Rosa Lafer-sousa; Karen Wang; Reza Azadi; Emily Lopez; Simon Bohn; Arash Afraz
Behavioral detectability of optogenetic stimulation of inferior temporal cortex varies with the size of concurrently viewed objects Journal Article
In: Current Research in Neurobiology, vol. 4, pp. 1–7, 2023.
We have previously demonstrated that macaque monkeys can behaviorally detect a subtle optogenetic impulse delivered to their inferior temporal (IT) cortex. We have also shown that the ability to detect the cortical stimulation impulse varies depending on some characteristics of the visual images viewed at the time of brain stimulation, revealing the visual nature of the perceptual events induced by stimulation of the IT cortex. Here we systematically studied the effect of the size of viewed objects on behavioral detectability of optogenetic stimulation of the central IT cortex. Surprisingly, we found that behavioral detection of the same optogenetic impulse highly varies with the size of the viewed object images. Reduction of the object size in four steps from 8 to 1 degree of visual angle significantly decreased detection performance. These results show that identical stimulation impulses delivered to the same neural population induce variable perceptual events depending on the mere size of the objects viewed at the time of brain stimulation. 1.
Lara Merken; Maarten Schelles; Frederik Ceyssens; Michael Kraft; Peter Janssen
Thin flexible arrays for long-term multi-electrode recordings in macaque primary visual cortex Journal Article
In: Journal of Neural Engineering, pp. 1–14, 2022.
Objective. Basic, translational and clinical neuroscience are increasingly focusing on large-scale invasive recordings of neuronal activity. However, in large animals such as nonhuman primates and humans – in which the larger brain size with sulci and gyri imposes additional challenges compared to rodents, there is a huge unmet need to record from hundreds of neurons simultaneously anywhere in the brain for long periods of time. Here, we tested the electrical and mechanical properties of thin, flexible multi-electrode arrays inserted into the primary visual cortex of two macaque monkeys, and assessed their Magnetic Resonance Imaging (MRI) compatibility and their capacity to record extracellular activity over a period of 1 year. Approach. To allow insertion of the floating arrays into the visual cortex, the 20 by 100 µm2 shafts were temporarily strengthened by means of a resorbable poly(lactic-co-glycolic acid) (PLGA) coating. Main results. After manual insertion of the arrays, the ex vivo and in vivo MRI compatibility of the arrays proved to be excellent. We recorded clear single-unit activity (SUA) from up to 50% of the electrodes, and multi-unit activity (MUA) on 60-100% of the electrodes, which allowed detailed measurements of the receptive fields and the orientation selectivity of the neurons. Even 1 year after insertion, we obtained significant MUA responses on 70-100% of the electrodes, while the receptive fields remained remarkably stable over the entire recording period. Significance. Thus, the thin and flexible multielectrode arrays we tested offer several crucial advantages compared to existing arrays, most notably in terms of brain tissue compliance, scalability, and brain coverage. Future brain-machine interface applications in humans may strongly benefit from this new generation of chronically implanted multi-electrode arrays.
Yang Zhou; Krithika Mohan; David J. Freedman
Abstract encoding of categorical decisions in medial superior temporal and lateral intraparietal cortices Journal Article
In: Journal of Neuroscience, vol. 42, no. 48, pp. 9069–9081, 2022.
Categorization is an essential cognitive and perceptual process for decision making and recognition. The posterior parietal cortex (PPC), particularly the lateral intraparietal (LIP) area has been suggested to transform visual feature encoding into abstract categorical representations. By contrast, areas closer to sensory input, such as the middle temporal (MT) area, encode stimulus features but not more abstract categorical information during categorization tasks. Here, we compare the contributions of the medial superior temporal (MST) and LIP areas in category computation by recording neuronal activity in both areas from two male rhesus macaques trained to perform a visual motion categorization task. MST is a core motion processing area interconnected with MT, and often considered an intermediate processing stage between MT and LIP. Here we show that MST exhibits robust decision-correlated motion category encoding and working memory encoding similar to LIP, suggesting that MST plays a substantial role in cognitive computation, extending beyond its widely recognized role in visual motion processing. SIGNIFICANCE STATEMENT: Categorization requires assigning incoming sensory stimuli into behaviorally relevant groups. Previous work found that parietal area LIP shows a strong encoding of the learned category membership of visual motion stimuli, while visual area MT shows strong direction tuning but not category tuning during a motion direction categorization task. Here we show that area MST, a visual motion processing area interconnected with both LIP and MT, shows strong visual category encoding similar to that observed in LIP. This suggests that MST plays a greater role in abstract cognitive functions, extending beyond it well known role in visual motion processing.
Sébastien Tremblay; Camille Testard; Ron W. Ditullio; Jeanne Inchauspé; Michael Petrides
Neural cognitive signals during spontaneous movements in the macaque Journal Article
In: Nature Neuroscience, pp. 1–19, 2022.
The single neuron basis of cognitive processing in primates has mostly been studied in laboratory settings where movements are severely restricted. It is unclear, therefore, how natural movements might affect neural signatures of cognition in the brain. Moreover, studies in mice indicate that body movements, when measured, account for most of the neural dynamics in the cortex. To examine this issue, we recorded from single neuron ensembles in the prefrontal cortex in moving monkeys performing a cognitive task and characterized eyes, head, and body movements using video tracking. Despite significant trial-to-trial movement variability, single neuron tuning could be precisely measured and decision signals accurately decoded on a single-trial basis. Creating or abolishing spontaneous movements through head restraint and task manipulations had no measurable impact on neural responses. However, encoding models showed that uninstructed movements explained as much neural variance as task variables, with most of them aligned to task events. These results demonstrate that cognitive signals in the cortex are robust to natural movements, but also that unmeasured movements are potential confounds in cognitive neurophysiology experiments.
Cem Uran; Alina Peter; Andreea Lazar; William Barnes; Johanna Klon-Lipok; Katharine A. Shapcott; Rasmus Roese; Pascal Fries; Wolf Singer; Martin Vinck
Predictive coding of natural images by V1 firing rates and rhythmic synchronization Journal Article
In: Neuron, vol. 110, no. 7, pp. 1240–1257, 2022.
Predictive coding is an important candidate theory of self-supervised learning in the brain. Its central idea is that sensory responses result from comparisons between bottom-up inputs and contextual predictions, a process in which rates and synchronization may play distinct roles. We recorded from awake macaque V1 and developed a technique to quantify stimulus predictability for natural images based on self-supervised, generative neural networks. We find that neuronal firing rates were mainly modulated by the contextual predictability of higher-order image features, which correlated strongly with human perceptual similarity judgments. By contrast, V1 gamma ($gamma$)-synchronization increased monotonically with the contextual predictability of low-level image features and emerged exclusively for larger stimuli. Consequently, $gamma$-synchronization was induced by natural images that are highly compressible and low-dimensional. Natural stimuli with low predictability induced prominent, late-onset beta ($beta$)-synchronization, likely reflecting cortical feedback. Our findings reveal distinct roles of synchronization and firing rates in the predictive coding of natural images.
Elena N. Waidmann; Kenji W. Koyano; Julie J. Hong; Brian E. Russ; David A. Leopold
Local features drive identity responses in macaque anterior face patches Journal Article
In: Nature Communications, vol. 13, no. 1, pp. 1–13, 2022.
Humans and other primates recognize one another in part based on unique structural details of the face, including both local features and their spatial configuration within the head and body. Visual analysis of the face is supported by specialized regions of the primate cerebral cortex, which in macaques are commonly known as face patches. Here we ask whether the responses of neurons in anterior face patches, thought to encode face identity, are more strongly driven by local or holistic facial structure. We created stimuli consisting of recombinant photorealistic images of macaques, where we interchanged the eyes, mouth, head, and body between individuals. Unexpectedly, neurons in the anterior medial (AM) and anterior fundus (AF) face patches were predominantly tuned to local facial features, with minimal neural selectivity for feature combinations. These findings indicate that the high-level structural encoding of face identity rests upon populations of neurons specialized for local features.
Chin-an Wang; Brian White; Douglas P. Munoz
Pupil-linked arousal signals in the midbrain superior colliculus Journal Article
In: Journal of Cognitive Neuroscience, vol. 34, no. 8, pp. 1340–1354, 2022.
The orienting response evoked by the appearance of a salient stimulus is modulated by arousal; however, neural under- pinnings for the interplay between orienting and arousal are not well understood. The superior colliculus (SC), causally involved in multiple components of the orienting response including gaze and attention shifts, receives not only multisensory and cognitive inputs but also arousal-regulated inputs from various cortical and subcortical structures. To investigate the impact of moment-by-moment fluctuations in arousal on orienting saccade responses, we used microstimulation of the monkey SC to trigger saccade responses, and we used pupil size and velocity to index the level ofarousal at stimulation onset because these measures correlate with changes in brain states and locus coeruleus activity. Saccades induced by SC microstimulation correlated with prestimulation pupil velocity, with higher pupil velocities on trials without evoked saccades than with evoked saccades. In contrast, prestimulation absolute pupil size did not correlate with saccade behavior. Moreover, pupil velocity correlated with evoked saccade latency and metrics. Together, our results demonstrated that small fluctuations in arousal, indexed by pupil velocity, can modulate the saccade response evoked by SC microstimulation in awake behaving monkeys.
Maya Zhe Wang; Benjamin Y. Hayden; Sarah R. Heilbronner
A structural and functional subdivision in central orbitofrontal cortex Journal Article
In: Nature Communications, vol. 13, no. 1, pp. 1–12, 2022.
Economic choice requires many cognitive subprocesses, including stimulus detection, valuation, motor output, and outcome monitoring; many of these subprocesses are associated with the central orbitofrontal cortex (cOFC). Prior work has largely assumed that the cOFC is a single region with a single function. Here, we challenge that unified view with convergent anatomical and physiological results from rhesus macaques. Anatomically, we show that the cOFC can be subdivided according to its much stronger (medial) or weaker (lateral) bidirectional anatomical connectivity with the posterior cingulate cortex (PCC). We call these subregions cOFCm and cOFCl, respectively. These two subregions have notable functional differences. Specifically, cOFCm shows enhanced functional connectivity with PCC, as indicated by both spike-field coherence and mutual information. The cOFCm-PCC circuit, but not the cOFCl-PCC circuit, shows signatures of relaying choice signals from a non-spatial comparison framework to a spatially framed organization and shows a putative bidirectional mutually excitatory pattern.
Taylor D. Webb; Matthew G. Wilson; Henrik Odéen; Jan Kubanek
Remus: System for remote deep brain interventions Journal Article
In: iScience, vol. 25, no. 11, pp. 1–13, 2022.
Transcranial-focused ultrasound brings personalized medicine to the human brain. Ultrasound can modulate neural activity or release drugs in specific neural circuits but this personalized approach requires a system that delivers ultrasound into specified targets flexibly and on command. We developed a remote ultrasound system (Remus) that programmatically targets deep brain regions with high spatiotemporal precision and in a multi-focal manner. We validated these functions by modulating two deep brain nuclei—the left and right lateral geniculate nucleus—in a task-performing nonhuman primate. This flexible system will enable researchers and clinicians to diagnose and treat specific deep brain circuits in a noninvasive yet targeted manner, thus embodying the promise of personalized treatments of brain disorders.
Hannah B. Weinberg-Wolf; Nick Fagan; Olga Dal Monte; Steve W. C. Chang
Increasing central serotonin with 5-hydroxytryptophan disrupts the inhibition of social gaze in nonhuman primates Journal Article
In: Journal of Neuroscience, vol. 42, no. 4, pp. 670–681, 2022.
To competently navigate the world, individuals must flexibly balance distinct aspects of social gaze, orienting toward others and inhibiting orienting responses, depending on the context. These behaviors are often disrupted amongst patient populations treated with serotonergic drugs. However, those in the field lack a clear understanding of how the serotonergic system mediates social orienting and inhibiting behaviors. Here, we tested how increasing central concentrations of serotonin with the direct precursor 5-hydroxytryptophan (5-HTP) would modulate the ability of rhesus macaques (both sexes) to use eye movements to flexibly orient to, or inhibit orienting to, faces. Systemic administrations of 5-HTP effectively increased central serotonin levels and impaired flexible orientation and inhibition. Critically, 5-HTP selectively impaired the ability of monkeys to inhibit orienting to face images, whereas it similarly impaired orienting to face and control images. 5-HTP also caused monkeys to perseverate on their gaze responses, making them worse at flexibly switching between orienting and inhibiting behaviors. Furthermore, the effects of 5-HTP on performance correlated with a constriction of the pupil, an increased time to initiate trials, and an increased reaction time, suggesting that the disruptive effects of 5-HTP on social gaze behaviors are likely driven by a downregulation of arousal and motivational states. Together, these findings provide causal evidence for a modulatory relationship between 5-HTP and social gaze behaviors in nonhuman primates and offer translational insights for the role of the serotonergic system in social gaze.
Jacob A. Westerberg; Michelle S. Schall; Alexander Maier; Geoffrey F. Woodman; Jeffrey D. Schall
Laminar microcircuitry of visual cortex producing attention-associated electric fields Journal Article
In: eLife, vol. 11, pp. 1–23, 2022.
Cognitive operations are widely studied by measuring electric fields through EEG and ECoG. However, despite their widespread use, the neural circuitry giving rise to these signals remains unknown because the functional architecture of cortical columns producing attention-associated electric fields has not been explored. Here we detail the laminar cortical circuitry underlying an attention-associated electric field measured over posterior regions of the brain in humans and monkeys. First, we identified visual cortical area V4 as one plausible contributor to this attention-associated electric field through inverse modeling of cranial EEG in macaque monkeys performing a visual attention task. Next, we performed laminar neurophysiological recordings on the prelunate gyrus and identified the electric-field-producing dipoles as synaptic activity in distinct cortical layers of area V4. Specifically, activation in the extragranular layers of cortex resulted in the generation of the attention-associated dipole. Feature selectivity of a given cortical column determined the overall contribution to this electric field. Columns selective for the attended feature contributed more to the electric field than columns selective for a different feature. Lastly, the laminar profile of synaptic activity generated by V4 was sufficient to produce an attention-associated signal measurable outside of the column. These findings suggest that the top-down recipient cortical layers produce an attention-associated electric field that can be measured extracortically with the relative contribution of each column depending upon the underlying functional architecture.
Benedict Wild; Amr Maamoun; Yifan Mayr; Ralf Brockhausen; Stefan Treue
Electrophysiological dataset from macaque visual cortical area MST in response to a novel motion stimulus Journal Article
In: Scientific Data, vol. 9, pp. 1–10, 2022.
Establishing the cortical neural representation of visual stimuli is a central challenge of systems neuroscience. Publicly available data would allow a broad range of scientific analyses and hypothesis testing, but are rare and largely focused on the early visual system. To address the shortage of open data from higher visual areas, we provide a comprehensive dataset from a neurophysiology study in macaque monkey visual cortex that includes a complete record of extracellular action potential recordings from the extrastriate medial superior temporal (MST) area, behavioral data, and detailed stimulus records. It includes spiking activity of 172 single neurons recorded in 139 sessions from 4 hemispheres of 3 rhesus macaque monkeys. The data was collected across 3 experiments, designed to characterize the response properties of MST neurons to complex motion stimuli. This data can be used to elucidate visual information processing at the level of single neurons in a high-level area of primate visual cortex. Providing open access to this dataset also promotes the 3R-principle of responsible animal research.
Jae Hyung Woo; Habiba Azab; Andrew Jahn; Benjamin Hayden; Joshua W. Brown
The PRO model accounts for the anterior cingulate cortex role in risky decision-making and monitoring Journal Article
In: Cognitive, Affective and Behavioral Neuroscience, vol. 22, no. 5, pp. 952–968, 2022.
