Abstract

Motor learning occurs through interactions between the cerebellar circuit and cellular plasticity at different sites. Previous work has established plasticity in brain slices and suggested plausible sites of behavioral learning. We now reveal what actually happens in the cerebellum during short-term learning. We monitor the expression of plasticity in the simple-spike firing of cerebellar Purkinje cells during trial-over-trial learning in smooth pursuit eye movements of monkeys. Our findings imply that: 1) a single complex-spike response driven by one instruction for learning causes short-term plasticity in a Purkinje cell's mossy fiber/parallel-fiber input pathways; 2) complex-spike responses and simple-spike firing rate are correlated across the Purkinje cell population; and 3) simple-spike firing rate at the time of an instruction for learning modulates the probability of a complex-spike response, possibly through a disynaptic feedback pathway to the inferior olive. These mechanisms may participate in long-term motor learning. DOI: http://dx.doi.org/10.7554/eLife.01574.001.

Highlights

  • Learning is an adaptive change in behavior that results from ‘plasticity’ in the cellular mechanisms of synaptic transmission and/or spike generation in the nervous system

  • Our long-term goal is to understand what happens in the brain to cause motor learning when an instructive target motion is repeated many times

  • The studies of neural responses in intact animals have measured neural representations of motor memories and have inferred what happened in the cerebellum during motor learning

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Summary

Introduction

Learning is an adaptive change in behavior that results from ‘plasticity’ in the cellular mechanisms of synaptic transmission and/or spike generation in the nervous system. Our thinking about how the brain learns has been influenced heavily by the discovery of a form of synaptic plasticity called long-term potentiation (aka ‘LTP’). Our premise is that behavioral learning involves multiple forms of plasticity at multiple sites in an essential neural circuit for the behavior. Different forms of plasticity may be deployed at different sites over different time courses during learning. It is critical to understand when and where different forms of plasticity contribute to learning, and how circuits transform plasticity into changes in neural activity patterns. We start by analyzing a form of learning that occurs on the time scale of a single learning trial, with the premise that the analysis of short-term events will provide insight into circuit dynamics and plasticity that might play roles during long-term learning

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