Abstract
Surprisingly little is known about neural activity in the sleeping cerebellum. Using long-term wireless recording, we characterised dynamic cerebro-thalamo-cerebellar interactions during natural sleep in monkeys. Similar sleep cycles were evident in both M1 and cerebellum as cyclical fluctuations in firing rates as well as a reciprocal pattern of slow waves and sleep spindles. Directed connectivity from motor cortex to the cerebellum suggested a neocortical origin of slow waves. Surprisingly however, spindles were associated with a directional influence from the cerebellum to motor cortex, conducted via the thalamus. Furthermore, the relative phase of spindle-band oscillations in the neocortex and cerebellum varied systematically with their changing amplitudes. We used linear dynamical systems analysis to show that this behaviour could only be explained by a system of two coupled oscillators. These observations appear inconsistent with a single spindle generator within the thalamo-cortical system, and suggest instead a cerebellar contribution to neocortical sleep spindles. Since spindles are implicated in the off-line consolidation of procedural learning, we speculate that this may involve communication via cerebello-thalamo-neocortical pathways in sleep.
Highlights
The cerebellum plays a key role in motor learning (Bastian, 2006), while sleep is vital for consolidating and even enhancing new motor skills (Nishida and Walker, 2007; Diekelmann and Born, 2010; Fogel, Albouy et al 2017)
In two animals we recorded simultaneous spiking activity from M1 and cerebellum using moveable microwires. Firing rates of both M1 and cerebellar neurons were generally lower in sleep than during the day, but activity in both areas fluctuated with a period of approximately 1 hour (Fig. 1C), matching the known sleep cycle in monkeys (Xu, de Carvalho et al 2019)
We have shown that the cerebellum is an active participant of sleep, exhibiting sleep cycles characterised by fluctuating firing patterns and reciprocal fast/slow oscillations that bear a remarkable similarity to the neocortex
Summary
The cerebellum plays a key role in motor learning (Bastian, 2006), while sleep is vital for consolidating and even enhancing new motor skills (Nishida and Walker, 2007; Diekelmann and Born, 2010; Fogel, Albouy et al 2017). Of particular interest are sleep spindles, as these are associated both with cerebellar BOLD responses (Schabus, Dang-Vu et al 2007; Fogel, Albouy et al 2017) as well as off-line consolidation of procedural tasks such as motor sequence learning (Nishida and Walker, 2007; Diekelmann and Born, 2010; Fogel, Albouy et al 2017). This would suggest that cerebellar activation associated with spindles reflects a downstream response, perhaps mediated via cortico-ponto-cerebellar pathways.
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