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

ABSTRACT: 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.SIGNIFICANCE STATEMENT Much is known about molecular mechanisms that facilitate sleep control. However, it is unclear how these pathways modulate neural circuit-level sensory processing or how misregulation of neural activity contributes to sleep disorders. The nematode Caenorhabditis elegans provides the ability to study neural circuitry with single-neuron resolution, and recent studies examined sleep states between developmental stages and when stressed. Here, we examine an additional form of spontaneous sleep in adult C. elegans at the behavioral and neural activity levels. Using a closed-loop system, we show that delayed behavioral responses to aversive chemical stimulation during sleep arise from sleep-dependent sensorimotor modulation localized presynaptic to the premotor circuit, rather than early sensory circuits.

SUBMITTER: Lawler DE

PROVIDER: S-EPMC7939084 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundAlthough behavioral unpredictability is widely described within-individual variability in behavior, its adaptive significance is little understood. Using a dynamic state variable model, this study investigated the conditions under which behavioral unpredictability (a component of within-individual variability) in foraging behavior is advantageous. The model considers a situation in which a forager forages for a fixed period, represented by discrete time steps. The outcome of foraging may change the level of a state (e.g., size and fat storage) of the forager at each time step, and variability in the foraging outcome is assumed to be positively correlated with behavioral unpredictability. The probability of death at each time step is influenced by the state at the same time step. Reproduction occurs after all the foraging steps and is influenced by the state level of a forager at the time of reproduction. According to the expected utility hypothesis, the relationship (e.g., curvature) between the state and fitness will determine the role of behavioral unpredictability. In the model, the relationship was obtained by using the backward iteration method for each foraging time step.ResultsState-dependent mortality adds curvature to the relationship between the state and fitness, which makes the effect of behavioral unpredictability on fitness either positive or negative. This conclusion holds for any state-dependent mortality (i.e., as long as mortality is not independent of the state factor). Given that state-dependent mortality is commonly described, conditions that benefit behavioral unpredictability are likely also common.ConclusionsWhen mortality depends on a state that is influenced by behavior, conditions that favor behavioral unpredictability may become common. How behavioral unpredictability influences the variability of behavioral outcomes is as important as how it influences the expectation of behavioral outcomes when studying the adaptive significance of behavioral unpredictability.

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

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