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.
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References
Allen AM, Dampney RAL, Mendelsohn FAO. Angiotensin receptor binding and pressor effects in the cat subretrofacial nucleus. Am J Physiol 255:H1011-H1017;1988.
Bruner CA, Fink GD. Neurohumoral contributions to chronic angiotensin-induced hypertension. Am J Physiol 250:H52-H61;1986.
Calaresu FR, Yardley CP. Medullary basal sympathetic tone. Ann Rev Physiol 50:511–524;1988.
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.
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.
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.
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.
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.
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.
Fink GD, Bruner CA, Mangiapane ML. Area postrema is critical for angiotensin-induced hypertension in rats. Hypertension 9:355–361;1987.
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.
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.
Gutman MB, Ciriello J, Mogenson GJ. Effects of plasma angiotensin II and hypernatremia on subfornical organ neurons. Am J Physiol 254:R746-R754;1988.
Haselton JR, Guyenet PG. Electrophysiological characterization of putative C1 adrenergic neurons in the rat. Neuroscience 30:199–214;1989.
Herman K, Phillips MI, Raizada MK. Metabolism of angiotensin peptides by neuronal and glial cultures from rat brain. J Neurochem 52:863–868;1989.
Hoffman WE, Phillips MI, Schmid P. Central angiotensin II-induced responses in spontaneously hypertensive rats. Am J Physiol 232:H426-H433;1977.
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.
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.
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.
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.
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.
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.
Muratani H, Averill DB, Ferrario CM. Effect of angiotensin II in ventrolateral medulla of spontaneously hypertensive rats. Am J Physiol 260:R977-R984;1991.
Muratani H, Ferrario CM, Averill DB. Ventrolateral medulla in spontaneously hypertensive rats: role of angiotensin II. Am J Physiol 264:R388-R395;1993.
Morin-Surun MP, Renavit-Saubie M. Rhythmic discharges in the perfused isolated brainstem preparation of adult guinea-pig. Neurosci Lett 101:57–61;1989.
Nabika T, Nara Y, Ikeda K, Endo J, Yamori Y. Genetic variability of the spontaneously hypertensive rats. Hypertension 18:12–16;1991.
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.
Palmer MR, Wuerthele SM, Hoffer BJ. Physical and physiological characteristics of micropressure ejection of drugs from multibarreled pipettes. Neuropharmacology 19:931–938;1980.
Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates, 2nd ed. New York, Academic Press; 1986.
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.
Raizada MK, Muther TP, Sumners C. Increased angiotensin II receptors in neuronal cultures from hypertensive rat brain. Am J Physiol 247:C364-C372;1984.
Sasaki S, Dampney AL. Tonic cardiovascular effects of angiotensin II in the ventrolateral medulla. Hypertension 15:274–283;1990.
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.
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.
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.
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.
Sun MK, Guyenet PG. Arterial baroreceptor and vagal input to medullary sympathoexcitatory neurons in rats. Am J Physiol 252:R699-R709;1987.
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.
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.
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
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.
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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
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DOI: https://doi.org/10.1007/BF02253100