Cerebellar contribution to preparatory activity in motor neocortex

In motor-related areas of the neocortex, preparatory neuronal activity predictive of specific actions emerges seconds in advance of movement and is maintained by a positive feedback loop with the thalamus. A major source of excitatory drive to the motor thalamus is the cerebellum, which has been implicated in coordination and timing of learned actions. However, the cerebellar contribution to neocortical signals coupled to movement planning remains poorly understood. Here we show that cerebellar output neurons in the dentate nucleus exhibit preparatory ramping activity in anticipation of expected rewards in a virtual reality conditioning task, a profile similar to that recorded in anterolateral motor neocortex (ALM). The preparatory activity in the dentate nucleus is controlled by a disinhibitory circuit involving inhibitory Purkinje cells in the cerebellar cortex, many of which suppress their firing in advance of rewards. Silencing the activity in the dentate nucleus by photoactivation of Purkinje cells caused robust, short-latency suppression in the majority of ALM neurons exhibiting preparatory activity. Thus, preparatory signals in motor neocortex require the output of the cerebellum. We suggest that the reciprocal circuitry between neocortex and cerebellum generates the sequence of activity required for planning and temporal coordination of learned, goal- directed actions.