Activity of the C. elegans egg-laying behavior circuit is controlled by competing activation and feedback inhibition

  1. Kevin M Collins  Is a corresponding author
  2. Addys Bode
  3. Robert W Fernandez
  4. Jessica E Tanis
  5. Jacob C Brewer
  6. Matthew S Creamer
  7. Michael R Koelle
  1. University of Miami, United States
  2. Yale University, United States

Abstract

Like many behaviors, Caenorhabditis elegans egg laying alternates between inactive and active states. To understand how the underlying neural circuit turns the behavior on and off, we optically recorded circuit activity in behaving animals while manipulating circuit function using mutations, optogenetics, and drugs. In the active state, the circuit shows rhythmic activity phased with the body bends of locomotion. The serotonergic HSN command neurons initiate the active state, but accumulation of unlaid eggs also promotes the active state independent of the HSNs. The cholinergic VC motor neurons slow locomotion during egg-laying muscle contraction and egg release. The uv1 neuroendocrine cells mechanically sense passage of eggs through the vulva and release tyramine to inhibit egg laying, in part via the LGC-55 tyramine-gated Cl- channel on the HSNs. Our results identify discrete signals that entrain or detach the circuit from the locomotion central pattern generator to produce active and inactive states.

Article and author information

Author details

  1. Kevin M Collins

    Department of Biology, University of Miami, Coral Gables, United States
    For correspondence
    kcollins@bio.miami.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9930-0924
  2. Addys Bode

    Department of Biology, University of Miami, Coral Gables, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Robert W Fernandez

    Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Jessica E Tanis

    Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Jacob C Brewer

    Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2780-2874
  6. Matthew S Creamer

    Interdepartmental Neuroscience Program, Yale University, New Haven, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Michael R Koelle

    Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9486-8481

Funding

American Heart Association (Postdoctoral Fellowship, POST4990016)

  • Kevin M Collins

National Institute of Neurological Disorders and Stroke (NS086932)

  • Kevin M Collins
  • Michael R Koelle

National Institute of Neurological Disorders and Stroke (NS036918)

  • Michael R Koelle

Yale Liver Center (DK34989)

  • Kevin M Collins

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

Version history

  1. Received: August 31, 2016
  2. Accepted: November 14, 2016
  3. Accepted Manuscript published: November 16, 2016 (version 1)
  4. Version of Record published: December 7, 2016 (version 2)

Copyright

© 2016, Collins 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. Kevin M Collins
  2. Addys Bode
  3. Robert W Fernandez
  4. Jessica E Tanis
  5. Jacob C Brewer
  6. Matthew S Creamer
  7. Michael R Koelle
(2016)
Activity of the C. elegans egg-laying behavior circuit is controlled by competing activation and feedback inhibition
eLife 5:e21126.
https://doi.org/10.7554/eLife.21126

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https://doi.org/10.7554/eLife.21126

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