Abstract

SummaryIn motor neocortex, preparatory activity predictive of specific movements is maintained by a positive feedback loop with the thalamus. Motor thalamus receives excitatory input from the cerebellum, which learns to generate predictive signals for motor control. The contribution of this pathway to neocortical preparatory signals remains poorly understood. Here, we show that, in a virtual reality conditioning task, cerebellar output neurons in the dentate nucleus exhibit preparatory activity similar to that in anterolateral motor cortex prior to reward acquisition. Silencing activity in dentate nucleus by photoactivating inhibitory Purkinje cells in the cerebellar cortex caused robust, short-latency suppression of preparatory activity in anterolateral motor cortex. Our results suggest that preparatory activity is controlled by a learned decrease of Purkinje cell firing in advance of reward under supervision of climbing fiber inputs signaling reward delivery. Thus, cerebellar computations exert a powerful influence on preparatory activity in motor neocortex.

Highlights

  • Persistent firing, a hallmark of cortical activity in frontal areas of the neocortex (Funahashi et al, 1989; Fuster and Alexander, 1971; Li et al, 2015; Tanji and Evarts, 1976; Wise, 1985), links past events to future actions

  • These results suggest that the cerebellum participates in programming future actions, but the details of how it may contribute to preparatory activity in the neocortex during goal-directed behavior remain to be determined

  • We identified the neural correlates of running, licking, or reward context by applying a generalized linear model (GLM) (Park et al, 2014) to classify anterolateral motor (ALM) neurons according to running speed, lick times, and reward times (Figure S2; see STAR Methods)

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Summary

Introduction

Persistent firing, a hallmark of cortical activity in frontal areas of the neocortex (Funahashi et al, 1989; Fuster and Alexander, 1971; Li et al, 2015; Tanji and Evarts, 1976; Wise, 1985), links past events to future actions. A positive thalamic feedback loop has been shown to be involved in the maintenance of preparatory signals in anterolateral motor (ALM) neocortex of mice (Guo et al, 2017), raising the possibility that extra-cortical inputs might regulate neocortical activity in advance of goal-directed movements (Kopec et al, 2015; Ohmae et al, 2017; Tanaka, 2007) via the thalamus. A recent study has established the existence of a loop between ALM and the cerebellum necessary for the maintenance of preparatory activity (Gao et al, 2018) These results suggest that the cerebellum participates in programming future actions, but the details of how it may contribute to preparatory activity in the neocortex during goal-directed behavior remain to be determined

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