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2019 |
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. |
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. |
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). |
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. |
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. |
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{SedaghatNejad2019, 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. |
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. |
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. |
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. |
Jan Churan; Doris I. Braun; Karl R. Gegenfurtner; Frank Bremmer Comparison of the precision of smooth pursuit in humans and head unrestrained monkeys Journal Article In: Journal of Eye Movement Research, vol. 11, no. 4, pp. 1–15, 2018. @article{Churan2018, Direct comparison of results of humans and monkeys is often complicated by differences in experimental conditions. We replicated in head unrestrained macaques experiments of a recent study comparing human directional precision during smooth pursuit eye movements (SPEM) and saccades to moving targets (Braun & Gegenfurtner, 2016). Directional precision of human SPEM follows an exponential decay function reaching optimal values of 1.5°-3° within 300 ms after target motion onset, whereas precision of initial saccades to moving targets is slightly better. As in humans, we found general agreement in the development of directional precision of SPEM over time and in the differences between directional precision of initial saccades and SPEM initiation. However, monkeys showed overall lower precision in SPEM compared to humans. This was most likely due to differences in experimental conditions, such as in the stabilization of the head, which was by a chin and a head rest in human subjects and unrestrained in monkeys. |
Suryadeep Dash; Tyler R. Peel; Stephen G. Lomber; Brian D. Corneil In: eNeuro, vol. 5, no. 2, pp. 1–16, 2018. @article{Dash2018, A neural correlate for saccadic reaction times (SRTs) in the gap saccade task is the level of low-frequency activity in the intermediate layers of the superior colliculus (iSC) just before visual target onset: greater levels of such preparatory iSC low-frequency activity precede shorter SRTs. The frontal eye fields (FEFs) are one likely source of iSC preparatory activity, since FEF preparatory activity is also inversely related to SRT. To better understand the FEF's role in saccade preparation, and the way in which such preparation relates to SRT, in two male rhesus monkeys, we compared iSC preparatory activity across unilateral reversible cryogenic inactivation of the FEF. FEF inactivation increased contralesional SRTs, and lowered ipsilesional iSC preparatory activity. FEF inactivation also reduced rostral iSC activity during the gap period. Importantly, the distributions of SRTs generated with or without FEF inactivation overlapped, enabling us to conduct a novel population-level analyses examining iSC preparatory activity just before generation of SRT-matched saccades. When matched for SRTs, we observed no change during FEF inactivation in the relationship between iSC preparatory activity and SRT-matched saccades across a range of SRTs, even for the occasional express saccade. Thus, while our results emphasize that the FEF has an overall excitatory influence on preparatory activity in the iSC, the communication between the iSC and downstream oculomotor brainstem is unaltered for SRT-matched saccades. |
Mohammad-Reza A. Dehaqani; Abdol-Hossein Vahabie; Mohammadbagher Parsa; Behrad Noudoost; Alireza Soltani Selective changes in noise correlations contribute to an enhanced representation of saccadic targets in prefrontal neuronal ensembles Journal Article In: Cerebral Cortex, vol. 28, no. 8, pp. 3046–3063, 2018. @article{Dehaqani2018, An ensemble of neurons can provide a dynamic representation of external stimuli, ongoing processes, or upcoming actions. This dynamic representation could be achieved by changes in the activity of individual neurons and/or their interactions. To investigate these possibilities, we simultaneously recorded from ensembles of prefrontal neurons in non-human primates during a memory-guided saccade task. Using both decoding and encoding methods, we examined changes in the information content of individual neurons and that of ensembles between visual encoding and saccadic target selection. We found that individual neurons maintained their limited spatial sensitivity between these cognitive states, whereas the ensemble selectively improved its encoding of spatial locations far from the neurons' preferred locations. This population- level “encoding expansion” was not due to the ceiling effect at the preferred locations and was accompanied by selective changes in noise correlations for non-preferred locations. Moreover, the encoding expansion was observed for ensembles of different types of neurons and could not be explained by shifts in the preferred location of individual neurons. Our results demonstrate that the representation of space by neuronal ensembles is dynamically enhanced prior to saccades, and this enhancement occurs alongside changes in noise correlations more than changes in the activity of individual neurons. |
R. Becket Ebitz; Eddy Albarran; Tirin Moore Exploration disrupts choice-predictive signals and alters dynamics in prefrontal cortex Journal Article In: Neuron, vol. 97, no. 2, pp. 450–461.e9, 2018. @article{Ebitz2018, In uncertain environments, decision-makers must balance two goals: they must “exploit” rewarding options but also “explore” in order to discover rewarding alternatives. Exploring and exploiting necessarily change how the brain responds to identical stimuli, but little is known about how these states, and transitions between them, change how the brain transforms sensory information into action. To address this question, we recorded neural activity in a prefrontal sensorimotor area while monkeys naturally switched between exploring and exploiting rewarding options. We found that exploration profoundly reduced spatially selective, choice-predictive activity in single neurons and delayed choice-predictive population dynamics. At the same time, reward learning was increased in brain and behavior. These results indicate that exploration is related to sudden disruptions in prefrontal sensorimotor control and rapid, reward-dependent reorganization of control dynamics. This may facilitate discovery through trial and error. Exploratory choices permit the discovery of new rewarding options. Ebitz et al. report that spatially selective, choice-predictive neurons in the prefrontal cortex do not predict choice before exploratory decisions. Reduced prefrontal control may underlie flexible decision-making and trial-and-error discovery. |
