Links from complex spikes to local plasticity and motor learning in the cerebellum of awake-behaving monkeys

The hypothesis of cerebellar learning proposes that complex spikes in Purkinje cells engage mechanisms of plasticity in the cerebellar cortex; in turn, changes in the cerebellum depress the simple spike response of Purkinje cells to a given stimulus and cause the adaptive modification of a motor behavior. Although many elements of this hypothesis have been supported by prior experiments, the links between complex spikes, simple spike plasticity, and behavior have not yet been examined simultaneously during the learning process. We now pioneer a trial-by-trial analysis of Purkinje cell responses in awake-behaving monkeys, with results that strongly favor a causal role for complex spikes in the induction of cerebellar plasticity during a simple motor learning task. We show that the presence of a complex spike on one learning trial is linked to a substantial depression of simple spike responses on the subsequent trial, at a time when behavioral learning is expressed.