move the eyes in the appropriate direction. So a saccade that moves the eyes to the right requires a specific group of neurons to be strongly activated – but, at the same time, the neurons responsible for movement to the left need to be less active.Imagine that you have to move your eyes as quickly as possible to look at a spot of light that appears on a screen. Some of the time your eyes will start to move about 100 milliseconds after the light appears. But on other attempts, your eyes will not start moving until 300 milliseconds after the light came on. What causes this variability?To find out, Hauser et al. recorded from neurons in monkeys trained to perform such a task. When the spot of light appeared many different neurons were active, suggesting there is conflict between the plan that would move the eyes toward the target and plans to look at other locations. That is, when the target appears, the monkey is already thinking of looking somewhere. The time required to resolve this conflict depends on how far apart the target and the competing locations are from one another, and on how much the competing neurons have increased their activity before the target appears.Similar mechanisms are likely to operate when we sit at the dinner table and look for the salt shaker, for example, and so the results presented by Hauser et al. will help us to understand how we direct our attention to different points in space. Understanding how these processes work in more detail will help us to discern what happens when they go wrong, as occurs in attention deficit disorders like ADHD. |
Masato Inoue; Shigeru Kitazawa Motor error in parietal area 5 and target error in area 7 drive distinctive adaptation in reaching Journal Article In: Current Biology, vol. 28, pp. 2250–2262, 2018. @article{Inoue2018,Errors in reaching drive trial-by-trial adaptation to compensate for the error. Parietal association areas are implicated in error coding, but whether the parietal error signals directly drive adaptation remains unknown. We first examined the activity of neurons in areas 5 and 7 while two monkeys performed rapid target reaching to clarify whether and how the parietal error signals drive adaptation in reaching. We introduced random errors using a motor-driven prism device to augment random motor errors in reaching. Neurons in both regions encoded information on the target position prior to reaching and information on the motor error after reaching. However, post-movement microstimulation caused trial-by-trial adaptation to cancel the motor error only when it was delivered to area 5. By contrast, stimulation to area 7 caused trial-by-trial adaptation so that the reaching endpoint was adjusted toward the target position. We further hypothesized that area 7 would encode target error that is caused by a target jump during the reach, and our results support this hypothesis. Area 7 neurons encoded target error information, but area 5 neurons did not encode this information. These results suggest that area 5 provides signals for adapting to motor errors and that area 7 provides signals to adapt to target errors. |
Kevin D. Johnston; Kevin Barker; David J. Schaeffer; Lauren Schaeffer; Stefan Everling Methods for chair restraint and training of the common marmoset on oculomotor tasks Journal Article In: Journal of Neurophysiology, vol. 119, no. 5, pp. 1636–1646, 2018. @article{Johnston2018,The oculomotor system is the most thoroughly understood sensorimotor system in the brain, due in large part to electrophysiological studies carried out in macaque monkeys trained to perform oculomotor tasks. A disadvantage of the macaque model is that many cortical oculomotor areas of interest lie within sulci, making high-density array and laminar recordings impractical. Many techniques of molecular biology developed in rodents, such as optogenetic manipulation of neuronal subtypes, are also limited in this species. The common marmoset (Callithrix jacchus) possesses a smooth cortex, allowing easy access to frontoparietal oculomotor areas, and may bridge the gap between systems neuroscience in macaques and molecular techniques. Techniques for restraint, training, and neural recording in these animals have been well developed in auditory neuroscience. Those for oculomotor neuroscience, however, remain at a relatively early stage. In this article we provide details of a custom-designed restraint chair for marmosets, a combination head restraint/recording chamber allowing access to cortical oculomotor areas and providing stability suitable for eye movement and neural recordings, as well as a training protocol for oculomotor tasks. We additionally report the results of a psychophysical study in marmosets trained to perform a saccade task using these methods, showing that, as in rhesus and humans, marmosets exhibit a “gap effect,” a decrease in reaction time when the fixation stimulus is removed before the onset of a visual saccade target. These results are the first evidence of this effect in marmosets and support the common marmoset model for neurophysiological investigations of oculomotor control. |
Peter Kaposvari; Susheel Kumar; Rufin Vogels Statistical learning signals in macaque inferior temporal cortex Journal Article In: Cerebral Cortex, vol. 28, no. 1, pp. 250–266, 2018. @article{Kaposvari2018,Humans are sensitive to statistical regularities in their visual environment, but the nature of the underlying neural statistical learning signals still remains to be clarified. As in human behavioral and neuroimaging studies of statistical learning, we exposed rhesus monkeys to a continuous stream of images, presented without interstimulus interval or reward association. The stimulus set consisted of 3 groups of 5 images each (quintets). The stimulus order within each quintet was fixed, but the quintets were presented repeatedly in a random order without interruption. Thus, only transitional probabilities defined quintets of images. Postexposure recordings in inferior temporal (IT) cortex showed an enhanced response to stimuli that violated the exposed sequence. This enhancement was found only for stimuli that were not predicted by the just preceding stimulus, reflecting a temporally adjacent stimulus relationship, and was sensitive to stimulus order. By comparing IT responses with sequences with and without statistical regularities, we observed a short latency, transient response suppression for stimuli of the sequence with regularities, in addition to a later sustained response enhancement to stimuli that violated the sequence with regularities. These findings constrain models of mechanisms underlying neural responses in predictable temporal sequences, such as predictive coding. |
Katsuhisa Kawaguchi; Stephane Clery; Paria Pourriahi; Lenka Seillier; Ralf M. Haefner; Hendrikje Nienborg Differentiating between models of perceptual decision making using pupil size inferred confidence Journal Article In: Journal of Neuroscience, vol. 38, no. 41, pp. 8874–8888, 2018. @article{Kawaguchi2018,During perceptual decisions, subjects often rely more strongly on early, rather than late, sensory evidence, even in tasks when both are equally informative about the correct decision. This early psychophysical weighting has been explained by an integration-to-bound decision process, in which the stimulus is ignored after the accumulated evidence reaches a certain bound, or confidence level. Here, we derive predictions about how the average temporal weighting of the evidence depends on a subject's decision confidence in this model. To test these predictions empirically, we devised a method to infer decision confidence from pupil size in 2 male monkeys performing a disparity discrimination task. Our animals' data confirmed the integration-to-bound predictions, with different internal decision bounds and different levels of correlation between pupil size and decision confidence accounting for differences between animals. However, the data were less compatible with two alternative accounts for early psychophysical weighting: attractor dynamics either within the decision area or due to feedback to sensory areas, or a feedforward account due to neuronal response adaptation. This approach also opens the door to using confidence more broadly when studying the neural basis of decision making. |
Jonas Knöll; Jonathan W. Pillow; Alexander C. Huk Lawful tracking of visual motion in humans, macaques, and marmosets in a naturalistic, continuous, and untrained behavioral context Journal Article In: Proceedings of the National Academy of Sciences, vol. 115, no. 44, pp. E10486–E10494, 2018. @article{Knoell2018,Much study of the visual system has focused on how humans and monkeys integrate moving stimuli over space and time. Such assessments of spatiotemporal integration provide fundamental grounding for the interpretation of neurophysiological data, as well as how the resulting neural signals support perceptual deci- sions and behavior. However, the insights supported by classical characterizations of integration performed in humans and rhesus monkeys are potentially limited with respect to both generality and detail: Standard tasks require extensive amounts of training, involve abstract stimulus–response mappings, and depend on combining data across many trials and/or sessions. It is thus of concern that the integration observed in classical tasks involves the recruitment of brain circuits that might not normally subsume natural behaviors, and that quantitative analyses have limited power for characterizing single-trial or single-session processes. Here we bridge these gaps by showing that three primate species (humans, macaques, and marmosets) track the focus of expansion of an optic flow field continuously and without substantial training. This flow-tracking behavior was volitional and reflected substantial temporal integration. Most strikingly, gaze patterns exhibited lawful and nuanced dependencies on random perturbations in the stimulus, such that repetitions of identical flow movies elicited remarkably similar eye movements over long and continuous time periods. These results demonstrate the generality of spatiotemporal integration in natural vision, and offer a means for studying integration outside of artificial tasks while maintaining lawful and highly reliable behavior. |
Matthew L. Leavitt; Florian Pieper; Adam J. Sachs; Julio C. Martinez-Trujillo A quadrantic bias in prefrontal representation of visual-mnemonic space Journal Article In: Cerebral Cortex, vol. 28, no. 7, pp. 2405–2421, 2018. @article{Leavitt2018,Single neurons in primate dorsolateral prefrontal cortex (dLPFC) are known to encode working memory (WM) representations of visual space. Psychophysical studies have shown that the horizontal and vertical meridians of the visual field can bias spatial information maintained in WM. However, most studies and models have tacitly assumed that dLPFC neurons represent mnemonic space homogenously. The anatomical organization of these representations has also eluded clear parametric description. We investigated these issues by recording from neuronal ensembles in macaque dLPFC with microelectrode arrays while subjects performed an oculomotor delayed-response task. We found that spatial WM representations in macaque dLPFC are biased by the vertical and horizontal meridians of the visual field, dividing mnemonic space into quadrants. This bias is reflected in single neuron firing rates, neuronal ensemble representations, the spike count correlation structure, and eye movement patterns. We also found that dLPFC representations of mnemonic space cluster anatomically in a nonretinotopic manner that partially reflects the organization of visual space. These results provide an explanation for known WM biases, and reveal novel principles of WM representation in prefrontal neuronal ensembles and across the cortical surface, as well as the need to reconceptualize models of WM to accommodate the observed representational biases. |
Aaron J. Levi; Jacob L. Yates; Alexander C. Huk; Leor N. Katz Strategic and dynamic temporal weighting for perceptual decisions in humans and macaques Journal Article In: eNeuro, vol. 5, no. 5, pp. 1–15, 2018. @article{Levi2018,Perceptual decision-making is often modeled as the accumulation of sensory evidence over time. Recent studies using psychophysical reverse correlation have shown that even though the sensory evidence is stationary over time, subjects may exhibit a time-varying weighting strategy, weighting some stimulus epochs more heavily than others. While previous work has explained time-varying weighting as a consequence of static decision mechanisms (e.g., decision bound or leak), here we show that time-varying weighting can reflect strategic adaptation to stimulus statistics, and thus can readily take a number of forms. We characterized the temporal weighting strategies of humans and macaques performing a motion discrimination task in which the amount of information carried by the motion stimulus was manipulated over time. Both species could adapt their temporal weighting strategy to match the time-varying statistics of the sensory stimulus. When early stimulus epochs had higher mean motion strength than late, subjects adopted a pronounced early weighting strategy, where early information was weighted more heavily in guiding perceptual decisions. When the mean motion strength was greater in later stimulus epochs, in contrast, subjects shifted to a marked late weighting strategy. These results demonstrate that perceptual decisions involve a temporally flexible weighting process in both humans and monkeys, and introduce a paradigm with which to manipulate sensory weighting in decision-making tasks. |
Liu D. Liu; Kenneth D. Miller; Christopher C. Pack A unifying motif for spatial and directional surround suppression Journal Article In: Journal of Neuroscience, vol. 38, no. 4, pp. 989–999, 2018. @article{Liu2018c,In the visual system, the response to a stimulus in a neuron's receptive field can be modulated by stimulus context, and the strength of these contextual influences vary with stimulus intensity. Recent work has shown how a theoretical model, the stabilized supralinear network (SSN), can account for such modulatory influences, using a small set of computational mechanisms. While the predictions of the SSN have been confirmed in primary visual cortex (V1), its computational principles apply with equal validity to any cortical structure. We have therefore tested the generality of the SSN by examining modulatory influences in the middle temporal area (MT) of the macaque visual cortex, using electrophysiological recordings and pharmacological manipulations. We developed a novel stimulus that can be adjusted parametrically to be larger or smaller in the space of all possible motion directions. We found, as predicted by the SSN, that MT neurons integrate across motion directions for low-contrast stimuli, but that they exhibit suppression by the same stimuli when they are high in contrast. These results are analogous to those found in visual cortex when stimulus size is varied in the space domain. We further tested the mechanisms of inhibition using pharmacologically manipulations of inhibitory efficacy. As predicted by the SSN, local manipulation of inhibitory strength altered firing rates, but did not change the strength of surround suppression. These results are consistent with the idea that the SSN can account for modulatory influences along different stimulus dimensions and in different cortical areas. |
Kaleb A. Lowe; Jeffrey D. Schall Functional categories of visuomotor neurons in macaque frontal eye field Journal Article In: eNeuro, vol. 5, no. 5, pp. 1–21, 2018. @article{Lowe2018,Frontal eye field (FEF) in macaque monkeys contributes to visual attention, visual-motor transformations and production of eye movements. Traditionally, neurons in FEF have been classified by the magnitude of increased discharge rates following visual stimulus presentation, during a waiting period, and associated with eye movement production. However, considerable heterogeneity remains within the traditional visual, visuomovement and movement categories. Cluster analysis is a data-driven method of identifying self-segregating groups within a dataset. Because many cluster analysis techniques exist and outcomes vary with analysis assumptions, consensus clustering aggregates over multiple analyses, identifying robust groups. To describe more comprehensively the neuronal composition of FEF, we applied a consensus clustering technique for unsupervised categorization of patterns of spike rate modulation measured during a memory-guided saccade task. We report ten functional categories, expanding on the traditional three. Categories were distinguished by latency, magnitude, and sign of visual response, presence of sustained activity, and dynamics, magnitude and sign of saccade-related modulation. Consensus clustering can include other metrics and can be applied to datasets from other brain regions to provide better information guiding microcircuit models of cortical function. |
Eric Lowet; Bruno Gomes; Karthik Srinivasan; Huihui Zhou; Robert John Schafer; Robert Desimone Enhanced neural processing by covert attention only during microsaccades directed toward the attended stimulus Journal Article In: Neuron, vol. 99, no. 1, pp. 207–214.e3, 2018. @article{Lowet2018,Attention can be “covertly” directed without eye movements; yet, even during fixation, there are continuous microsaccades (MSs). In areas V4 and IT of macaques, we found that firing rates and stimulus representations were enhanced by attention but only following a MS toward the attended stimulus. The onset of neural attentional modulations was tightly coupled to the MS onset. The results reveal a major link between the effects of covert attention on cortical visual processing and the overt movement of the eyes. |
