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2020 |
Benjamin Voloh; Mariann Oemisch; Thilo Womelsdorf Phase of firing coding of learning variables across the fronto-striatal network during feature-based learning Journal Article In: Nature Communications, vol. 11, pp. 4669, 2020. @article{Voloh2020,The prefrontal cortex and striatum form a recurrent network whose spiking activity encodes multiple types of learning-relevant information. This spike-encoded information is evident in average firing rates, but finer temporal coding might allow multiplexing and enhanced readout across the connected network. We tested this hypothesis in the fronto-striatal network of nonhuman primates during reversal learning of feature values. We found that populations of neurons encoding choice outcomes, outcome prediction errors, and outcome history in their firing rates also carry significant information in their phase-of-firing at a 10–25 Hz band-limited beta frequency at which they synchronize across lateral prefrontal cortex, anterior cingulate cortex and anterior striatum when outcomes were processed. The phase-of-firing code exceeds information that can be obtained from firing rates alone and is evident for inter-areal connections between anterior cingulate cortex, lateral prefrontal cortex and anterior striatum. For the majority of connections, the phase-of-firing information gain is maximal at phases of the beta cycle that were offset from the preferred spiking phase of neurons. Taken together, these findings document enhanced information of three important learning variables at specific phases of firing in the beta cycle at an inter-areally shared beta oscillation frequency during goal-directed behavior. |
Steven Wiesner; Ian W. Baumgart; Xin Huang Spatial arrangement drastically changes the neural representation of multiple visual stimuli that compete in more than one feature domain Journal Article In: The Journal of Neuroscience, vol. 40, no. 9, pp. 1834–1848, 2020. @article{Wiesner2020,Natural scenes often contain multiple objects and surfaces. However, how neurons in the visual cortex represent multiple visual stimuli is not well understood. Previous studies have shown that, when multiple stimuli compete in one feature domain, the evoked neuronal response is biased toward the stimulus that has a stronger signal strength. We recorded from two male macaques to investigate how neurons in the middle temporal cortex (MT) represent multiple stimuli that compete in more than one feature domain. Visual stimuli were two random-dot patches moving in different directions. One stimulus had low luminance contrast and moved with high coherence, whereas the other had high contrast and moved with low coherence. We found that how MT neurons represent multiple stimuli depended on the spatial arrangement. When two stimuli were overlapping, MT responses were dominated by the stimulus component that had high contrast. When two stimuli were spatially separated within the receptive fields, the contrast dominance was abolished. We found the same results when using contrast to compete with motion speed. Our neural data and computer simulations using a V1-MT model suggest that the contrast dominance found with overlapping stimuli is due to normalization occurring at an input stage fed to MT, and MT neurons cannot overturn this bias based on their own feature selectivity. The interaction between spatially separated stimuli can largely be explained by normalization within MT. Our results revealed new rules on stimulus competition and highlighted the impact of hierarchical processing on representing multiple stimuli in the visual cortex. |
Vanessa A. D. Wilson; Carolin Kade; Sebastian Moeller; Stefan Treue; Igor Kagan; Julia Fischer Macaque gaze responses to the primatar: A virtual macaque head for social cognition research Journal Article In: Frontiers in Psychology, vol. 11, pp. 1645, 2020. @article{Wilson2020a,Following the expanding use and applications of virtual reality in everyday life, realistic virtual stimuli are of increasing interest in cognitive studies. They allow for control of features such as gaze, expression, appearance, and movement, which may help to overcome limitations of using photographs or video recordings to study social responses. In using virtual stimuli however, one must be careful to avoid the uncanny valley effect, where realistic stimuli can be perceived as eerie, and induce an aversion response. At the same time, it is important to establish whether responses to virtual stimuli mirror responses to depictions of a real conspecific. In the current study, we describe the development of a new virtual monkey head with realistic facial features for experiments with nonhuman primates, the “Primatar.” As a first step toward validation, we assessed how monkeys respond to facial images of a prototype of this Primatar compared to images of real monkeys (RMs), and an unrealistic model. We also compared gaze responses between original images and scrambled as well as obfuscated versions of these images. We measured looking time to images in six freely moving long-tailed macaques (Macaca fascicularis) and gaze exploration behavior in three rhesus macaques (Macaca mulatta). Both groups showed more signs of overt attention to original images than scrambled or obfuscated images. In addition, we found no evidence for an uncanny valley effect; since for both groups, looking times did not differ between real, realistic, or unrealistic images. These results provide important data for further development of our Primatar for use in social cognition studies and more generally for cognitive research with virtual stimuli in nonhuman primates. Future research on the absence of an uncanny valley effect in macaques is needed, to elucidate the roots of this mechanism in humans. |
Seng Bum Michael Yoo; Benjamin Y. Hayden The transition from evaluation to selection involves neural subspace reorganization in core reward regions Journal Article In: Neuron, vol. 105, no. 4, pp. 712–724.e4, 2020. @article{Yoo2020,Economic choice proceeds from evaluation, in which we contemplate options, to selection, in which we weigh options and choose one. These stages must be differentiated so that decision makers do not proceed to selection before evaluation is complete. We examined responses of neurons in two core reward regions, orbitofrontal (OFC) and ventromedial prefrontal cortex (vmPFC), during two-option choice with asynchronous offer presentation. Our data suggest that neurons selective during the first (presumed evaluation) and second (presumed comparison and selection) offer epochs come from a single pool. Stage transition is accompanied by a shift toward orthogonality in the low-dimensional population response manifold. Nonetheless, the relative position of each option in driving responses in the population subspace is preserved. The orthogonalization we observe supports the hypothesis that the transition from evaluation to selection leads to reorganization of response subspace and suggests a mechanism by which value-related signals are prevented from prematurely driving choice. |
Mengxi Yun; Takashi Kawai; Masafumi Nejime; Hiroshi Yamada; Masayuki Matsumoto Signal dynamics of midbrain dopamine neurons during economic decision-making in monkeys Journal Article In: Science Advances, vol. 6, no. 27, pp. eaba4962, 2020. @article{Yun2020,When we make economic choices, the brain first evaluates available options and then decides whether to choose them. Midbrain dopamine neurons are known to reinforce economic choices through their signal evoked by outcomes after decisions are made. However, although critical internal processing is executed while decisions are being made, little is known about the role of dopamine neurons during this period. We found that dopamine neurons exhibited dynamically changing signals related to the internal processing while rhesus monkeys were making decisions. These neurons encoded the value of an option immediately after it was offered and then gradually changed their activity to represent the animal's upcoming choice. Similar dynamics were observed in the orbitofrontal cortex, a center for economic decision-making, but the value-to-choice signal transition was completed earlier in dopamine neurons. Our findings suggest that dopamine neurons are a key component of the neural network that makes choices from values during ongoing decision-making processes. |
Polina Zamarashkina; Dina V. Popovkina; Anitha Pasupathy Timing of response onset and offset in macaque V4: stimulus and task dependence Journal Article In: Journal of Neurophysiology, vol. 123, no. 6, pp. 2311–2325, 2020. @article{Zamarashkina2020,In the primate visual cortex, both the magnitude of the neuronal response and its timing can carry important information about the visual world, but studies typically focus only on response magnitude. Here, we examine the onset and offset latency of the responses of neurons in area V4 of awake, behaving macaques across several experiments in the context of a variety of stimuli and task paradigms. Our results highlight distinct contributions of stimuli and tasks to V4 response latency. We found that response onset latencies are shorter than typically cited (median = 75.5 ms), supporting a role for V4 neurons in rapid object and scene recognition functions. Moreover, onset latencies are longer for smaller stimuli and stimulus outlines, consistent with the hypothesis that longer latencies are associated with higher spatial frequency content. Strikingly, we found that onset latencies showed no significant dependence on stimulus occlusion, unlike in inferotemporal cortex, nor on task demands. Across the V4 population, onset latencies had a broad distribution, reflecting the diversity of feedforward, recurrent, and feedback connections that inform the responses of individual neurons. Response offset latencies, on the other hand, displayed the opposite tendency in their relationship to stimulus and task attributes: they are less influenced by stimulus appearance but are shorter in guided saccade tasks compared with fixation tasks. The observation that response latency is influenced by stimulus- and task-associated factors emphasizes a need to examine response timing alongside firing rate in determining the functional role of area V4.NEW & NOTEWORTHY Onset and offset timing of neuronal responses can provide information about visual environment and neuron's role in visual processing and its anatomical connectivity. In the first comprehensive examination of onset and offset latencies in the intermediate visual cortical area V4, we find neurons respond faster than previously reported, making them ideally suited to contribute to rapid object and scene recognition. While response onset reflects stimulus characteristics, timing of response offset is influenced more by behavioral task. |
2019 |
Ariana R. Andrei; Sorin A. Pojoga; Roger Janz; Valentin Dragoi Integration of cortical population signals for visual perception Journal Article In: Nature Communications, vol. 10, pp. 3832, 2019. @article{Andrei2019,Visual stimuli evoke heterogeneous responses across nearby neural populations. These signals must be locally integrated to contribute to perception, but the principles underlying this process are unknown. Here, we exploit the systematic organization of orientation preference in macaque primary visual cortex (V1) and perform causal manipulations to examine the limits of signal integration. Optogenetic stimulation and visual stimuli are used to simultaneously drive two neural populations with overlapping receptive fields. We report that optogenetic stimulation raises firing rates uniformly across conditions, but improves the detection of visual stimuli only when activating cells that are preferentially-tuned to the visual stimulus. Further, we show that changes in correlated variability are exclusively present when the optogenetically and visually-activated populations are functionally-proximal, suggesting that correlation changes represent a hallmark of signal integration. Our results demonstrate that information from functionally-proximal neurons is pooled for perception, but functionally-distal signals remain independent. Primary visual cortical neurons exhibit diverse responses to visual stimuli yet how these signals are integrated during visual perception is not well understood. Here, the authors show that optogenetic stimulation of neurons situated near the visually‐driven population leads to improved orientation detection in monkeys through changes in correlated variability. |
Maria C. Romero; Marco Davare; Marcelo Armendariz; Peter Janssen Neural effects of transcranial magnetic stimulation at the single-cell level Journal Article In: Nature Communications, vol. 10, pp. 2642, 2019. @article{Romero2019,Transcranial magnetic stimulation (TMS) can non-invasively modulate neural activity in humans. Despite three decades of research, the spatial extent of the cortical area activated by TMS is still controversial. Moreover, how TMS interacts with task-related activity during motor behavior is unknown. Here, we applied single-pulse TMS over macaque parietal cortex while recording single-unit activity at various distances from the center of stimulation during grasping. The spatial extent of TMS-induced activation is remarkably restricted, affecting the spiking activity of single neurons in an area of cortex measuring less than 2 mm in diameter. In task-related neurons, TMS evokes a transient excitation followed by reduced activity, paralleled by a significantly longer grasping time. Furthermore, TMS-induced activity and task-related activity do not summate in single neurons. These results furnish crucial experimental evidence for the neural effects of TMS at the single-cell level and uncover the neural underpinnings of behavioral effects of TMS. |
Seth W. Egger; Evan D. Remington; Chia-Jung Chang; Mehrdad Jazayeri Internal models of sensorimotor integration regulate cortical dynamics Journal Article In: Nature Neuroscience, vol. 22, pp. 1871–1882, 2019. @article{Egger2019,Sensorimotor control during overt movements is characterized in terms of three building blocks: a controller, a simulator and a state estimator. We asked whether the same framework could explain the control of internal states in the absence of movements. Recently, it was shown that the brain controls the timing of future movements by adjusting an internal speed command. We trained monkeys in a novel task in which the speed command had to be dynamically controlled based on the timing of a sequence of flashes. Recordings from the frontal cortex provided evidence that the brain updates the internal speed command after each flash based on the error between the timing of the flash and the anticipated timing of the flash derived from a simulated motor plan. These findings suggest that cognitive control of internal states may be understood in terms of the same computational principles as motor control. Control of movements can be understood in terms of the interplay between a controller, a simulator and an estimator. Egger et. al. show that cortical neurons establish the same building blocks to control cognitive states in the absence of movement. |
Ramina Adam; Kevin D. Johnston; Stefan Everling In: Journal of Neurophysiology, vol. 122, no. 2, pp. 672–690, 2019. @article{Adam2019,The caudal primate prefrontal cortex (PFC) is involved in target selection and visually guided saccades through both covert attention and overt orienting eye movements. Unilateral damage to the caudal PFC often leads to decreased awareness of a contralesional target alone, referred to as “neglect,” or when it is presented simultaneously with an ipsilesional target, referred to as “extinction.” In the current study, we examined whether deficits in contralesional target selection were due to contralesional oculomotor deficits, such as slower reaction times. We experimentally induced a focal ischemic lesion in the right caudal PFC of 4 male macaque monkeys using the vasoconstrictor endothelin-1 and measured saccade choice and reaction times on double-stimulus free-choice tasks and single-stimulus trials before and after the lesion. We found that 1) endothelin-1-induced lesions in the caudal PFC produced contralesional target selection deficits that varied in severity and duration based on lesion volume and location; 2) contralesional neglect-like deficits were transient and recovered by week 4 postlesion; 3) contralesional extinction-like deficits were longer lasting and recovered by weeks 8–16 postlesion; 4) contralesional reaction time returned to baseline well before the contralesional choice deficit had recovered; and 5) neither the mean reaction times nor the reaction time distributions could account for the degree of contralesional extinction on the free-choice task throughout recovery. These findings demonstrate that the saccade choice bias observed after a right caudal PFC lesion is not exclusively due to contralesional motor deficits, but instead reflects a combination of impaired motor and attentional processing. |
Kun Guo; Zhihan Li; Yin Yan; Wu Li Viewing heterospecific facial expressions: an eye-tracking study of human and monkey viewers Journal Article In: Experimental Brain Research, vol. 237, no. 8, pp. 2045–2059, 2019. @article{Guo2019,Common facial expressions of emotion have distinctive patterns of facial muscle movements that are culturally similar among humans, and perceiving these expressions is associated with stereotypical gaze allocation at local facial regions that are characteristic for each expression, such as eyes in angry faces. It is, however, unclear to what extent this ‘universality' view can be extended to process heterospecific facial expressions, and how ‘social learning' process contributes to heterospecific expression perception. In this eye-tracking study, we examined face-viewing gaze allocation of human (including dog owners and non-dog owners) and monkey observers while exploring expressive human, chimpanzee, monkey and dog faces (positive, neutral and negative expressions in human and dog faces; neutral and negative expressions in chimpanzee and monkey faces). Human observers showed species- and experience-dependent expression categorization accuracy. Furthermore, both human and monkey observers demonstrated different face-viewing gaze distributions which were also species dependent. Specifically, humans predominately attended at human eyes but animal mouth when judging facial expressions. Monkeys' gaze distributions in exploring human and monkey faces were qualitatively different from exploring chimpanzee and dog faces. Interestingly, the gaze behaviour of both human and monkey observers were further affected by their prior experience of the viewed species. It seems that facial expression processing is species dependent, and social learning may play a significant role in discriminating even rudimentary types of heterospecific expressions. |
Florian Sandhaeger; Constantin Nicolai; Earl K. Miller; Markus Siegel Monkey EEG links neuronal color and motion information across species and scales Journal Article In: eLife, vol. 8, pp. 1–21, 2019. @article{Sandhaeger2019,It remains challenging to relate EEG and MEG to underlying circuit processes and comparable experiments on both spatial scales are rare. To close this gap between invasive and non-invasive electrophysiology we developed and recorded human-comparable EEG in macaque monkeys during visual stimulation with colored dynamic random dot patterns. Furthermore, we performed simultaneous microelectrode recordings from 6 areas of macaque cortex and human MEG. Motion direction and color information were accessible in all signals. Tuning of the non- invasive signals was similar to V4 and IT, but not to dorsal and frontal areas. Thus, MEG and EEG were dominated by early visual and ventral stream sources. Source level analysis revealed corresponding information and latency gradients across cortex. We show how information-based methods and monkey EEG can identify analogous properties of visual processing in signals spanning spatial scales from single units to MEG – a valuable framework for relating human and animal studies. |
