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Published August 21, 2021 | Submitted
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Distinct neural circuits establish the same chemosensory behavior in C. elegans

Abstract

Animals frequently exhibit the same behavior under different environmental or physiological conditions. To what extent these behaviors are generated by similar vs. distinct mechanisms is unclear. Moreover, the circumstances under which divergent neural mechanisms establish the same behavior, and the molecular signals that regulate the same behavior across conditions, are poorly understood. We show that in C. elegans, distinct neural mechanisms mediate the same chemosensory behavior at two different life stages. Both dauer larvae and starved adults are attracted to carbon dioxide (CO₂), but CO₂ attraction is mediated by distinct sets of interneurons at the two life stages. Some interneurons mediate CO₂ response only in dauers, some show CO2-evoked activity in adults and dauers but contribute to CO₂ response only in adults, and some show CO₂-evoked activity that opposes CO₂ attraction in adults but promotes CO₂ attraction in dauers. We also identify a novel role for insulin signaling in establishing life-stage-specific CO₂ responses by modulating interneuron activity. Further, we show that a combinatorial code of both shared and life-stage-specific molecular signals regulate CO₂ attraction. Our results identify a mechanism by which the same chemosensory behavior can be generated by distinct neural circuits, revealing an unexpected complexity to chemosensory processing.

Additional Information

The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license. This version posted August 17, 2021. We thank the Caenorhabditis Genetics Centre, the C. elegans Knockout Consortium, Oliver Hobert, Cori Bargmann, Gary Ruvkun, Shai Shaham, Ikue Mori, Yuichi Iino, and Mario de Bono for strains. We thank Astra Bryant, Michelle Castelletto, and Ricardo Frausto for insightful comments on the manuscript. This work was funded by NIH F32 AI147617 (N.B.), NIH MARC T34 GM008563 (E.R.P.), NIH UF1 NS111697 (P.W.S.), and NIH R01 DC017959 and an HHMI Faculty Scholar Award (E.A.H.). Author Contributions: N.B., P.-Y.S., P.W.S., and E.A.H. conceived the study. N.B. and E.R.P. performed experiments. N.B. and E.R.P. analyzed the data. N.B., E.R.P., and E.A.H. wrote the manuscript. All authors read and approved the final manuscript. The authors declare no competing interests.

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Created:
August 20, 2023
Modified:
December 13, 2023