Summary
The distribution of fluorescent adrenergic nerve fibers in the proximal portion (horizontal segment, Hs) and the three distal portions (major branches) of the middle cerebral arteries (MCA) was examined in stroke-prone spontaneously hypertensive rats (SHRSP) aged 10, 30, 60, 90, and 180 days, by the glyoxylic acid method. The results were compared with those in agematched normotensive Wistar Kyoto (WKY) rats. While the distribution pattern of fluorescent nerve fibers in the proximal portion of WKY rats changed from a straight linear arrangement at 10 and 30 days of age to a network-like arrangement after 60 days, those from SHRSP showed a constant meshwork pattern throughout the entire examination period. In the distal portions of the MCA of both SHRSP and WKY rats at all ages examined, fluorescent nerve fibers formed a coarse network. The distribution densities of adrenergic nerve fibers in the proximal and distal portions of the MCA of SHRSP were significantly higher (P<0.01 and 0.05) than those of WKY rats at all ages examined, except in the proximal portion at 90 and 180 days of age. The difference in nerve fiber density between SHRSP and WKY rats reached a peak at 30 days of age in both proximal and distal portions, and then gradually decreased with age. The present study suggests that sympathetic hyperinnervation is an important factor in the development of hypertension, and is involved in its maintenance in SHRSP.
Similar content being viewed by others
References
Abel PW, Hermsmeyer K (1981) Sympathetic cross-innervation of SHR and genetic controls suggests a trophic influence on vascular muscle membranes. Circ Res 49:1311–1318
Alho H, Partanen M, Koistinaho J, Vaalasti A, Hervonen A (1984) Histochemically demonstrable catecholamines in sympathetic ganglia and carotid body of spontaneously hypertensive and normotensive rats. Histochemistry 80:457–462
Bevan RD (1984) Trophic effects of peripheral adrenergic nerves on vascular structure. Hypertension (suppl 3): 6:19–26
Bevan RD, Purdy RE, Su C, Bevan JA (1975) Evidence for an increase in adrenergic nerve function in blood vessels from experimental hypertensive rabbits. Circ Rec 37:503–508
Burnstock G, Griffith SG, Sneddon P (1984) Autonomic nerves in the precapillary vessel wall. J Cardiovasc Pharmacol (Suppl 2) 6:344–353
Cassis LA, Stitzel RE, Head RJ (1985) Hypernoradrenergic innervation of the caudal artery of the spontaneously hypertensive rat: An influence upon neuroeffector mechanisms. Am Soc Pharmacol Exp Ther 234:792–803
Chaldakov GN, Nara Y, Horie R, Yamori Y (1989) A new view of the arterial smooth muscle cells and autonomic nerve plexus by scanning electron microscopy in spontaneously hypertensive rats. Exp Pathol 36:181–184
Dhital KK, Gerli R, Lincoln J, Milner P, Tanganelli P, Weber G, Fruschelli C, Burnstock G (1988) Increased density of perivascular nerves to the major cerebral vessels of the spontaneously hypertensive rat: differential changes in noradrenaline and neuropeptide Y during development. Brain Res 444:33–45
Eccleston-Joyner CA, Gray SD (1988) Arterial hypertrophy in the fetal and neonatal sponatenously hypertensive rat. Hypertension 12:513–518
Folkow B, Hallback M, Lundgren Y, Weiss L (1972) The effects of immunosympathectomy on blood pressure and vascular reactivity in normal and spontaneously hypertensive rats. Acta Physiol Scand 84:512–523
Fujiwara T, Kondo M, Tabei R (1990) Morphological changes in cerebral vascular smooth muscle cells in stroke-prone spontaneously hypertensive rats (SHRSP). Virchows Arch B 58:377–382
