Mechanisms of motor learning in the cerebellum¹

Abstract

How the elaborate neuronal circuit in the cerebellum operates and is involved in motor learning is a question addressed in earnest in studies on the cerebellum. During the past four decades, experimental studies have revealed circuit and module structures of the cerebellum, established long-term depression (LTD) as a unique and characteristic type of synaptic plasticity in the cerebellum, and analysed signal contents of activates of cerebellar neurons related to motor learning. In the 1990s, these studies were developed to detailed analyses of the signal transduction underlying LTD, and to uncovering the involvement of the cerebellum in cognitive function. On the other hand, theoretical studies yielded epochal Marr–Albus network models of the cerebellum around 1970, and introduced control system principles explaining the essential roles of the cerebellum in motor learning as providing internal models, both forward and inverse. The author maintains the hypothesis that reorganisation of the neuronal circuit by error-driven induction of LTD constitutes the major memory and learning mechanisms of the cerebellum. In this article, we examine the validity of the hypothesis in light of currently available data in recent studies of the cerebellum.

Introduction

Motor learning is a function of the brain for acquiring new repertoires of movements and skills to perform them through practice, and it involves many areas of the brain. The prefrontal cerebral cortex is responsible for planning movements, and its premotor area for programming movements. The motor cortex, which forms commands sent to the lower motor centers in the brain stem and spinal cord, undergoes reorganization in motor learning [3]. Sensory and temporoparietal association areas may also be involved in learning to improve the perceptual capability required for movements. At subcortical levels, the basal ganglia and cerebellum are the two major structures involved in motor learning. Even the brain stem and spinal cord may contribute to motor learning to a certain extent based on their experience-dependent plasticity.

Results of classic lesion studies, as compiled by Dow and Moruzzi [14], suggest that the contribution of the cerebellum to motor learning is to enable us to learn to perform accurate and smooth movements, even at high speeds and without visual feedback. A central question addressed has been how this function originates from the elaborate neuronal circuit structure of the cerebellum as already described in detail early in the 20th century by Cajal [6]. Before 1960, while researchers with an experimental focus were engaged in anatomical [37] and lesion studies of the cerebellum [14], theorists formulated general neuronal network models as represented by Hebb’s [25] neuron assembly and Rosenblatt’s [72] Simple Perceptron. The two groups began to work closely with each other when an elaborate neuronal circuit in the cerebellum was revealed, as summarised in Eccles et al. [16] (Fig. 1). This experimental–theoretical interaction resulted in proposals of epochal network theories of the cerebellum by Marr [57], Albus [2] and others around 1970, which motivated subsequent experimental efforts to verify the theories. Much effort has since been devoted both theoretically and experimentally to produce a significant progress in our understanding of neural mechanisms of the cerebellum. In this article, we focus on the hypothesis that error-driven LTD-based reorganization of the neuronal circuit in a microcomplex, functional module of the cerebellum is a major mechanism of motor learning.