The anterior cingulate cortex (ACC) has been implicated in a number of functions, including performance monitoring and decision-making involving effort. The prediction of responses and outcomes (PRO) model has provided a unified account of much human and monkey ACC data involving anatomy, neurophysiology, EEG, fMRI, and behavior. We explored the computational nature of ACC with the PRO model, extending it to account specifically for both human and macaque monkey decision-making under risk, including both behavioral and neural data. We show that the PRO model can account for a number of additional effects related to outcome prediction, decision-making under risk, gambling behavior. In particular, we show that the ACC represents the variance of uncertain outcomes, suggesting a link between ACC function and mean-variance theories of decision making. The PRO model provides a unified account of a large set of data regarding the ACC.
Shengyi Wu; Tommy Blanchard; Emily Meschke; Richard N. Aslin; Benjamin Y. Hayden; Celeste Kidd
Macaques preferentially attend to intermediately surprising information Journal Article
In: Biology Letters, vol. 18, pp. 1–5, 2022.
Normative learning theories dictate that we should preferentially attend to informative sources, but only up to the point that our limited learning systems can process their content. Humans, including infants, show this predicted strategic deployment of attention. Here, we demonstrate that rhesus monkeys, much like humans, attend to events of moderate surprisingness over both more and less surprising events. They do this in the absence of any specific goal or contingent reward, indicating that the behavioural pattern is spontaneous. We suggest this U-shaped attentional preference represents an evolutionarily preserved strategy for guiding intelligent organisms toward material that is maximally useful for learning.
Jin Xie; Ting Yan; Jie Zhang; Zhengyu Ma; Huihui Zhou
Modulation of neuronal activity and saccades at theta rhythm during visual search in non-human primates Journal Article
In: Neuroscience Bulletin, vol. 38, no. 10, pp. 1183–1198, 2022.
Active exploratory behaviors have often been associated with theta oscillations in rodents, while theta oscillations during active exploration in non-human primates are still not well understood. We recorded neural activities in the frontal eye field (FEF) and V4 simultaneously when monkeys performed a free-gaze visual search task. Saccades were strongly phase-locked to theta oscillations of V4 and FEF local field potentials, and the phase-locking was dependent on saccade direction. The spiking probability of V4 and FEF units was significantly modulated by the theta phase in addition to the time-locked modulation associated with the evoked response. V4 and FEF units showed significantly stronger responses following saccades initiated at their preferred phases. Granger causality and ridge regression analysis showed modulatory effects of theta oscillations on saccade timing. Together, our study suggests phase-locking of saccades to the theta modulation of neural activity in visual and oculomotor cortical areas, in addition to the theta phase locking caused by saccade-triggered responses.
Cheng Xue; Lily E. Kramer; Marlene R. Cohen
Dynamic task-belief is an integral part of decision-making Journal Article
In: Neuron, vol. 110, no. 15, pp. 2503–2511, 2022.
Natural decisions involve two seemingly separable processes: inferring the relevant task (task-belief) and performing the believed-relevant task. The assumed separability has led to the traditional practice of studying task-switching and perceptual decision-making individually. Here, we used a novel paradigm to manipulate and measure macaque monkeys' task-belief and demonstrated inextricable neuronal links between flexible task-belief and perceptual decision-making. We showed that in animals, but not in artificial networks that performed as well or better than the animals, stronger task-belief is associated with better perception. Correspondingly, recordings from neuronal populations in cortical areas 7a and V1 revealed that stronger task-belief is associated with better discriminability of the believed-relevant, but not the believed-irrelevant, feature. Perception also impacts belief updating; noise fluctuations in V1 help explain how task-belief is updated. Our results demonstrate that complex tasks and multi-area recordings can reveal fundamentally new principles of how biology affects behavior in health and disease.
Qianli Yang; Zhongqiao Lin; Wenyi Zhang; Jianshu Li; Xiyuan Chen; Jiaqi Zhang; Tianming Yang
Monkey plays Pac-Man with compositional strategies and hierarchical decision-making Journal Article
In: eLife, vol. 11, pp. 1–39, 2022.
Humans can often handle daunting tasks with ease by developing a set of strategies to reduce decision-making into simpler problems. The ability to use heuristic strategies demands an advanced level of intelligence and has not been demonstrated in animals. Here, we trained macaque monkeys to play the classic video game Pac-Man. The monkeys' decision-making may be described with a strategy-based hierarchical decision-making model with over 90% accuracy. The model reveals that the monkeys adopted the take-the-best heuristic by using one dominating strategy for their decision-making at a time and formed compound strategies by assembling the basis strategies to handle particular game situations. With the model, the computationally complex but fully quan-tifiable Pac-Man behavior paradigm provides a new approach to understanding animals' advanced cognition.
Sang-Ah Yoo; Julio C. Martinez-Trujillo; Stefan Treue; John K. Tsotsos; Mazyar Fallah
Attention to visual motion suppresses neuronal and behavioral sensitivity in nearby feature space Journal Article
In: BMC Biology, vol. 20, no. 1, pp. 1–19, 2022.
Background: Feature-based attention prioritizes the processing of the attended feature while strongly suppressing the processing of nearby ones. This creates a non-linearity or “attentional suppressive surround” predicted by the Selective Tuning model of visual attention. However, previously reported effects of feature-based attention on neuronal responses are linear, e.g., feature-similarity gain. Here, we investigated this apparent contradiction by neurophysiological and psychophysical approaches. Results: Responses of motion direction-selective neurons in area MT/MST of monkeys were recorded during a motion task. When attention was allocated to a stimulus moving in the neurons' preferred direction, response tuning curves showed its minimum for directions 60–90° away from the preferred direction, an attentional suppressive surround. This effect was modeled via the interaction of two Gaussian fields representing excitatory narrowly tuned and inhibitory widely tuned inputs into a neuron, with feature-based attention predominantly increasing the gain of inhibitory inputs. We further showed using a motion repulsion paradigm in humans that feature-based attention produces a similar non-linearity on motion discrimination performance. Conclusions: Our results link the gain modulation of neuronal inputs and tuning curves examined through the feature-similarity gain lens to the attentional impact on neural population responses predicted by the Selective Tuning model, providing a unified framework for the documented effects of feature-based attention on neuronal responses and behavior.
Kaining Zhang; Ethan S. Bromberg-Martin; Fatih Sogukpinar; Kim Kocher; Ilya E. Monosov
Surprise and recency in novelty detection in the primate brain Journal Article
In: Current Biology, vol. 32, no. 10, pp. 2160–2173, 2022.
Primates and other animals must detect novel objects. However, the neuronal mechanisms of novelty detection remain unclear. Prominent theories propose that visual object novelty is either derived from the computation of recency (how long ago a stimulus was experienced) or is a form of sensory surprise (stimulus unpredictability). Here, we use high-channel electrophysiology in primates to show that in many primate prefrontal, temporal, and subcortical brain areas, object novelty detection is intertwined with the computations of recency and sensory surprise. Also, distinct circuits could be engaged by expected versus unexpected sensory surprise. Finally, we studied neuronal novelty-to-familiarity transformations during learning across many days. We found a diversity of timescales in neurons' learning rates and between-session forgetting rates, both within and across brain areas, that are well suited to support flexible behavior and learning in response to novelty. Our findings show that novelty sensitivity arises on multiple timescales across single neurons due to diverse but related computations of sensory surprise and recency and shed light on the computational underpinnings of novelty detection in the primate brain.
Mengmi Zhang; Marcelo Armendariz; Will Xiao; Olivia Rose; Katarina Bendtz; Margaret Livingstone; Carlos Ponce; Gabriel Kreiman
Look twice: A generalist computational model predicts return fixations across tasks and species Book
Primates constantly explore their surroundings via saccadic eye movements that bring different parts of an image into high resolution. In addition to exploring new regions in the visual field, primates also make frequent return fixations, revisiting previously foveated locations. We systematically studied a total of 44,328 return fixations out of 217,440 fixations. Return fixations were ubiquitous across different behavioral tasks, in monkeys and humans, both when subjects viewed static images and when subjects performed natural behaviors. Return fixations locations were consistent across subjects, tended to occur within short temporal offsets, and typically followed a 180-degree turn in saccadic direction. To understand the origin of return fixations, we propose a proof-of-principle, biologically-inspired and image-computable neural network model. The model combines five key modules: an image feature extractor, bottom-up saliency cues, task-relevant visual features, finite inhibition-of-return, and saccade size constraints. Even though there are no free parameters that are fine-tuned for each specific task, species, or condition, the model produces fixation sequences resembling the universal properties of return fixations. These results provide initial steps towards a mechanistic understanding of the trade-off between rapid foveal recognition and the need to scrutinize previous fixation locations.
Wenyi Zhang; Yang Xie; Tianming Yang
Reward salience but not spatial attention dominates the value representation in the orbitofrontal cortex Journal Article
In: Nature Communications, vol. 13, no. 1, pp. 1–12, 2022.
The orbitofrontal cortex (OFC) encodes value and plays a key role in value-based decision-making. However, the attentional modulation of the OFC's value encoding is poorly understood. We trained two monkeys to detect a luminance change at a cued location between a pair of visual stimuli, which were over-trained pictures associated with different amounts of juice reward and, thus, different reward salience. Both the monkeys' behavior and the dorsolateral prefrontal cortex neuronal activities indicated that the monkeys actively directed their spatial attention toward the cued stimulus during the task. However, the OFC's neuronal responses were dominated by the stimulus with higher reward salience and encoded its value. The value of the less salient stimulus was only weakly represented regardless of spatial attention. The results demonstrate that reward and spatial attention are distinctly represented in the prefrontal cortex and the OFC maintains a stable representation of reward salience minimally affected by attention.
Zhewei Zhang; Chaoqun Yin; Tianming Yang
Evidence accumulation occurs locally in the parietal cortex Journal Article
In: Nature Communications, vol. 13, no. 1, pp. 1–11, 2022.
Decision making often entails evidence accumulation, a process that is represented by neural activities in a network of multiple brain areas. Yet, it has not been identified where exactly the accumulation originates. We reason that a candidate brain area should both represent evidence accumulation and information that is used to compute evidence. Therefore, we designed a two-stage probabilistic reasoning task in which the evidence for accumulation had to be first determined from sensory signals orthogonal to decisions. With a linear encoding model, we decomposed the responses of posterior parietal neurons to each stimulus into an early and a late component that represented two dissociable stages of decision making. The former reflected the transformation from sensory inputs to accumulable evidence, and the latter reflected the accumulation of evidence and the formation of decisions. The presence of both computational stages indicates that evidence accumulation signal in the parietal cortex is computed locally.
Ricardo Kienitz; Kleopatra Kouroupaki; Michael C. Schmid
Microstimulation of visual area V4 improves visual stimulus detection Journal Article
In: Cell Reports, vol. 40, no. 12, pp. 1–11, 2022.
Neuronal activity in visual area V4 is well known to be modulated by selective attention, and there are reports on V4 lesions leading to attentional deficits. However, it remains unclear whether V4 microstimulation can elicit attentional benefits. To test this hypothesis, we performed local microstimulation in area V4 and explored its spatial and time dynamics in two macaque monkeys performing a visual detection task. Microstimulation was delivered via chronically implanted multi-electrode arrays. We found that microstimulation increases average performance by 35% and reduces luminance detection thresholds by −30%. This benefit critically depends on the onset of microstimulation relative to the stimulus, consistent with known dynamics of endogenous attention. These results show that local microstimulation of V4 can improve behavior and highlight the critical role of V4 for attention.
Matthew R. Krause; Pedro G. Vieira; Jean Philippe Thivierge; Christopher C. Pack
Brain stimulation competes with ongoing oscillations for control of spike timing in the primate brain Journal Article
In: PLoS Biology, vol. 20, no. 5, pp. 1–27, 2022.
Transcranial alternating current stimulation (tACS) is a popular method for modulating brain activity noninvasively. In particular, tACS is often used as a targeted intervention that enhances a neural oscillation at a specific frequency to affect a particular behavior. However, these interventions often yield highly variable results. Here, we provide a potential explanation for this variability: tACS competes with the brain's ongoing oscillations. Using neural recordings from alert nonhuman primates, we find that when neural firing is independent of ongoing brain oscillations, tACS readily entrains spiking activity, but when neurons are strongly entrained to ongoing oscillations, tACS often causes a decrease in entrainment instead. Consequently, tACS can yield categorically different results on neural activity, even when the stimulation protocol is fixed. Mathematical analysis suggests that this competition is likely to occur under many experimental conditions. Attempting to impose an external rhythm on the brain may therefore often yield precisely the opposite effect.
Satwant Kumar; Eline Mergan; Rufin Vogels
It is not just the category: Behavioral effects of fMRI-guided electrical microstimulation result from a complex interplay of factors Journal Article
In: Cerebral Cortex Communications, vol. 3, pp. 1–16, 2022.
Functional imaging and electrophysiological studies in primates revealed the existence of patches selective for visual categories in the inferior temporal cortex. Understanding the contribution of these patches to perception requires causal techniques that assess the effect of neural activity manipulations on perception. We used electrical microstimulation (EM) to determine the role of body patch activity in visual categorization in macaques. We tested the hypothesis that EM in a body patch would affect the categorization of bodies versus objects but not of other visual categories. We employed low-current EM of an anterior body patch (ASB) in the superior temporal sulcus, which was defined by functional magnetic resonance imaging and verified with electrophysiological recordings in each session. EM of ASB affected body categorization, but the EM effects were more complex than the expected increase of body-related choices: EM affected the categorization of both body and inanimate images and showed interaction with the choice target location, but its effect was location-specific (tested in 1 subject) on a millimeter scale. Our findings suggest that the behavioral effects of EM in a category-selective patch are not merely a manifestation of the category selectivity of the underlying neuronal population but reflect a complex interplay of multiple factors.
Koji Kuraoka; Kae Nakamura
Facial temperature and pupil size as indicators of internal state in primates Journal Article
In: Neuroscience Research, 2022.
Studies in human subjects have revealed that autonomic responses provide objective and biologically relevant information about cognitive and affective states. Measures of autonomic responses can also be applied to studies of non-human primates, which are neuro-anatomically and physically similar to humans. Facial temperature and pupil size are measured remotely and can be applied to physiological experiments in primates, preferably in a head-fixed condition. However, detailed guidelines for the use of these measures in non-human primates is lacking. Here, we review the neuronal circuits and methodological considerations necessary for measuring and analyzing facial temperature and pupil size in non-human primates. Previous studies have shown that the modulation of these measures primarily reflects sympathetic reactions to cognitive and emotional processes, including alertness, attention, and mental effort, over different time scales. Integrated analyses of autonomic, behavioral, and neurophysiological data in primates are promising methods that reflect multiple dimensions of emotion and could potentially provide tools for understanding the mechanisms underlying neuropsychiatric disorders and vulnerabilities characterized by cognitive and affective disturbances.
Hyunchan Lee; Okihide Hikosaka
Lateral habenula responses during eye contact in a reward conditioning task Journal Article
In: Frontiers in Behavioral Neuroscience, vol. 16, pp. 1–9, 2022.
For many animals, social interaction may have intrinsic reward value over and above its utility as a means to the desired end. Eye contact is the starting point of interactions in many social animals, including primates, and abnormal patterns of eye contact are present in many mental disorders. Whereas abundant previous studies have shown that negative emotions such as fear strongly affect eye contact behavior, modulation of eye contact by reward has received scant attention. Here we recorded eye movement patterns and neural activity in lateral habenula while monkeys viewed faces in the context of Pavlovian and instrumental conditioning tasks. Faces associated with larger rewards spontaneously elicited longer periods of eye contact from the monkeys, even though this behavior was not required or advantaged in the task. Concurrently, lateral habenula neurons were suppressed by faces signaling high value and excited by faces signaling low value. These results suggest that the reward signaling of lateral habenula may contribute to social behavior and disorders, presumably through its connections with the basal ganglia.
Hyunchan Lee; Okihide Hikosaka
Lateral habenula neurons signal step-by-step changes of reward prediction Journal Article
In: iScience, vol. 25, pp. 1–23, 2022.
