Development of AChE-positive, NA-containing and VIP- and NPY-immunoreactive nerves in the major cerebral arteries of the rat

Abstract

The development of cerebrovascular nerves containing noradrenaline (NA), acetylcholinesterase (AChE), neuropeptide Y (NPY), and vasoactive intestinal polypeptide (VIP) was studied in rats from before birth to adulthood. All these nerves entered the cranial cavity along the cerebral carotid, internal ethmoidal, and vertebral arteries during the early stages of development, but the subsequent growth and distribution of NA-containing and NPY-immunoreactive (IR) nerves differed greatly from that of AChE-positive and VIP-IR nerves. NA-containing and NPY-IR nerves extended rapidly from the cerebral carotid artery and spread over all the major arteries of the internal carotid system by postnatal day 3, as well as descending the posterior ramus of the cerebral carotid to mingle with nerves from the vertebral artery around the mid-basilar artery by day 5. AChE-positive and VIP-IR nerves from the internal ethmoidal artery covered the whole internal carotid system during the first postnatal week, and projected to the upper basilar artery after the second week, while those from the cerebral carotid artery remained limited to the middle cerebral artery throughout development. By day 21, all major arteries of the internal carotid system had dense plexuses of the four nerve types that were similar to those observed in adult rats. The vertebrobasilar system also had a well-organized network of NA-containing and NPY-IR nerves, but only a poor supply of AChE-positive and VIP-IR nerves. Even on day 30, the latter two nerve types were sometimes absent from the middle to caudal basilar artery, owing to a lack of interdigitation by nerves from the internal ethmoidal and vertebral arteries.

Development of Vasoactive Intestinal Polypeptide-Immunoreactive Nerves in the Major Cerebral Arteries of the Quail Anterior Circulation

“…Based on the pharmacological effects of VIP on vascular function [4,6,9], it may be related to the direct and/or indirect vasodilator roles for the regulation of cerebral circulation that is required for brain differentiation relevant to this precocial bird. In rat, cerebral perivascular VIP-IR nerves reach a peak density at one month of age that is maintained until the fourth month [2,11]. The present study confirms and extends the previous observation that VIP-IR neuronal projection to the rAR from the CCA, which is an indication for mature pattern of the quail cerebrovascular VIP innervation [3], has been accomplished in most of the young birds aged P15.…”

“…VIP-IR nerves via the CCA increase greatly in number and spread rapidly toward the anterior circulation, while those via the CEA are sparse all through the post-hatching stages, and mostly remain limited to this vessel wall. The observation described above is in contrast to the subsequent development of the same nerve type via the two vascular routes in the rat [2]. It does not correspond to the developmental pattern of cerebrovascular noradrenergic (NA) innervation reported previously for the quail [8]: NA nerves from the CEA, of which the first appearance is ascertained at E8, are greater in number and grow more fast than those from the CCA.…”

“…Previously, we noted that VIP-IR nerves supplying the rat anterior circulation came from the CCA and the internal ethmoidal artery (IEA) on E 20 [2]. In the quail, cerebral perivascular VIP-IR nerves appear on the wall of the CCA from the majority of embryos at E10, but are lacking in the CEA, which is homologous to the IEA in mammals, throughout embryonic development.…”

“…In the rat, the pattern of cerebrovascular innervation by parasympathetic VIP-IR and sympathetic NA nerves is till incomplete at birth (day 22 after gestation) [2,11]. It reorganizes abruptly toward the mature form at the beginning of the second postnatal week, with a marked increase of thin nerve fibers having many terminal varicosities.…”

“…The role of VIP as a neurotransmitter or neuromodulator for non-adrenergic and non-cholinergic vasodilatation in the cerebral vessels has been well documented pharmacologically [4,6,9]. There are also ontogenical studies on the age-related change of this peptidergic nerves in the rat cerebral arterial system [2,11].…”