Review
Complementary roles of basal ganglia and cerebellum in learning and motor control

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Abstract

The classical notion that the basal ganglia and the cerebellum are dedicated to motor control has been challenged by the accumulation of evidence revealing their involvement in non-motor, cognitive functions. From a computational viewpoint, it has been suggested that the cerebellum, the basal ganglia, and the cerebral cortex are specialized for different types of learning: namely, supervised learning, reinforcement learning and unsupervised learning, respectively. This idea of learning-oriented specialization is helpful in understanding the complementary roles of the basal ganglia and the cerebellum in motor control and cognitive functions.

Introduction

The basal ganglia and the cerebellum have long been known to be involved in motor control because of the marked motor deficits associated with their damage. However, the exact aspects of motor control that they are involved in under normal conditions has not been clear. Traditionally, the cerebellum was supposed to be involved in real-time fine tuning of movement [1], [2], whereas the basal ganglia were thought to be involved in the selection and inhibition of action commands [3]. However, these distinctions were by no means clear-cut [4]. Furthermore, an ever-increasing number of brain-imaging studies show that the basal ganglia and the cerebellum are involved in non-motor tasks, such as mental imagery [5], [6], sensory processing [7], [8], [9], planning [10], [11, [12], attention [13], and language [14], [15], [16], [17].

Both the basal ganglia and the cerebellum have recurrent connections with the cerebral cortex [1], [3]. Anatomical studies using transneuronally transported viruses [18], [19], [20], [21 have clearly shown that the projections from the basal ganglia and the cerebellum through the thalamus to the cortex constitute multiple ‘parallel’ channels. The diversity of the target cortical areas — not only the motor and premotor cortices but also the prefrontal [18], temporal [22], and parietal cortices [19] — is in agreement with their involvement in diverse functions. However, the neural activity tuning and the lesion effects of a subsection of the basal ganglia or the cerebellum tend to be similar to those of the cortical area to which it projects [21radical dotradical dot]. This makes it difficult to distinguish the specific roles of the basal ganglia and the cerebellum simply from recording or lesion results.

Is it then impossible to characterize the specific information processing in the basal ganglia and the cerebellum? Despite their diverse, overlapping target cortical areas, the basal ganglia and the cerebellum have unique local circuit architectures and synaptic mechanisms. This strongly suggests that each structure is specialized for a particular type of information processing [23]. In this review, a novel view is introduced in which the basal ganglia and the cerebellum are specialized for different types of learning algorithms: reward-based learning in the basal ganglia and error-based learning in the cerebellum [24radical dotradical dot]. Recent experimental as well as modeling studies on the basal ganglia and the cerebellum are reviewed from this viewpoint of learning-oriented specialization.

Section snippets

Learning-oriented specialization

Theoretical models of learning in different parts of the brain suggest that the cerebellum, the basal ganglia, and the cerebral cortex are specialized for different types of learning [23], [24 as summarized in Fig. 1. The cerebellum is specialized for supervised learning based on the error signal encoded in the climbing fibers [2], [25], [26], [27]. The basal ganglia are specialized for reinforcement learning (RL) based on the reward signal encoded in the dopaminergic fibers from the substantia

Collaboration of learning modules

In the above framework of learning-orientated specialization, each organization is not specialized in what to do, but in how to learn it. Specific behaviors or functions can be realized by a combination of multiple learning modules distributed among the basal ganglia, the cerebellum, and the cerebral cortex [23], [24.

The use of internal models of the body and the environment can improve the performance of motor control [57], [58. Such internal models could be acquired by supervised learning

Conclusion

A new hypothesis concerning the specialization of brain structures for different learning paradigms provides helpful clues as to the differential roles of the basal ganglia and the cerebellum [24radical dotradical dot]. Whereas the use of different learning algorithms is associated with differential involvement of the cerebellum, the basal ganglia and the cerebral cortex, the use of different representations is associated with differential involvement of the channels in cortico-basal ganglia loops and

Acknowledgements

The author is grateful to Mitsuo Kawato and Hiroyuki Nakahara for their helpful comments on the manuscript.

