Spinal V2b neurons reveal a role for ipsilateral inhibition in speed control

  1. Rebecca A Callahan
  2. Richard Roberts
  3. Mohini Sengupta
  4. Yukiko Kimura
  5. Shin-ichi Higashijima
  6. Martha W Bagnall  Is a corresponding author
  1. Washington University School of Medicine, United States
  2. National Institute for Basic Biology, Japan

Abstract

The spinal cord contains a diverse array of interneurons that govern motor output. Traditionally, models of spinal circuits have emphasized the role of inhibition in enforcing reciprocal alternation between left and right sides or flexors and extensors. However, recent work has shown that inhibition also increases coincident with excitation during contraction. Here, using larval zebrafish, we investigate the V2b (Gata3+) class of neurons, which contribute to flexor-extensor alternation but are otherwise poorly understood. Using newly generated transgenic lines we define two stable subclasses with distinct neurotransmitter and morphological properties. These V2b subclasses synapse directly onto motor neurons with differential targeting to speed-specific circuits. In vivo, optogenetic manipulation of V2b activity modulates locomotor frequency: suppressing V2b neurons elicits faster locomotion, whereas activating V2b neurons slows locomotion. We conclude that V2b neurons serve as a brake on axial motor circuits. Together, these results indicate a role for ipsilateral inhibition in speed control.

Data availability

Datasets have been deposited on Dryad, https://dx.doi.org/10.5061/dryad.1d78mt2

The following data sets were generated

Article and author information

Author details

  1. Rebecca A Callahan

    Department of Neuroscience, Washington University School of Medicine, St Louis, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Richard Roberts

    Department of Neuroscience, Washington University School of Medicine, St Louis, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Mohini Sengupta

    Department of Neuroscience, Washington University School of Medicine, St Louis, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Yukiko Kimura

    Division of Behavioral Neurobiology, National Institute for Basic Biology, Okazaki, Japan
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8381-8622
  5. Shin-ichi Higashijima

    Division of Behavioral Neurobiology, National Institute for Basic Biology, Okazaki, Japan
    Competing interests
    The authors declare that no competing interests exist.
  6. Martha W Bagnall

    Department of Neuroscience, Washington University School of Medicine, St Louis, United States
    For correspondence
    bagnall@wustl.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2102-6165

Funding

National BioResource Project

  • Shin-ichi Higashijima

National Institute on Deafness and Other Communication Disorders (R00 DC012536)

  • Martha W Bagnall

National Institute on Deafness and Other Communication Disorders (R01 DC016413)

  • Martha W Bagnall

National Institute of Neurological Disorders and Stroke (F32 NS103247)

  • Rebecca A Callahan

Alfred P. Sloan Foundation

  • Martha W Bagnall

Pew Charitable Trusts

  • Martha W Bagnall

McKnight Endowment Fund for Neuroscience

  • Martha W Bagnall

Children's Discovery Institute

  • Martha W Bagnall

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

Ethics

Animal experimentation: This research adheres to recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health and received approval by the Washington University Institutional Animal Care and Use Committee (protocol 20170228).

Reviewing Editor

  1. Claire Wyart, Hôpital Pitié-Salpêtrière, Sorbonne Universités, UPMC Univ Paris 06, Inserm, CNRS, France

Version history

  1. Received: April 20, 2019
  2. Accepted: July 26, 2019
  3. Accepted Manuscript published: July 29, 2019 (version 1)
  4. Version of Record published: August 20, 2019 (version 2)

Copyright

© 2019, Callahan 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. Rebecca A Callahan
  2. Richard Roberts
  3. Mohini Sengupta
  4. Yukiko Kimura
  5. Shin-ichi Higashijima
  6. Martha W Bagnall
(2019)
Spinal V2b neurons reveal a role for ipsilateral inhibition in speed control
eLife 8:e47837.
https://doi.org/10.7554/eLife.47837

Share this article

https://doi.org/10.7554/eLife.47837

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