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Input-dependent regulation of excitability controls dendritic maturation in somatosensory thalamocortical neurons

Input from the sensory organs is required to pattern neurons into topographical maps during development. Dendritic complexity critically determines this patterning process; yet, how signals from the periphery act to control dendritic maturation is unclear. Here, using genetic and surgical manipulati...

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Autores principales: Frangeul, Laura, Kehayas, Vassilis, Sanchez-Mut, Jose V., Fièvre, Sabine, Krishna-K, K., Pouchelon, Gabrielle, Telley, Ludovic, Bellone, Camilla, Holtmaat, Anthony, Gräff, Johannes, Macklis, Jeffrey D., Jabaudon, Denis
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5722950/
https://www.ncbi.nlm.nih.gov/pubmed/29222517
http://dx.doi.org/10.1038/s41467-017-02172-1
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author Frangeul, Laura
Kehayas, Vassilis
Sanchez-Mut, Jose V.
Fièvre, Sabine
Krishna-K, K.
Pouchelon, Gabrielle
Telley, Ludovic
Bellone, Camilla
Holtmaat, Anthony
Gräff, Johannes
Macklis, Jeffrey D.
Jabaudon, Denis
author_facet Frangeul, Laura
Kehayas, Vassilis
Sanchez-Mut, Jose V.
Fièvre, Sabine
Krishna-K, K.
Pouchelon, Gabrielle
Telley, Ludovic
Bellone, Camilla
Holtmaat, Anthony
Gräff, Johannes
Macklis, Jeffrey D.
Jabaudon, Denis
author_sort Frangeul, Laura
collection PubMed
description Input from the sensory organs is required to pattern neurons into topographical maps during development. Dendritic complexity critically determines this patterning process; yet, how signals from the periphery act to control dendritic maturation is unclear. Here, using genetic and surgical manipulations of sensory input in mouse somatosensory thalamocortical neurons, we show that membrane excitability is a critical component of dendritic development. Using a combination of genetic approaches, we find that ablation of N-methyl-d-aspartate (NMDA) receptors during postnatal development leads to epigenetic repression of Kv1.1-type potassium channels, increased excitability, and impaired dendritic maturation. Lesions to whisker input pathways had similar effects. Overexpression of Kv1.1 was sufficient to enable dendritic maturation in the absence of sensory input. Thus, Kv1.1 acts to tune neuronal excitability and maintain it within a physiological range, allowing dendritic maturation to proceed. Together, these results reveal an input-dependent control over neuronal excitability and dendritic complexity in the development and plasticity of sensory pathways.
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spelling pubmed-57229502017-12-11 Input-dependent regulation of excitability controls dendritic maturation in somatosensory thalamocortical neurons Frangeul, Laura Kehayas, Vassilis Sanchez-Mut, Jose V. Fièvre, Sabine Krishna-K, K. Pouchelon, Gabrielle Telley, Ludovic Bellone, Camilla Holtmaat, Anthony Gräff, Johannes Macklis, Jeffrey D. Jabaudon, Denis Nat Commun Article Input from the sensory organs is required to pattern neurons into topographical maps during development. Dendritic complexity critically determines this patterning process; yet, how signals from the periphery act to control dendritic maturation is unclear. Here, using genetic and surgical manipulations of sensory input in mouse somatosensory thalamocortical neurons, we show that membrane excitability is a critical component of dendritic development. Using a combination of genetic approaches, we find that ablation of N-methyl-d-aspartate (NMDA) receptors during postnatal development leads to epigenetic repression of Kv1.1-type potassium channels, increased excitability, and impaired dendritic maturation. Lesions to whisker input pathways had similar effects. Overexpression of Kv1.1 was sufficient to enable dendritic maturation in the absence of sensory input. Thus, Kv1.1 acts to tune neuronal excitability and maintain it within a physiological range, allowing dendritic maturation to proceed. Together, these results reveal an input-dependent control over neuronal excitability and dendritic complexity in the development and plasticity of sensory pathways. Nature Publishing Group UK 2017-12-08 /pmc/articles/PMC5722950/ /pubmed/29222517 http://dx.doi.org/10.1038/s41467-017-02172-1 Text en © The Author(s) 2017 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/.
spellingShingle Article
Frangeul, Laura
Kehayas, Vassilis
Sanchez-Mut, Jose V.
Fièvre, Sabine
Krishna-K, K.
Pouchelon, Gabrielle
Telley, Ludovic
Bellone, Camilla
Holtmaat, Anthony
Gräff, Johannes
Macklis, Jeffrey D.
Jabaudon, Denis
Input-dependent regulation of excitability controls dendritic maturation in somatosensory thalamocortical neurons
title Input-dependent regulation of excitability controls dendritic maturation in somatosensory thalamocortical neurons
title_full Input-dependent regulation of excitability controls dendritic maturation in somatosensory thalamocortical neurons
title_fullStr Input-dependent regulation of excitability controls dendritic maturation in somatosensory thalamocortical neurons
title_full_unstemmed Input-dependent regulation of excitability controls dendritic maturation in somatosensory thalamocortical neurons
title_short Input-dependent regulation of excitability controls dendritic maturation in somatosensory thalamocortical neurons
title_sort input-dependent regulation of excitability controls dendritic maturation in somatosensory thalamocortical neurons
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5722950/
https://www.ncbi.nlm.nih.gov/pubmed/29222517
http://dx.doi.org/10.1038/s41467-017-02172-1
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