Yiliang Lu; Jiapeng Yin; Zheyuan Chen; Hongliang Gong; Ye Liu; Liling Qian; Xiaohong Li; Rui Liu; Ian Max Andolina; Wei Wang Revealing detail along the visual hierarchy: Neural clustering preserves acuity from V1 to V4 Journal Article In: Neuron, vol. 98, no. 2, pp. 417–428.e3, 2018. @article{Lu2018a,How primates perceive objects along with their detailed features remains a mystery. This ability to make fine visual discriminations depends upon a high-acuity analysis of spatial frequency (SF) along the visual hierarchy from V1 to inferotemporal cortex. By studying the transformation of SF across macaque parafoveal V1, V2, and V4, we discovered SF-selective functional domains in V4 encoding higher SFs up to 12 cycles/°. These intermittent higher-SF-selective domains, surrounded by domains encoding lower SFs, violate the inverse relationship between SF preference and retinal eccentricity. The neural activities of higher- and lower-SF domains correspond to local and global features, respectively, of the same stimuli. Neural response latencies in high-SF domains are around 10 ms later than in low-SF domains, consistent with the coarse-to-fine nature of perception. Thus, our finding of preserved resolution from V1 into V4, separated both spatially and temporally, may serve as a connecting link for detailed object representation. How do we perceive scenes or objects yet resolve their fine details? Lu et al. found that high spatial detail organizes in spatiotemporally separated neural clusters within primate intermediate area V4, preserving visual acuity from early toward higher cortical areas. |
Thomas Zhihao Luo; John H. R. Maunsell Attentional changes in either criterion or sensitivity are associated with robust modulations in lateral prefrontal cortex Journal Article In: Neuron, vol. 97, no. 6, pp. 1382–1393.e7, 2018. @article{Luo2018a,Visual attention is associated with neuronal changes across the brain, and these widespread signals are generally assumed to underlie a unitary mechanism of attention. However, using signal detection theory, attention-related effects on performance can be partitioned into changes in either the subject's criterion or sensitivity. Neuronal modulations associated with only sensitivity changes were previously observed in visual cortex, raising questions about which structures mediate attention-related changes in criterion and whether individual neurons are involved in multiple components of attention. Here, we recorded from monkey lateral prefrontal cortex (LPFC) and found that, in contrast to visual cortex, neurons in LPFC changed their firing rates, pairwise correlation, and Fano factor when subjects changed either their criterion or their sensitivity. These results indicate that attention-related neuronal modulations in separate brain regions are not a monolithic signal and instead can be linked to distinct behavioral changes. Luo and Maunsell show that the modulations in prefrontal cortex correspond to multiple components of attention and differ from modulations in visual cortex, indicating that different brain structures underlie distinct attentional mechanisms and that attention is not a unitary process. |
Liya Ma; Kevin J. Skoblenick; Kevin D. Johnston; Stefan Everling Ketamine alters lateral prefrontal oscillations in a rule-based working memory gask Journal Article In: Journal of Neuroscience, vol. 38, no. 10, pp. 2482–2494, 2018. @article{Ma2018a,Acute administration of N-methyl-D-aspartate receptor (NMDAR) antagonists in healthy humans and animals produces working memory deficits similar to those observed in schizophrenia. However, it is unclear whether they also lead to altered low-frequency (<=60Hz) neural oscillatory activities similar to those associated with schizophrenia during working memory processes. Here we recorded local field potentials (LFPs) and single unit activity from the lateral prefrontal cortex (LPFC) of three male rhesus macaque monkeys while they performed a rule-based prosaccade and antisaccade working memory task, both before and after systemic injections of a subanesthetic dose (<=0.7mg/kg) of ketamine. Accompanying working-memory impairment, ketamine enhanced the low gamma band (30-60Hz) and dampened the beta band (13-30Hz) oscillatory activities in the LPFC during both delay periods and inter-trial intervals. It also increased task-related alpha-band activities, likely reflecting compromised attention. Beta-band oscillations may be especially relevant to working memory processes, as stronger beta power weakly but significantly predicted shorter saccadic reaction time. Also in beta band, ketamine reduced the performance-related oscillation as well as the rule information encoded in the spectral power. Ketamine also reduced rule information in the spike-field phase consistency in almost all frequencies up to 60Hz. Our findings support NMDAR antagonists in non-human primates as a meaningful model for altered neural oscillations and synchrony, which reflect a disorganized network underlying the working memory deficits in schizophrenia. |
Kazutaka Maeda; Jun Kunimatsu; Okihide Hikosaka Amygdala activity for the modulation of goal-directed behavior in emotional contexts Journal Article In: PLoS Biology, vol. 16, no. 6, pp. e2005339, 2018. @article{Maeda2018,Choosing valuable objects and rewarding actions is critical for survival. While such choices must be made in a way that suits the animal's circumstances, the neural mechanisms underlying such context-appropriate behavior are unclear. To address this question, we devised a context-dependent reward-seeking task for macaque monkeys. Each trial started with the appearance of one of many visual scenes containing two or more objects, and the monkey had to choose the good object by saccade to get a reward. These scenes were categorized into two dimensions of emotional context: dangerous versus safe and rich versus poor. We found that many amygdala neurons were more strongly activated by dangerous scenes, by rich scenes, or by both. Furthermore, saccades to target objects occurred more quickly in dangerous than in safe scenes and were also quicker in rich than in poor scenes. Thus, amygdala neuronal activity and saccadic reaction times were negatively correlated in each monkey. These results suggest that amygdala neurons facilitate targeting saccades predictably based on aspects of emotional context, as is necessary for goal-directed and social behavior. |
Alex J. Major; Susheel Vijayraghavan; Stefan Everling Cholinergic overstimulation attenuates rule selectivity in macaque prefrontal cortex Journal Article In: Journal of Neuroscience, vol. 38, no. 5, pp. 1137–1150, 2018. @article{Major2018,Acetylcholine is released in the prefrontal cortex (PFC) and is a key modulator of cognitive performance in primates. Cholinergic stimulation has been shown to have beneficial effects on performance of cognitive tasks, and cholinergic receptors are being actively explored as promising targets for ameliorating cognitive deficits in Alzheimer's disease.Wehypothesized that cholinergic stimulation of PFC during performance of a cognitive task would augment neuronal activity and neuronal coding of task attributes. We iontophoretically applied the general cholinergic receptor agonist carbachol onto neurons in dorsolateral PFC (DLPFC) of male rhesus macaques performing rule-guided prosaccades and antisaccades, a well established oculomotor task for testing cognitive control. Carbachol application had heterogeneous effects on neuronal excitability, with both excitation and suppression observed in significant proportions. Contrary to our prediction, neurons with rule-selective activity exhibited a reduction in selectivity during carbachol application. Cholinergic stimulation disrupted rule selectivity regardless of whether it had suppressive or excitatory effects on these neurons. In addition, cholinergic stimulation excited putative pyramidal neurons, whereas the activity of putative interneurons remained unchanged. Moreover, cholinergic stimulation attenuated saccade direction selectivity in putative pyramidal neurons due to nonspecific increases in activity. Our results suggest excessive cholinergic stimulation has detrimental effects on DLPFC representations of task attributes. These findings delineate the complexity and heterogeneity of neuromodulation of cerebral cortex by cholinergic stimulation, an area of active exploration with respect to the development of cognitive enhancers. |
Alexandria C. Marino; James A. Mazer Saccades trigger predictive updating of attentional topography in area V4 Journal Article In: Neuron, vol. 98, no. 2, pp. 429–438.e4, 2018. @article{Marino2018,During natural behavior, saccades and attention act together to allocate limited neural resources. Attention is generally mediated by retinotopic visual neurons; therefore, specific neurons representing attended features change with each saccade. We investigated the neural mechanisms that allow attentional targeting in the face of saccades. Specifically, we looked for predictive changes in attentional modulation state or receptive field position that could stabilize attentional representations across saccades in area V4, known to be necessary for attention-dependent behavior. We recorded from neurons in monkeys performing a novel spatiotopic attention task, in which performance depended on accurate saccade compensation. Measurements of attentional modulation revealed a predictive attentional “hand-off” corresponding to a presaccadic transfer of attentional state from neurons inside the attentional focus before the saccade to those that will be inside the focus after the saccade. The predictive nature of the hand-off ensures that attentional brain maps are properly configured immediately after each saccade. Using a novel behavioral task, Marino and Mazer report that the attentional modulation state of neurons in extrastriate area V4 is updated before saccade onset. This attentional hand-off is independent of changes in receptive field position and represents a new type of perisaccadic updating. |
Yaser Merrikhi; Kelsey Clark; Behrad Noudoost Concurrent influence of top-down and bottom-up inputs on correlated activity of Macaque extrastriate neurons Journal Article In: Nature Communications, vol. 9, pp. 5393, 2018. @article{Merrikhi2018,Correlations between neurons can profoundly impact the information encoding capacity of a neural population. We studied how maintenance of visuospatial information affects correlated activity in visual areas by recording the activity of neurons in visual area MT of rhesus macaques during a spatial working memory task. Correlations between MT neurons depended upon the spatial overlap between neurons' receptive fields. These correlations were influenced by the content of working memory, but the effect of a top-down memory signal differed in the presence or absence of bottom-up visual input. Neurons representing the same area of space showed increased correlations when remembering a location in their receptive fields in the absence of visual input, but decreased correlations in the presence of a visual stimulus. This set of results reveals the correlating nature of top-down signals influencing visual areas and uncovers how such a correlating signal, in interaction with bottom-up information, could enhance sensory representations. |
Jérôme Munuera; Mattia Rigotti; C. Daniel Salzman Shared neural coding for social hierarchy and reward value in primate amygdala Journal Article In: Nature Neuroscience, vol. 21, no. 3, pp. 415–423, 2018. @article{Munuera2018,The social brain hypothesis posits that dedicated neural systems process social information. In support of this, neurophysiological data have shown that some brain regions are specialized for representing faces. It remains unknown, however, whether distinct anatomical substrates also represent more complex social variables, such as the hierarchical rank of individuals within a social group. Here we show that the primate amygdala encodes the hierarchical rank of individuals in the same neuronal ensembles that encode the rewards associated with nonsocial stimuli. By contrast, orbitofrontal and anterior cingulate cortices lack strong representations of hierarchical rank while still representing reward values. These results challenge the conventional view that dedicated neural systems process social information. Instead, information about hierarchical rank—which contributes to the assessment of the social value of individuals within a group—is linked in the amygdala to representations of rewards associated with nonsocial stimuli. |
James E. Niemeyer; Michael A. Paradiso Saccade-based termination responses in macaque V1 and visual perception Journal Article In: Visual Neuroscience, vol. 35, pp. e025, 2018. @article{Niemeyer2018,Neurons in visual areas of the brain are generally characterized by the increase in firing rate that occurs when a stimulus is flashed on in the receptive field (RF). However, neurons also increase their firing rate when a stimulus is turned off. These “termination responses” or “after-discharges” that occur with flashed stimuli have been observed in area V1 and they may be important for vision as stimulus terminations have been shown to influence visual perception. The goal of the present study was to determine the strength of termination responses in the more natural situation in which eye movements move a stimulus out of an RF. We find that termination responses do occur in macaque V1 when termination results from a saccadic eye movement, but they are smaller in amplitude compared to flashed-off stimuli. Furthermore, there are termination responses even in the absence of visual stimulation. These findings demonstrate that termination responses are a component of naturalistic vision. They appear to be based on both visual and nonvisual signals in visual cortex. We speculate that the weakening of termination responses might be a neural correlate of saccadic suppression, the loss of perceptual sensitivity around the time of saccades. |
Atsushi Noritake; Taihei Ninomiya; Masaki Isoda Social reward monitoring and valuation in the macaque brain Journal Article In: Nature Neuroscience, vol. 21, no. 10, pp. 1452–1462, 2018. @article{Noritake2018,Behaviors are influenced by rewards to both oneself and others, but the neurons and neural connections that monitor and evaluate rewards in social contexts are unknown. To address this issue, we devised a social Pavlovian conditioning procedure for pairs of monkeys. Despite being constant in amount and probability, the subjective value of forthcoming self-rewards, as indexed by licking and choice behaviors, decreased as partner-reward probability increased. This value modulation was absent when the conspecific partner was replaced by a physical object. Medial prefrontal cortex neurons selectively monitored self-reward and partner-reward information, whereas midbrain dopaminergic neurons integrated this information into a subjective value. Recordings of local field potentials revealed that responses to reward-predictive stimuli in medial prefrontal cortex started before those in dopaminergic midbrain nuclei and that neural information flowed predominantly in a medial prefrontal cortex-to-midbrain direction. These findings delineate a dedicated pathway for subjective reward evaluation in social environments. |
Takaya Ogasawara; Masafumi Nejime; Masahiko Takada; Masayuki Matsumoto Primate nigrostriatal dopamine system regulates saccadic response inhibition Journal Article In: Neuron, vol. 100, no. 6, pp. 1513–1526.e4, 2018. @article{Ogasawara2018,Animals need to inhibit inappropriate actions that would lead to unwanted outcomes. Although this ability, called response inhibition, is impaired in neurological/psychiatric disorders with dopaminergic dysfunctions, how dopamine regulates response inhibition remains unclear. Here we investigated neuronal signals of the nigrostriatal dopamine system in monkeys performing a saccadic countermanding task. Subsets of dopamine neurons in the substantia nigra and striatal neurons receiving the dopaminergic input were activated when the monkey was required to cancel a planned saccadic eye movement. These activations were stronger when canceling the eye movements was successful compared with failed and were enhanced in demanding trials. The activated dopamine neurons were distributed mainly in the dorsolateral, but not in the ventromedial, part of the nigra. Furthermore, pharmacological blockade of dopaminergic neurotransmission in the striatum dampened the performance of canceling saccadic eye movements. The present findings indicate that disruption of nigrostriatal dopamine signaling causes impairments in response inhibition. |
Timothy D. Oleskiw; Amy Nowack; Anitha Pasupathy Joint coding of shape and blur in area V4 Journal Article In: Nature Communications, vol. 9, pp. 466, 2018. @article{Oleskiw2018,Edge blur, a prevalent feature of natural images, is believed to facilitate multiple visual processes including segmentation and depth perception. Furthermore, image descriptions that explicitly combine blur and shape information provide complete representations of naturalistic scenes. Here we report the first demonstration of blur encoding in primate visual cortex: neurons in macaque V4 exhibit tuning for both object shape and boundary blur, with observed blur tuning not explained by potential confounds including stimulus size, intensity, or curvature. A descriptive model wherein blur selectivity is cast as a distinct neural process that modulates the gain of shape-selective V4 neurons explains observed data, supporting the hypothesis that shape and blur are fundamental features of a sufficient neural code for natural image representation in V4. |
