New Aspects of Firing Pattern Autocontrol in Oxytocin and Vasopressin Neurones

Moos, Françoise; Gouzènes, Laurent; Brown, David W.; Dayanithi, Govindan; Sabatier, Nancy; Boissin, L.; Rabié, A.; Richard, Ph.

doi:10.1007/978-1-4615-4871-3_18

Cited by 49 publications

(36 citation statements)

References 26 publications

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“…AVP secretion could be excluded, as retrodialysis of the AVP V1 receptor antagonist into the SON did not alter plasma AVP concentrations, which is in line with recent observations (62). Somato-dendritically released AVP was shown to activate quiescent AVP cells (10,21,40). In contrast to AVP secretion under resting conditions, the stress-induced secretion of AVP into blood was not found to be further enhanced after local blockade of OXT receptor-mediated actions.…”

Section: Discussionsupporting

confidence: 86%

“…Administration of a selective OXT-A directly into the SON of conscious male rats via reversed microdialysis increased AVP secretion into blood under basal conditions, indicating an inhibitory tone of intra-SON released OXT upon AVP neurons projecting to the neurohypophysis in the conscious rat. This is surprising as electrophysiological studies failed to demonstrate OXT actions on AVP cells within the hypothalamic magnocellular nuclei in vitro (10,27,40). A negative feedback effect of locally released AVP on peripheral Fig.…”

Section: Discussionmentioning

confidence: 99%

“…Forced swimming represents an ethologically relevant combined physical and emotional stressor for rats (1) shown to increase plasma ACTH and corticosterone after an exposure time of either 60 s or longer (21,40,45,62), and AVP and OXT release within the SON and PVN after an exposure time of 10 min (58,62). With the microdialysis tubing and the extension tubing of the venous catheter still attached, rats were forced to swim for 60 s in a clear plastic cylinder (30 cm in diameter and 70 cm in height) filled with tap water (21°C) to a depth of ϳ60 cm.…”

Section: Forced Swimmingmentioning

confidence: 99%

“…Here, we want to test the hypothesis that OXT locally released within the SON/PVN is another candidate involved in the control of the somato-dendritic and neurohypophyseal release of AVP under both basal and/or stress conditions. Although electrophysiological studies indicate that OXT predominantly acts on OXT, but not AVP, neurons within the SON or PVN in an autocrineparacrine fashion (10,18,21,27,40), evidence from conscious animals under conditions of psychological stress is lacking.The stress response of the organism is characterized not only by an activation of the OXT/AVP system, but mainly by stimulation of the hypothalamo-pituitary-adrenal (HPA) axis, as well as the sympathetic nervous system. Brain OXT has been shown to generally inhibit the activity of the HPA axis.…”

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confidence: 99%

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Oxytocin actions within the supraoptic and paraventricular nuclei: differential effects on peripheral and intranuclear vasopressin release

