Acquisition of Neural Learning in Cerebellum and Cerebral Cortex for Smooth Pursuit Eye Movements

Abstract

We evaluated the emergence of neural learning in the frontal eye fields (FEF(SEM)) and the floccular complex of the cerebellum while monkeys learned a precisely timed change in the direction of pursuit eye movement. For each neuron, we measured the time course of changes in neural response across a learning session that comprised at least 100 repetitions of an instructive change in target direction. In both areas, the average population learning curves tracked the behavioral changes with high fidelity, consistent with possible roles in driving learning. However, the learning curves of individual neurons sometimes bore little relation to the smooth, monotonic progression of behavioral learning. In the FEF(SEM), neural learning was episodic. For individual neurons, learning appeared at different times during the learning session and sometimes disappeared by the end of the session. Different FEF(SEM) neurons expressed maximal learning at different times relative to the acquisition of behavioral learning. In the floccular complex, many Purkinje cells acquired learned simple-spike responses according to the same time course as behavioral learning and retained their learned responses throughout the learning session. A minority of Purkinje cells acquired learned responses late in the learning session, after behavioral learning had reached an asymptote. We conclude that learning in single neurons can follow a very different time course from behavioral learning. Both the FEF(SEM) and the floccular complex contain representations of multiple temporal components of learning, with different neurons contributing to learning at different times during the acquisition of a learned movement.