Abstract
Pheromone responses are highly context dependent. For example, the C. elegans pheromone ascaroside C9 (ascr#3) is repulsive to wild-type hermaphrodites, attractive to wild-type males, and usually neutral to "social" hermaphrodites with reduced activity of the npr-1 neuropeptide receptor gene. We show here that these distinct behavioral responses arise from overlapping push-pull circuits driven by two classes of pheromone-sensing neurons. The ADL sensory neurons detect C9 and, in wild-type hermaphrodites, drive C9 repulsion through their chemical synapses. In npr-1 mutant hermaphrodites, C9 repulsion is reduced by the recruitment of a gap junction circuit that antagonizes ADL chemical synapses. In males, ADL sensory responses are diminished; in addition, a second pheromone-sensing neuron, ASK, antagonizes C9 repulsion. The additive effects of these antagonistic circuit elements generate attractive, repulsive, or neutral pheromone responses. Neuronal modulation by circuit state and sex, and flexibility in synaptic output pathways, may permit small circuits to maximize their adaptive behavioral outputs.
| Original language | English |
|---|---|
| Pages (from-to) | 585-592 |
| Number of pages | 8 |
| Journal | Neuron |
| Volume | 75 |
| Issue number | 4 |
| DOIs | |
| State | Published - 23 Aug 2012 |
Bibliographical note
Funding Information:We are grateful to Eugene Kim and Andrew Gordus for assistance with ADL imaging experiments and analysis, the Caenorhabditis Genetics Center for strains, and Eve Marder for discussion. This work was supported by the NSF (IOS 0542372, P.S.; DMR-0820492, D.K. [MRSEC program]), the HFSP (RGY0042- P.S.), the NIH (core grant P30 NS45713 to the Brandeis Biology Department; F31 DC011467, D.M.Z.; R00 GM87533, R.A.B.), the DGIST MIREBrain and Convergence Science Center (12-BD-0403) and Basic Science Research Program (2012009385) of the Ministry of Education, Science and Technology, Korea (K.K.), the Natural Sciences and Engineering Research Council of Canada (PGS-D3), and the Brandeis National Committee (S.J.N.), a gift from the Jensam Foundation (C.I.B.), and the Howard Hughes Medical Institute (C.I.B.). C.I.B. is an Investigator of the Howard Hughes Medical Institute. Author contributions: H.J., K.K., S.J.N., and D.M.Z. performed the experiments; E.M., D.K. and R.B. provided reagents; H.J., K.K., C.I.B., and P.S. analyzed and interpreted data; C.I.B. and P.S. wrote the manuscript.