Shiva Farashahi; Habiba Azab; Benjamin Y. Hayden; Alireza Soltani On the flexibility of basic risk attitudes in monkeys Journal Article In: Journal of Neuroscience, vol. 38, no. 18, pp. 4383–4398, 2018. @article{Farashahi2018, Monkeys and other animals appear to share with humans two risk attitudes predicted by prospect theory: an inverse-S-shaped probability weighting function and a steeper utility curve for losses than for gains. These findings suggest that such preferences are stable traits with common neural substrates. We hypothesized instead that animals tailor their preferences to subtle changes in task contexts, making risk attitudes flexible. Previous studies used a limited number of outcomes, trial types, and contexts. To gain a broader perspective, we examined two large datasets of male macaques' risky choices: one from a task with real (juice) gains and another from a token task with gains and losses. In contrast to previous findings, monkeys were risk-seeking for both gains and losses (i.e. lacked a reflection effect) and showed steeper gain than loss curves (loss-seeking). Utility curves for gains were substantially different in the two tasks. Monkeys showed nearly linear probability weightings in one task and S-shaped ones in the other; neither task produced a consistent inverse-S-shaped curve. To account for these observations, we developed and tested various computational models of the processes involved in the construction of reward value. We found that adaptive differential weighting of prospective gamble outcomes could partially account for the observed differences in the utility functions across the two experiments and thus, provide a plausible mechanism underlying flexible risk attitudes. Together, our results support the idea that risky choices are constructed flexibly at the time of elicitation and place important constraints on neural models of economic choice. |
Jose A. Fernandez-Leon; Bryan J. Hansen; Valentin Dragoi Representation of rapid image sequences in V4 Networks Journal Article In: Cerebral Cortex, vol. 28, no. 8, pp. 2675–2684, 2018. @article{FernandezLeon2018, Natural viewing often consists of sequences of brief fixations to image patches of different structure. Whether and how briefly presented sequential stimuli are encoded in a temporal-position manner is poorly understood. Here, we performed multiple-electrode recordings in the visual cortex (area V4) of nonhuman primates (Macaca mulatta) viewing a sequence of 7 briefly flashed natural images, and measured correlations between the cue-triggered population response in the presence and absence of the stimulus. Surprisingly, we found significant correlations for images occurring at the beginning and the end of a sequence, but not for those in the middle. The correlation strength increased with stimulus exposure and favored the image position in the sequence rather than image identity. These results challenge the commonly held view that images are represented in visual cortex exclusively based on their informational content, and indicate that, in the absence of sensory information, neuronal populations exhibit reactivation of stimulus-evoked responses in a way that reflects temporal position within a stimulus sequence. |
Ian C. Fiebelkorn; Mark A. Pinsk; Sabine Kastner A dynamic interplay within the frontoparietal network underlies rhythmic spatial attention Journal Article In: Neuron, vol. 99, no. 4, pp. 842–853.e8, 2018. @article{Fiebelkorn2018, Classic studies of spatial attention assumed that its neural and behavioral effects were continuous over time. Recent behavioral studies have instead revealed that spatial attention leads to alternating periods of heightened or diminished perceptual sensitivity. Yet, the neural basis of these rhythmic fluctuations has remained largely unknown. We show that a dynamic interplay within the macaque frontoparietal network accounts for the rhythmic properties of spatial attention. Neural oscillations characterize functional interactions between the frontal eye fields (FEF) and the lateral intraparietal area (LIP), with theta phase (3–8 Hz) coordinating two rhythmically alternating states. The first is defined by FEF-dominated beta-band activity, associated with suppressed attentional shifts, and LIP-dominated gamma-band activity, associated with enhanced visual processing and better behavioral performance. The second is defined by LIP-specific alpha-band activity, associated with attenuated visual processing and worse behavioral performance. Our findings reveal how network-level interactions organize environmental sampling into rhythmic cycles. Fiebelkorn et al. use simultaneous recordings in two hubs of the macaque frontoparietal network to demonstrate a neural basis of rhythmic sampling during spatial attention. Theta-organized, alternating attentional states, characterized by different spatiotemporal dynamics, shape environmental sampling. |
Whitney S. Griggs; Hidetoshi Amita; Atul Gopal; Okihide Hikosaka Visual neurons in the superior colliculus discriminate many objects by their historical values Journal Article In: Frontiers in Neuroscience, vol. 12, pp. 396, 2018. @article{Griggs2018, The superior colliculus (SC) is an important structure in the mammalian brain that orients the animal towards distinct visual events. Visually-responsive neurons in SC are modulated by visual object features, including size, motion, and color. However, it remains unclear whether SC activity is modulated by non-visual object features, such as the reward value associated with the object. To address this question, three monkeys were trained (>10 days) to saccade to multiple fractal objects, half of which were consistently associated with large reward while other half were associated with small reward. This created historically high-valued (‘good') and low-valued (‘bad') objects. During the neuronal recordings from the SC, the monkeys maintained fixation at the center while the objects were flashed in the receptive field of the neuron without any reward. We found that approximately half of the visual neurons responded more strongly to the good than bad objects. In some neurons, this value-coding remained intact for a long time (>1 year) after the last object-reward association learning. Notably, the neuronal discrimination of reward values started about 100 ms after the appearance of visual objects and lasted for more than 100 ms. These results provide evidence that SC neurons can discriminate objects by their historical (long-term) values. This object value information may be provided by the basal ganglia, especially the circuit originating from the tail of the caudate nucleus. The information may be used by the neural circuits inside SC for motor (saccade) output or may be sent to the circuits outside SC for future behavior. |
Marcel Jan Haan; Thomas Brochier; Sonja Grün; Alexa Riehle; Frédéric V. Barthélemy Real-time visuomotor behavior and electrophysiology recording setup for use with humans and monkeys Journal Article In: Journal of Neurophysiology, vol. 120, no. 2, pp. 539–552, 2018. @article{Haan2018a, Large-scale network dynamics in multiple visuomotor areas is of great interest in the study of eye-hand coordination in both human and monkey. To explore this, it is essential to develop a setup that allows for precise tracking of eye and hand movements. It is desirable that it is able to generate mechanical or visual perturbations of hand trajec- tories so that eye-hand coordination can be studied in a variety of conditions. There are simple solutions that satisfy these requirements for hand movements performed in the horizontal plane while visual stimuli and hand feedback are presented in the vertical plane. How- ever, this spatial dissociation requires cognitive rules for eye-hand coordination different from eye-hand movements performed in the same space, as is the case in most natural conditions. Here we present an innovative solution for the precise tracking of eye and hand movements in a single reference frame. Importantly, our solution allows behavioral explorations under normal and perturbed conditions in both humans and monkeys. It is based on the integration of two noninvasive commercially available systems to achieve online control and synchronous recording of eye (EyeLink) and hand (KINARM) positions during interactive visuomotor tasks. We also present an eye calibration method compatible with different eye trackers that com- pensates for nonlinearities caused by the system's geometry. Our setup monitors the two effectors in real time with high spatial and temporal resolution and simultaneously outputs behavioral and neu- ronal data to an external data acquisition system using a common data format. |
