The contactin rig-6 transiently promotes GABA neuron remodeling with a sustained impact on male mating behavior in C. elegans.

Changes in neuronal and synaptic wiring contribute to neurological variations, including autism, schizophrenia, and major depressive disorder. Many developmental axon guidance cues, postsynaptic receptors, and other downstream molecular mechanisms govern axon and neurite extension required for circuit formation. Plasticity after development can include remodeling of neuron morphology and synapses to modify circuits and change behavior, but the signals and molecular mechanisms that regulate neurite remodeling after development are not well defined. We previously found that the synaptic adhesion molecules neurexin (nrx-1) and neuroligin (nlg-1) are required for adulthood remodeling of the GABAergic DVB neuron in male C. elegans. Here, we identify a role for the conserved contactin (CNTN1-6) gene, rig-6, in DVB neuron remodeling. We find that rig-6 is expressed in the male DVB neuron during development, with decreasing expression in adulthood. rig-6 mutants have reduced DVB neurite length and reduced time to spicule protraction only at day 1 of adulthood, which can be rescued by expression of the RIG-6d isoform in the DVB neuron. Loss of rig-6 reduces male mating efficiency at days 1 and 3, due to reduced ability to coordinate spicule protraction, required for sperm transfer. This demonstrates a dramatic and sustained impact of rig-6 and early DVB remodeling on adult male mating. This work provides insight into the temporal roles of genes and molecular mechanisms that function in GABAergic neuronal and behavioral plasticity, confirming careful orchestration of mechanisms that permit and promote neurite outgrowth after development.