Adam Pallus; Mark M. G. Walton; Michael J. Mustari Activity of near-response cells during disconjugate saccades in strabismic monkeys Journal Article In: Journal of Neurophysiology, vol. 120, no. 5, pp. 2282–2295, 2018. @article{Pallus2018,Infantile strabismus is a common disorder characterized by a chronic misalignment of the eyes, impairment of binocular vision, and oculomotor abnormalities. Nonhuman primates with strabismus, induced in infancy, show a pattern of abnormalities similar to those of strabismic children. This allows strabismic nonhuman primates to serve as an ideal animal model to examine neural mechanisms associated with aberrant oculomotor behavior. Here, we test the hypothesis that impairment of disparity vergence and horizontal saccade disconjugacy in exotropia and esotropia are associated with disrupted tuning of near-and far-response neurons in the supraoculomotor area (SOA). In normal animals, these neurons carry signals related to vergence position and/or velocity. We hypothesized that, in strabismus, these neurons modulate inappropriately in association with saccades between equidistant targets. We recorded from 62 SOA neurons from 4 strabismic animals (2 esotropes and 2 exotropes) during visually guided saccades to a target that stepped to different locations on a tangent screen. Under these same conditions, SOA neurons in normal animals show no detectable modulation. In our strabismic subjects, we found that a subset of SOA neurons carry weak vergence velocity signals during saccades. In addition, a subset of SOA neurons showed clear modulation associated with slow fluctuations of horizontal strabismus angle in the absence of a saccade. We suggest that abnormal SOA activity contributes to fixation instability but plays only a minor role in the horizontal disconjugacy of saccades that do not switch fixation from one eye to the other. NEW & NOTEWORTHY The present study is the first to investigate the activity of neurons in the supraoculomotor area (SOA) during horizontally disconjugate saccades in a nonhuman primate model of infantile strabismus. We report that fluctuations of horizontal strabismus angle, during fixation of static targets on a tangent screen, are associated with contextually inappropriate modulation of SOA activity. However, firing rate modulation during saccades is too weak to make a major contribution to horizontal disconjugacy. |
Angelo Pirrone; Habiba Azab; Benjamin Y. Hayden; Tom Stafford; James A. R. Marshall Evidence for the speed–value trade-Off: Human and monkey decision making Is magnitude sensitive Journal Article In: Decision, vol. 5, no. 2, pp. 129–142, 2018. @article{Pirrone2018,Complex natural systems from brains to bee swarms have evolved to make adaptive multifactorial decisions. Recent theoretical and empirical work suggests that many evolved systems may take advantage of common motifs across multiple domains. We are particularly interested in value sensitivity (i.e., sensitivity to the magnitude or intensity of the stimuli or reward under consideration) as a mechanism to resolve deadlocks adaptively. This mechanism favors long-term reward maximization over accuracy in a simple manner, because it avoids costly delays associated with ambivalence between similar options; speed–value trade-offs have been proposed to be evolutionarily advantageous for many kinds of decision. A key prediction of the value-sensitivity hypothesis is that choices between equally valued options will proceed faster when the options have a high value than when they have a low value. However, value sensitivity is not part of idealized choice models such as diffusion to bound. Here, we examine 2 different choice behaviors in 2 different species, perceptual decisions in humans and economic choices in rhesus monkeys, to test this hypothesis. We observe the same value sensitivity in both human perceptual decisions and monkey value-based decisions. These results endorse the idea that neural decision systems make use of the same basic principle of value sensitivity in order to resolve costly deadlocks and thus improve long-term reward intake. |
Evan D. Remington; Devika Narain; Eghbal A. Hosseini; Mehrdad Jazayeri Flexible sensorimotor computations through rapid reconfiguration of cortical dynamics Journal Article In: Neuron, vol. 98, no. 5, pp. 1005–1019.e5, 2018. @article{Remington2018a,Neural mechanisms that support flexible sensorimotor computations are not well understood. In a dynamical system whose state is determined by interactions among neurons, computations can be rapidly reconfigured by controlling the system's inputs and initial conditions. To investigate whether the brain employs such control mechanisms, we recorded from the dorsomedial frontal cortex of monkeys trained to measure and produce time intervals in two sensorimotor contexts. The geometry of neural trajectories during the production epoch was consistent with a mechanism wherein the measured interval and sensorimotor context exerted control over cortical dynamics by adjusting the system's initial condition and input, respectively. These adjustments, in turn, set the speed at which activity evolved in the production epoch, allowing the animal to flexibly produce different time intervals. These results provide evidence that the language of dynamical systems can be used to parsimoniously link brain activity to sensorimotor computations. Remington et al. employ a dynamical systems perspective to understand how the brain flexibly controls timed movements. Results suggest that neurons in the frontal cortex form a recurrent network whose behavior is flexibly controlled by inputs and initial conditions. |
Thomas R. Reppert; Mathieu Servant; Richard P. Heitz; Jeffrey D. Schall In: Journal of Neurophysiology, vol. 120, no. 1, pp. 372–384, 2018. @article{Reppert2018,Balancing the speed-accuracy tradeoff (SAT) is necessary for successful behavior. Using a visual search task with interleaved cues emphasizing speed or accuracy, we recently reported diverse contributions of frontal eye field (FEF) neurons instantiating salience evidence and response preparation. Here, we report replication of visual search SAT performance in two macaque monkeys, new information about variation of saccade dynamics with SAT, extension of the neurophysiological investigation to describe processes in the superior colliculus (SC), and a description of the origin of search errors in this task. Saccade vigor varied idiosyncratically across SAT conditions and monkeys but tended to decrease with response time. As observed in the FEF, speed-accuracy tradeoff was accomplished through several distinct adjustments in the superior colliculus. In “Accurate” relative to “Fast” trials, visually responsive neurons in SC as in FEF had lower baseline firing rates and later target selection. The magnitude of these adjustments in SC was indistinguishable from that in FEF. Search errors occurred when visual salience neurons in the FEF and the SC treated distractors as targets, even in the Accurate condition. Unlike FEF, the magnitude of visual responses in the SC did not vary across SAT conditions. Also unlike FEF, the activity of SC movement neurons when saccades were initiated was equivalent in Fast and Accurate trials. Saccade-related neural activity in SC, but not FEF, varied with saccade peak velocity. These results extend our understanding of the cortical and subcortical contributions to SAT. |
Douglas A. Ruff; David H. Brainard; Marlene R. Cohen Neuronal population mechanisms of lightness perception Journal Article In: Journal of Neurophysiology, vol. 120, no. 5, pp. 2296–2310, 2018. @article{Ruff2018,The way that humans and animals perceive the lightness of an object depends on its physical luminance as well as its surrounding context. While neuronal responses throughout the visual pathway are modulated by context, the relationship between neuronal responses and lightness perception is poorly understood. We searched for a neuronal mechanism of lightness by recording responses of neuronal populations in monkey primary visual cortex (V1) and area V4 to stimuli that produce a lightness illusion in humans, in which the lightness of a disk depends on the context in which it is embedded. We found that the way individual units encode the luminance (or equivalently for our stimuli, contrast) of the disk and its context is extremely heterogeneous. This motivated us to ask whether the population representation in either V1 or V4 satisfies three criteria: 1) disk luminance is represented with high fidelity, 2) the context surrounding the disk is also represented, and 3) the representations of disk luminance and context interact to create a representation of lightness that depends on these factors in a manner consistent with human psychophysical judgments of disk lightness. We found that populations of units in both V1 and V4 fulfill the first two criteria, but that we cannot conclude that the two types of information in either area interact in a manner that clearly predicts human psychophysical measurements: the interpretation of our population measurements depends on how subsequent areas read out lightness from the population responses. |
Jason M. Samonds; Wilson S. Geisler; Nicholas J. Priebe Natural image and receptive field statistics predict saccade sizes Journal Article In: Nature Neuroscience, vol. 21, no. 11, pp. 1591–1599, 2018. @article{Samonds2018,Humans and other primates sample the visual environment using saccadic eye movements that shift a high-resolution fovea toward regions of interest to create a clear perception of a scene across fixations. Many mammals, however, like mice, lack a fovea, which raises the question of why they make saccades. Here we describe and test the hypothesis that saccades are matched to natural scene statistics and to the receptive field sizes and adaptive properties of neural populations. Specifically, we determined the minimum amplitude of saccades in natural scenes necessary to provide uncorrelated inputs to model neural populations. This analysis predicts the distributions of observed saccade sizes during passive viewing for nonhuman primates, cats, and mice. Furthermore, disrupting the development of receptive field properties by monocular deprivation changed saccade sizes consistent with this hypothesis. Therefore, natural-scene statistics and the neural representation of natural images appear to be critical factors guiding saccadic eye movements. |
Joshua A. Seideman; Terrence R. Stanford; Emilio Salinas Saccade metrics reflect decision-making dynamics during urgent choices Journal Article In: Nature Communications, vol. 9, pp. 2907, 2018. @article{Seideman2018,A perceptual judgment is typically characterized by constructing psychometric and chronometric functions, i.e., by mapping the accuracies and reaction times of motor choices as functions of a sensory stimulus feature dimension. Here, we show that various saccade metrics (e.g., peak velocity) are similarly modulated as functions of sensory cue viewing time during performance of an urgent-decision task. Each of the newly discovered functions reveals the dynamics of the perceptual evaluation process inherent to the underlying judgment. Remarkably, saccade peak velocity correlates with statistical decision confidence, suggesting that saccade kinematics reflect the degree of certainty with which an urgent perceptual decision is made. The data were explained by a race-to-threshold model that also replicates standard performance measures and cortical oculomotor neuronal activity in the task. The results indicate that, although largely stereotyped, saccade metrics carry subtle but reliable traces of the underlying cognitive processes that give rise to each oculomotor choice. |
S. Shushruth; Mark Mazurek; Michael N. Shadlen Comparison of decision-related signals in sensory and motor preparatory responses of neurons in area LIP Journal Article In: Journal of Neuroscience, vol. 38, no. 28, pp. 6350–6365, 2018. @article{Shushruth2018,Neurons in the lateral intraparietal (LIP) area of Macaques exhibit both sensory and oculomotor preparatory responses. During perceptual decision making, the preparatory responses have been shown to track the state of the evolving evidence leading to the decision. The sensory responses are known to reflect categorical properties of visual stimuli, but it is not known whether these responses also track evolving evidence. We recorded neural responses from lateral intraparietal area of 2 female rhesus monkeys during a direction discrimination task. We compared sensory and oculomotor-preparatory responses in the same neurons when either the discriminandum (random dot motion) or an eye movement choice-target was in the neuron's response field. The neural responses in both configurations reflected the strength and direction of motion and were correlated with the animal's choice, albeit more prominently when the choice-target was in the response field. However, the variance and autocorrelation pattern of only the motor preparatory responses reflected the process of evidence accumulation. Simulations suggest that the task related activity of sensory responses could be inherited through lateral interactions with neurons that are carrying evidence accumulation signals in their motor-preparatory responses. The results are consistent with the proposal that evolving decision processes are supported by persistent neural activity in the service of actions or intentions, as opposed to high-order representations of stimulus properties. |
Adam C. Snyder; Deepa Issar; Matthew A. Smith What does scalp electroencephalogram coherence tell us about long-range cortical networks? Journal Article In: European Journal of Neuroscience, pp. 1–16, 2018. @article{Snyder2018,Long-range interactions between cortical areas are undoubtedly a key to the computational power of the brain. For healthy human subjects, the premier method for measuring brain activity on fast timescales is electroencephalography (EEG), and coherence between EEG signals is often used to assay functional connectivity between different brain regions. However, the nature of the underlying brain activity that is reflected in EEG coherence is currently the realm of speculation, because seldom have EEG signals been recorded simultaneously with intracranial recordings near cell bodies in multiple brain areas. Here, we take the early steps towards narrowing this gap in our understanding of EEG coherence by measuring local field potentials with microelectrode arrays in two brain areas (extrastriate visual area V4 and dorsolateral prefrontal cortex) simultaneously with EEG at the nearby scalp in rhesus macaque monkeys. Although we found inter-area coherence at both scales of measurement, we did not find that scalp-level coherence was reliably related to coherence between brain areas measured intracranially on a trial-to-trial basis, despite that scalp-level EEG was related to other important features of neural oscillations, such as trial-to-trial variability in overall amplitudes. This suggests that caution must be exercised when interpreting EEG coherence effects, and new theories devised about what aspects of neural activity long-range coherence in the EEG reflects. |
Adam C. Snyder; Byron M. Yu; Matthew A. Smith Distinct population codes for attention in the absence and presence of visual stimulation Journal Article In: Nature Communications, vol. 9, pp. 4382, 2018. @article{Snyder2018a,Visual neurons respond more vigorously to an attended stimulus than an unattended one. How the brain prepares for response gain in anticipation of that stimulus is not well understood. One prominent proposal is that anticipation is characterized by gain-like modulations of spontaneous activity similar to gains in stimulus responses. Here we test an alternative idea: anticipation is characterized by a mixture of both increases and decreases of spontaneous firing rates. Such a strategy would be adaptive as it supports a simple linear scheme for disentangling internal, modulatory signals from external, sensory inputs. We recorded populations of V4 neurons in monkeys performing an attention task, and found that attention states are signaled by different mixtures of neurons across the population in the presence or absence of a stimulus. Our findings support a move from a stimulation-invariant account of anticipation towards a richer view of attentional modulation in a diverse neuronal population. |
Jessica Taubert; Goedele Van Belle; Rufin Vogels; Bruno Rossion The impact of stimulus size and orientation on individual face coding in monkey face-selective cortex Journal Article In: Scientific Reports, vol. 8, pp. 10339, 2018. @article{Taubert2018,Face-selective neurons in the monkey temporal cortex discharge at different rates in response to pictures of different individual faces. Here we tested whether this pattern of response across single neurons in the face-selective area ML (located in the middle Superior Temporal Sulcus) tolerates two affine transformations; picture-plane inversion, known to decrease the average response of face- selective neurons and the other, stimulus size. We recorded the response of 57 ML neurons in two awake and fixating monkeys. Face stimuli were presented at two sizes (10 and 5 degrees of visual angle) and two orientations (upright and inverted). Different faces elicited distinct patterns of activity across ML neurons that were reliable (i.e., predictable with a classifier) within a specific size and orientation condition. Despite observing a reduction in the average response magnitude of face-selective neurons to inverted faces, compared to upright faces, classifier performance was above chance for both upright and inverted faces. While decoding was largely preserved across changes in stimulus size, a classifier trained with one orientation condition and tested on the other did not lead to performance above chance level. We conclude that different individual faces can be decoded from patterns of responses in the monkey area ML regardless of orientation or size, but with qualitatively different patterns of responses for upright and inverted faces. |
Kasper Vinken; Hans P. Op de Beeck; Rufin Vogels Face repetition probability does not affect repetition suppression in macaque inferotemporal cortex Journal Article In: Journal of Neuroscience, vol. 38, no. 34, pp. 7492–7504, 2018. @article{Vinken2018,Repetition suppression, which refers to reduced neural activity for repeated stimuli, is typically explained by bottom-up or local adaptation mechanisms. However, recent theories have emphasized the role of top-down processes, suggesting that this response reduction reflects the fulfillment of perceptual expectations. To support this, an influential human functional magnetic resonance imaging (fMRI) study showed that the magnitude of suppression is modulated by the probability of a repetition. No such repetition probability effect was found in macaque inferior temporal (IT) cortex for spiking activity, despite the presence of repetition suppression. Contrary to the human fMRI studies that showed an effect of repetition probability, the macaque single unit study employed a large variety of unfamiliar stimuli and the monkeys were not required to attend the stimuli. Here, as in the human fMRI studies, we employed faces as stimuli and made the monkeys attend to the stimulus content. We simultaneously recorded spiking activity and local field potentials (LFPs) in the middle lateral face patch (ML) of one monkey (male), and a face-responsive region of another (female). While we observed significant repetition suppression of spiking activity and high gamma band LFPs in both animals, there were no effects of repetition probability, even when repetitions were task-relevant and repetition probability affected behavioral decisions. In conclusion, despite the use of face stimuli and a stimulus-related task, no neural signature of repetition probability was present for faces in a face responsive patch of macaque IT. This further challenges a general perceptual expectation account of repetition suppression. |
