Subfornical organ-supraoptic nucleus connections: An electrophysiologic study in the rat

doi:10.1016/0006-8993(84)90205-1

Brain Research

Volume 303, Issue 1, 11 June 1984, Pages 7-13

https://doi.org/10.1016/0006-8993(84)90205-1 Get rights and content

Abstract

Extracellular recordings from antidromically-identified neurosecretory cells in the rat supraoptic nucleus (SON) indicate that electrical stimulation (1 Hz, 50 μs, 200 μA) in thesubfornical organ (SFO) alters the excitability of 89% (n= 31) of phasically-active (putative vasopressin-secreting) and 94% (n= 16) of continuously-active (putative oxytocin-secreting) neurons; 45% of cells display a long latency (mean 80.2 ± 20.5 ms, S.D.) prolonged (150–350 ms) increase in excitability; 26% of cells demonstrate a similar excitation, preceded by a brief decrease in firing at a latency of 30.5 ± 13.1 ms; 15% of cells display only a depression in their activity, lasting up to 150 ms. Ninety percent of non-neurosecretory (i.e. non-antidromic) neurons (n= 19) within or above the SON also display orthodromic excitatory or inhibitory responses to SFO stimulation; however, these cells usually respond with shorter latencies, and none demonstrate the prolonged excitation seen among neurosecretory cells. WithSON stimulation, antidromic activation observed from 6 of 18 SFO neurons (latency range of 12–27 ms) confirms a projection from SFO to the SON area. These data suggest a predominantly facilitatory influence of SFO neurons on the excitability of both vasopressinergicand oxytocinergic neurosecretory cells in the rat, thereby supporting a role for the SFO in body water balance.

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Cited by (87)