Neumann¹,

Torner²,

Toschi³

et al. 2006

American Journal of Physiology-Regulatory, Integrative and Comp

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(FS), AVP is released somato-dendritically within the supraoptic nucleus (SON) and paraventricular nucleus (PVN), but not from neurohypophyseal terminals into blood. Together with AVP, oxytocin (OXT) is released within the SON and PVN. Here, we studied the role of intra-SON and intra-PVN OXT in the regulation of local AVP release and into the blood in male rats. Within the SON, bilateral retrodialysis of an OXT receptor antagonist (OXT-A) increased local AVP release in response to FS [60 s, 21°C, vehicle twofold, not significant (ns); OXT-A: 15-fold increase, P Ͻ 0.05] without significantly affecting basal AVP release. In addition, local OXT-A elevated plasma AVP secretion under basal conditions (twofold increase, P Ͻ 0.05) without further elevation after FS. Within the PVN, exposure to FS elevated local AVP release, reaching significance only in the OXT-A group (vehicle: 1.4-fold, ns; OXT-A: 1.6-fold increase, P ϭ 0.050). Bilateral OXT-A into the PVN did not affect peripheral AVP secretion either under basal or stress conditions. Basal ACTH concentrations tended to be elevated by local OXT-A within the PVN (1.7-fold increase, P ϭ 0.076). In contrast, the swim-induced ACTH secretion was attenuated after retrodialysis of OXT-A within both the SON (at 5 min) and PVN (at 15 min) (P Ͻ 0.05 both) compared with vehicle. The results demonstrate a receptormediated effect of OXT within the SON and PVN on local and neurohypophyseal AVP release, which depends upon the activity conditions. Further, while exerting an inhibitory effect on hypothalamo-pituitary-adrenal axis activity under basal conditions, hypothalamic OXT is essential for an adequate acute ACTH response.plasma; hypothalamo-pituitary-adrenal axis; dendritic release; microdialysis; swim stress THE NEUROPEPTIDES OXYTOCIN (OXT) and AVP are mainly synthesized in magnocellular neurons of the hypothalamic supraoptic nucleus (SON) and the paraventricular nucleus (PVN). They are released from neurohypophyseal axon terminals directly into the systemic circulation, but also in a somatodendritic fashion within the hypothalamus in response to relevant physiological stimuli, including parturition, suckling, osmotic challenge, and hemorrhage (for a review, see Ref. 33).Similarly, such local release within the SON and PVN has been described for both peptides, for instance, in response to various psychological stressors, such as forced swimming in male and female rats (for a review, see Ref. 16). However, upon stressor exposure, only OXT is simultaneously released from the dendrites within the hypothalamic nuclei and from neurohypophyseal terminals into blood, as revealed by intracerebral microdialysis in conjunction with blood sampling in conscious rats. In contrast, AVP secretion into blood remains unchanged despite its release within the PVN, SON, and/or septum, for example, during forced swimming or exposure to social defeat (13,14,44,60,61).The phenomenon of independent release patterns of AVP from dendrites within the SON/PVN and from neurohypophyseal terminals, in par...

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Section: Discussionsupporting

confidence: 86%

Section: Discussionmentioning

confidence: 99%

Section: Forced Swimmingmentioning

confidence: 99%

mentioning

confidence: 99%

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Oxytocin actions within the supraoptic and paraventricular nuclei: differential effects on peripheral and intranuclear vasopressin release

Neumann¹,

Torner²,

Toschi³

et al. 2006

American Journal of Physiology-Regulatory, Integrative and Comp

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“…A recent study demonstrated that the V 2 -like receptor mediates the ability of somatodendritically released VP to facilitate cell volume regulation in VP neurons (56). In addition, somato-dendritic release of VP is known to modulate electrical activity of VP neurons primarily via the V 1a receptor (15,40,43,44). Nevertheless, the presence of V 2 -like receptors on VP neurons implies the possibility that the ␤-and ␥-subunits in VP neurons could be regulated by somatodendritic release of VP by mechanisms similar to their regulation in the nephron.…”

Section: Discussionmentioning

confidence: 99%

Epithelial Na⁺ sodium channels in magnocellular cells of the rat supraoptic and paraventricular nuclei

