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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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2021-04-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/62639 |
| _version_ | 1811180596085391360 |
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| 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 |
| 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 |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-04-11T09:06:02Z |
| format | Article |
| id | doaj.art-494cac047e70452eb08a221a9d92d323 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-11T09:06:02Z |
| publishDate | 2021-04-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-494cac047e70452eb08a221a9d92d3232022-12-22T04:32:39ZengeLife 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 |
| 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 |
| title | 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_short | 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 |
| topic | development spinal cord Renshaw cell firing pattern embryo biophysical modeling |
| url | https://elifesciences.org/articles/62639 |
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