Temporally and Spatially Distinct Thirst Satiation Signals

Vineet Augustine, Haruka Ebisu, Yuan Zhao, Sangjun Lee, Brittany Ho, Grace O. Mizuno, Lin Tian, Yuki Oka

Research output: Contribution to journalArticle

6 Citations (Scopus)

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. The mammalian thirst circuit receives temporally distinct satiation signals by both liquid gulping action and gut osmolality sensing. These thirst satiation signals are functionally separable from the reward-related circuit activity.

Original languageEnglish (US)
Pages (from-to)242-249.e4
JournalNeuron
Volume103
Issue number2
DOIs
StatePublished - Jul 17 2019

Fingerprint

Satiation
Thirst
Reward
Osmolar Concentration
Dopamine
Neurons
Drinking Behavior
Pleasure
Dopaminergic Neurons
Brain
Hypothalamus
Drinking

Keywords

  • appetite
  • gut-brain axis
  • homeostasis
  • reward circuit
  • satiation
  • thirst

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Augustine, V., Ebisu, H., Zhao, Y., Lee, S., Ho, B., Mizuno, G. O., ... Oka, Y. (2019). Temporally and Spatially Distinct Thirst Satiation Signals. Neuron, 103(2), 242-249.e4. https://doi.org/10.1016/j.neuron.2019.04.039

Temporally and Spatially Distinct Thirst Satiation Signals. / Augustine, Vineet; Ebisu, Haruka; Zhao, Yuan; Lee, Sangjun; Ho, Brittany; Mizuno, Grace O.; Tian, Lin; Oka, Yuki.

In: Neuron, Vol. 103, No. 2, 17.07.2019, p. 242-249.e4.

Research output: Contribution to journalArticle

Augustine, V, Ebisu, H, Zhao, Y, Lee, S, Ho, B, Mizuno, GO, Tian, L & Oka, Y 2019, 'Temporally and Spatially Distinct Thirst Satiation Signals', Neuron, vol. 103, no. 2, pp. 242-249.e4. https://doi.org/10.1016/j.neuron.2019.04.039
Augustine V, Ebisu H, Zhao Y, Lee S, Ho B, Mizuno GO et al. Temporally and Spatially Distinct Thirst Satiation Signals. Neuron. 2019 Jul 17;103(2):242-249.e4. https://doi.org/10.1016/j.neuron.2019.04.039
Augustine, Vineet ; Ebisu, Haruka ; Zhao, Yuan ; Lee, Sangjun ; Ho, Brittany ; Mizuno, Grace O. ; Tian, Lin ; Oka, Yuki. / Temporally and Spatially Distinct Thirst Satiation Signals. In: Neuron. 2019 ; Vol. 103, No. 2. pp. 242-249.e4.
@article{1f9056f8ee884999a19e79f1cb3a499c,
title = "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. The mammalian thirst circuit receives temporally distinct satiation signals by both liquid gulping action and gut osmolality sensing. These thirst satiation signals are functionally separable from the reward-related circuit activity.",
keywords = "appetite, gut-brain axis, homeostasis, reward circuit, satiation, thirst",
author = "Vineet Augustine and Haruka Ebisu and Yuan Zhao and Sangjun Lee and Brittany Ho and Mizuno, {Grace O.} and Lin Tian and Yuki Oka",
year = "2019",
month = "7",
day = "17",
doi = "10.1016/j.neuron.2019.04.039",
language = "English (US)",
volume = "103",
pages = "242--249.e4",
journal = "Neuron",
issn = "0896-6273",
publisher = "Cell Press",
number = "2",

}

TY - JOUR

T1 - Temporally and Spatially Distinct Thirst Satiation Signals

AU - Augustine, Vineet

AU - Ebisu, Haruka

AU - Zhao, Yuan

AU - Lee, Sangjun

AU - Ho, Brittany

AU - Mizuno, Grace O.

AU - Tian, Lin

AU - Oka, Yuki

PY - 2019/7/17

Y1 - 2019/7/17

N2 - 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. The mammalian thirst circuit receives temporally distinct satiation signals by both liquid gulping action and gut osmolality sensing. These thirst satiation signals are functionally separable from the reward-related circuit activity.

AB - 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. The mammalian thirst circuit receives temporally distinct satiation signals by both liquid gulping action and gut osmolality sensing. These thirst satiation signals are functionally separable from the reward-related circuit activity.

KW - appetite

KW - gut-brain axis

KW - homeostasis

KW - reward circuit

KW - satiation

KW - thirst

UR - http://www.scopus.com/inward/record.url?scp=85068744238&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85068744238&partnerID=8YFLogxK

U2 - 10.1016/j.neuron.2019.04.039

DO - 10.1016/j.neuron.2019.04.039

M3 - Article

C2 - 31153646

AN - SCOPUS:85068744238

VL - 103

SP - 242-249.e4

JO - Neuron

JF - Neuron

SN - 0896-6273

IS - 2

ER -