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ASICs Mediate Food Responses in an Enteric Serotonergic Neuron that Controls Foraging Behaviors

Rhoades, Jeffrey L., Nelson, Jessica C., Nwabudike, Ijeoma, Yu, Stephanie K., McLachlan, Ian G., Madan, Gurrein K., Abebe, Eden, Powers, Joshua R., Colón-Ramos, Daniel A., Flavell, Steven W.
Cell 2019 v.176 no.1-2 pp. 85-97.e14
animals, foraging, ingestion, ion channels, locomotion, point mutation, sensory neurons
Animals must respond to the ingestion of food by generating adaptive behaviors, but the role of gut-brain signaling in behavioral regulation is poorly understood. Here, we identify conserved ion channels in an enteric serotonergic neuron that mediate its responses to food ingestion and decipher how these responses drive changes in foraging behavior. We show that the C. elegans serotonergic neuron NSM acts as an enteric sensory neuron that acutely detects food ingestion. We identify the novel and conserved acid-sensing ion channels (ASICs) DEL-7 and DEL-3 as NSM-enriched channels required for feeding-dependent NSM activity, which in turn drives slow locomotion while animals feed. Point mutations that alter the DEL-7 channel change NSM dynamics and associated behavioral dynamics of the organism. This study provides causal links between food ingestion, molecular and physiological properties of an enteric serotonergic neuron, and adaptive feeding behaviors, yielding a new view of how enteric neurons control behavior.