Distinct Mechanisms Underlie Quiescence during Two Caenorhabditis elegans Sleep-Like States.
Electrophysiological recordings have enabled identification of physiologically distinct yet behaviorally similar states of mammalian sleep. In contrast, sleep in nonmammals has generally been identified behaviorally and therefore regarded as a physiologically uniform state characterized by quiescence of feeding and locomotion, reduced responsiveness, and rapid reversibility. The nematode Caenorhabditis elegans displays sleep-like quiescent behavior under two conditions: developmentally timed quiescence (DTQ) occurs during larval transitions, and stress-induced quiescence (SIQ) occurs in response to exposure to cellular stressors. Behaviorally, DTQ and SIQ appear identical. Here, we use optogenetic manipulations of neuronal and muscular activity, pharmacology, and genetic perturbations to uncover circuit and molecular mechanisms of DTQ and SIQ. We find that locomotion quiescence induced by DTQ- and SIQ-associated neuropeptides occurs via their action on the nervous system, although their neuronal target(s) and/or molecular mechanisms likely differ. Feeding quiescence during DTQ results from a loss of pharyngeal muscle excitability, whereas feeding quiescence during SIQ results from a loss of excitability in the nervous system. Together these results indicate that, as in mammals, quiescence is subserved by different mechanisms during distinct sleep-like states in C. elegans.
Department of Neurology and Department of Neuroscience, Perelman School of Medicine, University of Pennsylvania, Department of Bioengineering, School of Engineering and Applied Science, University of Pennsylvania, Philadelphia, Pennsylvania 19104, and.
Nicholas F
http://orcid.org/0000-0001-7317-2266
NF
Trojanowski
Department of Neurology and.
Matthew D
http://orcid.org/0000-0002-2085-8974
MD
Nelson
Howard Hughes Medical Institute, Lulu and Anthony Wang Laboratory of Neural Circuits and Behavior, The Rockefeller University, New York, New York 10065.
Steven W
SW
Flavell
Department of Neuroscience, Perelman School of Medicine, University of Pennsylvania, Department of Bioengineering, School of Engineering and Applied Science, University of Pennsylvania, Philadelphia, Pennsylvania 19104, and fangyen@seas.upenn.edu raizen@mail.med.upenn.edu.
Christopher
C
Fang-Yen
Department of Neurology and fangyen@seas.upenn.edu raizen@mail.med.upenn.edu.
David M
DM
Raizen
D000818:Animals; D017173:Caenorhabditis elegans / Q000502:physiology*; D029742:Caenorhabditis elegans Proteins / Q000235:genetics / Q000502:physiology; D005247:Feeding Behavior / Q000502:physiology; D007814:Larva / Q000254:growth & development / Q000502:physiology; D008124:Locomotion / Q000502:physiology; D009132:Muscles / Q000502:physiology; D009415:Nerve Net / Q000502:physiology; D009434:Neural Pathways / Q000254:growth & development / Q000502:physiology; D009474:Neurons / Q000502:physiology; D009479:Neuropeptides / Q000502:physiology; D062308:Optogenetics; D010609:Pharyngeal Muscles / Q000294:innervation / Q000502:physiology; D012890:Sleep / Q000502:physiology*; D013312:Stress, Physiological; D064348:Torpor / Q000502:physiology*
D029742:Caenorhabditis elegans Proteins; D009479:Neuropeptides
C. elegans; invertebrate; neural circuit; optogenetics; sleep