Skip to main content
SpringerLink
Log in

Effects of angiotensin II on the spontaneous activity of rostral ventrolateral medullary cardiovascular neurons and blood pressure in spontaneously hypertensive rats

  • Original Paper
  • Published:
Journal of Biomedical Science

Abstract

The interactive role of rostral ventrolateral medulla (RVL) cardiovascular neurons and brain angiotensin II (Ang II) in regulating the arterial blood pressure was examined by recording simultaneously the spontaneous activity of these spinal projecting neurons and the arterial blood pressure in the pentobarbital-anesthetized spontaneously hypertensive rat (SHR) and its normotensive control, the Wistar Kyoto rat (WKY). It was found that Ang II elicited dose-dependent excitatory responses in a subpopulation of RVL cardiovascular neurons, followed by a subsequent increase in blood pressure. These effects of Ang II were significantly greater in SHR than in WKY. The effects were attenuated or abolished by co-administration of Ang II antagonist, [Sar1, Ile8]-Ang II. Pre-administration of [Sar1, Ile8]-Ang II to RVL using bilateral microinjection attenuated the blood pressure effects of intracerebroventricularly administered Ang II by as much as 70%. These results indicated that spinal projecting RVL cardiovascular neurons are important in mediating the pressor action of Ang II. The enhanced sensitivity and responsiveness of RVL cardiovascular neurons to Ang II may be pertinent to the genesis of hypertension in adult SHR.

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

References

  1. Allen AM, Dampney RAL, Mendelsohn FAO. Angiotensin receptor binding and pressor effects in the cat subretrofacial nucleus. Am J Physiol 255:H1011-H1017;1988.

    PubMed  Google Scholar 

  2. Bruner CA, Fink GD. Neurohumoral contributions to chronic angiotensin-induced hypertension. Am J Physiol 250:H52-H61;1986.

    PubMed  Google Scholar 

  3. Calaresu FR, Yardley CP. Medullary basal sympathetic tone. Ann Rev Physiol 50:511–524;1988.

    Article  Google Scholar 

  4. Chan RKW, Chan YS, Wong TM. Cardiovascular responses to electrical stimulation of the ventrolateral medulla of the spontaneously hypertensive rat. Brain Res 522:99–106;1990.

    Article  PubMed  Google Scholar 

  5. Chan RKW, Chan YS, Wong TM. Electrophysiological properties of neurons in the rostral ventrolateral medulla of normotensive and spontaneously hypertensive rats. Brain Res 549:118–126;1991.

    Article  PubMed  Google Scholar 

  6. Chan RKW, Chan YS, Wong TM. Responses of cardiovascular neurons in the rostral ventrolateral medulla of the normotensive Wistar Kyoto and spontaneously hypertensive rats to iontophoretic application of angiotensin II. Brain Res 556:145–150;1991.

    Article  PubMed  Google Scholar 

  7. Chan RKW, Chan YS, Wong TM. Effects of chronic captopril treatment on the electrical-microstimulation-induced blood pressure changes and electrophysiological properties of cardiovascular neurons in the rostral ventrolateral medulla of the spontaneously hypertensive rat. Biol Signals 2:106–116;1993.

    PubMed  Google Scholar 

  8. Chan RKW, Chan YS, Wong TM. Effects of [Sar1, Ile8]-angiotensin II on rostral ventrolateral medulla neurons and blood pressure in spontaneously hypertensive rats. Neuroscience 63:267–277;1994.

    Article  PubMed  Google Scholar 

  9. Festing MFW. Maintenance of hypertensive rats, with special reference to the use of genetic markers for defining rat strains. In: Ganten D, de Jong W, eds. Handbook of Hypertension, Vol 16: Experimental and Genetic Models of Hypertension. Amsterdam, Elsevier, 202–227;1994.

    Google Scholar 

  10. Fink GD, Bruner CA, Mangiapane ML. Area postrema is critical for angiotensin-induced hypertension in rats. Hypertension 9:355–361;1987.

