Electrophysiological and Immunocytochemical Evidence for a cGMP-Mediated Inhibition of Subfornical Organ Neurons by Nitric Oxide

Rauch, Matthias; Schmid, Herbert; deVente, Jan; Simón, E.

doi:10.1523/jneurosci.17-01-00363.1997

Cited by 38 publications

(34 citation statements)

References 32 publications

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“…Several investigators have shown that Ang II can directly stimulate neurons in the SFO (19,25), and we have observed that the great majority of these neurons were also stimulated by relaxin in the perfusion medium. We have not made such recordings from the isolated OVLT, but in view of the relaxin binding present in this site (10), to which circulating relaxin should have access, it seems likely that relaxin also acts directly on neurons in the OVLT to stimulate neuronal activity there.…”

Section: Discussionmentioning

confidence: 50%

“…Temperature was held constant at 37°C by a Peltier element. Extracellular recordings were made from SFO neurons by using glass-coated platinum-iridium electrodes as described (19). The SFO could be identified easily by its protrusion into the third ventricle and the lateral blood vessels lining the organ on both sides.…”

Section: Immunohistochemical Detection Of Fos In Rat Brain Resulting mentioning

confidence: 99%

“…After a stable recording from a single spontaneously active neuron was obtained, its responsiveness to Ang II was tested by switching to a perfusion solution containing Ang II at 10 Ϫ7 M. The recorded action potentials were amplified and displayed on a storage oscilloscope (Gould, Erlensee, Germany) and, after passing a window discriminator (World Precision Instruments, Sarasota, FL), were analyzed with custom-made software (SPIKE 2, Cambridge Electronic Design, Cambridge, U.K.) on a computer. The concentration of Ang II (10 Ϫ7 M) was chosen according to published experiments (19), which showed that this concentration produced clearly visible responses with minimum desensitization. From the continuously recorded rate meter counts, the average discharge rate of each neuron was evaluated for 60 sec before the stimulus.…”

Section: Immunohistochemical Detection Of Fos In Rat Brain Resulting mentioning

confidence: 99%

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Circulating relaxin acts on subfornical organ neurons to stimulate water drinking in the rat

Sunn

Egli

Burazin

et al. 2002

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

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Relaxin, a peptide hormone secreted by the corpus luteum during pregnancy, exerts actions on reproductive tissues such as the pubic symphysis, uterus, and cervix. It may also influence body fluid balance by actions on the brain to stimulate thirst and vasopressin secretion. We mapped the sites in the brain that are activated by i.v. infusion of a dipsogenic dose of relaxin (25 g͞h) by immunohistochemically detecting Fos expression. Relaxin administration resulted in increased Fos expression in the subfornical organ (SFO), organum vasculosum of the lamina terminalis (OVLT), median preoptic nucleus, and magnocellular neurons in the supraoptic and paraventricular nuclei. Ablation of the SFO abolished relaxininduced water drinking, but did not prevent increased Fos expression in the OVLT, supraoptic or paraventricular nuclei. Although ablation of the OVLT did not inhibit relaxin-induced drinking, it did cause a large reduction in Fos expression in the supraoptic nucleus and posterior magnocellular subdivision of the paraventricular nucleus. In vitro single-unit recording of electrical activity of neurons in isolated slices of the SFO showed that relaxin (10 ؊7 M) added to the perfusion medium caused marked and prolonged increase in neuronal activity. Most of these neurons also responded to 10 ؊7 M angiotensin II. The data indicate that bloodborne relaxin can directly stimulate neurons in the SFO to initiate water drinking. It is likely that circulating relaxin also stimulates neurons in the OVLT that influence vasopressin secretion. These two circumventricular organs that lack a blood-brain barrier may have regulatory influences on fluid balance during pregnancy in rats.R elaxin is a peptide hormone secreted by the corpus luteum of the ovary during pregnancy. Relaxin acts on reproductive tissues such as the pubic symphysis, uterus, and cervix (1, 2), but it may also influence the brain (3). Evidence of this influence is presented in reports that the intracerebroventricular (i.c.v.) (1) injection of relaxin results in stimulation of oxytocin and vasopressin secretion, water drinking, and a pressor response (3-8). i.c.v. administration of relaxin also stimulates increased expression of c-fos in groups of neurons in the supraoptic nucleus (SON) and hypothalamic paraventricular nucleus (PVN), as well as in the subfornical organ (SFO), median preoptic nucleus (MnPO), and organum vasculosum of the lamina terminalis (OVLT) (9). Circulating relaxin probably has endocrine actions on the brain, because high-affinity-binding sites for relaxin are present in the SFO and OVLT of the rat (10), two brain regions that are accessible to circulating relaxin because they lack a blood-brain barrier (11). Also, i.v. infusion of relaxin causes vasopressin secretion and water drinking in the rat, effects that may be mediated through brain angiotensinergic mechanisms (12,13). Evidence that relaxin [together with other hormones such as angiotensin II (Ang II) and vasopressin] plays a physiological role in regulating body fluid homeostasis d...

