Cerebellar Modules and Their Role as Operational Cerebellar Processing Units

Richard Apps; Richard Hawkes; Sho Aoki; Fredrik Bengtsson; Amanda M. Brown; Gang Chen; Timothy J. Ebner; Philippe Isope; Henrik Jörntell; Elizabeth P. Lackey; Charlotte Lawrenson; Bridget Lumb; Martijn Schonewille; Roy V. Sillitoe; Ludovic Spaeth; Izumi Sugihara; Antoine Valera; Jan Voogd; Douglas R. Wylie; Tom J.H. Ruigrok

doi:10.1007/s12311-018-0952-3

Cerebellar Modules and Their Role as Operational Cerebellar Processing Units

Richard Apps, Richard Hawkes, Sho Aoki, Fredrik Bengtsson, Amanda M. Brown, Gang Chen, Timothy J. Ebner, Philippe Isope, Henrik Jörntell, Elizabeth P. Lackey, Charlotte Lawrenson, Bridget Lumb, Martijn Schonewille, Roy V. Sillitoe, Ludovic Spaeth, Izumi Sugihara, Antoine Valera, Jan Voogd, Douglas R. Wylie, Tom J.H. Ruigrok

Neuroscience

Research output: Contribution to journal › Review article › peer-review

99 Scopus citations

Abstract

The compartmentalization of the cerebellum into modules is often used to discuss its function. What, exactly, can be considered a module, how do they operate, can they be subdivided and do they act individually or in concert are only some of the key questions discussed in this consensus paper. Experts studying cerebellar compartmentalization give their insights on the structure and function of cerebellar modules, with the aim of providing an up-to-date review of the extensive literature on this subject. Starting with an historical perspective indicating that the basis of the modular organization is formed by matching olivocorticonuclear connectivity, this is followed by consideration of anatomical and chemical modular boundaries, revealing a relation between anatomical, chemical, and physiological borders. In addition, the question is asked what the smallest operational unit of the cerebellum might be. Furthermore, it has become clear that chemical diversity of Purkinje cells also results in diversity of information processing between cerebellar modules. An additional important consideration is the relation between modular compartmentalization and the organization of the mossy fiber system, resulting in the concept of modular plasticity. Finally, examination of cerebellar output patterns suggesting cooperation between modules and recent work on modular aspects of emotional behavior are discussed. Despite the general consensus that the cerebellum has a modular organization, many questions remain. The authors hope that this joint review will inspire future cerebellar research so that we are better able to understand how this brain structure makes its vital contribution to behavior in its most general form.

Original language	English (US)
Pages (from-to)	654-682
Number of pages	29
Journal	Cerebellum
Volume	17
Issue number	5
DOIs	https://doi.org/10.1007/s12311-018-0952-3
State	Published - Oct 1 2018

Bibliographical note

Funding Information:
Funding Information Sugihara was supported by JSPS KAKENHI research grant (16K070025). Wylie was supported by funding from the Canadian Institutes for Health Research (CIHR) and the Natural Sciences and Engineering Research Council of Canada (NSERC). Sillitoe was supported by funds from Baylor College of Medicine (BCM) and Texas Children’s Hospital (TCH). R.V.S. received support from BCM IDDRC grant U54HD083092 (Neurovisualization Core), the National Institutes of Neurological Disorders and Stroke (NINDS) R01NS089664, and the Hamill Foundation. A.M.B. received support from NINDS F31NS101891. Schonewille was supported by the Erasmus MC Rotterdam, the Dutch Scientific Organization Veni (NWO-ALW Veni), and the European Research Counsil Starting Grant (ERC-Stg, 680235). Ebner was supported in part by NIH grant R01 NS18338. Isope was supported by the CNRS, Université de Strasbourg, the Agence Nationale de la Recherche (Grant N°ANR-15-CE37-0001-01), and by the Fondation pour la Recherche Medicale (Grant N° DEQ20140329514). Ruigrok was supported by the Erasmus MC Rotterdam and the Dutch Ministry of Health, Welfare and Sports (T.R.), and JSPS Institutional Program for Young Researcher Overseas Visits (S.A.). Apps was supported by the Biotechnology and Biological Sciences Research Council (BBSRC, UK).

Publisher Copyright:
© 2018, The Author(s).

