Distinct neurogenetic mechanisms establish the same chemosensory valence state at different life stages in Caenorhabditis elegans

Creators: Banerjee, Navonil; Rojas Palato, Elisa J.; Shih, Pei-Yin; Sternberg, Paul W.¹; Hallem, Elissa A.

1. California Institute of Technology

Abstract

An animal's preference for many chemosensory cues remains constant despite dramatic changes in the animal's internal state. The mechanisms that maintain chemosensory preference across different physiological contexts remain poorly understood. We previously showed that distinct patterns of neural activity and motor output are evoked by carbon dioxide (CO₂) in starved adults vs dauers of Caenorhabditis elegans, despite the two life stages displaying the same preference (attraction) for CO₂. However, how the distinct CO₂-evoked neural dynamics and motor patterns contribute to CO₂ attraction at the two life stages remained unclear. Here, using a CO₂ chemotaxis assay, we show that different interneurons are employed to drive CO₂ attraction at the two life stages. We also investigate the molecular mechanisms that mediate CO₂ attraction in dauers vs adults. We show that insulin signaling promotes CO₂ attraction in dauers but not starved adults and that different combinations of neurotransmitters and neuropeptides are used for CO₂ attraction at the two life stages. Our findings provide new insight into the distinct molecular and cellular mechanisms used by C. elegans at two different life stages to generate attractive behavioral responses to CO₂.

Copyright and License

© The Author(s) 2023. Published by Oxford University Press on behalf of The Genetics Society of America. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

Acknowledgement

We thank Shai Shaham, Oliver Hobert, Cori Bargmann, Ikue Mori, and Gary Ruvkun for providing strains. Some strains were provided by the Caenorhabditis Genetics Center (CGC), which is funded by the National Institutes of Health Office of Research Infrastructure Programs (P40 OD010440).

Funding

This work was funded by National Institutes of Health F32 AI147617 (N.B.), National Institutes of Health MARC T34 GM008563 (E.J.R.P.), National Institutes of Health UF1 NS111697 (P.W.S.), and National Institutes of Health R01 DC017959 and a Howard Hughes Medical Institute Faculty Scholar Award (E.A.H.).

Contributions

N.B., P.-Y.S., P.W.S., and E.A.H. conceived the study. N.B. and E.J.R.P. performed experiments. N.B. and E.J.R.P. analyzed the data. N.B. and E.A.H. wrote the manuscript. All authors read and approved the final manuscript.

Data Availability

trains and plasmids are available upon request. All raw data and statistical analysis from this study are included in Supplementary File S1.

Supplemental material available at G3 online.

Conflict of Interest

The authors declare no conflict of interest.

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