The Supraoptic Nucleus as an Osmoreceptor

Leng, Gareth; Mason, William T.; Dyer, R. G.

doi:10.1159/000123280

Cited by 131 publications

(44 citation statements)

References 51 publications

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“…*P Ͻ 0.05 vs. isotonic NaCl; #P Ͻ 0.05 vs. hyperosmotic NaCl. (3,4,21,23,34,45), SON and PVN receive input from osmoreceptors in CVOs (18,28,33,40), and a disconnection of one CVO, the SFO, greatly reduces Fos expression in the SON and PVN after hyperosmotic intragastric loads (11,38). Thus, cells in the hypothalamus are activated both by native osmoreceptors and by afferents from the CVOs after hyperosmotic NaCl infusion.…”

Section: Discussionmentioning

confidence: 99%

Differential effects of intravenous hyperosmotic solutes on drinking latency and c-Fos expression in the circumventricular organs and hypothalamus of the rat

Ho¹,

Zierath²,

Savos³

et al. 2007

American Journal of Physiology-Regulatory, Integrative and Comp

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December 28, 2006; doi:10.1152/ajpregu.00547.2006.-Hyperosmotic intravenous infusions of NaCl are more potent for inducing drinking and vasopressin (AVP) secretion than equally osmotic solutions of glucose or urea. The fact that all three solutes increased cerebrospinal fluid osmolality and sodium concentration led the investigators to conclude that critical sodium receptors or osmoreceptors for stimulating drinking and AVP secretion were outside the blood-brain barrier (BBB) in the circumventricular organs (CVOs). We tested an obvious prediction of this hypothesis: that all three solutes should increase c-Fos-like immunoreactivity (Fos-ir) inside the BBB, but that only NaCl should increase Fos-ir in the CVOs. We gave intravenous infusions of 3.0 Osm/l NaCl, glucose, or urea to rats for 11 or 22 min at 0.14 ml/min and perfused the rats for assay of Fos-ir at 90 min. Controls received isotonic NaCl at the same volume. Drinking latency was measured, but water was then removed. Drinking consistently occurred with short latency during hyperosmotic NaCl infusions only. Fos-ir in the forebrain CVOs, the subfornical organ, and organum vasculosum laminae terminalis was consistently elevated only by hyperosmotic NaCl. However, all three hyperosmotic solutes potently stimulated Fos-ir in the supraoptic and paraventricular nuclei of the hypothalamus inside the BBB. Hyperosmotic NaCl greatly elevated Fos-ir in the area postrema, but even glucose and urea caused moderate elevations that may be related to volume expansion rather than osmolality. The data provide strong support for the conclusion that the osmoreceptors controlling drinking are located in the CVOs. area postrema; c-Fos; drinking; hypernatremia; organum vasculosum laminae terminalis; osmoreceptors; paraventricular nucleus of the hypothalamus; subfornical organ; supraoptic nucleus THE BRAIN AREAS THAT CONTAIN electrophysiologically defined osmoreceptive cells that function in the regulation of fluid and electrolyte balance include the circumventricular organs (CVOs), the median preoptic nucleus (MnPO), the hypothalamic supraoptic and paraventricular nuclei (SON and PVN), and the nucleus of the solitary tract (1,17,18,33,34,40,43). These areas are intricately interconnected by neural pathways into a network subserving fluid balance as originally described by Miselis (29). Candidate mechanisms for osmoreceptors have been identified among aquaporins, the vanilloid family of transient receptor potential channels, and mechanical gating of sodium currents (3,22,44,45). However, electrophysiological studies in single neurons or brain slices do little to differentiate which osmoreceptors are more important for functions such as AVP secretion or drinking.The concept that the critical osmoreceptors for these functions are located in the CVOs and in the peripheral nervous system stems from three influential studies that demonstrated drinking in sheep, dogs, and rats was elicited by intravenous hyperosmotic NaCl or sucrose but not by urea or glucose (8,26,41). The generally...

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Section: Discussionmentioning

confidence: 99%

Differential effects of intravenous hyperosmotic solutes on drinking latency and c-Fos expression in the circumventricular organs and hypothalamus of the rat

Ho¹,

Zierath²,

Savos³

et al. 2007

American Journal of Physiology-Regulatory, Integrative and Comp

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“…In a previous study, glutamate microstimulation of a region near here-dorsal to the SON and ϳ400 m rostral to the SON rx site-elicited an excitatory synaptic response in magnocellular neurons of the principal SON (6). It was also reported that this perinuclear zone receives collateral projections from SON magnocellular neurons (24,27) and that this area may provide recurrent feedback (16) via glutamatergic inputs to the SON (6,56). If the perinuclear zone is contiguous with the SON rx , as appears likely, then those findings combined with the findings presented here suggest that the SON rx -dorsochiasmatic area may provide glutamatergic synaptic inputs to magnocellular neurons of both the SON and PVN.…”

Section: Fig 7 Immunohistochemical Identification Of Responsive Pvnmentioning

confidence: 93%

Internuclear coupling of hypothalamic magnocellular nuclei by glutamate synaptic circuits

