ReviewComplementary roles of basal ganglia and cerebellum in learning and motor control
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 [21]. 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 [24]. 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 [24]. 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:
of special interest
of outstanding interest
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