Department of Molecular Biology, Massachusetts General Hospital, Boston, United States; Department of Neurobiology, Harvard Medical School, Boston, United States
Andrew Lauziere
National Institute of Biomedical Imaging and Bioengineering, National Institutes of Health, Bethesda, United States; Department of Mathematics, University of Maryland, College Park, United States
Stephen Xu
National Institute of Biomedical Imaging and Bioengineering, National Institutes of Health, Bethesda, United States
National Institute of Biomedical Imaging and Bioengineering, National Institutes of Health, Bethesda, United States; Fellows Program, Marine Biological Laboratory, Woods Hole, United States
Ryan Patrick Christensen
National Institute of Biomedical Imaging and Bioengineering, National Institutes of Health, Bethesda, United States
Department of Molecular Biology, Massachusetts General Hospital, Boston, United States; Department of Neurobiology, Harvard Medical School, Boston, United States
Department of Molecular Biology, Massachusetts General Hospital, Boston, United States; Department of Neurobiology, Harvard Medical School, Boston, United States
Hari Shroff
National 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 States
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.
