Functional properties and firing features of monkey premotor neurons during sleep

Decades of neurophysiological research in awake, behaving primates have elucidated the role of the premotor (PM) cortex in controlling movement execution, encoding of objects and actions performed by others through a variety of neuronal cell classes, such as motor, canonical, peripersonal and mirror neurons. How do the firing properties of these neurons change during the different stages of sleep compared to wakefulness? In this study, we addressed this issue by leveraging a recently developed neurobehavioral platform for wireless intracortical recordings from the PM cortex of two Rhesus Macaques during both wakefulness and natural unconstrained nighttime sleep. First, we developed a novel unsupervised method to automatically classify different brain states using only intracortical biomarkers. Next, we tested single neuron properties during a reaching-grasping visuo-motor task in a traditional laboratory setting to functionally characterize neurons as self-type, other-type, or self-and-other type, and then studied their firing properties during sleep on the night following the testing. Interestingly, self-type and self-and-other type neurons characterized by narrow spikes exhibited strong suppression during NREM sleep while enhanced their activity during REM sleep as during wakefulness. In contrast, we found a set of cells apparently task-unrelated during wakefulness that mostly exhibited broad spikes and significantly increased their activity during NREM sleep relative to wakefulness and REM sleep. These findings uncover a previously unknown sleep micro-architecture within the premotor cortex, suggesting a switch between PM cortex neuronal populations involved in the orchestration of behavior during wakefulness and a subpopulation that remain silent during wakefulness but becomes active during NREM sleep, possibly contributing to sleep-related functions.