Rapid Motor Adaptation via Population-level Modulation of Cerebellar Error Signals

Abstract

A core principle of cerebellar learning theories is that climbing fibers from the inferior olive convey error signals about movement execution to Purkinje cells in the cerebellar cortex. These inputs trigger synaptic changes which are purported to drive progressive adjustment of future movements. Individually, binary complex spike signals lack information about the sign and magnitude of errors which presents a problem for cerebellar learning paradigms exhibiting fast adaptation. Using a newly developed behavioral paradigm in mice, we introduced sensorimotor perturbations into a simple joystick pulling behavior and found parasagittal bands of Purkinje cells with reciprocal modulation of complex spike activity. Whereas complex spiking showed little modulation in the unperturbed condition, alternating bands were activated or inhibited when the perturbation was introduced, and this modulation encoded the sign and magnitude of the resulting sensorimotor mismatch. These findings provide an important piece of information for the understanding of cerebellar learning that helps to explain how the cerebellum could use supervised learning to quickly adapt motor behavior in response to perturbations. One-Sentence SummaryPopulations of Purkinje cells in the cerebellum facilitate trial-by-trial movement refinement by converting binary signals from movement errors into graded signals that encode the errors direction and magnitude.