Keywords

Aldolase C
Cerebellum
Climbing fibers
Compartments
Functional organization
Longitudinal stripes
Microzones
Mossy fibers
Purkinje cells
Zebrin

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10.1007/s12311-018-0952-3

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6132822

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Apps, R., Hawkes, R., Aoki, S., Bengtsson, F., Brown, A. M., Chen, G., Ebner, T. J., Isope, P., Jörntell, H., Lackey, E. P., Lawrenson, C., Lumb, B., Schonewille, M., Sillitoe, R. V., Spaeth, L., Sugihara, I., Valera, A., Voogd, J., Wylie, D. R., & Ruigrok, T. J. H. (2018). Cerebellar Modules and Their Role as Operational Cerebellar Processing Units. Cerebellum, 17(5), 654-682. https://doi.org/10.1007/s12311-018-0952-3

Apps, R, Hawkes, R, Aoki, S, Bengtsson, F, Brown, AM, Chen, G, Ebner, TJ, Isope, P, Jörntell, H, Lackey, EP, Lawrenson, C, Lumb, B, Schonewille, M, Sillitoe, RV, Spaeth, L, Sugihara, I, Valera, A, Voogd, J, Wylie, DR & Ruigrok, TJH 2018, 'Cerebellar Modules and Their Role as Operational Cerebellar Processing Units', Cerebellum, vol. 17, no. 5, pp. 654-682. https://doi.org/10.1007/s12311-018-0952-3

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abstract = "The compartmentalization of the cerebellum into modules is often used to discuss its function. What, exactly, can be considered a module, how do they operate, can they be subdivided and do they act individually or in concert are only some of the key questions discussed in this consensus paper. Experts studying cerebellar compartmentalization give their insights on the structure and function of cerebellar modules, with the aim of providing an up-to-date review of the extensive literature on this subject. Starting with an historical perspective indicating that the basis of the modular organization is formed by matching olivocorticonuclear connectivity, this is followed by consideration of anatomical and chemical modular boundaries, revealing a relation between anatomical, chemical, and physiological borders. In addition, the question is asked what the smallest operational unit of the cerebellum might be. Furthermore, it has become clear that chemical diversity of Purkinje cells also results in diversity of information processing between cerebellar modules. An additional important consideration is the relation between modular compartmentalization and the organization of the mossy fiber system, resulting in the concept of modular plasticity. Finally, examination of cerebellar output patterns suggesting cooperation between modules and recent work on modular aspects of emotional behavior are discussed. Despite the general consensus that the cerebellum has a modular organization, many questions remain. The authors hope that this joint review will inspire future cerebellar research so that we are better able to understand how this brain structure makes its vital contribution to behavior in its most general form.",

keywords = "Aldolase C, Cerebellum, Climbing fibers, Compartments, Functional organization, Longitudinal stripes, Microzones, Mossy fibers, Purkinje cells, Zebrin",

author = "Richard Apps and Richard Hawkes and Sho Aoki and Fredrik Bengtsson and Brown, {Amanda M.} and Gang Chen and Ebner, {Timothy J.} and Philippe Isope and Henrik J{\"o}rntell and Lackey, {Elizabeth P.} and Charlotte Lawrenson and Bridget Lumb and Martijn Schonewille and Sillitoe, {Roy V.} and Ludovic Spaeth and Izumi Sugihara and Antoine Valera and Jan Voogd and Wylie, {Douglas R.} and Ruigrok, {Tom J.H.}",

note = "Funding Information: Funding Information Sugihara was supported by JSPS KAKENHI research grant (16K070025). Wylie was supported by funding from the Canadian Institutes for Health Research (CIHR) and the Natural Sciences and Engineering Research Council of Canada (NSERC). Sillitoe was supported by funds from Baylor College of Medicine (BCM) and Texas Children{\textquoteright}s Hospital (TCH). R.V.S. received support from BCM IDDRC grant U54HD083092 (Neurovisualization Core), the National Institutes of Neurological Disorders and Stroke (NINDS) R01NS089664, and the Hamill Foundation. A.M.B. received support from NINDS F31NS101891. Schonewille was supported by the Erasmus MC Rotterdam, the Dutch Scientific Organization Veni (NWO-ALW Veni), and the European Research Counsil Starting Grant (ERC-Stg, 680235). Ebner was supported in part by NIH grant R01 NS18338. Isope was supported by the CNRS, Universit{\'e} de Strasbourg, the Agence Nationale de la Recherche (Grant N°ANR-15-CE37-0001-01), and by the Fondation pour la Recherche Medicale (Grant N° DEQ20140329514). Ruigrok was supported by the Erasmus MC Rotterdam and the Dutch Ministry of Health, Welfare and Sports (T.R.), and JSPS Institutional Program for Young Researcher Overseas Visits (S.A.). Apps was supported by the Biotechnology and Biological Sciences Research Council (BBSRC, UK). Publisher Copyright: {\textcopyright} 2018, The Author(s).",

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doi = "10.1007/s12311-018-0952-3",

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T1 - Cerebellar Modules and Their Role as Operational Cerebellar Processing Units

AU - Apps, Richard

AU - Hawkes, Richard

AU - Aoki, Sho

AU - Bengtsson, Fredrik

AU - Brown, Amanda M.

AU - Chen, Gang

AU - Ebner, Timothy J.