Furness JB, Costa M (1975) The use of glyoxylic acid for the fluorescence histochemical demonstration of peripheral stores of noradrenaline and 5-hydroxytryptamine in whole mounts. Histochemistry 41:335–352
Galloway MP, Westfall TC (1982) The release of endogenous norepinephrine from the coccygeal artery of spontaneously hypertensive and Wistar-Kyoto rats. Circ Res 51:225–232
Haebara H, Ichijima K, Motoyoshi T, Okamoto K (1968) Fluorescence microscopical studies on noradrenaline in the peripheral blood vessels of spontaneously hypertensive rats. Jpn Circ J 32:1391–1400
Hamada M, Nishio I, Baba A, Fukuda K, Takeda J, Ura M, Hano T, Kuchii M, Masuyama Y (1990) Enhanced DNA synthesis of cultured vascular smooth muscle cells from spontaneously hypertensive rats. Atherosclerosis 81:191–198
Hano T, Rho J (1989) Norepinephrine overflow in perfused mesenteric arteries of spontaneously hypertensive rats. Hypertension 14:44–53
Hart MN, Heistad DD, Brody MJ (1980) Effect of chronic hypertension and sympathetic denervation on wall/lumen ratio of cerebral vessels. Hypertension 2:419–423
Ichijima K (1969) Morphological studies on the peripheral small arteries of spontaneously hypertensive rats. Jpn Circ J 33:785–812
Kanbe T, Nara Y, Tagami M, Yamori Y (1983) Studies of hypertension-induced vascular hypertrophy in cultured smooth muscle cells from spontaneously hypertensive rats. Hypertension 5:887–892
Karr-Dullien V, Bloomquist EI, Beringer T, El-Bermani Al-W (1981) Arterial morphometry in neonatal and infant spontaneously hypertensive rats. Blood Vessels 18:253–262
Kawai Y, Ohhashi T (1986) Histochemical studies of the adrenergic innervation of canine cerebral arteries. J Autun Nerv Syst 15:103–108
Kawamura K, Ando K, Takebayashi S (1989) Perivascular innervation of the mesenteric artery in spontaneously hypertensive rats. Hypertension 14:660–665
Kobayashi S, Tsukahara S, Sugita K, Nagata T (1981) Adrenergic and cholinergic innervation of rat cerebral arteries. Histochemistry 70:129–138
Kondo M (1986) Autoradiographic study of3H-lysine uptake by superior cervical and stellate ganglia in prehypertensive spontaneously hypertensive rats. Virchows Arch B 52:299–304
Kondo M (1987) Autoradiographic study of3H-DOPA uptake by superior cervical and stellate ganglia of spontaneously hypertensive rats during the prehypertensive stage. Virchows Arch B 54:190–193
Kondo M, Terada M, Shimizu D, Fujiwara T, Tabei R (1990) Morphometric study of the superior cervical and stellate ganglia of spontaneously hypertensive rats during the prehypertensive stage. Virchows Arch B 58:371–376
Lais LT, Brody MJ (1978) Vasoconstrictor hyperresponsiveness: an early pathogenetic mechanism in the spontaneously hypertensive rat. Eur J Pharmacol 47:177–189
Lee RMKW (1985) Vascular changes at the prehypertensive phase in the mesenteric arteries from spontaneously hypertensive rats. Blood Vessels 22:105–126
Lee RMKW, Forrest JB, Garfield RE, Daniel EE (1983) Ultrastructural changes in mesenteric arteries from spontaneously hypertensive rats. Blood Vessels 20:72–91
Lee RMKW, Smeda JS (1985) Primary versus secondary structural changes of the blood vessels in hypertension. Can J Physiol Pharmacol 63:392–401
Lee RMKW, Triggle CR, Cheung DWT, Coughlin MD (1987) Structural and functional consequence of neonatal sympathectomy on the blood vessels of spontaneously hypertensive rats. Hypertension 10:328–338
Lee TJ-F, Saito A (1984) Altered cerebral vessel innervation in the spontaneously hypertensive rat. Circ Res 55:392–403