In real life, multiple objects of different values are mixed in a variety of environments. To survive, animals need to find rewarding objects that may be located but hidden in particular contexts (e.g., environments) with bad objects that are unassociated with reward. Then, animals and humans pay attention to the enriched environment so that they can find the rewarding object vigorously. How can the brain initiate such behavior based on the context? We thus created a behavioral task for monkeys in which multiple contextual events (environment, action cue) sequentially occurred before objects appeared. We then studied the lateral habenula (LHb), which inhibit dopamine neurons (Matsumoto and Hikosaka, 2007). LHb neurons showed phasic responses in each event step-by-step across the sequential events, whose direction (excitation or inhibition) corresponded to the immediate change of the predicted value. Moreover, LHb neurons sequentially compared detailed prediction errors based on their significance in multiple contexts.
Kaleb A. Lowe; Wolf Zinke; Joshua D. Cosman; Jeffrey D. Schall
Frontal eye fields in macaque monkeys: Prefrontal and premotor contributions to visually guided saccades Journal Article
In: Cerebral Cortex, vol. 32, pp. 5083–5107, 2022.
Neuronal spiking was sampled from the frontal eye field (FEF) and from the rostral part of area 6 that reaches to the superior limb of the arcuate sulcus, dorsal to the arcuate spur when present (F2vr) in macaque monkeys performing memory-guided saccades and visually guided saccades for visual search. Neuronal spiking modulation in F2vr resembled that in FEF in many but not all respects. A new consensus clustering algorithm of neuronal modulation patterns revealed that F2vr and FEF contain a greater variety of modulation patterns than previously reported. The areas differ in the proportions of visuomotor neuron types, the proportions of neurons discriminating a target from distractors during visual search, and the consistency of modulation patterns across tasks. However, between F2vr and FEF we found no difference in the magnitude of delay period activity, the timing of the peak discharge rate relative to saccades, or the time of search target selection. The observed similarities and differences between the 2 cortical regions contribute to other work establishing the organization of eye fields in the frontal lobe and may help explain why FEF in monkeys is identified within granular prefrontal area 8 but in humans is identified within agranular premotor area 6.
Wenbo Ma; Min Li; Junru Wu; Zhihao Zhang; Fangfang Jia; Mingsha Zhang; Hagai Bergman; Xuemei Li; Zhipei Ling; Xin Xu
Multiple step saccades in simply reactive saccades could serve as a complementary biomarker for the early diagnosis of Parkinson's disease Journal Article
In: Frontiers in Aging Neuroscience, vol. 14, pp. 1–14, 2022.
Objective: It has been argued that the incidence of multiple step saccades (MSS) in voluntary saccades could serve as a complementary biomarker for diagnosing Parkinson's disease (PD). However, voluntary saccadic tasks are usually difficult for elderly subjects to complete. Therefore, task difficulties restrict the application of MSS measurements for the diagnosis of PD. The primary objective of the present study is to assess whether the incidence of MSS in simply reactive saccades could serve as a complementary biomarker for the early diagnosis of PD. Materials and methods: There were four groups of human subjects: PD patients, mild cognitive impairment (MCI) patients, elderly healthy controls (EHCs), and young healthy controls (YHCs). There were four monkeys with subclinical hemi-PD induced by injection of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) through the unilateral internal carotid artery and three healthy control monkeys. The behavioral task was a visually guided reactive saccade. Results: In a human study, the incidence of MSS was significantly higher in PD than in YHC, EHC, and MCI groups. In addition, receiver operating characteristic (ROC) analysis could discriminate PD from the EHC and MCI groups, with areas under the ROC curve (AUCs) of 0.76 and 0.69, respectively. In a monkey study, while typical PD symptoms were absent, subclinical hemi-PD monkeys showed a significantly higher incidence of MSS than control monkeys when the dose of MPTP was greater than 0.4 mg/kg. Conclusion: The incidence of MSS in simply reactive saccades could be a complementary biomarker for the early diagnosis of PD.
Tatiana Malevich; Tong Zhang; Matthias P. Baumann; Amarender R. Bogadhi; Ziad M. Hafed
Faster detection of “darks” than “brights” by monkey superior colliculus neurons Journal Article
In: Journal of Neuroscience, vol. 45, no. 2, pp. 9356–9371, 2022.
Visual processing is segregated into ON and OFF channels as early as in the retina, and the 48 superficial (output) layers of the primary visual cortex are dominated by neurons preferring 49 dark stimuli. However, it is not clear how the timing of neural processing differs between “darks” and “brights” in general, especially in light of psychophysical evidence; it is also equally not clear how subcortical visual pathways that are critical for active orienting represent stimuli of positive (luminance increments) and negative (luminance decrements) contrast polarity. Here, we recorded from all visually-responsive neuron types in the 54 superior colliculus (SC) of two male rhesus macaque monkeys. We presented a disc (0.51 deg 55 radius) within the response fields (RF's) of neurons, and we varied, across trials, stimulus 56 Weber contrast relative to a gray background. We also varied contrast polarity. There was a large diversity of preferences for darks and brights across the population. However, regardless of individual neural sensitivity, most neurons responded significantly earlier to dark than bright stimuli. This resulted in a dissociation between neural preference and visual response onset latency: a neuron could exhibit a weaker response to a dark stimulus than to a bright stimulus of the same contrast, but it would still have an earlier response to the dark stimulus. Our results highlight an additional candidate visual neural pathway for explaining behavioral differences between the processing of darks and brights, and they demonstrate the importance of temporal aspects in the visual neural code for orienting eye movements.
Blake A. Mitchell; Kacie Dougherty; Jacob A. Westerberg; Brock M. Carlson; Loïc Daumail; Alexander Maier; Michele A. Cox
Stimulating both eyes with matching stimuli enhances V1 responses Journal Article
In: iScience, vol. 25, pp. 1–20, 2022.
Neurons in the primary visual cortex (V1) of primates play a key role in combining monocular inputs to form a binocular response. Although much has been gleaned from studying how V1 responds to discrepant (dichoptic) images, equally important is to understand how V1 responds to concordant (dioptic) images in the two eyes. Here, we investigated the extent to which concordant, balanced, zero-disparity binocular stimulation modifies V1 responses to varying stimulus contrast using intracranial multielectrode arrays. On average, binocular stimuli evoked stronger V1 activity than their monocular counterparts. This binocular facilitation scaled most proportionately with contrast during the initial transient. As V1 responses evolved, additional contrast-mediated dynamics emerged. Specifically, responses exhibited longer maintenance of facilitation for lower contrast and binocular suppression at high contrast. These results suggest that V1 processes concordant stimulation of both eyes in at least two sequential steps: initial response enhancement followed by contrast-dependent control of excitation.
Amy M. Ni; Brittany S. Bowes; Douglas A. Ruff; Marlene R. Cohen
Methylphenidate as a causal test of translational and basic neural coding hypotheses Journal Article
In: PNAS, vol. 119, no. 17, pp. 1–7, 2022.
Most systems neuroscience studies fall into one of two categories: basic science work aimed at understanding the relationship between neurons and behavior, or translational work aimed at developing treatments for neuropsychiatric disorders. Here we use these two approaches to inform and enhance each other. Our study both tests hypotheses about basic science neural coding principles and elucidates the neuronal mechanisms underlying clinically relevant behavioral effects of systemically administered methylphenidate (Ritalin). We discovered that orally administered methylphenidate, used clinically to treat attention deficit hyperactivity disorder (ADHD) and generally to enhance cognition, increases spatially selective visual attention, enhancing visual performance at only the attended location. Further, we found that this causal manipulation enhances vision in rhesus macaques specifically when it decreases the mean correlated variability of neurons in visual area V4. Our findings demonstrate that the visual system is a platform for understanding the neural underpinnings of both complex cognitive processes (basic science) and neuropsychiatric disorders (translation). Addressing basic science hypotheses, our results are consistent with a scenario in which methylphenidate has cognitively specific effects by working through naturally selective cognitive mechanisms. Clinically, our findings suggest that the often staggeringly specific symptoms of neuropsychiatric disorders may be caused and treated by leveraging general mechanisms.
James E. Niemeyer; Seth Akers-Campbell; Aaron Gregoire; Michael A. Paradiso
Perceptual enhancement and suppression correlate with V1 neural activity during active sensing Journal Article
In: Current Biology, vol. 32, pp. 2654–2667, 2022.
Perception in multiple sensory modalities is an active process that involves exploratory behaviors. In humans and other primates, vision results from sensory sampling guided by saccadic eye movements. Saccades are known to modulate visual perception, and a corollary discharge signal associated with saccades appears to establish a sense of visual stability. Neural recordings have shown that saccades also modulate activity widely across the brain. To investigate the neural basis of saccadic effects on perception, simultaneous recordings from multiple neurons in area V1 were made as animals performed a contrast detection task. Perceptual and neural measures were compared when the animal made real saccades that brought a stimulus into V1 receptive fields and when simulated saccades were made (identical retinal stimulation but no eye movement). When real saccades were made and low spatial frequency stimuli were presented, we observed a reduction in both perceptual sensitivity and neural activity compared with simulated saccades; conversely, with higher spatial frequency stimuli, saccades increased visual sensitivity and neural activity. The performance of neural decoders, which used the activity of the population of simultaneously recorded neurons, showed saccade effects on sensitivity that mirrored the frequency-dependent perceptual changes, suggesting that the V1 population activity could support the perceptual effects. A minority of V1 neurons had significant choice probabilities, and the saccades decreased both average choice probability and pairwise noise correlations. Taken together, the findings suggest that a signal related to saccadic eye movements alters V1 spiking to increase the independence of spiking neurons and bias the system toward processing higher spatial frequencies, presumably to enhance object recognition. The effects of saccades on visual perception and noise correlations appear to parallel effects observed in other sensory modalities, suggesting a general principle of active sensory processing.
Zuzanna Z. Balewski; Eric B. Knudsen; Joni D. Wallis
Fast and slow contributions to decision-making in corticostriatal circuits Journal Article
In: Neuron, vol. 110, no. 13, pp. 2170–2182, 2022.
We make complex decisions using both fast judgments and slower, more deliberative reasoning. For example, during value-based decision-making, animals make rapid value-guided orienting eye movements after stimulus presentation that bias the upcoming decision. The neural mechanisms underlying these processes remain unclear. To address this, we recorded from the caudate nucleus and orbitofrontal cortex while animals made value-guided decisions. Using population-level decoding, we found a rapid, phasic signal in caudate that predicted the choice response and closely aligned with animals' initial orienting eye movements. In contrast, the dynamics in orbitofrontal cortex were more consistent with a deliberative system serially representing the value of each available option. The phasic caudate value signal and the deliberative orbitofrontal value signal were largely independent from each other, consistent with value-guided orienting and value-guided decision-making being independent processes.
Diana C. Burk; David L. Sheinberg
Neurons in inferior temporal cortex are sensitive to motion trajectory during degraded object recognition Journal Article
In: Cerebral Cortex Communications, vol. 3, no. 3, pp. 1–18, 2022.
Our brains continuously acquire sensory information and make judgments even when visual information is limited. In some circumstances, an ambiguous object can be recognized from how it moves, such as an animal hopping or a plane flying overhead. Yet it remains unclear how movement is processed by brain areas involved in visual object recognition. Here we investigate whether inferior temporal (IT) cortex, an area known for its relevance in visual form processing, has access to motion information during recognition. We developed a matching task that required monkeys to recognize moving shapes with variable levels of shape degradation. Neural recordings in area IT showed that, surprisingly, some IT neurons responded stronger to degraded shapes than clear ones. Furthermore, neurons exhibited motion sensitivity at different times during the presentation of the blurry target. Population decoding analyses showed that motion patterns could be decoded from IT neuron pseudo-populations. Contrary to previous findings, these results suggest that neurons in IT can integrate visual motion and shape information, particularly when shape information is degraded, in a way that has been previously overlooked. Our results highlight the importance of using challenging multifeature recognition tasks to understand the role of area IT in naturalistic visual object recognition.
I Caprara; P Janssen
Effect of viewing distance on object responses in macaque areas 45B, F5a and F5p Journal Article
In: Scientific Reports, vol. 12, no. 1, pp. 1–13, 2022.
To perform tasks like grasping, the brain has to process visual object information so that the grip aperture can be adjusted before touching the object. Previous studies have demonstrated that the posterior subsector of the Anterior Intraparietal area is connected to area 45B, and its anterior counterpart to F5a. However, the role of area 45B and F5a in visually-guided grasping is poorly understood. Here, we investigated the role of area 45B, F5a and F5p in object processing during visually-guided grasping in two monkeys. We tested whether the presentation of an object in near peripersonal space activated F5p neurons more than objects with the same retinal size presented beyond reachable distance and conversely, whether neurons in 45B and F5a—which may encode a purely visual object representation—were less affected by viewing distance when equalizing retinal size. Contrary to our expectations, we found that most neurons in area 45B were object- and viewing distance-selective, and preferred mostly Near presentations. Area F5a showed much weaker object selectivity compared to 45B, with a similar preference for objects presented at the Near position. Finally, F5p neurons were less object selective and frequently Far-preferring. In sum, area 45B—but not F5p– prefers objects presented in peripersonal space.
Spencer Chin-Yu Chen; Giacomo Benvenuti; Yuzhi Chen; Satwant Kumar; Charu Ramakrishnan; Karl Deisseroth; Wilson S. Geisler; Eyal Seidemann
Similar neural and perceptual masking effects of low-power optogenetic stimulation in primate V1 Journal Article
In: eLife, vol. 11, pp. 1–21, 2022.
Can direct stimulation of primate V1 substitute for a visual stimulus and mimic its perceptual effect? To address this question, we developed an optical-genetic toolkit to ‘read' neural population responses using widefield calcium imaging, while simultaneously using optogenetics to ‘write' neural responses into V1 of behaving macaques. We focused on the phenomenon of visual masking, where detection of a dim target is significantly reduced by a co-localized medium-brightness mask (Cornsweet and Pinsker, 1965; Whittle and Swanston, 1974). Using our toolkit, we tested whether V1 optogenetic stimulation can recapitulate the perceptual masking effect of a visual mask. We find that, similar to a visual mask, low-power optostimulation can significantly reduce visual detection sensitivity, that a sublinear interaction between visual-and optogenetic-evoked V1 responses could account for this perceptual effect, and that these neural and behavioral effects are spatially selective. Our toolkit and results open the door for further exploration of perceptual substitutions by direct stimulation of sensory cortex.
Bennett A. Csorba; Matthew R. Krause; Theodoros P. Zanos; Christopher C. Pack
Long-range cortical synchronization supports abrupt visual learning Journal Article
In: Current Biology, vol. 32, no. 11, pp. 2467–2479, 2022.
Visual plasticity declines sharply after the critical period, yet we easily learn to recognize new faces and places, even as adults. Such learning is often characterized by a “moment of insight,” an abrupt and dramatic improvement in recognition. The mechanisms that support abrupt learning are unknown, but one hypothesis is that they involve changes in synchronization between brain regions. To test this hypothesis, we used a behavioral task in which non-human primates rapidly learned to recognize novel images and to associate them with specific responses. Simultaneous recordings from inferotemporal and prefrontal cortices revealed a transient synchronization of neural activity between these areas that peaked around the moment of insight. Synchronization was strongest between inferotemporal sites that encoded images and reward-sensitive prefrontal sites. Moreover, its magnitude intensified gradually over image exposures, suggesting that abrupt learning is the culmination of a search for informative signals within a circuit linking sensory information to task demands.
Olga Dal Monte; Siqi Fan; Nicholas A. Fagan; Cheng Chi J. Chu; Michael B. Zhou; Philip T. Putnam; Amrita R. Nair; Steve W. C. Chang
Widespread implementations of interactive social gaze neurons in the primate prefrontal-amygdala networks Journal Article
In: Neuron, vol. 110, pp. 2183–2197, 2022.
