Immunoelectron microscopic study of substance P-containing fibers in feline cerebral arteries

Liu‐Chen, Lee‐Yuan; Liszczak, Theodore M.; King, Joan C.; Moskowtiz, Michael A.

doi:10.1016/0006-8993(86)90508-1

Cited by 50 publications

(23 citation statements)

References 47 publications

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“…Cerebral blood vessels, arteries and veins, are surrounded by a moderately dense network ofSP-containing nerves [21,22,[24][25][26][27][28][29][30]. These findings have further been corro borated by immunoelectron-microscopic studies [31]. SP is a putative neurotransmit ter in 10-15 % of neurons in sensory ganglia, i.e.…”

Section: Parasympathetic Nervessupporting

confidence: 49%

Innervation and Effects of Dilatory Neuropeptides on Cerebral Vessels

Edvinsson

1991

J Vasc Res

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The cerebral circulation is supplied with two vasodilator systems: the parasympathetic system storing vasoactive intestinal peptide, peptide histidine isoleucine, acetylcholine and in a subpopulation of nerves neuropeptid Y, and the sensory system, mainly originating in the trigeminal ganglion, storing substance P, neurokinin A and calcitonin gene-related peptide (CGRP). Recent knowledge of the innervation and effects of the dilator neuropeptides in the cerebral circulation is reviewed. Their role in the pathophysiology of subarachnoid hemorrhage and migraine has now received attention, with documentation of a clear linkage with the release of CGRP. In subarachnoid hemorrhage, other perivascular peptides are, to a lesser extent, involved.

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Section: Parasympathetic Nervessupporting

confidence: 49%

Innervation and Effects of Dilatory Neuropeptides on Cerebral Vessels

Edvinsson

1991

J Vasc Res

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“…Substance P-and CGRP-like immunoreactivity in the trigeminal system is preferentially found in very thin nerve fibers (Liu-Chen et al 1986) and small ganglion cells (Tsai et al 1988;Hardebo et al 1989;Nozaki et al 1990). This also fits the measurements of the present study, since most of the peptidergic nerve fibers in the dura mater had small diameters.…”

Section: Morphological Differences Between Sensory and Sympathetic Inmentioning

confidence: 99%

“…A high density of mitochondria has been described as characteristic for sensory nerve endings in several tissues (e.g., Andres and von Dfiring 1973;Hoyes and Barber 1976;Yeh and Kruger 1984). Many small vesicles, on the other hand, are typically found in autonomic endings of intracranial vessels and other tissues (Iwayama et al 1970;Nielsen et al 1971;Tervo et al 1979;Burnstock 1981 ;Liu-Chen et al 1986;Dixon and Gilpin 1987). A high density of mitochondria has frequently been found in nerve fibers that also contain many densecore vesicles.…”

Section: Morphological Differences Between Sensory and Sympathetic Inmentioning

confidence: 99%

Innervation of the dura mater encephali of cat and rat: ultrastructure and calcitonin gene-related peptide-like and substance P-like immunoreactivity

et al. 1993

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Ultrastructural, immunocytochemical, and immunoelectron microscopical examinations are reported that describe the morphology of putative sensory nerve endings in the dura mater encephali of the rat and the cat. Morphometrical measurements and reconstructions showed that in the cat the mean diameter of axons, the bare area of axolemma, and the content of mitochondria and vesicles are highly variable in dural nerve endings. Nerve fibers with a high volume density of mitochondria are thought to be sensory, while nerve fibers containing many small vesicles are considered autonomic. There is, however, a broad overlap of mitochondria-rich and vesicle-rich nerve fibers in the dura, so that discrimination between sensory and autonomic endings by these characteristics frequently fails. Whole-mount preparations treated cytochemically for detection of substance P- and calcitonin gene-related peptide-like immunoreactivity in the rat and the cat showed a network of immunopositive nerve fibers in the vicinity of dural blood vessels. Most of these peptidergic and probably sensory nerve fibers were found terminating in the dural connective tissue far from vessels. Calcitonin gene-related peptide-positive nerve fibers were much more abundant than substance P-positive fibers. Immunoelectron microscopic preparations revealed that calcitonin gene-related peptide- and substance P-like immunoreactivity is found in a small proportion of generally thin unmyelinated nerve fibers. These proportions were very similar in the rat and the cat. Summarizing the recent literature, the morphological characteristics of putative sensory nerve fibers in the dura mater are discussed in relation to their possible functional significance for neurogenic inflammation and nociception.