Sébastien Ballesta; Camillo Padoa-Schioppa Economic decisions through circuit inhibition Journal Article In: Current Biology, vol. 29, no. 22, pp. 3814–3824, 2019. @article{Ballesta2019,Economic choices between goods are thought to rely on the orbitofrontal cortex (OFC), but the decision mechanisms remain poorly understood. To shed light on this fundamental issue, we recorded from the OFC of monkeys choosing between two juices offered sequentially. An analysis of firing rates across time windows revealed the presence of different groups of neurons similar to those previously identified under simultaneous offers. This observation suggested that economic decisions in the two modalities are formed in the same neural circuit. We then examined several hypotheses on the decision mechanisms. OFC neurons encoded good identities and values in a juice-based representation (labeled lines). Contrary to previous assessments, our data argued against the idea that decisions rely on mutual inhibition at the level of offer values. In fact, we showed that previous arguments for mutual inhibition were confounded by differences in value ranges. Instead, decisions seemed to involve mechanisms of circuit inhibition, whereby each offer value indirectly inhibited neurons encoding the opposite choice outcome. Our results reconcile a variety of previous findings and provide a general account for the neuronal underpinnings of economic choices. |
Annamaria Barczak; Saskia Haegens; Deborah A. Ross; Tammy McGinnis; Peter Lakatos; Charles E. Schroeder Dynamic modulation of cortical excitability during visual active sensing Journal Article In: Cell Reports, vol. 27, no. 12, pp. 3447–3459, 2019. @article{Barczak2019,Visual physiology is traditionally investigated by presenting stimuli with gaze held constant. However, during active viewing of a scene, information is actively acquired using systematic patterns of fixations and saccades. Prior studies suggest that during such active viewing, both nonretinal, saccade-related signals and “extra-classical” receptive field inputs modulate visual processing. This study used a set of active viewing tasks that allowed us to compare visual responses with and without direct foveal input, thus isolating the contextual eye movement-related influences. Studying nonhuman primates, we find strong contextual modulation in primary visual cortex (V1): excitability and response amplification immediately after fixation onset, transiting to suppression leading up to the next saccade. Time-frequency decomposition suggests that this amplification and suppression cycle stems from a phase reset of ongoing neuronal oscillatory activity. The impact of saccade-related contextual modulation on stimulus processing makes active visual sensing fundamentally different from the more passive processes investigated in traditional paradigms. By isolating contextual eye movement-related influences during active vision, Barczak et al. show that eye movements affect excitability in V1 such that responses are amplified immediately after fixation onset and suppressed as the next saccade approaches. This amplification and suppression cycle stems from a phase reset of ambient oscillatory activity in V1. |
Marie E. Bellet; Joachim Bellet; Hendrikje Nienborg; Ziad M. Hafed; Philipp Berens Human-level saccade detection performance using deep neural networks Journal Article In: Journal of Neurophysiology, vol. 121, no. 2, pp. 646–661, 2019. @article{Bellet2019,Saccades are ballistic eye movements that rapidly shift gaze from one location of visual space to another. Detecting saccades in eye movement recordings is important not only for studying the neural mechanisms underlying sensory, motor, and cognitive processes, but also as a clinical and diagnostic tool. However, automatically detecting saccades can be difficult, particularly when such saccades are generated in coordination with other tracking eye movements, like smooth pursuits, or when the saccade amplitude is close to eye tracker noise levels, like with microsaccades. In such cases, labeling by human experts is required, but this is a tedious task prone to variability and error. We developed a convolutional neural network to automatically detect saccades at human-level accuracy and with minimal training examples. Our algorithm surpasses state of the art according to common performance metrics and could facilitate studies of neurophysiological processes underlying saccade generation and visual processing. |
Narcisse P. Bichot; Rui Xu; Azriel Ghadooshahy; Michael L. Williams; Robert Desimone The role of prefrontal cortex in the control of feature attention in area V4 Journal Article In: Nature Communications, vol. 10, pp. 5727, 2019. @article{Bichot2019,When searching for an object in a cluttered scene, we can use our memory of the target object features to guide our search, and the responses of neurons in multiple cortical visual areas are enhanced when their receptive field contains a stimulus sharing target object features. Here we tested the role of the ventral prearcuate region (VPA) of prefrontal cortex in the control of feature attention in cortical visual area V4. VPA was unilaterally inactivated in monkeys performing a free-viewing visual search for a target stimulus in an array of stimuli, impairing monkeys' ability to find the target in the array in the affected hemifield, but leaving intact their ability to make saccades to targets presented alone. Simultaneous recordings in V4 revealed that the effects of feature attention on V4 responses were eliminated or greatly reduced while leaving the effects of spatial attention on responses intact. Altogether, the results suggest that feedback from VPA modulates processing in visual cortex during attention to object features. |
Rasmus M. Birn; Alexander K. Converse; Abigail Z. Rajala; Andrew L. Alexander; Walter F. Block; Alan B. McMillan; Bradley T. Christian; Caitlynn N. Filla; Dhanabalan Murali; Samuel A. Hurley; Rick L. Jenison; Luis C. Populin Changes in endogenous dopamine induced by methylphenidate predict functional connectivity in nonhuman primates Journal Article In: Journal of Neuroscience, vol. 39, no. 8, pp. 1436–1444, 2019. @article{Birn2019,Dopamine (DA) levels in the striatum are increased by many therapeutic drugs, such as methylphenidate (MPH), which also alters behavioral and cognitive functions thought to be controlled by the PFC dose-dependently. We linked DA changes and functional connectivity (FC) using simultaneous [18F]fallypride PET and resting-state fMRI in awake male rhesus monkeys after oral administration of various doses of MPH. We found a negative correlation between [18F]fallypride nondisplaceable binding potential (BPND) and MPH dose in the head of the caudate (hCd), demonstrating increased extracellular DA resulting from MPH administration. The decreased BPND was negatively correlated with FC between the hCd and the PFC. Subsequent voxelwise analyses revealed negative correlations with FC between the hCd and the dorsolateral PFC, hippocampus, and precuneus. These results, showing that MPH-induced changes in DA levels in the hCd predict resting-state FC, shed light on a mechanism by which changes in striatal DA could influence function in the PFC. |
Amarender R. Bogadhi; Anil Bollimunta; David A. Leopold; Richard J. Krauzlis Spatial attention deficits are causally linked to an area in macaque temporal cortex Journal Article In: Current Biology, vol. 29, no. 5, pp. 726–736, 2019. @article{Bogadhi2019,Spatial neglect is a common clinical syndrome involving disruption of the brain's attention-related circuitry, including the dorsocaudal temporal cortex. In macaques, the attention deficits associated with neglect can be readily modeled, but the absence of evidence for temporal cortex involvement has suggested a fundamental difference from humans. To map the neurological expression of neglect-like attention deficits in macaques, we measured attention-related fMRI activity across the cerebral cortex during experimental induction of neglect through reversible inactivation of the superior colliculus and frontal eye fields. During inactivation, monkeys exhibited hallmark attentional deficits of neglect in tasks using either motion or non-motion stimuli. The behavioral deficits were accompanied by marked reductions in fMRI attentional modulation that were strongest in a small region on the floor of the superior temporal sulcus; smaller reductions were also found in frontal eye fields and dorsal parietal cortex. Notably, direct inactivation of the mid-superior temporal sulcus (STS) cortical region identified by fMRI caused similar neglect-like spatial attention deficits. These results identify a putative macaque homolog to temporal cortex structures known to play a central role in human neglect. |
Xinying Cai; Camillo Padoa-Schioppa Neuronal evidence for good-based economic decisions under variable action costs Journal Article In: Nature Communications, vol. 10, pp. 393, 2019. @article{Cai2019,Previous work showed that economic decisions can be made independently of spatial contingencies. However, when goods available for choice bear different action costs, the decision necessarily reflects aspects of the action. One possibility is that "stimulus values" are combined with the corresponding action costs in a motor representation, and decisions are then made in actions space. Alternatively, action costs could be integrated with other determinants of value in a non-spatial representation. If so, decisions under variable action costs could take place in goods space. Here, we recorded from orbitofrontal cortex while monkeys chose between different juices offered in variable amounts. We manipulated action costs by varying the saccade amplitude, and we dissociated in time and space offer presentation from action planning. Neurons encoding the binary choice outcome did so well before the presentation of saccade targets, indicating that decisions were made in goods space. |
Chih-Yang Chen; Klaus-Peter Hoffmann; Claudia Distler; Ziad M. Hafed The foveal visual representation of the primate superior colliculus Journal Article In: Current Biology, vol. 29, no. 13, pp. 2109–2119, 2019. @article{Chen2019h,A defining feature of the primate visual system is its foveated nature. Processing of foveal retinal input is important not only for high-quality visual scene analysis but also for ensuring precise, albeit tiny, gaze shifts during high-acuity visual tasks. The representations of foveal retinal input in the primate lateral geniculate nucleus and early visual cortices have been characterized. However, how such representations translate into precise eye movements remains unclear. Here, we document functional and structural properties of the foveal visual representation of the midbrain superior colliculus. We show that the superior colliculus, classically associated with extra-foveal spatial representations needed for gaze shifts, is highly sensitive to visual input impinging on the fovea. The superior colliculus also represents such input in an orderly and very specific manner, and it magnifies the representation of foveal images in neural tissue as much as the primary visual cortex does. The primate superior colliculus contains a high-fidelity visual representation, with large foveal magnification, perfectly suited for active visuomotor control and perception. Chen et al. show that superior colliculus (SC) is highly sensitive to foveal visual input and that it magnifies foveal image representation much more than previously anticipated. Their topography data, with large foveal magnification, show that tiny foveal stimuli can activate a large portion of SC neural tissue due to fixational eye movements. |
Katherine E. Conen; X. Camillo Padoa-Schioppa Partial adaptation to the value range in the macaque orbitofrontal cortex Journal Article In: Journal of Neuroscience, vol. 39, no. 18, pp. 3498 –3513, 2019. @article{Conen2019,Values available for choice in different behavioral contexts can vary immensely. To compensate for this variability, neuronal circuits underlying economic decisions undergo adaptation. In orbitofrontal cortex (OFC), neurons encode the subjective value of offered and chosen goods in a quasilinear way. Previous experiments found that the gain of the encoding is lower when the value range is wider. However, the parameters OFC neurons adapted to remained unclear. Furthermore, previous studies did not examine additive changes in neuronal responses. Computational considerations indicate that these factors can directly impact choice behavior. Here we investigated how OFC neurons adapt to changes in the value range. We recorded from two male rhesus monkeys during a juice choice task. Each session was divided into two blocks of trials. In each block, juices were offered within a set range of values, and ranges changed between blocks. Across blocks, neuronal responses adapted to both the maximum and the minimum value, but only partially. As a result, the minimum neural activity was elevated in some value ranges relative to others. Through simulation of a linear decision model, we showed that increasing the minimum response increases choice variability, lowering the expected payoff. This effect is modulated by the balance between cells with positive and negative encoding. The presence of these two populations induces a non-monotonic relationship between the value range and choice efficacy, such that the expected payoff is highest for decisions in an intermediate value range. |
Michele A. Cox; Kacie Dougherty; Geoffrey K. Adams; Eric A. Reavis; Jacob A. Westerberg; Brandon S. Moore; David A. Leopold; Alexander Maier Spiking suppression precedes cued attentional enhancement of neural responses in primary visual cortex Journal Article In: Cerebral Cortex, vol. 29, no. 1, pp. 77–90, 2019. @article{Cox2019a,Attending to a visual stimulus increases its detectability, even if gaze is directed elsewhere. This covert attentional selection is known to enhance spiking across many brain areas, including the primary visual cortex (V1). Here we investigate the temporal dynamics of attention-related spiking changes in V1 of macaques performing a task that separates attentional selection from the onset of visual stimulation. We found that preceding attentional enhancement there was a sharp, transient decline in spiking following presentation of an attention-guiding cue. This disruption of V1 spiking was not observed in a task-naive subject that passively observed the same stimulus sequence, suggesting that sensory activation is insufficient to cause suppression. Following this suppression, attended stimuli evoked more spiking than unattended stimuli, matching previous reports of attention-related activity in V1. Laminar analyses revealed a distinct pattern of activation in feedback-associated layers during both the cue-induced suppression and subsequent attentional enhancement. These findings suggest that top-down modulation of V1 spiking can be bidirectional and result in either suppression or enhancement of spiking responses. |
Michele A. Cox; Kacie Dougherty; Jacob A. Westerberg; Michelle S. Schall; Alexander Maier Temporal dynamics of binocular integration in primary visual cortex Journal Article In: Journal of Vision, vol. 19, no. 12, pp. 1–21, 2019. @article{Cox2019,Whenever we open our eyes, our brain quickly integrates the two eyes' perspectives into a combined view. This process of binocular integration happens so rapidly that even incompatible stimuli are briefly fused before one eye's view is suppressed in favor of the other (binocular rivalry). The neuronal basis for this brief period of fusion during incompatible binocular stimulation is unclear. Neuroanatomically, the eyes provide two largely separate streams of information that are integrated into a binocular response by the primary visual cortex (V1). However, the temporal dynamics underlying the formation of this binocular response are largely unknown. To address this question, we examined the temporal profile of binocular responses in V1 of fixating monkeys. We found that V1 processes binocular stimuli in a dynamic sequence that comprises at least two distinct temporal phases. An initial transient phase is characterized by enhanced spiking responses for both compatible and incompatible binocular stimuli compared to monocular stimulation. This transient is followed by a sustained response that differed markedly between congruent and incongruent binocular stimulation. Specifically, incompatible binocular stimulation resulted in overall response reduction relative to monocular stimulation (binocular suppression). In contrast, responses to compatible stimuli were either suppressed or enhanced (binocular facilitation) depending on the neurons' ocularity (selectivity for one eye over the other) and laminar location. These results suggest that binocular integration in V1 occurs in at least two sequential steps that comprise initial additive combination of the two eyes' signals followed by widespread differentiation between binocular concordance and discordance. |
Alexandre Dizeux; Marc Gesnik; Harry Ahnine; Kévin Blaize; Fabrice Arcizet; Serge Picaud; José-Alain Sahel; Thomas Deffieux; Pierre Pouget; Mickael Tanter Functional ultrasound imaging of the brain reveals propagation of task-related brain activity in behaving primates Journal Article In: Nature Communications, vol. 10, pp. 1400, 2019. @article{Dizeux2019,Neuroimaging modalities such as MRI and EEG are able to record from the whole brain, but this comes at the price of either limited spatiotemporal resolution or limited sensitivity. Here, we show that functional ultrasound imaging (fUS) of the brain is able to assess local changes in cerebral blood volume during cognitive tasks, with sufficient temporal resolution to measure the directional propagation of signals. In two macaques, we observed an abrupt transient change in supplementary eye field (SEF) activity when animals were required to modify their behaviour associated with a change of saccade tasks. SEF activation could be observed in a single trial, without averaging. Simultaneous imaging of anterior cingulate cortex and SEF revealed a time delay in the directional functional connectivity of 0.27 ± 0.07 s and 0.9 ± 0.2 s for both animals. Cerebral hemodynamics of large brain areas can be measured at high spatiotemporal resolution using fUS. |
Kacie Dougherty; Michele A. Cox; Jacob A. Westerberg; Alexander Maier Binocular modulation of monocular V1 neurons Journal Article In: Current Biology, vol. 29, no. 3, pp. 381–391, 2019. @article{Dougherty2019,In humans and other primates, sensory signals from each eye remain separated until they arrive in the primary visual cortex (V1), but their exact meeting point is unknown. In V1, some neurons respond to stimulation of only one eye (monocular neurons), while most neurons respond to stimulation of either eye (binocular neurons). The main input layers of V1 contain most of the monocular neurons while binocular neurons dominate the layers above and below. This observation has given rise to the idea that the two eyes' signals remain separate until they converge outside V1's input layers. Here, we show that, despite responding to only one eye, monocular neurons in all layers, including the input layers, of V1 discriminate between stimulation of their driving eye alone and stimulation of both eyes. Some monocular V1 neurons' responses were significantly enhanced, or facilitated, when both eyes were stimulated. Binocular facilitation within V1's input layers tended to occur at the onset of the visual response, which could be explained by converging thalamocortical inputs. However, most V1 monocular neurons were significantly reduced, or suppressed, to binocular stimulation. In contrast to facilitation, binocular suppression occurred several milliseconds following the onset of the visual response, suggesting that the bulk of binocular modulation involves cortical inhibition. These findings, combined, suggest that binocular signals arise at an earlier processing stage than previously appreciated, as even so-called monocular neurons in V1's input layers encode what is shown to both eyes. |
