Polymodal Responses in C. elegans Phasmid Neurons Rely on Multiple Intracellular and Intercellular Signaling Pathways

Sci Rep. 2017 Feb 14:7:42295. doi: 10.1038/srep42295.

Abstract

Animals utilize specialized sensory neurons enabling the detection of a wide range of environmental stimuli from the presence of toxic chemicals to that of touch. However, how these neurons discriminate between different kinds of stimuli remains poorly understood. By combining in vivo calcium imaging and molecular genetic manipulation, here we investigate the response patterns and the underlying mechanisms of the C. elegans phasmid neurons PHA/PHB to a variety of sensory stimuli. Our observations demonstrate that PHA/PHB neurons are polymodal sensory neurons which sense harmful chemicals, hyperosmotic solutions and mechanical stimulation. A repulsive concentration of IAA induces calcium elevations in PHA/PHB and both OSM-9 and TAX-4 are essential for IAA-sensing in PHA/PHB. Nevertheless, the PHA/PHB neurons are inhibited by copper and post-synaptically activated by copper removal. Neuropeptide is likely involved in copper removal-induced calcium elevations in PHA/PHB. Furthermore, mechanical stimulation activates PHA/PHB in an OSM-9-dependent manner. Our work demonstrates how PHA/PHB neurons respond to multiple environmental stimuli and lays a foundation for the further understanding of the mechanisms of polymodal signaling, such as nociception, in more complex organisms.

Publication types

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

MeSH terms

  • Animals
  • Caenorhabditis elegans / drug effects
  • Caenorhabditis elegans / metabolism*
  • Caenorhabditis elegans Proteins / metabolism
  • Calcium / metabolism
  • Copper / pharmacology
  • Extracellular Space / metabolism*
  • Intracellular Space / metabolism*
  • Ion Channels / metabolism
  • Nerve Tissue Proteins / metabolism
  • Neurons / drug effects
  • Neurons / metabolism*
  • Odorants
  • Physical Stimulation
  • Sensory Receptor Cells / drug effects
  • Sensory Receptor Cells / metabolism
  • Signal Transduction*
  • TRPV Cation Channels / metabolism
  • Touch

Substances

  • Caenorhabditis elegans Proteins
  • Ion Channels
  • Nerve Tissue Proteins
  • OSM-9 protein, C elegans
  • TRPV Cation Channels
  • tax-4 protein, C elegans
  • Copper
  • Calcium