Thalamocortical interactions shape hierarchical neural variability during stimulus perception.

The brain is organized hierarchically to process sensory signals. But, how do functional connections within and across areas contribute to this hierarchical order? We addressed this problem in the thalamocortical network, while monkeys detected vibrotactile stimulus. During this task, we quantified neural variability and directed functional connectivity in simultaneously recorded neurons sharing the cutaneous receptive field within and across VPL and areas 3b and 1. Before stimulus onset, VPL and area 3b exhibited similar fast dynamics while area 1 showed slower timescales. During the stimulus presence, inter-trial neural variability increased along the network VPL-3b-1 while VPL established two main feedforward pathways with areas 3b and 1 to process the stimulus. This lower variability of VPL and area 3b was found to regulate feedforward thalamocortical pathways. Instead, intra-cortical interactions were only anticipated by higher intrinsic timescales in area 1. Overall, our results provide evidence of hierarchical functional roles along the thalamocortical network.

Neuronal Circuits for Social Decision-Making and Their Clinical Implications.

Social living facilitates individual access to rewards, cognitive resources, and objects that would not be otherwise accessible. There are, however, some drawbacks to social living, particularly when competing for scarce resources. Furthermore, variability in our ability to make social decisions can be associated with neuropsychiatric disorders. The neuronal mechanisms underlying social decision-making are beginning to be understood. The momentum to study this phenomenon has been partially carried over by the study of economic decision-making. Yet, because of the similarities between these different types of decision-making, it is unclear what is a social decision. Here, we propose a definition of social decision-making as choices taken in a context where one or more conspecifics are involved in the decision or the consequences of it. Social decisions can be conceptualized as complex economic decisions since they are based on the subjective preferences between different goods. During social decisions, individuals choose based on their internal value estimate of the different alternatives. These are complex decisions given that conspecifics beliefs or actions could modify the subject's internal valuations at every choice. Here, we first review recent developments in our collective understanding of the neuronal mechanisms and circuits of social decision-making in primates. We then review literature characterizing populations with neuropsychiatric disorders showing deficits in social decision-making and the underlying neuronal circuitries associated with these deficits.

Feed-forward information and zero-lag synchronization in the sensory thalamocortical circuit are modulated during stimulus perception.

The direction of functional information flow in the sensory thalamocortical circuit may play a role in stimulus perception, but, surprisingly, this process is poorly understood. We addressed this problem by evaluating a directional information measure between simultaneously recorded neurons from somatosensory thalamus (ventral posterolateral nucleus, VPL) and somatosensory cortex (S1) sharing the same cutaneous receptive field while monkeys judged the presence or absence of a tactile stimulus. During stimulus presence, feed-forward information (VPL → S1) increased as a function of the stimulus amplitude, while pure feed-back information (S1 → VPL) was unaffected. In parallel, zero-lag interaction emerged with increasing stimulus amplitude, reflecting externally driven thalamocortical synchronization during stimulus processing. Furthermore, VPL → S1 information decreased during error trials. Also, VPL → S1 and zero-lag interaction decreased when monkeys were not required to report the stimulus presence. These findings provide evidence that both the direction of information flow and the instant synchronization in the sensory thalamocortical circuit play a role in stimulus perception.

Multiple spatial representations interact to increase reach accuracy when coordinating a saccade with a reach.

Reaching is an essential behavior that allows primates to interact with the environment. Precise reaching to visual targets depends on our ability to localize and foveate the target. Despite this, how the saccade system contributes to improvements in reach accuracy remains poorly understood. To assess spatial contributions of eye movements to reach accuracy, we performed a series of behavioral psychophysics experiments in nonhuman primates (Macaca mulatta). We found that a coordinated saccade with a reach to a remembered target location increases reach accuracy without target foveation. The improvement in reach accuracy was similar to that obtained when the subject had visual information about the location of the current target in the visual periphery and executed the reach while maintaining central fixation. Moreover, we found that the increase in reach accuracy elicited by a coordinated movement involved a spatial coupling mechanism between the saccade and reach movements. We observed significant correlations between the saccade and reach errors for coordinated movements. In contrast, when the eye and arm movements were made to targets in different spatial locations, the magnitude of the error and the degree of correlation between the saccade and reach direction were determined by the spatial location of the eye and the hand targets. Hence, we propose that coordinated movements improve reach accuracy without target foveation due to spatial coupling between the reach and saccade systems. Spatial coupling could arise from a neural mechanism for coordinated visual behavior that involves interacting spatial representations.NEW & NOTEWORTHY How visual spatial representations guiding reach movements involve coordinated saccadic eye movements is unknown. Temporal coupling between the reach and saccade system during coordinated movements improves reach performance. However, the role of spatial coupling is unclear. Using behavioral psychophysics, we found that spatial coupling increases reach accuracy in addition to temporal coupling and visual acuity. These results suggest that a spatial mechanism to couple the reach and saccade systems increases the accuracy of coordinated movements.

