Stereotyped behavioral maturation and rhythmic quiescence in C. elegans embryos
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 systemat...
| Main Authors: | , , , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2022-08-01
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| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/76836 |
| _version_ | 1828108224588414976 |
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| author | Evan L Ardiel Andrew Lauziere Stephen Xu Brandon J Harvey Ryan Patrick Christensen Stephen Nurrish Joshua M Kaplan Hari Shroff |
| author_facet | Evan L Ardiel Andrew Lauziere Stephen Xu Brandon J Harvey Ryan Patrick Christensen Stephen Nurrish Joshua M Kaplan Hari Shroff |
| author_sort | Evan L Ardiel |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-04-11T10:42:59Z |
| format | Article |
| id | doaj.art-195c5b2757f14807b1c4f9a3b0ba51a0 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-11T10:42:59Z |
| publishDate | 2022-08-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-195c5b2757f14807b1c4f9a3b0ba51a02022-12-22T04:29:08ZengeLife Sciences Publications LtdeLife2050-084X2022-08-011110.7554/eLife.76836Stereotyped behavioral maturation and rhythmic quiescence in C. elegans embryosEvan L Ardiel0https://orcid.org/0000-0002-9366-5751Andrew Lauziere1Stephen Xu2Brandon J Harvey3https://orcid.org/0000-0002-7471-9937Ryan Patrick Christensen4Stephen Nurrish5https://orcid.org/0000-0002-2653-9384Joshua M Kaplan6https://orcid.org/0000-0001-7418-7179Hari Shroff7Department of Molecular Biology, Massachusetts General Hospital, Boston, United States; Department of Neurobiology, Harvard Medical School, Boston, United StatesNational Institute of Biomedical Imaging and Bioengineering, National Institutes of Health, Bethesda, United States; Department of Mathematics, University of Maryland, College Park, United StatesNational Institute of Biomedical Imaging and Bioengineering, National Institutes of Health, Bethesda, United StatesNational Institute of Biomedical Imaging and Bioengineering, National Institutes of Health, Bethesda, United States; Fellows Program, Marine Biological Laboratory, Woods Hole, United StatesNational Institute of Biomedical Imaging and Bioengineering, National Institutes of Health, Bethesda, United StatesDepartment of Molecular Biology, Massachusetts General Hospital, Boston, United States; Department of Neurobiology, Harvard Medical School, Boston, United StatesDepartment of Molecular Biology, Massachusetts General Hospital, Boston, United States; Department of Neurobiology, Harvard Medical School, Boston, United StatesNational Institute of Biomedical Imaging and Bioengineering, National Institutes of Health, Bethesda, United States; Fellows Program, Marine Biological Laboratory, Woods Hole, United States; Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United StatesSystematic 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.https://elifesciences.org/articles/76836embryobehaviorneuropeptides |
| spellingShingle | Evan L Ardiel Andrew Lauziere Stephen Xu Brandon J Harvey Ryan Patrick Christensen Stephen Nurrish Joshua M Kaplan Hari Shroff Stereotyped behavioral maturation and rhythmic quiescence in C. elegans embryos eLife embryo behavior neuropeptides |
| title | Stereotyped behavioral maturation and rhythmic quiescence in C. elegans embryos |
| title_full | Stereotyped behavioral maturation and rhythmic quiescence in C. elegans embryos |
| title_fullStr | Stereotyped behavioral maturation and rhythmic quiescence in C. elegans embryos |
| title_full_unstemmed | Stereotyped behavioral maturation and rhythmic quiescence in C. elegans embryos |
| title_short | Stereotyped behavioral maturation and rhythmic quiescence in C. elegans embryos |
| title_sort | stereotyped behavioral maturation and rhythmic quiescence in c elegans embryos |
| topic | embryo behavior neuropeptides |
| url | https://elifesciences.org/articles/76836 |
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