Lyndon Duong; Matthew Leavitt; Florian Pieper; Adam Sachs; Julio Martinez-Trujillo A normalization circuit underlying coding of spatial attention in primate lateral prefrontal cortex Journal Article In: eNeuro, vol. 6, no. 2, pp. 1–23, 2019. @article{Duong2019,Lateral prefrontal cortex (LPFC) neurons signal the allocation of voluntary attention; however, the neural computations underlying this function remain unknown. To investigate this, we recorded from neuronal ensembles in the LPFC of two Macaca fascicularis performing a visuospatial attention task. LPFC neural responses to a single stimulus were normalized when additional stimuli/distracters appeared across the visual field and were wellcharacterized by an averaging computation. Deploying attention toward an individual stimulus surrounded by distracters shifted neural activity from an averaging regime toward a regime similar to that when the attended stimulus was presented in isolation (winner-take-all; WTA). However, attentional modulation is both qualitatively and quantitatively dependent on a neuron's visuospatial tuning. Our results show that during attentive vision, LPFC neuronal ensemble activity can be robustly read out by downstream areas to generate motor commands, and/or fed back into sensory areas to filter out distracter signals in favor of target signals. |
Francesco Fabbrini; Chris Van den Haute; Marina De Vitis; Veerle Baekelandt; Wim Vanduffel; Rufin Vogels Probing the mechanisms of repetition suppression in inferior temporal cortex with optogenetics Journal Article In: Current Biology, vol. 29, no. 12, pp. 1988–1998, 2019. @article{Fabbrini2019,Neurons in macaque inferior temporal (IT) cortex show a decrease in the response with stimulus repetition, known as repetition suppression (RS). Several mechanisms may contribute to RS in IT, such as firing rate-dependent fatigue and transsynaptic mechanisms, like synaptic depression or reduced input from neurons within the same area or from up- or downstream areas. We examined the role of firing rate fatigue and transsynaptic mechanisms by stimulating directly IT neurons using optogenetics and measured the effect of photo-stimulation on their responses using timing parameters that resulted in RS for visual stimuli. Photo-stimulation of IT neurons resulted in a marginally decreased probability of spiking activity to a subsequent photo-stimulation or to a subsequent low-contrast visual stimulus. This response reduction was small relative to that for repeated visual stimuli and was related to post-stimulation inhibition of the activity during the interval between adapter and test stimuli. Presentation of a visual adapter did not change the response to subsequent photo-stimulation. In neurons whose response to the visual adapter was inhibited by simultaneous photo-stimulation, RS to visual stimuli was unaffected. Overall, these data imply that RS in IT has a transsynaptic origin, with little or no contribution of intrinsic firing rate fatigue. In addition, they suggest a limited contribution of both local synaptic depression and reduced input from nearby IT neurons, whose responses were postulated to be decreased by firing rate fatigue, to RS in IT. Using optogenetics, Fabbrini et al. show that repetition suppression in the inferior temporal cortex of macaques does not primarily depend on intrinsic firing rate fatigue: visual responses are largely unaffected by preceding photo-stimulation and alterations of the response to the adapter have minor or no influence on repetition suppression. |
Yang Fang; Ming Chen; Haoran Xu; Peichao Li; Chao Han; Jiaming Hu; Shude Zhu; Heng Ma; Haidong D. Lu An orientation map for disparity-defined edges in area V4 Journal Article In: Cerebral Cortex, vol. 29, no. 2, pp. 666–679, 2019. @article{Fang2019a,Binocular disparity information is an important source of 3D perception. Neurons sensitive to binocular disparity are found in almost all major visual areas in nonhuman primates. In area V4, disparity processes are suggested for the purposes of 3D-shape representation and fine disparity perception. However, whether neurons in V4 are sensitive to disparity-defined edges used in shape representation is not clear. Additionally, a functional organization for disparity edges has not been demonstrated so far. With intrinsic signal optical imaging, we studied functional organization for disparity edges in the monkey visual areas V1, V2, and V4. We found that there is an orientation map in V4 activated by edges purely defined by binocular disparity. This map is consistent with the orientation map obtained with regular luminance-defined edges, indicating a cue-invariant edge representation in this area. In contrast, such a map is much weaker in V2 and totally absent in V1. These findings reveal a hierarchical processing of 3D shape along the ventral pathway and the important role that V4 plays in shape-from-disparity detection. |
Shiva Farashahi; Christopher H. Donahue; Benjamin Y. Hayden; Daeyeol Lee; Alireza Soltani Flexible combination of reward information across primates Journal Article In: Nature Human Behaviour, vol. 3, no. 11, pp. 1215–1224, 2019. @article{Farashahi2019,A fundamental but rarely contested assumption in economics and neuroeconomics is that decision-makers compute subjective values of risky options by multiplying functions of reward probability and magnitude. By contrast, an additive strategy for valuation allows flexible combination of reward information required in uncertain or changing environments. We hypothesized that the level of uncertainty in the reward environment should determine the strategy used for valuation and choice. To test this hypothesis, we examined choice between risky options in humans and rhesus macaques across three tasks with different levels of uncertainty. We found that whereas humans and monkeys adopted a multiplicative strategy under risk when probabilities are known, both species spontaneously adopted an additive strategy under uncertainty when probabilities must be learned. Additionally, the level of volatility influenced relative weighting of certain and uncertain reward information, and this was reflected in the encoding of reward magnitude by neurons in the dorsolateral prefrontal cortex. |
Ian C. Fiebelkorn; Mark A. Pinsk; Sabine Kastner The mediodorsal pulvinar coordinates the macaque fronto-parietal network during rhythmic spatial attention Journal Article In: Nature Communications, vol. 10, pp. 215, 2019. @article{Fiebelkorn2019,Spatial attention is discontinuous, sampling behaviorally relevant locations in theta-rhythmic cycles (3-6 Hz). Underlying this rhythmic sampling are intrinsic theta oscillations in frontal and parietal cortices that provide a clocking mechanism for two alternating attentional states that are associated with either engagement at the presently attended location (and enhanced perceptual sensitivity) or disengagement (and diminished perceptual sensitivity). It has remained unclear, however, how these theta-dependent states are coordinated across the large-scale network that directs spatial attention. The pulvinar is a candidate for such coordination, having been previously shown to regulate cortical activity. Here, we examined pulvino-cortical interactions during theta-rhythmic sampling by simultaneously recording from macaque frontal eye fields (FEF), lateral intraparietal area (LIP), and pulvinar. Neural activity propagated from pulvinar to cortex during periods of engagement, and from cortex to pulvinar during periods of disengagement. A rhythmic reweighting of pulvino-cortical interactions thus defines functional dissociations in the attention network. |
Nico A. Flierman; Alla Ignashchenkova; Mario Negrello; Peter Thier; Chris I. De Zeeuw; Aleksandra Badura Glissades are altered by lesions to the oculomotor vermis but not by saccadic adaptation Journal Article In: Frontiers in Behavioral Neuroscience, vol. 13, pp. 194, 2019. @article{Flierman2019,Saccadic eye movements enable fast and precise scanning of the visual field, which is partially controlled by the posterior cerebellar vermis. Textbook saccades have a straight trajectory and a unimodal velocity profile, and hence have well-defined epochs of start and end. However, in practice only a fraction of saccades matches this description. One way in which a saccade can deviate from its trajectory is the presence of an overshoot or undershoot at the end of a saccadic eye movement just before fixation. This additional movement, known as a glissade, is regarded as a motor command error and was characterized decades ago but was almost never studied. Using rhesus macaques, we investigated the properties of glissades and changes to glissade kinematics following cerebellar lesions. Additionally, in monkeys with an intact cerebellum, we investigated whether the glissade amplitude can be modulated using multiple adaptation paradigms. Our results show that saccade kinematics are altered by the presence of a glissade, and that glissades do not appear to have any adaptive function as they do not bring the eye closer to the target. Quantification of these results establishes a detailed description of glissades. Further, we show that lesions to the posterior cerebellum have a deleterious effect on both saccade and glissade properties, which recovers over time. Finally, the saccadic adaptation experiments reveal that glissades cannot be modulated by this training paradigm. Together our work offers a functional study of glissades and provides new insight into the cerebellar involvement in this type of motor error. |
Maryam Ghahremani; Kevin D. Johnston; Liya Ma; Lauren K. Hayrynen; Stefan Everling Electrical microstimulation evokes saccades in posterior parietal cortex of common marmosets Journal Article In: Journal of Neurophysiology, vol. 122, no. 4, pp. 1765–1776, 2019. @article{Ghahremani2019,The common marmoset (Callithrix jacchus) is a small-bodied New World primate increasing in prominence as a model animal for neuroscience research. The lissencephalic cortex of this primate species provides substantial advantages for the application of electrophysiological techniques such as high-density and laminar recordings, which have the capacity to advance our understanding of local and laminar cortical circuits and their roles in cognitive and motor functions. This is particularly the case with respect to the oculomotor system, as critical cortical areas of this network such as the frontal eye fields (FEF) and lateral intraparietal area (LIP) lie deep within sulci in macaques. Studies of cytoarchitecture and connectivity have established putative homologies between cortical oculomotor fields in marmoset and macaque, but physiological investigations of these areas, particularly in awake marmosets, have yet to be carried out. Here we addressed this gap by probing the function of posterior parietal cortex of the common marmoset with electrical microstimulation. We implanted two animals with 32-channel Utah arrays at the location of the putative area LIP and applied microstimulation while they viewed a video display and made untrained eye movements. Similar to previous studies in macaques, stimulation evoked fixed-vector and goal-directed saccades, staircase saccades, and eyeblinks. These data demonstrate that area LIP of the marmoset plays a role in the regulation of eye movements, provide additional evidence that this area is homologous with that of the macaque, and further establish the marmoset as a valuable model for neurophysiological investigations of oculomotor and cognitive control. |
Seyed Alireza Hassani; Sofia Lendor; Ezel Boyaci; Janusz Pawliszyn; Thilo Womelsdorf Multi-neuromodulator measurements across fronto-striatal network areas of the behaving macaque using solid-phase microextraction Journal Article In: Journal of Neurophysiology, vol. 122, no. 4, pp. 1649–1660, 2019. @article{Hassani2019,Different neuromodulators rarely act independent from each other to modify neural processes but are instead coreleased, gated, or modulated. To understand this interdependence of neuromodulators and their collective influence on local circuits during different brain states, it is necessary to reliably extract local concentrations of multiple neuromodulators in vivo. Here we describe results using solid-phase microextraction (SPME), a method providing sensitive, multineuromodulator measurements. SPME is a sampling method that is coupled with mass spectrometry to quantify collected analytes. Reliable measurements of glutamate, dopamine, acetylcholine, and choline were made simultaneously within frontal cortex and striatum of two macaque monkeys (Macaca mulatta) during goal-directed behavior. We find glutamate concentrations several orders of magnitude higher than acetylcholine and dopamine in all brain regions. Dopamine was reliably detected in the striatum at tenfold higher concentrations than acetylcholine. Acetylcholine and choline concentrations were detected with high consistency across brain areas within monkeys and between monkeys. These findings illustrate that SPME microprobes provide a versatile novel tool to characterize multiple neuromodulators across different brain areas in vivo to understand the interdependence and covariation of neuromodulators during goal-directed behavior. Such data would be important to better distinguish between different behavioral states and characterize dysfunctional brain states that may be evident in psychiatric disorders. |
Simon Hong; Satoko Amemori; Emily Chung; Daniel J. Gibson; Ken-ichi Amemori; Ann M. Graybiel Predominant striatal input to the lateral habenula in macaques comes from striosomes Journal Article In: Current Biology, vol. 29, no. 1, pp. 51–61, 2019. @article{Hong2019,Striosomes, neurochemically specialized modules in the striatum, are thought to be nodes in circuits extending, via basal ganglia pathways, from mood-related neocortical regions to dopamine-containing neurons of the substantia nigra. Yet striosomes have remained beyond the reach of electrophysiological methods to identify them, especially in non-human primates. Such work is needed for translational as well as for basic science. Here we introduce a method to identify striosomes on-line in awake, behaving macaques. We combined electrical microstimulation of the striatum with simultaneous electrophysiological recording in the lateral habenula (LHb) followed by immunohistochemistry. We demonstrate that striosomes provide the predominant striatal input to the macaque pallido-habenular circuit, which is known to function in relation to reinforcement signaling. Further, our experiments suggest that striosomes from different striatal regions may convergently influence the lateral habenula. This work now opens the way to defining the functions of striosomes in behaving primates in relation to mood, motivation, and action. |
Shariq N. Iqbal; Lun Yin; Caroline B. Drucker; Qian Kuang; Jean-François Gariépy; Michael L. Platt; John M. Pearson Latent goal models for dynamic strategic interaction Journal Article In: PLoS Computational Biology, vol. 15, no. 3, pp. e1006895, 2019. @article{Iqbal2019,Understanding the principles by which agents interact with both complex environments and each other is a key goal of decision neuroscience. However, most previous studies have used experimental paradigms in which choices are discrete (and few), play is static, and optimal solutions are known. Yet in natural environments, interactions between agents typically involve continuous action spaces, ongoing dynamics, and no known optimal solution. Here, we seek to bridge this divide by using a "penalty shot" task in which pairs of monkeys competed against each other in a competitive, real-time video game. We modeled monkeys' strategies as driven by stochastically evolving goals, onscreen positions that served as set points for a control model that produced observed joystick movements. We fit this goal-based dynamical system model using approximate Bayesian inference methods, using neural networks to parameterize players' goals as a dynamic mixture of Gaussian components. Our model is conceptually simple, constructed of interpretable components, and capable of generating synthetic data that capture the complexity of real player dynamics. We further characterized players' strategies using the number of change points on each trial. We found that this complexity varied more across sessions than within sessions, and that more complex strategies benefited offensive players but not defensive players. Together, our experimental paradigm and model offer a powerful combination of tools for the study of realistic social dynamics in the laboratory setting. |
Anna Ivic Jasper; Seiji Tanabe; Adam Kohn Predicting perceptual decisions using visual cortical population responses and choice history Journal Article In: Journal of Neuroscience, vol. 39, no. 34, pp. 6714–6727, 2019. @article{Jasper2019,Our understanding ofthe neural basis ofperceptual decision making has been built in part on relating co-fluctuations ofsingle neuron responses to perceptual decisions on a trial-by-trial basis. The strength of this relationship is often compared across neurons or brain areas, recorded in different sessions, animals, or variants ofa task.Wesought to extend our understanding ofperceptual decision making in three ways. First, we measured neuronal activity simultaneously in early [primary visual cortex ( V1)] and midlevel (V4) visual cortex while macaque monkeys performed a fine orientation discrimination perceptual task. This allowed a direct comparison ofchoice signals in these two areas, including their dynamics. Second, we asked how our ability to predict animals' decisions would be improved by considering small simultaneously-recorded neuronal populations rather than individual units. Finally, we asked whether predictions would be improved by taking into account the animals' choice and reward histories, which can strongly influence decision making. We found that responses ofindividual V4 neurons were weakly predictive ofdecisions, but only in a briefepoch between stimulus offset and the indication of choice. In V1, few neurons showed significant decision-related activity. Analysis of neuronal population responses revealed robust choice-related information in V4 and substantially weaker signals in V1. Including choice- and reward-history informa- tion improved performance further, particularly when the recorded populations contained little decision-related information. Our work shows the power ofusing neuronal populations and decision history when relating neuronal responses to the perceptual decisions they are thought to underlie. |
