The C. elegans Male Exercises Directional Control during Mating through Cholinergic Regulation of Sex-Shared Command Interneurons

Abstract

BackgroundMating behaviors in simple invertebrate model organisms represent tractable paradigms for understanding the neural bases of sex-specific behaviors, decision-making and sensorimotor integration. However, there are few examples where such neural circuits have been defined at high resolution or interrogated.Methodology/Principal FindingsHere we exploit the simplicity of the nematode Caenorhabditis elegans to define the neural circuits underlying the male’s decision to initiate mating in response to contact with a mate. Mate contact is sensed by male-specific sensilla of the tail, the rays, which subsequently induce and guide a contact-based search of the hermaphrodite’s surface for the vulva (the vulva search). Atypically, search locomotion has a backward directional bias so its implementation requires overcoming an intrinsic bias for forward movement, set by activity of the sex-shared locomotory system. Using optogenetics, cell-specific ablation- and mutant behavioral analyses, we show that the male makes this shift by manipulating the activity of command cells within this sex-shared locomotory system. The rays control the command interneurons through the male-specific, decision-making interneuron PVY and its auxiliary cell PVX. Unlike many sex-shared pathways, PVY/PVX regulate the command cells via cholinergic, rather than glutamatergic transmission, a feature that likely contributes to response specificity and coordinates directional movement with other cholinergic-dependent motor behaviors of the mating sequence. PVY/PVX preferentially activate the backward, and not forward, command cells because of a bias in synaptic inputs and the distribution of key cholinergic receptors (encoded by the genes acr-18, acr-16 and unc-29) in favor of the backward command cells.Conclusion/SignificanceOur interrogation of male neural circuits reveals that a sex-specific response to the opposite sex is conferred by a male-specific pathway that renders subordinate, sex-shared motor programs responsive to mate cues. Circuit modifications of these types may make prominent contributions to natural variations in behavior that ultimately bring about speciation.

Encoding of Both Analog- and Digital-like Behavioral Outputs by One C. elegans Interneuron

“…Two major groups of nAChRs were identified in C. elegans : the levamisole-type nAChRs represented by UNC-29 and UNC-38, and the nicotine-type nAChRs such as ACR-16 (Francis et al, 2005; Richmond and Jorgensen, 1999; Touroutine et al, 2005). We decided to examine UNC-29 and ACR-16 since they both are expressed in RIB (Feng et al, 2006; Sherlekar et al, 2013). Loss of UNC-29 modestly but significantly compromised the ability of AIY (AIY::ChR2) to promote locomotion speed, consistent with a role for UNC-29 in regulating locomotion speed (Figure 5D–E).…”

C. elegans Ciliated Sensory Neurons Release Extracellular Vesicles that Function in Animal Communication

“…We noticed three instances of tail chasing behavior (in 27 recordings) in the wild-type ECV spot, in which the male tail curls to contact its own head and moves in a backward circle. Tail curling enables the male to contact and circle around the hermaphrodite body during mating [24]. Tail curling behavior may also culminate in male-self or male-male contact [25].…”

Ciliary ectosomes: transmissions from the cell's antenna

“…Both behaviors are relevant to the Caenorhabditis mating process in which the male worm responds to hermaphrodite contact by reversing his locomotive direction to scan the hermaphrodite's body surface with his tail. If the male reaches his partner's head or tail during this process, he executes a curling turn maneuver and continues scanning in a reverse direction until his tail contacts the vulva where mating is consummated by insertion of the copulatory spicules and ejaculation into the hermaphrodite uterus ( 52, 53 ). The tail-curling behavior induced by exposure to extracellular vesicles was dependent on their cargo content as evidenced by the fact that extracellular vesicles isolated from wildtype induced the tail-chasing behavior, while extracellular vesicles isolated from kinesin-3 mutants, which lack PKD2, did not ( 51 ).…”