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Thirst driving and suppressing signals encoded by distinct neural populations in the brain

Oka, Yuki and Ye, Mingyu and Zuker, Charles S. (2015) Thirst driving and suppressing signals encoded by distinct neural populations in the brain. Nature, 520 (7547). pp. 349-352. ISSN 0028-0836. PMCID PMC4401619. http://resolver.caltech.edu/CaltechAUTHORS:20150120-093554854

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[img] Image (JPEG) (Extended Data Figure 1: Fos induction by water deprivation in the SFO) - Supplemental Material
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[img] Image (JPEG) (Extended Data Figure 2: nNOS-positive neurons in the SFO co-express Vglut2, an excitatory neuronal marker) - Supplemental Material
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[img] Image (JPEG) (Extended Data Figure 3: Virally expressed ChR2–eYFP under the control of CamKII promoter co-localized with endogenous CamKII) - Supplemental Material
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[img] Image (JPEG) (Extended Data Figure 4: ChR2-dependent drinking requires activation of SFO CamKII-positive neurons concurrently with water presentation) - Supplemental Material
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[img] Image (JPEG) (Extended Data Figure 5: Three distinct cell populations in the SFO) - Supplemental Material
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[img] Image (JPEG) (Extended Data Figure 6: Angiotensin receptor AT1 is enriched in ETV-1+ neurons in the SFO) - Supplemental Material
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[img] Image (JPEG) (Extended Data Figure 7: Neural projections from Vgat- and Etv-1-positive SFO neurons) - Supplemental Material
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Abstract

Thirst is the basic instinct to drink water. Previously, it was shown that neurons in several circumventricular organs of the hypothalamus are activated by thirst-inducing conditions. Here we identify two distinct, genetically separable neural populations in the subfornical organ that trigger or suppress thirst. We show that optogenetic activation of subfornical organ excitatory neurons, marked by the expression of the transcription factor ETV-1, evokes intense drinking behaviour, and does so even in fully water-satiated animals. The light-induced response is highly specific for water, immediate and strictly locked to the laser stimulus. In contrast, activation of a second population of subfornical organ neurons, marked by expression of the vesicular GABA transporter VGAT, drastically suppresses drinking, even in water-craving thirsty animals. These results reveal an innate brain circuit that can turn an animal’s water-drinking behaviour on and off, and probably functions as a centre for thirst control in the mammalian brain.


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Additional Information:© 2015 Macmillan Publishers Limited. Received 02 September 2014; Accepted 24 November 2014; Published online 26 January 2015. We thank N. Propp for help with mouse husbandry. We also thank H. Fishman for suggestions, Z. Turan, N. Ryba and T. Usdin for technical support, and N. Ryba and members of the Zuker laboratory for comments. We acknowledge B. Lowell and M. Krashes for advice. Y.O. and M.Y. were supported by grants from the National Institute on Drug Abuse and National Institute of Neurological Disorders and Stroke to C.S.Z. C.S.Z. is an investigator of the Howard Hughes Medical Institute. Y.O. developed the research program, designed the study, carried out the experiments, and analysed data; M.Y. performed all slice patch clamp recordings; C.S.Z. analysed data, designed experiments and together with Y.O. wrote the paper. The authors declare no competing financial interests.
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Funding AgencyGrant Number
National Institute on Drug Abuse (NIDA)UNSPECIFIED
National Institute of Neurological Disorders and Stroke (NINDS)UNSPECIFIED
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
PubMed Central ID:PMC4401619
Record Number:CaltechAUTHORS:20150120-093554854
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20150120-093554854
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:53866
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:26 Jan 2015 17:28
Last Modified:18 Nov 2015 18:05

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