Social gaze interaction powerfully shapes interpersonal communication. However, compared with social perception, very little is known about the neuronal underpinnings of real-life social gaze interaction. Here, we studied a large number of neurons spanning four regions in primate prefrontal-amygdala networks and demonstrate robust single-cell foundations of interactive social gaze in the orbitofrontal, dorsomedial prefrontal, and anterior cingulate cortices, in addition to the amygdala. Many neurons in these areas exhibited high temporal heterogeneity for social discriminability, with a selectivity bias for looking at a conspecific compared with an object. Notably, a large proportion of neurons in each brain region parametrically tracked the gaze of self or other, providing substrates for social gaze monitoring. Furthermore, several neurons displayed selective encoding of mutual eye contact in an agent-specific manner. These findings provide evidence of widespread implementations of interactive social gaze neurons in the primate prefrontal-amygdala networks during social gaze interaction.
Julia Pai; Takaya Ogasawara; Ethan S. Bromberg-Martin; Kei Ogasawara; Robert W. Gereau; Ilya E. Monosov
Laser stimulation of the skin for quantitative study of decision-making and motivation Journal Article
In: Cell Reports Methods, vol. 2, no. 9, pp. 1–18, 2022.
Neuroeconomics studies how decision-making is guided by the value of rewards and punishments. But to date, little is known about how noxious experiences impact decisions. A challenge is the lack of an aversive stimulus that is dynamically adjustable in intensity and location, readily usable over many trials in a single experimental session, and compatible with multiple ways to measure neuronal activity. We show that skin laser stimulation used in human studies of aversion can be used for this purpose in several key animal models. We then use laser stimulation to study how neurons in the orbitofrontal cortex (OFC), an area whose many roles include guiding decisions among different rewards, encode the value of rewards and punishments. We show that some OFC neurons integrated the positive value of rewards with the negative value of aversive laser stimulation, suggesting that the OFC can play a role in more complex choices than previously appreciated.
Mansooreh Pakravan; Mojtaba Abbaszadeh; Ali Ghazizadeh
Coordinated multivoxel coding beyond univariate effects is not likely to be observable in fMRI data Journal Article
In: NeuroImage, vol. 247, pp. 1–14, 2022.
Simultaneous recording of activity across brain regions can contain additional information compared to regional recordings done in isolation. In particular, multivariate pattern analysis (MVPA) across voxels has been interpreted as evidence for distributed coding of cognitive or sensorimotor processes beyond what can be gleaned from a collection of univariate effects (UVE) using functional magnetic resonance imaging (fMRI). Here, we argue that regardless of patterns revealed, conventional MVPA is merely a decoding tool with increased sensitivity arising from considering a large number of ‘weak classifiers' (i.e., single voxels) in higher dimensions. We propose instead that ‘real' multivoxel coding should result in changes in higher-order statistics across voxels between conditions such as second-order multivariate effects (sMVE). Surprisingly, analysis of conditions with robust multivariate effects (MVE) revealed by MVPA failed to show significant sMVE in two species (humans and macaques). Further analysis showed that while both MVE and sMVE can be readily observed in the spiking activity of neuronal populations, the slow and nonlinear hemodynamic coupling and low spatial resolution of fMRI activations make the observation of higher-order statistics between voxels highly unlikely. These results reveal inherent limitations of fMRI signals for studying coordinated coding across voxels. Together, these findings suggest that care should be taken in interpreting significant MVPA results as representing anything beyond a collection of univariate effects.
Soo Hyun Park; Kenji W. Koyano; Brian E. Russ; Elena N. Waidmann; David B. T. McMahon; David A. Leopold
Parallel functional subnetworks embedded in the macaque face patch system Journal Article
In: Science Advances, vol. 8, pp. 1–8, 2022.
During normal vision, our eyes provide the brain with a continuous stream of useful information about the world. How visually specialized areas of the cortex, such as face-selective patches, operate under natural modes of behavior is poorly understood. Here we report that, during the free viewing of movies, cohorts of face-selective neurons in the macaque cortex fractionate into distributed and parallel subnetworks that carry distinct information. We classified neurons into functional groups on the basis of their movie-driven coupling with functional magnetic resonance imaging time courses across the brain. Neurons from each group were distributed across multiple face patches but intermixed locally with other groups at each recording site. These findings challenge prevailing views about functional segregation in the cortex and underscore the importance of naturalistic paradigms for cognitive neuroscience.
Dina V. Popovkina; Anitha Pasupathy
Task context modulates feature-selective responses in area v4 Journal Article
In: Journal of Neuroscience, vol. 42, no. 33, pp. 6408–6423, 2022.
Feature selectivity of visual cortical responses measured during passive fixation provides only a partial view of selectivity because it does not account for the influence of cognitive factors. Here we focus on primate area V4 and ask how neuronal tuning is modulated by task engagement. We investigated whether responses to colored shapes during active shape discrimination are simple, stimulus-agnostic, scaled versions of responses during passive fixation, akin to results from attentional studies. Alternatively, responses could be subject to stimulus-specific scaling, that is, responses to different stimuli are modulated differently, resulting in changes in underlying shape/color selectivity. Among 83 well-isolated V4 neurons in two male macaques, only a minority (16 of 83), which were weakly tuned to both shape and color, displayed responses during fixation and discrimination tasks that could be related by stimulus-agnostic scaling. The majority (67 of 83), which were strongly tuned to shape, color, or both, displayed stimulus-dependent response changes during discrimination. For some of these neurons (39 of 83), the shape or color of the stimulus dictated the magnitude of the change, and for others (28 of 83) it was the combination of stimulus shape and color. Importantly, for neurons with one strong and one weak tuning dimension, stimulus-dependent response changes during discrimination were associated with a relative increase in selectivity along the stronger tuning dimension, without changes in tuning peak. These results reveal that more strongly tuned V4 neurons may also be more flexible in their selectivity, and imbalances in selectivity are amplified during active task contexts.
Guangyao Qi; Wen Fang; Shenghao Li; Junru Li; Liping Wang
Neural dynamics of causal inference in the macaque frontoparietal circuit Journal Article
In: eLife, vol. 11, pp. 1–30, 2022.
Natural perception relies inherently on inferring causal structure in the environment. However, the neural mechanisms and functional circuits essential for representing and updating the hidden causal structure and corresponding sensory representations during multisensory processing are unknown. To address this, monkeys were trained to infer the probability of a potential common source from visual and proprioceptive signals based on their spatial disparity in a virtual reality system. The proprioceptive drift reported by monkeys demonstrated that they combined previous experience and current multisensory signals to estimate the hidden common source and subsequently updated the causal structure and sensory representation. Single-unit recordings in premotor and parietal cortices revealed that neural activity in the premotor cortex represents the core computation of causal inference, characterizing the estimation and update of the likelihood of integrating multiple sensory inputs at a trial-by-trial level. In response to signals from the premotor cortex, neural activity in the parietal cortex also represents the causal structure and further dynamically updates the sensory representation to maintain consistency with the causal inference structure. Thus, our results indicate how the premotor cortex integrates previous experience and sensory inputs to infer hidden variables and selectively updates sensory representations in the parietal cortex to support behavior. This dynamic loop of frontal-parietal interactions in the causal inference framework may provide the neural mechanism to answer long-standing questions regarding how neural circuits represent hidden structures for body awareness and agency.
Rishi Rajalingham; Aída Piccato; Mehrdad Jazayeri
Recurrent neural networks with explicit representation of dynamic latent variables can mimic behavioral patterns in a physical inference task Journal Article
In: Nature Communications, vol. 13, no. 1, pp. 1–15, 2022.
Primates can richly parse sensory inputs to infer latent information. This ability is hypothesized to rely on establishing mental models of the external world and running mental simulations of those models. However, evidence supporting this hypothesis is limited to behavioral models that do not emulate neural computations. Here, we test this hypothesis by directly comparing the behavior of primates (humans and monkeys) in a ball interception task to that of a large set of recurrent neural network (RNN) models with or without the capacity to dynamically track the underlying latent variables. Humans and monkeys exhibit similar behavioral patterns. This primate behavioral pattern is best captured by RNNs endowed with dynamic inference, consistent with the hypothesis that the primate brain uses dynamic inferences to support flexible physical predictions. Moreover, our work highlights a general strategy for using model neural systems to test computational hypotheses of higher brain function.
Maria C. Romero; Lara Merken; Peter Janssen; Marco Davare
Neural effects of continuous theta-burst stimulation in macaque parietal neurons Journal Article
In: eLife, vol. 11, pp. 1–19, 2022.
Theta-burst transcranial magnetic stimulation (TBS) has become a standard non-invasive technique to induce offline changes in cortical excitability in human volunteers. Yet, TBS suffers from a high variability across subjects. A better knowledge about how TBS affects neural activity in vivo could uncover its mechanisms of action and ultimately allow its mainstream use in basic science and clinical applications. To address this issue, we applied continuous TBS (cTBS, 300 pulses) in awake behaving rhesus monkeys and quantified its after-effects on neuronal activity. Overall, we observed a pronounced, long-lasting, and highly reproducible reduction in neuronal excitability after cTBS in individual parietal neurons, with some neurons also exhibiting periods of hyperexcitability during the recovery phase. These results provide the first experimental evidence of the effects of cTBS on single neurons in awake behaving monkeys, shedding new light on the reasons underlying cTBS variability.
Brian E. Brain E. Russ; Kenji W. Koyano; Julian Day-Cooney; Neda Perwez; David A. Leopold
Temporal continuity shapes visual responses of macaque face patch neurons Journal Article
In: Neuron, vol. 111, pp. 1–12, 2022.
Macaque inferior temporal cortex neurons respond selectively to complex visual images, with recent work showing that they are also entrained reliably by the evolving content of natural movies. To what extent does visual continuity itself shape the responses of high-level visual neurons? We addressed this question by measuring how cells in face-selective regions of the macaque temporal cortex were affected by the manipulation of a movie's temporal structure. Sampling the movie at 1s intervals, we measured neural responses to randomized, brief stimuli of different lengths, ranging from 800 ms dynamic movie snippets to 100 ms static frames. We found that the disruption of temporal continuity strongly altered neural response profiles, particularly in the early onset response period of the randomized stimulus. The results suggest that models of visual system function based on discrete and randomized visual presentations may not translate well to the brain's natural modes of operation.
Amirsaman Sajad; Steven P. Errington; Jeffrey D. Schall
Functional architecture of executive control and associated event-related potentials in macaques Journal Article
In: Nature Communications, vol. 13, no. 1, pp. 1–19, 2022.
The medial frontal cortex (MFC) enables executive control by monitoring relevant information and using it to adapt behavior. In macaques performing a saccade countermanding (stop-signal) task, we simultaneously recorded electrical potentials over MFC and neural spiking across all layers of the supplementary eye field (SEF). We report the laminar organization of neurons enabling executive control by monitoring the conflict between incompatible responses, the timing of events, and sustaining goal maintenance. These neurons were a mix of narrow-spiking and broad-spiking found in all layers, but those predicting the duration of control and sustaining the task goal until the release of operant control were more commonly narrow-spiking neurons confined to layers 2 and 3 (L2/3). We complement these results with evidence for a monkey homolog of the N2/P3 event-related potential (ERP) complex associated with response inhibition. N2 polarization varied with error-likelihood and P3 polarization varied with the duration of expected control. The amplitude of the N2 and P3 were predicted by the spike rate of different classes of neurons located in L2/3 but not L5/6. These findings reveal features of the cortical microcircuitry supporting executive control and producing associated ERPs.
Ehsan Sedaghat-Nejad; Jay S. Pi; Paul Hage; Mohammad Amin Fakharian; Reza Shadmehr
Synchronous spiking of cerebellar Purkinje cells during control of movements Journal Article
In: PNAS, vol. 119, no. 14, pp. 1–11, 2022.
The ability of the brain to accurately control a movement depends on the cerebellum. Yet, how the cerebellar neurons encode information relevant for this control remains poorly understood. The computations that are performed in the cerebellar cortex are transmitted to its nuclei via Purkinje cells (P cells), which are inhibitory neurons. How- ever, if the spiking activity within P cell populations were temporally synchronized, that inhibition would entrain nucleus neurons, making them fire. Do P cells transmit information by synchronously timing their spikes? We simultaneously recorded from multiple P cells while marmosets performed saccadic eye movements, and organized the neurons into populations that shared a complex spike response to error. Before move- ment onset, this population ofP cells increased their simple spike activity with a magni- tude that depended on the velocity of the upcoming saccade, and then sharply reduced their activity below baseline at saccade onset. During deceleration, the spikes became temporally aligned within the population. Thus, the P cells relied on disinhibition, combined with spike synchronization, to convey to the nucleus when to decelerate and potentially stop the movement.
Joshua A. Seideman; Terrence R. Stanford; Emilio Salinas
A conflict between spatial selection and evidence accumulation in area LIP Journal Article
In: Nature Communications, vol. 13, no. 1, pp. 1–11, 2022.
The lateral intraparietal area (LIP) contains spatially selective neurons that help guide eye movements and, according to numerous studies, do so by accumulating sensory evidence in favor of one choice (e.g., look left) or another (look right). To examine this functional link, we trained two monkeys on an urgent motion discrimination task, a task with which the evolution of both the recorded neuronal activity and the subject's choice can be tracked millisecond by millisecond. We found that while choice accuracy increased steeply with increasing sensory evidence, at the same time, the LIP selection signal became progressively weaker, as if it hindered performance. This effect was consistent with the transient deployment of spatial attention to disparate locations away from the relevant sensory cue. The results demonstrate that spatial selection in LIP is dissociable from, and may even conflict with, evidence accumulation during informed saccadic choices.
João D. Semedo; Anna I. Jasper; Amin Zandvakili; Aravind Krishna; Amir Aschner; Christian K. Machens; Adam Kohn; Byron M. Yu
Feedforward and feedback interactions between visual cortical areas use different population activity patterns Journal Article
In: Nature Communications, vol. 13, no. 1, pp. 1–14, 2022.
Brain function relies on the coordination of activity across multiple, recurrently connected brain areas. For instance, sensory information encoded in early sensory areas is relayed to, and further processed by, higher cortical areas and then fed back. However, the way in which feedforward and feedback signaling interact with one another is incompletely understood. Here we investigate this question by leveraging simultaneous neuronal population recordings in early and midlevel visual areas (V1–V2 and V1–V4). Using a dimensionality reduction approach, we find that population interactions are feedforward-dominated shortly after stimulus onset and feedback-dominated during spontaneous activity. The population activity patterns most correlated across areas were distinct during feedforward- and feedback-dominated periods. These results suggest that feedforward and feedback signaling rely on separate “channels”, which allows feedback signals to not directly affect activity that is fed forward.
Weikang Shi; Sebastien Ballesta; Camillo Padoa-Schioppa
Neuronal origins of reduced accuracy and biases in economic choices under sequential offers Journal Article
In: eLife, vol. 11, pp. 1–26, 2022.
Economic choices are characterized by a variety of biases. Understanding their origins is a long-term goal for neuroeconomics, but progress on this front has been limited. Here, we examined choice biases observed when two goods are offered sequentially. In the experiments, rhesus monkeys chose between different juices offered simultaneously or in sequence. Choices under sequential offers were less accurate (higher variability). They were also biased in favor of the second offer (order bias) and in favor of the preferred juice (preference bias). Analysis of neuronal activity recorded in the orbitofrontal cortex revealed that these phenomena emerged at different computational stages. Lower choice accuracy reflected weaker offer value signals (valuation stage), the order bias emerged during value comparison (decision stage), and the preference bias emerged late in the trial (post-comparison). By neuronal measures, each phenomenon reduced the value obtained on average in each trial and was thus costly to the monkey.
Weikang Shi; Sébastien Ballesta; Camillo Padoa-Schioppa
Economic choices under simultaneous or sequential offers rely on the same neural circuit Journal Article
In: Journal of Neuroscience, vol. 42, no. 1, pp. 33–43, 2022.
