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Flexible motor sequence generation during stereotyped escape responses

  1. Yuan Wang
  2. Xiaoqian Zhang
  3. Qi Xin
  4. Wesley Hung
  5. Jeremy Florman
  6. Jing Huo
  7. Tianqi Xu
  8. Yu Xie
  9. Mark J Alkema
  10. Mei Zhen
  11. Quan Wen  Is a corresponding author
  1. University of Science and Technology of China, China
  2. Mount Sinai Hospital, Canada
  3. University of Massachusetts Medical School, United States
  4. University of Toronto, Canada
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Cite this article as: eLife 2020;9:e56942 doi: 10.7554/eLife.56942

Abstract

Complex animal behaviors arise from a flexible combination of stereotyped motor primitives. Here we use the escape responses of the nematode Caenorhabditis elegans to study how a nervous system dynamically explores the action space. The initiation of the escape responses is predictable: the animal moves away from a potential threat, a mechanical or thermal stimulus. But the motor sequence and the timing that follow are variable. We report that a feedforward excitation between neurons encoding distinct motor states underlies robust motor sequence generation, while mutual inhibition between these neurons controls the flexibility of timing in a motor sequence. Electrical synapses contribute to feedforward coupling whereas glutamatergic synapses contribute to inhibition. We conclude that C. elegans generates robust and flexible motor sequences by combining an excitatory coupling and a winner-take-all operation via mutual inhibition between motor modules.

Article and author information

Author details

  1. Yuan Wang

    Hefei National Laboratory for Physical Sciences at the Microscale, University of Science and Technology of China, Hefei, China
    Competing interests
    The authors declare that no competing interests exist.
  2. Xiaoqian Zhang

    School of Life Sciences, University of Science and Technology of China, Hefei, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Qi Xin

    School of Life Sciences, University of Science and Technology of China, Hefei, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Wesley Hung

    Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  5. Jeremy Florman

    Neurobiology, University of Massachusetts Medical School, Worcester, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7578-3511
  6. Jing Huo

    School of Life Sciences, University of Science and Technology of China, Hefei, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Tianqi Xu

    Chinese Academy of Sciences Key Laboratory of Brain Function and Disease, School of Life Sciences, University of Science and Technology of China, Hefei, China
    Competing interests
    The authors declare that no competing interests exist.
  8. Yu Xie

    School of Physical Sciences, University of Science and Technology of China, Hefei, China
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3624-0252
  9. Mark J Alkema

    Department of Neurobiology, University of Massachusetts Medical School, Worcester, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1311-5179
  10. Mei Zhen

    Lunenfeld-Tanenbaum Research Institute, University of Toronto, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0086-9622
  11. Quan Wen

    Hefei National Laboratory for Physical Sciences at Microscale, University of Science and Technology of China, Hefei, China
    For correspondence
    qwen@ustc.edu.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0268-8403

Funding

National Science Foundation of China (NSFC-31471051 and NSFC-91632102)

  • Yuan Wang
  • Xiaoqian Zhang
  • Qi Xin
  • Jing Huo
  • Tianqi Xu
  • Yu Xie
  • Quan Wen

Strategic Priority Research Program of Chinese Academy of Sciences (XDPB10)

  • Yuan Wang
  • Xiaoqian Zhang
  • Qi Xin
  • Jing Huo
  • Tianqi Xu
  • Yu Xie
  • Quan Wen

CIHR (Foundation Scheme 154274)

  • Wesley Hung
  • Mei Zhen

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

Reviewing Editor

  1. Manuel Zimmer, Research Institute of Molecular Pathology, Vienna Biocenter and University of Vienna, Austria

Publication history

  1. Received: March 15, 2020
  2. Accepted: June 5, 2020
  3. Accepted Manuscript published: June 5, 2020 (version 1)

Copyright

© 2020, Wang 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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