Innervation Pattern of Substance P- and Calcitonin Gene-related Peptide-Immunoreactive Nerves of the Cerebral Arteries in the Quail

Abstract

ABSTRACT. The pattern of cerebrovascular substance P (SP)-and calcitonin gene-related peptide (CGRP)-immunoreactive (IR) innervation was investigated in the quail. SP-and CGRP-IR nerves were relatively a few in the rostral part of the anterior circulation, and very scanty or lacking in its caudal part and the whole of the posterior circulation. A significant finding was that the anterior circulation in the majority of individuals is furnished with a varying proportion of SP-IR nerves with or without CGRP immunoreactivity. There was a good correlation in the expression of CGRP immunoreactivity between SP-IR cells in the ophthalmic division of the trigeminal ganglion and SP-IR nerves supplying the major cerebral arteries. In the quail, SP-and CGRP-IR fiber bundles are usually present in the internal ethmoidal artery (IEA). From these and other findings, it is most probable that cerebral perivascular SP-and CGRP-IR nerves are mainly derived from the same categories of neurons in the primary sensory ganglion via the IEA. The close association of varicose SP-IR axons to the nerve cells in the pial arteries suggests that these intrinsic neurons may play some vasocontrolling roles through the modulatory effect of their pericellular SP-IR axons.-KEY WORDS: calcitonin gene-related peptide, cerebral artery, innervation, quail, substance P.The mammalian cerebral vascular bed is known to be supplied by nerves containing various types of bioactive peptides, such as vasoactive intestinal polypeptide, neuropeptide Y, substance P (SP) and calcitonin-gene related peptide (CGRP) [10,28]. Of the four distinct types of cerebrovascular peptidergic nerves, SP-and CGRPimmunoreactive (IR) nerves are almost equal in density, a n d p r o v o k e a s i g n i f i c a n t d e p l e t i o n o f t h i s immunoreactivity after capsaicin treatment, being indicative of the primary sensory origin [8,15]. Doubleimmunostaining has confirmed that SP and CGRP coexist in the same cerebral perivascular axons [9,20,29,31]. Both the origin and the pathway of cerebrovascular SP-and CGRP-IR innervations have also been corroborated by ganglionectomy and/or a retrograde tracing technique [24,27,30,31].The angioarchitecture of the cerebral arterial system in avian species is essentially divergent from that of mammal and other vertebrate groups [4,5,16]. Furthermore, our previous histochemical studies revealed that the density of cerebral perivascular acetylcholinesterase (AChE) nerves varied markedly between the quail and the duck, despite the very rich supply of noradrenergic nerves [3,4]. This is clearly different from the general mammalian pattern in that the major cerebral arteries are supplied by AChE and noradrenergic nerves with approximately the same density [32]. The above two studies [3,4] have also demonstrated the occurrence of AChE nerve cells in the major cerebral arteries which has not been reported in mammals. To determine a further explication of neuronal influence on the avian cerebral circulation, we investigated the overall distribution of...

Different Patterns of Vasoactive Intestinal Polypeptide (VIP)-Immunoreactive and Acetylcholinesterase (AChE)-Positive Innervation in the Internal Carotid Artery and Cerebral Arterial Tree of the Quail

“…From a line of the results mentioned above, it is highly suggestive that in the quail, cerebral perivascular VIP-IR nerves arise mainly from neurons in the nerve bundles within the carotid canal and enter the cranial cavity through the CCA. These ganglion cells do not emit catecholamine fluorescence [4] and usually have no substance P immunoreactivity [18]. Accordingly, they are interpreted as being parasympathetic in nature, probably homologous to the ICMG neurons reported from several mammalian species [15].…”

“…In this bird, the nerve bundles accompanying the ICA within the carotid canal contain a large number of VIP+/AChEnerve cells that correlate well with AChE reaction observed in most of the VIP-IR nerves surrounding the major cerebral arteries. In our preliminary experiment, the superior cervical and other cervical sympathetic ganglia and the two sensory (trigeminal and cervical dorsal root) ganglia, which are known to be principal or local sources for cerebrovascular sympathetic and sensory innervation in the quail [4,18], are equipped with no VIP-IR nerve cells. From a line of the results mentioned above, it is highly suggestive that in the quail, cerebral perivascular VIP-IR nerves arise mainly from neurons in the nerve bundles within the carotid canal and enter the cranial cavity through the CCA.…”

“…It also confirms and extends the previous observation [4] that a small number of AChE nerve cells, which often appear on the walls of these vascular regions, generally have no VIP immunoreactivity. Since no occurrence of nerve cells expressing either catecholamine fluorescence or SP immunoreactivity is found in the quail cerebral vasculature [4,18], these intrinsic neurons are considered to be the intracranial outflow from parasympathetic neuronal tract probably via the IEA. At any rate, the quail cerebral arterial tree, at least the rostral segment of the anterior circulation in some individuals, are multiply innervated by the extracranial and intracranial VIP+/AChE-, AChE+/VIP-and VIP+/AChE+ neurons.…”