References and recommended reading

Papers of particular interest, published within the annual period of review,have been highlighted as:

  • radical dot of special interest

  • radical dotradical dot of outstanding interest

References (80)

  • DM Wolpert et al.

    Internal models in the cerebellum

    Trends Cogn Sci

    (1998)
  • M Kawato

    Internal models for motor control and trajectory planning

    Curr Opin Neurobiol

    (1999)
  • H Deubel

    Separate adaptive mechanisms for the control of reactive and volitional saccadic eye movements

    Vision Res

    (1995)
  • G Gancarz et al.

    A neural model of saccadic eye movement control explains task-specific adaptation

    Vision Res

    (1999)
  • O Hikosaka et al.

    Parallel neural networks for learning sequential procedures

    Trends Neurosci

    (1999)
  • M Ito

    Movement and thought: identical control mechanisms by the cerebellum

    Trends Neurosci

    (1993)
  • FA Middleton et al.

    Basal ganglia output and cognition: evidence from anatomical, behavioral, and clinical studies

    Brain Cogn

    (2000)
  • B Van Golf Racht-Delatour et al.

    Rule-based learning impairment in rats with lesions to the dorsal striatum

    Neurobiol Learn Mem

    (1999)
  • GI Allen et al.

    Cerebro cerebellar communication systems

    Physiol Rev

    (1974)
  • M Ito

    The Cerebellum and Neural Control

    (1984)
  • WT Thach et al.

    Combining versus gating motor programs: differential roles for cerebellum and basal ganglia?

  • LM Parsons et al.

    Use of implicit motor imagery for visual shape discrimination as revealed by PET

    Nature

    (1995)
  • M Lotze et al.

    Activation of cortical and cerebellar motor areas during executed and imagined hand movements: an fMRI study

    J Cogn Neurosci

    (1999)
  • JH Gao et al.

    Cerebellum implicated in sensory acquisition and discrimination rather than motor control

    Science

    (1996)
  • RA Poldrack et al.

    Striatal activation during acquisition of a cognitive skill

    Neuropsychology

    (1999)
  • LM Parsons et al.

    Neuroimaging evidence implicating cerebellum in support of sensory/cognitive processes associated with thirst

    Proc Natl Acad Sci USA

    (2000)
  • S-G Kim et al.

    Activation of a cerebellar output nucleus during cognitive processing

    Science

    (1994)
  • A Dagher et al.

    Mapping the network for planning: a correlational PET activation study with the Tower of London task

    Brain

    (1999)
  • BJ Weder et al.

    Impaired somatosensory discrimination of shape in Parkinson's disease: association with caudate nucleus dopaminergic function

    Hum Brain Mapp

    (1999)
  • G Allen et al.

    Attentional activation of the cerebellum independent of motor involvement

    Science

    (1997)
  • JC Leiner et al.

    Cognitive and language functions of the cerebellum

    Trends Neurosci

    (1993)
  • JJ Kim et al.

    Direct comparison of the neural substrates of recognition memory for words and faces

    Brain

    (1999)
  • CJ Price et al.

    A functional imaging study of translation and language switching

    Brain

    (1999)
  • Y Dong et al.

    Essential role of the right superior parietal cortex in Japanese kana mirror reading: an fMRI study

    Brain

    (2000)
  • FA Middleton et al.

    Anatomical evidence for cerebellar and basal ganglia involvement in higher cognitive function

    Science

    (1994)
  • JE Hoover et al.

    The organization of cerebellar and basal ganglia outputs to primary motor cortex as revealed by retrograde transneuronal transport of herpes simplex virus type 1

    J Neurosci

    (1999)
  • FA Middleton et al.

    The temporal lobe is a target of output from the basal ganglia

    Proc Natl Acad Sci USA

    (1996)
  • JC Houk et al.

    Distributed modular architectures linking basal ganglia, cerebellum, and cerebral cortex: their role in planning and controlling action

    Cereb Cortex

    (1995)
  • D Marr

    A theory of cerebellar cortex

    J Physiol

    (1969)
  • M Kawato et al.

    A computational model of four regions of the cerebellum based on feedback-error learning

    Biol Cybern

    (1992)
  • Cited by (694)

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