Phase response analyses support a relaxation oscillator model of locomotor rhythm generation in Caenorhabditis elegans

Abstract

Neural circuits coordinate with muscles and sensory feedback to generate motor behaviors appropriate to an animal’s environment. In C. elegans, the mechanisms by which the motor circuit generates undulations and modulates them based on the environment are largely unclear. We quantitatively analyzed C. elegans locomotion during free movement and during transient optogenetic muscle inhibition. Undulatory movements were highly asymmetrical with respect to the duration of bending and unbending during each cycle. Phase response curves induced by brief optogenetic inhibition of head muscles showed gradual increases and rapid decreases as a function of phase at which the perturbation was applied. A relaxation oscillator model based on proprioceptive thresholds that switch the active muscle moment was developed and is shown to quantitatively agree with data from free movement, phase responses, and previous results for gait adaptation to mechanical loadings. Our results suggest a neuromuscular mechanism underlying C. elegans motor pattern generation within a compact circuit.

Data availability

All data and software have been deposited to a Dryad repository.

Article and author information

Author details

  1. Hongfei Ji

    Bioengineering, University of Pennsylvania, Philadelphia, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9617-6411
  2. Anthony D Fouad

    Bioengineering, University of Pennsylvania, Philadelphia, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4677-2968
  3. Shelly Teng

    Bioengineering, University of Pennsylvania, Philadelphia, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Alice Liu

    Bioengineering, University of Pennsylvania, Philadelphia, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Pilar Alvarez-Illera

    Bioengineering, University of Pennsylvania, Philadelphia, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Bowen Yao

    Bioengineering, University of Pennsylvania, Philadelphia, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Zihao Li Mr.

    Department of Bioengineering, University of Pennsylvania, Philadelphia, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4304-8322
  8. Christopher Fang-Yen

    Department of Bioengineering, University of Pennsylvania, Philadelphia, United States
    For correspondence
    cfangyen@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4568-3218

Funding

NIH (1R01NS084835)

  • Hongfei Ji
  • Anthony D Fouad
  • Christopher Fang-Yen

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, University of Vienna, Austria

Publication history

  1. Preprint posted: June 23, 2020 (view preprint)
  2. Received: April 29, 2021
  3. Accepted: September 24, 2021
  4. Accepted Manuscript published: September 27, 2021 (version 1)
  5. Version of Record published: November 1, 2021 (version 2)

Copyright

© 2021, Ji 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. Hongfei Ji
  2. Anthony D Fouad
  3. Shelly Teng
  4. Alice Liu
  5. Pilar Alvarez-Illera
  6. Bowen Yao
  7. Zihao Li Mr.
  8. Christopher Fang-Yen
(2021)
Phase response analyses support a relaxation oscillator model of locomotor rhythm generation in Caenorhabditis elegans
eLife 10:e69905.
https://doi.org/10.7554/eLife.69905

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