Reliability of an interneuron response depends on an integrated sensory state

Elife. 2019 Nov 13:8:e50566. doi: 10.7554/eLife.50566.

Abstract

The central nervous system transforms sensory information into representations that are salient to the animal. Here we define the logic of this transformation in a Caenorhabditis elegans integrating interneuron. AIA interneurons receive input from multiple chemosensory neurons that detect attractive odors. We show that reliable AIA responses require the coincidence of two sensory inputs: activation of AWA olfactory neurons that are activated by attractive odors, and inhibition of one or more chemosensory neurons that are inhibited by attractive odors. AWA activates AIA through an electrical synapse, while the disinhibitory pathway acts through glutamatergic chemical synapses. AIA interneurons have bistable electrophysiological properties consistent with their calcium dynamics, suggesting that AIA activation is a stereotyped response to an integrated stimulus. Our results indicate that AIA interneurons combine sensory information using AND-gate logic, requiring coordinated activity from multiple chemosensory neurons. We propose that AIA encodes positive valence based on an integrated sensory state.

Keywords: C. elegans; calcium imaging; electrophysiology; neural circuits; neuroscience; olfaction; optogenetics; sensory integration.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Caenorhabditis elegans / physiology*
  • Calcium / metabolism
  • Diacetyl / metabolism
  • Gap Junctions / metabolism
  • Glutamates / metabolism
  • Interneurons / physiology*
  • Optogenetics
  • Pentanols / metabolism
  • Sensation / physiology*
  • Sensory Receptor Cells / physiology
  • Synapses / physiology

Substances

  • Glutamates
  • Pentanols
  • isopentyl alcohol
  • Diacetyl
  • Calcium

Grants and funding

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.