Functional Dissection of the Sensory Rays in Caenorhabditis elegans Male Mating Behavior

The nematode Caenorhabditis elegans, with its sequenced genome, compact nervous system and stereotyped behaviors is an ideal model organism in which to study the integration of sensory input with motor output. Male mating behavior is among the most complex of these behaviors and males utilize a number of sensory organs in its execution. Among these are the rays, which are nine pairs of sensory organs that are arranged laterally along the male tail. Each ray is composed of two ultra-structurally distinct neuron types, an A type and a B type, surrounded by a glia-like structural cell. Though compositionally identical, each pair of rays maintains a unique, genetically-hardwired identity based on wiring, morphology, and neurotransmitter fate. Three techniques were used to investigate the role of the rays in male mating behavior. First, cauterization of the tips of the rays removed their sensory endings, leading to ray neuron death. Second, a heterologous light-activated cation channel was utilized to activate specific ray neuron types. Finally, ray neuron types were genetically targeted to undergo apoptosis by expression of heterologous caspases. The results show that the rays play important roles in multiple steps of male mating behavior, including contact response, scanning, and turning. The rays as a whole mediate posture change and backing during contact response. The ability to respond to hermaphrodite contact is shared among the rays, as is initiation of backward locomotion, though all rays are required for efficient, prolonged backward scanning. Both A and B neuron types appear capable of initiating contact response. Direct activation of B neurons through ChR2 causes a contact response-like ventral tail flexure, and elimination of both A and B neurons reduces contact response. A neurons additionally have a unique role in turning.