Christopher K. Hauser; Dantong Zhu; Terrence R. Stanford; Emilio Salinas Motor selection dynamics in FEF explain the reaction time variance of saccades to single targets Journal Article In: eLife, vol. 7, pp. 1–32, 2018. @article{Hauser2018, In studies of voluntary movement, a most elemental quantity is the reaction time (RT) between the onset of a visual stimulus and a saccade toward it. However, this RT demonstrates extremely high variability which, in spite of extensive research, remains unexplained. It is well established that, when a visual target appears, oculomotor activity gradually builds up until a critical level is reached, at which point a saccade is triggered. Here, based on computational work and single-neuron recordings from monkey frontal eye field (FEF), we show that this rise-to-threshold process starts from a dynamic initial state that already contains other incipient, internally driven motor plans, which compete with the target-driven activity to varying degrees. The ensuing conflict resolution process, which manifests in subtle covariations between baseline activity, build-up rate, and threshold, consists of fundamentally deterministic interactions, and explains the observed RT distributions while invoking only a small amount of intrinsic randomness.As we examine the space around us our eyes move in short steps, looking toward a new location about four times a second. Neurons in a region of the brain called the frontal eye field help initiate these eye movements, which are known as saccades. Each neuron contributes to a saccade with a specific direction and size. Before a saccade, the relevant neurons in the frontal eye field steadily increase their activity. When this activity reaches a critical threshold, the visual system issues a command to move the eyes in the appropriate direction. So a saccade that moves the eyes to the right requires a specific group of neurons to be strongly activated – but, at the same time, the neurons responsible for movement to the left need to be less active.Imagine that you have to move your eyes as quickly as possible to look at a spot of light that appears on a screen. Some of the time your eyes will start to move about 100 milliseconds after the light appears. But on other attempts, your eyes will not start moving until 300 milliseconds after the light came on. What causes this variability?To find out, Hauser et al. recorded from neurons in monkeys trained to perform such a task. When the spot of light appeared many different neurons were active, suggesting there is conflict between the plan that would move the eyes toward the target and plans to look at other locations. That is, when the target appears, the monkey is already thinking of looking somewhere. The time required to resolve this conflict depends on how far apart the target and the competing locations are from one another, and on how much the competing neurons have increased their activity before the target appears.Similar mechanisms are likely to operate when we sit at the dinner table and look for the salt shaker, for example, and so the results presented by Hauser et al. will help us to understand how we direct our attention to different points in space. Understanding how these processes work in more detail will help us to discern what happens when they go wrong, as occurs in attention deficit disorders like ADHD. |
Seng Bum Michael Yoo; Brianna J. Sleezer; Benjamin Y. Hayden Robust encoding of spatial information in orbitofrontal cortex and striatum Journal Article In: Journal of Cognitive Neuroscience, vol. 30, no. 6, pp. 898–913, 2018. @article{Yoo2018, Knowing whether core reward regions carry information about the positions of relevant objects is crucial for adjudicating between choice models. One limitation of previous studies, including our own, is that spatial positions can be consistently differentially associated with rewards, and thus position can be confounded with attention, motor plans, or target identity. We circumvented these problems by using a task in which value— and thus choices—was determined solely by a frequently changing rule, which was randomized relative to spatial position on each trial. We presented offers asynchronously, which allowed us to control for reward expectation, spatial attention, and motor plans in our analyses. We find robust encoding of the spatial position of both offers and choices in two core reward regions, orbitofrontal Area 13 and ventral striatum, as well as in dorsal striatum of macaques. The trial-by-trial correlation in noise in encoding of position was associated with variation in choice, an effect known as choice probability correlation, suggesting that the spatial encoding is associated with choice and is not incidental to it. Spatial information and reward information are not carried by separate sets of neurons, although the two forms of information are temporally dissociable. These results highlight the ubiquity of multiplexed information in association cortex and argue against the idea that these ostensible reward regions serve as part of a pure value domain. |
Tao Yao; Stefan Treue; B. Suresh Krishna Saccade-synchronized rapid attention shifts in macaque visual cortical area MT Journal Article In: Nature Communications, vol. 9, pp. 958, 2018. @article{Yao2018, While making saccadic eye-movements to scan a visual scene, humans and monkeys are able to keep track of relevant visual stimuli by maintaining spatial attention on them. This ability requires a shift of attentional modulation from the neuronal population representing the relevant stimulus pre-saccadically to the one representing it post-saccadically. For optimal performance, this trans-saccadic attention shift should be rapid and saccade-synchronized. Whether this is so is not known. We trained two rhesus monkeys to make saccades while maintaining covert attention at a fixed spatial location. We show that the trans-saccadic attention shift in cortical visual medial temporal (MT) area is well synchronized to saccades. Attentional modulation crosses over from the pre-saccadic to the post-saccadic neuronal representation by about 50 ms after a saccade. Taking response latency into account, the trans-saccadic attention shift is well timed to maintain spatial attention on relevant stimuli, so that they can be optimally tracked and processed across saccades. |
Sheng-Tao Yang; Min Wang; Constantinos D. Paspalas; Johanna L. Crimins; Marcus T. Altman; James A. Mazer; Amy F. T. Arnsten Core differences in synaptic signaling between primary visual and dorsolateral prefrontal cortex Journal Article In: Cerebral Cortex, vol. 28, no. 4, pp. 1458–1471, 2018. @article{Yang2018, Neurons in primary visual cortex (V1) are more resilient than those in dorsolateral prefrontal cortex (dlPFC) in aging, schizophrenia and Alzheimer's disease. The current study compared glutamate and neuromodulatory actions in macaque V1 to those in dlPFC, and found striking regional differences. V1 neuronal firing to visual stimuli depended on AMPA receptors, with subtle NMDA receptor contributions, while dlPFC depends primarily on NMDA receptors. Neuromodulatory actions also differed between regions. In V1, cAMP signaling increased neuronal firing, and the phosphodiesterase PDE4A was positioned to regulate cAMP effects on glutamate release from axons. HCN channels in V1 were classically located on distal dendrites, and enhanced cell firing. These data contrast with dlPFC, where PDE4A and HCN channels are concentrated in thin spines, and cAMP-HCN signaling gates inputs and weakens firing. These regional differences may explain why V1 neurons are more resilient than dlPFC neurons to the challenges of age and disease. |
