Origins and Pathways of Cerebrovascular Vasoactive Intestinal Polypeptide-Positive Nerves in Rat

Abstract

Summary: In order to clarify the origins and pathways of vasoactive intestinal polypeptide (VIP)-containing nerve fibers in cerebral blood vessels of rat, denervation exper iments and retrograde axonal tracing methods (true blue) were used. Numerous VIP-positive nerve cells were rec ognized in the sphenopalatine ganglion and in a mini-gan glion (internal carotid mini-ganglion) located on the in ternal carotid artery in the carotid canal, where the para sympathetic greater superficial petrosal nerve is joined by the sympathetic fibers from the internal carotid nerve, to form the Vidian nerve. VIP fiber bridges in the greater deep petrosal nerve and the internal carotid nerve reached the wall of the internal carotid artery. Two weeks after bilateral removal of the sphenopalatine ganglion or sectioning of the structures in the ethmoidal foramen, VIP fibers in the anterior part of the circle of Willis com pletely disappeared. Very few remained in the middle ce rebral artery, the posterior cerebral artery, and rostral Cerebral blood vessels are well supplied with classic adrenergic and cholinergic nerve fibers as well as with peptide-containing fibers (Owman et aI. , 1986). Among these, the vasodilatory peptide, vasoactive intestinal polypeptide (VIP), has been demonstrated by immunohistochemistry in whole mount preparations of major pial cerebral arteries from mouse, rat, hamster, guinea pig, gerbil, rabbit, cat, dog, pig, cow, monkey, and man (Larsson et aI., 1976; Edvinsson et aI., 1980; Kobayashi et aI. , 1983; Matsuyama et aI. , 1983 andEdvinsson and Ekman, 1984; Itakura et aI. , 1984; Gibbins et aI., 1984;Brayden and Bevan, 1986).In most species little is known about the origin and distribution of the VIP nerves to the cerebral blood vessels. In cat they appear to originate from several miniganglia associated with nerves around Received December 7, 1987; accepted February 19, 1988. Address correspondence and reprint requests to Dr. N. Suzuki at Department of Medical Cell Research, University of Lund, Biskopsgatan 5, S-223 62 Lund, Sweden.Abbreviations used: AChE, acetylcholinesterase; ChAT, cho line acetyltransferase; VIP, vasoactive intestinal polypeptide. 697two-thirds of the basilar artery, whereas they remained in the caudal one-third of the basilar artery, the vertebral artery, and intracranial and carotid canal segments of the internal carotid artery. One week after application of true blue to the middle cerebral artery, dye accumulated in the ganglion cells in the sphenopalatine, otic and internal ca rotid mini-ganglion; some of the cells were positive for VIP. The results show that the VIP nerves in rat cerebral blood vessels originate: (a) in the sphenopalatine, and otic ganglion to innervate the circle of Willis and its branches from anterior and caudally and (b) from the in ternal carotid mini-ganglion to innervate the internal ca rotid artery at the level of the carotid canal and to some extent its intracranial extensions.

Inhibition of Nitric Oxide Synthase Attenuates the Cerebral Blood Flow Response to Stimulation of Postganglionic Parasympathetic Nerves in the Rat

“…, 1993). Neuropeptide Y and vasoac tive intestinal polypeptide are also present as trans mitters in the parasympathetic nerves (Suzuki et al, 1988(Suzuki et al, , 1990b) and exert their vasoconstrictor or dilator action without contribution from endothe lium-linked mechanisms (Uddman and Edvinsson, 1989). Other as yet unidentified transmitters may be present in these nerves with an influence on vascu lar tone that may be endothelium dependent.…”

Acetylcholine Levels and Choline Acetyltransferase Activity in Rat Cerebrovascular Bed after Uni- or Bilateral Sphenopalatine Ganglionectomy

“…Uni-or bilateral sphenopalatine ganglionec tomy or sham operation was performed by a zygomatico lacrimal approach, as described by Rosen et al (1940) and more recently by Suzuki et al (1988). The zygomatic bone was exposed through a skin incision and cut at both extremities; the masseter muscle was then retracted in order to uncover the fifth nerve trunk, which was cleaned…”

“…In the rat, it has been elegantly shown that VIP positive nerves originate mainly from the SPG (Hara et aI., 1985;Suzuki et al, 1988) and to a lesser extent the otic ganglia to innervate the circle of Willis and its branches, and from the internal carotid miniganglion to innervate the internal ca rotid artery (Suzuki et aI., 1988). Based on the co existence of VIP and AChE in cerebrovascular fi bers and in the SPG (Kobayashi et aI., 1983;ltakura et aI.…”

“…U sing the same surgical ap proach as that described by Suzuki et al (1988), we examined the effect of sphenopalatine ganglionec tomy on the two most specific cholinergic markers, namely the endogenous acetylcholine (ACh) levels and ChAT activity in the rat main basal arteries and pial vessels. In addition, ACh content and ChAT activity were measured in a series of vascular and nervous tissues.…”

Innervation of the rat pineal gland by nerve fibres originating in the sphenopalatine, otic and trigeminal ganglia. A retrograde in vivo neuronal tracing study

“…Thus, the otic ganglion contains many VIPergic perikarya and is known to innervate brain vasculature [31,33]. Whether this ganglion projects to the pineal gland is at the moment unknown.…”