Oculomatic: High speed, reliable, and accurate open-source eye tracking for humans and non-human primates.

BACKGROUND: Video-based noninvasive eye trackers are an extremely useful tool for many areas of research. Many open-source eye trackers are available but current open-source systems are not designed to track eye movements with the temporal resolution required to investigate the mechanisms of oculomotor behavior. Commercial systems are available but employ closed source hardware and software and are relatively expensive, limiting wide-spread use. NEW METHOD: Here we present Oculomatic, an open-source software and modular hardware solution to eye tracking for use in humans and non-human primates. RESULTS: Oculomatic features high temporal resolution (up to 600Hz), real-time eye tracking with high spatial accuracy (<0.5°), and low system latency (∼1.8ms, 0.32ms STD) at a relatively low-cost. COMPARISON WITH EXISTING METHOD(S): Oculomatic compares favorably to our existing scleral search-coil system while being fully non invasive. CONCLUSIONS: We propose that Oculomatic can support a wide range of research into the properties and neural mechanisms of oculomotor behavior.

Thalamocortical rhythms during a vibrotactile detection task.

To explore the role of oscillatory dynamics of the somatosensory thalamocortical network in perception and decision making, we recorded the simultaneous neuronal activity in the ventral posterolateral nucleus (VPL) of the somatosensory thalamus and primary somatosensory cortex (S1) in two macaque monkeys performing a vibrotactile detection task. Actively detecting a vibrotactile stimulus and reporting its perception elicited a sustained poststimulus beta power increase in VPL and an alpha power decrease in S1, in both stimulus-present and stimulus-absent trials. These oscillatory dynamics in the somatosensory thalamocortical network depended on the behavioral context: they were stronger for the active detection condition than for a passive stimulation condition. Furthermore, contrasting stimulus-present vs. stimulus-absent responses, we found that poststimulus theta power increased in both VPL and S1, and alpha/beta power decreased in S1, reflecting the monkey's perceptual decision but not the motor response per se. Additionally, higher prestimulus alpha power in S1 correlated with an increased probability of the monkey reporting a stimulus, regardless of the actual presence of a stimulus. Thus, we found task-related modulations in oscillatory activity, not only in the neocortex but also in the thalamus, depending on behavioral context. Furthermore, oscillatory modulations reflected the perceptual decision process and subsequent behavioral response. We conclude that these early sensory regions, in addition to their primary sensory functions, may be actively involved in perceptual decision making.

Transformation of the neural code for tactile detection from thalamus to cortex.

To understand how sensory-driven neural activity gives rise to perception, it is essential to characterize how various relay stations in the brain encode stimulus presence. Neurons in the ventral posterior lateral (VPL) nucleus of the somatosensory thalamus and in primary somatosensory cortex (S1) respond to vibrotactile stimulation with relatively slow modulations (∼100 ms) of their firing rate. In addition, faster modulations (∼10 ms) time-locked to the stimulus waveform are observed in both areas, but their contribution to stimulus detection is unknown. Furthermore, it is unclear whether VPL and S1 neurons encode stimulus presence with similar accuracy and via the same response features. To address these questions, we recorded single neurons while trained monkeys judged the presence or absence of a vibrotactile stimulus of variable amplitude, and their activity was analyzed with a unique decoding method that is sensitive to the time scale of the firing rate fluctuations. We found that the maximum detection accuracy of single neurons is similar in VPL and S1. However, VPL relies more heavily on fast rate modulations than S1, and as a consequence, the neural code in S1 is more tolerant: its performance degrades less when the readout method or the time scale of integration is suboptimal. Therefore, S1 neurons implement a more robust code, one less sensitive to the temporal integration window used to infer stimulus presence downstream. The differences between VPL and S1 responses signaling the appearance of a stimulus suggest a transformation of the neural code from thalamus to cortex.