Yin Yan; Li Zhaoping; Wu Li Bottom-up saliency and top-down learning in the primary visual cortex of monkeys Journal Article In: Proceedings of the National Academy of Sciences, vol. 115, no. 41, pp. 10499–10504, 2018. @article{Yan2018a, Early sensory cortex is better known for representing sensory inputs but less for the effect of its responses on behavior. Here we explore the behavioral correlates of neuronal responses in primary visual cortex (V1) in a task to detect a uniquely oriented bar-the orientation singleton-in a background of uniformly oriented bars. This singleton is salient or inconspicuous when the orientation contrast between the singleton and background bars is sufficiently large or small, respectively. Using implanted microelectrodes, we measured V1 activities while monkeys were trained to quickly saccade to the singleton. A neuron's responses to the singleton within its receptive field had an early and a late component, both increased with the orientation contrast. The early component started from the outset of neuronal responses; it remained unchanged before and after training on the singleton detection. The late component started ∼40 ms after the early one; it emerged and evolved with practicing the detection task. Training increased the behavioral accuracy and speed of singleton detection and increased the amount of information in the late response component about a singleton's presence or absence. Furthermore, for a given singleton, faster detection performance was associated with higher V1 responses; training increased this be-havioral-neural correlate in the early V1 responses but decreased it in the late V1 responses. Therefore, V1's early responses are directly linked with behavior and represent the bottom-up saliency signals. Learning strengthens this link, likely serving as the basis for making the detection task more reflexive and less top-down driven. |
Yang Xie; Chechang Nie; Tianming Yang Covert shift of attention modulates the value encoding in the orbitofrontal cortex Journal Article In: eLife, vol. 7, pp. 1–21, 2018. @article{Xie2018, During value-based decision making, we often evaluate the value of each option sequentially by shifting our attention, even when the options are presented simultaneously. The orbitofrontal cortex (OFC) has been suggested to encode value during value-based decision making. Yet it is not known how its activity is modulated by attention shifts. We investigated this question by employing a passive viewing task that allowed us to disentangle effects of attention, value, choice and eye movement. We found that the attention modulated OFC activity through a winner-take-all mechanism. When we attracted the monkeys' attention covertly, the OFC neuronal activity reflected the reward value of the newly attended cue. The shift of attention could be explained by a normalization model. Our results strongly argue for the hypothesis that the OFC neuronal activity represents the value of the attended item. They provide important insights toward understanding the OFC's role in value-based decision making. |
Liya Ma; Kevin J. Skoblenick; Kevin D. Johnston; Stefan Everling Ketamine alters lateral prefrontal oscillations in a rule-based working memory gask Journal Article In: Journal of Neuroscience, vol. 38, no. 10, pp. 2482–2494, 2018. @article{Ma2018a, Acute administration of N-methyl-D-aspartate receptor (NMDAR) antagonists in healthy humans and animals produces working memory deficits similar to those observed in schizophrenia. However, it is unclear whether they also lead to altered low-frequency (<=60Hz) neural oscillatory activities similar to those associated with schizophrenia during working memory processes. Here we recorded local field potentials (LFPs) and single unit activity from the lateral prefrontal cortex (LPFC) of three male rhesus macaque monkeys while they performed a rule-based prosaccade and antisaccade working memory task, both before and after systemic injections of a subanesthetic dose (<=0.7mg/kg) of ketamine. Accompanying working-memory impairment, ketamine enhanced the low gamma band (30-60Hz) and dampened the beta band (13-30Hz) oscillatory activities in the LPFC during both delay periods and inter-trial intervals. It also increased task-related alpha-band activities, likely reflecting compromised attention. Beta-band oscillations may be especially relevant to working memory processes, as stronger beta power weakly but significantly predicted shorter saccadic reaction time. Also in beta band, ketamine reduced the performance-related oscillation as well as the rule information encoded in the spectral power. Ketamine also reduced rule information in the spike-field phase consistency in almost all frequencies up to 60Hz. Our findings support NMDAR antagonists in non-human primates as a meaningful model for altered neural oscillations and synchrony, which reflect a disorganized network underlying the working memory deficits in schizophrenia. |
Kazutaka Maeda; Jun Kunimatsu; Okihide Hikosaka Amygdala activity for the modulation of goal-directed behavior in emotional contexts Journal Article In: PLoS Biology, vol. 16, no. 6, pp. e2005339, 2018. @article{Maeda2018, Choosing valuable objects and rewarding actions is critical for survival. While such choices must be made in a way that suits the animal's circumstances, the neural mechanisms underlying such context-appropriate behavior are unclear. To address this question, we devised a context-dependent reward-seeking task for macaque monkeys. Each trial started with the appearance of one of many visual scenes containing two or more objects, and the monkey had to choose the good object by saccade to get a reward. These scenes were categorized into two dimensions of emotional context: dangerous versus safe and rich versus poor. We found that many amygdala neurons were more strongly activated by dangerous scenes, by rich scenes, or by both. Furthermore, saccades to target objects occurred more quickly in dangerous than in safe scenes and were also quicker in rich than in poor scenes. Thus, amygdala neuronal activity and saccadic reaction times were negatively correlated in each monkey. These results suggest that amygdala neurons facilitate targeting saccades predictably based on aspects of emotional context, as is necessary for goal-directed and social behavior. |
Alex J. Major; Susheel Vijayraghavan; Stefan Everling Cholinergic overstimulation attenuates rule selectivity in macaque prefrontal cortex Journal Article In: Journal of Neuroscience, vol. 38, no. 5, pp. 1137–1150, 2018. @article{Major2018, Acetylcholine is released in the prefrontal cortex (PFC) and is a key modulator of cognitive performance in primates. Cholinergic stimulation has been shown to have beneficial effects on performance of cognitive tasks, and cholinergic receptors are being actively explored as promising targets for ameliorating cognitive deficits in Alzheimer's disease.Wehypothesized that cholinergic stimulation of PFC during performance of a cognitive task would augment neuronal activity and neuronal coding of task attributes. We iontophoretically applied the general cholinergic receptor agonist carbachol onto neurons in dorsolateral PFC (DLPFC) of male rhesus macaques performing rule-guided prosaccades and antisaccades, a well established oculomotor task for testing cognitive control. Carbachol application had heterogeneous effects on neuronal excitability, with both excitation and suppression observed in significant proportions. Contrary to our prediction, neurons with rule-selective activity exhibited a reduction in selectivity during carbachol application. Cholinergic stimulation disrupted rule selectivity regardless of whether it had suppressive or excitatory effects on these neurons. In addition, cholinergic stimulation excited putative pyramidal neurons, whereas the activity of putative interneurons remained unchanged. Moreover, cholinergic stimulation attenuated saccade direction selectivity in putative pyramidal neurons due to nonspecific increases in activity. Our results suggest excessive cholinergic stimulation has detrimental effects on DLPFC representations of task attributes. These findings delineate the complexity and heterogeneity of neuromodulation of cerebral cortex by cholinergic stimulation, an area of active exploration with respect to the development of cognitive enhancers. |
