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Task-specific modulation of corticospinal neuron activity during motor learning in mice

Motor skill learning relies on the plasticity of the primary motor cortex as task acquisition drives cortical motor network remodeling. Large-scale cortical remodeling of evoked motor outputs occurs during the learning of corticospinal-dependent prehension behavior, but not simple, non-dexterous tas...

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Autores principales: Serradj, Najet, Marino, Francesca, Moreno-López, Yunuen, Bernstein, Amanda, Agger, Sydney, Soliman, Marwa, Sloan, Andrew, Hollis, Edmund
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10175564/
https://www.ncbi.nlm.nih.gov/pubmed/37169765
http://dx.doi.org/10.1038/s41467-023-38418-4
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author Serradj, Najet
Marino, Francesca
Moreno-López, Yunuen
Bernstein, Amanda
Agger, Sydney
Soliman, Marwa
Sloan, Andrew
Hollis, Edmund
author_facet Serradj, Najet
Marino, Francesca
Moreno-López, Yunuen
Bernstein, Amanda
Agger, Sydney
Soliman, Marwa
Sloan, Andrew
Hollis, Edmund
author_sort Serradj, Najet
collection PubMed
description Motor skill learning relies on the plasticity of the primary motor cortex as task acquisition drives cortical motor network remodeling. Large-scale cortical remodeling of evoked motor outputs occurs during the learning of corticospinal-dependent prehension behavior, but not simple, non-dexterous tasks. Here we determine the response of corticospinal neurons to two distinct motor training paradigms and assess the role of corticospinal neurons in the execution of a task requiring precise modulation of forelimb movement and one that does not. In vivo calcium imaging in mice revealed temporal coding of corticospinal activity coincident with the development of precise prehension movements, but not more simplistic movement patterns. Transection of the corticospinal tract and optogenetic regulation of corticospinal activity show the necessity for patterned corticospinal network activity in the execution of precise movements but not simplistic ones. Our findings reveal a critical role for corticospinal network modulation in the learning and execution of precise motor movements.
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spelling pubmed-101755642023-05-13 Task-specific modulation of corticospinal neuron activity during motor learning in mice Serradj, Najet Marino, Francesca Moreno-López, Yunuen Bernstein, Amanda Agger, Sydney Soliman, Marwa Sloan, Andrew Hollis, Edmund Nat Commun Article Motor skill learning relies on the plasticity of the primary motor cortex as task acquisition drives cortical motor network remodeling. Large-scale cortical remodeling of evoked motor outputs occurs during the learning of corticospinal-dependent prehension behavior, but not simple, non-dexterous tasks. Here we determine the response of corticospinal neurons to two distinct motor training paradigms and assess the role of corticospinal neurons in the execution of a task requiring precise modulation of forelimb movement and one that does not. In vivo calcium imaging in mice revealed temporal coding of corticospinal activity coincident with the development of precise prehension movements, but not more simplistic movement patterns. Transection of the corticospinal tract and optogenetic regulation of corticospinal activity show the necessity for patterned corticospinal network activity in the execution of precise movements but not simplistic ones. Our findings reveal a critical role for corticospinal network modulation in the learning and execution of precise motor movements. Nature Publishing Group UK 2023-05-11 /pmc/articles/PMC10175564/ /pubmed/37169765 http://dx.doi.org/10.1038/s41467-023-38418-4 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Serradj, Najet
Marino, Francesca
Moreno-López, Yunuen
Bernstein, Amanda
Agger, Sydney
Soliman, Marwa
Sloan, Andrew
Hollis, Edmund
Task-specific modulation of corticospinal neuron activity during motor learning in mice
title Task-specific modulation of corticospinal neuron activity during motor learning in mice
title_full Task-specific modulation of corticospinal neuron activity during motor learning in mice
title_fullStr Task-specific modulation of corticospinal neuron activity during motor learning in mice
title_full_unstemmed Task-specific modulation of corticospinal neuron activity during motor learning in mice
title_short Task-specific modulation of corticospinal neuron activity during motor learning in mice
title_sort task-specific modulation of corticospinal neuron activity during motor learning in mice
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10175564/
https://www.ncbi.nlm.nih.gov/pubmed/37169765
http://dx.doi.org/10.1038/s41467-023-38418-4
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