Activity of the C. elegans egg-laying behavior circuit is controlled by competing activation and feedback inhibition

Elife. 2016 Nov 16:5:e21126. doi: 10.7554/eLife.21126.

Abstract

Like many behaviors, Caenorhabditis elegans egg laying alternates between inactive and active states. To understand how the underlying neural circuit turns the behavior on and off, we optically recorded circuit activity in behaving animals while manipulating circuit function using mutations, optogenetics, and drugs. In the active state, the circuit shows rhythmic activity phased with the body bends of locomotion. The serotonergic HSN command neurons initiate the active state, but accumulation of unlaid eggs also promotes the active state independent of the HSNs. The cholinergic VC motor neurons slow locomotion during egg-laying muscle contraction and egg release. The uv1 neuroendocrine cells mechanically sense passage of eggs through the vulva and release tyramine to inhibit egg laying, in part via the LGC-55 tyramine-gated Cl- channel on the HSNs. Our results identify discrete signals that entrain or detach the circuit from the locomotion central pattern generator to produce active and inactive states.

Keywords: C. elegans; behavior; calcium; circuit; neuromodulator; neuroscience; serotonin; tyramine.

Publication types

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

MeSH terms

  • Animals
  • Caenorhabditis elegans / drug effects
  • Caenorhabditis elegans / genetics*
  • Caenorhabditis elegans / growth & development
  • Caenorhabditis elegans / metabolism
  • Caenorhabditis elegans Proteins / genetics*
  • Caenorhabditis elegans Proteins / metabolism
  • Chloride Channels / genetics*
  • Chloride Channels / metabolism
  • Choline / metabolism
  • Choline / pharmacology
  • Feedback, Physiological*
  • Female
  • Gene Expression Regulation
  • Locomotion
  • Motor Neurons / cytology
  • Motor Neurons / drug effects
  • Motor Neurons / metabolism
  • Muscle Contraction / drug effects
  • Muscle Contraction / genetics
  • Optogenetics
  • Oviposition / drug effects
  • Oviposition / genetics*
  • Periodicity
  • Receptors, Biogenic Amine / genetics*
  • Receptors, Biogenic Amine / metabolism
  • Serotonin / metabolism
  • Serotonin / pharmacology
  • Sexual Behavior, Animal / drug effects
  • Sexual Behavior, Animal / physiology*
  • Signal Transduction
  • Tyramine / metabolism
  • Tyramine / pharmacology

Substances

  • Caenorhabditis elegans Proteins
  • Chloride Channels
  • LGC-55 protein, c elegans
  • Receptors, Biogenic Amine
  • Serotonin
  • Choline
  • Tyramine