Skip to main content
SpringerLink
Log in

Excitatory and inhibitory responses caused by norepinephrine in duck subfornical organ neurons are mediated by β- and α 2-adrenoceptor activation

  • Original Paper
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

The responsiveness of spontaneously active neurons in the subfornical organ (SFO) of adult ducks to angiotensin II (ANGII), norepinephrine (NE), isoproterenol (Iso, β-agonist), phenylephrine (Phe, α 1-agonist) and clonidine (Clo, α 2-agonist) was investigated in brain slices with extracellular recording technique. 64% (n=90) of the neurons increased their activity after superfusion with ANGII, the rest were unresponsive. Application of NE activated 10 and inhibited 8 neurons (n=22); the excitation being correlated with an excitatory ANGII responsiveness of the same neurons and the inhibition with the absence of an ANGII responsiveness. Iso activated 74% (n=58) and Clo inhibited 88% (n=16) of the investigated neurons. Phe did not have an effect on the majority (60%) of the neurons and produced both excitatory and inhibitory actions on the remaining cells. These results offer a plausible explanation for the dose dependent dipsogenic effect of Iso and the failure of NE to elicit dose dependent drinking, which can be explained by its dual, excitatory and inhibitory effect on SFO neurons. It is further concluded, that peripherally applied Iso exerts its dipsogenic action in high concentration by a direct excitatory effect on SFO neurons via the open blood brain barrier. Under physiological conditions, afferent neuronal input of still unknown origin might specifically modulate the activity of SFO neurons, because plasma concentrations of NE are probably not high enough to activate SFO neurons from the blood side of the blood brain barrier.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

ACSF :

artificial cerebrospinal fluid

ANGII :

angiotensin II

Clo :

clonidine

Iso :

isoproterenol

NE :

norepinephrine

NTS :

nucleus of the solitary tract

Phe :

phenylephrine

SFO :

subfornical organ

References

  • Brummermann M, Simon E (1990) Arterial hypotension adapted to high salt intake. J Comp Physiol B 60: 127–137

    Google Scholar 

  • DeLuca LA Jr, Camarga LAA, Menani JV, Renzi A, Saad WA (1994) On a possible dual role for central noradrenaline in the control of hydromineral fluid intake. Brazilian J Med Biol Res 27: 905–914

    Google Scholar 

  • Fitzsimons JT, Szczepanska-Sadowska EK (1973) Drinking elicited by isoprenaline in the dog. J Physiol 223: 19–20

    Google Scholar 

  • Fregly MJ, Rowland NE, Greenleaf JE (1983) Clonidine antagonism of angiotensin-related drinking: a central site of action? Brain Res 298: 321–327

    Google Scholar 

  • Fregly MJ, Threatte RM, Barney CC, Katovich MJ (1993) Effect of acute administration of isoproterenol, angiotensin II, separately and in combination, on water intake and blood pressure of rats. Brain Res Bull 10: 327–332

    Google Scholar 

  • Houpt KA, Epstein A (1971) The clomplete dependence of beta adrenergic drinking on the renal dipsogen. Physiol Behav 7: 897–902

    Google Scholar 

  • Hudson DM, Jones DR (1982) Remarkable blood catecholamine levels in forced dived ducks. J exp Zool 224: 451–459

    Google Scholar 

  • Gerstberger R, Müller AR, Simon-Oppermann C (1992) Functional hypothalamic angiotensin II and catecholamine receptor systems inside and outside the blood-brain barrier. Progr Brain Res 91: 423–433

    Google Scholar 

  • Grossmann SP (1990) Thirst and sodium appetite. Physiological basis. Academic Press Inc, San Diego New York London

    Google Scholar 

  • LeDuarec J, Schmitt H, Lucet B (1971) Influence de la clonidine et des substances alpha sympathomimetiques sur la prise d'eau chez le rat assoiffe. J de Pharmacologie 2: 434–444

    Google Scholar 

  • Lehr D, Mallow J, Krukowski M (1967) Copious drinking and simultaneous inhibition of urine flow elicited by beta-adrenergic stimulation and the contrary effect of alpha adrenergic stimulation. J Pharmacol Exp Ther 158: 150–163

    Google Scholar 

  • Matsumura K, Simon E (1990a) Locations and properties of angiotensin II responsive neurons in the circumventricular region of the duck brain. J Physiol (Lond) 429: 281–296

    Google Scholar 

  • Matsumura K, Simon E (1990b) Increase in basal firing rate and sensitivity to angiotensin II in subfornical organ neurons of ducks adapted to salt water. J Physiol (Lond) 429: 297–308

    Google Scholar 

  • McCarty R, Kvetnansky R, Kopin IJ (1981) Plasma catecholamines in rats: Daily variations in basal levels and increments in response to stress. Physiol Behav 26: 27–31

    Google Scholar 

  • McKinley MJ, McAllen RM, Mendelsohn FAO, Allen AM, Chai SY, Oldfield BJ (1990) Circumventricular organs: neuroendocrine interfaces between the brain and the hemal milieu. Frontiers in Neuroendocrinology 11: 91–127

    Google Scholar 

  • Menani JV, Saad WA, Camargo LAA, Antunes-Rodrigues JA, Covian MR, Saad WA (1984) Effect of cholinergic and adrenergic stimulation of the subfornical organ on water intake. Pharmacol Biochem Behav 20: 301–306