A series of studies in which monkeys chose between two juices offered in variable amounts identified in the orbitofrontal cortex (OFC) different groups of neurons encoding the value of individual options ( offer value ), the binary choice outcome ( chosen juice ) and the chosen value . These variables capture both the input and the output of the choice process, suggesting that the cell groups identified in OFC constitute the building blocks of a decision circuit. Several lines of evidence support this hypothesis. However, in previous experiments offers were presented simultaneously, raising the question of whether current notions generalize to when goods are presented or are examined in sequence. Recently, [Ballesta and Padoa-Schioppa (2019)] examined OFC activity under sequential offers. An analysis of neuronal responses across time windows revealed that a small number of cell groups encoded specific sequences of variables. These sequences appeared analogous to the variables identified under simultaneous offers, but the correspondence remained tentative. Thus in the present study we examined the relation between cell groups found under sequential versus simultaneous offers. We recorded from the OFC while monkeys chose between different juices. Trials with simultaneous and sequential offers were randomly interleaved in each session. We classified cells in each choice modality and we examined the relation between the two classifications. We found a strong correspondence – in other words, the cell groups measured under simultaneous offers and under sequential offers were one and the same. This result indicates that economic choices under simultaneous or sequential offers rely on the same neural circuit. Significance Statement Research in the past 20 years has shed light on the neuronal underpinnings of economic choices. A large number of results indicates that decisions between goods are formed in a neural circuit within the orbitofrontal cortex (OFC). In most previous studies, subjects chose between two goods offered simultaneously. Yet, in daily situations, goods available for choice are often presented or examined in sequence. Here we recorded neuronal activity in the primate OFC alternating trials under simultaneous and under sequential offers. Our analyses demonstrate that the same neural circuit supports choices in the two modalities. Hence current notions on the neuronal mechanisms underlying economic decisions generalize to choices under sequential offers. ### Competing Interest Statement The authors have declared no competing interest.
Mathilda Froesel; Maëva Gacoin; Simon Clavagnier; Marc Hauser; Quentin Goudard; Suliann Ben Hamed
Socially meaningful visual context either enhances or inhibits vocalisation processing in the macaque brain Journal Article
In: Nature Communications, vol. 13, no. 1, pp. 1–17, 2022.
Social interactions rely on the interpretation of semantic and emotional information, often from multiple sensory modalities. Nonhuman primates send and receive auditory and visual communicative signals. However, the neural mechanisms underlying the association of visual and auditory information based on their common social meaning are unknown. Using heart rate estimates and functional neuroimaging, we show that in the lateral and superior temporal sulcus of the macaque monkey, neural responses are enhanced in response to species-specific vocalisations paired with a matching visual context, or when vocalisations follow, in time, visual information, but inhibited when vocalisation are incongruent with the visual context. For example, responses to affiliative vocalisations are enhanced when paired with affiliative contexts but inhibited when paired with aggressive or escape contexts. Overall, we propose that the identified neural network represents social meaning irrespective of sensory modality.
Supriya Ghosh; John H. R. Maunsell
Neuronal correlates of selective attention and effort in visual area V4 are invariant of motivational context Journal Article
In: Science Advances, vol. 8, no. 23, pp. 1–16, 2022.
Task demands can differentially engage two fundamental attention components: selectivity (spatial bias) and effort (total nonselective attentional intensity). The relative contributions and interactions of these components in modulating neuronal signals remain unknown. We recorded V4 neurons while monkeys' spatially selective attention and effort were independently controlled by adjusting either task difficulty or reward size at two locations. Neurons were robustly modulated by either selective attention or effort. Notably, increasing overall effort to improve performance at a distant site reduced neuronal responses even when performance was unchanged for receptive field stimuli. This interaction between attentional selectivity and effort was evident in single-trial spiking and can be explained by divisive normalization of spatially distributed behavioral performance at the single-neuron level. Changing motivation using task difficulty or reward produced indistinguishable effects. These results provide a cellular-level mechanism of how attention components integrate to modulate sensory processing in different motivational contexts.
Camille Giacometti; Audrey Dureux; Delphine Autran-Clavagnier; Charles R. E. Wilson; Jérôme Sallet; Manon Dirheimer; Emmanuel Procyk; Fadila Hadj-Bouziane; Céline Amiez
Frontal cortical functional connectivity is impacted by anaesthesia in macaques Journal Article
In: Cerebral Cortex, vol. 32, pp. 4050–4067, 2022.
A critical aspect of neuroscience is to establish whether and how brain networks evolved across primates. To date, most comparative studies have used resting-state functional magnetic resonance imaging (rs-fMRI) in anaesthetized nonhuman primates and in awake humans. However, anaesthesia strongly affects rs-fMRI signals. The present study investigated the impact of the awareness state (anaesthesia vs. awake) within the same group of macaque monkeys on the rs-fMRI functional connectivity organization of a well-characterized network in the human brain, the cingulo-frontal lateral network. Results in awake macaques show that rostral seeds in the cingulate sulcus exhibited stronger correlation strength with rostral compared to caudal lateral frontal cortical areas, while more caudal seeds displayed stronger correlation strength with caudal compared to anterior lateral frontal cortical areas. Critically, this inverse rostro-caudal functional gradient was abolished under anaesthesia. This study demonstrated a similar functional connectivity (FC) organization of the cingulo-frontal cortical network in awake macaque to that previously uncovered in the human brain pointing toward a preserved FC organization from macaque to human. However, it can only be observed in awake state suggesting that this network is sensitive to anaesthesia and warranting significant caution when comparing FC patterns across species under different states.
Christopher A. Henry; Adam Kohn
Feature representation under crowding in macaque V1 and V4 neuronal populations Journal Article
In: Current Biology, vol. 32, no. 23, pp. 5126–5137, 2022.
Visual perception depends strongly on spatial context. A profound example is visual crowding, whereby the presence of nearby stimuli impairs the discriminability of object features. Despite extensive work on perceptual crowding and the spatial integrative properties of visual cortical neurons, the link between these two aspects of visual processing remains unclear. To understand better the neural basis of crowding, we recorded activity simultaneously from neuronal populations in V1 and V4 of fixating macaque monkeys. We assessed the information available from the measured responses about the orientation of a visual target both for tar- gets presented in isolation and amid distractors. Both single neuron and population responses had less information about target orientation when distractors were present. Information loss was moderate in V1 and more substantial in V4. Information loss could be traced to systematic divisive and additive changes in neuronal tuning. Additive and multiplicative changes in tuning were more severe in V4; in addition, tuning ex- hibited other, non-affine transformations that were greater in V4, further restricting the ability of a fixed sen- sory readout strategy to extract accurate feature information across displays. Our results provide a direct test of crowding effects at different stages of the visual hierarchy. They reveal how crowded visual environments alter the spiking activity of cortical populations by which sensory stimuli are encoded and connect these changes to established mechanisms of neuronal spatial integration.
Jerome Herpers; Wim Vanduffel; Rufin Vogels
Limited pairings of electrical micro-stimulation of the ventral tegmental area and a visual stimulus enhance visual cortical responses Journal Article
In: Journal of Cognitive Neuroscience, vol. 34, pp. 1259–1273, 2022.
Previous studies demonstrated that pairing a visual stimulus and electrical micro-stimulation of the ventral tegmental area (VTA-EM) for multiple days is sufficient to induce visual cortical plasticity and changes perception. However, a brief epoch of VTA-EM–stimulus pairing within a single day has been shown to result in a behavioral preference for the paired stimulus. Here, we investigated whether a brief single-day session of VTA-EM–stimulus pairings is sufficient to induce changes in visual cortical responses. We examined macaque posterior infe- rior temporal (PIT) cortex because previous studies demon- strated response changes after VTA-EM stimulus pairing in that area. Multi-unit recordings in PIT were interleaved with VTA- EM–stimulus pairing epochs. During the short VTA-EM–stimulus pairing epochs (60 pairings), one image (fractal) was paired with VTA-EM (STIM) whereas another, unpaired fractal was pre- sented as control. Two other fractals (dummies) were presented only during the recordings. The difference in response between the STIM and control fractals already increased after the first VTA-EM–stimulus pairing epoch, reflecting a relative increase of the response to the STIM fractal. However, the response to the STIM fractal did not increase further with more VTA-EM– stimulus pairing epochs. The relative increase in firing rate for the paired fractal was present early in the response, in line with a local/ bottom–up origin. These effects were absent when com- paring the responses to the dummies pre- and post-VTA-EM. This study shows that pairing a visual image and VTA-EM in a brief single-day session is sufficient to increase the response for the paired image in macaque PIT.
Beatriz Herrera; Jacob A. Westerberg; Michelle S. Schall; Alexander Maier; Geoffrey F. Woodman; Jeffrey D. Schall; Jorge J. Riera
Resolving the mesoscopic missing link: Biophysical modeling of EEG from cortical columns in primates Journal Article
In: NeuroImage, vol. 263, pp. 1–14, 2022.
Event-related potentials (ERP) are among the most widely measured indices for studying human cognition. While their timing and magnitude provide valuable insights, their usefulness is limited by our understanding of their neural generators at the circuit level. Inverse source localization offers insights into such generators, but their solutions are not unique. To address this problem, scientists have assumed the source space generating such signals comprises a set of discrete equivalent current dipoles, representing the activity of small cortical regions. Based on this notion, theoretical studies have employed forward modeling of scalp potentials to understand how changes in circuit-level dynamics translate into macroscopic ERPs. However, experimental validation is lacking because it requires in vivo measurements of intracranial brain sources. Laminar local field potentials (LFP) offer a mechanism for estimating intracranial current sources. Yet, a theoretical link between LFPs and intracranial brain sources is missing. Here, we present a forward modeling approach for estimating mesoscopic intracranial brain sources from LFPs and predict their contribution to macroscopic ERPs. We evaluate the accuracy of this LFP-based representation of brain sources utilizing synthetic laminar neurophysiological measurements and then demonstrate the power of the approach in vivo to clarify the source of a representative cognitive ERP component. To that end, LFP was measured across the cortical layers of visual area V4 in macaque monkeys performing an attention demanding task. We show that area V4 generates dipoles through layer-specific transsynaptic currents that biophysically recapitulate the ERP component through the detailed forward modeling. The constraints imposed on EEG production by this method also revealed an important dissociation between computational and biophysical contributors. As such, this approach represents an important bridge between laminar microcircuitry, through the mesoscopic activity of cortical columns to the patterns of EEG we measure at the scalp.
Michelle R Heusser; Clara Bourrelly; Neeraj J Gandhi
Decoding the time course of spatial information from spiking and local field potential activities in the superior colliculus. Journal Article
In: eNeuro, vol. 9, no. 6, pp. 1–13, 2022.
Place code representation is ubiquitous in circuits that encode spatial parameters. For visually guided eye movements, neurons in many brain regions emit spikes when a stimulus is presented in their receptive fields and/or when a movement is directed into their movement fields. Crucially, individual neurons respond for a broad range of directions or eccentricities away from the optimal vector, making it difficult to decode the stimulus location or the saccade vector from each cell's activity. We investigated whether it is possible to decode the spatial parameter with a population-level analysis, even when the optimal vectors are similar across neurons. Spiking activity and local field potentials (LFP) in the superior colliculus were recorded with a laminar probe as monkeys performed a delayed saccade task to one of eight targets radially equidistant in direction. A classifier was applied offline to decode the spatial configuration as the trial progresses from sensation to action. For spiking activity, decoding performance across all eight directions was highest during the visual and motor epochs and lower but well above chance during the delay period. Classification performance followed a similar pattern for LFP activity too, except the performance during the delay period was limited mostly to the preferred direction. Increasing the number of neurons in the population consistently increased classifier performance for both modalities. Overall, this study demonstrates the power of population activity for decoding spatial information not possible from individual neurons.
Uday K. Jagadisan; Neeraj J. Gandhi
Population temporal structure supplements the rate code during sensorimotor transformations Journal Article
In: Current Biology, vol. 32, pp. 1010–1025, 2022.
Sensorimotor transformations are mediated by premotor brain networks where individual neurons represent sensory, cognitive, and movement-related information. Such multiplexing poses a conundrum—how does a decoder know precisely when to initiate a movement if its inputs are active at times when a movement is not desired (e.g., in response to sensory stimulation)? Here, we propose a novel hypothesis: movement is triggered not only by an increase in firing rate but, critically, also by a reliable temporal pattern in the population response. Laminar recordings in the macaque superior colliculus (SC), a midbrain hub of orienting control, and pseudo-population analyses in SC and cortical frontal eye fields (FEFs) corroborated this hypothesis. Specifically, using a measure that captures the fidelity of the population code—here called temporal stability—we show that the temporal structure fluctuates during the visual response but becomes increasingly stable during the movement command. Importantly, we used spatiotemporally patterned microstimulation to causally test the contribution of population temporal stability in gating movement initiation and found that stable stimulation patterns were more likely to evoke a movement. Finally, a spiking neuron model was able to discriminate between stable and unstable input patterns, providing a putative biophysical mechanism for decoding temporal structure. These findings offer new insights into the long-standing debate on motor preparation and generation by situating the movement gating signal in temporal features of activity in shared neural substrates, and they highlight the importance of short-term population history in neuronal communication and behavior.
Danique Jeurissen; S. Shushruth; Yasmine El-Shamayleh; Gregory D. Horwitz; Michael N. Shadlen
Deficits in decision-making induced by parietal cortex inactivation are compensated at two timescales Journal Article
In: Neuron, vol. 110, pp. 1924–1931, 2022.
Perceptual decisions arise through the transformation of samples of evidence into a commitment to a proposition or plan of action. Such transformation is thought to involve cortical circuits capable of computation over timescales associated with working memory, attention, and planning. Neurons in the lateral intraparietal area (LIP) play a role in these functions, and much of what is known about the neurobiology of decision-making has been influenced by studies of LIP and its network of connections. However, the causal role of LIP remains controversial. In this study, we used pharmacological and chemogenetic methods to inactivate LIP in one brain hemisphere of four rhesus monkeys. This inactivation produced biases in decisions, but the effects dissipated despite persistent neural inactivation, implying compensation by unaffected areas. Compensation occurred rapidly within an experimental session and more gradually across sessions. These findings resolve disparate studies and inform the interpretation of focal perturbations of brain function.
Yaoguang Jiang; Feng Sheng; Naz Belkaya; Michael L. Platt
Oxytocin and testosterone administration amplify viewing preferences for sexual images in male rhesus macaques Journal Article
In: Philosophical Transactions of the Royal Society B: Biological Sciences, vol. 377, pp. 1–12, 2022.
Social stimuli, like faces, and sexual stimuli, like genitalia, spontaneously attract visual attention in both human and non-human primates. Social orienting behaviour is thought to be modulated by neuropeptides as well as sex hormones. Using a free viewing task in which paired images of monkey faces and anogenital regions were presented simultaneously, we found that male rhesus macaques overwhelmingly preferred to view images of anogenital regions over faces. They were more likely to make an initial gaze shift towards, and spent more time viewing, anogenital regions compared with faces, and this preference was accompanied by relatively constricted pupils. On face images, monkeys mostly fixated on the forehead and eyes. These viewing preferences were found for images of both males and females. Both oxytocin (OT), a neuropeptide linked to social bonding and affiliation, and testosterone (TE), a sex hormone implicated in mating and aggression, amplified the pre-existing orienting bias for female genitalia over female faces; neither treatment altered the viewing preference for male anogenital regions over male faces. Testosterone but not OT increased the probability of monkeys making the first gaze shift towards female anogenital rather than face pictures, with the strongest effects on anogenital images of young and unfamiliar females. Finally, both OT and TE promoted viewing of the forehead region of both female and male faces, which display sexual skins, but decreased the relative salience of the eyes of older males. Together, these results invite the hypothesis that both OT and TE regulate reproductive behaviours by acting as a gain control on the visual orienting network to increase attention to mating-relevant signals in the environment. This article is part of the theme issue 'Interplays between oxytocin and other neuromodulators in shaping complex social behaviours'.
