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      Heterogeneity of Vascular Innervation in Hamster Cheek Pouch and Retractor Muscle

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          The hamster cheek pouch and its retractor muscle have provided valuable insights into microvascular physiology of an epithelial tissue and striated muscle, respectively. Nevertheless, the innervation of these vascular beds has not been resolved. This study has investigated the nature of autonomic and sensory innervation of these vascular beds and has tested whether it varies within or between tissues. Multiple-labelling immunohistochemistry identified autonomic and peptide-containing sensory nerve fibres. Presumptive sympathetic vasoconstrictor axons with immunoreactivity (IR) for tyrosine hydroxylase (TH) and neuropeptide Y (NPY) innervated feed arteries and arterioles (but not veins or venules) of the retractor and anterior (muscular) cheek pouch; these axons were absent from the posterior (epithelial) region of the cheek pouch, as confirmed by catecholamine fluorescence. Presumptive autonomic vasodilator axons with IR for vasoactive intestinal peptide (VIP) consistently innervated feed arteries and proximal arterioles of the cheek pouch, but generally not those of the retractor muscle nor distal arterioles of either tissue. Sparse presumptive sensory axons with IR for calcitonin gene-related peptide (CGRP) and substance P were found near arterial and venous vessels in all regions of the cheek pouch and retractor muscle; CGRP-IR was also located in motor end plates associated with striated muscle fibres. Such regional differences in vascular innervation by autonomic and sensory neurons may selectively effect local and regional control of blood flow between and within vascular beds.

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          Most cited references 7

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          Co-localization of calcitonin gene-related peptide-like immunoreactivity with substance P in cutaneous, vascular and visceral sensory neurons of guinea pigs.

          Calcitonin gene-related peptide (CGRP) has been immunohistochemically co-localized with substance P (SP) in capsaicin-sensitive, varicose axons supplying the skin, viscera and cardiovascular system of the guinea pig. After treatment with colchicine in vitro, 82% of SP neurons in the dorsal root ganglia contained CGRP-like immunoreactivity while 96% of CGRP neurons were immunoreactive for SP. Both CGRP- and SP-like immunoreactive material are transported peripherally and centrally from dorsal root ganglia. Thus, in tissues such as the gut where there are intrinsic nerves containing SP but lacking CGRP, CGRP-like immunoreactivity is a useful means of specifically labelling axons of most sensory neurons containing SP.
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            Perivascular nerves with immunoreactivity to vasoactive intestinal polypeptide in cephalic arteries of the cat: distribution, possible origins and functional implications.

            The distribution of nerves containing vasoactive intestinal polypeptide(VIP)-immunoreactive material was examined in the cephalic arteries and cranial nerves of cats using an indirect immunofluorescence procedure on whole mounts. Perivascular VIP-immunoreactive nerves were widely distributed in arteries and arterioles supplying glands, muscles and mucous membranes of the face. Within the cerebral circulation, perivascular VIP-immunoreactive nerves were most abundant in the circle of Willis and the proximal portions of the major cerebral arteries and their proximal branches supplying the rostral brainstem and ventral areas of the cerebral cortex. Nerves containing VIP-immunoreactive material were absent from distal portions of arteries supplying the posterior brainstem, cerebellum and dorsal cerebral cortex. Cerebral perivascular VIP-immunoreactive nerves had extracerebral origins probably from VIP-immunoreactive perikarya within microganglia in the cavernous plexus and external rete. Extracerebral perivascular VIP-immunoreactive nerves probably arose from VIP-immunoreactive perikarya in microganglia associated with the tympanic plexus, chorda tympani, lingual nerve and Vidian nerve as well as from cells in the otic, sphenopalatine, submandibular and sublingual ganglia. Therefore, it seems likely that each major segment of the cephalic circulation is supplied by local VIP-immunoreactive neurons. If the VIP-immunoreactive nerves cause vasodilation, they are well placed to allow redistribution of arterial blood flow within the head. During heat stress, neurogenic vasodilation of the appropriate beds would permit efficient cooling of cerebral blood, particularly that supplying the rostral brainstem and surrounding areas of the cerebral cortex.
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              Sympathetic noradrenergic neurons containing dynorphin but not neuropeptide Y innervate small cutaneous blood vessels of guinea-pigs.

              We have used double-labelling immunofluorescence techniques and retrograde axonal transport of Fast Blue to characterize three populations of sympathetic noradrenergic neurons innervating blood vessels in the hairless skin of the ears and paws of guinea-pigs. Each population of neurons innervated a specific level of the vascular bed, and had a distinctive content of neuropeptides. Sympathetic noradrenergic neurons innervating large distributing arteries contained immunoreactivity to neuropeptide Y. Neurons innervating smaller cutaneous arteries contained immunoreactivity to prodynorphin-derived peptides in addition to neuropeptide Y. Finally, sympathetic neurons innervating the smallest arterioles, and arterio-venous anastomoses, contained immunoreactivity to prodynorphin-derived peptides, but had no detectable neuropeptide Y. Although the major form of dynorphin immunoreactivity in perivascular sympathetic axons was dynorphin A(1-8), immunoreactivity to both dynorphin A(1-8) and dynorphin A(1-17) occurred in the cell bodies of these neurons, suggesting that dynorphin A is processed during axonal transport to the terminals. The perivascular sympathetic neurons containing prodynorphin-derived peptides but not neuropeptide Y are most likely to be involved in the regulation of thermoregulatory cutaneous vascular circuits.

                Author and article information

                J Vasc Res
                Journal of Vascular Research
                S. Karger AG
                December 1999
                24 December 1999
                : 36
                : 6
                : 465-476
                aDepartment of Anatomy and Histology, and Centre for Neuroscience, School of Medicine, Flinders University of South Australia, Adelaide, S.A., Australia; bThe John B. Pierce Laboratory Inc., and Department of Cellular and Molecular Physiology, Yale University School of Medicine, New Haven, Conn., USA
                25689 J Vasc Res 1999;36:465–476
                © 1999 S. Karger AG, Basel

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                Page count
                Figures: 6, Tables: 3, References: 46, Pages: 12
                Research Paper


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