Lee TJ-F, Saito A (1986) Altered cerebral vessel innervation in spontaneously hypertensive and renal hypertensive rats. J Hypertension 4 (suppl 3):s201-s203
Longhurst PA, Stitzel RE, Head RJ (1986) Perfusion of the intact and partially isolated rat mesenteric vascular bed: Application to vessels from hypertensive and normotensive rats. Blood Vessels 23:288–296
Masuyama Y, Tsuda K, Kusuyama Y, Hano T, Kuchii M, Nishio I (1984) Neurotransmitter release, vascular responsiveness and their calcium-mediated regulation in perfused mesenteric preparation of spontaneously hypertensive rats and DOCA-salt hypertension. J Hypertension 2 (suppl 3):99–102
Miller BG, Connors BA, Bohlen G, Evan AP (1987) Cell and wall morphology of intestinal arterioles from 4- to 6- and 17-to 19-week-old Wistar-Kyoto and spontaneously hypertensive rats. Hypertension 9:59–68
Mione MC, Dhital KK, Amenta F, Burnstock G (1988b) An increase in the expression of neuropeptidergic vasodilator, but not vasoconstrictor, cerebrovascular nerves in aging rats. Brain Res 460:103–113
Mione MC, Erdo SL, Kiss B, Ricci A, Amenta F (1988a) Agerelated changes of noradrenergic innervation of rat splanchnic blood vessels: a histofluorescence and neurochemical study. J Autun Nerv Syst 25:27–33
Mulvany MJ, Baandrup U, Gundersen HJG (1985) Evidence for hyperplasia in mesenteric resistance vessels of spontaneously hypertensive rats using a three-dimensional disector. Circ Res 57:794–800
Nordborg C, Fredriksson K, Johansson BB (1985) The morphometry of consecutive segments in cerebral arteries of normotensive and spontaneously hypertensive rats. Stroke 16:313–320
Owens GK, Schwartz SM (1982) Alterations in vascular smooth muscle mass in the spontaneously hypertensive rats; Role of cellular hypertrophy, hyperploidy, and hyperplasia. Circ Rec 51:280–289
Schon F, Allen JM, Yeats JC, Allen YS, Ballesta J, Polak JM, Kelly JS, Bloom SR (1985) Neuropeptide Y innervation of the rodent pineal gland and cerebral blood vessels. Neurosci Lett 57:65–71
Scott TM, Pang SC (1983) The correlation between the development of sympathetic innervation and the development of medial hypertrophy in jejunal arteries in normotensive and spontaneously hypertensive rats. J Autun Nerv Syst 8:25–32
Sinaiko AR, Cooper MJ, Mirkin BL (1980) Effect of neonatal sympathectomy with 6-hydroxydopamine on the reactivity of the renin-angiotensin system in the spontaneously hypertensive rat. Clin Sci 59:123–129
Tsuda K, Kuchii M, Nishio I, Masuyama Y (1986) Effects of epinephrine and dopamine on norepinephrine release from the sympathetic nerve endings in hypertension. J Hypertension 4 (suppl 5):s45-s48
Tsuda K, Shima H, Ura M, Takeda J, Kimura K, Nishio I, Masuyama Y (1988) Protein kinase C-dependent and calmodulin-dependent regulation of neurotransmitter release and vascular responsiveness in spontaneously hypertensive rats. J Hypertension 6 (suppl 4):s565–567
Yang H, Morton W, Lee RMKW, Kajetanowicz A, Forrest JB (1989) Autoradiographic study of smooth muscle cell proliferation in spontaneously hypertensive rats. Clin Sci 76:475–478
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Kondo, M., Miyazaki, T., Fujiwara, T. et al. Increased density of fluorescent adrenergic fibers around the middle cerebral arteries of stroke-prone spontaneously hypertensive rats. Virchows Archiv B Cell Pathol 61, 117–122 (1992). https://doi.org/10.1007/BF02890413
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF02890413