Richard Johnston; Adam C. Snyder; Rachel S. Schibler; Matthew A. Smith
EEG signals index a global signature of arousal embedded in neuronal population recordings Journal Article
In: eNeuro, vol. 9, no. 3, pp. 1–16, 2022.
Electroencephalography (EEG) has long been used to index brain states, from early studies describing activity in the presence and absence of visual stimulation to modern work employing complex perceptual tasks. These studies have shed light on brain-wide signals but often lack explanatory power at the single neuron level. Similarly, single neuron recordings can suffer from an inability to measure brain-wide signals accessible using EEG. Here, we combined these techniques while monkeys performed a change detection task and discovered a novel link between spontaneous EEG activity and a neural signal embedded in the spiking responses of neuronal populations. This “slow drift” was associated with fluctuations in the subjects' arousal levels over time: decreases in prestimulus a power were accompanied by increases in pupil size and decreases in microsaccade rate. These re- sults show that brain-wide EEG signals can be used to index modes of activity present in single neuron recordings, that in turn reflect global changes in brain state that influence perception and behavior.
Natasha Kharas; Ariana Andrei; Samantha R. Debes; Valentin Dragoi
Brain state limits propagation of neural signals in laminar cortical circuits Journal Article
In: PNAS, vol. 119, no. 30, pp. 1–10, 2022.
Our perception of the environment relies on the efficient propagation of neural signals across cortical networks. During the time course of a day, neural responses fluctuate dramatically as the state of the brain changes to possibly influence how electrical signals propagate across neural circuits. Despite the importance of this issue, how patterns of spiking activity propagate within neuronal circuits in different brain states remains unknown. Here, we used multielectrode laminar arrays to reveal that brain state strongly modulates the propagation of neural activity across the layers of early visual cortex (V1). We optogenetically induced synchronized state transitions within a group of neurons and examined how far electrical signals travel during wakefulness and rest. Although optogenetic stimulation elicits stronger neural responses during wakefulness relative to rest, signals propagate only weakly across the cortical column during wakefulness, and the extent of spread is inversely related to arousal level. In contrast, the lightinduced population activity vigorously propagates throughout the entire cortical column during rest, even when neurons are in a desynchronized wake-like state prior to light stimulation. Mechanistically, the influence of global brain state on the propagation of spiking activity across laminar circuits can be explained by state-dependent changes in the coupling between neurons. Our results impose constraints on the conclusions of causal manipulation studies attempting to influence neural function and behavior, as well as on previous computational models of perception assuming robust signal propagation across cortical layers and areas.
Manoj K. Eradath; Mark A. Pinsk; Sabine Kastner
A causal role for the pulvinar in coordinating task-independent cortico–cortical interactions Journal Article
In: Journal of Comparative Neurology, vol. 529, no. 17, pp. 3772–3784, 2021.
The pulvinar is the largest nucleus in the primate thalamus and has topographically organized connections with multiple cortical areas, thereby forming extensive cortico-pulvino-cortical input–output loops. Neurophysiological studies have suggested a role for these transthalamic pathways in regulating information transmission between cortical areas. However, evidence for a causal role of the pulvinar in regulating cortico–cortical interactions is sparse and it is not known whether pulvinar's influences on cortical networks are task-dependent or, alternatively, reflect more basic large-scale network properties that maintain functional connectivity across networks regardless of active task demands. In the current study, under passive viewing conditions, we conducted simultaneous electrophysiological recordings from ventral (area V4) and dorsal (lateral intraparietal area [LIP]) nodes of macaque visual system, while reversibly inactivating the dorsal part of the lateral pulvinar (dPL), which shares common anatomical connectivity with V4 and LIP, to probe a causal role of the pulvinar. Our results show a significant reduction in local field potential phase coherence between LIP and V4 in low frequencies (4–15 Hz) following muscimol injection into dPL. At the local level, no significant changes in firing rates or LFP power were observed in LIP or in V4 following dPL inactivation. Synchronization between pulvinar spikes and cortical LFP phase decreased in low frequencies (4–15 Hz) both in LIP and V4, while the low frequency synchronization between LIP spikes and pulvinar phase increased. These results indicate a causal role for pulvinar in synchronizing neural activity between interconnected cortical nodes of a large-scale network, even in the absence of an active task state.
Francesco Fabbrini; Rufin Vogels
Within- and between-hemifield generalization of repetition suppression in inferior temporal cortex Journal Article
In: Journal of Neurophysiology, vol. 125, no. 1, pp. 120–139, 2021.
The decrease in response with stimulus repetition is a common property observed in many sensory brain areas. This repetition suppression (RS) is ubiquitous in neurons of macaque inferior temporal (IT) cortex, the end-stage of the ventral visual pathway. The neural mechanisms of RS in IT are still unclear, and one possibility is that it is inherited from areas upstream to IT that show also RS. Since neurons in IT have larger receptive fields compared with earlier visual areas, we examined the inheritance hypothesis by presenting adapter and test stimuli at widely different spatial locations along both vertical and horizontal meridians and across hemifields. RS was present for distances between adapter and test stimuli up to 22° and when the two stimuli were presented in different hemifields. Also, we examined the position tolerance of the stimulus selectivity of adaptation by comparing the responses to a test stimulus following the same (repetition trial) or a different (alternation trial) adapter at a position different from the test stimulus. Stimulus-selective adaptation was still present and consistently stronger in the later phase of the response for distances up to 18°. Finally, we observed stimulus-selective adaptation in repetition trials even without a measurable excitatory response to the adapter stimulus. To accommodate these and previous data, we propose that at least part of the stimulusselective adaptation in IT is based on short-term plasticity mechanisms within IT and/or reflects top-down activity from areas downstream to IT.
Francesco Fabbrini; Rufin Vogels
Within- and between-hemifields generalization of repetition suppression in inferior temporal cortex Journal Article
In: Journal of Neurophysiology, vol. 125, no. 1, pp. 1–20, 2021.
The decrease in response with stimulus repetition is a common property observed in many sensory brain areas. This repetition suppression (RS) is ubiquitous in neurons of macaque inferior temporal (IT) cortex, the end-stage of the ventral visual pathway. The neural mechanisms of RS in IT are still unclear, and one possibility is that it is inherited from areas upstream to IT that show also RS. Since neurons in IT have larger receptive fields compared to earlier visual areas, we examined the inheritance hypothesis by presenting adapter and test stimuli at widely different spatial locations along both vertical and horizontal meridians, and across hemifields. RS was present for distances between adapter and test stimuli up to 22°, and when the two stimuli were presented in different hemifields. Also, we examined the position tolerance of the stimulus selectivity of adaptation by comparing the responses to a test stimulus following the same (repetition trial) or a different adapter (alternation trial) at a different position than the test stimulus. Stimulus-selective adaptation was still present and consistently stronger in the later phase of the response for distances up to 18°. Finally, we observed stimulus-selective adaptation in repetition trials even without a measurable excitatory response to the adapter stimulus. To accommodate these and previous data, we propose that at least part of the stimulus-selective adaptation in IT is based on short-term plasticity mechanisms within IT and/or reflects top-down activity from areas downstream to IT.
Dylan Festa; Amir Aschner; Aida Davila; Adam Kohn; Ruben Coen-Cagli
Neuronal variability reflects probabilistic inference tuned to natural image statistics Journal Article
In: Nature Communications, vol. 12, pp. 3635, 2021.
Neuronal activity in sensory cortex fluctuates over time and across repetitions of the same input. This variability is often considered detrimental to neural coding. The theory of neural sampling proposes instead that variability encodes the uncertainty of perceptual inferences. In primary visual cortex (V1), modulation of variability by sensory and non-sensory factors supports this view. However, it is unknown whether V1 variability reflects the statistical structure of visual inputs, as would be required for inferences correctly tuned to the statistics of the natural environment. Here we combine analysis of image statistics and recordings in macaque V1 to show that probabilistic inference tuned to natural image statistics explains the widely observed dependence between spike count variance and mean, and the modulation of V1 activity and variability by spatial context in images. Our results show that the properties of a basic aspect of cortical responses—their variability—can be explained by a probabilistic representation tuned to naturalistic inputs.
Ian C. Fiebelkorn; Sabine Kastner
Spike timing in the attention network predicts behavioral outcome prior to target selection Journal Article
In: Neuron, vol. 109, no. 1, pp. 177–188, 2021.
There has been little evidence linking changes in spiking activity that occur prior to a spatially predictable target (i.e., prior to target selection) to behavioral outcomes, despite such preparatory changes being widely assumed to enhance the sensitivity of sensory processing. We simultaneously recorded from frontal and parietal nodes of the attention network while macaques performed a spatial cueing task. When anticipating a spatially predictable target, different patterns of coupling between spike timing and the oscillatory phase in local field potentials—but not changes in spike rate—were predictive of different behavioral outcomes. These behaviorally relevant differences in local and between-region synchronization occurred among specific cell types that were defined based on their sensory and motor properties, providing insight into the mechanisms underlying enhanced sensory processing prior to target selection. We propose that these changes in neural synchronization reflect differential anticipatory engagement of the network nodes and functional units that shape attention-related sampling.
Supriya Ghosh; John H. R. Maunsell
Single trial neuronal activity dynamics of attentional intensity in monkey visual area V4 Journal Article
In: Nature Communications, vol. 12, pp. 2003, 2021.
Understanding how activity of visual neurons represents distinct components of attention and their dynamics that account for improved visual performance remains elusive because single-unit experiments have not isolated the intensive aspect of attention from attentional selectivity. We isolated attentional intensity and its single trial dynamics as determined by spatially non-selective attentional performance in an orientation discrimination task while recording from neurons in monkey visual area V4. We found that attentional intensity is a distinct cognitive signal that can be distinguished from spatial selectivity, reward expectations and motor actions. V4 spiking on single trials encodes a combination of sensory and cognitive signals on different time scales. Attentional intensity and the detection of behaviorally relevant sensory signals are well represented, but immediate reward expectation and behavioral choices are poorly represented in V4 spiking. These results provide a detailed representation of perceptual and cognitive signals in V4 that are crucial for attentional performance.
Jay A. Hennig; Emily R. Oby; Matthew D. Golub; Lindsay A. Bahureksa; Patrick T. Sadtler; Kristin M. Quick; Stephen I. Ryu; Elizabeth C. Tyler-Kabara; Aaron P. Batista; Steven M. Chase; Byron M. Yu
Learning is shaped by abrupt changes in neural engagement Journal Article
In: Nature Neuroscience, vol. 24, no. 5, pp. 727–736, 2021.
Internal states such as arousal, attention and motivation modulate brain-wide neural activity, but how these processes interact with learning is not well understood. During learning, the brain modifies its neural activity to improve behavior. How do internal states affect this process? Using a brain–computer interface learning paradigm in monkeys, we identified large, abrupt fluctuations in neural population activity in motor cortex indicative of arousal-like internal state changes, which we term ‘neural engagement.' In a brain–computer interface, the causal relationship between neural activity and behavior is known, allowing us to understand how neural engagement impacted behavioral performance for different task goals. We observed stereotyped changes in neural engagement that occurred regardless of how they impacted performance. This allowed us to predict how quickly different task goals were learned. These results suggest that changes in internal states, even those seemingly unrelated to goal-seeking behavior, can systematically influence how behavior improves with learning.
Jerome Herpers; John T. Arsenault; Wim Vanduffel; Rufin Vogels
Stimulation of the ventral tegmental area induces visual cortical plasticity at the neuronal level Journal Article
In: Cell Reports, vol. 37, no. 6, pp. 109998, 2021.
fMRI studies have shown that pairing a task-irrelevant visual feature with electrical micro-stimulation of the ventral tegmental area (VTA-EM) is sufficient to increase the sensory cortical representation of the paired feature and to improve perceptual performance. However, since fMRI provides an indirect measure of neural activity, the neural response changes underlying the fMRI activations are unknown. Here, we pair a task-irrelevant grating orientation with VTA-EM while attention is directed to a difficult orthogonal task. We examine the changes in neural response properties in macaques by recording spiking activity in the posterior inferior temporal cortex, the locus of fMRI-defined plasticity in previous studies. We observe a relative increase in mean spike rate and preference for the VTA-EM paired orientation compared to an unpaired orientation, which is unrelated to attention. These results demonstrate that VTA-EM-stimulus pairing is sufficient to induce sensory cortical plasticity at the spiking level in nonhuman primates.
Georgin Jacob; Harish Katti; Thomas Cherian; Jhilik Das; K. A. Zhivago; S. P. Arun
A naturalistic environment to study visual cognition in unrestrained monkeys Journal Article
In: eLife, vol. 10, pp. 1–30, 2021.
Macaque monkeys are widely used to study vision. In the traditional approach, monkeys are brought into a lab to perform visual tasks while they are restrained to obtain stable eye tracking and neural recordings. Here, we describe a novel environment to study visual cognition in a more natural setting as well as other natural and social behaviors. We designed a naturalistic environment with an integrated touchscreen workstation that enables high-quality eye tracking in unrestrained monkeys. We used this environment to train monkeys on a challenging same-different task. We also show that this environment can reveal interesting novel social behaviors. As proof of concept, we show that two naïve monkeys were able to learn this complex task through a combination of socially observing trained monkeys and through solo trialand-error. We propose that such naturalistic environments can be used to rigorously study visual cognition as well as other natural and social behaviors in freely moving monkeys.
Patrick Jendritza; Frederike J. Klein; Gustavo Rohenkohl; Pascal Fries
Visual neuroscience methods for marmosets: Efficient receptive field mapping and head-free eye tracking Journal Article
In: eNeuro, vol. 8, no. 3, pp. 1–16, 2021.
The marmoset has emerged as a promising primate model system, in particular for visual neuroscience. Many common experimental paradigms rely on head fixation and an extended period of eye fixation during the pre-sentation of salient visual stimuli. Both of these behavioral requirements can be challenging for marmosets. Here, we present two methodological developments, each addressing one of these difficulties. First, we show that it is possible to use a standard eye-tracking system without head fixation to assess visual behavior in the marmoset. Eye-tracking quality from head-free animals is sufficient to obtain precise psychometric functions from a visual acuity task. Second, we introduce a novel method for efficient receptive field (RF) mapping that does not rely on moving stimuli but uses fast flashing annuli and wedges. We present data recorded during head-fixation in areas V1 and V6 and show that RF locations are readily obtained within a short period of recording time. Thus, the methodological advancements presented in this work will contribute to establish the marmoset as a valuable model in neuroscience.
Ahmad Jezzini; Ethan S. Bromberg-Martin; Lucas R. Trambaiolli; Suzanne N. Haber; Ilya E. Monosov
A prefrontal network integrates preferences for advance information about uncertain rewards and punishments Journal Article
In: Neuron, vol. 109, no. 14, pp. 2339–2352, 2021.
Humans and animals can be strongly motivated to seek information to resolve uncertainty about rewards and punishments. In particular, despite its clinical and societal relevance, very little is known about information seeking about punishments. We show that attitudes toward information about punishments and rewards are distinct and separable at both behavioral and neuronal levels. We demonstrate the existence of prefrontal neuronal populations that anticipate opportunities to gain information in a relatively valence-specific manner, separately anticipating information about either punishments or rewards. These neurons are located in anatomically interconnected subregions of anterior cingulate cortex (ACC) and ventrolateral prefrontal cortex (vlPFC) in area 12o/47. Unlike ACC, vlPFC also contains a population of neurons that integrate attitudes toward both reward and punishment information, to encode the overall preference for information in a bivalent manner. This cortical network is well suited to mediate information seeking by integrating the desire to resolve uncertainty about multiple, distinct motivational outcomes.