Boudaba¹,

Tasker²

2006

American Journal of Physiology-Regulatory, Integrative and Comp

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Magnocellular neurons of the supraoptic nucleus (SON) and paraventricular nucleus (PVN) display bursting activity that is synchronized under certain conditions. They receive excitatory synaptic inputs from intrahypothalamic glutamate circuits, some of which are activated by norepinephrine. Ascending noradrenergic afferents and intrahypothalamic glutamate circuits may be responsible for the generation of synchronous bursting among oxytocin neurons and/or asynchronous bursting among vasopressin neurons located in the bilateral supraoptic and paraventricular nuclei. Here, we tested whether magnocellular neurons of the PVN receive excitatory synaptic input from the contralateral PVN and the region of the retrochiasmatic SON (SONrx) via norepinephrine-sensitive internuclear glutamate circuits. Whole cell patch-clamp recordings were performed in PVN magnocellular neurons in coronal hypothalamic slices from male rats, and the ipsilateral SONrx region and contralateral PVN were stimulated using electrical and chemical stimulation. Electrical and glutamate microdrop stimulation of the ipsilateral SONrx region or contralateral PVN elicited excitatory postsynaptic potentials/currents (EPSP/Cs) in PVN magnocellular neurons mediated by glutamate release, revealing internuclear glutamatergic circuits. Microdrop application of norepinephrine also elicited EPSP/Cs, suggesting that these circuits could be activated by activation of noradrenergic receptors. Repetitive electrical stimulation and drop application of norepinephrine, in some cases, elicited bursts of action potentials. Our data reveal glutamatergic synaptic circuits that interconnect the magnocellular nuclei and that can be activated by norepinephrine. These internuclear glutamatergic circuits may provide the functional architecture to support burst generation and/or burst synchronization in hypothalamic magnocellular neurons under conditions of activation. supraoptic nucleus; paraventricular nucleus; oxytocin; vasopressin; excitatory postsynaptic currents; excitatory postsynaptic potentials MAGNOCELLULAR NEURONS of the hypothalamic supraoptic nucleus (SON) and paraventricular nucleus (PVN) release either of the two hormones, vasopressin and oxytocin, directly into the bloodstream from their axon terminals located in the neurohypophysis. Under a variety of physiological conditions (e.g., dehydration, hypovolemia, lactation), these neurons display bursting activities that produce a large increase in the circulating concentrations of oxytocin and vasopressin. There is considerable evidence to suggest that glutamate plays an important role in the generation of bursts in these neurons. Glutamatergic terminals are abundant on hypothalamic magnocellular neurons (20) and glutamate is responsible for the fast excitatory synaptic input to the magnocellular neurons (54, 57). Glutamate appears to be essential for the onset and maintenance of bursting activity in both vasopressin and oxytocin neurons in vitro (18, 21) and in vivo (31,35,36). Glutamate circuits also carry informa...

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“…However, if those neurons are also receiving extensive afferent input, then even a small tonic depolarisation becomes effective, because it increases the probability that depolarisations that arise from afferent input will exceed spike threshold. Thus, although the magnocellular neurons are osmoreceptors, when they are deafferented, they cannot increase their firing rates in response to osmotic stimulation -this response requires at least a tonic afferent input (Leng et al 1982). They get such a tonic input from a set of anterior brain structures that includes two circumventricular organs -the subfornical organ and the organum vasculosum of the laminae terminalis -that are also osmoreceptive in the same way that magnocellular neurons are (Bourque 2008).…”

Section: Vasopressin Secretionmentioning

confidence: 99%

60 YEARS OF NEUROENDOCRINOLOGY: The posterior pituitary, from Geoffrey Harris to our present understanding

Leng¹,

Pineda²,

Sabatier³

et al. 2015

Journal of Endocrinology

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Geoffrey Harris pioneered our understanding of the posterior pituitary, mainly with experiments that involved the electrical stimulation of the supraoptico-hypophysial tract. In the present essay, we explain how his observations included clues to the pulsatile nature of the oxytocin signal -clues that were followed up by subsequent workers, including his students and their students. These studies ultimately led to our present understanding of the milk-ejection reflex and of the role of oxytocin in parturition. Discoveries of wide significance followed, including: the recognition of the importance of pulsatile hormone secretion; the recognition of the importance of stimulus-secretion coupling mechanisms in interpreting the patterned electrical activity of neurons; the physiological importance of peptide release in the brain; the recognition that peptide release comes substantially from dendrites and can be regulated independently of nerve terminal secretion; and the importance of dynamic morphological changes to neuronal function in the hypothalamus. All of these discoveries followed from the drive to understand the milk-ejection reflex. We also reflect on Harris's observations on vasopressin secretion, on the effects of stress, and on oxytocin secretion during sexual activity.

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The Supraoptic Nucleus as an Osmoreceptor

Cited by 131 publications

References 51 publications

Differential effects of intravenous hyperosmotic solutes on drinking latency and c-Fos expression in the circumventricular organs and hypothalamus of the rat

Differential effects of intravenous hyperosmotic solutes on drinking latency and c-Fos expression in the circumventricular organs and hypothalamus of the rat

Internuclear coupling of hypothalamic magnocellular nuclei by glutamate synaptic circuits

60 YEARS OF NEUROENDOCRINOLOGY: The posterior pituitary, from Geoffrey Harris to our present understanding

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