The Neural and Molecular Mechanisms Regulating Male Locomotion during Caenorhabditis elegans Mating Behavior
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In key survival behaviors like predator-prey interactions and mating, animals have to integrate dynamic sensory inputs from a moving target and regulate their motor outputs on moment-to-moment basis. The molecular underpinnings of such goal-oriented behaviors are not well understood because of the genomic and neural system complexities of many animals. Here I take advantage of the anatomical simplicity of the nematode worm Caenorhabditis elegans and its amenability to optogenetics to interrogate the neural mechanisms underlying male mating behavior. Male mating is a goal oriented behavioral sequence and serves as a useful paradigm for exploring neural control of sex-specific behaviors, behavioral sequence execution and decision-making. When not engaged in mating the male, like the hermaphrodite, explores his environment with predominantly forward locomotion. However, when the male contacts a potential mate he immediately places his tail against her surface and searches for the vulva, moving backwards. Male-specific sensory rays of the tail are responsible for sensing mate contact, inducing tail apposition and backward movement. Using a combination of cell-specific laser ablation, optogentics and mutant analyses, I show that the male exploits the sex-shared locomotory system to control his mating movement. The rays exert their affect by acting through at least two downstream pathways. One pathway is defined by male-specific interneurons PVY and PVX which activate backward command interneurons AVA(L/R) and shift the directional bias to backward. This AVA activation is mediated by cholinergic receptor subunits ACR-18, ACR-16 and UNC-29, which is an atypical mode for command interneuron regulation. The second pathway is defined by male-specific interneurons EF1-3. EFs may promote backing by inhibiting sex-shared AVB(L/R) forward command interneurons. Upon vulva detection by the hook sensilla, locomotion ceases by the redundant action of hook neurons HOA and HOB. Surprisingly, PVY/PVX and EFs activity is required for holding the tail at the vulva. Taken together these data suggest that a distributed processing strategy underlies male’s accurate, rapid and robust movement control during mating. The male-specific nature of his behavior is due male-specific control of sex-shared circuitry. Conceivably, similar design and processing strategies may underlie the circuitry controlling analogous behaviors in more complex nervous systems.
Sherlekar, Amrita Laxman (2015). The Neural and Molecular Mechanisms Regulating Male Locomotion during Caenorhabditis elegans Mating Behavior. Doctoral dissertation, Texas A & M University. Available electronically from