Elizabeth J. Jun; Alex R. Bautista; Michael D. Nunez; Daicia C. Allen; Jung H. Tak; Eduardo Alvarez; Michele A. Basso
Causal role for the primate superior colliculus in the computation of evidence for perceptual decisions Journal Article
In: Nature Neuroscience, vol. 24, no. 8, pp. 1121–1131, 2021.
Trained monkeys performed a two-choice perceptual decision-making task in which they reported the perceived orientation of a dynamic Glass pattern, before and after unilateral, reversible, inactivation of a brainstem area—the superior colliculus (SC)—involved in preparing eye movements. We found that unilateral SC inactivation produced significant decision biases and changes in reaction times consistent with a causal role for the primate SC in perceptual decision-making. Fitting signal detection theory and sequential sampling models to the data showed that SC inactivation produced a decrease in the relative evidence for contralateral decisions, as if adding a constant offset to a time-varying evidence signal for the ipsilateral choice. The results provide causal evidence for an embodied cognition model of perceptual decision-making and provide compelling evidence that the SC of primates (a brainstem structure) plays a causal role in how evidence is computed for decisions—a process usually attributed to the forebrain.
Joonyoung Kang; Hyeji Kim; Seong Hwan Hwang; Minjun Han; Sue-Hyun Lee; Hyoung F. Kim
Primate ventral striatum maintains neural representations of the value of previously rewarded objects for habitual seeking Journal Article
In: Nature Communications, vol. 12, pp. 2100, 2021.
The ventral striatum (VS) is considered a key region that flexibly updates recent changes in reward values for habit learning. However, this update process may not serve to maintain learned habitual behaviors, which are insensitive to value changes. Here, using fMRI in humans and single-unit electrophysiology in macaque monkeys we report another role of the primate VS: that the value memory subserving habitual seeking is stably maintained in the VS. Days after object-value associative learning, human and monkey VS continue to show increased responses to previously rewarded objects, even when no immediate reward outcomes are expected. The similarity of neural response patterns to each rewarded object increases after learning among participants who display habitual seeking. Our data show that long-term memory of high-valued objects is retained as a single representation in the VS and may be utilized to evaluate visual stimuli automatically to guide habitual behavior.
Kohitij Kar; James J. DiCarlo
Fast recurrent processing via ventrolateral prefrontal cortex Is needed by the primate ventral stream for robust core visual object recognition Journal Article
In: Neuron, vol. 109, no. 1, pp. 164–176, 2021.
Distributed neural population spiking patterns in macaque inferior temporal (IT) cortex that support core object recognition require additional time to develop for specific, “late-solved” images. This suggests the necessity of recurrent processing in these computations. Which brain circuits are responsible for computing and transmitting these putative recurrent signals to IT? To test whether the ventrolateral prefrontal cortex (vlPFC) is a critical recurrent node in this system, here, we pharmacologically inactivated parts of vlPFC and simultaneously measured IT activity while monkeys performed object discrimination tasks. vlPFC inactivation deteriorated the quality of late-phase (>150 ms from image onset) IT population code and produced commensurate behavioral deficits for late-solved images. Finally, silencing vlPFC caused the monkeys' IT activity and behavior to become more like those produced by feedforward-only ventral stream models. Together with prior work, these results implicate fast recurrent processing through vlPFC as critical to producing behaviorally sufficient object representations in IT.
Amit P. Khandhadia; Aidan P. Murphy; Lizabeth M. Romanski; Jennifer K. Bizley; David A. Leopold
Audiovisual integration in macaque face patch neurons Journal Article
In: Current Biology, vol. 31, no. 9, pp. 1826–1835, 2021.
Primate social communication depends on the perceptual integration of visual and auditory cues, reflected in the multimodal mixing of sensory signals in certain cortical areas. The macaque cortical face patch network, identified through visual, face-selective responses measured with fMRI, is assumed to contribute to visual social interactions. However, whether face patch neurons are also influenced by acoustic information, such as the auditory component of a natural vocalization, remains unknown. Here, we recorded single-unit activity in the anterior fundus (AF) face patch, in the superior temporal sulcus, and anterior medial (AM) face patch, on the undersurface of the temporal lobe, in macaques presented with audiovisual, visual-only, and auditory-only renditions of natural movies of macaques vocalizing. The results revealed that 76% of neurons in face patch AF were significantly influenced by the auditory component of the movie, most often through enhancement of visual responses but sometimes in response to the auditory stimulus alone. By contrast, few neurons in face patch AM exhibited significant auditory responses or modulation. Control experiments in AF used an animated macaque avatar to demonstrate, first, that the structural elements of the face were often essential for audiovisual modulation and, second, that the temporal modulation of the acoustic stimulus was more important than its frequency spectrum. Together, these results identify a striking contrast between two face patches and specifically identify AF as playing a potential role in the integration of audiovisual cues during natural modes of social communication.
Geoffrey K. Adams; Wei Song Ong; John M. Pearson; Karli K. Watson; Michael L. Platt
Neurons in primate prefrontal cortex signal valuable social information during natural viewing Journal Article
In: Philosophical Transactions of the Royal Society B: Biological Sciences, vol. 376, pp. 1–16, 2021.
Information about social partners is innately valuable to primates. Decisions about which sources of information to consume are highly naturalistic but also complex and place unusually strong demands on the brain's decision network. In particular, both the orbitofrontal cortex (OFC) and lateral prefrontal cortex (LPFC) play key roles in decision making and social behaviour, suggesting a likely role in social information-seeking as well. To test this idea, we developed a 'channel surfing' task in which monkeys were shown a series of 5 s video clips of conspecifics engaged in natural behaviours at a field site. Videos were annotated frame-by-frame using an ethogram of species-typical behaviours, an important source of social information. Between each clip, monkeys were presented with a choice between targets that determined which clip would be seen next. Monkeys' gaze during playback indicated differential engagement depending on what behaviours were presented. Neurons in both OFC and LPFC responded to choice targets and to video, and discriminated a subset of the behaviours in the ethogram during video viewing. These findings suggest that both OFC and LPFC are engaged in processing social information that is used to guide dynamic information-seeking decisions. This article is part of the theme issue 'Existence and prevalence of economic behaviours among non-human primates'.
Amir Akbarian; Kelsey Clark; Behrad Noudoost; Neda Nategh
A sensory memory to preserve visual representations across eye movements Journal Article
In: Nature Communications, vol. 12, pp. 6449, 2021.
Saccadic eye movements (saccades) disrupt the continuous flow of visual information, yet our perception of the visual world remains uninterrupted. Here we assess the representation of the visual scene across saccades from single-trial spike trains of extrastriate visual areas, using a combined electrophysiology and statistical modeling approach. Using a model-based decoder we generate a high temporal resolution readout of visual information, and identify the specific changes in neurons' spatiotemporal sensitivity that underly an integrated perisaccadic representation of visual space. Our results show that by maintaining a memory of the visual scene, extrastriate neurons produce an uninterrupted representation of the visual world. Extrastriate neurons exhibit a late response enhancement close to the time of saccade onset, which preserves the latest pre-saccadic information until the post-saccadic flow of retinal information resumes. These results show how our brain exploits available information to maintain a representation of the scene while visual inputs are disrupted.
Ariana R. Andrei; Samantha Debes; Mircea Chelaru; Xiaoqin Liu; Elsa Rodarte; John L. Spudich; Roger Janz; Valentin Dragoi
Heterogeneous side effects of cortical inactivation in behaving animals Journal Article
In: eLife, vol. 10, pp. e66400, 2021.
Cortical inactivation represents a key causal manipulation allowing the study of cortical circuits and their impact on behavior. A key assumption in inactivation studies is that the neurons in the target area become silent while the surrounding cortical tissue is only negligibly impacted. However, individual neurons are embedded in complex local circuits composed of excitatory and inhibitory cells with connections extending hundreds of microns. This raises the possibility that silencing one part of the network could induce complex, unpredictable activity changes in neurons outside the targeted inactivation zone. These off-target side effects can potentially complicate inter-pretations of inactivation manipulations, especially when they are related to changes in behavior. Here, we demonstrate that optogenetic inactivation of glutamatergic neurons in the superficial layers of monkey primary visual cortex (V1) induces robust suppression at the light-targeted site, but destabilizes stimulus responses in the neighboring, untargeted network. We identified four types of stimulus-evoked neuronal responses within a cortical column, ranging from full suppression to facil-itation, and a mixture of both. Mixed responses were most prominent in middle and deep cortical layers. These results demonstrate that response modulation driven by lateral network connectivity is diversely implemented throughout a cortical column. Importantly, consistent behavioral changes induced by optogenetic inactivation were only achieved when cumulative network activity was homogeneously suppressed. Therefore, careful consideration of the full range of network changes outside the inactivated cortical region is required, as heterogeneous side effects can confound inter-pretation of inactivation experiments.
Benjamin M. Basile; Jessica A. Joiner; Olga Dal Monte; Nicholas A. Fagan; Chloe L. Karaskiewicz; Daniel R. Lucas; Steve W. C. Chang; Elisabeth A. Murray
Autonomic arousal tracks outcome salience not valence in monkeys making social decisions Journal Article
In: Behavioral Neuroscience, vol. 135, no. 3, pp. 443–452, 2021.
The evolutionary and neural underpinnings of human prosociality are still being identified. A growing body of evidence suggests that some species find the sight of another individual receiving a reward reinforcing, called vicarious reinforcement, and that this capacity is supported by a network of brain areas including the anterior cingulate cortex (ACC) and the amygdala. At the same time, analyses of autonomic arousal have been increasingly used to contextualize and guide neural research, especially for studies of reward processing. Here, we characterized the autonomic pupil response of eight monkeys across two laboratories in two different versions of a vicarious reinforcement paradigm. Monkeys were cued as to whether an upcoming reward would be delivered to them, another monkey, or nobody and could accept or decline the offer. As expected, all monkeys in both laboratories showed a marked preference for juice to the self, together with a reliable prosocial preference for juice to a social partner compared to juice to nobody. However, contrary to our expectations, we found that pupils were widest in anticipation of juice to the self, moderately sized in anticipation of juice to nobody, and narrowest in anticipation of juice to a social partner. This effect was seen across both laboratories and regardless of specific task parameters. The seemingly paradoxical pupil effect can be explained by a model in which pupil size tracks outcome salience, prosocial tendencies track outcome valence, and the relation between salience and valence is U-shaped. (PsycInfo Database Record (c) 2021 APA, all rights reserved)
André M. Bastos; Jacob A. Donoghue; Scott L. Brincat; Meredith Mahnke; Jorge Yanar; Josefina Correa; Ayan S. Waite; Mikael Lundqvist; Jefferson Roy; Emery N. Brown; Earl K. Miller
Neural effects of propofol-induced unconsciousness and its reversal using thalamic stimulation Journal Article
In: eLife, vol. 10, pp. e60824, 2021.
The specific circuit mechanisms through which anesthetics induce unconsciousness have not been completely characterized. We recorded neural activity from the frontal, parietal, and temporal cortices and thalamus while maintaining unconsciousness in non-human primates (NHPs) with the anesthetic propofol. Unconsciousness was marked by slow frequency ($sim$1 Hz) oscillations in local field potentials, entrainment of local spiking to Up states alternating with Down states of little or no spiking activity, and decreased coherence in frequencies above 4 Hz. Thalamic stimulation ‘awakened' anesthetized NHPs and reversed the electrophysiologic features of unconsciousness. Unconsciousness is linked to cortical and thalamic slow frequency synchrony coupled with decreased spiking, and loss of higher-frequency dynamics. This may disrupt cortical communication/integration.
Amarender R. Bogadhi; Leor N. Katz; Anil Bollimunta; David A. Leopold; Richard J. Krauzlis
Midbrain activity shapes high-level visual properties in the primate temporal cortex Journal Article
In: Neuron, vol. 109, no. 4, pp. 690–699.e5, 2021.
Recent fMRI experiments identified an attention-related region in the macaque temporal cortex, here called the floor of the superior temporal sulcus (fSTS), as the primary cortical target of superior colliculus (SC) activity. However, it remains unclear which aspects of attention are processed by fSTS neurons and how or why these might depend on SC activity. Here, we show that SC inactivation decreases attentional modulations in fSTS neurons by increasing their activity for ignored stimuli in addition to decreasing their activity for attended stimuli. Neurons in the fSTS also exhibit event-related activity during attention tasks linked to detection performance, and this link is eliminated during SC inactivation. Finally, fSTS neurons respond selectively to particular visual objects, and this selectivity is reduced markedly during SC inactivation. These diverse, high-level properties of fSTS neurons all involve visual signals that carry behavioral relevance. Their dependence on SC activity could reflect a circuit that prioritizes cortical processing of events detected subcortically. Bogadhi and Katz et al. determine how activity from the midbrain superior colliculus (SC) is necessary for expression of high-level visual properties—attention-related modulation, event detection activity, and object-selective responses—in a newly identified region of the temporal cortex (fSTS) in primates.
Anna Bognár; Rufin Vogels
Moving a shape behind a slit: Partial shape representations in inferior temporal cortex Journal Article
In: Journal of Neuroscience, vol. 41, no. 30, pp. 6484–6501, 2021.
Current models of object recognition are based on spatial representations build from object features that are simultaneously present in the retinal image. However, one can recognize an object when it moves behind a static occlude, and only a small fragment of its shape is visible through a slit at a given moment in time. Such anorthoscopic perception requires spatiotemporal integration of the successively presented shape parts during slit-viewing. Human fMRI studies suggested that ventral visual stream areas represent whole shapes formed through temporal integration during anorthoscopic perception. To examine the time course of shape-selective responses during slit-viewing, we recorded the responses of single inferior temporal (IT) neurons of rhesus monkeys to moving shapes that were only partially visible through a static narrow slit. The IT neurons signaled shape identity by their response when that was cumulated across the duration of the shape presentation. Their shape preference during slit-viewing equaled that for static, whole-shape presentations. However, when analyzing their responses at a finer time scale, we showed that the IT neurons responded to particular shape fragments that were revealed by the slit. We found no evidence for temporal integration of slit-views that result in a whole-shape representation, even when the monkey was matching slit-views of a shape to static whole-shape presentations. These data suggest that, although the temporally integrated response of macaque IT neurons can signal shape identity in slit-viewing conditions, the spatiotemporal integration needed for the formation of a whole-shape percept occurs in other areas, perhaps downstream to IT.
Scott L. Brincat; Jacob A. Donoghue; Meredith K. Mahnke; Simon Kornblith; Mikael Lundqvist; Earl K. Miller
Interhemispheric transfer of working memories Journal Article
In: Neuron, vol. 109, no. 6, pp. 1055–1066, 2021.
Visual working memory (WM) storage is largely independent between the left and right visual hemifields/cerebral hemispheres, yet somehow WM feels seamless. We studied how WM is integrated across hemifields by recording neural activity bilaterally from lateral prefrontal cortex. An instructed saccade during the WM delay shifted the remembered location from one hemifield to the other. Before the shift, spike rates and oscillatory power showed clear signatures of memory laterality. After the shift, the lateralization inverted, consistent with transfer of the memory trace from one hemisphere to the other. Transferred traces initially used different neural ensembles from feedforward-induced ones, but they converged at the end of the delay. Around the time of transfer, synchrony between the two prefrontal hemispheres peaked in theta and beta frequencies, with a directionality consistent with memory trace transfer. This illustrates how dynamics between the two cortical hemispheres can stitch together WM traces across visual hemifields.
Sophie Brulé; Bastien Herlin; Pierre Pouget; Marcus Missal
Ketamine reduces temporal expectation in the rhesus monkey Journal Article
In: Psychopharmacology, vol. 238, no. 2, pp. 559–567, 2021.