Jing Wang; Devika Narain; Eghbal A. Hosseini; Mehrdad Jazayeri Flexible timing by temporal scaling of cortical responses Journal Article In: Nature Neuroscience, vol. 21, no. 1, pp. 102–112, 2018. @article{Wang2018,Musicians can perform at different tempos, speakers can control the cadence of their speech, and children can flexibly vary their temporal expectations of events. To understand the neural basis of such flexibility, we recorded from the medial frontal cortex of nonhuman primates trained to produce different time intervals with different effectors. Neural responses were heterogeneous, nonlinear, and complex, and they exhibited a remarkable form of temporal invariance: firing rate profiles were temporally scaled to match the produced intervals. Recording from downstream neurons in the caudate and from thalamic neurons projecting to the medial frontal cortex indicated that this phenomenon originates within cortical networks. Recurrent neural network models trained to perform the task revealed that temporal scaling emerges from nonlinearities in the network and that the degree of scaling is controlled by the strength of external input. These findings demonstrate a simple and general mechanism for conferring temporal flexibility upon sensorimotor and cognitive functions. |
Hannah Weinberg-Wolf; Nicholas A. Fagan; George M. Anderson; Marios Tringides; Olga Dal Monte; Steve W. C. Chang The effects of 5-hydroxytryptophan on attention and central serotonin neurochemistry in the rhesus macaque Journal Article In: Neuropsychopharmacology, vol. 43, no. 7, pp. 1589–1594, 2018. @article{WeinbergWolf2018,Psychiatric disorders, particularly depression and anxiety, are often associated with impaired serotonergic function. However, serotonergic interventions yield inconsistent effects on behavioral impairments. To better understand serotonin's role in these pathologies, we investigated the role of serotonin in a behavior frequently impaired in depression and anxiety, attention. In this study, we used a quantitative, repeated, within-subject, design to test how L-5-hydroxytryptophan (5-HTP), the immediate serotonin precursor, modulates central serotoninergic function and attention in macaques. We observed that intramuscular 5-HTP administration increased cisternal cerebrospinal fluid (CSF) 5-HTP and serotonin. In addition, individuals' baseline looking duration, during saline sessions, predicted the direction and magnitude in which 5-HTP modulated attention. We found that 5-HTP decreased looking duration in animals with high baseline attention, but increased looking duration in low baseline attention animals. Furthermore, individual differences in 5-HTP's effects were also reflected in how engaged individuals were in the task and how they allocated attention to salient facial features - the eyes and mouth - of stimulus animals. However, 5-HTP constricted pupil size in all animals, suggesting that the bi-directional effects of 5-HTP cannot be explained by serotonin-mediated changes in autonomic arousal. Critically, high and low baseline attention animals exhibited different baseline CSF concentrations of 5-HTP and serotonin, an index of extracellular functionally active serotonin. Thus, our results suggest that baseline central serotonergic functioning may underlie and predict variation in serotonin's effects on cognitive operation. Our findings may help inform serotonin's role in psychopathology and help clinicians predict how serotonergic interventions will influence pathologies. |
Andreas Wutz; Roman Loonis; Jefferson E. Roy; Jacob A. Donoghue; Earl K. Miller Different levels of category abstraction by different dynamics in different prefrontal areas Journal Article In: Neuron, vol. 97, no. 3, pp. 716–726.e8, 2018. @article{Wutz2018,Categories can be grouped by shared sensory attributes (i.e., cats) or a more abstract rule (i.e., animals). We explored the neural basis of abstraction by recording from multi-electrode arrays in prefrontal cortex (PFC) while monkeys performed a dot-pattern categorization task. Category abstraction was varied by the degree of exemplar distortion from the prototype pattern. Different dynamics in different PFC regions processed different levels of category abstraction. Bottom-up dynamics (stimulus-locked gamma power and spiking) in the ventral PFC processed more low-level abstractions, whereas top-down dynamics (beta power and beta spike-LFP coherence) in the dorsal PFC processed more high-level abstractions. Our results suggest a two-stage, rhythm-based model for abstracting categories. Wutz et al. show that different levels of category abstraction engage different oscillatory dynamics in different prefrontal cortex (PFC) areas. This suggests a functional specialization within PFC for low-level, stimulus-based categories (e.g., cats) and high-level, rule-based categories (e.g., animals). |
Yang Xie; Chechang Nie; Tianming Yang Covert shift of attention modulates the value encoding in the orbitofrontal cortex Journal Article In: eLife, vol. 7, pp. 1–21, 2018. @article{Xie2018,During value-based decision making, we often evaluate the value of each option sequentially by shifting our attention, even when the options are presented simultaneously. The orbitofrontal cortex (OFC) has been suggested to encode value during value-based decision making. Yet it is not known how its activity is modulated by attention shifts. We investigated this question by employing a passive viewing task that allowed us to disentangle effects of attention, value, choice and eye movement. We found that the attention modulated OFC activity through a winner-take-all mechanism. When we attracted the monkeys' attention covertly, the OFC neuronal activity reflected the reward value of the newly attended cue. The shift of attention could be explained by a normalization model. Our results strongly argue for the hypothesis that the OFC neuronal activity represents the value of the attended item. They provide important insights toward understanding the OFC's role in value-based decision making. |
Yin Yan; Li Zhaoping; Wu Li Bottom-up saliency and top-down learning in the primary visual cortex of monkeys Journal Article In: Proceedings of the National Academy of Sciences, vol. 115, no. 41, pp. 10499–10504, 2018. @article{Yan2018a,Early sensory cortex is better known for representing sensory inputs but less for the effect of its responses on behavior. Here we explore the behavioral correlates of neuronal responses in primary visual cortex (V1) in a task to detect a uniquely oriented bar-the orientation singleton-in a background of uniformly oriented bars. This singleton is salient or inconspicuous when the orientation contrast between the singleton and background bars is sufficiently large or small, respectively. Using implanted microelectrodes, we measured V1 activities while monkeys were trained to quickly saccade to the singleton. A neuron's responses to the singleton within its receptive field had an early and a late component, both increased with the orientation contrast. The early component started from the outset of neuronal responses; it remained unchanged before and after training on the singleton detection. The late component started ∼40 ms after the early one; it emerged and evolved with practicing the detection task. Training increased the behavioral accuracy and speed of singleton detection and increased the amount of information in the late response component about a singleton's presence or absence. Furthermore, for a given singleton, faster detection performance was associated with higher V1 responses; training increased this be-havioral-neural correlate in the early V1 responses but decreased it in the late V1 responses. Therefore, V1's early responses are directly linked with behavior and represent the bottom-up saliency signals. Learning strengthens this link, likely serving as the basis for making the detection task more reflexive and less top-down driven. |
Sheng-Tao Yang; Min Wang; Constantinos D. Paspalas; Johanna L. Crimins; Marcus T. Altman; James A. Mazer; Amy F. T. Arnsten Core differences in synaptic signaling between primary visual and dorsolateral prefrontal cortex Journal Article In: Cerebral Cortex, vol. 28, no. 4, pp. 1458–1471, 2018. @article{Yang2018,Neurons in primary visual cortex (V1) are more resilient than those in dorsolateral prefrontal cortex (dlPFC) in aging, schizophrenia and Alzheimer's disease. The current study compared glutamate and neuromodulatory actions in macaque V1 to those in dlPFC, and found striking regional differences. V1 neuronal firing to visual stimuli depended on AMPA receptors, with subtle NMDA receptor contributions, while dlPFC depends primarily on NMDA receptors. Neuromodulatory actions also differed between regions. In V1, cAMP signaling increased neuronal firing, and the phosphodiesterase PDE4A was positioned to regulate cAMP effects on glutamate release from axons. HCN channels in V1 were classically located on distal dendrites, and enhanced cell firing. These data contrast with dlPFC, where PDE4A and HCN channels are concentrated in thin spines, and cAMP-HCN signaling gates inputs and weakens firing. These regional differences may explain why V1 neurons are more resilient than dlPFC neurons to the challenges of age and disease. |
Tao Yao; Stefan Treue; B. Suresh Krishna Saccade-synchronized rapid attention shifts in macaque visual cortical area MT Journal Article In: Nature Communications, vol. 9, pp. 958, 2018. @article{Yao2018,While making saccadic eye-movements to scan a visual scene, humans and monkeys are able to keep track of relevant visual stimuli by maintaining spatial attention on them. This ability requires a shift of attentional modulation from the neuronal population representing the relevant stimulus pre-saccadically to the one representing it post-saccadically. For optimal performance, this trans-saccadic attention shift should be rapid and saccade-synchronized. Whether this is so is not known. We trained two rhesus monkeys to make saccades while maintaining covert attention at a fixed spatial location. We show that the trans-saccadic attention shift in cortical visual medial temporal (MT) area is well synchronized to saccades. Attentional modulation crosses over from the pre-saccadic to the post-saccadic neuronal representation by about 50 ms after a saccade. Taking response latency into account, the trans-saccadic attention shift is well timed to maintain spatial attention on relevant stimuli, so that they can be optimally tracked and processed across saccades. |
Seng Bum Michael Yoo; Brianna J. Sleezer; Benjamin Y. Hayden Robust encoding of spatial information in orbitofrontal cortex and striatum Journal Article In: Journal of Cognitive Neuroscience, vol. 30, no. 6, pp. 898–913, 2018. @article{Yoo2018,Knowing whether core reward regions carry information about the positions of relevant objects is crucial for adjudicating between choice models. One limitation of previous studies, including our own, is that spatial positions can be consistently differentially associated with rewards, and thus position can be confounded with attention, motor plans, or target identity. We circumvented these problems by using a task in which value— and thus choices—was determined solely by a frequently changing rule, which was randomized relative to spatial position on each trial. We presented offers asynchronously, which allowed us to control for reward expectation, spatial attention, and motor plans in our analyses. We find robust encoding of the spatial position of both offers and choices in two core reward regions, orbitofrontal Area 13 and ventral striatum, as well as in dorsal striatum of macaques. The trial-by-trial correlation in noise in encoding of position was associated with variation in choice, an effect known as choice probability correlation, suggesting that the spatial encoding is associated with choice and is not incidental to it. Spatial information and reward information are not carried by separate sets of neurons, although the two forms of information are temporally dissociable. These results highlight the ubiquity of multiplexed information in association cortex and argue against the idea that these ostensible reward regions serve as part of a pure value domain. |
2017 |
Jordi Aguila; F. Javier Cudeiro; Casto Rivadulla In: Cerebral Cortex, vol. 27, no. 6, pp. 3331–3345, 2017. @article{Aguila2017,In awake monkeys, we used repetitive transcranial magnetic stimulation (rTMS) to focally inactivate visual cortex while measuring the responsiveness of parvocellular lateral geniculate nucleus (LGN) neurons. Effects were noted in 64/75 neurons, and could be divided into 2 main groups: (1) for 39 neurons, visual responsiveness decreased and visual latency increased without apparent shift in receptive field (RF) position and (2) a second group (n = 25, 33% of the recorded cells) whose excitability was not compromised, but whose RF position shifted an average of 4.5°. This change is related to the retinotopic correspondence observed between the recorded thalamic area and the affected cortical zone. The effect of inactivation for this group of neurons was compatible with silencing the original retinal drive and unmasking a second latent retinal drive onto the studied neuron. These results indicate novel and remarkable dynamics in thalamocortical circuitry that force us to reassess constraints on retinogeniculate transmission. |
Habiba Azab; Benjamin Y. Hayden Correlates of decisional dynamics in the dorsal anterior cingulate cortex Journal Article In: PLoS Biology, vol. 15, no. 11, pp. e2003091, 2017. @article{Azab2017,We hypothesized that during binary economic choice, decision makers use the first option they attend as a default to which they compare the second. To test this idea, we recorded activity of neurons in the dorsal anterior cingulate cortex (dACC) of macaques choosing between gambles presented asynchronously. We find that ensemble encoding of the value of the first offer includes both choice-dependent and choice-independent aspects, as if reflecting a partial decision. That is, its responses are neither entirely pre- nor post-decisional. In contrast, coding of the value of the second offer is entirely decision dependent (i.e., post-decisional). This result holds even when offer-value encodings are compared within the same time period. Additionally, we see no evidence for 2 pools of neurons linked to the 2 offers; instead, all comparison appears to occur within a single functionally homogenous pool of task-selective neurons. These observations suggest that economic choices reflect a context-dependent evaluation of attended options. Moreover, they raise the possibility that value representations reflect, to some extent, a tentative commitment to a choice. |
Sahand Babapoor-Farrokhran; Martin Vinck; Thilo Womelsdorf; Stefan Everling Theta and beta synchrony coordinate frontal eye fields and anterior cingulate cortex during sensorimotor mapping Journal Article In: Nature Communications, vol. 8, pp. 13967, 2017. @article{BabapoorFarrokhran2017,The frontal eye fields (FEFs) and the anterior cingulate cortex (ACC) are commonly coacti- vated for cognitive saccade tasks, but whether this joined activation indexes coordinated activity underlying successful guidance of sensorimotor mapping is unknown. Here we test whether ACC and FEF circuits coordinate through phase synchronization of local field potential and neural spiking activity in macaque monkeys performing memory-guided and pro- and anti-saccades. We find that FEF and ACC showed prominent synchronization at a 3–9 Hz theta and a 12–30 Hz beta frequency band during the delay and preparation periods with a strong Granger-causal influence from ACC to FEF. The strength of theta- and beta- band coherence between ACC and FEF but not variations in power predict correct task performance. Taken together, the results support a role of ACC in cognitive control of fron- toparietal networks and suggest that narrow-band theta and to some extent beta rhythmic activity indexes the coordination of relevant information during periods of enhanced control demands. |
David L. Barack; Steve W. C. Chang; Michael L. Platt Posterior cingulate neurons dynamically signal decisions to disengage during foraging Journal Article In: Neuron, vol. 96, no. 2, pp. 339–347.e5, 2017. @article{Barack2017,Foraging for resources is a fundamental behavior balancing systematic search and strategic disengagement. The foraging behavior of primates is especially complex and requires long-term memory, value comparison, strategic planning, and decision-making. Here we provide evidence from two different foraging tasks that neurons in primate posterior cingulate cortex (PCC) signal decision salience during foraging to motivate disengagement from the current strategy. In our foraging tasks, salience refers to the difference between decision thresholds and the net harvested reward. Salience signals were stronger in poor foraging contexts than rich ones, suggesting low harvest rates recruit mechanisms in PCC that regulate strategic disengagement and exploration during foraging. Barack et al. report that foraging salience motivated strategic disengagement in two distinct tasks. Posterior cingulate neurons preferentially signaled salience and forecast divergent choices when reward rates were low, suggesting a role in the strategic control of behavior. |
