Reciprocal inhibition between sensory ASH and ASI neurons modulates nociception and avoidance in Caenorhabditis elegans

Nat Commun. 2015 Jan 13;6:5655. doi: 10.1038/ncomms6655.

Abstract

Sensory modulation is essential for animal sensations, behaviours and survival. Peripheral modulations of nociceptive sensations and aversive behaviours are poorly understood. Here we identify a biased cross-inhibitory neural circuit between ASH and ASI sensory neurons. This inhibition is essential to drive normal adaptive avoidance of a CuSO4 (Cu(2+)) challenge in Caenorhabditis elegans. In the circuit, ASHs respond to Cu(2+) robustly and suppress ASIs via electro-synaptically exciting octopaminergic RIC interneurons, which release octopamine (OA), and neuroendocrinally inhibit ASI by acting on the SER-3 receptor. In addition, ASIs sense Cu(2+) and permit a rapid onset of Cu(2+)-evoked responses in Cu(2+)-sensitive ADF neurons via neuropeptides possibly, to inhibit ASHs. ADFs function as interneurons to mediate ASI inhibition of ASHs by releasing serotonin (5-HT) that binds with the SER-5 receptor on ASHs. This elaborate modulation among sensory neurons via reciprocal inhibition fine-tunes the nociception and avoidance behaviour.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Avoidance Learning*
  • Behavior, Animal
  • Biomechanical Phenomena
  • Caenorhabditis elegans / physiology*
  • Caenorhabditis elegans Proteins / metabolism
  • Calcium / metabolism
  • Copper / chemistry
  • Copper Sulfate / chemistry
  • Genotype
  • Interneurons / physiology*
  • Microscopy, Confocal
  • Mutation
  • Neurons / physiology*
  • Neuropeptides / chemistry
  • Nociception / physiology*
  • Nociceptors / metabolism
  • Octopamine / chemistry
  • Sensory Receptor Cells / physiology
  • Serotonin / chemistry
  • Signal Transduction / physiology*

Substances

  • Caenorhabditis elegans Proteins
  • Neuropeptides
  • Octopamine
  • Serotonin
  • Copper
  • Copper Sulfate
  • Calcium