4.7 Article

Sleep Analysis in Adult C. elegans Reveals State-Dependent Alteration of Neural and Behavioral Responses

Journal

JOURNAL OF NEUROSCIENCE
Volume 41, Issue 9, Pages 1892-1907

Publisher

SOC NEUROSCIENCE
DOI: 10.1523/JNEUROSCI.1701-20.2020

Keywords

arousal threshold; calcium imaging; closed-loop stimulation; microfluidics; sensory processing; sleep dynamics

Categories

Funding

  1. National Institutes of Health (NIH) Office of Research Infrastructure Programs [P40 OD010440]
  2. National Science Foundation (NSF) Chemical, Bioengineering, Environmental and Transport Systems Grant [1605679]
  3. Division of Emerging Frontiers Grant [1724026]
  4. NIH [R01DC016058]
  5. Career Award at the Scientific Interface (CASI) from the Burroughs Wellcome Fund
  6. NSF Integrated Graduate Research Traineeship Award [DGE 1144804]
  7. EMBO Long-term Fellowship [ALTF 403-2016]
  8. Whitman Fellowship from the Marine Biological Laboratories, NIH [R01NS076558, DP1NS111778]
  9. Howard Hughes Medical Institute Scholar Award
  10. Ruth L. Kirschstein National Research Service Award (NIH) [F32MH105063]
  11. Div Of Chem, Bioeng, Env, & Transp Sys
  12. Directorate For Engineering [1605679] Funding Source: National Science Foundation

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Research on adult C. elegans showed sleep-like states and neural modulation mainly occurring within interneurons presynaptic to premotor interneurons, with sleep prolonging responses in chemosensory neurons. This suggests that sleep modulates responsiveness specifically across sensory systems rather than broadly damping global circuit activity.
Sleep, a state of quiescence associated with growth and restorative processes, is conserved across species. Invertebrates including the nematode Caenorhabditis elegans exhibit sleep-like states during development, satiety, and stress. Here, we describe behavior and neural activity during sleep and awake states in adult C. elegans hermaphrodites using new microfluidic methods. We observed effects of fluid flow, oxygen, feeding, odors, and genetic perturbations on long-term sleep behavior over 12 h. We developed a closed-loop sleep detection system to automatically deliver chemical stimuli to assess sleep-dependent changes to evoked neural responses in individual animals. Sleep increased the arousal threshold to aversive stimulation, yet the associated sensory neuron and first-layer interneuron responses were unchanged. This localizes adult sleep-dependent neuromodulation within interneurons presynaptic to the premotor interneurons, rather than afferent sensory circuits. However, sleep prolonged responses in appetitive chemosensory neurons, suggesting that sleep modulates responsiveness specifically across sensory systems rather than broadly damping global circuit activity.

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