Pharyngeal pumping in Caenorhabditis elegans depends on tonic and phasic signaling from the nervous system

Sci Rep. 2016 Mar 15;6:22940. doi: 10.1038/srep22940.

Abstract

Rhythmic movements are ubiquitous in animal locomotion, feeding, and circulatory systems. In some systems, the muscle itself generates rhythmic contractions. In others, rhythms are generated by the nervous system or by interactions between the nervous system and muscles. In the nematode Caenorhabditis elegans, feeding occurs via rhythmic contractions (pumping) of the pharynx, a neuromuscular feeding organ. Here, we use pharmacology, optogenetics, genetics, and electrophysiology to investigate the roles of the nervous system and muscle in generating pharyngeal pumping. Hyperpolarization of the nervous system using a histamine-gated chloride channel abolishes pumping, and optogenetic stimulation of pharyngeal muscle in these animals causes abnormal contractions, demonstrating that normal pumping requires nervous system function. In mutants that pump slowly due to defective nervous system function, tonic muscle stimulation causes rapid pumping, suggesting tonic neurotransmitter release may regulate pumping. However, tonic cholinergic motor neuron stimulation, but not tonic muscle stimulation, triggers pumps that electrophysiologically resemble typical rapid pumps. This suggests that pharyngeal cholinergic motor neurons are normally rhythmically, and not tonically active. These results demonstrate that the pharynx generates a myogenic rhythm in the presence of tonically released acetylcholine, and suggest that the pharyngeal nervous system entrains contraction rate and timing through phasic neurotransmitter release.

Publication types

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

MeSH terms

  • Animals
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / physiology*
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / physiology
  • Chloride Channels / genetics
  • Chloride Channels / physiology
  • Cholinergic Neurons / metabolism
  • Cholinergic Neurons / physiology
  • Electrophysiological Phenomena / drug effects
  • Electrophysiological Phenomena / genetics
  • Feeding Behavior / drug effects
  • Feeding Behavior / physiology
  • Histamine / metabolism
  • Motor Neurons / metabolism
  • Motor Neurons / physiology*
  • Muscle Contraction / genetics
  • Muscle Contraction / physiology*
  • Mutation
  • Nervous System Physiological Phenomena / drug effects
  • Nervous System Physiological Phenomena / genetics
  • Optogenetics / methods
  • Pharyngeal Muscles / metabolism
  • Pharyngeal Muscles / physiology*
  • Pharynx / innervation
  • Pharynx / metabolism
  • Pharynx / physiology*
  • Serotonin / pharmacology
  • Serotonin Receptor Agonists / pharmacology
  • Signal Transduction / genetics
  • Signal Transduction / physiology*

Substances

  • Caenorhabditis elegans Proteins
  • Chloride Channels
  • Serotonin Receptor Agonists
  • Serotonin
  • Histamine