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Feeding state sculpts a circuit for sensory valence in Caenorhabditis elegans

Rengarajan, Sophie and Yankura, Kristen A. and Guillermin, Manon L. and Fung, Wendy and Hallem, Elissa A. (2019) Feeding state sculpts a circuit for sensory valence in Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the United States of America, 116 (5). pp. 1776-1781. ISSN 0027-8424. http://resolver.caltech.edu/CaltechAUTHORS:20190123-103653883

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Abstract

Hunger affects the behavioral choices of all animals, and many chemosensory stimuli can be either attractive or repulsive depending on an animal’s hunger state. Although hunger-induced behavioral changes are well documented, the molecular and cellular mechanisms by which hunger modulates neural circuit function to generate changes in chemosensory valence are poorly understood. Here, we use the CO_2 response of the free-living nematode Caenorhabditis elegans to elucidate how hunger alters valence. We show that CO_2 response valence shifts from aversion to attraction during starvation, a change that is mediated by two pairs of interneurons in the CO_2 circuit, AIY and RIG. The transition from aversion to attraction is regulated by biogenic amine signaling. Dopamine promotes CO_2 repulsion in well-fed animals, whereas octopamine promotes CO_2 attraction in starved animals. Biogenic amines also regulate the temporal dynamics of the shift from aversion to attraction such that animals lacking octopamine show a delayed shift to attraction. Biogenic amine signaling regulates CO_2 response valence by modulating the CO_2-evoked activity of AIY and RIG. Our results illuminate a new role for biogenic amine signaling in regulating chemosensory valence as a function of hunger state.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1073/pnas.1807454116DOIArticle
https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.1807454116/-/DCSupplementalPublisherSupporting Information
Additional Information:© 2019 National Academy of Sciences. Published under the PNAS license. Edited by H. Robert Horvitz, Massachusetts Institute of Technology, Cambridge, MA, and approved December 12, 2018 (received for review May 1, 2018). PNAS published ahead of print January 16, 2019. We thank C. Bargmann (Rockefeller University, New York), M. de Bono (MRC Laboratory of Molecular Biology, Cambridge, United Kingdom), A. Maricq (University of Utah, Salt Lake City), I. Mori (Nagoya University, Nagoya, Japan), S. Mitani (Tokyo Women’s Medical University, Tokyo), S. Srinivasan (The Scripps Research Institute, La Jolla, CA), S. Suo (University of Tokyo, Tokyo), and the Caenorhabditis Genetics Center for C. elegans strains. We also thank Navonil Banerjee, Astra Bryant, Albert Kao, and Jesse Marshall for insightful comments on the manuscript. This work was supported by UCLA-Caltech Medical Scientist Training Program Grant T32GM008042, UCLA Neural Microcircuit Training Grant T32NS058280, and NIH NIGMS F30 Predoctoral Training Grant 1F30GM116810 (to S.R.); an Undergraduate Research Fellowship (Edith and Lew Wasserman Fund for Undergraduate Support) (to W.F.); NSF Graduate Research Fellowship DGE-1144087 and UCLA Cellular and Molecular Biology Training Grant GM007185 (to M.L.G.); and NSF Division of Integrative Organismal Systems Grant IOS-1456064, a McKnight Scholar Award, and an HHMI Faculty Scholar Award (to E.A.H.). Author contributions: S.R., K.A.Y., M.L.G., W.F., and E.A.H. designed research; S.R., K.A.Y., M.L.G., and W.F. performed research; S.R., K.A.Y., M.L.G., W.F., and E.A.H. analyzed data; and S.R. and E.A.H. wrote the paper. The authors declare no conflict of interest. This article is a PNAS Direct Submission. This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1807454116/-/DCSupplemental.
Funders:
Funding AgencyGrant Number
NIH Predoctoral FellowshipT32GM008042
NIH Predoctoral FellowshipT32NS058280
NIH Predoctoral Fellowship1F30GM116810
Edith and Lew Wasserman FundUNSPECIFIED
NSF Graduate Research FellowshipDGE-1144087
NIHGM007185
NSFIOS-1456064
McKnight FoundationUNSPECIFIED
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Subject Keywords:C. elegans; carbon dioxide; sensory valence; biogenic amines; starvation
Record Number:CaltechAUTHORS:20190123-103653883
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20190123-103653883
Official Citation:Feeding state sculpts a circuit for sensory valence in Caenorhabditis elegans. Sophie Rengarajan, Kristen A. Yankura, Manon L. Guillermin, Wendy Fung, Elissa A. Hallem. Proceedings of the National Academy of Sciences Jan 2019, 116 (5) 1776-1781; DOI: 10.1073/pnas.1807454116
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:92425
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:23 Jan 2019 18:50
Last Modified:29 Jan 2019 21:47

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