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Section: Discussionmentioning

confidence: 50%

Section: Immunohistochemical Detection Of Fos In Rat Brain Resulting mentioning

confidence: 99%

Section: Immunohistochemical Detection Of Fos In Rat Brain Resulting mentioning

confidence: 99%

See 1 more Smart Citation

Circulating relaxin acts on subfornical organ neurons to stimulate water drinking in the rat

Sunn

Egli

Burazin

et al. 2002

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

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“…Conversely, it has been shown that direct application of the NO-donor sodium nitroprusside (SNP) reduces AngII-induced water-intake (Nicolaidis and Fitzsimons, 1975) and inhibits the majority of AngII-sensitive SFO-neurons in an in vitro slice preparation (Rauch et al, 1997). Endogenous NO, which is produced by the neuronal NO-synthase (NOS) and released within the SFO (Jurzak et al, 1994b;Rauch et al, 1997) exerts its inhibitory effect most likely by stimulating the soluble guanylyl-cyclase, as indicated by the increase in cGMP after stimulation with different NO-donors and by the inhibitory effect of mem-brane-permeable 8Br-cGMP on neuronal activity (Rauch et al, 1997).…”

Section: Introductionmentioning

confidence: 99%

Effect of glutamate and angiotensin II on whole cell currents and release of nitric oxide in the rat subfornical organ

Schmid

1998

Amino Acids

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Blood-borne angiotensin II (AngII) is known to mediate water-intake by its excitatory effect on neurons in the subfornical organ (SFO). Conversely, nitric oxide (NO) has exclusively inhibitory effects on rat SFO-neurons and on SFO-mediated water-intake. Extracellular and patch-clamp recordings from freshly dissociated rat SFO-neurons showed that glutamate activates AngII-sensitive SFO-neurons by opening ligand-gated cation channels. An immunocytochemical study showed that activation of glutamate receptors increased the concentration of the inhibitory second messenger cGMP in the SFO. A model is proposed suggesting that NO protects SFO-neurons from overexcitability by excitatory neurotransmitters.

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“…NO may play one or more different roles in such neurons. In many spontaneously-firing neuron types, NO may directly modulate firing rate [Pehl and Schmid, 1997;Rauch et al, 1997;Kobayashi et al, 2000;Smith and Otis, 2003]. Another possible role is in protecting rapidly firing neurons from damage due to hyperactivity.…”

Section: Discussionmentioning

confidence: 99%

L-Citrulline Immunoreactivity Reveals Nitric Oxide Production in the Electromotor and Electrosensory Systems of the Weakly Electric Fish, <i>Apteronotus leptorhynchus</i>

Smith

Allen²,

Oestreich³

et al. 2004

Brain Behav Evol

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Weakly electric fish produce electric organ discharges (EODs) used for electrolocation and communication. In the brown ghost knifefish, Apteronotus leptorhynchus, several neuron types in brain regions that control the EOD or process electrosensory information express nitric oxide synthase (NOS). The present study used immunoreactivity for L-citrulline, a byproduct of the production of nitric oxide (NO) by NOS, to assess NO production in NOS-expressing neurons. A polyclonal antibody against L-citrulline produced specific labeling in most neuronal populations previously identified to express NOS. Specifically, several cell types that precisely encode temporal information and/or fire at high frequencies, including spherical cells in the electrosensory lateral line lobe, giant cells in layer VI of the dorsal torus semicircularis, and pacemaker and relay cells in the pacemaker nucleus, were strongly immunoreactive for L-citrulline. This suggests that these neurons produced high levels of NO. Notably, electromotor neurons, which also strongly express NOS, were not immunoreactive for L-citrulline, suggesting that NOS did not produce high levels of NO in these neurons. No apparent differences in L-citrulline distribution or intensity were observed between socially isolated fish and fish exposed to playback stimuli simulating the presence of a conspecific. This suggests that social stimulation by electrocommunication signals is not necessary for high levels of NO production in many NOS-positive neurons. Future studies focusing on regulation of NO production in these systems, and the effects of NO on electrosensory processing and electromotor pattern generation will help elucidate the function of NO signaling pathways in this system.

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Electrophysiological and Immunocytochemical Evidence for a cGMP-Mediated Inhibition of Subfornical Organ Neurons by Nitric Oxide

Cited by 38 publications

References 32 publications

Circulating relaxin acts on subfornical organ neurons to stimulate water drinking in the rat

Circulating relaxin acts on subfornical organ neurons to stimulate water drinking in the rat

Effect of glutamate and angiotensin II on whole cell currents and release of nitric oxide in the rat subfornical organ

L-Citrulline Immunoreactivity Reveals Nitric Oxide Production in the Electromotor and Electrosensory Systems of the Weakly Electric Fish, <i>Apteronotus leptorhynchus</i>

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