Rogelio Luna

α-Oscillations in the monkey sensorimotor network influence discrimination performance by rhythmical inhibition of neuronal spiking

Extensive work in humans using magneto- and electroencephalography strongly suggests that decreased oscillatory α-activity (8–14 Hz) facilitates processing in a given region, whereas increased α-activity serves to actively suppress irrelevant or interfering processing. However, little work has been done to understand how α-activity is linked to neuronal firing. Here, we simultaneously recorded local field potentials and spikes from somatosensory, premotor, and motor regions while a trained monkey performed a vibrotactile discrimination task. In the local field potentials we observed strong activity in the α-band, which decreased in the sensorimotor regions during the discrimination task. This α-power decrease predicted better discrimination performance. Furthermore, the α-oscillations demonstrated a rhythmic relation with the spiking, such that firing was highest at the trough of the α-cycle. Firing rates increased with a decrease in α-power. These findings suggest that α-oscillations exercise a strong inhibitory influence on both spike timing and firing rate. Thus, the pulsed inhibition by α-oscillations plays an important functional role in the extended sensorimotor system.

Neural codes for perceptual discrimination in primary somatosensory cortex

We sought to determine the neural code(s) for frequency discrimination of vibrotactile stimuli. We tested five possible candidate codes by analyzing the responses of single neurons recorded in primary somatosensory cortex of trained monkeys while they discriminated between two consecutive vibrotactile stimuli. Differences in the frequency of two stimuli could be discriminated using information from (i) time intervals between spikes, (ii) average spiking rate during each stimulus, (iii) absolute number of spikes elicited by each stimulus, (iv) average rate of bursts of spikes or (v) absolute number of spike bursts elicited by each stimulus. However, only a spike count code, in which spikes are integrated over a time window that has most of its mass in the first 250 ms of each stimulus period, covaried with behavior on a trial-by-trial basis, was consistent with psychophysical biases induced by manipulation of stimulus duration, and produced neurometric discrimination thresholds similar to behavioral psychophysical thresholds.

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 monkeys 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.

Beta oscillations in the monkey sensorimotor network reflect somatosensory decision making

The neuronal correlate of perceptual decision making has been extensively studied in the monkey somatosensory system by using a vibrotactile discrimination task, showing that stimulus encoding, retention, and comparison are widely distributed across cortical areas. However, from a network perspective, it is not known what role oscillations play in this task. We recorded local field potentials (LFPs) from diverse cortical areas of the sensorimotor system while one monkey performed the vibrotactile discrimination task. Exclusively during stimulus presentation, a periodic response reflecting the stimulus frequency was observed in the somatosensory regions, suggesting that after initial processing, the frequency content of the stimulus is coded in some other way than entrainment. Interestingly, we found that oscillatory activity in the beta band reflected the dynamics of decision making in the monkey sensorimotor network. During the comparison and decision period, beta activity showed a categorical response that reflected the decision of the monkey and distinguished correct from incorrect responses. Importantly, this differential activity was absent in a control condition that involved the same stimulation and response but no decision making required, suggesting it does not merely reflect the maintenance of a motor plan. We conclude that beta band oscillations reflect the temporal and spatial dynamics of the accumulation and processing of evidence in the sensorimotor network leading to the decision outcome.

Do Sensory Cortices Process More than One Sensory Modality during Perceptual Judgments

Recent studies have reported that sensory cortices process more than one sensory modality, challenging the long-lasting concept that they process only one. However, both the identity of these multimodal responses and whether they contribute to perceptual judgments is unclear. We recorded from single neurons in somatosensory cortices and primary auditory cortex while trained monkeys discriminated, on interleaved trials, either between two tactile flutter stimuli or between two acoustic flutter stimuli, and during discrimination sets that combined these two sensory modalities. We found neurons in these sensory cortices that responded to stimuli that are not of their principal sensory modality during these tasks. However, the identity of the stimulus could only be decoded from responses to their principal sensory modality during the stimulation periods and not during the processing steps that link sensation and decision making. These results suggest that multimodal encoding and perceptual judgments in these tasks occur outside the sensory cortices studied here.