Alexandria C. Marino; James A. Mazer Saccades trigger predictive updating of attentional topography in area V4 Journal Article In: Neuron, vol. 98, no. 2, pp. 429–438.e4, 2018. @article{Marino2018, During natural behavior, saccades and attention act together to allocate limited neural resources. Attention is generally mediated by retinotopic visual neurons; therefore, specific neurons representing attended features change with each saccade. We investigated the neural mechanisms that allow attentional targeting in the face of saccades. Specifically, we looked for predictive changes in attentional modulation state or receptive field position that could stabilize attentional representations across saccades in area V4, known to be necessary for attention-dependent behavior. We recorded from neurons in monkeys performing a novel spatiotopic attention task, in which performance depended on accurate saccade compensation. Measurements of attentional modulation revealed a predictive attentional “hand-off” corresponding to a presaccadic transfer of attentional state from neurons inside the attentional focus before the saccade to those that will be inside the focus after the saccade. The predictive nature of the hand-off ensures that attentional brain maps are properly configured immediately after each saccade. Using a novel behavioral task, Marino and Mazer report that the attentional modulation state of neurons in extrastriate area V4 is updated before saccade onset. This attentional hand-off is independent of changes in receptive field position and represents a new type of perisaccadic updating. |
Adam Pallus; Mark M. G. Walton; Michael J. Mustari Activity of near-response cells during disconjugate saccades in strabismic monkeys Journal Article In: Journal of Neurophysiology, vol. 120, no. 5, pp. 2282–2295, 2018. @article{Pallus2018, Infantile strabismus is a common disorder characterized by a chronic misalignment of the eyes, impairment of binocular vision, and oculomotor abnormalities. Nonhuman primates with strabismus, induced in infancy, show a pattern of abnormalities similar to those of strabismic children. This allows strabismic nonhuman primates to serve as an ideal animal model to examine neural mechanisms associated with aberrant oculomotor behavior. Here, we test the hypothesis that impairment of disparity vergence and horizontal saccade disconjugacy in exotropia and esotropia are associated with disrupted tuning of near-and far-response neurons in the supraoculomotor area (SOA). In normal animals, these neurons carry signals related to vergence position and/or velocity. We hypothesized that, in strabismus, these neurons modulate inappropriately in association with saccades between equidistant targets. We recorded from 62 SOA neurons from 4 strabismic animals (2 esotropes and 2 exotropes) during visually guided saccades to a target that stepped to different locations on a tangent screen. Under these same conditions, SOA neurons in normal animals show no detectable modulation. In our strabismic subjects, we found that a subset of SOA neurons carry weak vergence velocity signals during saccades. In addition, a subset of SOA neurons showed clear modulation associated with slow fluctuations of horizontal strabismus angle in the absence of a saccade. We suggest that abnormal SOA activity contributes to fixation instability but plays only a minor role in the horizontal disconjugacy of saccades that do not switch fixation from one eye to the other. NEW & NOTEWORTHY The present study is the first to investigate the activity of neurons in the supraoculomotor area (SOA) during horizontally disconjugate saccades in a nonhuman primate model of infantile strabismus. We report that fluctuations of horizontal strabismus angle, during fixation of static targets on a tangent screen, are associated with contextually inappropriate modulation of SOA activity. However, firing rate modulation during saccades is too weak to make a major contribution to horizontal disconjugacy. |
Angelo Pirrone; Habiba Azab; Benjamin Y. Hayden; Tom Stafford; James A. R. Marshall Evidence for the speed–value trade-Off: Human and monkey decision making Is magnitude sensitive Journal Article In: Decision, vol. 5, no. 2, pp. 129–142, 2018. @article{Pirrone2018, Complex natural systems from brains to bee swarms have evolved to make adaptive multifactorial decisions. Recent theoretical and empirical work suggests that many evolved systems may take advantage of common motifs across multiple domains. We are particularly interested in value sensitivity (i.e., sensitivity to the magnitude or intensity of the stimuli or reward under consideration) as a mechanism to resolve deadlocks adaptively. This mechanism favors long-term reward maximization over accuracy in a simple manner, because it avoids costly delays associated with ambivalence between similar options; speed–value trade-offs have been proposed to be evolutionarily advantageous for many kinds of decision. A key prediction of the value-sensitivity hypothesis is that choices between equally valued options will proceed faster when the options have a high value than when they have a low value. However, value sensitivity is not part of idealized choice models such as diffusion to bound. Here, we examine 2 different choice behaviors in 2 different species, perceptual decisions in humans and economic choices in rhesus monkeys, to test this hypothesis. We observe the same value sensitivity in both human perceptual decisions and monkey value-based decisions. These results endorse the idea that neural decision systems make use of the same basic principle of value sensitivity in order to resolve costly deadlocks and thus improve long-term reward intake. |
Evan D. Remington; Devika Narain; Eghbal A. Hosseini; Mehrdad Jazayeri Flexible sensorimotor computations through rapid reconfiguration of cortical dynamics Journal Article In: Neuron, vol. 98, no. 5, pp. 1005–1019.e5, 2018. @article{Remington2018a, Neural mechanisms that support flexible sensorimotor computations are not well understood. In a dynamical system whose state is determined by interactions among neurons, computations can be rapidly reconfigured by controlling the system's inputs and initial conditions. To investigate whether the brain employs such control mechanisms, we recorded from the dorsomedial frontal cortex of monkeys trained to measure and produce time intervals in two sensorimotor contexts. The geometry of neural trajectories during the production epoch was consistent with a mechanism wherein the measured interval and sensorimotor context exerted control over cortical dynamics by adjusting the system's initial condition and input, respectively. These adjustments, in turn, set the speed at which activity evolved in the production epoch, allowing the animal to flexibly produce different time intervals. These results provide evidence that the language of dynamical systems can be used to parsimoniously link brain activity to sensorimotor computations. Remington et al. employ a dynamical systems perspective to understand how the brain flexibly controls timed movements. Results suggest that neurons in the frontal cortex form a recurrent network whose behavior is flexibly controlled by inputs and initial conditions. |
