Conserved Population Dynamics in the Cerebro-Cerebellar System between Waking and Sleep

Despite the importance of the cerebellum for motor learning, and the recognized role of sleep in motor memory consolidation, surprisingly little is known about neural activity in the sleeping cerebro-cerebellar system. Here, we used wireless recording from primary motor cortex (M1) and the cerebellum in three female monkeys to examine the relationship between patterns of single-unit spiking activity observed during waking behavior and in natural sleep. Across the population of recorded units, we observed similarities in the timing of firing relative to local field potential features associated with both movements during waking and up state during sleep. We also observed a consistent pattern of asymmetry in pairwise cross-correlograms, indicative of preserved sequential firing in both wake and sleep at low frequencies. Despite the overall similarity in population dynamics between wake and sleep, there was a global change in the timing of cerebellar activity relative to motor cortex, from contemporaneous in the awake state to motor cortex preceding the cerebellum in sleep. We speculate that similar population dynamics in waking and sleep may imply that cerebellar internal models are activated in both states, despite the absence of movement when asleep. Moreover, spindle frequency coherence between the cerebellum and motor cortex may provide a mechanism for cerebellar computations to influence sleep-dependent learning processes in the motor cortex.SIGNIFICANCE STATEMENT It is well known that sleep can lead to improved motor performance. One possibility is that off-line learning results from neural activity during sleep in brain areas responsible for the control of movement. In this study we show for the first time that neuronal patterns in the cerebro-cerebellar system are conserved during both movements and sleep up-states, albeit with a shift in the relative timing between areas. Additionally, we show the presence of simultaneous M1-cerebellar spike coherence at spindle frequencies associated with up-state replay and postulate that this is a mechanism whereby a cerebellar internal model can shape plasticity in neocortical circuits during sleep.