Functionally distinct Purkinje cell types show temporal precision in encoding locomotion

Purkinje cells, the principal neurons of cerebellar computations, are believed to comprise a uniform neuronal population of cells, each with similar functional properties. Here, we show an undiscovered heterogeneity of adult zebrafish Purkinje cells, revealing the existence of anatomically and funct...

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Published in:	Proceedings of the National Academy of Sciences - PNAS Vol. 117; no. 29; pp. 17330 - 17337
Main Authors:	Chang, Weipang, Pedroni, Andrea, Hohendorf, Victoria, Giacomello, Stefania, Hibi, Masahiko, Köster, Reinhard W., Ampatzis, Konstantinos
Format:	Journal Article
Language:	English
Published:	Washington National Academy of Sciences 21-07-2020
Subjects:	Biological Sciences central pattern generator Cerebellum Circuits Danio rerio Heterogeneity Locomotion Medicin och hälsovetenskap Purkinje cells Synapses Zebrafish
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Abstract	Purkinje cells, the principal neurons of cerebellar computations, are believed to comprise a uniform neuronal population of cells, each with similar functional properties. Here, we show an undiscovered heterogeneity of adult zebrafish Purkinje cells, revealing the existence of anatomically and functionally distinct cell types. Dual patch-clamp recordings showed that the cerebellar circuit contains all Purkinje cell types that cross-communicate extensively using chemical and electrical synapses. Further activation of spinal central pattern generators (CPGs) revealed unique phaselocked activity from each Purkinje cell type during the locomotor cycle. Thus, we show intricately organized Purkinje cell networks in the adult zebrafish cerebellum that encode the locomotion rhythm differentially, and we suggest that these organizational properties may also apply to other cerebellar functions
AbstractList	Purkinje cells, the principal neurons of cerebellar computations, are believed to comprise a uniform neuronal population of cells, each with similar functional properties. Here, we show an undiscovered heterogeneity of adult zebrafish Purkinje cells, revealing the existence of anatomically and functionally distinct cell types. Dual patch-clamp recordings showed that the cerebellar circuit contains all Purkinje cell types that cross-communicate extensively using chemical and electrical synapses. Further activation of spinal central pattern generators (CPGs) revealed unique phaselocked activity from each Purkinje cell type during the locomotor cycle. Thus, we show intricately organized Purkinje cell networks in the adult zebrafish cerebellum that encode the locomotion rhythm differentially, and we suggest that these organizational properties may also apply to other cerebellar functions Purkinje cells, the key cells for cerebellar computations, are thought to function similarly throughout the cerebellum and to comprise a uniform neuronal population. Here, we challenge this notion by providing detailed evidence that the Purkinje cells are organized into distinct types, each exhibiting specific activity patterns that are associated with a particular phase of the zebrafish swim cycle during locomotion. Connectivity experiments suggest that all the identified Purkinje cell types participate in orchestrating the cerebellar circuit ensembles, which are, therefore, highly heterogeneous. Purkinje cells, the principal neurons of cerebellar computations, are believed to comprise a uniform neuronal population of cells, each with similar functional properties. Here, we show an undiscovered heterogeneity of adult zebrafish Purkinje cells, revealing the existence of anatomically and functionally distinct cell types. Dual patch-clamp recordings showed that the cerebellar circuit contains all Purkinje cell types that cross-communicate extensively using chemical and electrical synapses. Further activation of spinal central pattern generators (CPGs) revealed unique phase-locked activity from each Purkinje cell type during the locomotor cycle. Thus, we show intricately organized Purkinje cell networks in the adult zebrafish cerebellum that encode the locomotion rhythm differentially, and we suggest that these organizational properties may also apply to other cerebellar functions. Purkinje cells, the principal neurons of cerebellar computations, are believed to comprise a uniform neuronal population of cells, each with similar functional properties. Here, we show an undiscovered heterogeneity of adult zebrafish Purkinje cells, revealing the existence of anatomically and functionally distinct cell types. Dual patch-clamp recordings showed that the cerebellar circuit contains all Purkinje cell types that cross-communicate extensively using chemical and electrical synapses. Further activation of spinal central pattern generators (CPGs) revealed unique phase-locked activity from each Purkinje cell type during the locomotor cycle. Thus, we show intricately organized Purkinje cell networks in the adult zebrafish cerebellum that encode the locomotion rhythm differentially, and we suggest that these organizational properties may also apply to other cerebellar functions.
Author	Hibi, Masahiko Ampatzis, Konstantinos Giacomello, Stefania Köster, Reinhard W. Pedroni, Andrea Hohendorf, Victoria Chang, Weipang
Author_xml	– sequence: 1 givenname: Weipang surname: Chang fullname: Chang, Weipang – sequence: 2 givenname: Andrea surname: Pedroni fullname: Pedroni, Andrea – sequence: 3 givenname: Victoria surname: Hohendorf fullname: Hohendorf, Victoria – sequence: 4 givenname: Stefania surname: Giacomello fullname: Giacomello, Stefania – sequence: 5 givenname: Masahiko surname: Hibi fullname: Hibi, Masahiko – sequence: 6 givenname: Reinhard W. surname: Köster fullname: Köster, Reinhard W. – sequence: 7 givenname: Konstantinos surname: Ampatzis fullname: Ampatzis, Konstantinos
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Edited by Peter L. Strick, University of Pittsburgh, Pittsburgh, PA, and approved June 5, 2020 (received for review March 25, 2020) 1W.C. and A.P. contributed equally to this work. Author contributions: K.A. designed research; W.C., A.P., V.H., and K.A. performed research; M.H. and R.W.K. contributed new reagents/analytic tools; W.C., A.P., V.H., S.G., and K.A. analyzed data; and K.A. wrote the paper.
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SubjectTerms	Biological Sciences central pattern generator Cerebellum Circuits Danio rerio Heterogeneity Locomotion Medicin och hälsovetenskap Purkinje cells Synapses Zebrafish
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Title	Functionally distinct Purkinje cell types show temporal precision in encoding locomotion
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