Sexually dimorphic architecture and function of a mechanosensory circuit in C. elegans

Abstract

How sensory perception is processed by the two sexes of an organism is still only partially understood. Despite some evidence for sexual dimorphism in auditory and olfactory perception, whether touch is sensed in a dimorphic manner has not been addressed. Here we find that the neuronal circuit for tail mechanosensation in C. elegans is wired differently in the two sexes and employs a different combination of sex-shared sensory neurons and interneurons in each sex. Reverse genetic screens uncovered cell- and sex-specific functions of the alpha-tubulin mec-12 and the sodium channel tmc-1 in sensory neurons, and of the glutamate receptors nmr-1 and glr-1 in interneurons, revealing the underlying molecular mechanisms that mediate tail mechanosensation. Moreover, we show that only in males, the sex-shared interneuron AVG is strongly activated by tail mechanical stimulation, and accordingly is crucial for their behavioral response. Importantly, sex reversal experiments demonstrate that the sexual identity of AVG determines both the behavioral output of the mechanosensory response and the molecular pathways controlling it. Our results present for the first time extensive sexual dimorphism in a mechanosensory circuit at both the cellular and molecular levels.

Integration of spatially opposing cues by a single interneuron guides decision making inC. elegans

“…Additionally, ASH neurons show an OFF response only at a high concentration, implying that it may mediate some concentration-dependent behaviors. Finally, we discovered that the PHA neuron, which innervates PHB and AVG, but not AVA (in hermaphrodites), displays concentration-dependent ON and OFF responses, which correspond to neuronal responses in AVG following tail exposure to touch and high-concentration osmotic shock 62,63 . This finding suggests an additional parallel pathway, mediated by PHA>AVG, that respond to osmotic shock applied to the tail, but its contribution to behavioral decisions remain unclear.…”

Modulation by NPYR underlies experience-dependent, sexually dimorphic learning

“…The two sexes of C. elegans display sexually dimorphic behaviors, such as mechanosensory responses to tail touch, dosage-dependent differences in nociceptive behaviors, and chemoattraction to odors and chemicals. Some of these differences have been mapped to corresponding network changes 8,23,24 .…”