Two opposite voltage-dependent currents control the unusual early development pattern of embryonic Renshaw cell electrical activity

Renshaw cells (V1R) are excitable as soon as they reach their final location next to the spinal motoneurons and are functionally heterogeneous. Using multiple experimental approaches, in combination with biophysical modeling and dynamical systems theory, we analyzed, for the first time, the mechanis...

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Main Authors: Juliette Boeri, Claude Meunier, Hervé Le Corronc, Pascal Branchereau, Yulia Timofeeva, François-Xavier Lejeune, Christine Mouffle, Hervé Arulkandarajah, Jean Marie Mangin, Pascal Legendre, Antonny Czarnecki
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2021-04-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/62639
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spelling doaj-494cac047e70452eb08a221a9d92d3232021-05-21T15:42:04ZengeLife Sciences Publications LtdeLife2050-084X2021-04-011010.7554/eLife.62639Two opposite voltage-dependent currents control the unusual early development pattern of embryonic Renshaw cell electrical activityJuliette Boeri0Claude Meunier1https://orcid.org/0000-0002-8216-3991Hervé Le Corronc2Pascal Branchereau3https://orcid.org/0000-0003-3972-8229Yulia Timofeeva4https://orcid.org/0000-0003-3178-7830François-Xavier Lejeune5Christine Mouffle6Hervé Arulkandarajah7Jean Marie Mangin8Pascal Legendre9https://orcid.org/0000-0002-5086-4515Antonny Czarnecki10https://orcid.org/0000-0002-5104-034XINSERM, UMR_S 1130, CNRS, UMR 8246, Neuroscience Paris Seine, Institute of Biology Paris Seine, Sorbonne Univ, Paris, FranceCentre de Neurosciences Intégratives et Cognition, CNRS UMR 8002, Institut Neurosciences et Cognition, Université de Paris, Paris, FranceINSERM, UMR_S 1130, CNRS, UMR 8246, Neuroscience Paris Seine, Institute of Biology Paris Seine, Sorbonne Univ, Paris, France; Univ Angers, Angers, FranceUniv. Bordeaux, CNRS, EPHE, INCIA, Bordeaux, FranceDepartment of Computer Science and Centre for Complexity Science, University of Warwick, Coventry, United Kingdom; Department of Clinical and Experimental Epilepsy, UCL Queen Square Institute of Neurology, University College London, London, United KingdomInstitut du Cerveau et de la Moelle Epinière, Centre de Recherche CHU Pitié-Salpétrière, INSERM, U975, CNRS, UMR 7225, Sorbonne Univ, Paris, FranceINSERM, UMR_S 1130, CNRS, UMR 8246, Neuroscience Paris Seine, Institute of Biology Paris Seine, Sorbonne Univ, Paris, FranceINSERM, UMR_S 1130, CNRS, UMR 8246, Neuroscience Paris Seine, Institute of Biology Paris Seine, Sorbonne Univ, Paris, FranceINSERM, UMR_S 1130, CNRS, UMR 8246, Neuroscience Paris Seine, Institute of Biology Paris Seine, Sorbonne Univ, Paris, FranceINSERM, UMR_S 1130, CNRS, UMR 8246, Neuroscience Paris Seine, Institute of Biology Paris Seine, Sorbonne Univ, Paris, FranceINSERM, UMR_S 1130, CNRS, UMR 8246, Neuroscience Paris Seine, Institute of Biology Paris Seine, Sorbonne Univ, Paris, France; Univ. Bordeaux, CNRS, EPHE, INCIA, Bordeaux, FranceRenshaw cells (V1R) are excitable as soon as they reach their final location next to the spinal motoneurons and are functionally heterogeneous. Using multiple experimental approaches, in combination with biophysical modeling and dynamical systems theory, we analyzed, for the first time, the mechanisms underlying the electrophysiological properties of V1R during early embryonic development of the mouse spinal cord locomotor networks (E11.5–E16.5). We found that these interneurons are subdivided into several functional clusters from E11.5 and then display an unexpected transitory involution process during which they lose their ability to sustain tonic firing. We demonstrated that the essential factor controlling the diversity of the discharge pattern of embryonic V1R is the ratio of a persistent sodium conductance to a delayed rectifier potassium conductance. Taken together, our results reveal how a simple mechanism, based on the synergy of two voltage-dependent conductances that are ubiquitous in neurons, can produce functional diversity in embryonic V1R and control their early developmental trajectory.https://elifesciences.org/articles/62639developmentspinal cordRenshaw cellfiring patternembryobiophysical modeling
collection DOAJ
language English
format Article
sources DOAJ
author Juliette Boeri
Claude Meunier
Hervé Le Corronc
Pascal Branchereau
Yulia Timofeeva
François-Xavier Lejeune
Christine Mouffle
Hervé Arulkandarajah
Jean Marie Mangin
Pascal Legendre
Antonny Czarnecki
spellingShingle Juliette Boeri
Claude Meunier
Hervé Le Corronc
Pascal Branchereau
Yulia Timofeeva
François-Xavier Lejeune
Christine Mouffle
Hervé Arulkandarajah
Jean Marie Mangin
Pascal Legendre
Antonny Czarnecki
Two opposite voltage-dependent currents control the unusual early development pattern of embryonic Renshaw cell electrical activity
eLife
development
spinal cord
Renshaw cell
firing pattern
embryo
biophysical modeling
author_facet Juliette Boeri
Claude Meunier
Hervé Le Corronc
Pascal Branchereau
Yulia Timofeeva
François-Xavier Lejeune
Christine Mouffle
Hervé Arulkandarajah
Jean Marie Mangin
Pascal Legendre
Antonny Czarnecki
author_sort Juliette Boeri
title Two opposite voltage-dependent currents control the unusual early development pattern of embryonic Renshaw cell electrical activity
title_short Two opposite voltage-dependent currents control the unusual early development pattern of embryonic Renshaw cell electrical activity
title_full Two opposite voltage-dependent currents control the unusual early development pattern of embryonic Renshaw cell electrical activity
title_fullStr Two opposite voltage-dependent currents control the unusual early development pattern of embryonic Renshaw cell electrical activity
title_full_unstemmed Two opposite voltage-dependent currents control the unusual early development pattern of embryonic Renshaw cell electrical activity
title_sort two opposite voltage-dependent currents control the unusual early development pattern of embryonic renshaw cell electrical activity
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2021-04-01
description Renshaw cells (V1R) are excitable as soon as they reach their final location next to the spinal motoneurons and are functionally heterogeneous. Using multiple experimental approaches, in combination with biophysical modeling and dynamical systems theory, we analyzed, for the first time, the mechanisms underlying the electrophysiological properties of V1R during early embryonic development of the mouse spinal cord locomotor networks (E11.5–E16.5). We found that these interneurons are subdivided into several functional clusters from E11.5 and then display an unexpected transitory involution process during which they lose their ability to sustain tonic firing. We demonstrated that the essential factor controlling the diversity of the discharge pattern of embryonic V1R is the ratio of a persistent sodium conductance to a delayed rectifier potassium conductance. Taken together, our results reveal how a simple mechanism, based on the synergy of two voltage-dependent conductances that are ubiquitous in neurons, can produce functional diversity in embryonic V1R and control their early developmental trajectory.
topic development
spinal cord
Renshaw cell
firing pattern
embryo
biophysical modeling
url https://elifesciences.org/articles/62639
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