C. elegans AWA Olfactory Neurons Fire Calcium-Mediated All-or-None Action Potentials

Cell. 2018 Sep 20;175(1):57-70.e17. doi: 10.1016/j.cell.2018.08.018. Epub 2018 Sep 13.

Abstract

Neurons in Caenorhabditis elegans and other nematodes have been thought to lack classical action potentials. Unexpectedly, we observe membrane potential spikes with defining characteristics of action potentials in C. elegans AWA olfactory neurons recorded under current-clamp conditions. Ion substitution experiments, mutant analysis, pharmacology, and modeling indicate that AWA fires calcium spikes, which are initiated by EGL-19 voltage-gated CaV1 calcium channels and terminated by SHK-1 Shaker-type potassium channels. AWA action potentials result in characteristic signals in calcium imaging experiments. These calcium signals are also observed when intact animals are exposed to odors, suggesting that natural odor stimuli induce AWA spiking. The stimuli that elicit action potentials match AWA's specialized function in climbing odor gradients. Our results provide evidence that C. elegans neurons can encode information through regenerative all-or-none action potentials, expand the computational repertoire of its nervous system, and inform future modeling of its neural coding and network dynamics.

Keywords: C. elegans; action potential; calcium channels; chemotaxis; neurophysiology; olfaction.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / physiology*
  • Animals
  • Caenorhabditis elegans / physiology
  • Caenorhabditis elegans Proteins / metabolism
  • Calcium / metabolism
  • Calcium Channels / physiology
  • Chemotaxis / physiology
  • Membrane Potentials / physiology
  • Odorants
  • Olfactory Nerve / physiology*
  • Olfactory Receptor Neurons / metabolism
  • Smell / physiology*

Substances

  • Caenorhabditis elegans Proteins
  • Calcium Channels
  • Calcium