The subfornical organ and organum vasculosum of the lamina terminalis: Critical roles in cardiovascular regulation and the control of fluid balance
2021, Handbook of Clinical Neurology
Citation Excerpt :
Sgro et al. subsequently carried out a study to examine the functional connectivity of such a projection. By using extracellular recordings to antidromically identify neurosecretory neurons in the SON, they demonstrated that stimulation of SFO neurons drove action potential activity in both vasopressinergic and oxytocinergic neurons by both monosynaptic and polysynaptic connections (Sgro et al., 1984). Moreover, they also demonstrated afferent connections in the SFO from the SON.
In this chapter, we review the extensive literature describing the roles of the subfornical organ (SFO), the organum vasculosum of the terminalis (OVLT), and the median preoptic nucleus (MnPO), comprising the lamina terminalis, in cardiovascular regulation and the control of fluid balance. We present this information in the context of both historical and technological developments which can effectively be overlaid upon each other. We describe intrinsic anatomy and connectivity and then discuss early work which described how circulating angiotensin II acts at the SFO to stimulate drinking and increase blood pressure. Extensive studies using direct administration and lesion approaches to highlight the roles of all regions of the lamina terminalis are then discussed. At the cellular level we describe c-Fos and electrophysiological work, which has highlighted an extensive group of circulating hormones which appear to influence the activity of specific neurons in the SFO, OVLT, and MnPO. We highlight optogenetic studies that have begun to unravel the complexities of circuitries underlying physiological outcomes, especially those related to different components of drinking. Finally, we describe the somewhat limited human literature supporting conclusions that these structures play similar and potentially important roles in human physiology.
Electrophysiological properties of rat subfornical organ neurons expressing calbindin D28K
2019, Neuroscience
Citation Excerpt :
Neurons from the sSFO and cSFO have been proposed to play different physiological roles, as dictated by their projections and receptor expression. Neurons from the sSFO project to hypothalamic sites including the supraoptic nucleus (SON), paraventricular nucleus (PVN), median preoptic nucleus and lateral hypothalamic nucleus (Miselis et al., 1979; Saper and Levisohn, 1983; Sgro et al., 1984; McKinley et al., 2003; Duan et al., 2008), which are important regulation centers for fluid and energy balance. Neurons from the cSFO project to the PVN and the rostral bed nucleus of stria terminalis (Swanson and Lind, 1986).
The subfornical organ (SFO) is forebrain sensory circumventricular organ, characterized by lack of a blood–brain barrier. Neurons of the SFO can detect circulating molecules such as peptide hormones and communicate this information to regulatory centers behind the blood–brain barrier, thus playing a critical role in homeostatic processes including regulation of energy balance, hydromineral balance and cardiovascular control. The SFO contains two subregions defined by neuronal expression of molecular markers: the dorsolateral peripheral or shell SFO (sSFO) neurons express calretinin, and the ventromedial core (cSFO) neurons express calbindin D28K. Neurons from these two subregions project to different locations to subserve different roles in homeostatic regulation. It is unknown whether neurons from these two subregions exhibit unique or identifiable electrophysiological properties. This study used a gold nanoparticle-conjugated RNA fluorescent probe on dissociated SFO neuron cultures and patch clamp electrophysiology to characterize the intrinsic electrophysiological properties of cSFO and sSFO neurons. Our studies revealed that neurons originating from the core region exhibited significantly more action potential bursting, while neurons from non-core regions exhibited more tonic firing neurons, albeit at a higher overall frequency. The difference in activity is correlated with a more depolarized resting membrane potential and a higher density of voltage gated Na⁺ currents.
Mechanosensing in hypothalamic osmosensory neurons
2017, Seminars in Cell and Developmental Biology
Citation Excerpt :
In contrast, these responses are exaggerated in SON neurons treated with jasplakinolide, a drug that promotes actin stabilization and polymerization [35,55] (Fig. 3C). Another study demonstrated that angiotensin II, an excitatory neuropeptide that is released from subfornical organ during hypovolemia [57,58] and hypotension [59] to increase VP secretion [60,61], potentiates the osmotically-induced activation of SON neurons [55]. The effect of angiotensin II is mediated by phospholipase C, and a calcium-dependent form of protein kinase C, which induce an increase in cortical actin density in osmosensory neurons.
Osmosensory neurons are specialized cells activated by increases in blood osmolality to trigger thirst, secretion of the antidiuretic hormone vasopressin, and elevated sympathetic tone during dehydration. In addition to multiple extrinsic factors modulating their activity, osmosensory neurons are intrinsically osmosensitive, as they are activated by increased osmolality in the absence of neighboring cells or synaptic contacts. This intrinsic osmosensitivity is a mechanical process associated with osmolality-induced changes in cell volume. This review summarises recent findings revealing molecular mechanisms underlying the mechanical activation of osmosensory neurons and highlighting important roles of microtubules, actin, and mechanosensitive ion channels in this process.
