Purkinje Cell Activity Determines the Timing of Sensory-Evoked Motor Initiation

Shinichiro Tsutsumi,Oscar Chadney,Tin-Long Yiu,Edgar Bäumler,Lavinia Faraggiana,Maxime Beau,Michael Häusser

doi:10.1016/j.celrep.2020.108537

Abstract

SummaryCerebellar neurons can signal sensory and motor events, but their role in active sensorimotor processing remains unclear. We record and manipulate Purkinje cell activity during a task that requires mice to rapidly discriminate between multisensory and unisensory stimuli before motor initiation. Neuropixels recordings show that both sensory stimuli and motor initiation are represented by short-latency simple spikes. Optogenetic manipulation of short-latency simple spikes abolishes or delays motor initiation in a rate-dependent manner, indicating a role in motor initiation and its timing. Two-photon calcium imaging reveals task-related coherence of complex spikes organized into conserved alternating parasagittal stripes. The coherence of sensory-evoked complex spikes increases with learning and correlates with enhanced temporal precision of motor initiation. These results suggest that both simple spikes and complex spikes govern sensory-driven motor initiation: simple spikes modulate its latency, and complex spikes refine its temporal precision, providing specific cellular substrates for cerebellar sensorimotor control.

Highlights

Timed initiation of motor actions in a rapidly changing environment is essential for survival
Our findings indicate that both simple spikes and complex spikes contribute to the initiation of sensorydriven behavior, in which simple spikes can modulate the timing of initiation and coherent complex spikes sharpen its temporal precision
The sensory-evoked lick rate remained unchanged regardless of the presence of photostimulation once initiated (Hit versus Hit trials with photostimulation (Hit+S); n = 72 and 30 trials; 7 ± 1 versus 7 ± 2 licks/ s; p = 0.38) (Figures S1N and S1O). These results suggest that in this task, physiological simple spike firing in Crus I Purkinje cells is crucial for the rapid initiation of sensory-driven motor actions, but not for the motor actions per se

Summary

Introduction

Timed initiation of motor actions in a rapidly changing environment is essential for survival. The cerebellum is well positioned to participate in this process, because it receives sensory and motor information from the periphery and from neocortical sources This information is conveyed to the cerebellar cortex via two routes: the mossy fiber-granule cell-parallel fiber pathway and the inferior oliveclimbing fiber pathway. It is known that whiskerrelated neocortical sensory and motor streams converge on lobule Crus I (Proville et al, 2014) in the lateral cerebellum, which communicates with higher-order brain areas (Dum et al, 2002) and is important in active sensory processing for purposeful behavior (Bower, 1997; Gao et al, 1996) This suggests that Crus I is an ideal target for understanding how sensory and motor representations are linked

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Conclusion