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An adaptive behavioral control motif mediated by cortical axo-axonic inhibition

Genetically defined subgroups of inhibitory interneurons are thought to play distinct roles in learning, but heterogeneity within these subgroups has limited our understanding of the scope and nature of their specific contributions. Here we reveal that the chandelier cell (ChC), an interneuron type...

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Autores principales: Jung, Kanghoon, Chang, Minhyeok, Steinecke, André, Burke, Benjamin, Choi, Youngjin, Oisi, Yasuhiro, Fitzpatrick, David, Taniguchi, Hiroki, Kwon, Hyung-Bae
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group US 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10400431/
https://www.ncbi.nlm.nih.gov/pubmed/37474640
http://dx.doi.org/10.1038/s41593-023-01380-x
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author Jung, Kanghoon
Chang, Minhyeok
Steinecke, André
Burke, Benjamin
Choi, Youngjin
Oisi, Yasuhiro
Fitzpatrick, David
Taniguchi, Hiroki
Kwon, Hyung-Bae
author_facet Jung, Kanghoon
Chang, Minhyeok
Steinecke, André
Burke, Benjamin
Choi, Youngjin
Oisi, Yasuhiro
Fitzpatrick, David
Taniguchi, Hiroki
Kwon, Hyung-Bae
author_sort Jung, Kanghoon
collection PubMed
description Genetically defined subgroups of inhibitory interneurons are thought to play distinct roles in learning, but heterogeneity within these subgroups has limited our understanding of the scope and nature of their specific contributions. Here we reveal that the chandelier cell (ChC), an interneuron type that specializes in inhibiting the axon-initial segment (AIS) of pyramidal neurons, establishes cortical microcircuits for organizing neural coding through selective axo-axonic synaptic plasticity. We found that organized motor control is mediated by enhanced population coding of direction-tuned premotor neurons, with tuning refined through suppression of irrelevant neuronal activity. ChCs contribute to learning-dependent refinements by providing selective inhibitory control over individual pyramidal neurons rather than global suppression. Quantitative analysis of structural plasticity across axo-axonic synapses revealed that ChCs redistributed inhibitory weights to individual pyramidal neurons during learning. These results demonstrate an adaptive logic of the inhibitory circuit motif responsible for organizing distributed neural representations. Thus, ChCs permit efficient cortical computation in a targeted cell-specific manner.
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spelling pubmed-104004312023-08-05 An adaptive behavioral control motif mediated by cortical axo-axonic inhibition Jung, Kanghoon Chang, Minhyeok Steinecke, André Burke, Benjamin Choi, Youngjin Oisi, Yasuhiro Fitzpatrick, David Taniguchi, Hiroki Kwon, Hyung-Bae Nat Neurosci Article Genetically defined subgroups of inhibitory interneurons are thought to play distinct roles in learning, but heterogeneity within these subgroups has limited our understanding of the scope and nature of their specific contributions. Here we reveal that the chandelier cell (ChC), an interneuron type that specializes in inhibiting the axon-initial segment (AIS) of pyramidal neurons, establishes cortical microcircuits for organizing neural coding through selective axo-axonic synaptic plasticity. We found that organized motor control is mediated by enhanced population coding of direction-tuned premotor neurons, with tuning refined through suppression of irrelevant neuronal activity. ChCs contribute to learning-dependent refinements by providing selective inhibitory control over individual pyramidal neurons rather than global suppression. Quantitative analysis of structural plasticity across axo-axonic synapses revealed that ChCs redistributed inhibitory weights to individual pyramidal neurons during learning. These results demonstrate an adaptive logic of the inhibitory circuit motif responsible for organizing distributed neural representations. Thus, ChCs permit efficient cortical computation in a targeted cell-specific manner. Nature Publishing Group US 2023-07-20 2023 /pmc/articles/PMC10400431/ /pubmed/37474640 http://dx.doi.org/10.1038/s41593-023-01380-x 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
Jung, Kanghoon
Chang, Minhyeok
Steinecke, André
Burke, Benjamin
Choi, Youngjin
Oisi, Yasuhiro
Fitzpatrick, David
Taniguchi, Hiroki
Kwon, Hyung-Bae
An adaptive behavioral control motif mediated by cortical axo-axonic inhibition
title An adaptive behavioral control motif mediated by cortical axo-axonic inhibition
title_full An adaptive behavioral control motif mediated by cortical axo-axonic inhibition
title_fullStr An adaptive behavioral control motif mediated by cortical axo-axonic inhibition
title_full_unstemmed An adaptive behavioral control motif mediated by cortical axo-axonic inhibition
title_short An adaptive behavioral control motif mediated by cortical axo-axonic inhibition
title_sort adaptive behavioral control motif mediated by cortical axo-axonic inhibition
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10400431/
https://www.ncbi.nlm.nih.gov/pubmed/37474640
http://dx.doi.org/10.1038/s41593-023-01380-x
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