Autonomic innervation of cerebral blood vessels decreases in renal hypertensive rats.

Abstract

SUMMARY The ultrastructural distribution of the autonomic nerves of brain arteries was investigated in renal (one-kidney, one clip) hypertensive and normotensive Wistar-Kyoto rats. Sympathetic and nonsympathetic nerve terminals were found only in the adventitial layer of brain arteries of renal hypertensive and normotensive rats. In both normotensive and renal hypertensive rats the total nerve endings were dense in anterior cerebral artery, moderately dense in middle cerebral artery, and sparse in basilar artery. In normotensive rats, nonsympathetic nerves outnumbered sympathetic nerves in anterior cerebral, middle cerebral, and basilar arteries. In renal hypertensive rats these two types of nerve terminals in close apposition to smooth muscle decreased in anterior cerebral and basilar arteries, while those in middle cerebral arteries remained unchanged. These results suggest that the potential neurogenic control of cerebral blood vessels as well as the trophic effect of sympathetic nerves on brain blood vessels may decrease in renal hypertensive rats. As this finding contrasts with that in spontaneously hypertensive rats, the pattern of innervation in brain arteries may differ in different types of hypertension. (Hypertension 7: 514-518, 1985) KEY Tissue concentrations of norepinephrine are reported to be decreased in mesenteric artery and heart in renal hypertensive animals.10 " On the other hand, the density of sympathetic innervation has been shown to increase in brain arteries of the spontaneously hypertensive rats (SHR).5 -l2 Furthermore, autoregulation of lower and higher limits of cerebral blood flow has been reported to change in hypertensive animals. 13 "" These results suggest that autonomic nerves undergo some changes when the animal becomes hypertensive. Alterations in the pattern of autonomic nerves may be different depending on the type of hypertensive model. In this study, we therefore examined and compared the ultrastructural distribution of sympathetic and nonsympathetic nerve terminals and their relationship to smooth muscle cells in the cerebral arterial walls of renal (one-kidney, one clip) hypertensive rats (RHR) and normotensive rats (NR). MethodsThe experiments were performed on normotensive male Wistar-Kyoto rats. Chronic renal hypertension was induced in 7-week-old rats by placing a silver clip (internal diameter, 0.25 mm) over the left renal artery through a left lumbar incision and followed 1 week later by contralateral nephrectomy. The control animals were sham-operated. The left kidney was exposed after a lumbar incision and was manipulated without compressing the artery. The operating time was approximately the same as that of the procedure for artery clipping. One week later the contralateral kidney was also exposed but not removed. All of the procedures were accomplished with the rats under sodium pentobarbital (Nembutal, 50 mg/ml). The systol-

Altered cerebral vessel innervation in the spontaneously hypertensive rat.

“…It is interesting to note that GVN increase in all cerebral arteries examined, and AVN decrease or remain unchanged in cerebral arteries of SHR (present study), whereas both GVN and AVN terminals decrease in cerebral arteries of renal hypertensive rats (RHR) (Saito and Lee, 1983). These results suggest that the active neurogenic vasodilation for increasing cerebral blood flow may be weakened or impaired in both RHR and SHR, and the active cerebral vasoconstriction may be improved in SHR but weakened in RHR.…”

“…The increase in GVN terminals in SHR cerebral arteries is probably not due to high blood pressure either. In renal hypertensive rats, both the AVN and GVN terminals per cross-section decrease in the anterior cerebral and basilar arteries (Saito and Lee, 1983). These results suggest that alteration of AVN and GVN in hypertensive animals may be due to factors other than the high blood pressure itself.…”

Sympathetic activation increases basilar arterial blood flow in normotensive but not hypertensive rats

“…This is based on reported results that distribution of cerebral perivascular sympathetic and parasympathetic nerve terminals changes in hypertension (30,31,42). The density of the sympathetic nerve terminals increases in the spontaneously hypertensive rat (SHR) but decreases in the renovascular hypertensive rat (RHR).…”

Inhibition by ketamine and amphetamine analogs of the neurogenic nitrergic vasodilations in porcine basilar arteries

“…The physiological significance of this axo-axonal interaction mechanism in the large arteries at the base of the brain is supported by the findings that the axo-axonal interaction mechanismmediated nitrergic vasodilation is diminished in hypertension (Chang et al, 2012). Although the exact reasons underlying this change in hypertension remain to be examined, it has been reported that the parasympathetic nerve terminals significantly decrease while the sympathetic nerve terminals increase or decrease depending on type of hypertension (Lee and Saito, 1984;Saito and Lee, 1985). These morphological alterations in hypertension obviously diminish anatomical basis for the axo-axonal interaction leading to decreased neurogenic nitrergic vasodilation in hypertension (Lee and Saito, 1984;Saito and Lee, 1985;Chang et al, 2012).…”

“…Although the exact reasons underlying this change in hypertension remain to be examined, it has been reported that the parasympathetic nerve terminals significantly decrease while the sympathetic nerve terminals increase or decrease depending on type of hypertension (Lee and Saito, 1984;Saito and Lee, 1985). These morphological alterations in hypertension obviously diminish anatomical basis for the axo-axonal interaction leading to decreased neurogenic nitrergic vasodilation in hypertension (Lee and Saito, 1984;Saito and Lee, 1985;Chang et al, 2012). Accordingly, the axo-axonal interaction mechanism-mediated neurogenic vasodilation may play an important role, especially, as a protective mechanism in increasing brainstem blood flow to meet the O 2 demand when facing an acutely stressful situation (Chang et al, 2012).…”