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The Cellular Mechanism for Water Detection in the Mammalian Taste System

Zocchi, Dhruv and Wennemuth, Gunther and Oka, Yuki (2017) The Cellular Mechanism for Water Detection in the Mammalian Taste System. Nature Neuroscience, 20 (7). pp. 927-933. ISSN 1097-6256. doi:10.1038/nn.4575.

[img] Video (MPEG) (Video 1: Photostimulation of PKD2L1-expressing TRCs in a Pdk2l1ChR2 mouse elicits sustained licking behavior) - Supplemental Material
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[img] Video (MPEG) (Video 2: Photostimulation of PKD2L1-expressing TRCs in a control mouse does not elicit licking behavior) - Supplemental Material
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Initiation of drinking behavior relies on both internal state and peripheral water detection. While central neural circuits regulating thirst have been well studied, it is still unclear how mammals recognize external water. Here we show that acid-sensing taste receptor cells (TRCs) that were previously suggested as the sour taste sensors also mediate taste responses to water. Genetic silencing of these TRCs abolished water-evoked responses in taste nerves. Optogenetic self-stimulation of acid-sensing TRCs in thirsty animals induced robust drinking responses toward light even without water. This behavior was only observed when animals were water-deprived but not under food- or salt-depleted conditions, indicating that the hedonic value of water-evoked responses is highly internal-state dependent. Conversely, thirsty animals lacking functional acid-sensing TRCs showed compromised discrimination between water and nonaqueous fluids. Taken together, this study revealed a function of mammalian acid-sensing TRCs that provide a cue for external water.

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Additional Information:© 2017 Macmillan Publishers Limited, part of Springer Nature. Received 30 March 2017; Accepted 30 April 2017; Published online 29 May 2017. We thank B. Ho for help with mouse husbandry. We also thank K. Scott, M. Meister and D.J. Anderson for helpful suggestions. We thank C.S. Zuker (Columbia) and N. Ryba (NIDCR) for generously sharing Pkd2l1-Cre and TRPM5 knockout transgenic animals, H. Matsunami (Duke) for PKD2L1 antibody, S. Lee for technical support and members of the Oka laboratory for comments. This work was supported by Startup funds from the President and Provost of California Institute of Technology and the Biology and Biological Engineering Division of California Institute of Technology. Y.O. is also supported by the Searle Scholars Program, the Mallinckrodt Foundation, the Okawa Foundation, the McKnight Foundation and the Klingenstein-Simons Foundation. Support was provided by DFG WE 2344/9-1 to G.W. Y.O. have disclosed these methods and findings to the Caltech Office of Technology Transfer. Author Contributions: D.Z. and Y.O. conceived the research program. D.Z. and Y.O. designed and carried out the experiments and analyzed data. G.W. maintained and provided CA4 knockout animals. D.Z. analyzed data and, together with Y.O., wrote the paper. Y.O. supervised the entire work. The authors declare no competing financial interests.
Group:Tianqiao and Chrissy Chen Institute for Neuroscience
Funding AgencyGrant Number
Searle Scholars ProgramUNSPECIFIED
Edward Mallinckrodt, Jr. FoundationUNSPECIFIED
Okawa FoundationUNSPECIFIED
McKnight FoundationUNSPECIFIED
Klingenstein-Simons FoundationUNSPECIFIED
Deutsche Forschungsgemeinschaft (DFG)WE 2344/9-1
Issue or Number:7
Record Number:CaltechAUTHORS:20170501-103831958
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Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:77104
Deposited By: George Porter
Deposited On:30 May 2017 18:03
Last Modified:15 Nov 2021 17:28

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