The median preoptic nucleus: front and centre for the regulation of body fluid, sodium, temperature, sleep and cardiovascular homeostasis

McKinley, Michael J.; Yao, Song T.; Uschakov, Aaron; McAllen, Robin M.; Rundgren, Mats; Martelli, Davide

doi:10.1111/apha.12487

Cited by 158 publications

(126 citation statements)

References 204 publications

(453 reference statements)

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“…However, we showed that individual thirst-related neuronal populations of the lamina terminalis are hierarchically organized, and that MnPO nNOS neurons are the behavioural output neurons. Previous lesion studies in rats and sheep have proposed a model in which the MnPO serves as a critical site that integrates inputs from osmosensory neurons of the SFO and the OVLT 36 – 38 . Our findings well explain and further advance the concept of this model with cell-type-specific precision.…”

Section: Discussionmentioning

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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Section: Discussionmentioning

confidence: 99%

Hierarchical neural architecture underlying thirst regulation

Augustine

Gökçe

Lee

et al. 2018

Nature

131

139

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“…In addition to maternal behavior, the MPOA has a number of important homeostatic roles, including thermoregulation, sleep, and social reward (21,22). Potentially, maternal behavior could be impacted if losing the influence of prolactin on these functions also impaired pregnancyrelated adaptations in the maternal brain.…”

Section: Discussionmentioning

confidence: 99%

Prolactin action in the medial preoptic area is necessary for postpartum maternal nursing behavior

Brown

Aoki

Ladyman

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

127

147

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Pregnancy hormones, such as prolactin, sensitize neural circuits controlling parental interactions to induce timely activation of maternal behaviors immediately after parturition. While the medial preoptic area (MPOA) is known to be critical for maternal behavior, the specific role of prolactin in this brain region has remained elusive. Here, we evaluated the role of prolactin action in the MPOA using complementary genetic strategies in mice. We characterized prolactin-responsive neurons within the MPOA at different hormonal stages and delineated their projections in the brain. We found that MPOA neurons expressing prolactin receptors (Prlr) form the nexus of a complex prolactin-responsive neural circuit, indicating that changing prolactin levels can act at multiple sites and thus, impinge on the overall activity of a distributed network of neurons. Conditional KO of Prlr from neuronal subpopulations expressing the neurotransmitters GABA or glutamate within this circuit markedly reduced the capacity for prolactin action both in the MPOA and throughout the network. Each of these manipulations, however, produced only subtle impacts on maternal care, suggesting that this distributed circuit is robust with respect to alterations in prolactin signaling. In contrast, acute deletion of Prlr in all MPOA neurons of adult female mice resulted in profound deficits in maternal care soon after birth. All mothers abandoned their pups, showing that prolactin action on MPOA neurons is necessary for the normal expression of postpartum maternal behavior in mice. Our data establish a critical role for prolactin-induced behavioral responses in the maternal brain, ensuring survival of mammalian offspring.maternal behavior | prolactin | prolactin receptor | medial preoptic area M aternal care is critical to survival of dependent offspring in mammals. Seminal work from Rosenblatt (1), published 50 y ago, showed that maternal behavior can be exhibited in ovariectomized, hypophysectomized rats, suggesting an underlying neural basis that was not dependent on hormonal inputs. Subsequent studies have characterized a complex neural circuitry controlling parental interactions (2, 3), with distributed sites mediating different components of the behavior (4). While the neural circuit controlling maternal behavior is not thought to be dependent on hormonal inputs, it is clear that pregnancy hormones, particularly rising levels of estradiol, oxytocin, prolactin, and placental lactogen, coupled with an abrupt decrease in progesterone can sensitize the underlying circuitry to induce timely activation of maternal behaviors immediately after parturition (5). The medial preoptic area (MPOA) forms a critical nexus (2, 3), integrating a range of hormonal and sensory inputs into the maternal circuit.Within the complex hormonal milieu of pregnancy, the specific role of prolactin in maternal behavior has remained elusive. This is largely because prolactin and the related placental lactogen have an obligate role in sustaining ovarian progesterone productio...

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“…Males: inIGF1RKO, n = 5, and controls, n = 5; females: inIGF1RKO, n = 8, and controls, n = 8. *P < 0.05; **P < 0.01; ***P < 0.001. structures integrating and controlling thermoregulation in the central nervous system (34). Several areas in POA, for instance, ventrolateral preoptic nucleus (35), receive afferents from forebrain circuitry; namely, through the lateral septal nucleus, but also directly from cortical areas.…”

Section: Discussionmentioning

confidence: 99%

Insulin-like growth factor 1 receptor regulates hypothermia during calorie restriction

Cintrón-Colón

Sanchez‐Alavez

Nguyen

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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When food resources are scarce, endothermic animals can lower core body temperature (T b ). This phenomenon is believed to be part of an adaptive mechanism that may have evolved to conserve energy until more food becomes available. Here, we found in the mouse that the insulin-like growth factor 1 receptor (IGF-1R) controls this response in the central nervous system. Pharmacological or genetic inhibition of IGF-1R enhanced the reduction of temperature and of energy expenditure during calorie restriction. Full blockade of IGF-1R affected female and male mice similarly. In contrast, genetic IGF-1R dosage was effective only in females, where it also induced transient and estrusspecific hypothermia in animals fed ad libitum. These effects were regulated in the brain, as only central, not peripheral, pharmacological activation of IGF-1R prevented hypothermia during calorie restriction. Targeted IGF-1R knockout selectively in forebrain neurons revealed that IGF signaling also modulates calorie restriction-dependent T b regulation in regions rostral of the canonical hypothalamic nuclei involved in controlling body temperature. In aggregate, these data identify central IGF-1R as a mediator of the integration of nutrient and temperature homeostasis. They also show that calorie restriction, IGF-1R signaling, and body temperature, three of the main regulators of metabolism, aging, and longevity, are components of the same pathway.IGF-1R | temperature | calorie restriction | energy homeostasis | aging

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The median preoptic nucleus: front and centre for the regulation of body fluid, sodium, temperature, sleep and cardiovascular homeostasis

Cited by 158 publications

References 204 publications

Hierarchical neural architecture underlying thirst regulation

Hierarchical neural architecture underlying thirst regulation

Prolactin action in the medial preoptic area is necessary for postpartum maternal nursing behavior

Insulin-like growth factor 1 receptor regulates hypothermia during calorie restriction

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