Kevin D. Johnston; Liya Ma; Lauren Schaeffer Alpha oscillations modulate preparatory activity in marmoset area 8Ad Journal Article In: Journal of Neuroscience, vol. 39, no. 10, pp. 855–1866, 2019. @article{Johnston2019,Cognitive control often requires suppression of prepotent stimulus-driven responses in favor of less potent alternatives. Suppression of prepotent saccades has been shown to require proactive inhibition in the frontoparietal saccade network. Electrophysiological evidence in macaque monkeys has revealed neural correlates of such inhibition in this network; however, the interlaminar instantiation of inhibitory processes remains poorly understood because these areas lie deep within sulci in macaques, rendering them inaccessible to laminar recordings. Here, we addressed this gap by exploiting the mostly lissencephalic cortex of the common marmoset (Callithrix jacchus). We inserted linear electrode arrays into areas 8Ad-the putative marmoset frontal eye field-and the lateral intraparietal area of two male marmosets and recorded neural activity during performance of a task comprised of alternating blocks of trials requiring a saccade either toward a large, high-luminance stimulus or the inhibition of this prepotent response in favor of a saccade toward a small, low-luminance stimulus. We observed prominent task-dependent activity in both alpha/gamma bands of the LFP and discharge rates of single neurons in area 8Ad during a prestimulus task epoch in which the animals had been instructed which of these two tasks to perform but before peripheral stimulus onset. These data are consistent with a model in which rhythmic alpha-band activity in deeper layers inhibits spiking in upper layers to support proactive inhibitory saccade control. |
Kohitij Kar; Jonas Kubilius; Kailyn Schmidt; Elias B. Issa; James J. DiCarlo Evidence that recurrent circuits are critical to the ventral stream's execution of core object recognition behavior Journal Article In: Nature Neuroscience, vol. 22, pp. 974–983, 2019. @article{Kar2019,Non-recurrent deep convolutional neural networks (CNNs) are currently the best at modeling core object recognition, a behavior that is supported by the densely recurrent primate ventral stream, culminating in the inferior temporal (IT) cortex. If recurrence is critical to this behavior, then primates should outperform feedforward-only deep CNNs for images that require additional recurrent processing beyond the feedforward IT response. Here we first used behavioral methods to discover hundreds of these ‘challenge' images. Second, using large-scale electrophysiology, we observed that behaviorally sufficient object identity solutions emerged ~30 ms later in the IT cortex for challenge images compared with primate performance-matched ‘control' images. Third, these behaviorally critical late-phase IT response patterns were poorly predicted by feedforward deep CNN activations. Notably, very-deep CNNs and shallower recurrent CNNs better predicted these late IT responses, suggesting that there is a functional equivalence between additional nonlinear transformations and recurrence. Beyond arguing that recurrent circuits are critical for rapid object identification, our results provide strong constraints for future recurrent model development. |
Sanjeev B. Khanna; Adam C. Snyder; Matthew A. Smith Distinct sources of variability affect eye movement preparation Journal Article In: Journal of Neuroscience, vol. 39, no. 23, pp. 4511–4526, 2019. @article{Khanna2019,The sequence of events leading to an eye movement to a target begins the moment visual information has reached the brain, well in advance of the eye movement itself. The process by which visual information is encoded and used to generate a motor plan has been the focus of substantial interest partly because of the rapid and reproducible nature of saccadic eye movements, and the key role that they play in primate behavior. Signals related to eye movements are present in much of the primate brain, yet most neurophysiological studies of the transition from vision to eye movements have measured the activity of one neuron at a time. Less is known about how the coordinated action of populations of neurons contribute to the initiation of eye movements. One cortical area of particular interest in this process is the frontal eye fields, a region of prefrontal cortex that has descending projections to oculomotor control centers. We recorded from populations of frontal eye field neurons in macaque monkeys engaged in a memory-guided saccade task. We found a variety of neurons with visually evoked responses, saccade-aligned responses, and mixtures of both. We took advantage of the simultaneous nature of the recordings to measure variability in individual neurons and pairs of neurons from trial-to-trial, as well as the moment-to-moment population activity structure.Wefound that these measures were related to saccadic reaction times, suggesting that the population-level organization of frontal eye field activity is important for the transition from perception to movement. |
Seolmin Kim; Jeongjun Park; Joonyeol Lee Effect of prior direction expectation on the accuracy and precision of smooth pursuit eye movements Journal Article In: Frontiers in Systems Neuroscience, vol. 13, pp. 71, 2019. @article{Kim2019d,The integration of sensory with top–down cognitive signals for generating appropriate sensory–motor behaviors is an important issue in understanding the brain's information processes. Recent studies have demonstrated that the interplay between sensory and high-level signals in oculomotor behavior could be explained by Bayesian inference. Specifically, prior knowledge for motion speed introduces a bias in the speed of smooth pursuit eye movements. The other important prediction of Bayesian inference is variability reduction by prior expectation; however, there is insufficient evidence in oculomotor behaviors to support this prediction. In the present study, we trained monkeys to switch the prior expectation about motion direction and independently controlled the strength of the motion stimulus. Under identical sensory stimulus conditions, we tested if prior knowledge about the motion direction reduced the variability of open-loop smooth pursuit eye movements. We observed a significant reduction when the prior expectation was strong; this was consistent with the prediction of Bayesian inference. Taking advantage of the open-loop smooth pursuit, we investigated the temporal dynamics of the effect of the prior to the pursuit direction bias and variability. This analysis demonstrated that the strength of the sensory evidence depended not only on the strength of the sensory stimulus but also on the time required for the pursuit system to form a neural sensory representation. Finally, we demonstrated that the variability and directional bias change by prior knowledge were quantitatively explained by the Bayesian observer model. |
Taekjun Kim; Wyeth Bair; Anitha Pasupathy Neural coding for shape and texture in macaque area V4 Journal Article In: Journal of Neuroscience, vol. 39, no. 24, pp. 4760–4774, 2019. @article{Kim2019e,The distinct visual sensations of shape and texture have been studied separately in cortex; therefore, it remains unknown whether separate neuronal populations encode each of these properties or one population carries a joint encoding. We directly compared shape and texture selectivity of individual V4 neurons in awake macaques (1 male, 1 female) and found that V4 neurons lie along a continuum from strong tuning for boundary curvature of shapes to strong tuning for perceptual dimensions of texture. Among neurons tuned to both attributes, tuning for shape and texture were largely separable, with the latter delayed by ~30 ms. We also found that shape stimuli typically evoked stronger, more selective responses than did texture patches, regardless of whether the latter were contained within or extended beyond the receptive field. These results suggest that there are separate specializations in mid-level cortical processing for visual attributes of shape and texture. |
Satwant Kumar; Ivo D. Popivanov; Rufin Vogels Transformation of visual representations across ventral stream body-selective patches Journal Article In: Cerebral Cortex, vol. 29, no. 1, pp. 215–229, 2019. @article{Kumar2019a,Although the neural processing of visual images of bodies is critical for survival, it is much less well understood than face processing. Functional imaging studies demonstrated body selective regions in primate inferior temporal cortex. To advance our understanding of how the visual brain represents bodies, we compared the representation of animate and inanimate objects in two such body patches with fMRI-guided single unit recordings in rhesus monkeys. We found that the middle Superior Temporal Sulcus body patch (MSB) distinguishes to a greater extent bodies from non-bodies than the anterior Superior Temporal Sulcus body patch (ASB). Importantly, ASB carried more viewpoint-tolerant information about body posture and body identity than MSB, while MSB showed greater orientation selectivity. Combined with previous work on faces, this suggests that an increase in view-tolerant representations, coupled with a refined individuation, along the visual hierarchy is a general property of information processing within the inferior temporal cortex. |
Satwant Kumar; Rufin Vogels Body patches in inferior temporal cortex encode categories with different temporal dynamics Journal Article In: Journal of Cognitive Neuroscience, vol. 31, no. 11, pp. 1699–1709, 2019. @article{Kumar2019,An unresolved question in cognitive neuroscience is how representations of object categories at different levels (basic and superordinate) develop during the course of the neural response within an area. To address this, we decoded categories of different levels from the spiking responses of populations of neurons recorded in two fMRI-defined body patches in the macaque STS. Recordings of the two patches were made in thesameanimals with thesamestimuli. Support vector machine classifiers were trained at brief response epochs and tested at the same or different epochs, thus assessing whether category representations change during the course of the response. In agreement with hierarchical processing within the body patch network, the posterior body patch mid STS body (MSB) showed an earlier onset of categorization compared with the anterior body patch anterior STS body (ASB), irrespective of the categorization level. Decoding of the superordinate body versus nonbody categories was less dynamic in MSB than in ASB, with ASB showing a biphasic temporal pattern. Decoding of the ordinate-level category human versus monkey bodies showed similar temporal patterns in both patches. The decoding onset of superordinate categorizations involving bodies was as early as for basic-level categorization, suggesting that previously reported differences between the onset of basic and superordinate categorizations may depend on the area. The qualitative difference between areas in their dynamics of category representation may hinder the interpretation of decoding dynamics based on EEG or MEG, methods that may mix signals of different areas. |
Noga Larry; Merav Yarkoni; Adi Lixenberg; Mati Joshua Cerebellar climbing fibers encode expected reward size Journal Article In: eLife, vol. 8, pp. 1–16, 2019. @article{Larry2019,Climbing fiber inputs to the cerebellum encode error signals that instruct learning. Recently, evidence has accumulated to suggest that the cerebellum is also involved in the processing of reward. To study how rewarding events are encoded, we recorded the activity of climbing fibers when monkeys were engaged in an eye movement task. At the beginning of each trial, the monkeys were cued to the size of the reward that would be delivered upon successful completion of the trial. Climbing fiber activity increased when the monkeys were presented with a cue indicating a large reward size. Reward size did not modulate activity at reward delivery or during eye movements. Comparison between climbing fiber and simple spike activity indicated different interactions for coding of movement and reward. These results indicate that climbing fibers encode the expected reward size and suggest a general role of the cerebellum in associative learning beyond error correction. |
Yin S. Li; Matthew R. Nassar; Joseph W. Kable; Joshua I. Gold Individual neurons in the cingulate cortex encode action monitoring, not selection, during adaptive decision-making Journal Article In: Journal of Neuroscience, vol. 39, no. 34, pp. 6668–6683, 2019. @article{Li2019g,The cingulate cortex contributes to complex, adaptive behaviors, but the exact nature of its contributions remains unresolved. Proposals from previous studies, including evaluating past actions or selecting future ones, have been difficult to distinguish in part because of an incomplete understanding of the task-relevant variables that are encoded by individual cingulate neurons. In this study, we recorded from individual neurons in parts ofboth the anterior cingulate cortex (ACC) and posterior cingulate cortex (PCC) in 2 male rhesus monkeys performing a saccadic reward task. The task required them to use adaptive, feedback-driven strategies to infer the spatial location ofa rewarded saccade target in the presence ofdifferent forms ofuncertainty. We found that task-relevant, spatially selective feedback signals were encoded by the activity of individual neurons in both brain regions, with stronger selectivity for spatial choice and reward-target signals in PCC and stronger selectivity for feedback in ACC. Moreover, neurons in both regions were sensitive to sequential effects of feedback that partly reflected sequential behavioral patterns. However, neither brain region exhibited systematic modulations by the blockwise conditions that governed the reliability of the trial-by-trial feedback and drove adaptive behavioral patterns. There was also little evidence that single-neuron responses in either brain region directly predicted the extent to which feedback and contextual information were used to inform choices on the subsequent trial. Thus, certain cingulate neurons encode diverse, evaluative signals needed for adaptive, feedback-driven decision-making, but those signals may be integrated elsewhere in the brain to guide actions. |
Zhihan Li; An Yan; Kun Guo; Wu Li Fear-related signals in the primary visual cortex Journal Article In: Current Biology, vol. 29, no. 23, pp. 4078–4083, 2019. @article{Li2019h,Neuronal responses in the primary visual cortex (V1) are driven by simple stimuli, but these stimulus- evoked responses can be markedly modulated by non-sensory factors, such as attention and reward [1], and shaped by perceptual training [2]. In real-life situations, neutral visual stimuli can become emotionally tagged by experience, resulting in altered perceptual abilities to detect and discriminate these stimuli [3–5]. Human imaging [4] and electroencephalography (EEG) studies [6–9] have shown that visual fear learning (the acquisition of aversive emotion associated with a visual stimulus) affects the activities in visual cortical areas as early as in V1. However, it remains elusive as to whether the fear-related activities seen in the early visual cortex have to do with feedback influences from other cortical areas; it is also unclear whether and how the response properties of V1 cells are modified during the fear learning. In the current study, we addressed these issues by recording from V1 of awake monkeys implanted with an array of microelectrodes. We found that responses of V1 neurons were rapidly modified when a given orientation of grating stimulus was repeatedly associated with an aversive stimulus. The output visual signals from V1 cells conveyed, from their response outset, fear-related signals that were specific to the fear-associated grating orientation and visual-field location. The specific fear signals were independent of neurons' orientation preferences and were present even though the fear-associated stimuli were rendered invisible. Our findings suggest a bottom-up mechanism that allows for proactive labeling of visual inputs that are predictive of imminent danger. |
Junxiang Luo; Keyan He; Ian Max Andolina; Xiaohong Li; Jiapeng Yin; Zheyuan Chen; Yong Gu; Wei Wang Going with the flow: The neural mechanisms underlying illusions of complex-flow motion Journal Article In: Journal of Neuroscience, vol. 39, no. 14, pp. 2664 –2685, 2019. @article{Luo2019,Studying the mismatch between perception and reality helps us better understand the constructive nature of the visual brain. The Pinna-Brelstaff motion illusion is a compelling example illustrating how a complex moving pattern can generate an illusory motion perception. When an observer moves toward (expansion) or away (contraction) from the Pinna-Brelstaff figure, the figure appears to rotate. The neural mechanisms underlying the illusory complex-flow motion of rotation, expansion, and contraction remain unknown. We studied this question at both perceptual and neuronal levels in behaving male macaques by using carefully parametrized Pinna-Brelstaff figures that induce the above motion illusions. We first demonstrate that macaques perceive illusory motion in a manner similar to that of human observers. Neurophysiological recordings were subsequently performed in the middle temporal area (MT) and the dorsal portion of the medial superior temporal area (MSTd). We find that subgroups of MSTd neurons encoding a particular global pattern of real complex-flow motion (rotation, expansion, contraction) also represent illusory motion patterns of the same class. They require an extra 15 ms to reliably discriminate the illusion. In contrast, MT neurons encode both real and illusory local motions with similar temporal delays. These findings reveal that illusory complex-flow motion is first represented in MSTd by the same neurons that normally encode real complex-flow motion. However, the extraction of global illusory motion in MSTd from other classes of real complex-flow motion requires extra processing time. Our study illustrates a cascaded integration mechanism from MT to MSTd underlying the transformation from external physical to internal nonveridical flow-motion perception. |
Liya Ma; Jason L. Chan; Kevin D. Johnston; Stephen G. Lomber; Stefan Everling Macaque anterior cingulate cortex deactivation impairs performance and alters lateral prefrontal oscillatory activities in a rule-switching task Journal Article In: PLoS Biology, vol. 17, no. 7, pp. e3000045, 2019. @article{Ma2019b,In primates, both the dorsal anterior cingulate cortex (dACC) and the dorsolateral prefrontal cortex (dlPFC) are key regions of the frontoparietal cognitive control network. To study the role of the dACC and its communication with the dlPFC in cognitive control, we recorded local field potentials (LFPs) from the dlPFC before and during the reversible deactivation of the dACC, in macaque monkeys engaging in uncued switches between 2 stimulus-response rules, namely prosaccade and antisaccade. Cryogenic dACC deactivation impaired response accuracy during maintenance of—but not the initial switching to—the cognitively demanding antisaccade rule, which coincided with a reduction in task-related theta activity and the correct-error (C-E) difference in dlPFC beta-band power. During both rule switching and maintenance, dACC deactivation prolonged the animals' reaction time and reduced task-related alpha power in the dlPFC. Our findings support a role of the dACC in prefrontal oscillatory activities that are involved the maintenance of a new, challenging task rule. |