Thomas R. Reppert; Mathieu Servant; Richard P. Heitz; Jeffrey D. Schall In: Journal of Neurophysiology, vol. 120, no. 1, pp. 372–384, 2018. @article{Reppert2018, Balancing the speed-accuracy tradeoff (SAT) is necessary for successful behavior. Using a visual search task with interleaved cues emphasizing speed or accuracy, we recently reported diverse contributions of frontal eye field (FEF) neurons instantiating salience evidence and response preparation. Here, we report replication of visual search SAT performance in two macaque monkeys, new information about variation of saccade dynamics with SAT, extension of the neurophysiological investigation to describe processes in the superior colliculus (SC), and a description of the origin of search errors in this task. Saccade vigor varied idiosyncratically across SAT conditions and monkeys but tended to decrease with response time. As observed in the FEF, speed-accuracy tradeoff was accomplished through several distinct adjustments in the superior colliculus. In “Accurate” relative to “Fast” trials, visually responsive neurons in SC as in FEF had lower baseline firing rates and later target selection. The magnitude of these adjustments in SC was indistinguishable from that in FEF. Search errors occurred when visual salience neurons in the FEF and the SC treated distractors as targets, even in the Accurate condition. Unlike FEF, the magnitude of visual responses in the SC did not vary across SAT conditions. Also unlike FEF, the activity of SC movement neurons when saccades were initiated was equivalent in Fast and Accurate trials. Saccade-related neural activity in SC, but not FEF, varied with saccade peak velocity. These results extend our understanding of the cortical and subcortical contributions to SAT. |
Douglas A. Ruff; David H. Brainard; Marlene R. Cohen Neuronal population mechanisms of lightness perception Journal Article In: Journal of Neurophysiology, vol. 120, no. 5, pp. 2296–2310, 2018. @article{Ruff2018, The way that humans and animals perceive the lightness of an object depends on its physical luminance as well as its surrounding context. While neuronal responses throughout the visual pathway are modulated by context, the relationship between neuronal responses and lightness perception is poorly understood. We searched for a neuronal mechanism of lightness by recording responses of neuronal populations in monkey primary visual cortex (V1) and area V4 to stimuli that produce a lightness illusion in humans, in which the lightness of a disk depends on the context in which it is embedded. We found that the way individual units encode the luminance (or equivalently for our stimuli, contrast) of the disk and its context is extremely heterogeneous. This motivated us to ask whether the population representation in either V1 or V4 satisfies three criteria: 1) disk luminance is represented with high fidelity, 2) the context surrounding the disk is also represented, and 3) the representations of disk luminance and context interact to create a representation of lightness that depends on these factors in a manner consistent with human psychophysical judgments of disk lightness. We found that populations of units in both V1 and V4 fulfill the first two criteria, but that we cannot conclude that the two types of information in either area interact in a manner that clearly predicts human psychophysical measurements: the interpretation of our population measurements depends on how subsequent areas read out lightness from the population responses. |
Jason M. Samonds; Wilson S. Geisler; Nicholas J. Priebe Natural image and receptive field statistics predict saccade sizes Journal Article In: Nature Neuroscience, vol. 21, no. 11, pp. 1591–1599, 2018. @article{Samonds2018, Humans and other primates sample the visual environment using saccadic eye movements that shift a high-resolution fovea toward regions of interest to create a clear perception of a scene across fixations. Many mammals, however, like mice, lack a fovea, which raises the question of why they make saccades. Here we describe and test the hypothesis that saccades are matched to natural scene statistics and to the receptive field sizes and adaptive properties of neural populations. Specifically, we determined the minimum amplitude of saccades in natural scenes necessary to provide uncorrelated inputs to model neural populations. This analysis predicts the distributions of observed saccade sizes during passive viewing for nonhuman primates, cats, and mice. Furthermore, disrupting the development of receptive field properties by monocular deprivation changed saccade sizes consistent with this hypothesis. Therefore, natural-scene statistics and the neural representation of natural images appear to be critical factors guiding saccadic eye movements. |
Yaser Merrikhi; Kelsey Clark; Behrad Noudoost Concurrent influence of top-down and bottom-up inputs on correlated activity of Macaque extrastriate neurons Journal Article In: Nature Communications, vol. 9, pp. 5393, 2018. @article{Merrikhi2018, Correlations between neurons can profoundly impact the information encoding capacity of a neural population. We studied how maintenance of visuospatial information affects correlated activity in visual areas by recording the activity of neurons in visual area MT of rhesus macaques during a spatial working memory task. Correlations between MT neurons depended upon the spatial overlap between neurons' receptive fields. These correlations were influenced by the content of working memory, but the effect of a top-down memory signal differed in the presence or absence of bottom-up visual input. Neurons representing the same area of space showed increased correlations when remembering a location in their receptive fields in the absence of visual input, but decreased correlations in the presence of a visual stimulus. This set of results reveals the correlating nature of top-down signals influencing visual areas and uncovers how such a correlating signal, in interaction with bottom-up information, could enhance sensory representations. |
Jérôme Munuera; Mattia Rigotti; C. Daniel Salzman Shared neural coding for social hierarchy and reward value in primate amygdala Journal Article In: Nature Neuroscience, vol. 21, no. 3, pp. 415–423, 2018. @article{Munuera2018, The social brain hypothesis posits that dedicated neural systems process social information. In support of this, neurophysiological data have shown that some brain regions are specialized for representing faces. It remains unknown, however, whether distinct anatomical substrates also represent more complex social variables, such as the hierarchical rank of individuals within a social group. Here we show that the primate amygdala encodes the hierarchical rank of individuals in the same neuronal ensembles that encode the rewards associated with nonsocial stimuli. By contrast, orbitofrontal and anterior cingulate cortices lack strong representations of hierarchical rank while still representing reward values. These results challenge the conventional view that dedicated neural systems process social information. Instead, information about hierarchical rank—which contributes to the assessment of the social value of individuals within a group—is linked in the amygdala to representations of rewards associated with nonsocial stimuli. |
