Postsynaptic ERG potassium channels limit muscle excitability to allow distinct egg-laying behavior states in Caenorhabditis elegans

J Neurosci. 2013 Jan 9;33(2):761-75. doi: 10.1523/JNEUROSCI.3896-12.2013.

Abstract

Caenorhabditis elegans regulates egg laying by alternating between an inactive phase and a serotonin-triggered active phase. We found that the conserved ERG [ether-a-go-go (EAG) related gene] potassium channel UNC-103 enables this two-state behavior by limiting excitability of the egg-laying muscles. Using both high-speed video recording and calcium imaging of egg-laying muscles in behaving animals, we found that the muscles appear to be excited at a particular phase of each locomotor body bend. During the inactive phase, this rhythmic excitation infrequently evokes calcium transients or contraction of the egg-laying muscles. During the serotonin-triggered active phase, however, these muscles are more excitable and each body bend is accompanied by a calcium transient that drives twitching or full contraction of the egg-laying muscles. We found that ERG-null mutants lay eggs too frequently, and that ERG function is necessary and sufficient in the egg-laying muscles to limit egg laying. ERG K(+) channels localize to postsynaptic sites in the egg-laying muscle, and mutants lacking ERG have more frequent calcium transients and contractions of the egg-laying muscles even during the inactive phase. Thus ERG channels set postsynaptic excitability at a threshold so that further adjustments of excitability by serotonin generate two distinct behavioral states.

Publication types

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

MeSH terms

  • 3' Untranslated Regions / genetics
  • Animals
  • Behavior, Animal / physiology*
  • Caenorhabditis elegans / physiology*
  • Calcium Signaling / physiology
  • DNA / biosynthesis
  • DNA / genetics
  • Ether-A-Go-Go Potassium Channels / physiology*
  • Female
  • Microscopy, Confocal
  • Muscle Contraction / physiology
  • Muscles / innervation*
  • Muscles / physiology*
  • Oviposition / physiology*
  • PDZ Domains / genetics
  • Polymerase Chain Reaction
  • Serotonin / physiology
  • Synapses / physiology*
  • Synapses / ultrastructure
  • Transgenes / genetics

Substances

  • 3' Untranslated Regions
  • Ether-A-Go-Go Potassium Channels
  • Serotonin
  • DNA