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Functionally asymmetric motor neurons contribute to coordinating locomotion of Caenorhabditis elegans

Research Article
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Cite this article as: eLife 2018;7:e34997 doi: 10.7554/eLife.34997

Abstract

Locomotion circuits developed in simple animals, and circuit motifs further evolved in higher animals. To understand locomotion circuit motifs, they must be characterized in many models. The nematode Caenorhabditis elegans possesses one of the best-studied circuits for undulatory movement. Yet, for 1/6th of the cholinergic motor neurons (MNs), the AS MNs, functional information is unavailable. Ventral nerve cord (VNC) MNs coordinate undulations, in small circuits of complementary neurons innervating opposing muscles. AS MNs differ, as they innervate muscles and other MNs asymmetrically, without complementary partners. We characterized AS MNs by optogenetic, behavioral and imaging analyses. They generate asymmetric muscle activation, enabling navigation, and contribute to coordination of dorso-ventral undulation as well as anterio-posterior bending wave propagation. AS MN activity correlated with forward and backward locomotion, and they functionally connect to premotor interneurons (PINs) for both locomotion regimes. Electrical feedback from AS MNs via gap junctions may affect only backward PINs.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files are videos from live cell imaging and behavioral experiments. They are several terabytes in size and can therefore be provided upon request to the corresponding author.

Article and author information

Author details

  1. Oleg Tolstenkov

    Buchmann Institute for Molecular Life Sciences, Goethe University, Frankfurt, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Petrus Van der Auwera

    Buchmann Institute for Molecular Life Sciences, Goethe University, Frankfurt, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7540-4788
  3. Wagner Steuer Costa

    Buchmann Institute for Molecular Life Sciences, Goethe University, Frankfurt, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7707-2596
  4. Olga Bazhanova

    Buchmann Institute for Molecular Life Sciences, Goethe University, Frankfurt, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Tim M Gemeinhardt

    Buchmann Institute for Molecular Life Sciences, Goethe University, Frankfurt, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Amelie CF Bergs

    Buchmann Institute for Molecular Life Sciences, Goethe University, Frankfurt, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Alexander Gottschalk

    Buchmann Institute for Molecular Life Sciences, Goethe University, Frankfurt, Germany
    For correspondence
    a.gottschalk@em.uni-frankfurt.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1197-6119

Funding

Deutsche Forschungsgemeinschaft (GO1011/4-2)

  • Petrus Van der Auwera
  • Wagner Steuer Costa
  • Alexander Gottschalk

Goethe University (GO-IN)

  • Oleg Tolstenkov

European Union Marie Curie Actions (PCOFUND-GA-2011-291776)

  • Oleg Tolstenkov

Deutsche Forschungsgemeinschaft (GO1011/8-1)

  • Oleg Tolstenkov
  • Alexander Gottschalk

Deutsche Forschungsgemeinschaft (EXC115/3)

  • Petrus Van der Auwera
  • Wagner Steuer Costa
  • Alexander Gottschalk

Max-Planck-Research School (IMPReS Membrane Biology)

  • Amelie CF Bergs

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

Reviewing Editor

  1. Oliver Hobert, Howard Hughes Medical Institute, Columbia University, United States

Publication history

  1. Received: January 11, 2018
  2. Accepted: September 9, 2018
  3. Accepted Manuscript published: September 11, 2018 (version 1)
  4. Version of Record published: October 5, 2018 (version 2)

Copyright

© 2018, Tolstenkov 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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