James E. Niemeyer; Michael A. Paradiso Saccade-based termination responses in macaque V1 and visual perception Journal Article In: Visual Neuroscience, vol. 35, pp. e025, 2018. @article{Niemeyer2018, Neurons in visual areas of the brain are generally characterized by the increase in firing rate that occurs when a stimulus is flashed on in the receptive field (RF). However, neurons also increase their firing rate when a stimulus is turned off. These “termination responses” or “after-discharges” that occur with flashed stimuli have been observed in area V1 and they may be important for vision as stimulus terminations have been shown to influence visual perception. The goal of the present study was to determine the strength of termination responses in the more natural situation in which eye movements move a stimulus out of an RF. We find that termination responses do occur in macaque V1 when termination results from a saccadic eye movement, but they are smaller in amplitude compared to flashed-off stimuli. Furthermore, there are termination responses even in the absence of visual stimulation. These findings demonstrate that termination responses are a component of naturalistic vision. They appear to be based on both visual and nonvisual signals in visual cortex. We speculate that the weakening of termination responses might be a neural correlate of saccadic suppression, the loss of perceptual sensitivity around the time of saccades. |
Atsushi Noritake; Taihei Ninomiya; Masaki Isoda Social reward monitoring and valuation in the macaque brain Journal Article In: Nature Neuroscience, vol. 21, no. 10, pp. 1452–1462, 2018. @article{Noritake2018, Behaviors are influenced by rewards to both oneself and others, but the neurons and neural connections that monitor and evaluate rewards in social contexts are unknown. To address this issue, we devised a social Pavlovian conditioning procedure for pairs of monkeys. Despite being constant in amount and probability, the subjective value of forthcoming self-rewards, as indexed by licking and choice behaviors, decreased as partner-reward probability increased. This value modulation was absent when the conspecific partner was replaced by a physical object. Medial prefrontal cortex neurons selectively monitored self-reward and partner-reward information, whereas midbrain dopaminergic neurons integrated this information into a subjective value. Recordings of local field potentials revealed that responses to reward-predictive stimuli in medial prefrontal cortex started before those in dopaminergic midbrain nuclei and that neural information flowed predominantly in a medial prefrontal cortex-to-midbrain direction. These findings delineate a dedicated pathway for subjective reward evaluation in social environments. |
Takaya Ogasawara; Masafumi Nejime; Masahiko Takada; Masayuki Matsumoto Primate nigrostriatal dopamine system regulates saccadic response inhibition Journal Article In: Neuron, vol. 100, no. 6, pp. 1513–1526.e4, 2018. @article{Ogasawara2018, Animals need to inhibit inappropriate actions that would lead to unwanted outcomes. Although this ability, called response inhibition, is impaired in neurological/psychiatric disorders with dopaminergic dysfunctions, how dopamine regulates response inhibition remains unclear. Here we investigated neuronal signals of the nigrostriatal dopamine system in monkeys performing a saccadic countermanding task. Subsets of dopamine neurons in the substantia nigra and striatal neurons receiving the dopaminergic input were activated when the monkey was required to cancel a planned saccadic eye movement. These activations were stronger when canceling the eye movements was successful compared with failed and were enhanced in demanding trials. The activated dopamine neurons were distributed mainly in the dorsolateral, but not in the ventromedial, part of the nigra. Furthermore, pharmacological blockade of dopaminergic neurotransmission in the striatum dampened the performance of canceling saccadic eye movements. The present findings indicate that disruption of nigrostriatal dopamine signaling causes impairments in response inhibition. |
Timothy D. Oleskiw; Amy Nowack; Anitha Pasupathy Joint coding of shape and blur in area V4 Journal Article In: Nature Communications, vol. 9, pp. 466, 2018. @article{Oleskiw2018, Edge blur, a prevalent feature of natural images, is believed to facilitate multiple visual processes including segmentation and depth perception. Furthermore, image descriptions that explicitly combine blur and shape information provide complete representations of naturalistic scenes. Here we report the first demonstration of blur encoding in primate visual cortex: neurons in macaque V4 exhibit tuning for both object shape and boundary blur, with observed blur tuning not explained by potential confounds including stimulus size, intensity, or curvature. A descriptive model wherein blur selectivity is cast as a distinct neural process that modulates the gain of shape-selective V4 neurons explains observed data, supporting the hypothesis that shape and blur are fundamental features of a sufficient neural code for natural image representation in V4. |
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. |
Masato Inoue; Shigeru Kitazawa Motor error in parietal area 5 and target error in area 7 drive distinctive adaptation in reaching Journal Article In: Current Biology, vol. 28, pp. 2250–2262, 2018. @article{Inoue2018, Errors in reaching drive trial-by-trial adaptation to compensate for the error. Parietal association areas are implicated in error coding, but whether the parietal error signals directly drive adaptation remains unknown. We first examined the activity of neurons in areas 5 and 7 while two monkeys performed rapid target reaching to clarify whether and how the parietal error signals drive adaptation in reaching. We introduced random errors using a motor-driven prism device to augment random motor errors in reaching. Neurons in both regions encoded information on the target position prior to reaching and information on the motor error after reaching. However, post-movement microstimulation caused trial-by-trial adaptation to cancel the motor error only when it was delivered to area 5. By contrast, stimulation to area 7 caused trial-by-trial adaptation so that the reaching endpoint was adjusted toward the target position. We further hypothesized that area 7 would encode target error that is caused by a target jump during the reach, and our results support this hypothesis. Area 7 neurons encoded target error information, but area 5 neurons did not encode this information. These results suggest that area 5 provides signals for adapting to motor errors and that area 7 provides signals to adapt to target errors. |
Kevin D. Johnston; Kevin Barker; David J. Schaeffer; Lauren Schaeffer; Stefan Everling Methods for chair restraint and training of the common marmoset on oculomotor tasks Journal Article In: Journal of Neurophysiology, vol. 119, no. 5, pp. 1636–1646, 2018. @article{Johnston2018, The oculomotor system is the most thoroughly understood sensorimotor system in the brain, due in large part to electrophysiological studies carried out in macaque monkeys trained to perform oculomotor tasks. A disadvantage of the macaque model is that many cortical oculomotor areas of interest lie within sulci, making high-density array and laminar recordings impractical. Many techniques of molecular biology developed in rodents, such as optogenetic manipulation of neuronal subtypes, are also limited in this species. The common marmoset (Callithrix jacchus) possesses a smooth cortex, allowing easy access to frontoparietal oculomotor areas, and may bridge the gap between systems neuroscience in macaques and molecular techniques. Techniques for restraint, training, and neural recording in these animals have been well developed in auditory neuroscience. Those for oculomotor neuroscience, however, remain at a relatively early stage. In this article we provide details of a custom-designed restraint chair for marmosets, a combination head restraint/recording chamber allowing access to cortical oculomotor areas and providing stability suitable for eye movement and neural recordings, as well as a training protocol for oculomotor tasks. We additionally report the results of a psychophysical study in marmosets trained to perform a saccade task using these methods, showing that, as in rhesus and humans, marmosets exhibit a “gap effect,” a decrease in reaction time when the fixation stimulus is removed before the onset of a visual saccade target. These results are the first evidence of this effect in marmosets and support the common marmoset model for neurophysiological investigations of oculomotor control. |
