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Comments on Jang, Heeun et al. (2011) International Worm Meeting "Internal state and sex regulate an ambivalent circuit for pheromone responses." (0)
Overview
Jang, Heeun, Kim, Kyuhyung, Butcher, Rebecca, Sengupta, Piali, & Bargmann, Cori (2011). Internal state and sex regulate an ambivalent circuit for pheromone responses presented in International Worm Meeting. Unpublished information; cite only with author permission.
Animals respond flexibly to environmental cues based on internal and external context. Cocktails of several ascarosides, the components of C.elegans pheromones, are repulsive to wild-type hermaphrodites from the solitary strain N2 but are less repulsive or even mildly attractive to social hermaphrodites with reduced activity of the npr-1 neuropeptide receptor gene. We have examined the circuit mechanisms underlying these alternative behavioral responses to pheromones using behavioral assays and in vivo imaging with genetically encoded Ca2+ sensors. We found that the C9 ascaroside (also called ascr#3) evokes strong avoidance behaviors in N2 hermaphrodites. This avoidance is mediated by the ADL chemosensory neurons, which directly sense C9. Interestingly, pheromone attraction in npr-1 mutant hermaphrodites also requires ADL, which cooperates with the previously described ASK sensory neurons to detect blends of ascarosides C9 and C3 (also called ascr#5) that are not individually attractive. ADL and ASK both belong to a hub-and-spoke circuit of neurons connected through gap junctions to the central hub neuron RMG, which is regulated by npr-1. Attraction to C9 and C3 requires RMG synaptic activity, but avoidance of C9 does not. Conversely, avoidance of C9 requires ADL synaptic activity, but attraction to C9 and C3 does not. Our results suggest that the balance between avoidance and attraction can be regulated by changing the relative strengths of ADL chemical synapses compared to the ADL/ASK-RMG gap junction circuit. A parallel mechanism generates sexual dimorphism in pheromone responses. Males exhibit reduced avoidance of high C9 concentrations, and their ADL sensory neurons are less responsive to C9 than those of hermaphrodites. The effects of sexual dimorphism are additive with the effects of npr-1, suggesting that these pathways function independently. Modulation of neuronal responses by neuropeptide signaling and sex may permit small neuronal circuits to maximize their adaptive responses and behavioral outputs.
Affiliations:
- University of Florida, Gainesville, FL
- equal contributions
- Brandeis University, Waltham, MA
- Rockefeller University, New York, NY