Corentin Massot; Uday K. Jagadisan; Neeraj J. Gandhi In: Communications Biology, vol. 2, pp. 1–14, 2019. @article{Massot2019,The superior colliculus (SC) is an excellent substrate to study sensorimotor transformations. To date, the spatial and temporal properties of population activity along its dorsoventral axis have been inferred from single electrode studies. Here, we recorded SC population activity in non-human primates using a linear multi-contact array during delayed saccade tasks. We show that during the visual epoch, information appeared first in dorsal layers and systematically later in ventral layers. During the delay period, the laminar organization of low-spiking rate activity matched that of the visual epoch. During the pre-saccadic epoch, spiking activity emerged first in a more ventral layer, ~ 100 ms before saccade onset. This buildup of activity appeared later on nearby neurons situated both dorsally and ventrally, culminating in a synchronous burst across the dorsoventral axis, ~ 28 ms before saccade onset. Collectively, these results reveal a principled spatiotemporal organization of SC population activity underlying sensorimotor transformation for the control of gaze. |
Vincent B. McGinty Overt attention toward appetitive cues enhances their subjective value, independent of orbitofrontal cortex activity Journal Article In: eNeuro, vol. 6, no. 6, pp. 1–19, 2019. @article{McGinty2019,Neural representations of value underlie many behaviors that are crucial for survival. Previously, we found that value representations in primate orbitofrontal cortex (OFC) are modulated by attention, specifically, by overt shifts of gaze toward or away from reward-associated visual cues (McGinty et al., 2016). Here, we investigate the influence of overt attention on behavior by asking how gaze shifts correlate with reward anticipatory responses and whether activity in OFC mediates this correlation. Macaque monkeys viewed pavlovian conditioned appetitive cues on a visual display, while the fraction of time they spent looking toward or away from the cues was measured using an eye tracker. Also measured during cue presentation were the reward anticipation, indicated by conditioned licking responses (CRs), and single-neuron activity in OFC. In general, gaze allocation predicted subsequent licking responses: the longer the monkeys spent looking at a cue at a given time point in a trial, the more likely they were to produce an anticipatory CR later in that trial, as if the subjective value of the cue were increased. To address neural mechanisms, mediation analysis measured the extent to which the gaze–CR correlation could be statistically explained by the concurrently recorded firing of OFC neurons. The resulting mediation effects were indistinguishable from chance. Therefore, while overt attention may increase the subjective value of reward-associated cues (as revealed by anticipatory behaviors), the underlying mechanism remains unknown, as does the functional significance of gaze-driven modulation of OFC value signals. |
Priyanka S. Mehta; Jiaxin Cindy Tu; Giuliana A. LoConte; Meghan C. Pesce; Benjamin Y. Hayden Ventromedial prefrontal cortex tracks multiple environmental variables during search Journal Article In: Journal of Neuroscience, vol. 39, no. 27, pp. 5336–5350, 2019. @article{Mehta2019,To make efficient foraging decisions, we must combine information about the values of available options with nonvalue information. Some accounts of ventromedial PFC (vmPFC) suggest that it has a narrow role limited to evaluating immediately available options. We examined responses of neurons in area 14 (a putative macaque homolog of human vmPFC) as 2 male macaques performed a novel foraging search task. Although many neurons encoded the values of immediately available offers, they also independently encoded several other variables that influence choice, but that are conceptually distinct from offer value. These variables include average reward rate, number of offers viewed per trial, previous offer values, previous outcome sizes, and the locations of the currently attended offer.We conclude that, rather than serving as specialized economic value center, vmPFC plays a broad role in integrating relevant environmental information to drive foraging decisions. |
Adam P. Morris; Bart Krekelberg A stable visual world in primate primary visual cortex Journal Article In: Current Biology, vol. 29, no. 9, pp. 1471–1480, 2019. @article{Morris2019,Humans and other primates rely on eye movements to explore visual scenes and to track moving objects. As a result, the image that is projected onto the retina—and propagated throughout the visual cortical hierarchy—is almost constantly changing and makes little sense without taking into account the momentary direction of gaze. How is this achieved in the visual system? Here, we show that in primary visual cortex (V1), the earliest stage of cortical vision, neural representations carry an embedded “eye tracker” that signals the direction of gaze associated with each image. Using chronically implanted multi-electrode arrays, we recorded the activity of neurons in area V1 of macaque monkeys during tasks requiring fast (exploratory) and slow (pursuit) eye movements. Neurons were stimulated with flickering, full-field luminance noise at all times. As in previous studies, we observed neurons that were sensitive to gaze direction during fixation, despite comparable stimulation of their receptive fields. We trained a decoder to translate neural activity into metric estimates of gaze direction. This decoded signal tracked the eye accurately not only during fixation but also during fast and slow eye movements. After a fast eye movement, the eye-position signal arrived in V1 at approximately the same time at which the new visual information arrived from the retina. Using simulations, we show that this V1 eye-position signal could be used to take into account the sensory consequences of eye movements and map the fleeting positions of objects on the retina onto their stable position in the world. Visual input arrives as a series of snapshots, each taken from a different line of sight, due to eye movements from one part of a scene to another. How do we nevertheless see a stable visual world? Morris and Krekelberg show that in primary visual cortex, the neural representation of each snapshot includes “metadata” that tracks gaze direction. |
Aidan P. Murphy; David A. Leopold A parameterized digital 3D model of the Rhesus macaque face for investigating the visual processing of social cues Journal Article In: Journal of Neuroscience Methods, vol. 324, pp. 1–14, 2019. @article{Murphy2019,Background: Rhesus macaques are the most popular model species for studying the neural basis of visual face processing and social interaction using intracranial methods. However, the challenge of creating realistic, dynamic, and parametric macaque face stimuli has limited the experimental control and ethological validity of existing approaches. New method: We performed statistical analyses of in vivo computed tomography data to generate an anatomically accurate, three-dimensional representation of Rhesus macaque cranio-facial morphology. The surface structures were further edited, rigged and textured by a professional digital artist with careful reference to photographs of macaque facial expression, colouration and pelage. Results: The model offers precise, continuous, parametric control of craniofacial shape, emotional expression, head orientation, eye gaze direction, and many other parameters that can be adjusted to render either static or dynamic high-resolution faces. Example single-unit responses to such stimuli in macaque inferotemporal cortex demonstrate the value of parametric control over facial appearance and behaviours. Comparison with existing method(s): The generation of such a high-dimensionality and systematically controlled stimulus set of conspecific faces, with accurate craniofacial modelling and professional finalization of facial details, is currently not achievable using existing methods. Conclusions: The results herald a new set of possibilities in adaptive sampling of a high-dimensional and socially meaningful feature space, thus opening the door to systematic testing of hypotheses about the abundant neural specialization for faces found in the primate. |
Sunny Nigam; Sorin Pojoga; Valentin Dragoi Synergistic coding of visual information in columnar networks Journal Article In: Neuron, vol. 104, no. 2, pp. 402–411.e4, 2019. @article{Nigam2019,Incoming stimuli are encoded collectively by populations of cortical neurons, which transmit information by using a neural code thought to be predominantly redundant. Redundant coding is widely believed to reflect a design choice whereby neurons with overlapping receptive fields sample environmental stimuli to convey similar information. Here, we performed multi-electrode laminar recordings in awake monkey V1 to report significant synergistic interactions between nearby neurons within a cortical column. These interactions are clustered non-randomly across cortical layers to form synergy and redundancy hubs. Homogeneous sub-populations comprising synergy hubs decode stimulus information significantly better compared to redundancy hubs or heterogeneous sub-populations. Mechanistically, synergistic interactions emerge from the stimulus dependence of correlated activity between neurons. Our findings suggest a refinement of the prevailing ideas regarding coding schemes in sensory cortex: columnar populations can efficiently encode information due to synergistic interactions even when receptive fields overlap and shared noise between cells is high. |
Kaiser Niknam; Amir Akbarian; Kelsey Clark; Yasin Zamani; Behrad Noudoost; Neda Nategh Characterizing and dissociating multiple time-varying modulatory computations influencing neuronal activity Journal Article In: PLoS Computational Biology, vol. 15, no. 9, pp. e1007275, 2019. @article{Niknam2019,In many brain areas, sensory responses are heavily modulated by factors including attentional state, context, reward history, motor preparation, learned associations, and other cognitive variables. Modelling the effect of these modulatory factors on sensory responses has proven challenging, mostly due to the time-varying and nonlinear nature of the underlying computations. Here we present a computational model capable of capturing and dissociating multiple time-varying modulatory effects on neuronal responses on the order of milliseconds. The model's performance is tested on extrastriate perisaccadic visual responses in nonhuman primates. Visual neurons respond to stimuli presented around the time of saccades differently than during fixation. These perisaccadic changes include sensitivity to the stimuli presented at locations outside the neuron's receptive field, which suggests a contribution of multiple sources to perisaccadic response generation. Current computational approaches cannot quantitatively characterize the contribution of each modulatory source in response generation, mainly due to the very short timescale on which the saccade takes place. In this study, we use a high spatiotemporal resolution experimental paradigm along with a novel extension of the generalized linear model framework (GLM), termed the sparse-variable GLM, to allow for time-varying model parameters representing the temporal evolution of the system with a resolution on the order of milliseconds. We used this model framework to precisely map the temporal evolution of the spatiotemporal receptive field of visual neurons in the middle temporal area during the execution of a saccade. Moreover, an extended model based on a factorization of the sparse-variable GLM allowed us to disassociate and quantify the contribution of individual sources to the perisaccadic response. Our results show that our novel framework can precisely capture the changes in sensitivity of neurons around the time of saccades, and provide a general framework to quantitatively track the role of multiple modulatory sources over time. |
Mariann Oemisch; Stephanie Westendorff; Marzyeh Azimi; Seyed Alireza Hassani; Salva Ardid; Paul Tiesinga; Thilo Womelsdorf Feature-specific prediction errors and surprise across macaque fronto-striatal circuits Journal Article In: Nature Communications, vol. 10, pp. 176, 2019. @article{Oemisch2019,To adjust expectations efficiently, prediction errors need to be associated with the precise features that gave rise to the unexpected outcome, but this credit assignment may be problematic if stimuli differ on multiple dimensions and it is ambiguous which feature dimension caused the outcome. Here, we report a potential solution: neurons in four recorded areas of the anterior fronto-striatal networks encode prediction errors that are specific to feature values of different dimensions of attended multidimensional stimuli. The most ubiquitous prediction error occurred for the reward-relevant dimension. Feature-specific prediction error signals a) emerge on average shortly after non-specific prediction error signals, b) arise earliest in the anterior cingulate cortex and later in dorsolateral prefrontal cortex, caudate and ventral striatum, and c) contribute to feature-based stimulus selection after learning. Thus, a widely-distributed feature-specific eligibility trace may be used to update synaptic weights for improved feature-based attention. |
Davide Paoletti; Christoph Braun; Elisabeth Julie Vargo; Wieske Zoest Spontaneous pre-stimulus oscillatory activity shapes the way we look: A concurrent imaging and eye-movement study Journal Article In: European Journal of Neuroscience, vol. 49, pp. 137–149, 2019. @article{Paoletti2019,Previous behavioural studies have accrued evidence that response time plays a critical role in determining whether selection is influenced by stimulus saliency or target template. In the present work, we investigated to what extent the variations in timing and consequent oculomotor controls are influenced by spontaneous variations in pre-stimulus alpha oscillations. We recorded simultaneously brain activity using magnetoencephalography (MEG) and eye movements while participants performed a visual search task. Our results show that slower saccadic reaction times were predicted by an overall stronger alpha power in the 500 ms time window preceding the stimulus onset, while weaker alpha power was a signature of faster responses. When looking separately at performance for fast and slow responses, we found evidence for two specific sources of alpha activity predicting correct versus incorrect responses. When saccades were quickly elicited, errors were predicted by stronger alpha activity in posterior areas, comprising the angular gyrus in the temporal-parietal junction (TPJ) and possibly the lateral intraparietal area (LIP). Instead, when participants were slower in responding, an increase of alpha power in frontal eye fields (FEF), supplementary eye fields (SEF) and dorsolateral pre-frontal cortex (DLPFC) predicted erroneous saccades. In other words, oculomotor accuracy in fast responses was predicted by alpha power differences in more posterior areas, while the accuracy in slow responses was predicted by alpha power differences in frontal areas, in line with the idea that these areas may be differentially related to stimulus-driven and goal-driven control of selection. |
Michael A. Paradiso; Seth Akers-Campbell; Octavio Ruiz; James E. Niemeyer; Stuart Geman; Jackson Loper Transsacadic information and corollary discharge in local field potentials of macaque V1 Journal Article In: Frontiers in Integrative Neuroscience, vol. 12, pp. 63, 2019. @article{Paradiso2019,Approximately three times per second, human visual perception is interrupted by a saccadic eye movement. In addition to taking the eyes to a new location, several lines of evidence suggest that the saccades play multiple roles in visual perception. Indeed, it may be crucial that visual processing is informed about movements of the eyes in order to analyze visual input distinctly and efficiently on each fixation and preserve stable visual perception of the world across saccades. A variety of studies has demonstrated that activity in multiple brain areas is modulated by saccades. The hypothesis tested here is that these signals carry significant information that could be used in visual processing. To test this hypothesis, local field potentials (LFPs) were simultaneously recorded from multiple electrodes in macaque primary visual cortex (V1); support vector machines (SVMs) were used to classify the peri-saccadic LFPs. We find that LFPs in area V1 carry information that can be used to distinguish neural activity associated with fixations from saccades, precisely estimate the onset time of fixations, and reliably infer the directions of saccades. This information may be used by the brain in processes including visual stability, saccadic suppression, receptive field (RF) remapping, fixation amplification, and trans-saccadic visual perception. |
Aishwarya Parthasarathy; Cheng Tang; Roger Herikstad; Loong Fah Cheong; Shih-Cheng Yen; Camilo Libedinsky Time-invariant working memory representations in the presence of code-morphing in the lateral prefrontal cortex Journal Article In: Nature Communications, vol. 10, pp. 4995, 2019. @article{Parthasarathy2019,Maintenance of working memory is thought to involve the activity of prefrontal neuronal populations with strong recurrent connections. However, it was recently shown that distractors evoke a morphing of the prefrontal population code, even when memories are maintained throughout the delay. How can a morphing code maintain time-invariant memory information? We hypothesized that dynamic prefrontal activity contains time-invariant memory information within a subspace of neural activity. Using an optimization algorithm, we found a low-dimensional subspace that contains time-invariant memory information. This information was reduced in trials where the animals made errors in the task, and was also found in periods of the trial not used to find the subspace. A bump attractor model replicated these properties, and provided predictions that were confirmed in the neural data. Our results suggest that the high-dimensional responses of prefrontal cortex contain subspaces where different types of information can be simultaneously encoded with minimal interference. |
Alina Peter; Cem Uran; Johanna Klon-Lipok; Rasmus Roese; Sylvia Stijn; William Barnes; Jarrod R. Dowdall; Wolf Singer; Pascal Fries; Martin Vinck Surface color and predictability determine contextual modulation of V1 firing and gamma oscillations Journal Article In: eLife, vol. 8, pp. 1–38, 2019. @article{Peter2019,The integration of direct bottom-up inputs with contextual information is a core feature of neocortical circuits. In area V1, neurons may reduce their firing rates when their receptive field input can be predicted by spatial context. Gamma-synchronized (30–80 Hz) firing may provide a complementary signal to rates, reflecting stronger synchronization between neuronal populations receiving mutually predictable inputs. We show that large uniform surfaces, which have high spatial predictability, strongly suppressed firing yet induced prominent gamma synchronization in macaque V1, particularly when they were colored. Yet, chromatic mismatches between center and surround, breaking predictability, strongly reduced gamma synchronization while increasing firing rates. Differences between responses to different colors, including strong gamma-responses to red, arose from stimulus adaptation to a full-screen background, suggesting prominent differences in adaptation between M- and L-cone signaling pathways. Thus, synchrony signaled whether RF inputs were predicted from spatial context, while firing rates increased when stimuli were unpredicted from context. |
