The neural basis of homeostatic and anticipatory thirst

Gizowski, Claire; Bourque, Charles W.

doi:10.1038/nrneph.2017.149

Cited by 113 publications

(111 citation statements)

References 242 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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“…Osmolarity- and angiotensinsensitive neurons in the subfornical organ (SFO) and vascular organ of the lamina terminalis project to the median preoptic nucleus (MnPO), which integrates these physiological signals and relays that information to multiple downstream nuclei (17) (Fig. 1A).…”

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confidence: 99%

Thirst regulates motivated behavior through modulation of brainwide neural population dynamics

Allen

Chen

Pichamoorthy

et al. 2019

Science

276

142

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Neuron activity across the brain How is it that groups of neurons dispersed through the brain interact to generate complex behaviors? Three papers in this issue present brain-scale studies of neuronal activity and dynamics (see the Perspective by Huk and Hart). Allen et al. found that in thirsty mice, there is widespread neural activity related to stimuli that elicit licking and drinking. Individual neurons encoded task-specific responses, but every brain area contained neurons with different types of response. Optogenetic stimulation of thirst-sensing neurons in one area of the brain reinstated drinking and neuronal activity across the brain that previously signaled thirst. Gründemann et al. investigated the activity of mouse basal amygdala neurons in relation to behavior during different tasks. Two ensembles of neurons showed orthogonal activity during exploratory and nonexploratory behaviors, possibly reflecting different levels of anxiety experienced in these areas. Stringer et al. analyzed spontaneous neuronal firing, finding that neurons in the primary visual cortex encoded both visual information and motor activity related to facial movements. The variability of neuronal responses to visual stimuli in the primary visual area is mainly related to arousal and reflects the encoding of latent behavioral states. Science , this issue p. eaav3932 , p. eaav8736 , p. eaav7893 ; see also p. 236

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“…By contrast, drinking is terminated rapidly when animals have ingested a sufficient amount of water, which generally precedes the absorption of the ingested fluid 5–10 . To achieve such accurate fluid regulation, the brain needs to monitor both internal water balance and fluid ingestion on a real-time basis 11,12 . How the brain integrates homeostatic and behavioural inputs to coordinate drinking behaviour is an unsolved question.…”

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confidence: 99%

Hierarchical neural architecture underlying thirst regulation

Augustine

Gökçe

Lee

et al. 2018

Nature

119

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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The neural basis of homeostatic and anticipatory thirst

Cited by 113 publications

References 242 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

Thirst regulates motivated behavior through modulation of brainwide neural population dynamics

Hierarchical neural architecture underlying thirst regulation

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