AU - Isope, Philippe

AU - Jörntell, Henrik

AU - Lackey, Elizabeth P.

AU - Lawrenson, Charlotte

AU - Lumb, Bridget

AU - Schonewille, Martijn

AU - Sillitoe, Roy V.

AU - Spaeth, Ludovic

AU - Sugihara, Izumi

AU - Valera, Antoine

AU - Voogd, Jan

AU - Wylie, Douglas R.

AU - Ruigrok, Tom J.H.

N1 - Funding Information: Funding Information Sugihara was supported by JSPS KAKENHI research grant (16K070025). Wylie was supported by funding from the Canadian Institutes for Health Research (CIHR) and the Natural Sciences and Engineering Research Council of Canada (NSERC). Sillitoe was supported by funds from Baylor College of Medicine (BCM) and Texas Children’s Hospital (TCH). R.V.S. received support from BCM IDDRC grant U54HD083092 (Neurovisualization Core), the National Institutes of Neurological Disorders and Stroke (NINDS) R01NS089664, and the Hamill Foundation. A.M.B. received support from NINDS F31NS101891. Schonewille was supported by the Erasmus MC Rotterdam, the Dutch Scientific Organization Veni (NWO-ALW Veni), and the European Research Counsil Starting Grant (ERC-Stg, 680235). Ebner was supported in part by NIH grant R01 NS18338. Isope was supported by the CNRS, Université de Strasbourg, the Agence Nationale de la Recherche (Grant N°ANR-15-CE37-0001-01), and by the Fondation pour la Recherche Medicale (Grant N° DEQ20140329514). Ruigrok was supported by the Erasmus MC Rotterdam and the Dutch Ministry of Health, Welfare and Sports (T.R.), and JSPS Institutional Program for Young Researcher Overseas Visits (S.A.). Apps was supported by the Biotechnology and Biological Sciences Research Council (BBSRC, UK). Publisher Copyright: © 2018, The Author(s).

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N2 - The compartmentalization of the cerebellum into modules is often used to discuss its function. What, exactly, can be considered a module, how do they operate, can they be subdivided and do they act individually or in concert are only some of the key questions discussed in this consensus paper. Experts studying cerebellar compartmentalization give their insights on the structure and function of cerebellar modules, with the aim of providing an up-to-date review of the extensive literature on this subject. Starting with an historical perspective indicating that the basis of the modular organization is formed by matching olivocorticonuclear connectivity, this is followed by consideration of anatomical and chemical modular boundaries, revealing a relation between anatomical, chemical, and physiological borders. In addition, the question is asked what the smallest operational unit of the cerebellum might be. Furthermore, it has become clear that chemical diversity of Purkinje cells also results in diversity of information processing between cerebellar modules. An additional important consideration is the relation between modular compartmentalization and the organization of the mossy fiber system, resulting in the concept of modular plasticity. Finally, examination of cerebellar output patterns suggesting cooperation between modules and recent work on modular aspects of emotional behavior are discussed. Despite the general consensus that the cerebellum has a modular organization, many questions remain. The authors hope that this joint review will inspire future cerebellar research so that we are better able to understand how this brain structure makes its vital contribution to behavior in its most general form.

AB - The compartmentalization of the cerebellum into modules is often used to discuss its function. What, exactly, can be considered a module, how do they operate, can they be subdivided and do they act individually or in concert are only some of the key questions discussed in this consensus paper. Experts studying cerebellar compartmentalization give their insights on the structure and function of cerebellar modules, with the aim of providing an up-to-date review of the extensive literature on this subject. Starting with an historical perspective indicating that the basis of the modular organization is formed by matching olivocorticonuclear connectivity, this is followed by consideration of anatomical and chemical modular boundaries, revealing a relation between anatomical, chemical, and physiological borders. In addition, the question is asked what the smallest operational unit of the cerebellum might be. Furthermore, it has become clear that chemical diversity of Purkinje cells also results in diversity of information processing between cerebellar modules. An additional important consideration is the relation between modular compartmentalization and the organization of the mossy fiber system, resulting in the concept of modular plasticity. Finally, examination of cerebellar output patterns suggesting cooperation between modules and recent work on modular aspects of emotional behavior are discussed. Despite the general consensus that the cerebellum has a modular organization, many questions remain. The authors hope that this joint review will inspire future cerebellar research so that we are better able to understand how this brain structure makes its vital contribution to behavior in its most general form.

KW - Aldolase C

KW - Cerebellum

KW - Climbing fibers

KW - Compartments

KW - Functional organization

KW - Longitudinal stripes

KW - Microzones

KW - Mossy fibers

KW - Purkinje cells

KW - Zebrin

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Cerebellar Modules and Their Role as Operational Cerebellar Processing Units

Abstract

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Keywords

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