Monoaminergic orchestration of motor programs in a complex C. elegans behavior

PLoS Biol. 2013;11(4):e1001529. doi: 10.1371/journal.pbio.1001529. Epub 2013 Apr 2.

Abstract

Monoamines provide chemical codes of behavioral states. However, the neural mechanisms of monoaminergic orchestration of behavior are poorly understood. Touch elicits an escape response in Caenorhabditis elegans where the animal moves backward and turns to change its direction of locomotion. We show that the tyramine receptor SER-2 acts through a Gαo pathway to inhibit neurotransmitter release from GABAergic motor neurons that synapse onto ventral body wall muscles. Extrasynaptic activation of SER-2 facilitates ventral body wall muscle contraction, contributing to the tight ventral turn that allows the animal to navigate away from a threatening stimulus. Tyramine temporally coordinates the different phases of the escape response through the synaptic activation of the fast-acting ionotropic receptor, LGC-55, and extrasynaptic activation of the slow-acting metabotropic receptor, SER-2. Our studies show, at the level of single cells, how a sensory input recruits the action of a monoamine to change neural circuit properties and orchestrate a compound motor sequence.

Publication types

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

MeSH terms

  • Aldicarb / pharmacology
  • Animals
  • Caenorhabditis elegans / cytology
  • Caenorhabditis elegans / physiology*
  • Caenorhabditis elegans Proteins / metabolism
  • Cholinesterase Inhibitors / pharmacology
  • Escape Reaction / physiology*
  • GABAergic Neurons / metabolism
  • GTP-Binding Protein alpha Subunits, Gi-Go / genetics
  • GTP-Binding Protein alpha Subunits, Gi-Go / metabolism
  • Motor Neurons / metabolism
  • Muscle Contraction
  • Neuromuscular Junction / drug effects
  • Neuromuscular Junction / physiology
  • Neurotransmitter Agents / pharmacology
  • Neurotransmitter Agents / physiology*
  • Receptors, Biogenic Amine / genetics
  • Receptors, Biogenic Amine / metabolism
  • Sequence Deletion
  • Synaptic Transmission
  • Tyramine / pharmacology
  • Tyramine / physiology*

Substances

  • Caenorhabditis elegans Proteins
  • Cholinesterase Inhibitors
  • LGC-55 protein, c elegans
  • Neurotransmitter Agents
  • Receptors, Biogenic Amine
  • SER-2 protein, C elegans
  • Aldicarb
  • GTP-Binding Protein alpha Subunits, Gi-Go
  • Tyramine