Charles B. Beaman; Sarah L. Eagleman; Valentin Dragoi Sensory coding accuracy and perceptual performance are improved during the desynchronized cortical state Journal Article In: Nature Communications, vol. 8, pp. 1308, 2017. @article{Beaman2017,Cortical activity changes continuously during the course of the day. At a global scale, population activity varies between the ‘synchronized' state during sleep and ‘desynchronized' state during waking. However, whether local fluctuations in population synchrony during wakefulness modulate the accuracy of sensory encoding and behavioral performance is poorly understood. Here, we show that populations of cells in monkey visual cortex exhibit rapid fluctuations in synchrony ranging from desynchronized responses, indicative of high alertness, to highly synchronized responses. These fluctuations are local and control the trial variability in population coding accuracy and behavioral performance in a discrimination task. When local population activity is desynchronized, the correlated variability between neurons is reduced, and network and behavioral performance are enhanced. These findings demonstrate that the structure of variability in local cortical populations is not noise but rather controls how sensory information is optimally integrated with ongoing processes to guide network coding and behavior. |
Joachim Bellet; Chih-Yang Chen; Ziad M. Hafed Sequential hemifield gating of alpha and beta behavioral performance oscillations after microsaccades Journal Article In: Journal of Neurophysiology, vol. 118, pp. 2789–2805, 2017. @article{Bellet2017,Microsaccades are tiny saccades that occur during gaze fixation. Even though visual processing has been shown to be strongly modulated close to the time of microsaccades, both at central and peripheral eccentricities, it is not clear how these eye movements might influence longer term fluctuations in brain activity and behavior. Here we found that visual processing is significantly affected and, in a rhythmic manner, even several hundreds of milliseconds after a microsaccade. Human visual detection efficiency, as measured by reaction time, exhibited coherent rhythmic oscillations in the ? - and ? -frequency bands for up to ~650–700 ms after a microsaccade. Surprisingly, the oscillations were sequentially pulsed across visual hemifields relative to microsaccade direction, first occurring in the same hemifield as the movement vector for ~400 ms and then the opposite. Such pulsing also affected perceptual detection performance. Our results suggest that visual processing is subject to long-lasting oscillations that are phase locked to microsaccade generation, and that these oscillations are dependent on microsaccade direction. |
Kelly R. Bullock; Florian Pieper; Adam J. Sachs; Julio C. Martinez-Trujillo Visual and presaccadic activity in area 8Ar of the macaque monkey lateral prefrontal cortex Journal Article In: Journal of Neurophysiology, vol. 118, no. 1, pp. 15–28, 2017. @article{Bullock2017,Common trends observed in many visual and oculomotor-related cortical areas include retinotopically organized receptive and movement fields exhibiting a Gaussian shape and increasing size with eccentricity. These trends are demonstrated in the frontal eye fields (FEF), many visual areas, and the superior colliculus (SC), but have not been thoroughly characterized in prearcuate area 8Ar of the prefrontal cortex. This is important since area 8Ar, located anterior to the FEF, is more cytoarchitectonically similar to prefrontal areas than premotor areas. Here we recorded the responses of 166 neurons in area 8Ar of two male macaques while the animals made visually guided saccades to a peripheral sine-wave grating stimulus positioned at one of 40 possible locations (8 angles along 5 eccentricities). To characterize the neurons' receptive and movement fields, we fit a bivariate Gaussian model to the baseline-subtracted average firing rate during stimulus presentation (early and late visual epoch) and prior to saccade onset (presaccadic epoch). 121/166 neurons showed spatially selective visual and presaccadic responses. Of the visually selective neurons, 76% preferred the contralateral visual hemifield, whereas 24% preferred the ipsilateral hemifield. The angular width of visual and movement-related fields scaled positively with increasing eccentricity. Moreover, responses of neurons with visual receptive fields were modulated by target contrast exhibiting sigmoid tuning curves that resemble those of visual neurons in upstream areas such as MT and V4. Finally, we found that neurons with receptive fields at similar spatial locations were clustered within the area; however, this organization did not appear retinotopic. |
Jason L. Chan; Michael J. Koval; Kevin D. Johnston; Stefan Everling Neural correlates for task switching in the macaque superior colliculus Journal Article In: Journal of Neurophysiology, vol. 118, pp. 2156–2170, 2017. @article{Chan2017,Successful task switching requires a network of brain areas to select, maintain, implement, and execute the appropriate task. Although frontoparietal brain areas are thought to play a critical role in task switching by selecting and encoding task rules and exerting top-down control, how brain areas closer to the execution of tasks participate in task switching is unclear. The superior colliculus (SC) integrates information from various brain areas to generate saccades and is likely influenced by task switching. Here, we investigated switch costs in nonhuman primates and their neural correlates in the activity of SC saccade-related neurons in monkeys performing cued, randomly interleaved pro- and anti-saccade trials. We predicted that behavioral switch costs would be associated with differential modulations of SC activity in trials on which the task was switched vs. repeated, with activity on the current trial resembling that associated with the task set of the previous trial when a switch occurred. We observed both error rate and reaction time switch costs and changes in the discharge rate and timing of activity in SC neurons between switch and repeat trials. These changes were present later in the task only after fixation on the cue stimuli but before saccade onset. These results further establish switch costs in macaque monkeys and suggest that SC activity is modulated by task-switching processes in a manner inconsistent with the concept of task set inertia. |
Benjamin W. Corrigan; Roberto A. Gulli; Guillaume Doucet; Julio C. Martinez-Trujillo Characterizing eye movement behaviors and kinematics of non-human primates during virtual navigation tasks Journal Article In: Journal of Vision, vol. 17, no. 12, pp. 1–22, 2017. @article{Corrigan2017,Virtual environments (VE) allow testing complex behaviors in naturalistic settings by combining highly controlled visual stimuli with spatial navigation and other cognitive tasks. They also allow for the recording of eye movements using high-precision eye tracking techniques, which is important in electrophysiological studies examining the response properties of neurons in visual areas of nonhuman primates. However, during virtual navigation, the pattern of retinal stimulation can be highly dynamic which may influence eye movements. Here we examine whether and how eye movement patterns change as a function of dynamic visual stimulation during virtual navigation tasks, relative to standard oculomotor tasks. We trained two rhesus macaques to use a joystick to navigate in a VE to complete two tasks. To contrast VE behavior with classic measurements, the monkeys also performed a simple Cued Saccade task. We used a robust algorithm for rapid classification of saccades, fixations, and smooth pursuits. We then analyzed the kinematics of saccades during all tasks, and specifically during different phases of the VE tasks. We found that fixation to smooth pursuit ratios were smaller in VE tasks (4:5) compared to the Cued Saccade task (7:1), reflecting a more intensive use of smooth pursuit to foveate targets in VE than in a standard visually guided saccade task or during spontaneous fixations. Saccades made to rewarded targets (exploitation) tended to have increased peak velocities compared to saccades made to unrewarded objects (exploration). VE exploitation saccades were 6% slower than saccades to discrete targets in the Cued Saccade task. Virtual environments represent a technological advance in experimental design for nonhuman primates. Here we provide a framework to study the ways that eye movements change between and within static and dynamic displays. |
Olga Dal Monte; Matthew Piva; Kevin M. Anderson; Marios Tringides; Avram J. Holmes; Steve W. C. Chang Oxytocin under opioid antagonism leads to supralinear enhancement of social attention Journal Article In: Proceedings of the National Academy of Sciences, vol. 114, no. 20, pp. 5247–5252, 2017. @article{DalMonte2017,To provide new preclinical evidence toward improving the efficacy of oxytocin (OT) in treating social dysfunction, we tested the benefit of administering OT under simultaneously induced opioid antagonism during dyadic gaze interactions in monkeys. OT coadministered with a μ-opioid receptor antagonist, naloxone, invoked a supralinear enhancement of prolonged and selective social attention, producing a stronger effect than the summed effects of each administered separately. These effects were consistently observed when averaging over entire sessions, as well as specifically following events of particular social importance, including mutual eye contact and mutual reward receipt. Furthermore, attention to various facial regions was differentially modulated depending on social context. Using the Allen Institute's transcriptional atlas, we further established the colocalization of μ-opioid and κ-opioid receptor genes and OT genes at the OT-releasing sites in the human brain. These data across monkeys and humans support a regulatory relationship between the OT and opioid systems and suggest that administering OT under opioid antagonism may boost the therapeutic efficacy of OT for enhancing social cognition. |
Nicholas K. DeWind; Jiyun Peng; Andrew Luo; Elizabeth M. Brannon; Michael L. Platt Pharmacological inactivation does not support a unique causal role for intraparietal sulcus in the discrimination of visual number Journal Article In: PLoS ONE, vol. 12, no. 12, pp. e0188820, 2017. @article{DeWind2017,The "number sense" describes the intuitive ability to quantify without counting. Single neu-ron recordings in non-human primates and functional imaging in humans suggest the intra-parietal sulcus is an important neuroanatomical locus of numerical estimation. Other lines of inquiry implicate the IPS in numerous other functions, including attention and decision mak-ing. Here we provide a direct test of whether IPS has functional specificity for numerosity judgments. We used muscimol to reversibly and independently inactivate the ventral and lat-eral intraparietal areas in two monkeys performing a numerical discrimination task and a color discrimination task, roughly equilibrated for difficulty. Inactivation of either area caused parallel impairments in both tasks and no evidence of a selective deficit in numerical pro-cessing. These findings do not support a causal role for the IPS in numerical discrimination, except insofar as it also has a role in the discrimination of color. We discuss our findings in light of several alternative hypotheses of IPS function, including a role in orienting responses, a general cognitive role in attention and decision making processes and a more specific role in ordinal comparison that encompasses both number and color judgments. |
Kacie Dougherty; Michele A. Cox; Taihei Ninomiya; David A. Leopold; Alexander Maier Ongoing alpha activity in V1 regulates visually driven spiking responses Journal Article In: Cerebral Cortex, vol. 27, no. 2, pp. 1113–1124, 2017. @article{Dougherty2017,The interlaminar connections in the primate primary visual cortex (V1) are well described, as is the presence of ongoing alpha-range (7-14 Hz) fluctuations in this area. Less well understood is how these interlaminar connections and ongoing fluctuations contribute to the regulation of visual spiking responses. Here, we investigate the relationship between alpha fluctuations and spiking responses to visual stimuli across cortical layers. Using laminar probes in macaque V1, we show that neural firing couples with the phase of alpha fluctuations, and that magnitude of this coupling is particularly pronounced during visual stimulation. The strongest modulation of spiking activity was observed in layers 2/3. Alpha-spike coupling and current source density analysis pointed to an infragranular origin of the alpha fluctuations. Taken together, these results indicate that ongoing infragranular alpha-range fluctuations in V1 play a role in regulating columnar visual activity. |
R. Becket Ebitz; Tirin Moore Selective modulation of the pupil light reflex by microstimulation of prefrontal cortex Journal Article In: Journal of Neuroscience, vol. 37, no. 19, pp. 5008–5018, 2017. @article{Ebitz2017,The prefrontal cortex (PFC) is thought to flexibly regulate sensorimotor responses, perhaps through modulating activity in other circuits. However, the scope of that control remains unknown: it remains unclear whether the PFC can modulate basic reflexes. One canonical example of a central reflex is the pupil light reflex (PLR): the automatic constriction of the pupil in response to luminance increments. Unlike pupil size, which depends on the interaction of multiple physiological and neuromodulatory influences, the PLR reflects the action of a simple brainstem circuit. However, emerging behavioral evidence suggests that the PLR may be modulated by cognitive processes. Although the neural basis of these modulations remains unknown, one possible source is the PFC, particularly the frontal eye field (FEF), an area of the PFC implicated in the control of attention. We show that microstimulation of the rhesus macaque FEF alters the magnitude of the PLR in a spatially specific manner. FEF microstimulation enhanced the PLR to probes presented within the stimulated visual field, but suppressed the PLR to probes at nonoverlapping locations. The spatial specificity of this effect parallels the effect of FEF stimulation on attention and suggests that FEF is capable of modulating visuomotor transformations performed at a lower level than was previously known. These results provide evidence of the selective regulation of a basic brainstem reflex by the PFC. |
Hongwei Fan; Xiaochuan Pan; Rubin Wang; Masamichi Sakagami Differences in reward processing between putative cell types in primate prefrontal cortex Journal Article In: PLoS ONE, vol. 12, no. 12, pp. e0189771, 2017. @article{Fan2017a,Single-unit studies in monkeys have demonstrated that neurons in the prefrontal cortex predict the reward type, reward amount or reward availability associated with a stimulus. To examine contributions of pyramidal cells and interneurons in reward processing, single-unit activity was extracellularly recorded in prefrontal cortices of four monkeys performing a reward prediction task. Based on their shapes of spike waveforms, prefrontal neurons were classified into broad-spike and narrow-spike units that represented putative pyramidal cells and interneurons, respectively. We mainly observed that narrow-spike neurons showed higher firing rates but less bursty discharges than did broad-spike neurons. Both narrow-spike and broad-spike cells selectively responded to the stimulus, reward and their interaction, and the proportions of each type of selective neurons were similar between the two cell classes. Moreover, the two types of cells displayed equal reliability of reward or stimulus discrimination. Furthermore, we found that broad-spike and narrow-spike cells showed distinct mechanisms for encoding reward or stimulus information. Broad-spike neurons raised their firing rate relative to the baseline rate to represent the preferred reward or stimulus information, whereas narrow-spike neurons inhibited their firing rate lower than the baseline rate to encode the non-preferred reward or stimulus information. Our results suggest that narrow-spike and broad-spike cells were equally involved in reward and stimulus processing in the prefrontal cortex. They utilized a binary strategy to complementarily represent reward or stimulus information, which was consistent with the task structure in which the monkeys were required to remember two reward conditions and two visual stimuli. |
Amber M. Fyall; Yasmine El-Shamayleh; Hannah Choi; Eric Shea-Brown; Anitha Pasupathy Dynamic representation of partially occluded objects in primate prefrontal and visual cortex Journal Article In: eLife, vol. 6, pp. 1–25, 2017. @article{Fyall2017,Successful recognition of partially occluded objects is presumed to involve dynamic interactions between brain areas responsible for vision and cognition, but neurophysiological evidence for the involvement of feedback signals is lacking. Here, we demonstrate that neurons in the ventrolateral prefrontal cortex (vlPFC) of monkeys performing a shape discrimination task respond more strongly to occluded than unoccluded stimuli. In contrast, neurons in visual area V4 respond more strongly to unoccluded stimuli. Analyses of V4 response dynamics reveal that many neurons exhibit two transient response peaks, the second of which emerges after vlPFC response onset and displays stronger selectivity for occluded shapes. We replicate these findings using a model of V4/vlPFC interactions in which occlusion-sensitive vlPFC neurons feed back to shape- selective V4 neurons, thereby enhancing V4 responses and selectivity to occluded shapes. These results reveal how signals from frontal and visual cortex could interact to facilitate object recognition under occlusion. |
