Mechanosensory neurons control the timing of spinal microcircuit selection during locomotion

Abstract

Despite numerous physiological studies about reflexes in the spinal cord, the contribution of mechanosensory feedback to active locomotion and the nature of underlying spinal circuits remains elusive. Here we investigate how mechanosensory feedback shapes active locomotion in a genetic model organism exhibiting simple locomotion—the zebrafish larva. We show that mechanosensory feedback enhances the recruitment of motor pools during active locomotion. Furthermore, we demonstrate that inputs from mechanosensory neurons increase locomotor speed by prolonging fast swimming at the expense of slow swimming during stereotyped acoustic escape responses. This effect could be mediated by distinct mechanosensory neurons. In the spinal cord, we show that connections compatible with monosynaptic inputs from mechanosensory Rohon-Beard neurons onto ipsilateral V2a interneurons selectively recruited at high speed can contribute to the observed enhancement of speed. Altogether, our study reveals the basic principles and a circuit diagram enabling speed modulation by mechanosensory feedback in the vertebrate spinal cord.

Article and author information

Author details

  1. Claire Wyart

    Institut du Cerveau et la Moelle épinière, Hôpital Pitié-Salpêtrière, Sorbonne Universités, UPMC Univ Paris 06, Inserm, CNRS, Paris, France
    For correspondence
    claire.wyart@icm-institute.org
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1668-4975
  2. Steven Knafo

    Institut du Cerveau et la Moelle épinière, Hôpital Pitié-Salpêtrière, Sorbonne Universités, UPMC Univ Paris 06, Inserm, CNRS, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Kevin Fidelin

    Institut du Cerveau et la Moelle épinière, Hôpital Pitié-Salpêtrière, Sorbonne Universités, UPMC Univ Paris 06, Inserm, CNRS, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Andrew Prendergast

    Institut du Cerveau et la Moelle épinière, Hôpital Pitié-Salpêtrière, Sorbonne Universités, UPMC Univ Paris 06, Inserm, CNRS, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Po-En Brian Tseng

    Institut du Cerveau et la Moelle épinière, Hôpital Pitié-Salpêtrière, Sorbonne Universités, UPMC Univ Paris 06, Inserm, CNRS, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  6. Alexandre Parrin

    Institut du Cerveau et la Moelle épinière, Hôpital Pitié-Salpêtrière, Sorbonne Universités, UPMC Univ Paris 06, Inserm, CNRS, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  7. Charles William Dickey

    Institut du Cerveau et la Moelle épinière, Hôpital Pitié-Salpêtrière, Sorbonne Universités, UPMC Univ Paris 06, Inserm, CNRS, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  8. Urs Lucas Böhm

    Institut du Cerveau et la Moelle épinière, Hôpital Pitié-Salpêtrière, Sorbonne Universités, UPMC Univ Paris 06, Inserm, CNRS, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  9. Sophie Nunes FIgueiredo

    Institut du Cerveau et la Moelle épinière, Hôpital Pitié-Salpêtrière, Sorbonne Universités, UPMC Univ Paris 06, Inserm, CNRS, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  10. Olivier Thouvenin

    Institut du Cerveau et la Moelle épinière, Hôpital Pitié-Salpêtrière, Sorbonne Universités, UPMC Univ Paris 06, Inserm, CNRS, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4853-7555
  11. Hugues Pascal-Moussellard

    Institut du Cerveau et la Moelle épinière, Hôpital Pitié-Salpêtrière, Sorbonne Universités, UPMC Univ Paris 06, Inserm, CNRS, Paris, France
    Competing interests
    The authors declare that no competing interests exist.

Funding

European Research Council (311673)

  • Claire Wyart

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

Reviewing Editor

  1. Ronald L Calabrese, Emory University, United States

Ethics

Animal experimentation: All procedures were approved by the Institutional Ethics Committee at the Institut du Cerveau et de la Moelle épinière (ICM), Paris, France, the Ethical Committee Charles Darwin and received subsequent approval from the EEC (2010/63/EU).

Version history

  1. Received: January 19, 2017
  2. Accepted: June 17, 2017
  3. Accepted Manuscript published: June 17, 2017 (version 1)
  4. Accepted Manuscript updated: June 19, 2017 (version 2)
  5. Version of Record published: July 6, 2017 (version 3)

Copyright

© 2017, Wyart 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. Claire Wyart
  2. Steven Knafo
  3. Kevin Fidelin
  4. Andrew Prendergast
  5. Po-En Brian Tseng
  6. Alexandre Parrin
  7. Charles William Dickey
  8. Urs Lucas Böhm
  9. Sophie Nunes FIgueiredo
  10. Olivier Thouvenin
  11. Hugues Pascal-Moussellard
(2017)
Mechanosensory neurons control the timing of spinal microcircuit selection during locomotion
eLife 6:e25260.
https://doi.org/10.7554/eLife.25260

Share this article

https://doi.org/10.7554/eLife.25260

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