Proximal and distal spinal neurons innervating multiple synergist and antagonist motor pools

Abstract

Motoneurons control muscle contractions, and their recruitment by premotor circuits is tuned to produce accurate motor behaviours. To understand how these circuits coordinate movement across and between joints, it is necessary to understand whether spinal neurons pre-synaptic to motor pools have divergent projections to more than one motoneuron population. Here, we used modified rabies virus tracing in mice to investigate premotor INs projecting to synergist flexor or extensor motoneurons, as well as those projecting to antagonist pairs of muscles controlling the ankle joint. We show that similar proportions of premotor neurons diverge to synergist and antagonist motor pools. Divergent premotor neurons were seen throughout the spinal cord, with decreasing numbers but increasing proportion with distance from the hindlimb enlargement. In the cervical cord, divergent long descending propriospinal neurons were found in contralateral lamina VIII, had large somata, were neither glycinergic, nor cholinergic, and projected to both lumbar and cervical motoneurons. We conclude that distributed spinal premotor neurons coordinate activity across multiple motor pools and that there are spinal neurons mediating co-contraction of antagonist muscles.

Data availability

All data generated during this study are included in the manuscript and supporting files. Source data files have been provided as Supplementary information for Figures 1 to 7 in the main text and for supplementary Figures S1 to S5. The data in supplementary Figure 1 are reported in the Supplementary Table 3

Article and author information

Author details

  1. Remi Ronzano

    Department of Neuromuscular Diseases, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  2. Camille Lancelin

    Department of Neuromuscular Diseases, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Gardave Singh Bhumbra

    Department of Neuroscience Physiology and Pharmacology, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Robert M Brownstone

    Department of Neuromuscular Diseases, University College London, London, United Kingdom
    For correspondence
    r.browstone@ucl.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5135-2725
  5. Marco Beato

    Neuroscience, Physiology and Pharmacology, University College London, London, United Kingdom
    For correspondence
    m.beato@ucl.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7283-8318

Funding

Leverhulme Trust (RPG-2013-176)

  • Marco Beato

Biotechnology and Biological Sciences Research Council (BB/L001454)

  • Marco Beato

Wellcome Trust (110193)

  • Robert M Brownstone

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

Reviewing Editor

  1. Muriel Thoby-Brisson, CNRS Université de Bordeaux, France

Ethics

Animal experimentation: All experiments were performed in strict adherence to the Animals (Scientific Procedures) Act UK (1986) and certified by the UCL AWERB committee, under project licence number 70/7621. All surgeries were performed under general isofluorane anaesthesia and before surgery animals were injected subcutaneously with an analgesic (carprofen, 1 μl, 10% w/v) and the mice were closely monitored for a 24 hours period following surgery to detect any sign of distress or motor impairment. Every effort was made to minimize suffering

Version history

  1. Received: May 31, 2021
  2. Preprint posted: June 3, 2021 (view preprint)
  3. Accepted: November 1, 2021
  4. Accepted Manuscript published: November 2, 2021 (version 1)
  5. Version of Record published: November 30, 2021 (version 2)

Copyright

© 2021, Ronzano 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. Remi Ronzano
  2. Camille Lancelin
  3. Gardave Singh Bhumbra
  4. Robert M Brownstone
  5. Marco Beato
(2021)
Proximal and distal spinal neurons innervating multiple synergist and antagonist motor pools
eLife 10:e70858.
https://doi.org/10.7554/eLife.70858

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https://doi.org/10.7554/eLife.70858

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