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

Cell. 2019 Jan 10;176(1-2):85-97.e14. doi: 10.1016/j.cell.2018.11.023. Epub 2018 Dec 20.

Abstract

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.

Keywords: ASIC; C. elegans; behavioral states; feeding; foraging; gut-brain signaling; hunger; ion channels; neural circuits; serotonin.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Acid Sensing Ion Channels / metabolism*
  • Acid Sensing Ion Channels / physiology
  • Animals
  • Caenorhabditis elegans / metabolism
  • Caenorhabditis elegans / physiology
  • Caenorhabditis elegans Proteins / metabolism
  • Enteric Nervous System / metabolism*
  • Enteric Nervous System / physiology
  • Feeding Behavior / physiology*
  • Food
  • Ion Channels / metabolism
  • Ion Channels / physiology
  • Locomotion
  • Neurons / metabolism
  • Sensory Receptor Cells / metabolism
  • Serotonergic Neurons / metabolism
  • Serotonergic Neurons / physiology
  • Serotonin
  • Signal Transduction

Substances

  • Acid Sensing Ion Channels
  • Caenorhabditis elegans Proteins
  • Ion Channels
  • Serotonin