Dissection of neuronal gap junction circuits that regulate social behavior in <i>Caenorhabditis elegans</i>.

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 <i>Caenorhabditis elegans</i> The molecular composition of the gap junctions connecting RMG hub neurons with sensory spoke neurons is unknown. We show here that the innexin gene <i>unc-9</i> 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 <i>unc-9</i>-based gap junctions with dominant-negative <i>unc-1</i> transgenes. <i>unc-1(dn)</i> alters a stomatin-like protein that regulates <i>unc-9</i> electrical signaling; its disruptive effects can be rescued by a constitutively active UNC-9::GFP protein, demonstrating specificity. Expression of <i>unc-1(dn)</i> in RMG hub neurons, ADL or ASK pheromone-sensing neurons, or URX oxygen-sensing neurons disrupts specific elements of aggregation-related behaviors. In ADL, <i>unc-1(dn)</i> 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.