Temporally and Spatially Distinct Thirst Satiation Signals
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.
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.Attached Files
Accepted Version - nihms-1067496.pdf
Supplemental Material - 1-s2.0-S0896627319303964-mmc1.pdf
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Additional details
- PMCID
- PMC7335596
- Eprint ID
- 95881
- DOI
- 10.1016/j.neuron.2019.04.039
- Resolver ID
- CaltechAUTHORS:20190529-103834599
- Caltech
- Caltech Division of Biology and Biological Engineering
- Searle Scholars Program
- Edward Mallinckrodt, Jr. Foundation
- McKnight Foundation
- Klingenstein-Simons Foundation
- NIH
- R01NS109997
- NIH
- R56MH113030
- Uehara Memorial Foundation
- Japan Society for the Promotion of Science (JSPS)
- Created
-
2019-05-29Created from EPrint's datestamp field
- Updated
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2022-02-15Created from EPrint's last_modified field