Diego A. Gutnisky; Charles B. Beaman; Sergio E. Lew; Valentin Dragoi Spontaneous fluctuations in visual cortical responses influence population coding accuracy Journal Article In: Cerebral Cortex, vol. 27, no. 2, pp. 1409–1427, 2017. @article{Gutnisky2017,Information processing in the cerebral cortex depends not only on the nature of incoming stimuli, but also on the state of neuronal networks at the time of stimulation. That is, the same stimulus will be processed differently depending on the neuronal context in which it is received. A major factor that could influence neuronal context is the background, or ongoing neuronal activity before stimulation. In visual cortex, ongoing activity is known to play a critical role in the development of local circuits, yet whether it influences the coding of visual features in adult cortex is unclear. Here, we investigate whether and how the information encoded by individual neurons and populations in primary visual cortex (V1) depends on the ongoing activity before stimulus presentation. We report that when individual neurons are in a "low" prestimulus state, they have a higher capacity to discriminate stimulus features, such as orientation, despite their reduction in evoked responses. By measuring the distribution of prestimulus activity across a population of neurons, we found that network discrimination accuracy is improved in the low prestimulus state. Thus, the distribution of ongoing activity states across the network creates an "internal context" that dynamically filters incoming stimuli to modulate the accuracy of sensory coding. The modulation of stimulus coding by ongoing activity state is consistent with recurrent network models in which ongoing activity dynamically controls the balanced background excitation and inhibition to individual neurons. |
Diego A. Gutnisky; Charles Beaman; Sergio E. Lew; Valentin Dragoi Cortical response states for enhanced sensory discrimination Journal Article In: eLife, vol. 6, pp. 1–23, 2017. @article{Gutnisky2017a,Brain activity during wakefulness is characterized by rapid fluctuations in neuronal responses. Whether these fluctuations play any role in modulating the accuracy of behavioral responses is poorly understood. Here, we investigated whether and how trial changes in the population response impact sensory coding in monkey V1 and perceptual performance. Although the responses of individual neurons varied widely across trials, many cells tended to covary with the local population. When population activity was in a 'low' state, neurons had lower evoked responses and correlated variability, yet higher probability to predict perceptual accuracy. The impact of firing rate fluctuations on network and perceptual accuracy was strongest 200-ms before stimulus presentation, and it greatly diminished when the number of cells used to measure the state of the population was decreased. These findings indicate that enhanced perceptual discrimination occurs when population activity is in a 'silent' response mode in which neurons increase information extraction. |
Gerald Hahn; Adrian Ponce-Alvarez; Cyril Monier; Giacomo Benvenuti; Arvind Kumar; Frédéric Chavane; Gustavo Deco; Yves Frégnac Spontaneous cortical activity is transiently poised close to criticality Journal Article In: PLoS Computational Biology, vol. 13, no. 5, pp. e1005543, 2017. @article{Hahn2017,Brain activity displays a large repertoire of dynamics across the sleep-wake cycle and even during anesthesia. It was suggested that criticality could serve as a unifying principle underlying the diversity of dynamics. This view has been supported by the observation of spontaneous bursts of cortical activity with scale-invariant sizes and durations, known as neuronal avalanches, in recordings of mesoscopic cortical signals. However, the existence of neuronal avalanches in spiking activity has been equivocal with studies reporting both its presence and absence. Here, we show that signs of criticality in spiking activity can change between synchronized and desynchronized cortical states. We analyzed the spontaneous activity in the primary visual cortex of the anesthetized cat and the awake monkey, and found that neuronal avalanches and thermodynamic indicators of criticality strongly depend on collective synchrony among neurons, LFP fluctuations, and behavioral state. We found that synchronized states are associated to criticality, large dynamical repertoire and prolonged epochs of eye closure, while desynchronized states are associated to sub-criticality, reduced dynamical repertoire, and eyes open conditions. Our results show that criticality in cortical dynamics is not stationary, but fluctuates during anesthesia and between different vigilance states. |
S. A. Hassani; Mariann Oemisch; M. Balcarras; Stephanie Westendorff; S. Ardid; M. A. Meer; P. Tiesinga; T. Womelsdorf In: Scientific Reports, vol. 7, pp. 40606, 2017. @article{Hassani2017,Noradrenaline is believed to support cognitive flexibility through the alpha 2A noradrenergic receptor (a2A-NAR) acting in prefrontal cortex. Enhanced flexibility has been inferred from improved working memory with the a2A-NA agonist Guanfacine. But it has been unclear whether Guanfacine improves specific attention and learning mechanisms beyond working memory, and whether the drug effects can be formalized computationally to allow single subject predictions. We tested and confirmed these suggestions in a case study with a healthy nonhuman primate performing a feature-based reversal learning task evaluating performance using Bayesian and Reinforcement learning models. In an initial dose-testing phase we found a Guanfacine dose that increased performance accuracy, decreased distractibility and improved learning. In a second experimental phase using only that dose we examined the faster feature-based reversal learning with Guanfacine with single-subject computational modeling. Parameter estimation suggested that improved learning is not accounted for by varying a single reinforcement learning mechanism, but by changing the set of parameter values to higher learning rates and stronger suppression of non-chosen over chosen feature information. These findings provide an important starting point for developing nonhuman primate models to discern the synaptic mechanisms of attention and learning functions within the context of a computational neuropsychiatry framework. |
James P. Herman; Richard J. Krauzlis Color-change detection activity in the primate superior colliculus Journal Article In: eNeuro, vol. 4, no. 2, pp. 1–16, 2017. @article{Herman2017,The primate superior colliculus (SC) is a midbrain structure that participates in the control of spatial attention. Previous studies examining the role of the SC in attention have mostly used luminance-based visual features (e.g., motion, contrast) as the stimuli and saccadic eye movements as the behavioral response, both of which are known to modulate the activity of SC neurons. To explore the limits of the SC's involvement in the control of spatial attention, we recorded SC neuronal activity during a task using color, a visual feature dimension not traditionally associated with the SC, and required monkeys to detect threshold-level changes in the saturation of a cued stimulus by releasing a joystick during maintained fixation. Using this color-based spatial attention task, we found substantial cue-related modulation in all categories of visually responsive neurons in the intermediate layers of the SC. Notably, near-threshold changes in color saturation, both increases and decreases, evoked phasic bursts of activity with magnitudes as large as those evoked by stimulus onset. This change-detection activity had two distinctive features: activity for hits was larger than for misses, and the timing of change-detection activity accounted for 67% of joystick release latency, even though it preceded the release by at least 200 ms. We conclude that during attention tasks, SC activity denotes the behavioral relevance of the stimulus regardless of feature dimension and that phasic event-related SC activity is suitable to guide the selection of manual responses as well as saccadic eye movements. |
Markus A. Hietanen; Nicholas S. C. Price; Shaun L. Cloherty; Kostas Hadjidimitrakis; Michael R. Ibbotson Long-term sensorimotor adaptation in the ocular following system of primates Journal Article In: PLoS ONE, vol. 12, no. 12, pp. e0189030, 2017. @article{Hietanen2017,The sudden movement of a wide-field image leads to a reflexive eye tracking response referred to as short-latency ocular following. If the image motion occurs soon after a saccade the initial speed of the ocular following is enhanced, a phenomenon known as post-saccadic enhancement. We show in macaque monkeys that repeated exposure to the same stimulus regime over a period of months leads to progressive increases in the initial speeds of ocular following. The improvement in tracking speed occurs for ocular following with and without a prior saccade. As a result of the improvement in ocular following speeds, the influence of post-saccadic enhancement wanes with increasing levels of training. The improvement in ocular following speed following repeated exposure to the same oculomotor task represents a novel form of sensori-motor learning in the context of a reflexive movement. |
Guilhem Ibos; David J. Freedman Sequential sensory and decision processing in posterior parietal cortex Journal Article In: eLife, vol. 6, pp. 1–19, 2017. @article{Ibos2017,<p>Decisions about the behavioral significance of sensory stimuli often require comparing sensory inference of what we are looking at to internal models of what we are looking for. Here, we test how neuronal selectivity for visual features is transformed into decision-related signals in posterior parietal cortex (area LIP). Monkeys performed a visual matching task that required them to detect target stimuli composed of conjunctions of color and motion-direction. Neuronal recordings from area LIP revealed two main findings. First, the sequential processing of visual features and the selection of target-stimuli suggest that LIP is involved in transforming sensory information into decision-related signals. Second, the patterns of color and motion selectivity and their impact on decision-related encoding suggest that LIP plays a role in detecting target stimuli by comparing bottom-up sensory inputs (what the monkeys were looking at) and top-down cognitive encoding inputs (what the monkeys were looking for).</p> |
Nan Jia; Scott L. Brincat; Andrés F. Salazar-Gómez; Mikhail Panko; Frank H. Guenther; Earl K. Miller Decoding of intended saccade direction in an oculomotor brain-computer interface Journal Article In: Journal of Neural Engineering, vol. 14, no. 4, pp. 1–13, 2017. @article{Jia2017a,OBJECTIVE: To date, invasive brain-computer interface (BCI) research has largely focused on replacing lost limb functions using signals from of hand/arm areas of motor cortex. However, the oculomotor system may be better suited to BCI applications involving rapid serial selection from spatial targets, such as choosing from a set of possible words displayed on a computer screen in an augmentative and alternative communication (AAC) application. Here we aimed to demonstrate the feasibility of a BCI utilizing the oculomotor system. APPROACH: We developed a chronic intracortical BCI in monkeys to decode intended saccadic eye movement direction using activity from multiple frontal cortical areas. MAIN RESULTS: Intended saccade direction could be decoded in real time with high accuracy, particularly at contralateral locations. Accurate decoding was evident even at the beginning of the BCI session; no extensive BCI experience was necessary. High-frequency (80-500 Hz) local field potential magnitude provided the best performance, even over spiking activity, thus simplifying future BCI applications. Most of the information came from the frontal and supplementary eye fields, with relatively little contribution from dorsolateral prefrontal cortex. SIGNIFICANCE: Our results support the feasibility of high-accuracy intracortical oculomotor BCIs that require little or no practice to operate and may be ideally suited for 'point and click' computer operation as used in most current AAC systems. |
Yoshinao Kajikawa; John F. Smiley; Charles E. Schroeder Primary generators of visually evoked field potentials recorded in the macaque auditory cortex Journal Article In: Journal of Neuroscience, vol. 37, no. 42, pp. 10139–10153, 2017. @article{Kajikawa2017,Prior studies have reported “local” field potential (LFP) responses to faces in the macaque auditory cortex and have suggested that such face-LFPs may be substrates of audiovisual integration. However, although field potentials (FPs) may reflect the synaptic currents of neurons near the recording electrode, due to the use of a distant reference electrode, they often reflect those of synaptic activity occurring in distant sites as well. Thus, FP recordings within a given brain region (e.g., auditory cortex) may be “contaminated” by activity generated elsewhere in the brain. To determine whether face responses are indeed generated within macaque auditory cortex, we recorded FPs and concomitant multiunit activity with linear array multielectrodes across auditory cortex in three macaques (one female), and applied current source density (CSD) analysis to the laminar FP profile. CSD analysis revealed no appreciable local generator contribution to the visual FP in auditory cortex, although we did note an increase in the amplitude of visual FP with cortical depth, suggesting that their generators are located below auditory cortex. In the underlying inferotemporal cortex, we found polarity inversions of the main visual FP components accompanied by robust CSD responses and large-amplitude multiunit activity. These results indicate that face-evoked FP responses in auditory cortex are not generated locally but are volume-conducted from other face-responsive regions. In broader terms, our results underscore the caution that, unless far-field contamination is removed, LFPs in general may reflect such “far-field” activity, in addition to, or in absence of, local synaptic responses. |
Kohitij Kar; Jacob Duijnhouwer; Bart Krekelberg Transcranial alternating current stimulation attenuates neuronal adaptation Journal Article In: Journal of Neuroscience, vol. 37, no. 9, pp. 2325–2335, 2017. @article{Kar2017,We previously showed that brief application of 2 mA (peak-to-peak) transcranial currents alternating at 10 Hz significantly reduces motion adaptation in humans. This is but one of many behavioral studies showing that weak currents applied to the scalp modulate neural processing. Transcranial stimulation has been shown to improve perception, learning, and a range of clinical symptoms. Few studies, however, have measured the neural consequences of transcranial current stimulation. We capitalized on the strong link between motion perception and neural activity in the middle temporal (MT) area of the macaque monkey to study the neural mechanisms that underlie the behavioral consequences of transcranial alternating current stimulation. First, we observed that 2 mA currents generated substantial intracranial fields, which were much stronger in the stimulated hemisphere (0.12 V/m) than on the opposite side of the brain (0.03 V/m). Second, we found that brief application of transcranial alternating current stimulation at 10 Hz reduced spike-frequency adaptation of MT neurons and led to a broadband increase in the power spectrum of local field potentials. Together, these findings provide a direct demonstration that weak electric fields applied to the scalp significantly affect neural processing in the primate brain and that this includes a hitherto unknown mechanism that attenuates sensory adaptation. |
Steffen Klingenhoefer; Bart Krekelberg Perisaccadic visual perception Journal Article In: Journal of Vision, vol. 17, no. 9, pp. 1–14, 2017. @article{Klingenhoefer2017,Primates use frequent, rapid eye movements to sample their visual environment. This is a fruitful strategy to make the best use of the highly sensitive foveal part of the retina, but it requires neural mechanisms to bind the rapidly changing visual input into a single, stable percept. Studies investigating these neural mechanisms have typically assumed that perisaccadic perception in nonhuman primates matches that of humans. We tested this assumption by performing identical experiments in human and nonhuman primates. Our data confirm that perisaccadic visual perception of macaques and humans is qualitatively similar. Specifically, we found a reduction in detectability and mislocalization of targets presented at the time of saccades. We also found substantial differences between human and nonhuman primates. Notably, in nonhuman primates, localization that requires knowledge of eye position was less precise, nonhuman primates detected fewer perisaccadic stimuli, and perisaccadic compression was not towards the saccade target. The qualitative similarities between species support the view that the nonhuman primate is ideally suited to study aspects of brain function-such as those relying on foveal vision-that are uniquely developed in primates. The quantitative differences, however, demonstrate the need for a reassessment of the models purportedly linking neural response changes at the time of saccades with the behavioral phenomena of perisaccadic reduction of detectability and mislocalization. |
Matthew R. Krause; Theodoros P. Zanos; Bennett A. Csorba; Praveen K. Pilly; Jaehoon Choe; Matthew E. Phillips; Abhishek Datta; Christopher C. Pack Transcranial direct current stimulation facilitates associative learning and alters functional connectivity in the primate brain Journal Article In: Current Biology, vol. 27, no. 20, pp. 3086–3096, 2017. @article{Krause2017,There has been growing interest in transcranial direct current stimulation (tDCS), a non-invasive technique purported to modulate neural activity via weak, externally applied electric fields. Although some promising preliminary data have been reported for applications ranging from stroke rehabilitation to cognitive enhancement, little is known about how tDCS affects the human brain, and some studies have concluded that it may have no effect at all. Here, we describe a macaque model of tDCS that allows us to simultaneously examine the effects of tDCS on brain activity and behavior. We find that applying tDCS to right prefrontal cortex improves monkeys' performance on an associative learning task. While firing rates do not change within the targeted area, tDCS does induce large low-frequency oscillations in the underlying tissue. These oscillations alter functional connectivity, both locally and between distant brain areas, and these long-range changes correlate with tDCS's effects on behavior. Together, these results are consistent with the idea that tDCS leads to widespread changes in brain activity and suggest that it may be a valuable method for cheaply and non-invasively altering functional connectivity in humans. Krause et al. test transcranial direct current stimulation (tDCS) in a realistic non-human primate model. Stimulation of prefrontal cortex (PFC) improved animals' associative learning while altering coherence between PFC and sensory areas. Their data suggest that tDCS may act by altering long-range connectivity between PFC and other brain areas. |