    PubMed  Google Scholar 

  11. Ganten D, Hermann K, Bayer C, Unger T, Lang RE. Angiotensin synthesis in the brain and increased turnover in hypertensive rats. Science 221:869–871;1983.

    Google Scholar 

  12. Granata AR, Kitai ST. Intracellular analysis in vivo of different barosensitive bulbospinal neurons in the rat rostral ventrolateral medulla. J Neurosci 12:1–20;1992.

    PubMed  Google Scholar 

  13. Gutman MB, Ciriello J, Mogenson GJ. Effects of plasma angiotensin II and hypernatremia on subfornical organ neurons. Am J Physiol 254:R746-R754;1988.

    PubMed  Google Scholar 

  14. Haselton JR, Guyenet PG. Electrophysiological characterization of putative C1 adrenergic neurons in the rat. Neuroscience 30:199–214;1989.

    Article  PubMed  Google Scholar 

  15. Herman K, Phillips MI, Raizada MK. Metabolism of angiotensin peptides by neuronal and glial cultures from rat brain. J Neurochem 52:863–868;1989.

    PubMed  Google Scholar 

  16. Hoffman WE, Phillips MI, Schmid P. Central angiotensin II-induced responses in spontaneously hypertensive rats. Am J Physiol 232:H426-H433;1977.

    PubMed  Google Scholar 

  17. Jensen LL, Harding JW, Wright JW. Role of paraventricular nucleus in control of blood pressure and drinking in rats. Am J Physiol 262:F1068-F1075;1992.

    PubMed  Google Scholar 

  18. Lind RW, Ganten D. Angiotensin. In: Bjorklund A, Hokfelt T, eds. Handbook of Chemical Neuroanatomy, Vol 9: Neuropeptides in the CNS, Part II. Amsterdam, Elsevier, 165–286;1990.

    Google Scholar 

  19. Lipski J. Antidromic activation of neurons as an analytic tool in the study of the central nervous system. J Neurosci Methods 4:1–32;1981.

    Article  PubMed  Google Scholar 

  20. Lundberg JM, Hamberger B. Frequency- and reserpine-dependent chemical coding of sympathetic transmission: differential release of noradrenaline and neuropeptide Y from pig spleen. Neurosci Lett 63:96–100;1986.

    Article  PubMed  Google Scholar 

  21. Miura M, Takayama K, Okada J. Difference in sensitivity of cardiovascular and respiratory control neurons in the subretrofacial nucleus to glutamate receptor subtype agonists in SHR, WKY and cats. J Auton Nerv Syst 36:1–12;1991.

    Article  PubMed  Google Scholar 

  22. Morrison SF, Milner TA, Reis DJ. Reticular vasomotor neurons of the rat rostral ventrolateral medulla: relationship to sympathetic nerve activity and the C1 adrenergic cell group. J Neurosci 8:1286–1301;1988.

    PubMed  Google Scholar 

  23. Muratani H, Averill DB, Ferrario CM. Effect of angiotensin II in ventrolateral medulla of spontaneously hypertensive rats. Am J Physiol 260:R977-R984;1991.

    PubMed  Google Scholar 

  24. Muratani H, Ferrario CM, Averill DB. Ventrolateral medulla in spontaneously hypertensive rats: role of angiotensin II. Am J Physiol 264:R388-R395;1993.

    PubMed  Google Scholar 

  25. Morin-Surun MP, Renavit-Saubie M. Rhythmic discharges in the perfused isolated brainstem preparation of adult guinea-pig. Neurosci Lett 101:57–61;1989.

    Article  PubMed  Google Scholar 

  26. Nabika T, Nara Y, Ikeda K, Endo J, Yamori Y. Genetic variability of the spontaneously hypertensive rats. Hypertension 18:12–16;1991.

    PubMed  Google Scholar 

  27. Nilsson H, Ljung B, Sjoblom N, Walin BJ. The influence of the sympathetic impulse pattern on contractile responses of rat mesenteric arteries and veins. Acta Physiol Scand 123:303–309;1985.

