Development of Nitric Oxide Synthase-Immunoreactive Nerves in the Cerebral Arteries of the Rat

Abstract

ABSTRACT. Development of cerebrovascular nitrergic nerves was investigated in the rat, using immunohistochemistry for nitric oxide synthase (NOS) and quantitative analysis. Cerebral perivascular NOS nerves usually appeared on the walls of both the intracranial part of the internal carotid artery (ICA) and the internal ethmoidal arteries ( IEA) at birth. NOS nerves via the IEA grew more rapidly than those via the ICA. They extended over all the major arteries located more rostral than the middle part of the basilar arteries during the third postnatal week, while those from the ICA remained limited to the caudal segment of the anterior circulation and to the ros tral segment of the posterior circulation throughout development. The appearance of NOS nerves on the vertebrate artery (VA) was not demonstrated before the third postnatal week, being apparently far late in development as compared to that of the same nerve type on the ICA and IEA. KEY WORDS: cerebrovascular innervation, development, nitrergic nerve, rat.J. Vet. Med. Sci. 66(8): 933-940, 2004 The cerebral arterial tree is formed by the connection of the anterior and posterior circulations that develop independently from the internal carotid and vertebral arteries (ICA, VA). It has also been established that the two cerebral arterial systems in mammals are multiply and differentially supplied by noradrenergic and cholinergic nerves [21], and by various types of peptidergic nerves [23].Nitric oxide (NO), highly diffusible gaseous molecule, has been identified as an intercellular chemical messenger, first in the vascular endothelium and later in the central and peripheral nervous systems [14,16]. Neuronal NO is synthesized from L-arginine by the constitutive enzyme NO synthase (NOS), of which the biochemical property is different from another constitutive NOS produced by vascular endothelial cells. NOS also exhibits diaphorase activity in addition to the synthesis of NO. Thus, neurons synthesizing NO, nitrergic neurons, can be visualized by immunohistochemical staining with an antibody against neuronal NOS, or by histochemistry for nicotinamide adenine dinucleotide phosphate diaphorase (NADPHd). Actually, by mean of these two staining methods, the rich supply of nerves immunoreactive for NOS and positive NADPHd has been demonstrated for the cerebral arterial systems in a variety of mammals including man [1,4,8,10,12,15,22]. Some of these studies, in combination with denervation and/or retrograde tracing techniques, have also provided conclusive evidence that cerebral perivascular NOS and NADPHd nerves, as well as nerves positive for acetylcholinesterase (AChE) and immunoreactive for vasoactive intestinal polypeptide (VIP), are parasympathetic in nature and have their major origin at the sphenopalatine ganglion. Pharmacological experiments have shown that NO released from cerebral perivascular nerves plays a crucial role as a neurotransmitter for non-adrenergic and non-cholinergic vasodilatation in the cerebral vessels [6,9,11,19].As to the ontogenetic stud...

Separate Development of Nitric Oxide Synthase- and Vasoactive Intestinal Polypeptide-Immunoreactive Nerves Arising from the Vertebral Artery in the Rat

“…As reported previously [2,3], NOS-IR and VIP-IR nerves, which arose from the fiber bundles on the wall of the IEA, spread over all the major arteries of the anterior circulation on PND 5. Caudally oriented nerves from this vascular route, together with those via the cerebral carotid artery (CCA), also projected to the posterior circulation through the posterior ramus (PR), and sometimes penetrated into the posterior communicating artery (PCOMA) (Fig.…”

“…NOS-IR and VIP-IR neurons from another two parasympathetic ganglia, the internal carotid mini-ganglion and the otic ganglion, also project, to some extent, to the circle of Willis through the CCA, but do not reach caudally to the BA [5,11,12]. Our previous ontogenical studies, which are carried out using single staining, have revealed that NOS-IR and VIP-IR neuronal projections from the anterior circulation to the mBA resemble strikingly VIP-IR ones in the developmental pattern, being usually accomplished at the beginning of the third postnatal week [2,3]. This observation is confirmed and extended by the present double immunohistochemistry showing that at the PND 15, the rostral half of the BA is almost all covered by a moderate number of NOS + /VIP + nerves, whereas its caudal half has in most cases no supply of nerves with detectable level of NOS immunoreactivity.…”

“…Our recent study has accumulated additional information on the rat cerebrovascular nitrergic innervation, that is, NOS-IR nerves appear along the internal ethmoidal artery (IEA) before birth as fiber bundles [3]. The immunoreactive nerves from here usually extend as far as the rostral two third of the basilar artery (BA) at the beginning of the third postnatal week.…”

Neuromeric Distribution of Nicotinamide Adenine Dinucleotide Phosphate-Diaphorase Activity in the Adult Lamprey Brain

“…In accordance with this result, the presence of nitrergic cells in the striatum and septum is a general feature reported in all sarcopterygian vertebrates, with the exception of the infrared-sensitive snake, Trimeresurus flavoviridis (Jiang and Terashima, 1996), which lacks NADPH-d activity in all telencephalic structures. Similarly, the subpallial areas equivalent to basal ganglia and septal regions in the everted telencephalon of actinopterygian fishes (González et al, 2014) also display nitrergic cells (Brüning et al, 1995;Anken and Rahmann, 1996;Ando et al, 2004;Giraldez-Perez et al, 2008López et al, 2016López et al, , 2017, with the exception of the teleost Clarias batrachus (Gaikwad et al, 2009) that lacks nitrergic cells in the telencephalon.…”