Motor learning selectively strengthens cortical and striatal synapses of motor engram neurons.

corticostriatal circuit dendritic spines memory engram motor learning synaptic clustering synaptic plasticity two-photon imaging

Journal

Neuron
ISSN: 1097-4199
Titre abrégé: Neuron
Pays: United States
ID NLM: 8809320

Informations de publication

Date de publication:
07 09 2022
Historique:
received: 26 10 2021
revised: 21 03 2022
accepted: 07 06 2022
pubmed: 10 7 2022
medline: 14 9 2022
entrez: 9 7 2022
Statut: ppublish

Résumé

Learning and consolidation of new motor skills require plasticity in the motor cortex and striatum, two key motor regions of the brain. However, how neurons undergo synaptic changes and become recruited during motor learning to form a memory engram remains unknown. Here, we train mice on a motor learning task and use a genetic approach to identify and manipulate behavior-relevant neurons selectively in the primary motor cortex (M1). We find that the degree of M1 engram neuron reactivation correlates with motor performance. We further demonstrate that learning-induced dendritic spine reorganization specifically occurs in these M1 engram neurons. In addition, we find that motor learning leads to an increase in the strength of M1 engram neuron outputs onto striatal spiny projection neurons (SPNs) and that these synapses form clusters along SPN dendrites. These results identify a highly specific synaptic plasticity during the formation of long-lasting motor memory traces in the corticostriatal circuit.

Identifiants

pubmed: 35809573
pii: S0896-6273(22)00544-X
doi: 10.1016/j.neuron.2022.06.006
pmc: PMC9464700
mid: NIHMS1817035
pii:
doi:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

2790-2801.e5

Subventions

Organisme : NINDS NIH HHS
ID : R01 NS091144
Pays : United States

Informations de copyright

Copyright © 2022 The Author(s). Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

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Auteurs

Fuu-Jiun Hwang (FJ)

Department of Neurosurgery, Stanford University, Stanford, CA 94305, USA.

Richard H Roth (RH)

Department of Neurosurgery, Stanford University, Stanford, CA 94305, USA.

Yu-Wei Wu (YW)

Department of Neurosurgery, Stanford University, Stanford, CA 94305, USA.

Yue Sun (Y)

Department of Neurosurgery, Stanford University, Stanford, CA 94305, USA.

Destany K Kwon (DK)

Department of Neurosurgery, Stanford University, Stanford, CA 94305, USA.

Yu Liu (Y)

Department of Neurosurgery, Stanford University, Stanford, CA 94305, USA.

Jun B Ding (JB)

Department of Neurosurgery, Stanford University, Stanford, CA 94305, USA; Department of Neurology and Neurological Sciences, Stanford University, Stanford, CA 94305, USA. Electronic address: dingjun@stanford.edu.

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Classifications MeSH