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“…Fibers primarily from the ophthalmic division (7,8) join sympathetic and parasympathetic fibers within the cavernous plexus (11) from which they distribute to the ipsilateral internal carotid artery and the circle of Willis. Trigeminovascular fibers are mainly unmyelinated (16), reside within the adventitial layer, transmit nociceptive information (17,18), and contain substance P (12), neurokinin A (19), calcitonin gene-related peptide (13), and cholecystokinin 8 (20).…”

mentioning

confidence: 99%

Trigeminovascular fibers increase blood flow in cortical gray matter by axon reflex-like mechanisms during acute severe hypertension or seizures.

Sakas

Moskowitz

Wei

et al. 1989

Proc. Natl. Acad. Sci. U.S.A.

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Cerebral blood flow was measured and compared in 10 symmetrical brain regions following unilateral trigeminal ganglionectomy (n = 13), sham operation (n = 6), or trigeminal root section (rhizotomy) (n = 8) in cats. Multiple determinations were obtained in anesthetized and paralyzed animals using radiolabeled mict-ospheres during (i) normocapnia-normotension, (ii) hypercappia (5% C02/95% room air), A third major pathway was recently defined innervating cerebral blood vessels (7). Perivascular sensory axons projecting from the trigeminal ganglia were demonstrated by retrograde (7-9) and orthograde (10) axonal transport techniques as well as by Wallerian degeneration techniques (11) or by surgical lesioning combined with immunohistochemistry (12, 13) or radioimmunoassay (14, 15). Fibers primarily from the ophthalmic division (7, 8) join sympathetic and parasympathetic fibers within the cavernous plexus (11) from which they distribute to the ipsilateral internal carotid artery and the circle of Willis. Trigeminovascular fibers are mainly unmyelinated (16), reside within the adventitial layer, transmit nociceptive information (17, 18), and contain substance P (12), neurokinin A (19), calcitonin gene-related peptide (13), and cholecystokinin 8 (20).In this report, we examined the possibility that sensory axons participate in the regulation of cerebral blood flow based on knowledge that (i) substance P (21, 22), neurokinin A (23), and calcitonin gene-related peptide (13) are cerebrovasodilating molecules; (ii) peptides are released from pial vessels in vitro by depolarizing stimuli (24); and (iii) release mediates vasodilation and/or increases in blood flow following electrical stimulation of sensory nerves in other tissues (25-27). Blood flow was examined during perturbations previously shown to involve nonneurogenic (hypercapnia) and neurogenic mechanisms (at least in part). We conclude that increases in brain blood flow during severe hypertension are not totally passive to the perfusion pressure. Furthermore, increases in flow associated with generalized seizures or hypertension are mediated in part by the trigeminal nerve via local "axon reflex-like" mechanisms involving neuropeptide release from perivascular nerve endings. MATERIALS AND METHODSSham and Lesioning Procedures. Male and female adult mongrel cats (3.0-4.5 kg) were anesthetized with ketamine hydrochloride (30 mg/kg, i.m.) and sodium pentobarbital (10-15 mg/kg, i.p.) and mechanically respirated with halothane anesthesia (0.5-2.0%) as needed. Animals were subjected to unilateral trigeminalectomy as described (15). In this procedure, trigeminal ganglia cell bodies are destroyed and perivascular fibers degenerate accordingly. Shamoperated animals were subjected to craniectomy, exposure of the trigeminal ganglia, as well as an equivalent amount of brain retraction as required for the ganglionectomy.The trigeminal root (that section between the ganglion and the brainstem) was approached by a left suboccipital craniectomy, which extended laterally and ...

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Immunoelectron microscopic study of substance P-containing fibers in feline cerebral arteries

Cited by 50 publications

References 47 publications

Innervation and Effects of Dilatory Neuropeptides on Cerebral Vessels

Innervation and Effects of Dilatory Neuropeptides on Cerebral Vessels

Innervation of the dura mater encephali of cat and rat: ultrastructure and calcitonin gene-related peptide-like and substance P-like immunoreactivity

Trigeminovascular fibers increase blood flow in cortical gray matter by axon reflex-like mechanisms during acute severe hypertension or seizures.

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