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Cell-type-specific plasticity shapes neocortical dynamics for motor learning

Neocortical spiking dynamics control aspects of behavior, yet how these dynamics emerge during motor learning remains elusive. Activity-dependent synaptic plasticity is likely a key mechanism, as it reconfigures network architectures that govern neural dynamics. Here, we examined how the mouse premo...

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Autores principales: Majumder, Shouvik, Hirokawa, Koichi, Yang, Zidan, Paletzki, Ronald, Gerfen, Charles R., Fontolan, Lorenzo, Romani, Sandro, Jain, Anant, Yasuda, Ryohei, Inagaki, Hidehiko K.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10441538/
https://www.ncbi.nlm.nih.gov/pubmed/37609277
http://dx.doi.org/10.1101/2023.08.09.552699
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author Majumder, Shouvik
Hirokawa, Koichi
Yang, Zidan
Paletzki, Ronald
Gerfen, Charles R.
Fontolan, Lorenzo
Romani, Sandro
Jain, Anant
Yasuda, Ryohei
Inagaki, Hidehiko K.
author_facet Majumder, Shouvik
Hirokawa, Koichi
Yang, Zidan
Paletzki, Ronald
Gerfen, Charles R.
Fontolan, Lorenzo
Romani, Sandro
Jain, Anant
Yasuda, Ryohei
Inagaki, Hidehiko K.
author_sort Majumder, Shouvik
collection PubMed
description Neocortical spiking dynamics control aspects of behavior, yet how these dynamics emerge during motor learning remains elusive. Activity-dependent synaptic plasticity is likely a key mechanism, as it reconfigures network architectures that govern neural dynamics. Here, we examined how the mouse premotor cortex acquires its well-characterized neural dynamics that control movement timing, specifically lick timing. To probe the role of synaptic plasticity, we have genetically manipulated proteins essential for major forms of synaptic plasticity, Ca(2+)/calmodulin-dependent protein kinase II (CaMKII) and Cofilin, in a region and cell-type-specific manner. Transient inactivation of CaMKII in the premotor cortex blocked learning of new lick timing without affecting the execution of learned action or ongoing spiking activity. Furthermore, among the major glutamatergic neurons in the premotor cortex, CaMKII and Cofilin activity in pyramidal tract (PT) neurons, but not intratelencephalic (IT) neurons, is necessary for learning. High-density electrophysiology in the premotor cortex uncovered that neural dynamics anticipating licks are progressively shaped during learning, which explains the change in lick timing. Such reconfiguration in behaviorally relevant dynamics is impeded by CaMKII manipulation in PT neurons. Altogether, the activity of plasticity-related proteins in PT neurons plays a central role in sculpting neocortical dynamics to learn new behavior.
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spelling pubmed-104415382023-08-22 Cell-type-specific plasticity shapes neocortical dynamics for motor learning Majumder, Shouvik Hirokawa, Koichi Yang, Zidan Paletzki, Ronald Gerfen, Charles R. Fontolan, Lorenzo Romani, Sandro Jain, Anant Yasuda, Ryohei Inagaki, Hidehiko K. bioRxiv Article Neocortical spiking dynamics control aspects of behavior, yet how these dynamics emerge during motor learning remains elusive. Activity-dependent synaptic plasticity is likely a key mechanism, as it reconfigures network architectures that govern neural dynamics. Here, we examined how the mouse premotor cortex acquires its well-characterized neural dynamics that control movement timing, specifically lick timing. To probe the role of synaptic plasticity, we have genetically manipulated proteins essential for major forms of synaptic plasticity, Ca(2+)/calmodulin-dependent protein kinase II (CaMKII) and Cofilin, in a region and cell-type-specific manner. Transient inactivation of CaMKII in the premotor cortex blocked learning of new lick timing without affecting the execution of learned action or ongoing spiking activity. Furthermore, among the major glutamatergic neurons in the premotor cortex, CaMKII and Cofilin activity in pyramidal tract (PT) neurons, but not intratelencephalic (IT) neurons, is necessary for learning. High-density electrophysiology in the premotor cortex uncovered that neural dynamics anticipating licks are progressively shaped during learning, which explains the change in lick timing. Such reconfiguration in behaviorally relevant dynamics is impeded by CaMKII manipulation in PT neurons. Altogether, the activity of plasticity-related proteins in PT neurons plays a central role in sculpting neocortical dynamics to learn new behavior. Cold Spring Harbor Laboratory 2023-08-14 /pmc/articles/PMC10441538/ /pubmed/37609277 http://dx.doi.org/10.1101/2023.08.09.552699 Text en https://creativecommons.org/licenses/by-nc-nd/4.0/This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (https://creativecommons.org/licenses/by-nc-nd/4.0/) , which allows reusers to copy and distribute the material in any medium or format in unadapted form only, for noncommercial purposes only, and only so long as attribution is given to the creator.
spellingShingle Article
Majumder, Shouvik
Hirokawa, Koichi
Yang, Zidan
Paletzki, Ronald
Gerfen, Charles R.
Fontolan, Lorenzo
Romani, Sandro
Jain, Anant
Yasuda, Ryohei
Inagaki, Hidehiko K.
Cell-type-specific plasticity shapes neocortical dynamics for motor learning
title Cell-type-specific plasticity shapes neocortical dynamics for motor learning
title_full Cell-type-specific plasticity shapes neocortical dynamics for motor learning
title_fullStr Cell-type-specific plasticity shapes neocortical dynamics for motor learning
title_full_unstemmed Cell-type-specific plasticity shapes neocortical dynamics for motor learning
title_short Cell-type-specific plasticity shapes neocortical dynamics for motor learning
title_sort cell-type-specific plasticity shapes neocortical dynamics for motor learning
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10441538/
https://www.ncbi.nlm.nih.gov/pubmed/37609277
http://dx.doi.org/10.1101/2023.08.09.552699
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