Dissection of neuronal gap junction circuits that regulate social behavior in Caenorhabditis elegans

Heeun Jang, Sagi Levy, Steven W. Flavell, Fanny Mende, Richard Latham, Manuel Zimmer, Cornelia I. Bargmann

Research output: Contribution to journalArticlepeer-review

Abstract

A hub-and-spoke circuit of neurons connected by gap junctions controls aggregation behavior and related behavioral responses to oxygen, pheromones, and food in Caenorhabditis elegans. The molecular composition of the gap junctions connecting RMG hub neurons with sensory spoke neurons is unknown. We show here that the innexin gene unc-9 is required in RMG hub neurons to drive aggregation and related behaviors, indicating that UNC-9-containing gap junctions mediate RMG signaling. To dissect the circuit in detail, we developed methods to inhibit unc-9-based gap junctions with dominant-negative unc-1 transgenes. unc-1(dn) alters a stomatin-like protein that regulates unc-9 electrical signaling; its disruptive effects can be rescued by a constitutively active UNC-9::GFP protein, demonstrating specificity. Expression of unc-1(dn) in RMG hub neurons, ADL or ASK pheromone-sensing neurons, or URX oxygen-sensing neurons disrupts specific elements of aggregation-related behaviors. In ADL, unc-1(dn) has effects opposite to those of tetanus toxin light chain, separating the roles of ADL electrical and chemical synapses. These results reveal roles of gap junctions in a complex behavior at cellular resolution and provide a tool for similar exploration of other gap junction circuits.

Original languageEnglish
Pages (from-to)E1263-E1272
JournalProceedings of the National Academy of Sciences of the United States of America
Volume114
Issue number7
DOIs
StatePublished - 14 Feb 2017
Externally publishedYes

Keywords

  • Electrical synapses
  • Innexin
  • Neural circuits
  • Sensory behavior
  • Stomatin

All Science Journal Classification (ASJC) codes

  • General

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