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.
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. choice probability | neurometrics | psychophysics D etection of a sensory stimulus arises from evoked neural activity starting in the sensory receptors (1) and spanning several subcortical relay stations up to the cortex (2). Previous studies have described the neural activity of relay neurons within the sensory thalamus and its association with cortical activity; however, most of these studies were performed in anesthetized animals (3-7). Only a few studies have recorded thalamic neural activity from behaving subjects (8-11). Thus, the relationship between neuronal activity in the sensory thalamus and a subject's performance is not clear. In the case of the primate somatosensory thalamus, it is not known how neurons in the primate ventral posterior lateral (VPL) nucleus encode tactile stimuli and impact the animal's psychophysical behavior.To further investigate this relationship, we recorded the activity of single neurons in the VPL nucleus while trained monkeys reported the presence or absence of a mechanical vibration of variable amplitude applied to the skin of a fingertip (2). This task allowed us to study how the firing activity that encodes features of the stimulus is related to the animal's psychophysical performance and decision making capacity. We found that VPL neurons with either quickly adapting (QA) or slowly adapting (SA) response properties modulate their firing rates as functions of stimulus amplitude. On average, these modulations accounted for the monkeys' detection performance, in that neural and behavioral sensitivities were statistically the same, although the sensitivity of most neurons was lower than that of the monkeys when relatively short integration windows were used to measure the rate modulations. Moreover, variations in the firing rate of VPL neurons did not predict the monkeys' perceptual judgments or motor reports. Finally, the sensitivity to changes in stimulus amplitude was...
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. (1-4), and as the signal is relayed from one layer to the next, its representation in spatiotemporal patterns of activity may change (1). Previous studies have shown that, when a tactile vibratory stimulus is presented, neurons in the ventral posterior lateral (VPL) nucleus in the somatosensory thalamus and primary somatosensory cortex (S1, areas 3b and 1) respond by modulating their firing rates computed over a time scale of hundreds of milliseconds (5-9). Because these slow firing rate modulations occurring within relatively long time windows depend on amplitude and vibration frequency, they encode these key stimulus features. In addition, to varying degrees, evoked spikes in both areas also tend to be synchronized to the waveform of the applied mechanical stimulus, which, for frequencies <40 Hz, varies on a time scale of tens of milliseconds. This entrainment, which corresponds to fast firing rate modulations, also depends on stimulus amplitude (9), and so it too carries information about stimulus presence. However, it is unknown whether both the slow (∼100 ms) and fast (∼10 ms) modulations in firing rate contribute to perceptual performance during stimulus detection. Moreover, it is not clear whether the two time scales are equally important in VPL and S1, nor whether the capacity to signal stimulus presence changes from one area to the next.To investigate these issues, we recorded activity from single neurons in the VPL nucle...
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 m 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.monkeys ͉ multiple microelectrodes ͉ neuronal ensembles ͉ temporal interactions ͉ brain circuits
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.
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