    Google Scholar 

  • Oksche A, Leonhardt H, Niessing K, Scharrer E, Scharrer B, Weitzman M, Wittkowski W (1980) Handbuch der mikroskopischeAnatomie des Menschen, Band 4, Nervensystem, l0.Teil. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Phillips MI (1987) Functions of angiotensin in the central nervous system. Annu Rev Physiol 49: 413–435

    Google Scholar 

  • Raby WN, Renaud LP (1989) Dorsomedial medulla stimulation activates rat supraoptic oxytocin and vasopressin neurons through different pathways. J Physiol (Lond) 417: 279–294

    Google Scholar 

  • Rettig R, Johnson AK (1986) Aortic baroreceptor deafferentation diminishes saline induced drinking in rats. Brain Res 370: 29–37

    Google Scholar 

  • Rettig R, Ganten D, Johnson AK (1981) Isoproterenol induced thirst: renal and extrarenal mechanisms. Am J Physiol 241: R152-R157

    Google Scholar 

  • Rolls BJ, Rolls ET (1982) Thirst. Cambridge University Press, Cambridge

    Google Scholar 

  • Saad WA, Menani JV, Camargo LAA, Abrao-Saad W (1985) Interaction between cholinergic and adrenergic synapses of rat subfornical organ and the thirst-inducing effect of angiotensin II. Brazilian J Med Biol Res 18: 37–46

    Google Scholar 

  • Sawchenko PE, Swanson LW (1982) The organization of noradrenergic pathways from the brainstem to the paraventricular and supraoptic nuclei in the rat. Brain Res Rev 4: 275–325

    Google Scholar 

  • Schmid MA, Pierau Jr. K (1993) Temperature sensitivity of neurons in slices of the rat PO/AH hypothalamic area: effect of calcium. Am J Physiol 264: R440-R448

    Google Scholar 

  • Schmid HA, Simon E (1992) Effect of angiotensin II and atrial natriuretic factor on neurons in the subfornical organ of ducks and rats in vitro. Brain Res 588: 324–328

    Google Scholar 

  • Shioda S, Nakai Y (1992) Noradrenergic innervation of vasopressin-containing neurons in the rat hypothalamic supraoptic nucleus. Neurosci Lett 140: 215–218

    Google Scholar 

  • Shioya M, Tanaka J (1989) Inputs from the nucleus of the solitary tract to subfornical organ neurons projecting to the paraventricular nucleus in the rat. Neurosci Lett 483: 192–195

    Google Scholar 

  • Simon E, Gerstberger R, Gray DA (1992) Central nervous angiotensin II responsiveness in birds. In: Kerkut GA (ed) Progress in neurobiology 39. Pergamon Press, Oxford, pp 179–207

    Google Scholar 

  • Stricker EM (1977) The renin-angiotensin system and thirst: a reevaluation. II. Drinking elicited in rats by caval ligation and isoproterenol. J Comp Physiol Psychol 91: 1220–1231

    Google Scholar 

  • Summy-Long JY (1985) Biochemistry. In: Gross PM (ed) Circumventricular organs and body fluids, Vol I. CRC Press, Florida, pp 59–78

    Google Scholar 

  • Szczepanska-Sadowska EK, Fitzsimons JT (1975) The effects of angiotensin II, renin and isoprenaline on drinking in the dog. In: Peters G, Fitzsimons JT, Peters-Haefeli L (eds), Control mechanisms of drinking. Springer, New York, pp 69–73

    Google Scholar 

  • Takei Y, Kobayashi H, Yanagisawa M, Bando T (1979) Involvement of catecholaminergic nerve fibers in the angiotensin II-induced drinking in the Japanese quail, Coturnix Coturnix Japonica. Brain Res 174: 229–244

    Google Scholar 

  • Tanaka J, Seto K (1988) Neurons in the nucleus of the solitary tract with ascending projections to the subfornical organ in the rat. Neurosci Lett 89: 152–155

    Google Scholar 

  • Unnerstall JR, Kopaijtic TA, Kuhar MJ (1984) Distribution of α 2-agonist binding sites in the rat and human central nervous system: analysis of some functional, anatomic correlates of the pharmacologic effects of clonidine and related adrenergic agents. Brain Res Rev 7: 69–101

    Google Scholar 

  • Zardetto-Smith AM, Gray TS (1987) A direct neural projection from the nucleus of the solitary tract to the subfornical organ in the rat. Neurosci Lett 80: 163–166

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Max-Planck-Institut für physiologische und klinische Forschung, W.G. Kerckhoff-Institut, Parkstrasse 1, D-61231, Bad Nauheim, Germany

    H. A. Schmid, F. Schäfer, H. Sann & E. Simon

Authors
  1. H. A. Schmid
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. F. Schäfer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. H. Sann
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. E. Simon
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schmid, H.A., Schäfer, F., Sann, H. et al. Excitatory and inhibitory responses caused by norepinephrine in duck subfornical organ neurons are mediated by β- and α 2-adrenoceptor activation. J Comp Physiol A 176, 149–158 (1995). https://doi.org/10.1007/BF00239918

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00239918

Key words

Search

Navigation