Hierarchical neural architecture underlying thirst regulation

Augustine, Vineet; Gökçe, Sertan Kutal; Lee, Sang-Jun; Wang, Bo; Davidson, Thomas J.; Reimann, Frank; Gribble, Fiona M.; Deisseroth, Karl; Lois, Carlos; Oka, Yuki

doi:10.1038/nature25488

Cited by 131 publications

(150 citation statements)

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“…Which of these efferent pathways shown to project from the subfornical organ or OVLT was responsible for transmitting thirst-related signals could not be determined from these tracing studies; however, a relay via the MnPO appeared to be likely. Evidence obtained in rats support- 56 These data indicate that neural signals, arising from osmotic, angiotensin or relaxin stimulation of the subfornical organ and OVLT, are relayed onward through a glutamatergic synapse within the MnPO to other sites in the brain including cortical regions ( Figure 2). It should also be noted that many neurones within the MnPO are sodium sensitive, 57 which may explain the profound effects that changes in cerebrospinal fluid Na + concentration have on thirst and water intake in sheep and goats.…”

Section: Cleus [Pvt] and Median Preoptic Nucleus [Mnpo]mentioning

confidence: 85%

“…50 56 These data indicate that neural signals, arising from osmotic, angiotensin or relaxin stimulation of the subfornical organ and OVLT, are relayed onward through a glutamatergic synapse within the MnPO to other sites in the brain including cortical regions ( Figure 2). 50 56 These data indicate that neural signals, arising from osmotic, angiotensin or relaxin stimulation of the subfornical organ and OVLT, are relayed onward through a glutamatergic synapse within the MnPO to other sites in the brain including cortical regions ( Figure 2).…”

Section: A Synaptic Relay In the Median Preoptic Nucleusmentioning

confidence: 95%

“…Recent studies in mice reveal that glucagon-like peptide-1 (GLP-1) receptor-expressing neurones in the MnPO, which are probably GABAergic, inhibit the thirst promoting glutamatergic neurones in the subfornical organ, 56 suggesting that peripheral signals for quenching thirst reach the subfornical organ indirectly via brainstem nuclei and the MnPO. Although the precise phenotype of the relevant neuronal populations involved in inhibiting thirst within each brain region remains to be identified, GABAergic neuronal populations within the subfornical organ, as well as those in the MnPO, have been shown to decrease water consumption when activated.…”

Section: Inhibitory Signals From Sensory Cvos Mediating the Satiatimentioning

confidence: 99%

“…These signals are likely to be carried via the vagal (X) nerve to the nucleus of the solitary tract (NTS) and lateral parabrachial nucleus, including oxytocin receptorexpressing neurones in the lateral parabrachial nucleus that project to the OVLT and MnPO 64. This declining activity continues over several minutes until the water deficit has been repaired, in mice reveal that glucagon-like peptide-1 (GLP-1) receptor-expressing neurones in the MnPO, which are probably GABAergic, inhibit the thirst promoting glutamatergic neurones in the subfornical organ,56 suggesting that peripheral signals for quenching thirst reach the subfornical organ indirectly via brainstem nuclei and the MnPO. These studies have revealed that activity in thirst-promoting neurones in the subfornical organ (ie, SFO Glut ) and MnPO declines the moment when thirsty mice start licking water.…”

mentioning

confidence: 99%

“…when the channel-rhodopsin within their terminals in the MnPO is stimulated by light, drinking occurs immediately 14,38. Furthermore, when such MnPO neurones that receive input from SFO Glut neurones are genetically modified to express caspase3, thereby resulting in their ablation, water drinking caused by stimulation of SFO Glut or glutamatergic neurones within OVLT (OVLT Glut ) is greatly reduced,56 as is drinking caused by dehydration 56. However, as long as these MnPO neurones are intact, ablation of SFO Glut , either individually or in combination with OVLT Glut neurones, does not affect the drinking response to photo-stimulation of MnPO neurones 54.…”

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confidence: 99%

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From sensory circumventricular organs to cerebral cortex: Neural pathways controlling thirst and hunger