Matthew L. Leavitt; Florian Pieper; Adam J. Sachs; Julio C. Martinez-Trujillo Correlated variability modifies working memory fidelity in primate prefrontal neuronal ensembles Journal Article In: Proceedings of the National Academy of Sciences, vol. 114, no. 12, pp. E2494–E2503, 2017. @article{Leavitt2017a,Neurons in the primate lateral prefrontal cortex (LPFC) encode working memory (WM) representations via sustained firing, a phenomenon hypothesized to arise from recurrent dynamics within ensembles of interconnected neurons. Here, we tested this hypothesis by using microelectrode arrays to examine spike count correlations (rsc) in LPFC neuronal ensembles during a spatial WM task. We found a pattern of pairwise rsc during WM maintenance indicative of stronger coupling between similarly tuned neurons and increased inhibition between dissimilarly tuned neurons. We then used a linear decoder to quantify the effects of the high-dimensional rsc structure on information coding in the neuronal ensembles. We found that the rsc structure could facilitate or impair coding, depending on the size of the ensemble and tuning properties of its constituent neurons. A simple optimization procedure demonstrated that near-maximum decoding performance could be achieved using a relatively small number of neurons. These WM- optimized subensembles were more signal correlation (rsignal)- diverse and anatomically dispersed than predicted by the statistics of the full recorded population of neurons, and they often con- tained neurons that were poorly WM-selective, yet enhanced cod- ing fidelity by shaping the ensemble's rsc structure. We observed a pattern of rsc between LPFC neurons indicative of recurrent dynamics as a mechanism for WM-related activity and that the rsc structure can increase the fidelity ofWM representations. Thus, WM coding in LPFC neuronal ensembles arises from a complex synergy between single neuron coding properties and multidimensional, ensemble-level phenomena. |
Jeyeon Lee; Hoseok Choi; Seho Lee; Baek Hwan Cho; Kyoung-ha Ahn; In Young Kim; Kyoung-Min Lee; Dong-Pyo Jang Decoding saccadic directions using epidural ECoG in non-human primates Journal Article In: Journal of Korean Medical Science, vol. 32, no. 8, pp. 1243–1250, 2017. @article{Lee2017,A brain-computer interface (BCI) can be used to restore some communication as an alternative interface for patients suffering from locked-in syndrome. However, most BCI systems are based on SSVEP, P300, or motor imagery, and a diversity of BCI protocols would be needed for various types of patients. In this paper, we trained the choice saccade (CS) task in 2 non-human primate monkeys and recorded the brain signal using an epidural electrocorticogram (eECoG) to predict eye movement direction. We successfully predicted the direction of the upcoming eye movement using a support vector machine (SVM) with the brain signals after the directional cue onset and before the saccade execution. The mean accuracies were 80% for 2 directions and 43% for 4 directions. We also quantified the spatial-spectro-temporal contribution ratio using SVM recursive feature elimination (RFE). The channels over the frontal eye field (FEF), supplementary eye field (SEF), and superior parietal lobule (SPL) area were dominantly used for classification. The α-band in the spectral domain and the time bins just after the directional cue onset and just before the saccadic execution were mainly useful for prediction. A saccade based BCI paradigm can be projected in the 2D space, and will hopefully provide an intuitive and convenient communication platform for users. |
Roman F. Loonis; Scott L. Brincat; Evan G. Antzoulatos; Earl K. Miller A meta-analysis suggests different neural correlates for implicit and explicit learning Journal Article In: Neuron, vol. 96, no. 2, pp. 521–534.e7, 2017. @article{Loonis2017,A meta-analysis of non-human primates performing three different tasks (Object-Match, Category-Match, and Category-Saccade associations) revealed signatures of explicit and implicit learning. Performance improved equally following correct and error trials in the Match (explicit) tasks, but it improved more after correct trials in the Saccade (implicit) task, a signature of explicit versus implicit learning. Likewise, error-related negativity, a marker for error processing, was greater in the Match (explicit) tasks. All tasks showed an increase in alpha/beta (10–30 Hz) synchrony after correct choices. However, only the implicit task showed an increase in theta (3–7 Hz) synchrony after correct choices that decreased with learning. In contrast, in the explicit tasks, alpha/beta synchrony increased with learning and decreased thereafter. Our results suggest that explicit versus implicit learning engages different neural mechanisms that rely on different patterns of oscillatory synchrony. Loonis et al. find that explicit and implicit learning use feedback about correct choices versus errors differently. Implicit learning relies more on theta synchrony (3–7 Hz) while explicit learning relies on alpha/beta synchrony (10–30 Hz). |
Nicolas Y. Masse; Jonathan M. Hodnefield; David J. Freedman Mnemonic encoding and cortical organization in parietal and prefrontal cortices Journal Article In: Journal of Neuroscience, vol. 37, no. 25, pp. 6098–6112, 2017. @article{Masse2017,Persistent activity within the frontoparietal network is consistently observed during tasks that require working memory. However, the neural circuit mechanisms underlying persistent neuronal encoding within this network remain unresolved. Here, we ask how neural circuits support persistent activity by examining population recordings from posterior parietal (PPC) and prefrontal (PFC) cortices in two male monkeys that performed spatial and motion direction-based tasks that required working memory. While spatially selective persistent activity was observed in both areas, robust selective persistent activity for motion direction was only observed in PFC. Crucially, we find that this difference between mnemonic encoding in PPC and PFC is associated with the presence offunctional clustering: PPC and PFC neurons up to ~700 μm apart preferred similar spatial locations, and PFC neurons up to ~700 μm apart preferred similar motion directions. In contrast, motion-direction tuning similarity between nearby PPC neurons was much weaker and decayed rapidly beyond ~200 μm. We also observed a similar association between persistent activity and functional clustering in trained recurrent neural network models embedded with a columnar topology. These results suggest that functional clustering facilitates mnemonic encoding of sensory information. |
Diego Mendoza-Halliday; Julio C. Martinez-Trujillo Neuronal population coding of perceived and memorized visual features in the lateral prefrontal cortex Journal Article In: Nature Communications, vol. 8, pp. 15471, 2017. @article{MendozaHalliday2017,The primate lateral prefrontal cortex (LPFC) encodes visual stimulus features while they are perceived and while they are maintained in working memory. However, it remains unclear whether perceived and memorized features are encoded by the same or different neurons and population activity patterns. Here we record LPFC neuronal activity while monkeys perceive the motion direction of a stimulus that remains visually available, or memorize the direction if the stimulus disappears. We find neurons with a wide variety of combinations of coding strength for perceived and memorized directions: some neurons encode both to similar degrees while others preferentially or exclusively encode either one. Reading out the combined activity of all neurons, a machine-learning algorithm reliably decode the motion direction and determine whether it is perceived or memorized. Our results indicate that a functionally diverse population of LPFC neurons provides a substrate for discriminating between perceptual and mnemonic representations of visual features. |
Yaser Merrikhi; Kelsey Clark; Eddy Albarran; Mohammadbagher Parsa; Marc Zirnsak; Tirin Moore; Behrad Noudoost Spatial working memory alters the efficacy of input to visual cortex Journal Article In: Nature Communications, vol. 8, pp. 15041, 2017. @article{Merrikhi2017,Prefrontal cortex modulates sensory signals in extrastriate visual cortex, in part via its direct projections from the frontal eye field (FEF), an area involved in selective attention. We find that working memory-related activity is a dominant signal within FEF input to visual cortex. Although this signal alone does not evoke spiking responses in areas V4 and MT during memory, the gain of visual responses in these areas increases, and neuronal receptive fields expand and shift towards the remembered location, improving the stimulus representation by neuronal populations. These results provide a basis for enhancing the representation of working memory targets and implicate persistent FEF activity as a basis for the interdependence of working memory and selective attention. |
Juri Minxha; Clayton Mosher; Jeremiah K. Morrow; Adam N. Mamelak; Ralph Adolphs; Katalin M. Gothard; Ueli Rutishauser Fixations gate species-specific responses to free viewing of faces in the human and macaque amygdala Journal Article In: Cell Reports, vol. 18, no. 4, pp. 878–891, 2017. @article{Minxha2017,Neurons in the primate amygdala respond prominently to faces. This implicates the amygdala in the processing of socially significant stimuli, yet its contribution to social perception remains poorly understood. We evaluated the representation of faces in the primate amygdala during naturalistic conditions by recording from both human and macaque amygdala neurons during free viewing of identical arrays of images with concurrent eye tracking. Neurons responded to faces only when they were fixated, suggesting that neuronal activity was gated by visual attention. Further experiments in humans utilizing covert attention confirmed this hypothesis. In both species, the majority of face-selective neurons preferred faces of conspecifics, a bias also seen behaviorally in first fixation preferences. Response latencies, relative to fixation onset, were shortest for conspecific-selective neurons and were ∼100 ms shorter in monkeys compared to humans. This argues that attention to faces gates amygdala responses, which in turn prioritize species-typical information for further processing. |
Ilya E. Monosov Anterior cingulate is a source of valence-specific information about value and uncertainty Journal Article In: Nature Communications, vol. 8, pp. 134, 2017. @article{Monosov2017,Anterior cingulate cortex (ACC) is thought to control a wide range of reward, punishment, and uncertainty-related behaviors. However, how it does so is unclear. Here, in a Pavlovian procedure in which monkeys displayed a diverse repertoire of reward-related, punishment-related, and uncertainty-related behaviors, we show that many ACC-neurons represent expected value and uncertainty in a valence-specific manner, signaling value or uncertainty predictions about either rewards or punishments. Other ACC-neurons signal prediction information about rewards and punishments by displaying excitation to both (rather than excitation to one and inhibition to the other). This diversity in valence representations may support the role of ACC in many behavioral states that are either enhanced by reward and punishment (e.g., vigilance) or specific to either reward or punishment (e.g., approach and avoidance). Also, this first demonstration of punishment-uncertainty signals in the brain suggests that ACC could be a target for the treatment of uncertainty-related disorders of mood. |
Sujaya Neupane; Daniel Guitton; Christopher C. Pack Coherent alpha oscillations link current and future receptive fields during saccades Journal Article In: Proceedings of the National Academy of Sciences, vol. 114, no. 29, pp. E5979–E5985, 2017. @article{Neupane2017,Oscillations are ubiquitous in the brain, and they can powerfully influence neural coding. In particular, when oscillations at distinct sites are coherent, they provide a means of gating the flow of neural signals between different cortical regions. Coherent oscillations also occur within individual brain regions, although the purpose of this coherence is not well understood. Here, we report that within a single brain region, coherent alpha oscillations link stimulus representations as they change in space and time. Specifically, in primate cortical area V4, alpha coherence links sites that encode the retinal location of a visual stimulus before and after a saccade. These coherence changes exhibit properties similar to those of receptive field remapping, a phenomenon in which individual neurons change their receptive fields according to the metrics of each saccade. In particular, alpha coherence, like remapping, is highly dependent on the saccade vector and the spatial arrangement of current and future receptive fields. Moreover, although visual stimulation plays a modulatory role, it is neither necessary nor sufficient to elicit alpha coherence. Indeed, a similar pattern of coherence is observed even when saccades are made in darkness. Together, these results show that the pattern of alpha coherence across the retinotopic map in V4 matches many of the properties of receptive field remapping. Thus, oscillatory coherence might play a role in constructing the stable representation of visual space that is an essential aspect of conscious perception. |
James E. Niemeyer; Michael A. Paradiso Contrast sensitivity, V1 neural activity, and natural vision Journal Article In: Journal of Neurophysiology, vol. 117, no. 2, pp. 492–508, 2017. @article{Niemeyer2017,Contrast sensitivity is fundamental to natural visual processing and an important tool for characterizing both visual function and clinical disorders. We simultaneously measured contrast sensitivity and neural contrast response functions and compared measurements in common laboratory conditions with naturalistic conditions. In typical experiments, a subject holds fixation and a stimulus is flashed on, whereas in natural vision, saccades bring stimuli into view. Motivated by our previous V1 findings, we tested the hypothesis that perceptual contrast sensitivity is lower in natural vision and that this effect is associated with corresponding changes in V1 activity. We found that contrast sensitivity and V1 activity are correlated and that the relationship is similar in laboratory and naturalistic paradigms. However, in the more natural situation, contrast sensitivity is reduced up to 25% compared with that in a standard fixation paradigm, particularly at lower spatial frequencies, and this effect correlates with significant reductions in V1 responses. Our data suggest that these reductions in natural vision result from fast adaptation on one fixation that lowers the response on a subsequent fixation. This is the first demonstration of rapid, naturalimage adaptation that carries across saccades, a process that appears to constantly influence visual sensitivity in natural vision. NEW & NOTEWORTHY Visual sensitivity and activity in brain area V1 were studied in a paradigm that included saccadic eye movements and natural visual input. V1 responses and contrast sensitivity were significantly reduced compared with results in common laboratory paradigms. The parallel neural and perceptual effects of eye movements and stimulus complexity appear to be due to a form of rapid adaptation that carries across saccades. |
Soo Hyun Park; Brian E. Russ; David B. T. McMahon; Kenji W. Koyano; Rebecca A. Berman; David A. Leopold Functional subpopulations of neurons in a macaque face patch revealed by single-unit fMRI mapping Journal Article In: Neuron, vol. 95, no. 4, pp. 971–981.e5, 2017. @article{Park2017,Neurons within fMRI-defined face patches of the macaque brain exhibit shared categorical responses to flashed images but diverge in their responses under more natural viewing conditions. Here we investigate functional diversity among neurons in the anterior fundus (AF) face patch, combining whole-brain fMRI with longitudinal single-unit recordings in a local population (<1 mm3). For each cell, we computed a whole-brain correlation map based on its shared time course with voxels throughout the brain during naturalistic movie viewing. Based on this mapping, neighboring neurons showed markedly different affiliation with distant visually responsive areas and fell coarsely into subpopulations. Of these, only one subpopulation (∼16% of neurons) yielded similar correlation maps to the local fMRI signal. The results employ the readout of large-scale fMRI networks and, by indicating multiple functional domains within a single voxel, present a new view of functional diversity within a local neural population. |