Dina V. Popovkina; Wyeth Bair; Anitha Pasupathy Modeling diverse responses to filled and outline shapes in macaque V4 Journal Article In: Journal of Neurophysiology, vol. 121, no. 3, pp. 1059–1077, 2019. @article{Popovkina2019,Visual area V4 is an important midlevel cortical processing stage that subserves object recognition in primates. Studies investigating shape coding in V4 have largely probed neuronal responses with filled shapes, i.e., shapes defined by both a boundary and an interior fill. As a result, we do not know whether form-selective V4 responses are dictated by boundary features alone or if interior fill is also important. We studied 43 V4 neurons in two male macaque monkeys ( Macaca mulatta) with a set of 362 filled shapes and their corresponding outlines to determine how interior fill modulates neuronal responses in shape-selective neurons. Only a minority of neurons exhibited similar response strength and shape preferences for filled and outline stimuli. A majority responded preferentially to one stimulus category (either filled or outline shapes) and poorly to the other. Our findings are inconsistent with predictions of the hierarchical-max (HMax) V4 model that builds form selectivity from oriented boundary features and takes little account of attributes related to object surface, such as the phase of the boundary edge. We modified the V4 HMax model to include sensitivity to interior fill by either removing phase-pooling or introducing unoriented units at the V1 level; both modifications better explained our data without increasing the number of free parameters. Overall, our results suggest that boundary orientation and interior surface information are both maintained until at least the midlevel visual representation, consistent with the idea that object fill is important for recognition and perception in natural vision. |
Romain Quentin; Jean Rémi King; Etienne Sallard; Nathan Fishman; Ryan Thompson; Ethan R. Buch; Leonardo G. Cohen Differential brain mechanisms of selection and maintenance of information during working memory Journal Article In: Journal of Neuroscience, vol. 39, no. 19, pp. 3728–3740, 2019. @article{Quentin2019,Working memory is our ability to select and temporarily hold information as needed for complex cognitive operations. The temporal dynamics of sustained and transient neural activity supporting the selection and holding of memory content is not known. To address this problem, we recorded magnetoencephalography in healthy participants performing a retro-cue working memory task in which the selection rule and the memory content varied independently. Multivariate decoding and source analyses showed that selecting the memory content relies on prefrontal and parieto-occipital persistent oscillatory neural activity. By contrast, the memory content was reactivated in a distributed occipitotemporal posterior network, preceding the working memory decision and in a different format than during the visual encoding. These results identify a neural signature of content selection and characterize differentiated spatiotemporal constraints for subprocesses of working memory. |
Rishi Rajalingham; James J. DiCarlo Reversible inactivation of different millimeter-scale regions of primate IT results in rifferent patterns of core object recognition deficits Journal Article In: Neuron, vol. 102, no. 2, pp. 493–505.e5, 2019. @article{Rajalingham2019,Rajalingham and DiCarlo show that inactivating millimeter-scale IT subregions results in selective object recognition deficits, providing direct evidence for a causal role of IT in this behavior. Inactivating different subregions resulted in different deficit patterns, revealing an underlying topographical organization. |
Douglas A. Ruff; Marlene R. Cohen Simultaneous multi-area recordings suggest that attention improves performance by reshaping stimulus representations Journal Article In: Nature Neuroscience, vol. 22, pp. 1669–1676, 2019. @article{Ruff2019,Visual attention dramatically improves individuals' ability to see and modulates the responses of neurons in every known visual and oculomotor area, but whether such modulations can account for perceptual improvements is unclear. We measured the relationship between populations of visual neurons, oculomotor neurons and behavior during detection and discrimination tasks. We found that neither of the two prominent hypothesized neuronal mechanisms underlying attention (which concern changes in information coding and the way sensory information is read out) provide a satisfying account of the observed behavioral improvements. Instead, our results are more consistent with the hypothesis that attention reshapes the representation of attended stimuli to more effectively influence behavior. Our results suggest a path toward understanding the neural underpinnings of perception and cognition in health and disease by analyzing neuronal responses in ways that are constrained by behavior and interactions between brain areas. |
Amirsaman Sajad; David C. Godlove; Jeffrey D. Schall Cortical microcircuitry of performance monitoring Journal Article In: Nature Neuroscience, vol. 22, pp. 265–274, 2019. @article{Sajad2019,The medial frontal cortex enables performance monitoring, indexed by the error-related negativity (ERN) and manifested by performance adaptations. We recorded electroencephalogram over and neural spiking across all layers of the supplementary eye field, an agranular cortical area, in monkeys performing a saccade-countermanding (stop signal) task. Neurons signaling error production, feedback predicting reward gain or loss, and delivery of fluid reward had different spike widths and were concentrated differently across layers. Neurons signaling error or loss of reward were more common in layers 2 and 3 (L2/3), whereas neurons signaling gain of reward were more common in layers 5 and 6 (L5/6). Variation of error– and reinforcement-related spike rates in L2/3 but not L5/6 predicted response time adaptation. Variation in error-related spike rate in L2/3 but not L5/6 predicted ERN magnitude. These findings reveal novel features of cortical microcircuitry supporting performance monitoring and confirm one cortical source of the ERN. |
Jason M. Samonds; Veronica Choi; Nicholas J. Priebe Mice discriminate stereoscopic surfaces without fixating in depth Journal Article In: Journal of Neuroscience, vol. 39, no. 41, pp. 8024–8037, 2019. @article{Samonds2019,Stereopsis is aubiquitous feature ofprimatemammalianvision, but little is knownabout ifandhowrodentssuchasmiceuse stereoscopic vision. We used random dot stereograms to test for stereopsis in male and female mice, and they were able to discriminate near from far surfaces over a range of disparities, with diminishing performance for small and large binocular disparities. Based on two-photon measurements of disparity tuning, the range of disparities represented in the visual cortex aligns with the behavior and covers a broad range ofdisparities. Whenwe examined their binocular eye movements, we found that, unlike primates, mice did not systematically vary relative eye positions or use vergence eye movements when presented with different disparities. Nonetheless, the representation of disparity tuning was wide enough to capture stereoscopic information over a range of potential vergence angles. Although mice share fundamental characteristics of stereoscopic vision with primates and carnivores, their lack ofdisparity-dependent vergence eye move- ments and wide neuronal representation suggests that they may use a distinct strategy for stereopsis. |
Morteza Sarafyazd; Mehrdad Jazayeri Hierarchical reasoning by neural circuits in the frontal cortex Journal Article In: Science, vol. 364, pp. 1–11, 2019. @article{Sarafyazd2019,Humans process information hierarchically. In the presence of hierarchies, sources of failures are ambiguous. Humans resolve this ambiguity by assessing their confidence after one or more attempts. To understand the neural basis of this reasoning strategy, we recorded from dorsomedial frontal cortex (DMFC) and anterior cingulate cortex (ACC) of monkeys in a task in which negative outcomes were caused either by misjudging the stimulus or by a covert switch between two stimulus-response contingency rules. We found that both areas harbored a representation of evidence supporting a rule switch. Additional perturbation experiments revealed that ACC functioned downstream of DMFC and was directly and specifically involved in inferring covert rule switches. These results reveal the computational principles of hierarchical reasoning, as implemented by cortical circuits. |
Veronica E. Scerra; M. Gabriela Costello; Emilio Salinas; Terrence R. Stanford All-or-none context dependence delineates limits of FEF visual target selection Journal Article In: Current Biology, vol. 29, no. 2, pp. 294–305, 2019. @article{Scerra2019,Choices of where to look are informed by perceptual judgments, which locate objects of current value or interest within the visual scene. This perceptual-motor transform is partly implemented in the frontal eye field (FEF), where visually responsive neurons appear to select behaviorally relevant visual targets and, subsequently, saccade-related neurons select the movements required to look at them. Here, we use urgent decision-making tasks to show (1) that FEF motor activity can direct accurate, visually informed choices in the complete absence of prior target-distracter discrimination by FEF visual responses and (2) that such discrimination by FEF visual cells shows an all-or-none reliance on the presence of stimulus attributes strongly associated with saliency-driven attentional allocation. The present findings suggest that FEF visual target selection is specific to visual judgments made on the basis of saliency and may not play a significant role in guiding saccadic choices informed solely by feature content. |
Ehsan Sedaghat-Nejad; David J. Herzfeld; Paul Hage; Kaveh Karbasi; Tara Palin; Xiaoqin Wang; Reza Shadmehr Behavioral training of marmosets and electrophysiological recording from the cerebellum Journal Article In: Journal of Neurophysiology, vol. 122, no. 4, pp. 1502–1517, 2019. @article{Sedaghat-Nejad2019,The common marmoset (Callithrix jacchus) is a promising new model for study of neurophysiological basis of behavior in primates. Like other primates, it relies on saccadic eye movements to monitor and explore its environment. Previous reports have demonstrated some success in training marmosets to produce goal-directed actions in the laboratory. However, the number of trials per session has been relatively small, thus limiting the utility of marmosets as a model for behavioral and neurophysiological studies. In this article, we report the results of a series of new behavioral training and neurophysiological protocols aimed at increasing the number of trials per session while recording from the cerebellum. To improve the training efficacy, we designed a precisely calibrated food regulation regime that motivates the subjects to perform saccade tasks, resulting in ~1,000 reward-driven trials on a daily basis. We then developed a multichannel recording system that uses imaging to target a desired region of the cerebellum, allowing for simultaneous isolation of multiple Purkinje cells in the vermis. In this report, we describe 1) the design and surgical implantation of a computer tomography (CT)guided, subject-specific head post, 2) the design of a CT- and MRI-guided alignment tool for trajectory guidance of electrodes mounted on an absolute encoder microdrive, 3) development of a protocol for behavioral training of subjects, and 4) simultaneous recordings from pairs of Purkinje cells during a saccade task. |
Janahan Selvanayagam; Kevin D. Johnston; David J. Schaeffer; Lauren K. Hayrynen; Stefan Everling Functional localization of the frontal eye fields in the common marmoset using microstimulation Journal Article In: Journal of Neuroscience, vol. 39, no. 46, pp. 9197–9206, 2019. @article{Selvanayagam2019,The frontal eye field (FEF) is a critical region for the deployment of overt and covert spatial attention. Although investigations in the macaque continue to provide insight into the neural underpinnings of the FEF, due to its location within a sulcus, the macaque FEF is virtually inaccessible to electrophysiological techniques such as high-density and laminar recordings. With a largely lissencephalic cortex, the common marmoset (Callithrix jacchus) is a promising alternative primate model for studying FEF microcircuitry. Putative homologies have been established with the macaque FEF on the basis of cytoarchitecture and connectivity; however, physiological investigation in awake, behaving marmosets is necessary to physiologically locate this area. Here, we addressed this gap using intracortical microstimulation in a broad range of frontal cortical areas in three adult marmosets (two males, one female). We implanted marmosets with 96-channel Utah arrays and applied microstimulation trains while they freely viewed video clips. We evoked short-latency fixed vector saccades at low currents (<50 μA) in areas 45, 8aV, 8C, and 6DR. We observed a topography of saccade direction and amplitude consistent with findings in macaques and humans: small saccades in ventrolateral FEF and large saccades combined with contralateral neck and shoulder movements encoded in dorsomedial FEF. Our data provide compelling evidence supporting homology between marmoset and macaque FEF and suggest that the marmoset is a useful primate model for investigating FEF microcircuitry and its contributions to oculomotor and cognitive functions.SIGNIFICANCE STATEMENT The frontal eye field (FEF) is a critical cortical region for overt and covert spatial attention. The microcircuitry of this area remains poorly understood because in the macaque, the most commonly used model, it is embedded within a sulcus and is inaccessible to modern electrophysiological and imaging techniques. The common marmoset is a promising alternative primate model due to its lissencephalic cortex and potential for genetic manipulation. However, evidence for homologous cortical areas in this model remains limited and unclear. Here, we applied microstimulation in frontal cortical areas in marmosets to physiologically identify FEF. Our results provide compelling evidence for an FEF in the marmoset and suggest that the marmoset is a useful model for investigating FEF microcircuitry. |
Neda Shahidi; Ariana R. Andrei; Ming Hu; Valentin Dragoi High-order coordination of cortical spiking activity modulates perceptual accuracy Journal Article In: Nature Neuroscience, vol. 22, pp. 1148–1158, 2019. @article{Shahidi2019,The accurate relay of electrical signals within cortical networks is key to perception and cognitive function. Theoretically, it has long been proposed that temporal coordination of neuronal spiking activity controls signal transmission and behavior. However, whether and how temporally precise neuronal coordination in population activity influences perception are unknown. Here, we recorded populations of neurons in early and mid-level visual cortex (areas V1 and V4) simultaneously to discover that the precise temporal coordination between the spiking activity of three or more cells carries information about visual perception in the absence of firing rate modulation. The accuracy of perceptual responses correlated with high-order spiking coordination within V4, but not V1, and with feedforward coordination between V1 and V4. These results indicate that while visual stimuli are encoded in the discharge rates of neurons, perceptual accuracy is related to temporally precise spiking coordination within and between cortical networks. |
Hansem Sohn; Devika Narain; Nicolas Meirhaeghe; Mehrdad Jazayeri Bayesian computation through cortical latent dynamics Journal Article In: Neuron, vol. 103, no. 5, pp. 934–947.e5, 2019. @article{Sohn2019,Statistical regularities in the environment create prior beliefs that we rely on to optimize our behavior when sensory information is uncertain. Bayesian theory formalizes how prior beliefs can be leveraged and has had a major impact on models of perception, sensorimotor function, and cognition. However, it is not known how recurrent interactions among neurons mediate Bayesian integration. By using a time-interval reproduction task in monkeys, we found that prior statistics warp neural representations in the frontal cortex, allowing the mapping of sensory inputs to motor outputs to incorporate prior statistics in accordance with Bayesian inference. Analysis of recurrent neural network models performing the task revealed that this warping was enabled by a low-dimensional curved manifold and allowed us to further probe the potential causal underpinnings of this computational strategy. These results uncover a simple and general principle whereby prior beliefs exert their influence on behavior by sculpting cortical latent dynamics. Sohn et al. found that prior beliefs warp neural representations in the frontal cortex. This warping provides a substrate for the optimal integration of prior beliefs with sensory evidence during sensorimotor behavior. |
Sébastien Tremblay; Florian Pieper; Adam Sachs; Ridha Joober; Julio Martinez-Trujillo The effects of methylphenidate (Ritalin) on the neurophysiology of the monkey caudal prefrontal cortex Journal Article In: eNeuro, vol. 6, no. 1, pp. 1–17, 2019. @article{Tremblay2019,Methylphenidate (MPH), commonly known as Ritalin, is the most widely prescribed drug worldwide to treat patients with attention deficit disorders. Although MPH is thought to modulate catecholamine neurotransmission in the brain, it remains unclear how these neurochemical effects influence neuronal activity and lead to attentional enhancements. Studies in rodents overwhelmingly point to the lateral prefrontal cortex (LPFC) as a main site of action of MPH. To understand the mechanism of action of MPH in a primate brain, we recorded the responses of neuronal populations using chronic multielectrode arrays implanted in the caudal LPFC of two macaque monkeys while the animals performed an attention task (N 2811 neuronal recordings). Over different recording sessions (N 55), we orally administered either various doses of MPH or a placebo to the animals. Behavioral analyses revealed positive effects of MPH on task performance at specific doses. However, analyses of individual neurons activity, noise correlations, and neuronal ensemble activity using machine learning algorithms revealed no effects of MPH. Our results suggest that the positive behavioral effects of MPH observed in primates (including humans) may not be mediated by changes in the activity of caudal LPFC neurons. MPH may enhance cognitive performance by modulating neuronal activity in other regions of the attentional network in the primate brain. |
Kasper Vinken; Rufin Vogels A behavioral face preference deficit in a monkey with an incomplete face patch system Journal Article In: NeuroImage, vol. 189, pp. 415–424, 2019. @article{Vinken2019,Primates are experts in face perception and naturally show a preference for faces under free-viewing conditions. The primate ventral stream is characterized by a network of face patches that selectively responds to faces, but it remains uncertain how important such parcellation is for face perception. Here we investigated free-viewing behavior in a female monkey who naturally lacks fMRI-defined posterior and middle lateral face patches. We presented a series of content-rich images of scenes that included faces or other objects to that monkey during a free-viewing task and tested a group of 10 control monkeys on the same task for comparison. We found that, compared to controls, the monkey with missing face patches showed a marked reduction of face viewing preference that was most pronounced for the first few fixations. In addition, her gaze fixation patterns were substantially distinct from those of controls, especially for pictures with a face. These data demonstrate an association between the clustering of neurons in face selective patches and a behavioral bias for faces in natural images. |
