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

  1. Juliette Boeri
  2. Claude Meunier
  3. Hervé Le Corronc
  4. Pascal Branchereau
  5. Yulia Timofeeva
  6. François-Xavier Lejeune
  7. Christine Mouffle
  8. Hervé Arulkandarajah
  9. Jean Marie Mangin
  10. Pascal Legendre  Is a corresponding author
  11. Antonny Czarnecki  Is a corresponding author
  1. Sorbonne University, France
  2. Université de Paris, France
  3. Université de Bordeaux, CNRS, France
  4. UCL Queen Square Institute of Neurology, University College London, United Kingdom
  5. Institut du Cerveau et de la Moelle Épinière, France

Abstract

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.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for Figures 3 (Source data files for cluster analysis).

Article and author information

Author details

  1. Juliette Boeri

    INSERM, UMR_S 1130, CNRS, UMR 8246, Neuroscience Paris Seine, Institute of Biology Paris Seine, Sorbonne University, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  2. Claude Meunier

    Centre de Neurosciences Intégratives et Cognition, CNRS UMR 8002, Institut Neurosciences et Cognition, Université de Paris, PARIS, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Hervé Le Corronc

    INSERM, UMR_S 1130, CNRS, UMR 8246, Neuroscience Paris Seine, Institute of Biology Paris Seine, Sorbonne University, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Pascal Branchereau

    Institut de Neurosciences Cognitives et Intégratives d'Aquitaine (INCIA) - UMR 5287, Université de Bordeaux, CNRS, Bordeaux, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3972-8229
  5. Yulia Timofeeva

    Department of Clinical and Experimental Epilepsy, UCL Queen Square Institute of Neurology, University College London, LONDON, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  6. François-Xavier Lejeune

    U1127 INSERM, Institut du Cerveau et de la Moelle Épinière, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  7. Christine Mouffle

    INSERM, UMR_S 1130, CNRS, UMR 8246, Neuroscience Paris Seine, Institute of Biology Paris Seine, Sorbonne University, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  8. Hervé Arulkandarajah

    INSERM, UMR_S 1130, CNRS, UMR 8246, Neuroscience Paris Seine, Institute of Biology Paris Seine, Sorbonne University, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  9. Jean Marie Mangin

    INSERM, UMR_S 1130, CNRS, UMR 8246, Neuroscience Paris Seine, Institute of Biology Paris Seine, Sorbonne University, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  10. Pascal Legendre

    INSERM, UMR_S 1130, CNRS, UMR 8246, Neuroscience Paris Seine, Institute of Biology Paris Seine, Sorbonne University, Paris, France
    For correspondence
    pascal.legendre@inserm.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5086-4515
  11. Antonny Czarnecki

    INSERM, UMR_S 1130, CNRS, UMR 8246, Neuroscience Paris Seine, Institute of Biology Paris Seine, Sorbonne University, Paris, France
    For correspondence
    antonny.czarnecki@u-bordeaux.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5104-034X

Funding

Fondation pour la recherche medicale (DEQ20160334891)

  • Pascal Legendre

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: Experiments were performed in accordance with European Community guiding principles on the care and use of animals (86/609/CEE, CE Off J no. L358, 18 December 1986), French decree no. 97/748 of October 19, 1987 (Journal Officiel République Française, 20 October 1987, pp. 12245-12248). All procedures were carried out in accordance with the local ethics committee of local Universities and recommendations from the CNRS. pregnant mice were anesthetized by intramuscular injection of a mix of ketamine and xylazine and sacrificed using a lethal dose of CO2 after embryos of either sex were removed. Every effort was made to minimize suffering.

Reviewing Editor

  1. Jeffrey C Smith, National Institute of Neurological Disorders and Stroke, United States

Version history

  1. Received: August 31, 2020
  2. Accepted: April 24, 2021
  3. Accepted Manuscript published: April 26, 2021 (version 1)
  4. Accepted Manuscript updated: April 29, 2021 (version 2)
  5. Version of Record published: May 21, 2021 (version 3)

Copyright

© 2021, Boeri et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Juliette Boeri
  2. Claude Meunier
  3. Hervé Le Corronc
  4. Pascal Branchereau
  5. Yulia Timofeeva
  6. François-Xavier Lejeune
  7. Christine Mouffle
  8. Hervé Arulkandarajah
  9. Jean Marie Mangin
  10. Pascal Legendre
  11. Antonny Czarnecki
(2021)
Two opposite voltage-dependent currents control the unusual early development pattern of embryonic Renshaw cell electrical activity
eLife 10:e62639.
https://doi.org/10.7554/eLife.62639

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https://doi.org/10.7554/eLife.62639