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Temporally and Spatially Distinct Thirst Satiation Signals

Augustine, Vineet and Ebisu, Haruka and Zhao, Yuan and Lee, Sangjun and Ho, Brittany and Mizuno, Grace O. and Tian, Lin and Oka, Yuki (2019) Temporally and Spatially Distinct Thirst Satiation Signals. Neuron, 103 (2). pp. 242-249. ISSN 0896-6273. https://resolver.caltech.edu/CaltechAUTHORS:20190529-103834599

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Abstract

For thirsty animals, fluid intake provides both satiation and pleasure of drinking. How the brain processes these factors is currently unknown. Here, we identified neural circuits underlying thirst satiation and examined their contribution to reward signals. We show that thirst-driving neurons receive temporally distinct satiation signals by liquid-gulping-induced oropharyngeal stimuli and gut osmolality sensing. We demonstrate that individual thirst satiation signals are mediated by anatomically distinct inhibitory neural circuits in the lamina terminalis. Moreover, we used an ultrafast dopamine (DA) sensor to examine whether thirst satiation itself stimulates the reward-related circuits. Interestingly, spontaneous drinking behavior but not thirst drive reduction triggered DA release. Importantly, chemogenetic stimulation of thirst satiation neurons did not activate DA neurons under water-restricted conditions. Together, this study dissected the thirst satiation circuit, the activity of which is functionally separable from reward-related brain activity.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1016/j.neuron.2019.04.039DOIArticle
Additional Information:© 2019 Elsevier. Received 15 January 2019, Revised 27 March 2019, Accepted 26 April 2019, Available online 29 May 2019. We thank Drs. Joshua Berke and Anne Andrews and the members of the Oka laboratory for helpful discussion and 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 McKnight Foundation, the Klingenstein-Simons Foundation, and NIH (R01NS109997 and R56MH113030). H.E. is supported by the Uehara Memorial Foundation and Japan Society for the Promotion of Science. Author Contributions: V.A., H.E., and Y.O. conceived the research program and designed experiments. V.A. and H.E. carried out the experiments and analyzed the data with help from S.L. and B.H. Y.Z. performed all slice patch-clamp recordings. L.T. and G.O.M. provided dLight1.3 viruses and performed in vitro experiments. V.A., H.E., and Y.O. wrote the paper. Y.O. supervised the entire work. The authors declare no competing interests.
Funders:
Funding AgencyGrant Number
CaltechUNSPECIFIED
Caltech Division of Biology and Biological EngineeringUNSPECIFIED
Searle Scholars ProgramUNSPECIFIED
Edward Mallinckrodt, Jr. FoundationUNSPECIFIED
McKnight FoundationUNSPECIFIED
Klingenstein-Simons FoundationUNSPECIFIED
NIHR01NS109997
NIHR56MH113030
Uehara Memorial FoundationUNSPECIFIED
Japan Society for the Promotion of Science (JSPS)UNSPECIFIED
Subject Keywords:homeostasis; appetite; thirst; satiation; gut-brain axis; reward circuit
Issue or Number:2
Record Number:CaltechAUTHORS:20190529-103834599
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20190529-103834599
Official Citation:Vineet Augustine, Haruka Ebisu, Yuan Zhao, Sangjun Lee, Brittany Ho, Grace O. Mizuno, Lin Tian, Yuki Oka, Temporally and Spatially Distinct Thirst Satiation Signals, Neuron, Volume 103, Issue 2, 2019, Pages 242-249.e4, ISSN 0896-6273, https://doi.org/10.1016/j.neuron.2019.04.039. (http://www.sciencedirect.com/science/article/pii/S0896627319303964)
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:95881
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:29 May 2019 17:43
Last Modified:03 Oct 2019 21:17

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