Pascal Wallisch; J. Anthony Movshon Responses of neurons in macaque MT to unikinetic plaids Journal Article In: Journal of Neurophysiology, vol. 122, no. 5, pp. 1937–1945, 2019. @article{Wallisch2019,Response properties of MT neurons are often studied with “bikinetic” plaid stimuli, which consist of two superimposed sine wave gratings moving in different directions. Oculomotor studies using “unikinetic plaids” in which only one of the two superimposed gratings moves suggest that the eyes first move reflexively in the direction of the moving grating and only later converge on the perceived direction of the moving pattern. MT has been implicated as the source of visual signals that drives these responses. We wanted to know whether stationary gratings, which have little effect on MT cells when presented alone, would influence MT responses when paired with a moving grating. We recorded extracellularly from neurons in area MT and measured responses to stationary and moving gratings, and to their sums: bikinetic and unikinetic plaids. As expected, stationary gratings presented alone had a very modest influence on the activity of MT neurons. Responses to moving gratings and bikinetic plaids were similar to those previously reported and revealed cells selective for the motion of plaid patterns and of their components (pattern and component cells). When these neurons were probed with unikinetic plaids, pattern cells shifted their direction preferences in a way that revealed the influence of the static grating. Component cell preferences shifted little or not at all. These results support the notion that pattern-selective neurons in area MT integrate component motions that differ widely in speed, and that they do so in a way that is consistent with an intersection-of-constraints model. |
Maya Zhe Wang; Benjamin Y. Hayden Monkeys are curious about counterfactual outcomes Journal Article In: Cognition, vol. 189, pp. 1–10, 2019. @article{Wang2019g,Many non-human animals show exploratory behaviors. It remains unclear whether any possess human-like curiosity. We previously proposed three criteria for applying the term curiosity to animal behavior: (1) the subject is willing to sacrifice reward to obtain information, (2) the information provides no immediate instrumental or strategic benefit, and (3) the amount the subject is willing to pay depends systematically on the amount of information available. In previous work on information-seeking in animals, information generally predicts upcoming rewards, and animals' decisions may therefore be a byproduct of reinforcement processes. Here we get around this potential confound by taking advantage of macaques' ability to reason counterfactually (that is, about outcomes that could have occurred had the subject chosen differently). Specifically, macaques sacrificed fluid reward to obtain information about counterfactual outcomes. Moreover, their willingness to pay scaled with the information (Shannon entropy) offered by the counterfactual option. These results demonstrate the existence of human-like curiosity in non-human primates according to our criteria, which circumvent several confounds associated with less stringent criteria. |
Jacob A. Westerberg; Michele A. Cox; Kacie Dougherty; Alexander Maier V1 microcircuit dynamics: Altered signal propagation suggests intracortical origins for adaptation in response to visual repetition Journal Article In: Journal of Neurophysiology, vol. 121, no. 5, pp. 1938–1952, 2019. @article{Westerberg2019,Repetitive visual stimulation profoundly changes sensory processing in the primary visual cortex (V1). We show how the associated adaptive changes are linked to an altered flow of synaptic activation across the V1 laminar microcircuit. Using repeated visual stimulation, we recorded layer-specific responses in V1 of two fixating monkeys. We found that repetition-related spiking suppression was most pronounced outside granular V1 layers that receive the main retinogeniculate input. This repetition-related response suppression was robust to alternating stimuli between the eyes, in line with the notion that repetition-related adaptation is predominantly of cortical origin. Most importantly, current source density (CSD) analysis, which provides an estimate of local net depolarization, revealed that synaptic processing during repeated stimulation was most profoundly affected within supragranular layers, which harbor the bulk of corticocortical connections. Direct comparison of the temporal evolution of laminar CSD and spiking activity showed that stimulus repetition first affected supragranular synaptic currents, which translated into a reduction of stimulus-evoked spiking across layers. Together, these results suggest that repetition induces an altered state of intracortical processing that underpins visual adaptation. |
Brian J. White; Laurent Itti; Douglas P. Munoz Superior colliculus encodes visual saliency during smooth pursuit eye movements Journal Article In: European Journal of Neuroscience, pp. 1–11, 2019. @article{White2019,The saliency map has played a long-standing role in models and theories of visual attention, and it is now supported by neurobiological evidence from several cortical and subcortical brain areas. While visual saliency is computed during moments of active fixation, it is not known whether the same is true while engaged in smooth pursuit of a moving stimulus, which is very common in real-world vision. Here, we examined extrafoveal saliency coding in the superior colliculus, a midbrain area associated with attention and gaze, during smooth pursuit eye movements. We found that SC neurons from the superficial visual layers showed a robust representation of peripheral saliency evoked by a conspicuous stimulus embedded in a wide-field array of goal-irrelevant stimuli. In contrast, visuomotor neurons from the intermediate saccade-related layers showed a poor saliency representation, even though most of these neurons were visually responsive during smooth pursuit. These results confirm and extend previous findings that place the SCs in a unique role as a saliency map that monitors peripheral vision during foveation of stationary and now moving objects. |
J. Kael White; Ethan S. Bromberg-Martin; Sarah R. Heilbronner; Kaining Zhang; Julia Pai; Suzanne N. Haber; Ilya E. Monosov A neural network for information seeking Journal Article In: Nature Communications, vol. 10, pp. 5168, 2019. @article{White2019a,Humans and other animals often show a strong desire to know the uncertain rewards their future has in store, even when they cannot use this information to influence the outcome. However, it is unknown how the brain predicts opportunities to gain information and motivates this information-seeking behavior. Here we show that neurons in a network of interconnected subregions of primate anterior cingulate cortex and basal ganglia predict the moment of gaining information about uncertain rewards. Spontaneous increases in their information prediction signals are followed by gaze shifts toward objects associated with resolving uncertainty, and pharmacologically disrupting this network reduces the motivation to seek information. These findings demonstrate a cortico-basal ganglia mechanism responsible for motivating actions to resolve uncertainty by seeking knowledge about the future. |
Konstantin F. Willeke; Xiaoguang Tian; Antimo Buonocore; Joachim Bellet; Araceli Ramirez-Cardenas; Ziad M. Hafed Memory-guided microsaccades Journal Article In: Nature Communications, vol. 10, pp. 3710, 2019. @article{Willeke2019,Despite strong evidence to the contrary in the literature, microsaccades are overwhelmingly described as involuntary eye movements. Here we show in both human subjects and monkeys that individual microsaccades of any direction can easily be triggered: (1) on demand, based on an arbitrary instruction, (2) without any special training, (3) without visual guidance by a stimulus, and (4) in a spatially and temporally accurate manner. Subjects voluntarily generated instructed “memory-guided” microsaccades readily, and similarly to how they made normal visually-guided ones. In two monkeys, we also observed midbrain superior colliculus neurons that exhibit movement-related activity bursts exclusively for memory-guided microsaccades, but not for similarly-sized visually-guided movements. Our results demonstrate behavioral and neural evidence for voluntary control over individual microsaccades, supporting recently discovered functional contributions of individual microsaccade generation to visual performance alterations and covert visual selection, as well as observations that microsaccades optimize eye position during high acuity visually-guided behavior. |
Ting Yan; Hui Hui Zhou Synchronization between frontal eye field and area V4 during free-gaze visual search Journal Article In: Zoological research, vol. 40, no. 5, pp. 394–403, 2019. @article{Yan2019d,Information flow between the prefrontal and visual cortices is critical for visual behaviors such as visual search. To investigate its mechanisms, we simultaneously recorded spike and local field potential (LFP) signals in the frontal eye field (FEF) and area V4 while monkeys performed a free-gaze visual search task. During free-gaze search, spike-LFP coherence between FEF and V4 was enhanced in the theta rhythm (4-8 Hz) but suppressed in the alpha rhythm (8-13 Hz). Cross-frequency couplings during the Cue period before the search phase were related to monkey performance, with higher FEF theta-V4 gamma coupling and lower FEF alpha-V4 gamma coupling associated with faster search. Finally, feature-based attention during search enhanced spike-LFP coherence between FEF and V4 in the gamma and beta rhythms, whereas overt spatial attention reduced coherence at frequencies up to 30 Hz. These results suggest that oscillatory coupling may play an important role in mediating interactions between the prefrontal and visual cortices during visual search. |
Man Yi Yim; Xinying Cai; Xiao-Jing Wang Transforming the choice outcome to an action plan in monkey lateral prefrontal cortex: A neural circuit model Journal Article In: Neuron, vol. 103, no. 3, pp. 520–532.e5, 2019. @article{Yim2019,In economic decisions, we make a good-based choice first, then we transform the outcome into an action to obtain the good. To elucidate the network mechanisms for such transformation, we constructed a neural circuit model consisting of modules representing choice, integration of choice with target locations, and the final action plan. We examined three scenarios regarding how the final action plan could emerge in the neural circuit and compared their implications with experimental data. Our model with heterogeneous connectivity predicts the coexistence of three types of neurons with distinct functions, confirmed by analyzing the neural activity in the lateral prefrontal cortex (LPFC) of behaving monkeys. We obtained a much more distinct classification of functional neuron types in the ventral than the dorsal region of LPFC, suggesting that the action plan is initially generated in ventral LPFC. Our model offers a biologically plausible neural circuit architecture that implements good-to-action transformation during economic choice. Yim et al. propose a circuit model that implements good-to-action transformation during economic choice. Heterogeneity in circuit synaptic connections is crucial for the coexistence of distinct functional neuron types, which is confirmed by cluster analysis of neuronal activity in LPFC. |
Andrew D. Zaharia; Robbe L. T. Goris; J. Anthony Movshon; Eero P. Simoncelli Compound stimuli reveal the structure of visual motion selectivity in macaque MT neurons Journal Article In: eNeuro, vol. 6, no. 6, pp. 1–19, 2019. @article{Zaharia2019,Motion selectivity in primary visual cortex (V1) is approximately separable in orientation, spatial frequency, and temporal frequency (“frequency-separable”). Models for area MT neurons posit that their selectivity arises by combining direction-selective V1 afferents whose tuning is organized around a tilted plane in the frequency domain, specifying a particular direction and speed (“velocity-separable”). This construction explains “pattern direction-selective” MT neurons, which are velocity-selective but relatively invariant to spatial structure, including spatial frequency, texture and shape. We designed a set of experiments to distinguish frequency-separable and velocity-separable models and executed them with single-unit recordings in macaque V1 and MT. Surprisingly, when tested with single drifting gratings, most MT neurons' responses are fit equally well by models with either form of separability. However, responses to plaids (sums of two moving gratings) tend to be better described as velocity-separable, especially for pattern neurons. We conclude that direction selectivity in MT is primarily computed by summing V1 afferents, but pattern-invariant velocity tuning for complex stimuli may arise from local, recurrent interactions. |
Kaining Zhang; Charles D. Chen; Ilya E. Monosov Novelty, salience, and surprise timing are signaled by neurons in the basal forebrain Journal Article In: Current Biology, vol. 29, no. 1, pp. 134–142, 2019. @article{Zhang2019g,The basal forebrain (BF) is a principal source of modulation of the neocortex [1–6] and is thought to regulate cognitive functions such as attention, motivation, and learning by broadcasting information about salience [2, 3, 5, 7–19]. However, events can be salient for multiple reasons—such as novelty, surprise, or reward prediction errors [20–24]—and to date, precisely which salience-related information the BF broadcasts isunclear.Here, wereport that theprimate BF contains at least two types of neurons that often process salient events in distinct manners: one with phasic burst responses to cues predicting salient events and one with ramping activity anticipating such events. Bursting neurons respond to cues that convey predictions about the magnitude, probability, and timing of primary reinforcements. They also burst to the reinforcement itself, particularly when it is unexpected. However, they do not have a selective response to reinforcement omission (the unexpected absence of an event). Thus, bursting neurons do not convey value-prediction errors but do signal surprise associated with external events. Indeed, they are not limited to processing primary reinforcement: they discriminate fully expected novel visual objects from familiar objects and respond to object-sequence violations. In contrast, ramping neurons predict the timing of many salient, novel, and surprising events. Their ramping activity is highly sensitive to the subjects' confidence in event timing and on average encodes the subjects' surprise after unexpected events occur. These data suggest that the primate BF contains mechanisms to anticipate the timing of a diverse set of important external events (via ramping activity) and to rapidly deploy cognitive resources when these events occur (via short latency bursting). |
2018 |
Ricardo Kienitz; Joscha T. Schmiedt; Katharine A. Shapcott; Kleopatra Kouroupaki; Richard C. Saunders; Michael C. Schmid Theta rhythmic neuronal activity and reaction times arising from cortical receptive field interactions during distributed attention Journal Article In: Current Biology, vol. 28, no. 15, pp. 2377–2387, 2018. @article{Kienitz2018,Growing evidence suggests that distributed spatial attention may invoke theta (3–9 Hz) rhythmic sampling processes. The neuronal basis of such attentional sampling is, however, not fully understood. Here we show using array recordings in visual cortical area V4 of two awake macaques that presenting separate visual stimuli to the excitatory center and suppressive surround of neuronal receptive fields (RFs) elicits rhythmic multi-unit activity (MUA)at 3–6 Hz. This neuronal rhythm did not depend on small fixational eye movements. In the context of a distributed spatial attention task, during which the monkeys detected a spatially and temporally uncertain target, reaction times (RTs) exhibited similar rhythmic fluctuations. RTs were fast or slow depend-ing on the target occurrence during high or low MUA, resulting in rhythmic MUA-RT cross-correlations at theta frequencies. These findings show that theta rhythmic neuronal activity can arise from competitiveRF interactions and that this rhythm may result in rhythmic RTs potentially subserving attentional sampling. |
Joshua D. Cosman; Kaleb A. Lowe; Wolf Zinke; Geoffrey F. Woodman; Jeffrey D. Schall Prefrontal control of visual distraction Journal Article In: Current Biology, vol. 28, no. 3, pp. 414–420, 2018. @article{Cosman2018,Avoiding distraction by conspicuous but irrelevant stimuli is critical to accomplishing daily tasks. Regions of prefrontal cortex control attention by enhancing the representation of task-relevant information in sensory cortex, which can be measured in modulation of both single neurons and event-related electrical potentials (ERPs) on the cranial surface [1, 2]. When irrelevant information is particularly conspicuous, it can distract attention and interfere with the selection of behaviorally relevant information. Such distraction can be minimized via top-down control [3–5], but the cognitive and neural mechanisms giving rise to this control over distraction remain uncertain and debated [6–9]. Bridging neurophysiology to electrophysiology, we simultaneously recorded neurons in prefrontal cortex and ERPs over extrastriate visual cortex to track the processing of salient distractors during a visual search task. Critically, when the salient distractor was successfully ignored, but not otherwise, we observed robust suppression of salient distractor representations. Like target selection, the distractor suppression was observed in prefrontal cortex before it appeared over extrastriate cortical areas. Furthermore, all prefrontal neurons that showed suppression of the task-irrelevant distractor also contributed to selecting the target. This suggests a common prefrontal mechanism is responsible for both selecting task-relevant and suppressing task-irrelevant information in sensory cortex. Taken together, our results resolve a long-standing debate over the mechanisms that prevent distraction, and provide the first evidence directly linking suppressed neural firing in prefrontal cortex with surface ERP measures of distractor suppression. |
Amir-Mohammad Alizadeh; Ilse C. Van Dromme; Peter Janssen Single-cell responses to three-dimensional structure in a functionally defined patch in macaque area TEO Journal Article In: Journal of Neurophysiology, vol. 120, no. 6, pp. 2806–2818, 2018. @article{Alizadeh2018,Both dorsal and ventral visual pathways harbor several areas sensitive to gradients of binocular disparity (i.e., higher-order disparity). Although a wealth of information exists about disparity processing in early visual (V1, V2, and V3) and end-stage areas, TE in the ventral stream, and the anterior intraparietal area (AIP) in the dorsal stream, little is known about midlevel area TEO in the ventral pathway. We recorded single-unit responses to disparity-defined curved stimuli in a functional magnetic resonance imaging (fMRI) activation elicited by curved surfaces compared with flat surfaces in the macaque area TEO. This fMRI activation contained a small proportion of disparity- selective neurons, with very few of them second-order disparity selective. Overall, this population of TEO neurons did not preserve its three-dimensional structure selectivity across positions in depth, in- dicating a lack of higher-order disparity selectivity, but showed stronger responses to flat surfaces than to curved surfaces, as predicted by the fMRI experiment. The receptive fields of the responsive TEO cells were relatively small and generally foveal. A linear support vector machine classifier showed that this population of disparity-selective TEO neurons contains reliable information about the sign of curvature and the position in depth of the stimulus. |
