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The basal ganglia and the cerebellum: nodes in an integrated network

Abstract

The basal ganglia and the cerebellum are considered to be distinct subcortical systems that perform unique functional operations. The outputs of the basal ganglia and the cerebellum influence many of the same cortical areas but do so by projecting to distinct thalamic nuclei. As a consequence, the two subcortical systems were thought to be independent and to communicate only at the level of the cerebral cortex. Here, we review recent data showing that the basal ganglia and the cerebellum are interconnected at the subcortical level. The subthalamic nucleus in the basal ganglia is the source of a dense disynaptic projection to the cerebellar cortex. Similarly, the dentate nucleus in the cerebellum is the source of a dense disynaptic projection to the striatum. These observations lead to a new functional perspective that the basal ganglia, the cerebellum and the cerebral cortex form an integrated network. This network is topographically organized so that the motor, cognitive and affective territories of each node in the network are interconnected. This perspective explains how synaptic modifications or abnormal activity at one node can have network-wide effects. A future challenge is to define how the unique learning mechanisms at each network node interact to improve performance.

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Fig. 1: Organization of basal ganglia and cerebellar outputs to the cerebral cortex.
Fig. 2: Anatomical connections.
Fig. 3: Neuroimaging evidence for basal ganglia and cerebellar interactions in disease.
Fig. 4: Neuroimaging evidence for basal ganglia and cerebellar interactions in normal function.
Fig. 5: Learning specializations of cortico–basal ganglia and cortico–cerebellar loops.
Fig. 6: Action planning.

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Acknowledgements

The preparation of this manuscript was supported in part by US National Institutes of Health grants R01 NS24328, P40 OD010996 and P30 NS076405 (all to P.L.S.).

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Nature Reviews Neuroscience thanks O. Hikosaka, K. Khodakhah and S. Wang for their contribution to the peer review of this work.

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Both authors researched data for the article, made a substantial contribution to the discussion of content and contributed to the writing, reviewing and editing of the manuscript before submission.

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Glossary

Rabies virus

An RNA virus that is highly neurotropic and can be used as a retrograde transneuronal tracer. Rabies virus is transported retrogradely to neurons that project to an injection site (that is, first-order neurons). The virus replicates in the first-order neurons and is transmitted transneuronally to neurons that project to the first-order neurons. The virus continues to replicate and move transneuronally through chains of synaptically connected neurons in a time-dependent fashion.

Direct pathway

A monosynaptic pathway that connects one type of MSN in the striatum with neurons in the GPi and the SNpr.

Indirect pathway

A polysynaptic pathway that connects another type of MSN in the striatum to neurons in the GPi and the SNpr.

Reward-based (reinforcement) learning

Learning process (algorithm) that allows reward signals to optimize performance.

Error-based learning

Learning process (algorithm) that allows error signals to improve performance in a gradual manner.

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Bostan, A.C., Strick, P.L. The basal ganglia and the cerebellum: nodes in an integrated network. Nat Rev Neurosci 19, 338–350 (2018). https://doi.org/10.1038/s41583-018-0002-7

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