McKinley

Denton

Ryan

et al. 2019

J Neuroendocrinology

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Much progress has been made during the past 30 years with respect to elucidating the neural and endocrine pathways by which bodily needs for water and energy are brought to conscious awareness through the generation of thirst and hunger. One way that circulating hormones influence thirst and hunger is by acting on neurones within sensory circumventricular organs (CVOs). This is possible because the subfornical organ and organum vasculosum of the lamina terminalis (OVLT), the sensory CVOs in the forebrain, and the area postrema in the hindbrain lack a normal blood‐brain barrier such that neurones within them are exposed to blood‐borne agents. The neural signals generated by hormonal action in these sensory CVOs are relayed to several sites in the cerebral cortex to stimulate or inhibit thirst or hunger. The subfornical organ and OVLT respond to circulating angiotensin II, relaxin and hypertonicity to drive thirst‐related neural pathways, whereas circulating amylin, leptin and possibly glucagon‐like peptide‐1 act at the area postrema to influence neural pathways inhibiting food intake. As a result of investigations using functional brain imaging techniques, the insula and anterior cingulate cortex, as well as several other cortical sites, have been implicated in the conscious perception of thirst and hunger in humans. Viral tracing techniques show that the anterior cingulate cortex and insula receive neural inputs from thirst‐related neurones in the subfornical organ and OVLT, with hunger‐related neurones in the area postrema having polysynaptic efferent connections to these cortical regions. For thirst, initially, the median preoptic nucleus and, subsequently, the thalamic paraventricular nucleus and lateral hypothalamus have been identified as likely sites of synaptic links in pathways from the subfornical organ and OVLT to the cortex. The challenge remains to identify the links in the neural pathways that relay signals originating in sensory CVOs to cortical sites subserving either thirst or hunger.

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Section: Cleus [Pvt] and Median Preoptic Nucleus [Mnpo]mentioning

confidence: 85%

Section: A Synaptic Relay In the Median Preoptic Nucleusmentioning

confidence: 95%

Section: Inhibitory Signals From Sensory Cvos Mediating the Satiatimentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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From sensory circumventricular organs to cerebral cortex: Neural pathways controlling thirst and hunger

McKinley

Denton

Ryan

et al. 2019

J Neuroendocrinology

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Morphological and neurochemical characterization of glycinergic neurons in laminae I–IV of the mouse spinal dorsal horn

Miranda

Hegedüs

Wildner

et al. 2021

J of Comparative Neurology

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A growing body of experimental evidence shows that glycinergic inhibition plays vital roles in spinal pain processing. In spite of this, however, our knowledge about the morphology, neurochemical characteristics, and synaptic relations of glycinergic neurons in the spinal dorsal horn is very limited. The lack of this knowledge makes our understanding about the specific contribution of glycinergic neurons to spinal pain processing quite vague. Here we investigated the morphology and neurochemical characteristics of glycinergic neurons in laminae I-IV of the spinal dorsal horn using a GlyT2::CreERT2-tdTomato transgenic mouse line. Confirming previous reports, we show that glycinergic neurons are sparsely distributed in laminae I-II, but their densities are much higher in lamina III and especially in lamina IV. First in the literature, we provide experimental evidence indicating that in addition to neurons in which glycine colocalizes with GABA, there are glycinergic neurons in laminae I-II that do not express GABA and can thus be referred to as glycine-only neurons. According to the shape and size of cell bodies and dendritic morphology, we divided the tdTomato-labeled glycinergic neurons into three and six morphological groups in laminae I-II and laminae III-IV, respectively. We also demonstrate that most of the glycinergic neurons co-express neuronal nitric oxide synthase, parvalbumin, the receptor tyrosine kinase RET, and the retinoic acid-related orphan nuclear receptor β (RORβ), but there might be others that need further neurochemical characterization. The present findings may foster our understanding about the contribution of glycinergic inhibition to spinal pain processing.

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Structure and Function of the Blood–Brain Barrier (BBB)

Benz

Liebner

2020

Handbook of Experimental Pharmacology

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Hierarchical neural architecture underlying thirst regulation

Cited by 131 publications

References 45 publications

From sensory circumventricular organs to cerebral cortex: Neural pathways controlling thirst and hunger

From sensory circumventricular organs to cerebral cortex: Neural pathways controlling thirst and hunger

Morphological and neurochemical characterization of glycinergic neurons in laminae I–IV of the mouse spinal dorsal horn

Structure and Function of the Blood–Brain Barrier (BBB)

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