Amir-Mohammad Alizadeh; Ilse C. Van Dromme; Bram-Ernst Verhoef; Peter Janssen Caudal Intraparietal Sulcus and three-dimensional vision: A combined functional magnetic resonance imaging and single-cell study Journal Article In: NeuroImage, vol. 166, pp. 46–59, 2018. @article{Alizadeh2018a,The cortical network processing three-dimensional (3D) object structure defined by binocular disparity spans both the ventral and dorsal visual streams. However, very little is known about the neural representation of 3D structure at intermediate levels of the visual hierarchy. Here, we investigated the neural selectivity for 3D surfaces in the macaque Posterior Intraparietal area (PIP) in the medial bank of the caudal intraparietal sulcus (IPS). We first identified a region sensitive to depth-structure information in the medial bank of the caudal IPS using functional Magnetic Resonance Imaging (fMRI), and then recorded single-cell activity within this fMRI activation in the same animals. Most PIP neurons were selective for the 3D orientation of planar surfaces (first-order disparity) at very short latencies, whereas a very small fraction of PIP neurons were selective for curved surfaces (second-order disparity). A linear support vector machine classifier could reliably identify the direction of the disparity gradient in planar and curved surfaces based on the responses of a population of disparity-selective PIP neurons. These results provide the first detailed account of the neuronal properties in area PIP, which occupies an intermediate position in the hierarchy of visual areas involved in processing depth structure from disparity. |
Ken-ichi Amemori; Satoko Amemori; Daniel J. Gibson; Ann M. Graybiel Striatal microstimulation induces persistent and repetitive negative decision-making predicted by striatal beta-band oscillation Journal Article In: Neuron, vol. 99, no. 4, pp. 829–841.e6, 2018. @article{Amemori2018,Persistent thoughts inducing irrationally pessimistic and repetitive decisions are often symptoms of mood and anxiety disorders. Regional neural hyperactivities have been associated with these disorders, but it remains unclear whether there is a specific brain region causally involved in these persistent valuations. Here, we identified potential sources of such persistent states by microstimulating the striatum of macaques performing a task by which we could quantitatively estimate their subjective pessimistic states using their choices to accept or reject conflicting offers. We found that this microstimulation induced irrationally repetitive choices with negative evaluations. Local field potentials recorded in the same microstimulation sessions exhibited modulations of beta-band oscillatory activity that paralleled the persistent negative states influencing repetitive decisions. These findings demonstrate that local striatal zones can causally affect subjective states influencing persistent negative valuation and that abnormal beta-band oscillations can be associated with persistency in valuation accompanied by an anxiety-like state. Amemori et al. identified candidate subcortical loci potentially related to persistency of anxiety-like states and inflexibility in OCD. The authors' work in non-human primates shows that striatal stimulation induces repetitive negative choice pattern, accompanied by modulation of striatal beta oscillation. |
Fabrice Arcizet; Richard J. Krauzlis Covert spatial selection in primate basal ganglia Journal Article In: PLoS Biology, vol. 16, no. 10, pp. e2005930, 2018. @article{Arcizet2018,The basal ganglia are important for action selection. They are also implicated in perceptual and cognitive functions that seem far removed from motor control. Here, we tested whether the role of the basal ganglia in selection extends to nonmotor aspects of behavior by recording neuronal activity in the caudate nucleus while animals performed a covert spatial attention task. We found that caudate neurons strongly select the spatial location of the relevant stimulus throughout the task even in the absence of any overt action. This spatially selective activity was dependent on task and visual conditions and could be dissociated from goal-directed actions. Caudate activity was also sufficient to correctly identify every epoch in the covert attention task. These results provide a novel perspective on mechanisms of attention by demonstrating that the basal ganglia are involved in spatial selection and tracking of behavioral states even in the absence of overt orienting movements. |
Habiba Azab; Benjamin Y. Hayden Correlates of economic decisions in the dorsal and subgenual anterior cingulate cortices Journal Article In: European Journal of Neuroscience, vol. 47, no. 8, pp. 979–993, 2018. @article{Azab2018,The anterior cingulate cortex can be divided into distinct ventral (subgenual, sgACC) and dorsal (dACC), portions. The role of dACC in value-based decision-making is hotly debated, while the role of sgACC is poorly understood. We recorded neuronal activity in both regions in rhesus macaques performing a token-gambling task. We find that both encode many of the same vari- ables; including integrated offered values of gambles, primary as well as secondary reward outcomes, number of current tokens and anticipated rewards. Both regions exhibit memory traces for offer values and putative value comparison signals. Both regions use a consistent scheme to encode the value of the attended option. This result suggests that neurones do not appear to be spe- cialized for specific offers (that is, neurones use an attentional as opposed to labelled line coding scheme). We also observed some differences between the two regions: (i) coding strengths in dACC were consistently greater than those in sgACC, (ii) neu- rones in sgACC responded especially to losses and in anticipation of primary rewards, while those in dACC showed more bal- anced responding and (iii) responses to the first offer were slightly faster in sgACC. These results indicate that sgACC and dACC have some functional overlap in economic choice, and are consistent with the idea, inspired by neuroanatomy, which sgACC may serve as input to dACC. |
Theda Backen; Stefan Treue; Julio C. Martinez-Trujillo Encoding of spatial attention by primate prefrontal cortex neuronal ensembles Journal Article In: eNeuro, vol. 5, no. 1, pp. 1–19, 2018. @article{Backen2018,Single neurons in the primate lateral prefrontal cortex (LPFC) encode information about the allocation of visual attention and the features of visual stimuli. However, how this compares to the performance of neuronal ensembles at encoding the same information is poorly understood. Here, we recorded the responses of neuronal ensembles in the LPFC of two macaque monkeys while they performed a task that required attending to one of two moving random dot patterns positioned in different hemifields and ignoring the other pattern. We found single units selective for the location of the attended stimulus as well as for its motion direction. To determine the coding of both variables in the population of recorded units, we used a linear classifier and progressively built neuronal ensembles by iteratively adding units according to their individual performance (best single units), or by iteratively adding units based on their contribution to the ensemble performance (best ensemble). For both methods, ensembles of relatively small sizes (n < 60) yielded substantially higher decoding performance relative to individual single units. However, the decoder reached similar performance using fewer neurons with the best ensemble building method compared to the best single units method. Our results indicate that neuronal ensembles within the LPFC encode more information about the attended spatial and non-spatial features of visual stimuli than individual neurons. They further suggest that efficient coding of attention can be achieved by relatively small neuronal ensembles characterized by a certain relationship between signal and noise correlation structures. Significance Statement Single neurons in the primate lateral prefrontal cortex (LPFC) are known to encode the spatial location of attended stimuli as well as other visual features. Here, we investigate how these single neuron coding properties translate into how ensembles of neurons encode information. Our results show that LPFC neuronal ensembles encode both the allocation of attention and the direction of motion of moving stimuli with higher efficiency than single units. Furthermore, relatively small ensembles reach the same decoding accuracy as the full ensembles. Our findings indicate that information coding by neuronal ensembles within the LPFC depends on complex network properties that cannot be solely estimated from coding properties of individual neurons. |
Zahra Bahmani; Mohammad Reza Daliri; Yaser Merrikhi; Kelsey Clark; Behrad Noudoost Working memory enhances cortical representations via spatially specific coordination of spike times Journal Article In: Neuron, vol. 97, no. 4, pp. 967–979.e6, 2018. @article{Bahmani2018,The online maintenance and manipulation of information in working memory (WM) is essential for guiding behavior based on our goals. Understanding how WM alters sensory processing in pursuit of different behavioral objectives is therefore crucial to establish the neural basis of our goal-directed behavior. Here we show that, in the middle temporal (MT) area of rhesus monkeys, the power of the local field potentials in the αβ band (8–25 Hz) increases, reflecting the remembered location and the animal's performance. Moreover, the content of WM determines how coherently MT sites oscillate and how synchronized spikes are relative to these oscillations. These changes in spike timing are not only sufficient to carry sensory and memory information, they can also account for WM-induced sensory enhancement. These results provide a mechanistic-level understanding of how WM alters sensory processing by coordinating the timing of spikes across the neuronal population, enhancing the sensory representation of WM targets. When examining primate extrastriate visual responses, Bahmani et al. find that, in the absence of rate changes, working memory mainly affects αβ oscillations and spike timing. These changes are associated with better visual processing, suggesting how working memory benefits sensory areas. |
Giacomo Benvenuti; Yuzhi Chen; Charu Ramakrishnan; Karl Deisseroth; Wilson S. Geisler; Eyal Seidemann Scale-invariant visual capabilities explained by topographic representations of luminance and texture in primate V1 Journal Article In: Neuron, vol. 100, no. 6, pp. 1504–1512.e4, 2018. @article{Benvenuti2018,Benvenuti et al. describe a novel retinotopic representation of low-spatial-frequency luminance stimuli in V1 of behaving macaques. This distributed representation could solve the “aperture problem” for computation of orientation of low-spatial-frequency stimuli by single V1 neurons. |
Anil Bollimunta; Amarender R. Bogadhi; Richard J. Krauzlis Comparing frontal eye field and superior colliculus contributions to covert spatial attention Journal Article In: Nature Communications, vol. 9, pp. 3553, 2018. @article{Bollimunta2018,The causal roles of the frontal eye fields (FEF) and superior colliculus (SC) in spatial selective attention have not been directly compared. Reversible inactivation is an established method for testing causality but comparing results between FEF and SC is complicated by differences in size and morphology of the two brain regions. Here we exploited the fact that inactivation of FEF and SC also changes the metrics of saccadic eye movements, providing an independent benchmark for the strength of the causal manipulation. Using monkeys trained to covertly perform a visual motion-change detection task, we found that inactivation of either FEF or SC could cause deficits in attention task performance. However, SC-induced attention deficits were found with saccade changes half the size needed to get FEF-induced attention deficits. Thus, performance in visual attention tasks is vulnerable to loss of signals from either structure, but suppression of SC activity has a more devastating effect. |
Yehudit Botschko; Merav Yarkoni; Mati Joshua Smooth pursuit eye movement of monkeys naive to laboratory setups with pictures and artificial stimuli Journal Article In: Frontiers in Systems Neuroscience, vol. 12, pp. 15, 2018. @article{Botschko2018,When animal behavior is studied in a laboratory environment, the animals are often extensively trained to shape their behavior. A crucial question is whether the behavior observed after training is part of the natural repertoire of the animal or represents an outlier in the animal's natural capabilities. This can be investigated by assessing the extent to which the target behavior is manifested during the initial stages of training and the time course of learning. We explored this issue by examining smooth pursuit eye movements in monkeys naïve to smooth pursuit tasks. We recorded the eye movements of monkeys from the first days of training on a step-ramp paradigm. We used bright spots, monkey pictures and scrambled versions of the pictures as moving targets. We found that during the initial stages of training, the pursuit initiation was largest for the monkey pictures and in some direction conditions close to target velocity. When the pursuit initiation was large, the monkeys mostly continued to track the target with smooth pursuit movements while correcting for displacement errors with small saccades. Two weeks of training increased the pursuit eye velocity in all stimulus conditions, whereas further extensive training enhanced pursuit slightly more. The training decreased the coefficient of variation of the eye velocity. Anisotropies that grade pursuit across directions were observed from the first day of training and mostly persisted across training. Thus, smooth pursuit in the step-ramp paradigm appears to be part of the natural repertoire of monkeys' behavior and training adjusts monkeys' natural predisposed behavior. |
Irene Caprara; Peter Janssen; Maria C. Romero Investigating object representations in the macaque dorsal visual stream using single-unit recordings Journal Article In: Journal of Visualized Experiments, no. 138, pp. 1–10, 2018. @article{Caprara2018a,Previous studies have shown that neurons in parieto-frontal areas of the macaque brain can be highly selective for real-world objects, disparity-defined curved surfaces, and images of real-world objects (with and without disparity) in a similar manner as described in the ventral visual stream. In addition, parieto-frontal areas are believed to convert visual object information into appropriate motor outputs, such as the pre-shaping of the hand during grasping. To better characterize object selectivity in the cortical network involved in visuomotor transformations, we provide a battery of tests intended to analyze the visual object selectivity of neurons in parieto-frontal regions. |
Irene Caprara; Elsie Premereur; Maria C. Romero; Pedro Faria; Peter Janssen Shape responses in a macaque frontal area connected to posterior parietal cortex Journal Article In: NeuroImage, vol. 179, pp. 298–312, 2018. @article{Caprara2018,The primate dorsal visual stream processes object shape to guide actions involving an object, but the transmission of shape information beyond posterior parietal cortex remains largely unknown. To clarify the information flow between parietal and frontal cortex, we applied electrical microstimulation during functional Magnetic Resonance Imaging (fMRI) in a shape-selective patch in the posterior part of the Anterior Intraparietal area (pAIP) to chart its connectivity. Subsequently, we recorded single-unit responses to images of objects in the fMRI activation in prefrontal cortex, corresponding to area 45B, elicited by pAIP microstimulation. Neurons in area 45B had properties similar to neurons in pAIP, responding selectively to shape contours and to very small shape fragments measuring less than one deg at exceedingly short latencies. However, contrary to the prevailing view on the hierarchical organization of cortical areas, neurons in area 45B preferred even smaller shape fragments and had smaller receptive fields than neurons in pAIP. These findings provide the first evidence for ultra-fast shape processing in prefrontal cortex, and suggest that the pathway from pAIP to area 45B may not be important for object grasping. |
Chih-Yang Chen; Lukas Sonnenberg; Simone Weller; Thede Witschel; Ziad M. Hafed Spatial frequency sensitivity in macaque midbrain Journal Article In: Nature Communications, vol. 9, pp. 2852, 2018. @article{Chen2018c,Visual brain areas exhibit tuning characteristics well suited for image statistics present in our natural environment. However, visual sensation is an active process, and if there are any brain areas that ought to be particularly in tune with natural scene statistics, it would be sensory-motor areas critical for guiding behavior. Here we found that the rhesus macaque superior colliculus, a structure instrumental for rapid visual exploration with saccades, detects low spatial frequencies, which are the most prevalent in natural scenes, much more rapidly than high spatial frequencies. Importantly, this accelerated detection happens independently of whether a neuron is more or less sensitive to low spatial frequencies to begin with. At the population level, the superior colliculus additionally over-represents low spatial frequencies in neural response sensitivity, even at near-foveal eccentricities. Thus, the superior colliculus possesses both temporal and response gain mechanisms for efficient gaze realignment in low-spatial-frequency-dominated natural environments. |
Hoseok Choi; Seho Lee; Jeyeon Lee; Kyeongran Min; Seokbeen Lim; Jinsick Park; Kyoung-ha Ahn; In Young Kim; Kyoung-Min Lee; Dong Pyo Jang Long-term evaluation and feasibility study of the insulated screw electrode for ECoG recording Journal Article In: Journal of Neuroscience Methods, vol. 308, pp. 261–268, 2018. @article{Choi2018,Background: A screw-shaped electrode can offer a compromise between signal quality and invasiveness. However, the standard screw electrode can be vulnerable to electrical noise while directly contact with the skull or skin, and the feasibility and stability for chronic implantation in primate have not been fully evaluated. New Method: We designed a novel screw electrocorticogram (ECoG) electrode composed of three parts: recording electrode, insulator, and nut. The recording electrode was made of titanium with high biocompatibility and high electrical conductivity. Zirconia is used for insulator and nut to prevent electrical noise. Result: In computer simulations, the screw ECoG with insulator showed a significantly higher performance in signal acquisition compared to the condition without insulator. In a non-human primate, using screw ECoG, clear visual-evoked potential (VEP) waveforms were obtained, VEP components were reliably maintained, and the electrode's impedance was stable during the whole evaluation period. Moreover, it showed higher SNR and wider frequency band compared to the electroencephalogram (EEG). We also observed the screw ECoG has a higher sensitivity that captures different responses on various stimuli than the EEG. Comparison: The screw ECoG showed reliable electrical characteristic and biocompatibility for three months, that shows great promise for chronic implants. These results contrasted with previous reports that general screw electrode was only applicable for acute applications. Conclusion: The suggested electrode can offer whole-brain monitoring with high signal quality and minimal invasiveness. The screw ECoG can be used to provide more in-depth understanding, not only relationship between functional networks and cognitive behavior, but also pathomechanisms in brain diseases. |