Aishwarya Parthasarathy; Roger Herikstad; Jit Hon Bong; Felipe Salvador Medina; Camilo Libedinsky; Shih-Cheng Yen Mixed selectivity morphs population codes in prefrontal cortex Journal Article In: Nature Neuroscience, vol. 20, no. 12, pp. 1770–1779, 2017. @article{Parthasarathy2017,The prefrontal cortex plays an important role in the maintenance of working memory, as evidenced by studies using microelectrode recordings 1, lesions 2, inactivation 3, micro-stimulation 4, 5, and functional neuroimaging 6. Furthermore, the pre-frontal cortex suppresses task-irrelevant stimuli, or distractors 3, 7, 8. This has led to the notion that the prefrontal cortex plays a central role in the maintenance of working memory and the suppression of distractors, which are cornerstones of executive processing. Individual neurons in the lateral prefrontal cortex (LPFC; Brodmann area 46) show selective, sustained activity during the delay period of working memory and only as long as the memory is maintained 1,9,10. Populations of LPFC neurons form a stable memory code during the delay period of a working memory task 11. Distractors are thought to be suppressed in the LPFC, since it responds less to distractors than to task-relevant stimuli 3, 7, 8. Notably, sustained activity of LPFC neurons persists even after distractors are presented 3, 10. Thus, it is reasonable to hypothesize that the stable code observed during the delay period persists after a distractor is presented, forming a persistent code throughout the memory period. Recent studies have shown that the LPFC hosts an abundance of neurons with mixed selectivity 12-19. These cells encode multiple parameters of the task simultaneously, such as sensory stimuli, task rule, or motor response. In particular, neurons with nonlinear mixed selectivity (NMS) are thought to play a key role in the encoding of information 18, 20. In the context of a working memory task with interfering distractors, mixed selectivity could lead to a change in code after the distractor is presented. Thus, it is also reasonable to hypothesize that the code does not persist throughout the memory period but rather that it is flexible, with the ability to adapt to new task contingencies, such as the presentation of a distractor. Here we found that the LPFC morphs its code, as the latter hypothesis predicts , while the frontal eye fields (FEF) maintain a stable code, in agreement with the former hypothesis. Results Two monkeys were trained to perform a delayed saccade task (Fig. 1a). Overall performance of both animals was higher than 75% correct (Fig. 1b). We recorded a total of 256 neurons from the LPFC (144 from Monkey A and 112 from Monkey B; the positions of the implanted electrode arrays are shown in red in Fig. 1c) and 137 neurons from the FEF (125 from Monkey A and 12 from Monkey B; electrode arrays are shown in blue in Fig. 1c) while the animals performed the task. Of the neurons recorded, more than 40% displayed selectiv-ity to target location in at least one stage during the trial (Fig. 1d). Examples of the responses of an LPFC and an FEF neuron are shown in Supplementary Fig. 1a,b. To quantify the magnitude of this selec-tivity, we computed the percentage of explained variance (PEV) for spatial selectivity in each neuron. The average PEVs across significant neurons (Methods) are shown in Fig. 1d. In the LPFC, we observed that target information in selective cells (n = 107, 42% of the LPFC population) increased during the target presentation period and remained stable throughout the rest of the trial (Fig. 1d). In addition, in Supplementary Fig. 1c, we show that the distractor information was much lower in these same neurons during the Delay 2 period (P < 0.001, Hedges' g = 23.99). A previous study found a sharp decrease in target information following distractor presentation , together with an increase of distractor information 21. Our results, however, did not replicate these observations. Rather, we found that target information remained stable, and distractor information stayed close to baseline throughout the trial (Supplementary Fig. 1c). This difference may reflect the simpler nature of our task and the comparatively lower behavioral saliency of the distractor we used. It may also reflect differences in the ways different types of information are encoded; perhaps the working memory code for numerosity in LPFC is more susceptible to distractors than the code for spatial locations. In contrast, in the FEF we observed The prefrontal cortex maintains working memory information in the presence of distracting stimuli. It has long been thought that sustained activity in individual neurons or groups of neurons was responsible for maintaining information in the form of a persistent, stable code. Here we show that, upon the presentation of a distractor, information in the lateral prefrontal cortex was reorganized into a different pattern of activity to create a morphed stable code without losing information. In contrast, the code in the frontal eye fields persisted across different delay periods but exhibited substantial instability and information loss after the presentation of a distractor. We found that neurons with mixed-selective responses were necessary and sufficient for the morphing of code and that these neurons were more abundant in the lateral prefrontal cortex than the frontal eye fields. This suggests that mixed selectivity provides populations with code-morphing capability, a property that may underlie cognitive flexibility. |
Tyler R. Peel; Suryadeep Dash; Stephen G. Lomber; Brian D. Corneil Frontal eye field inactivation diminishes superior colliculus activity, but delayed saccadic accumulation governs reaction time increases Journal Article In: Journal of Neuroscience, vol. 37, no. 48, pp. 11715–11730, 2017. @article{Peel2017,Stochastic accumulator models provide a comprehensive framework for how neural activity could produce behavior. Neural activity within the frontal eye fields (FEFs) and intermediate layers of the superior colliculus (iSC) support such models for saccade initiation by relating variations in saccade reaction time (SRT) to variations in such parameters as baseline, rate of accumulation of activity, and threshold. Here, by recording iSC activity during reversible cryogenic inactivation of the FEF in four male nonhuman primates, we causally tested which parameter(s) best explains concomitant increases in SRT. While FEF inactivation decreased all aspects of ipsilesional iSC activity, decreases in accumulation rate and threshold poorly predicted accompanying increases in SRT. Instead, SRT increases best correlated with delays in the onset of saccade-related accumulation. We conclude that FEF signals govern the onset of saccade-related accumulation within the iSC, and that the onset of accumulation is a relevant parameter for stochastic accumulation models of saccade initiation. |
Joel Reithler; Judith C. Peters; Rainer Goebel In: NeuroImage, vol. 152, pp. 551–562, 2017. @article{Reithler2017,Visual scenes are initially processed via segregated neural pathways dedicated to either of the two visual hemifields. Although higher-order visual areas are generally believed to utilize invariant object representations (abstracted away from features such as stimulus position), recent findings suggest they retain more spatial information than previously thought. Here, we assessed the nature of such higher-order object representations in human cortex using high-resolution fMRI at 7T, supported by corroborative 3T data. We show that multi-voxel activation patterns in both the contra- and ipsilateral hemisphere can be exploited to successfully classify the object category of unilaterally presented stimuli. Moreover, robustly identified rank order-based response profiles demonstrated a strong contralateral bias which frequently outweighed object category preferences. Finally, we contrasted different combinatorial operations to predict the responses during bilateral stimulation conditions based on responses to their constituent unilateral elements. Results favored a max operation predominantly reflecting the contralateral stimuli. The current findings extend previous work by showing that configuration-dependent modulations in higher-order visual cortex responses as observed in single unit activity have a counterpart in human neural population coding. They furthermore corroborate the emerging view that position coding is a fundamental functional characteristic of ventral visual stream processing. |
Douglas A. Ruff; Marlene R. Cohen A normalization model suggests that attention changes the weighting of inputs between visual areas Journal Article In: Proceedings of the National Academy of Sciences, vol. 114, no. 20, pp. E4085–E4094, 2017. @article{Ruff2017,Models of divisive normalization can explain the trial-averaged responses of neurons in sensory, association, and motor areas under a wide range of conditions, including how visual attention changes the gains of neurons in visual cortex. Attention, like other modulatory processes, is also associated with changes in the extent to which pairs of neurons share trial-to-trial variability. We showed recently that in addition to decreasing correlations between similarly tuned neurons within the same visual area, attention increases correlations between neurons in primary visual cortex (V1) and the middle temporal area (MT) and that an extension of a classic normalization model can account for this correlation increase. One of the benefits of having a descriptive model that can account for many physiological observations is that it can be used to probe the mechanisms underlying processes such as attention. Here, we use electrical microstimulation in V1 paired with recording in MT to provide causal evidence that the relationship between V1 and MT activity is nonlinear and is well described by divisive normalization. We then use the normalization model and recording and microstimulation experiments to show that the attention dependence of V1-MT correlations is better explained by a mechanism in which attention changes the weights of connections between V1 and MT than by a mechanism that modulates responses in either area. Our study shows that normalization can explain interactions between neurons in different areas and provides a framework for using multiarea recording and stimulation to probe the neural mechanisms underlying neuronal computations. |
Aldo Rustichini; Katherine E. Conen; Xinying Cai; Camillo Padoa-Schioppa Optimal coding and neuronal adaptation in economic decisions Journal Article In: Nature Communications, vol. 8, pp. 1208, 2017. @article{Rustichini2017,During economic decisions, offer value cells in orbitofrontal cortex (OFC) encode the values of offered goods. Furthermore, their tuning functions adapt to the range of values available in any given context. A fundamental and open question is whether range adaptation is behaviorally advantageous. Here we present a theory of optimal coding for economic decisions. We propose that the representation of offer values is optimal if it ensures maximal expected payoff. In this framework, we examine offer value cells in non-human primates. We show that their responses are quasi-linear even when optimal tuning functions are highly non-linear. Most importantly, we demonstrate that for linear tuning functions range adaptation maximizes the expected payoff. Thus value coding in OFC is functionally rigid (linear tuning) but parametrically plastic (range adaptation with optimal gain). Importantly, the benefit of range adaptation outweighs the cost of functional rigidity. While generally suboptimal, linear tuning may facilitate transitive choices. |
Philipp Schwedhelm; Daniel Baldauf; Stefan Treue Electrical stimulation of macaque lateral prefrontal cortex modulates oculomotor behavior indicative of a disruption of top-down attention Journal Article In: Scientific Reports, vol. 7, pp. 17715, 2017. @article{Schwedhelm2017,The lateral prefrontal cortex (lPFC) of primates is hypothesized to be heavily involved in decision-making and selective visual attention. Recent neurophysiological evidence suggests that information necessary for an orchestration of those high-level cognitive factors are indeed represented in the lPFC. However, we know little about the specific contribution of sub-networks within lPFC to the deployment of top-down influences that can be measured in extrastriate visual cortex. Here, we systematically applied electrical stimulations to areas 8Av and 45 of two macaque monkeys performing a concurrent goal-directed saccade task. Despite using currents well above saccadic thresholds of the directly adjacent Frontal Eye Fields (FEF), saccades were only rarely evoked by the stimulation. Instead, two types of behavioral effects were observed: Stimulations of caudal sites in 8Av (close to FEF) shortened or prolonged saccadic reaction times, depending on the task-instructed saccade, while rostral stimulations of 8Av/45 seem to affect the relative attentional weighting of saccade targets as well as saccadic reaction times. These results illuminate important differences in the causal involvement of different sub-networks within the lPFC and are most compatible with a stimulation-induced biasing of stimulus processing that accelerates the detection of saccade targets presented ipsilateral to stimulation through a disruption of contralaterally deployed top-down attention. |
Lenka Seillier; Corinna Lorenz; Katsuhisa Kawaguchi; Torben Ott; Andreas Nieder; Paria Pourriahi; Hendrikje Nienborg Serotonin decreases the gain of visual responses in awake macaque V1 Journal Article In: Journal of Neuroscience, vol. 37, no. 47, pp. 11390 –11405 Systems/Circuits, 2017. @article{Seillier2017,Serotonin, an important neuromodulator in the brain, is implicated in affective and cognitive functions. However, its role even for basic cortical processes is controversial. For example, in the mammalian primary visual cortex (V1), heterogenous serotonergic modulation has been observed in anesthetized animals. Here, we combined extracellular single-unit recordings with iontophoresis in awake animals. We examined the role of serotonin on well-defined tuning properties (orientation, spatial frequency, contrast, and size) in V1 of two male macaque monkeys. We find that in the awake macaque the modulatory effect of serotonin is surprisingly uniform: it causes a mainly multiplicative decrease of the visual responses and a slight increase in the stimulus-selective response latency. Moreover, serotonin neither systematically changes the selectivity or variability of the response, nor the interneuronal correlation unexplained by the stimulus ("noise-correlation"). The modulation by serotonin has qualitative similarities with that for a decrease in stimulus contrast, but differs quantitatively from decreasing contrast. It can be captured by a simple additive change to a threshold-linear spiking nonlinearity. Together, our results show that serotonin is well suited to control the response gain of neurons in V1 depending on the animal's behavioral or motivational context, complementing other known state-dependent gain-control mechanisms. |
Brianna J. Sleezer; Giuliana A. LoConte; Meghan D. Castagno; Benjamin Y. Hayden Neuronal responses support a role for orbitofrontal cortex in cognitive set reconfiguration Journal Article In: European Journal of Neuroscience, vol. 45, pp. 940–951, 2017. @article{Sleezer2017,We are often faced with the need to abandon no-longer beneficial rules and adopt new ones. This process, known as cognitive set reconfiguration, is a hallmark of executive control. Although cognitive functions like reconfiguration are most often associated with dorsal prefrontal structures, recent evidence suggests that the orbitofrontal cortex (OFC) may play an important role as well. We recorded the activity of OFC neurons while rhesus macaques performed an analogue of the Wisconsin Card Sorting Task that involved a trial and error stage. The OFC neurons demonstrated two types of switch-related activity, an early (switch-away) signal and a late (switch-to) signal, when the new task set was established. We also found a pattern of match modulation: a sig- nificant change in activity for the stimulus that matched the current perceptual rule (and would therefore be selected). These results extend our understanding of the executive functions of the OFC. They also allow us to directly compare the OFC with the complementary datasets we previously collected in the ventral (VS) and dorsal (DS) striatum. Although both effects are observed in all three areas, the timing of responses aligns the OFC more closely with DS than with VS. |
Courtney Turrin; Nicholas A. Fagan; Olga Dal Monte; Steve W. C. Chang Social resource foraging is guided by the principles of the Marginal Value Theorem Journal Article In: Scientific Reports, vol. 7, pp. 11274, 2017. @article{Turrin2017,Optimality principles guide how animals adapt to changing environments. During foraging for nonsocial resources such as food and water, species across taxa obey a strategy that maximizes resource harvest rate. However, it remains unknown whether foraging for social resources also obeys such a strategic principle. We investigated how primates forage for social information conveyed by conspecific facial expressions using the framework of optimal foraging theory. We found that the canonical principle of Marginal Value Theorem (MVT) also applies to social resources. Consistent with MVT, rhesus macaques (Macaca mulatta) spent more time foraging for social information when alternative sources of information were farther away compared to when they were closer by. A comparison of four models of patch-leaving behavior confirmed that the MVT framework provided the best fit to the observed foraging behavior. This analysis further demonstrated that patch-leaving decisions were not driven simply by the declining value of the images in the patch, but instead were dependent upon both the instantaneous social value intake rate and current time in the patch. |
Bram-Ernst Verhoef; John H. R. Maunsell Attention-related changes in correlated neuronal activity arise from normalization mechanisms Journal Article In: Nature Neuroscience, vol. 20, no. 7, pp. 969–977, 2017. @article{Verhoef2017,Attention is believed to enhance perception by altering the activity-level correlations between pairs of neurons. How attention changes neuronal activity correlations is unknown. Using multielectrodes in monkey visual cortex, we measured spike-count correlations when single or multiple stimuli were presented and when stimuli were attended or unattended. When stimuli were unattended, adding a suppressive, nonpreferred stimulus beside a preferred stimulus increased spike-count correlations between pairs of similarly tuned neurons but decreased spike-count correlations between pairs of oppositely tuned neurons. A stochastic normalization model containing populations of oppositely tuned, mutually suppressive neurons explains these changes and also explains why attention decreased or increased correlations: as an indirect consequence of attention-related changes in the inputs to normalization mechanisms. Our findings link normalization mechanisms to correlated neuronal activity and attention, showing that normalization mechanisms shape response correlations and that these correlations change when attention biases normalization mechanisms. |