Stereotyped behavioral maturation and rhythmic quiescence in C.elegans embryos
- Massachusetts General Hospital, United States
- 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.
Article and author information
Author details
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
- Matthieu Louis, University of California, Santa Barbara, United States
Publication history
- Preprint posted: December 10, 2021 (view preprint)
- Received: January 6, 2022
- Accepted: August 1, 2022
- Accepted Manuscript published: August 5, 2022 (version 1)
- Accepted Manuscript updated: August 8, 2022 (version 2)
- Version of Record published: September 5, 2022 (version 3)
- 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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Stereotyped behavioral maturation and rhythmic quiescence in C.elegans embryos
eLife 11:e76836.
https://doi.org/10.7554/eLife.76836
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