Neural correlates of a postponed decision report

Depending on environmental demands, a decision based on a sensory evaluation may be either immediately reported or postponed for later report. If postponed, the decision must be held in memory. But what exactly is stored by the underlying memory circuits, the final decision itself or the sensory information that led to it? Here, we report that, during a postponed decision report period, the activity of medial premotor cortex neurons encodes both the result of the sensory evaluation that corresponds to the monkeys possible choices and past sensory information on which the decision is based. These responses could switch back and forth with remarkable flexibility across the postponed decision report period. Moreover, these responses covaried with the animals decision report. We propose that maintaining in working memory the original stimulus information on which the decision is based could serve to continuously update the postponed decision report in this task.

From sensation to action.

Key to understanding somatosensation is the form of how the mechanical stimuli are represented in the evoked neuronal activity of the brain. Here, we focus on studies that address the question of which components of the evoked neuronal activity in the somatosensory system represent the stimulus features. We review experiments that probe whether these neuronal representations are essential to somatosensation. We also discuss recent results that suggest how the somatosensory stimuli are represented in the brain during short-term memory. Finally, we review data that show the neuronal correlates of a decision during somatosensory perception.

Dynamics of Cortical Neuronal Ensembles Transit from Decision Making to Storage for Later Report

Decisions based on sensory evaluation during single trials may depend on the collective activity of neurons distributed across brain circuits. Previous studies have deepened our understanding of how the activity of individual neurons relates to the formation of a decision and its storage for later report. However, little is known about how decision-making and decision maintenance processes evolve in single trials. We addressed this problem by studying the activity of simultaneously recorded neurons from different somatosensory and frontal lobe cortices of monkeys performing a vibrotactile discrimination task. We used the hidden Markov model to describe the spatiotemporal pattern of activity in single trials as a sequence of firing rate states. We show that the animals decision was reliably maintained in frontal lobe activity through a selective state sequence, initiated by an abrupt state transition, during which many neurons changed their activity in a concomitant way, and for which both latency and variability depended on task difficulty. Indeed, transitions were more delayed and more variable for difficult trials compared with easy trials. In contrast, state sequences in somatosensory cortices were weakly decision related, had less variable transitions, and were not affected by the difficulty of the task. In summary, our results suggest that the decision process and its subsequent maintenance are dynamically linked by a cascade of transient events in frontal lobe cortices.

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 μm 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.

Coding perceptual discrimination in the somatosensory thalamus.

The sensory thalamus is classically viewed as a relay station of sensory information to cortex, but recent studies suggest that it is sensitive to cognitive demands. There are, however, few experiments designed to test whether this is so. We addressed this problem by analyzing the responses of single neurons recorded in the somatosensory thalamus while trained monkeys reported a decision based on the comparison of two mechanical vibration frequencies applied sequentially to one fingertip. In this task, monkeys must hold the first stimulus frequency (f1) in working memory and compare it to the current sensory stimulus (f2) and must postpone the decision report until a cue triggers the decision motor report, i.e., whether f2 > f1 or f2 < f1. We found that thalamic somatosensory neurons encoded the stimulus frequency either in their periodicity and firing-rate responses, but only during the stimulus periods and not during the working memory and decision components of this task. Furthermore, correlation analysis between behavior and stimulus coding showed that only the firing rate modulations accounted for the overall psychophysical performance. However, these responses did not predict the animal’s decision reports on individual trials. Moreover, the sensitivity to changes in stimulus frequency was similar when the monkeys performed the vibrotactile discrimination task and when they were not required to report discrimination. These results suggest that the somatosensory thalamus behaves as a relay station of sensory information to the cortex and that it is insensitive to the cognitive demands of the task used here.