Neural circuits underlying thirst and fluid homeostasis

Zimmerman, Christopher A.; Leib, David E.; Knight, Zachary A.

doi:10.1038/nrn.2017.71

Cited by 226 publications

(227 citation statements)

References 187 publications

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“…Canonical neural populations and circuits that regulate energy balance and appetite [1, 2] are separate from those that regulate sleep homeostasis and sleep state transitions [3, 4]. Homeostatic systems for thirst [5, 6] and body temperature [7, 8] also seem to have their own dedicated neural systems and networks. Therefore, fascinating areas for future investigation include measuring the effect that these separate populations exert over each other during changing survival needs, and determining how the brain ultimately integrates several distinct homeostatic cues into a single, focused behavioral choice.…”

Section: Discussionmentioning

confidence: 99%

Hypothalamic Neurons that Regulate Feeding Can Influence Sleep/Wake States Based on Homeostatic Need

et al. 2018

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SUMMARY Eating and sleeping represent two mutually exclusive behaviors that satisfy distinct homeostatic needs. Because an animal cannot eat and sleep at the same time, brain systems that regulate energy homeostasis are likely to influence sleep/wake behavior. Indeed, previous studies indicate that animals adjust sleep cycles around periods of food need and availability. Furthermore, hormones that affect energy homeostasis also affect sleep/wake states: the orexigenic hormone ghrelin promotes wakefulness, while the anorexigenic hormones leptin and insulin increase the duration of slow wave sleep. However, whether neural populations that regulate feeding can influence sleep/wake states is unknown. The hypothalamic arcuate nucleus contains two neuronal populations that exert opposing effects on energy homeostasis: agouti-related protein (AgRP)-expressing neurons detect caloric need and orchestrate food-seeking behavior, while activity in pro-opiomelanocortin (POMC)-expressing neurons induces satiety. We tested the hypotheses that AgRP neurons affect sleep homeostasis by promoting states of wakefulness, while POMC neurons promote states of sleep. Indeed, optogenetic or chemogenetic stimulation of AgRP neurons in mice promoted wakefulness while decreasing the quantity and integrity of sleep. Inhibition of AgRP neurons rescued sleep integrity in food-deprived mice, highlighting the physiological importance of AgRP neuron activity for the suppression of sleep by hunger. Conversely, stimulation of POMC neurons promoted sleep states and decreased sleep fragmentation in food-deprived mice. Interestingly, we also found that sleep deprivation attenuated the effects of AgRP neuron activity on food intake and wakefulness. These results indicate that homeostatic feeding neurons can hierarchically affect behavioral outcomes depending on homeostatic need.

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Section: Discussionmentioning

confidence: 99%

Hypothalamic Neurons that Regulate Feeding Can Influence Sleep/Wake States Based on Homeostatic Need

et al. 2018

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“…An illustration of new data described in this review on the cell type-specific neural circuits that underlie thirst and fluid homeostasis in the mouse brain (modified from [2]; [27], and from Gizowski and Bourque [5]) is shown in Figure 2. The LT consists of 2 sensory circumventricular organs (the SFO and organum vasculosum of the LT [OVLT]) and an integrative structure (the MnPO).…”

Section: Coordination Of Eating Drinking and Vasopressin Releasementioning

confidence: 99%

“…I am now describing a detailed wiring map for thirst (i.e., including anticipatory signals for thirst and vasopressin release converging on the same homeostatic neurons), circumventricular organs that monitor the composition of the blood [2], and the identification of specific water receptor taste cells [3]. The median preoptic nucleus (MnPO) of the hypothalamus could integrate multiple thirst-generating stimuli [4,5].…”

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confidence: 99%

Vasopressin and the Regulation of Thirst

Bichet¹

2018

Ann Nutr Metab

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Recent experiments using optogenetic tools allow the identification and functional analysis of thirst neurons and vasopressin producing neurons. Two major advances provide a detailed anatomy of taste for water and arginine-vasopressin (AVP) release: (1) thirst and AVP release are regulated not only by the classical homeostatic, intero-sensory plasma osmolality negative feedback, but also by novel, extero-sensory, anticipatory signals. These anticipatory signals for thirst and vasopressin release converge on the same homeostatic neurons of circumventricular organs that monitor the composition of the blood; (2) acid-sensing taste receptor cells (which express polycystic kidney disease 2-like 1 protein) on the tongue that were previously suggested as the sour taste sensors also mediate taste responses to water. The tongue has a taste for water. The median preoptic nucleus (MnPO) of the hypothalamus could integrate multiple thirst-generating stimuli including cardiopulmonary signals, osmolality, angiotensin II, oropharyngeal and gastric signals, the latter possibly representing anticipatory signals. Dehydration is aversive and MnPO neuron activity is proportional to the intensity of this aversive state.

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“…How the brain integrates homeostatic and behavioural inputs to coordinate drinking behaviour is an unsolved question. As such, uncovering the neural circuits that process these regulatory signals is a critical step in understanding the neural logic of thirst regulation 13–15 .…”

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confidence: 99%

Hierarchical neural architecture underlying thirst regulation

Augustine

Gökçe

Lee

et al. 2018

Nature

131

139

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Neural circuits for appetites are regulated by both homeostatic perturbations and ingestive behaviour. However, the circuit organization that integrates these internal and external stimuli is unclear. Here we show in mice that excitatory neural populations in the lamina terminalis form a hierarchical circuit architecture to regulate thirst. Among them, nitric oxide synthase-expressing neurons in the median preoptic nucleus (MnPO) are essential for the integration of signals from the thirst-driving neurons of the subfornical organ (SFO). Conversely, a distinct inhibitory circuit, involving MnPO GABAergic neurons that express glucagon-like peptide 1 receptor (GLP1R), is activated immediately upon drinking and monosynaptically inhibits SFO thirst neurons. These responses are induced by the ingestion of fluids but not solids, and are time-locked to the onset and offset of drinking. Furthermore, loss-of-function manipulations of GLP1R-expressing MnPO neurons lead to a polydipsic, overdrinking phenotype. These neurons therefore facilitate rapid satiety of thirst by monitoring real-time fluid ingestion. Our study reveals dynamic thirst circuits that integrate the homeostatic-instinctive requirement for fluids and the consequent drinking behaviour to maintain internal water balance.

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Neural circuits underlying thirst and fluid homeostasis

Cited by 226 publications

References 187 publications

Hypothalamic Neurons that Regulate Feeding Can Influence Sleep/Wake States Based on Homeostatic Need

Hypothalamic Neurons that Regulate Feeding Can Influence Sleep/Wake States Based on Homeostatic Need

Vasopressin and the Regulation of Thirst

Hierarchical neural architecture underlying thirst regulation

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