Peter Kaposvari; Susheel Kumar; Rufin Vogels Statistical learning signals in macaque inferior temporal cortex Journal Article In: Cerebral Cortex, vol. 28, no. 1, pp. 250–266, 2018. @article{Kaposvari2018, Humans are sensitive to statistical regularities in their visual environment, but the nature of the underlying neural statistical learning signals still remains to be clarified. As in human behavioral and neuroimaging studies of statistical learning, we exposed rhesus monkeys to a continuous stream of images, presented without interstimulus interval or reward association. The stimulus set consisted of 3 groups of 5 images each (quintets). The stimulus order within each quintet was fixed, but the quintets were presented repeatedly in a random order without interruption. Thus, only transitional probabilities defined quintets of images. Postexposure recordings in inferior temporal (IT) cortex showed an enhanced response to stimuli that violated the exposed sequence. This enhancement was found only for stimuli that were not predicted by the just preceding stimulus, reflecting a temporally adjacent stimulus relationship, and was sensitive to stimulus order. By comparing IT responses with sequences with and without statistical regularities, we observed a short latency, transient response suppression for stimuli of the sequence with regularities, in addition to a later sustained response enhancement to stimuli that violated the sequence with regularities. These findings constrain models of mechanisms underlying neural responses in predictable temporal sequences, such as predictive coding. |
Katsuhisa Kawaguchi; Stephane Clery; Paria Pourriahi; Lenka Seillier; Ralf M. Haefner; Hendrikje Nienborg Differentiating between models of perceptual decision making using pupil size inferred confidence Journal Article In: Journal of Neuroscience, vol. 38, no. 41, pp. 8874–8888, 2018. @article{Kawaguchi2018, During perceptual decisions, subjects often rely more strongly on early, rather than late, sensory evidence, even in tasks when both are equally informative about the correct decision. This early psychophysical weighting has been explained by an integration-to-bound decision process, in which the stimulus is ignored after the accumulated evidence reaches a certain bound, or confidence level. Here, we derive predictions about how the average temporal weighting of the evidence depends on a subject's decision confidence in this model. To test these predictions empirically, we devised a method to infer decision confidence from pupil size in 2 male monkeys performing a disparity discrimination task. Our animals' data confirmed the integration-to-bound predictions, with different internal decision bounds and different levels of correlation between pupil size and decision confidence accounting for differences between animals. However, the data were less compatible with two alternative accounts for early psychophysical weighting: attractor dynamics either within the decision area or due to feedback to sensory areas, or a feedforward account due to neuronal response adaptation. This approach also opens the door to using confidence more broadly when studying the neural basis of decision making. |
Jonas Knöll; Jonathan W. Pillow; Alexander C. Huk Lawful tracking of visual motion in humans, macaques, and marmosets in a naturalistic, continuous, and untrained behavioral context Journal Article In: Proceedings of the National Academy of Sciences, vol. 115, no. 44, pp. E10486–E10494, 2018. @article{Knoell2018, Much study of the visual system has focused on how humans and monkeys integrate moving stimuli over space and time. Such assessments of spatiotemporal integration provide fundamental grounding for the interpretation of neurophysiological data, as well as how the resulting neural signals support perceptual deci- sions and behavior. However, the insights supported by classical characterizations of integration performed in humans and rhesus monkeys are potentially limited with respect to both generality and detail: Standard tasks require extensive amounts of training, involve abstract stimulus–response mappings, and depend on combining data across many trials and/or sessions. It is thus of concern that the integration observed in classical tasks involves the recruitment of brain circuits that might not normally subsume natural behaviors, and that quantitative analyses have limited power for characterizing single-trial or single-session processes. Here we bridge these gaps by showing that three primate species (humans, macaques, and marmosets) track the focus of expansion of an optic flow field continuously and without substantial training. This flow-tracking behavior was volitional and reflected substantial temporal integration. Most strikingly, gaze patterns exhibited lawful and nuanced dependencies on random perturbations in the stimulus, such that repetitions of identical flow movies elicited remarkably similar eye movements over long and continuous time periods. These results demonstrate the generality of spatiotemporal integration in natural vision, and offer a means for studying integration outside of artificial tasks while maintaining lawful and highly reliable behavior. |
Matthew L. Leavitt; Florian Pieper; Adam J. Sachs; Julio C. Martinez-Trujillo A quadrantic bias in prefrontal representation of visual-mnemonic space Journal Article In: Cerebral Cortex, vol. 28, no. 7, pp. 2405–2421, 2018. @article{Leavitt2018, Single neurons in primate dorsolateral prefrontal cortex (dLPFC) are known to encode working memory (WM) representations of visual space. Psychophysical studies have shown that the horizontal and vertical meridians of the visual field can bias spatial information maintained in WM. However, most studies and models have tacitly assumed that dLPFC neurons represent mnemonic space homogenously. The anatomical organization of these representations has also eluded clear parametric description. We investigated these issues by recording from neuronal ensembles in macaque dLPFC with microelectrode arrays while subjects performed an oculomotor delayed-response task. We found that spatial WM representations in macaque dLPFC are biased by the vertical and horizontal meridians of the visual field, dividing mnemonic space into quadrants. This bias is reflected in single neuron firing rates, neuronal ensemble representations, the spike count correlation structure, and eye movement patterns. We also found that dLPFC representations of mnemonic space cluster anatomically in a nonretinotopic manner that partially reflects the organization of visual space. These results provide an explanation for known WM biases, and reveal novel principles of WM representation in prefrontal neuronal ensembles and across the cortical surface, as well as the need to reconceptualize models of WM to accommodate the observed representational biases. |