Rationale: Ketamine, a well-known general dissociative anesthetic agent that is a non-competitive antagonist of the N-methyl-D-aspartate receptor, perturbs the perception of elapsed time and the expectation of upcoming events. Objective: The objective of this study was to determine the influence of ketamine on temporal expectation in the rhesus monkey. Methods: Two rhesus monkeys were trained to make a saccade between a central warning stimulus and an eccentric visual target that served as imperative stimulus. The delay between the warning and the imperative stimulus could take one of four different values randomly with the same probability (variable foreperiod paradigm). During experimental sessions, a subanesthetic low dose of ketamine (0.25–0.35 mg/kg) was injected i.m. and the influence of the drug on movement latency was measured. Results: We found that in the control conditions, saccadic latencies strongly decreased with elapsed time before the appearance of the visual target showing that temporal expectation built up during the delay period between the warning and the imperative stimulus. However, after ketamine injection, temporal expectation was significantly reduced in both subjects. In addition, ketamine also increased average movement latency but this effect could be dissociated from the reduction of temporal expectation. Conclusion: In conclusion, a subanesthetic dose of ketamine could have two independent effects: increasing reaction time and decreasing temporal expectation. This alteration of temporal expectation could explain cognitive deficits observed during ketamine use.
Matan Cain; Yehudit Botschko; Mati Joshua
Passive motor learning: Oculomotor adaptation in the absence of behavioral errors Journal Article
In: eNeuro, vol. 8, no. 2, pp. 1–12, 2021.
Motor adaptation is commonly thought to be a trial-and-error process in which the accuracy of movement improves with repetition of behavior. We challenged this view by testing whether erroneous movements are necessary for motor adaptation. In the eye movement system, the association between movements and errors can be disentangled, since errors in the predicted stimulus trajectory can be perceived even without movements. We modified a smooth pursuit eye movement adaptation paradigm in which monkeys learn to make an eye movement that predicts an upcoming change in target direction. We trained the monkeys to fixate on a target while covertly, an additional target initially moved in one direction and then changed direction after 250 ms. The monkeys showed a learned response to infre-quent probe trials in which they were instructed to follow the moving target. Additional experiments confirmed that probing learning or residual eye movements during fixation did not drive learning. These results show that motor adaptation can be elicited in the absence of movement and provide an animal model for studying the implementation of passive motor learning. Current models assume that the interaction between movement and error signals underlies adaptive motor learning. Our results point to other mechanisms that may drive learning in the absence of movement.
I. Caprara; P. Janssen
The causal role of three frontal cortical areas in grasping Journal Article
In: Cerebral Cortex, vol. 31, no. 9, pp. 4274–4288, 2021.
Efficient object grasping requires the continuous control of arm and hand movements based on visual information. Previous studies have identified a network of parietal and frontal areas that is crucial for the visual control of prehension movements. Electrical microstimulation of 3D shape-selective clusters in AIP during functional magnetic resonance imaging activates areas F5a and 45B, suggesting that these frontal areas may represent important downstream areas for object processing during grasping, but the role of area F5a and 45B in grasping is unknown. To assess their causal role in the frontal grasping network, we reversibly inactivated 45B, F5a, and F5p during visually guided grasping in macaque monkeys. First, we recorded single neuron activity in 45B, F5a, and F5p to identify sites with object responses during grasping. Then, we injected muscimol or saline to measure the grasping deficit induced by the temporary disruption of each of these three nodes in the grasping network. The inactivation of all three areas resulted in a significant increase in the grasping time in both animals, with the strongest effect observed in area F5p. These results not only confirm a clear involvement of F5p, but also indicate causal contributions of area F5a and 45B in visually guided object grasping.
Valeria C. Caruso; Daniel S. Pages; Marc A. Sommer; Jennifer M. Groh
Compensating for a shifting world: A quantitative comparison of the reference frame of visual and auditory signals across three multimodal brain areas Journal Article
In: Journal of Neurophysiology, vol. 126, pp. 82–94, 2021.
Stimulus locations are detected differently by different sensory systems, but ultimately they yield similar percepts and behavioral responses. How the brain transcends initial differences to compute similar codes is unclear. We quantitatively compared the reference frames of two sensory modalities, vision and audition, across three interconnected brain areas involved in generating saccades, namely the frontal eye fields (FEF), lateral and medial parietal cortex (LIP/MIP), and superior colliculus (SC). We recorded from single neurons in head-restrained monkeys performing auditory- and visually-guided saccades from variable initial fixation locations, and evaluated whether their receptive fields were better described as eye-centered, head-centered, or hybrid (i.e. not anchored uniquely to head- or eye-orientation). We found a progression of reference frames across areas and across time, with considerable hybrid-ness and persistent differences between modalities during most epochs/brain regions. For both modalities, the SC was more eye-centered than the FEF, which in turn was more eye-centered than the predominantly hybrid LIP/MIP. In all three areas and temporal epochs from stimulus onset to movement, visual signals were more eye-centered than auditory signals. In the SC and FEF, auditory signals became more eye-centered at the time of the saccade than they were initially after stimulus onset, but only in the SC at the time of the saccade did the auditory signals become predominantly eye-centered. The results indicate that visual and auditory signals both undergo transformations, ultimately reaching the same final reference frame but via different dynamics across brain regions and time. SIGNIFICANCE STATEMENT Models for visual-auditory integration posit that visual signals are eye-centered throughout the brain, while auditory signals are converted from head-centered to eye-centered coordinates. We show instead that both modalities largely employ hybrid reference frames: neither fully head-nor eye-centered. In three multimodal regions involved in orienting behaviors (Intraparietal Cortex, Frontal Eye Field and Superior Colliculus) these mixed codes persist in various proportions, shifting towards eye-centeredness both across time and across brain areas. Throughout, visual signals are more eye-centered than auditory signals, until a common predominantly eye-centered code for sound finally emerges during the saccade burst in the Superior Colliculus. In summary, visual and auditory signals reach the same final reference frame but via different dynamics across brain regions and time.
Mircea I. Chelaru; Sarah Eagleman; Ariana R. Andrei; Russell Milton; Natasha Kharas; Valentin Dragoi
High-order interactions explain the collective behavior of cortical populations in executive but not sensory areas Journal Article
In: Neuron, vol. 109, no. 24, pp. 3954–3961, 2021.
One influential view in neuroscience is that pairwise cell interactions explain the firing patterns of large populations. Despite its prevalence, this view originates from studies in the retina and visual cortex of anesthetized animals. Whether pairwise interactions predict the firing patterns of neurons across multiple brain areas in behaving animals remains unknown. Here, we performed multi-area electrical recordings to find that 2nd-order interactions explain a high fraction of entropy of the population response in macaque cortical areas V1 and V4. Surprisingly, despite the brain-state modulation of neuronal responses, the model based on pairwise interactions captured ∼90% of the spiking activity structure during wakefulness and sleep. However, regardless of brain state, pairwise interactions fail to explain experimentally observed entropy in neural populations from the prefrontal cortex. Thus, while simple pairwise interactions explain the collective behavior of visual cortical networks across brain states, explaining the population dynamics in downstream areas involves higher-order interactions.
Jan Churan; Andre Kaminiarz; Jakob C. B. Schwenk; Frank Bremmer
Coding of interceptive saccades in parietal cortex of macaque monkeys Journal Article
In: Brain Structure and Function, vol. 226, no. 8, pp. 2707–2723, 2021.
The oculomotor system can initiate remarkably accurate saccades towards moving targets (interceptive saccades) the processing of which is still under debate. The generation of these saccades requires the oculomotor centers to have information about the motion parameters of the target that then must be extrapolated to bridge the inherent processing delays. We investigated to what degree the information about motion of a saccade target is available in the lateral intra-parietal area (area LIP) of macaque monkeys for generation of accurate interceptive saccades. When a multi-layer neural network was trained based on neural discharges from area LIP around the time of saccades towards stationary targets, it was also able to predict the end points of saccades directed towards moving targets. This prediction, however, lagged behind the actual post-saccadic position of the moving target by $sim$ 80 ms when the whole neuronal sample of 105 neurons was used. We further found that single neurons differentially code for the motion of the target. Selecting neurons with the strongest representation of target motion reduced this lag to $sim$ 30 ms which represents the position of the moving target approximately at the onset of the interceptive saccade. We conclude that—similarly to recent findings from the Superior Colliculus (Goffart et al. J Neurophysiol 118(5):2890–2901)—there is a continuum of contributions of individual LIP neurons to the accuracy of interceptive saccades. A contribution of other gaze control centers (like the cerebellum or the frontal eye field) that further increase the saccadic accuracy is, however, likely.
Jan Churan; Andre Kaminiarz; Jakob C. B. Schwenk; Frank Bremmer
Action-dependent processing of self-motion in parietal cortex of macaque monkeys Journal Article
In: Journal of Neurophysiology, vol. 125, no. 6, pp. 2432–2443, 2021.
Successful interaction with the environment requires the dissociation of self-induced from externally induced sensory stimulation. Temporal proximity of action and effect is hereby often used as an indicator of whether an observed event should be interpreted as a result of own actions or not. We tested how the delay between an action (press of a touch bar) and an effect (onset of simulated self-motion) influences the processing of visually simulated self-motion in the ventral intraparietal area (VIP) of macaque monkeys. We found that a delay between the action and the start of the self-motion stimulus led to a rise of activity above the baseline activity before motion onset in a subpopulation of 21% of the investigated neurons. In the responses to the stimulus, we found a significantly lower sustained activity when the press of a touch bar and the motion onset were contiguous compared to the condition when the motion onset was delayed. We speculate that this weak inhibitory effect might be part of a mechanism that sharpens the tuning of VIP neurons during self-induced motion and thus has the potential to increase the precision of heading information that is required to adjust the orientation of self-motion in everyday navigational tasks. NEW & NOTEWORTHY Neurons in macaque ventral intraparietal area (VIP) are responding to sensory stimulation related to self-motion, e.g. visual optic flow. Here, we found that self-motion induced activation depends on the sense of agency, i.e., it differed when optic flow was perceived as self- or externally induced. This demonstrates that area VIP is well suited for study of the interplay between active behavior and sensory processing during self-motion.
Thomas Decramer; Elsie Premereur; Irene Caprara; Tom Theys; Peter Janssen
Temporal dynamics of neural activity in macaque frontal cortex assessed with large-scale recordings Journal Article
In: NeuroImage, vol. 236, pp. 118088, 2021.
The cortical network controlling the arm and hand when grasping objects consists of several areas in parietal and frontal cortex. Recently, more anterior prefrontal areas have also been implicated in object grasping, but their exact role is currently unclear. To investigate the neuronal encoding of objects during grasping in these prefrontal regions and their relation with other cortical areas of the grasping network, we performed large-scale recordings (more than 2000 responsive sites) in frontal cortex of monkeys during a saccade-reach-grasp task. When an object appeared in peripheral vision, the first burst of activity emerged in prearcuate areas (the FEF and area 45B), followed by dorsal and ventral premotor cortex, and a buildup of activity in primary motor cortex. After the saccade, prearcuate activity remained elevated while primary motor and premotor activity rose in anticipation of the upcoming arm and hand movement. Remarkably, a large number of premotor and prearcuate sites responded when the object appeared in peripheral vision and remained active when the object came into foveal vision. Thus, prearcuate and premotor areas continuously encode object information when directing gaze and grasping objects.
Kacie Dougherty; Brock M. Carlson; Michele A. Cox; Jacob A. Westerberg; Wolf Zinke; Michael C. Schmid; Paul R. Martin; Alexander Maier
Binocular suppression in the macaque lateral geniculate nucleus reveals early competitive interactions between the eyes Journal Article
In: eNeuro, vol. 8, no. 2, pp. 1–12, 2021.
The lateral geniculate nucleus (LGN) of the dorsal thalamus is the primary recipient of the two eyes' outputs. Most LGN neurons are monocular in that they are activated by visual stimulation through only one (dominant) eye. However, there are both intrinsic connections and inputs from binocular structures to the LGN that could provide these neurons with signals originating from the other (non-dominant) eye. Indeed, previous work introducing luminance differences across the eyes or using a single-contrast stimulus showed binocular modulation for single unit activity in anesthetized macaques and multiunit activity in awake macaques. Here, we sought to determine the influence of contrast viewed by both the non-dominant and dominant eyes on LGN single-unit responses in awake macaques. To do this, we adjusted each eye's signal strength by independently varying the contrast of stimuli presented to the two eyes. Specifically, we recorded LGN single unit spiking activity in two awake macaques while they viewed drifting gratings of varying contrast. We found that LGN neurons of all types [parvocellular (P), magno-cellular (M), and koniocellular (K)] were significantly suppressed when stimuli were presented at low contrast to the dominant eye and at high contrast to the non-dominant eye. Further, the inputs of the two eyes showed antagonistic interaction, whereby the magnitude of binocular suppression diminished with high contrast in the dominant eye, or low contrast in the non-dominant eye. These results suggest that the LGN represents a site of precortical binocular processing involved in resolving discrepant contrast differences between the eyes.
Norihiro Takakuwa; Kaoru Isa; Hirotaka Onoe; Jun Takahashi; Tadashi Isa
Contribution of the pulvinar and lateral geniculate nucleus to the control of visually guided saccades in blindsight monkeys Journal Article
In: Journal of Neuroscience, vol. 41, no. 8, pp. 1755–1768, 2021.
After damage to the primary visual cortex (V1), conscious vision is impaired. However, some patients can respond to visual stimuli presented in their lesion-affected visual field using residual visual pathways bypassing V1. This phenomenon is called “blindsight.” Many studies have tried to identify the brain regions responsible for blindsight, and the pulvinar and/or lateral geniculate nucleus (LGN) are suggested to play key roles as the thalamic relay of visual signals. However, there are critical problems regarding these preceding studies in that subjects with different sized lesions and periods of time after lesioning were investigated; furthermore, the ability of blindsight was assessed with different measures. In this study, we used double dissociation to clarify the roles of the pulvinar and LGN by pharmacological inactivation of each region and investigated the effects in a simple task with visually guided saccades (VGSs) using monkeys with a unilateral V1 lesion, by which nearly all of the contralesional visual field was affected. Inactivating either the ipsilesional pulvinar or LGN impaired VGS toward a visual stimulus in the affected field. In contrast, inactivation of the contralesional pulvinar had no clear effect, but inactivation of the contralesional LGN impaired VGS to the intact visual field. These results suggest that the pulvinar and LGN play key roles in performing the simple VGS task after V1 lesioning, and that the visuomotor functions of blindsight monkeys were supported by plastic changes in the visual pathway involving the pulvinar, which emerged after V1 lesioning.
Ryuji Takeya; Shuntaro Nakamura; Masaki Tanaka
Spontaneous grouping of saccade timing in the presence of task-irrelevant objects Journal Article
In: PLoS ONE, vol. 16, no. 3, pp. e0248530, 2021.
Sequential movements are often grouped into several chunks, as evidenced by the modulation of the timing of each elemental movement. Even during synchronized tapping with a metronome, we sometimes feel subjective accent for every few taps. To examine whether motor segmentation emerges during synchronized movements, we trained monkeys to generate a series of predictive saccades synchronized with visual stimuli which sequentially appeared for a fixed interval (400 or 600 ms) at six circularly arranged landmark locations. We found two types of motor segmentations that featured periodic modulation of saccade timing. First, the intersaccadic interval (ISI) depended on the target location and saccade direction, indicating that particular combinations of saccades were integrated into motor chunks. Second, when a task-irrelevant rectangular contour surrounding three landmarks ("inducer") was presented, the ISI significantly modulated depending on the relative target location to the inducer. All patterns of individual differences seen in monkeys were also observed in humans. Importantly, the effects of the inducer greatly decreased or disappeared when the animals were trained to generate only reactive saccades (latency >100 ms), indicating that the motor segmentation may depend on the internal rhythms. Thus, our results demonstrate two types of motor segmentation during synchronized movements: one is related to the hierarchical organization of sequential movements and the other is related to the spontaneous grouping of rhythmic events. This experimental paradigm can be used to investigate the underlying neural mechanism of temporal grouping during rhythm production.