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

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Abstract

Renshaw cells (V1^R) 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 V1^R 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 V1^R and control their early developmental trajectory.

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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).

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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.
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.
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.
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.

"This ORCID iD identifies the author of this article:" 0000-0003-3972-8229
Yulia Timofeeva

Department of Clinical and Experimental Epilepsy, UCL Queen Square Institute of Neurology, University College London, LONDON, United Kingdom

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The authors declare that no competing interests exist.
François-Xavier Lejeune

U1127 INSERM, Institut du Cerveau et de la Moelle Épinière, Paris, France

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The authors declare that no competing interests exist.
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.
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.
Jean Marie Mangin

INSERM, UMR_S 1130, CNRS, UMR 8246, Neuroscience Paris Seine, Institute of Biology Paris Seine, Sorbonne University, Paris, France

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The authors declare that no competing interests exist.
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.

"This ORCID iD identifies the author of this article:" 0000-0002-5086-4515
Antonny Czarnecki

Neurosciences Paris Seine (UM119 UPMC, UMR8246 CNRS, U1130 INSERM), Université Pierre et Marie Curie, Paris, France

For correspondence
antonny.czarnecki@u-bordeaux.fr

Competing interests
The authors declare that no competing interests exist.

"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.

Copyright

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.