    PubMed  Google Scholar 

  28. Palmer MR, Wuerthele SM, Hoffer BJ. Physical and physiological characteristics of micropressure ejection of drugs from multibarreled pipettes. Neuropharmacology 19:931–938;1980.

    Article  PubMed  Google Scholar 

  29. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates, 2nd ed. New York, Academic Press; 1986.

    Google Scholar 

  30. Punnen S, Krieger AJ, Sapru HN. Exaggerated blood pressure responses to microinjection of angiotensin-II into the medullary pressor area of spontaneously hypertensive rats. Fed Proc 43:443;1984.

    Google Scholar 

  31. Raizada MK, Muther TP, Sumners C. Increased angiotensin II receptors in neuronal cultures from hypertensive rat brain. Am J Physiol 247:C364-C372;1984.

    PubMed  Google Scholar 

  32. Sasaki S, Dampney AL. Tonic cardiovascular effects of angiotensin II in the ventrolateral medulla. Hypertension 15:274–283;1990.

    PubMed  Google Scholar 

  33. Sawchenko PE, Cunningham ET, Mortrud MT, Pfeiffer SW, Gerfen CR. Phaseolus vulgaris leucoagglutinin anterograde axonal transport technique. In: Conn PM, ed. Methods in Neuroscience, Vol 3. New York, Academic Press, 247–260;1990.

    Google Scholar 

  34. Scholkens BA, Jung W, Rascher W, Dietz R, Ganten D. Intracerebroventricular angiotensin increases arterial blood pressure in rhesus monkeys by stimulation of pituitary hormones and the sympathetic nervous system. Experientia 3:469–470;1982.

    Article  Google Scholar 

  35. Song K, Allen AM, Paxinos G, Mendelsohn FAO. Mapping of angiotensin II receptor subtype heterogeneity in rat brain. J Comp Neurol 316:467–484;1982.

    Article  Google Scholar 

  36. Speth RC, Warmsley JK, Gehlert DR, Chernicky CL, Barnes KL, Ferrario CM. Angiotensin II receptor localization in the canine central nervous system. Brain Res 326:137–143;1985.

    Article  PubMed  Google Scholar 

  37. Sun MK, Guyenet PG. Arterial baroreceptor and vagal input to medullary sympathoexcitatory neurons in rats. Am J Physiol 252:R699-R709;1987.

    PubMed  Google Scholar 

  38. Unger T, Becker H, Petty M, Demmert G, Schneider B, Ganten D, Lang RE. Differential effects of central angiotensin II and substance P on sympathetic nerve activity in conscious rats. Circ Res 56:563–575;1985.

    PubMed  Google Scholar 

  39. Wright JW, Sullivan MJ, Bredl CR, Hanes-worth JM, Cushing LL, Harding JW. Delayed cerebroventricular metabolism [125I] angiotensins in the spontaneously hypertensive rat. J Neurochem 49:651–654;1987.

    PubMed  Google Scholar 

  40. Wright JW, Sullivan MJ, Quirk WS, Cbatt CM, Harding JW. Heightened blood pressure and drinking responsiveness to intracerebroventricularly applied angiotensins in the spontaneously hypertensive rat. Brain Res 420:289–294;1987

    Article  PubMed  Google Scholar 

  41. Yamori Y. Development of the spontaneously hypertensive rat (SHR) and of various spontaneous rat models, and their implications. In: de Jong W, ed. Handbook of Hypertension, Vol 4: Experimental and Genetic Models of Hypertension. Amsterdam, Elsevier, 224–239;1984.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Physiology, Faculty of Medicine, The University of Hong Kong, 5 Sassoon Road, Hong Kong

    R. K. W. Chan,  Y. S. Chan & T. M. Wong

Authors
  1. R. K. W. Chan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Y. S. Chan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. T. M. Wong
    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

Chan, R.K.W., Chan, Y.S. & Wong, T.M. Effects of angiotensin II on the spontaneous activity of rostral ventrolateral medullary cardiovascular neurons and blood pressure in spontaneously hypertensive rats. J Biomed Sci 3, 191–202 (1996). https://doi.org/10.1007/BF02253100

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02253100

Key words

Search

Navigation