Neural coding and perceptual detection in the primate somatosensory thalamus.

The contribution of the sensory thalamus to perception and decision making is not well understood. We addressed this problem by recording single neurons in the ventral posterior lateral (VPL) nucleus of the somatosensory thalamus while trained monkeys judged the presence or absence of a vibrotactile stimulus of variable amplitude applied to the skin of a fingertip. We found that neurons in the VPL nucleus modulated their firing rate as a function of stimulus amplitude, and that such modulations accounted for the monkeys' overall psychophysical performance. These neural responses did not predict the animals' decision reports in individual trials, however. Moreover, the sensitivity to changes in stimulus amplitude was similar when the monkeys' performed the detection task and when they were not required to report stimulus detection. These results suggest that the primate somatosensory thalamus likely provides a reliable neural representation of the sensory input to the cerebral cortex, where sensory information is transformed and combined with other cognitive components associated with behavioral performance.

Rivalry between afterimages and real images: the influence of the percept and the eye.

In binocular rivalry, the conscious percept alternates stochastically between two images shown to the two eyes. Both suppressed and dominant images form afterimages (AIs) whose strength depends on the perceptual state during induction. Counterintuitively, when these two AIs rival, the AI of the previously suppressed percept gains initial dominance, even when it is weaker. Here, we examined rivalry between afterimages, between real images, and between both to examine eye-based and binocular contributions to this effect. In all experiments, we found that for both AIs and real images, the suppressed percept consistently gained initial dominance following a long suppression period. Dominance reversals failed to occur following short suppression periods and depended on an abrupt change (removal) of the stimulus. With real images, results were replicated also when eye channels were exchanged during the abrupt change. The initial dominance of the weaker, previously suppressed percept is thus not due to its weaker contrast, to it being an afterimage, or to monocular adaptation effects as previously suggested. Instead, it is due to binocular, higher level effects that favor a perceptual switch after prolonged dominance. We discuss a plausible neural account for these findings in terms of neural interactions between binocular and eye-related stages.

Decoding a perceptual decision process across cortex.

Perceptual decisions arise from the activity of neurons distributed across brain circuits. But, decoding the mechanisms behind this cognitive operation across brain circuits has long posed a difficult problem. We recorded the neuronal activity of diverse cortical areas, while monkeys performed a vibrotactile discrimination task. We find that the encoding of the stimuli during the stimulus periods, working memory, and comparison periods is widely distributed across cortical areas. Notably, during the comparison and postponed decision report periods the activity of frontal brain circuits encode both the result of the sensory evaluation that corresponds to the monkey's possible choices and past information on which the decision is based. These results suggest that frontal lobe circuits are more engaged in the readout of sensory information from working memory, when it is required to be compared with other sensory inputs, than simply engaged in motor responses during this task.

Procedure for recording the simultaneous activity of single neurons distributed across cortical areas during sensory discrimination.

We report a procedure for recording the simultaneous activity of single neurons distributed across five cortical areas in behaving monkeys. The procedure consists of a commercially available microdrive adapted to a commercially available neural data collection system. The critical advantage of this procedure is that, in each cortical area, a configuration of seven microelectrodes spaced 250-500 mum can be inserted transdurally and each can be moved independently in the z axis. For each microelectrode, the data collection system can record the activity of up to five neurons together with the local field potential (LFP). With this procedure, we normally monitor the simultaneous activity of 70-100 neurons while trained monkeys discriminate the difference in frequency between two vibrotactile stimuli. Approximately 20-60 of these neurons have response properties previously reported in this task. The neuronal recordings show good signal-to-noise ratio, are remarkably stable along a 1-day session, and allow testing several protocols. Microelectrodes are removed from the brain after a 1-day recording session, but are reinserted again the next day by using the same or different x-y microelectrode array configurations. The fact that microelectrodes can be moved in the z axis during the recording session and that the x-y configuration can be changed from day to day maximizes the probability of studying simultaneous interactions, both local and across distant cortical areas, between neurons associated with the different components of this task.