A neural circuit state change underlying skilled movements.


Journal

Cell
ISSN: 1097-4172
Titre abrégé: Cell
Pays: United States
ID NLM: 0413066

Informations de publication

Date de publication:
08 07 2021
Historique:
received: 07 10 2020
revised: 09 05 2021
accepted: 01 06 2021
pubmed: 3 7 2021
medline: 4 1 2022
entrez: 2 7 2021
Statut: ppublish

Résumé

In motor neuroscience, state changes are hypothesized to time-lock neural assemblies coordinating complex movements, but evidence for this remains slender. We tested whether a discrete change from more autonomous to coherent spiking underlies skilled movement by imaging cerebellar Purkinje neuron complex spikes in mice making targeted forelimb-reaches. As mice learned the task, millimeter-scale spatiotemporally coherent spiking emerged ipsilateral to the reaching forelimb, and consistent neural synchronization became predictive of kinematic stereotypy. Before reach onset, spiking switched from more disordered to internally time-locked concerted spiking and silence. Optogenetic manipulations of cerebellar feedback to the inferior olive bi-directionally modulated neural synchronization and reaching direction. A simple model explained the reorganization of spiking during reaching as reflecting a discrete bifurcation in olivary network dynamics. These findings argue that to prepare learned movements, olivo-cerebellar circuits enter a self-regulated, synchronized state promoting motor coordination. State changes facilitating behavioral transitions may generalize across neural systems.

Identifiants

pubmed: 34214470
pii: S0092-8674(21)00702-9
doi: 10.1016/j.cell.2021.06.001
pmc: PMC8844704
mid: NIHMS1720166
pii:
doi:

Substances chimiques

Calcium SY7Q814VUP

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

3731-3747.e21

Subventions

Organisme : Howard Hughes Medical Institute
Pays : United States

Informations de copyright

Copyright © 2021 Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests O.R., M.J.S., J.L., T.H.K., and J.S. are inventors on a patent, assigned to Stanford, for the two-photon mesoscope. K.D. and C.R. have disclosed all novel opsins to Stanford, which has submitted patent applications to facilitate commercial application and translation; all opsin methods, protocols, clones, and sequences are freely available to nonprofit institutions and investigators.

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Auteurs

Mark J Wagner (MJ)

Neurosciences Program, Stanford University, Stanford, CA 94305, USA; Howard Hughes Medical Institute, Stanford University, Stanford, CA 94305, USA; CNC Program, Stanford University, Stanford, CA 94305, USA; Department of Biology, Stanford University, Stanford, CA 94305, USA. Electronic address: mjwagner@stanford.edu.

Joan Savall (J)

Howard Hughes Medical Institute, Stanford University, Stanford, CA 94305, USA; CNC Program, Stanford University, Stanford, CA 94305, USA.

Oscar Hernandez (O)

CNC Program, Stanford University, Stanford, CA 94305, USA.

Gabriel Mel (G)

Neurosciences Program, Stanford University, Stanford, CA 94305, USA.

Hakan Inan (H)

CNC Program, Stanford University, Stanford, CA 94305, USA; Department of Electrical Engineering, Stanford University, Stanford, CA 94305, USA.

Oleg Rumyantsev (O)

CNC Program, Stanford University, Stanford, CA 94305, USA; Department of Applied Physics, Stanford University, Stanford, CA 94305, USA.

Jérôme Lecoq (J)

CNC Program, Stanford University, Stanford, CA 94305, USA; Department of Biology, Stanford University, Stanford, CA 94305, USA.

Tony Hyun Kim (TH)

Howard Hughes Medical Institute, Stanford University, Stanford, CA 94305, USA; CNC Program, Stanford University, Stanford, CA 94305, USA; Department of Electrical Engineering, Stanford University, Stanford, CA 94305, USA.

Jin Zhong Li (JZ)

CNC Program, Stanford University, Stanford, CA 94305, USA; Department of Biology, Stanford University, Stanford, CA 94305, USA.

Charu Ramakrishnan (C)

Howard Hughes Medical Institute, Stanford University, Stanford, CA 94305, USA; Department of Bioengineering, Stanford University, Stanford, CA 94305, USA.

Karl Deisseroth (K)

Howard Hughes Medical Institute, Stanford University, Stanford, CA 94305, USA; Department of Bioengineering, Stanford University, Stanford, CA 94305, USA.

Liqun Luo (L)

Howard Hughes Medical Institute, Stanford University, Stanford, CA 94305, USA; Department of Biology, Stanford University, Stanford, CA 94305, USA.

Surya Ganguli (S)

Department of Applied Physics, Stanford University, Stanford, CA 94305, USA.

Mark J Schnitzer (MJ)

Howard Hughes Medical Institute, Stanford University, Stanford, CA 94305, USA; CNC Program, Stanford University, Stanford, CA 94305, USA; Department of Biology, Stanford University, Stanford, CA 94305, USA; Department of Applied Physics, Stanford University, Stanford, CA 94305, USA. Electronic address: mschnitz@stanford.edu.

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