Stereotyped behavioral maturation and rhythmic quiescence in C.elegans embryos

  1. Evan L Ardiel  Is a corresponding author
  2. Andrew Lauziere
  3. Stephen Xu
  4. Brandon J Harvey
  5. Ryan Patrick Christensen
  6. Stephen Nurrish
  7. Joshua M Kaplan
  8. Hari Shroff
  1. Massachusetts General Hospital, United States
  2. National Institute of Biomedical Imaging and Bioengineering, United States

Abstract

Systematic analysis of rich behavioral recordings is being used to uncover how circuits encode complex behaviors. Here we apply this approach to embryos. What are the first embryonic behaviors and how do they evolve as early neurodevelopment ensues? To address these questions, we present a systematic description of behavioral maturation for Caenorhabditis elegans embryos. Posture libraries were built using a genetically encoded motion capture suit imaged with light-sheet microscopy and annotated using custom tracking software. Analysis of cell trajectories, postures, and behavioral motifs revealed a stereotyped developmental progression. Early movement is dominated by flipping between dorsal and ventral coiling, which gradually slows into a period of reduced motility. Late-stage embryos exhibit sinusoidal waves of dorsoventral bends, prolonged bouts of directed motion, and a rhythmic pattern of pausing, which we designate slow wave twitch (SWT). Synaptic transmission is required for late-stage motion but not for early flipping nor the intervening inactive phase. A high-throughput behavioral assay and calcium imaging revealed that SWT is elicited by the rhythmic activity of a quiescence-promoting neuron (RIS). Similar periodic quiescent states are seen prenatally in diverse animals and may play an important role in promoting normal developmental outcomes.

Data availability

Annotated image volumes are available on FigShare. Code for MHHT is available on GitHub.

The following data sets were generated

Article and author information

Author details

  1. Evan L Ardiel

    Department of Molecular Biology, Massachusetts General Hospital, Boston, United States
    For correspondence
    ardiel@molbio.mgh.harvard.edu
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9366-5751
  2. Andrew Lauziere

    National Institute of Biomedical Imaging and Bioengineering, Bethesda, United States
    Competing interests
    No competing interests declared.
  3. Stephen Xu

    National Institute of Biomedical Imaging and Bioengineering, Bethesda, United States
    Competing interests
    No competing interests declared.
  4. Brandon J Harvey

    National Institute of Biomedical Imaging and Bioengineering, Bethesda, United States
    Competing interests
    Brandon J Harvey, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7471-9937
  5. Ryan Patrick Christensen

    National Institute of Biomedical Imaging and Bioengineering, Bethesda, United States
    Competing interests
    No competing interests declared.
  6. Stephen Nurrish

    Department of Molecular Biology, Massachusetts General Hospital, Boston, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2653-9384
  7. Joshua M Kaplan

    Department of Molecular Biology, Massachusetts General Hospital, Boston, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7418-7179
  8. Hari Shroff

    National Institute of Biomedical Imaging and Bioengineering, Bethesda, United States
    Competing interests
    No competing interests declared.

Funding

William Randolph Hearst Foundation

  • Evan L Ardiel

National Science Foundation (DGE-1632976)

  • Andrew Lauziere

National Institutes of Health (NS32196)

  • Joshua M Kaplan

National Institutes of Health (NS121182)

  • Joshua M Kaplan

National Institute of Biomedical Imaging and Bioengineering

  • Hari Shroff

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

Reviewing Editor

  1. Matthieu Louis, University of California, Santa Barbara, United States

Version history

  1. Preprint posted: December 10, 2021 (view preprint)
  2. Received: January 6, 2022
  3. Accepted: August 1, 2022
  4. Accepted Manuscript published: August 5, 2022 (version 1)
  5. Accepted Manuscript updated: August 8, 2022 (version 2)
  6. Version of Record published: September 5, 2022 (version 3)
  7. Version of Record updated: September 13, 2022 (version 4)

Copyright

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

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  1. Evan L Ardiel
  2. Andrew Lauziere
  3. Stephen Xu
  4. Brandon J Harvey
  5. Ryan Patrick Christensen
  6. Stephen Nurrish
  7. Joshua M Kaplan
  8. Hari Shroff
(2022)
Stereotyped behavioral maturation and rhythmic quiescence in C.elegans embryos
eLife 11:e76836.
https://doi.org/10.7554/eLife.76836

Share this article

https://doi.org/10.7554/eLife.76836

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