Availability of a rich source of sodium during the perinatal period programs the fluid balance restoration pattern in adult offspring
2012, Physiology and Behavior
Citation Excerpt :
Several studies have clearly identified mechanisms through which increases in CSF sodium concentration and circulating ANGII may exert effects on SFO excitability, and have also addressed the central pathways through which such activation controls neuroendocrine and autonomic output, such as vasopressin, oxytocin, and ACTH secretion as well as sympathetic modulation. One of the main pathways involved in these functions comprises the SFO efferent projections to the supraoptic and the paraventricular nuclei [42–47]. It seems likely, therefore, that, during the present imprinting, SFO excitability may trigger SFO-SON pathway sensitization and, when the offspring is challenged by a hypovolemic thirst model, the vasopressinergic cells are more active and in this way modulate fluid drinking secondarily.
Osmoregulatory mechanisms can be vulnerable to electrolyte and/or endocrine environmental changes during the perinatal period, differentially programming the developing offspring and affecting them even in adulthood. The aim of this study was to evaluate whether availability of hypertonic sodium solution during the perinatal period may induce a differential programming in adult offspring osmoregulatory mechanisms. With this aim, we studied water and sodium intake after Furosemide–sodium depletion in adult offspring exposed to hypertonic sodium solution from 1 week before mating until postnatal day 28 of the offspring, used as a perinatal manipulation model [PM-Na group]. In these animals, we also identified the cell population groups in brain nuclei activated by Furosemide–sodium depletion treatment, analyzing the spatial patterns of Fos and Fos–vasopressin immunoreactivity.
In sodium depleted rats, sodium and water intake were significantly lower in the PM-Na group vs. animals without access to hypertonic sodium solution [PM-Ctrol group]. Interestingly, when comparing the volumes consumed of both solutions in each PM group, our data show the expected significant differences between both solutions ingested in the PM-Ctrol group, which makes an isotonic cocktail; however, in the PM-Na group there were no significant differences in the volumes of both solutions consumed after Furosemide–sodium depletion, and therefore the sodium concentration of total fluid ingested by this group was significantly higher than that in the PM-Ctrol group.
With regard to brain Fos immunoreactivity, we observed that Furosemide–sodium depletion in the PM-Na group induced a higher number of activated cells in the subfornical organ, ventral subdivision of the paraventricular nucleus and vasopressinergic neurons of the supraoptic nucleus than in the PM-Ctrol animals. Moreover, along the brainstem, we found a decreased number of sodium depletion-activated cells within the nucleus of the solitary tract of the PM-Na group.
Our data indicate that early sodium availability induces a long-term effect on fluid drinking and on the cell activity of brain nuclei involved in the control of hydromineral balance. These results also suggest that availability of a rich source of sodium during the perinatal period may provoke a larger anticipatory response in the offspring, activating the vasopressinergic system and reducing thirst after water and sodium depletion, as a result of central osmosensitive mechanism alterations.
Circumventricular Organs
2012, The Human Nervous System, Third Edition
Osmosensation in vasopressin neurons: changing actin density to optimize function
2010, Trends in Neurosciences
Citation Excerpt :
Previous studies have shown that neurons in the subfornical organ (SFO) are excited during hypovolemia [72,73] and hypotension [74]. SFO neurons project axons onto MNCs [75,76], where they might contribute to the potentiation of osmotically-evoked action potential firing and VP release in the neurohypophysis [77,78]. A body of evidence indicates that SFO neurons contain angiotensin II (Ang II) [74,76] and that the release of this peptide can lead to excitation of MNCs [78,79], as well as an increase in the osmotic activation of MNCs [47,80,81].
The proportional relation between circulating vasopressin concentration and plasma osmolality is fundamental for body fluid homeostasis. Although changes in the sensitivity of this relation are associated with pathophysiological conditions, central mechanisms modulating osmoregulatory gain are unknown. Here, we review recent data that sheds important light on this process. The cell autonomous osmosensitivity of vasopressin neurons depends on cation channels comprising a variant of the transient receptor potential vanilloid 1 (TRPV1) channel. Hyperosmotic activation is mediated by a mechanical process where sensitivity increases in proportion with actin filament density. Moreover, angiotensin II amplifies osmotic activation by a rapid stimulation of actin polymerization, suggesting that neurotransmitter-induced changes in cytoskeletal organization in osmosensory neurons can mediate central changes in osmoregulatory gain.

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Subfornical organ-supraoptic nucleus connections: An electrophysiologic study in the rat

Abstract

Brain Research

Brain Research

Brain Research

Brain Research

Neuroscience

Brain Research

Brain Research

Brain Research

Brain Research

Neurosci. Lett.

Characterization of the responses of oxytocin- and vasopressin-secreting neurones in the supraoptic nucleus to osmotic stimulation

J. Physiol. (Lond.)

Subfornical organ: a dypsogenic site of action of angiotensin II

Science

The neuronal organization of the rat subfornical organ in vitro and a test of the osmo- and morphine-receptor hypothesis

J. Physiol. (Lond.)