Teruyama

Sakuraba

Wilson

et al. 2012

American Journal of Physiology-Endocrinology and Metabolism

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Teruyama R, Sakuraba M, Wilson LL, Wandrey NE, Armstrong WE. Epithelial Na ϩ sodium channels in magnocellular cells of the rat supraoptic and paraventricular nuclei. Am J Physiol Endocrinol Metab 302: E273-E285, 2012. First published November 1, 2011; doi:10.1152/ajpendo.00407.2011.-The epithelial Na ϩ channels (ENaCs) are present in kidney and contribute to Na ϩ and water homeostasis. All three ENaC subunits (␣, ␤, and ␥) were demonstrated in the cardiovascular regulatory centers of the rat brain, including the magnocellular neurons (MNCs) in the supraoptic nucleus (SON) and the paraventricular nucleus (PVN). However, the functional significance of ENaCs in vasopressin (VP) and oxytocin (OT) synthesizing MNCs is completely unknown. In this study, we show with immunocytochemical double-labeling that the ␣-ENaC is colocalized with either VP or OT in MNCs in the SON and PVN. In addition, parvocellular neurons in the dorsal, ventrolateral, and posterior subregions of the PVN (not immunoreactive to VP or OT) are also immunoreactive for ␣-ENaC. In contrast, immunoreactivity to ␤-and ␥-ENaC is colocalized with VP alone within the MNCs. Furthermore, immunoreactivity for a known target for ENaC expression, the mineralcorticoid receptor (MR), is colocalized with both VP and OT in MNCs. Using single-cell RT-PCR, we detected mRNA for all three ENaC subunits and MR in cDNA libraries derived from single MNCs. In whole cell voltage clamp recordings, application of the ENaC blocker benzamil reversibly reduced a steady-state inward current and decreased cell membrane conductance approximately twofold. Finally, benzamil caused membrane hyperpolarization in a majority of VP and about one-half of OT neurons in both spontaneously firing and quiet cells. These results strongly suggest the presence of functional ENaCs that may affect the firing patterns of MNCs, which ultimately control the secretion of VP and OT. aldodsterone; vasopressin; oxytocin THE NEUROHYPOPHYSIAL HORMONES vasopressin (VP) and oxytocin (OT) are synthesized in the magnocellular neurons (MNCs) located within the paraventricular nucleus (PVN) and the supraoptic nucleus (SON) of the hypothalamus and released from the neurohypophysis into the general circulation in response to physiological demands. The secretion of VP increases in response to hyperosmolality, hypovolemia, and hypotension and produces antidiuretic and pressor effects (59). In addition to the well-known effects of OT during parturition and lactation, plasma OT also increases with hyperosmolality and hypernatremia (32) and induces natriuresis (13, 31).The non-voltage-dependent, amiloride-sensitive epithelial Na ϩ channels (ENaCs) are present in the apical membrane of epithelial cells in a variety of tissues, such as urinary bladder, renal collecting duct, distal colon, sweat and salivary glands, lung, and taste buds, and are known to mediate the transport of Na ϩ across epithelia (7, 21). Thus, together with the Na ϩ /K ϩ -ATPase present in the basal membrane of epithelial cells, ENaCs regulate transe...

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Magnocellular Neurons and Posterior Pituitary Function

Brown

2016

Comprehensive Physiology

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The posterior pituitary gland secretes oxytocin and vasopressin (the antidiuretic hormone) into the blood system. Oxytocin is required for normal delivery of the young and for delivery of milk to the young during lactation. Vasopressin increases water reabsorption in the kidney to maintain body fluid balance and causes vasoconstriction to increase blood pressure. Oxytocin and vasopressin secretion occurs from the axon terminals of magnocellular neurons whose cell bodies are principally found in the hypothalamic supraoptic nucleus and paraventricular nucleus. The physiological functions of oxytocin and vasopressin depend on their secretion, which is principally determined by the pattern of action potentials initiated at the cell bodies. Appropriate secretion of oxytocin and vasopressin to meet the challenges of changing physiological conditions relies mainly on integration of afferent information on reproductive, osmotic, and cardiovascular status with local regulation of magnocellular neurons by glia as well as intrinsic regulation by the magnocellular neurons themselves. This review focuses on the control of magnocellular neuron activity with a particular emphasis on their regulation by reproductive function, body fluid balance, and cardiovascular status. © 2016 American Physiological Society. Compr Physiol 6:1701-1741, 2016.

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New Aspects of Firing Pattern Autocontrol in Oxytocin and Vasopressin Neurones

Cited by 49 publications

References 26 publications

Oxytocin actions within the supraoptic and paraventricular nuclei: differential effects on peripheral and intranuclear vasopressin release

Oxytocin actions within the supraoptic and paraventricular nuclei: differential effects on peripheral and intranuclear vasopressin release

Epithelial Na⁺ sodium channels in magnocellular cells of the rat supraoptic and paraventricular nuclei

Magnocellular Neurons and Posterior Pituitary Function

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New Aspects of Firing Pattern Autocontrol in Oxytocin and Vasopressin Neurones

Cited by 49 publications

References 26 publications

Oxytocin actions within the supraoptic and paraventricular nuclei: differential effects on peripheral and intranuclear vasopressin release

Oxytocin actions within the supraoptic and paraventricular nuclei: differential effects on peripheral and intranuclear vasopressin release

Epithelial Na+ sodium channels in magnocellular cells of the rat supraoptic and paraventricular nuclei

Magnocellular Neurons and Posterior Pituitary Function

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Epithelial Na⁺ sodium channels in magnocellular cells of the rat supraoptic and paraventricular nuclei