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.T he prominent posterior α-rhythm (8-14 Hz) was first described by Hans Berger (1) and long considered to reflect cortical idling (2, 3). To a large extent, the α-rhythm has been ignored by animal neurophysiologists (but see ref. 4) and considered to be of little functional relevance. Thus, it remains largely unknown how ongoing α-oscillations relate to neuronal firing.In contrast to the idling hypothesis, converging electrophysiological evidence in humans suggests that α-oscillations play an important functional role in cognitive processing (5-7). In particular, α-activity might serve to shape the state of sensory brain regions to direct the flow of information and optimize performance (8). In support of this idea, several studies on visual perception have shown that anticipatory α-activity reflects the orienting of attention (9-14) and influences detection performance (15-17). Recently, it was shown that the functionality of α-oscillations can be generalized to the somatosensory system (18-21). Furthermore, α-activity has been implicated in visual (22-25), auditory (26), and somatosensory working-memory performance (27).These studies strongly suggest that decreased α-activity facilitates processing in task-relevant brain regions, whereas increased α-activity functions to suppress distracting input in task-irrelevant regions. However, given the strong oscillatory nature of the α-activity, it is less clear how it influences processing in a phasic manner. It has been suggested that α-oscillations serve to depress processing every ∼100 ms by a mechanism of pulsed inhibition (5,(28)(29)(30). In support of this notion, it has recently been demonstrated that perception is modulated by the prestimulus phase of the α-rhythm (31, 32). Likewise, it was recently shown that the magnitude of the blood-oxygen level-dependent signal in response to a visual...

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 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. P erceptual decision making has been extensively studied in the monkey somatosensory system (1-3) by using a vibrotactile discrimination task (4). Various task aspects (e.g., stimulus encoding, retention, and comparison) turned out to be widely distributed across cortical areas. Notably, during the comparison and decision periods, spike rates in several premotor, motor, and prefrontal regions encoded both the result of the decision process and information on which it was based (2, 3, 5, 6).Although important insight has been gained from these studies focusing on single-unit spikes, additional aspects of neuronal (population) dynamics are reflected by oscillatory activity. From a network perspective, it is still largely unknown what role oscillations in the LFPs play in perceptual decision making. Work in humans using magneto/electro-encephalography (M/EEG) suggests that oscillations in the beta and gamma bands play a significant role in perceptual working memory and decision making (reviewed in refs. 7 and 8), which was recently confirmed for the somatosensory system (9, 10). How these oscillations detected at the scalp level are reflected by intracranially recorded neuronal oscillatory activity remains largely unexplored (but see ref. 11).Here, we asked how oscillatory activity contributes to the perceptual decision process. We recorded LFPs across five cortical areas within the sensorimotor network in a monkey performing a somatosensory discrimination task (12). LFPs reflect synchronized activity in a populatio...

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 animal's 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.

Coherent oscillations in the theta-to-gamma frequency range have been proposed as a mechanism that coordinates neural activity in large-scale cortical networks in sensory, motor, and cognitive tasks. Whether this mechanism also involves coherent oscillations at delta frequencies (1-4 Hz) is not known. Rather, delta oscillations have been associated with slow-wave sleep. Here, we show coherent oscillations in the delta frequency band between parietal and frontal cortices during the decision-making component of a somatosensory discrimination task. Importantly, the magnitude of this delta-band coherence is modulated by the different decision alternatives. Furthermore, during control conditions not requiring decision making, delta-band coherences are typically much reduced. Our work indicates an important role for synchronous activity in the delta frequency band when large-scale, distant cortical networks coordinate their neural activity during decision making.synchrony | low-frequency rhythm | brain circuits