Elsevier

Neuroscience

Volume 60, Issue 3, June 1994, Pages 745-759
Neuroscience

Projections of nitric oxide synthase-containing fibers from the sphenopalatine ganglion to cerebral arteries in the rat

https://doi.org/10.1016/0306-4522(94)90502-9Get rights and content

Abstract

The origin and distribution of cerebral perivascular nerves containing nitric oxide, a short-acting messenger or neurotransmitter, have been studied in the rat by histochemistry for reduced nicotinamide adenine dinucleotide phosphate-diaphorase activity, a specific marker for neuronal nitric oxide synthase. Positively stained nerve fibers were distributed throughout the major vessels of the cerebral arteries, though the fiber density was higher in the anterior circulation, including the circle of Willis, than in the posterior arteries. Examination using axonal transport methods indicated that nitric oxide-containing neurons in the sphenopalatine ganglion innervate the cerebral arteries bilaterally. Nitric oxide synthase in these ganglionic cells often co-existed with vasoactive intestinal polypeptide.

The anatomical information obtained is discussed in terms of non-adrenergic, non-cholinergic neuronal transmission in the cerebral arteries.

References (54)

  • MatsuyamaT. et al.

    Overall distribution of vasoactive intestinal polypeptide-containing nerves on the wall of cerebral arteries: an immunohistochemical study using whole-mounts

    Neuroscience

    (1983)
  • SawchenkoP.E. et al.

    A method for tracing biochemically defined pathways in the central nervous system using combined fluorescence retrograde transport and immunohistochemical techniques

    Brain Res.

    (1981)
  • SuzukiN. et al.

    Cerebrovascular NADPH diaphorase-containing nerve fibers in the rat

    Neurosci. Lett.

    (1993)
  • SuzukiN. et al.

    Neuropeptide Y co-exists with vasoactive intestinal polypeptide and acetylcholine in parasympathetic cerebrovascular nerves originating in the sphenopalatine, otic, and internal carotid ganglia of the rat

    Neuroscience

    (1990)
  • TodaN. et al.

    Modification by l-NG-monomethyl arginine (l-NMMA) of the response to nerve stimulation in isolated dog mesenteric and cerebral arteries

    Jap. J. Pharmac.

    (1990)
  • TodaN. et al.

    Possible role of nitric oxide in transmitting information from vasodilator nerve to cerebroarterial muscle

    Biochem. biophys. Res. Commun.

    (1990)
  • TohyamaI. et al.

    Quantitative morphometric analysis of two types of serotonin-immunoreactive nerve fibres differentially responding to p-chlorophenylalanine treatment in the rat brain

    Neuroscience

    (1988)
  • TomimotoH. et al.

    An economic anterograde axonal tracing method using Phaseolus vulgaris agglutinin (PHA) P-form

    J. Neurosci. Meth.

    (1987)
  • TomimotoH. et al.

    Descending projections of the basal forebrain in the rat demonstrated by the anterograde neural tracer Phaseolus vulgaris leucoagglutinin (PHA-L)

    Brain Res.

    (1987)
  • AfeworkM. et al.

    Colocalization of nitric oxide synthase and NADPH-diaphorase in rat adrenal gland

    Neuroreport

    (1992)
  • AimiY. et al.

    Localization of NADPH-diaphorase-containing neurons in sensory ganglia of the rat

    J. comp. Neurol.

    (1991)
  • BredtD.S. et al.

    Localization of nitric oxide synthase indicating a neural role for nitric oxide

    Nature

    (1990)
  • BultH. et al.

    Nitric oxide as an inhibitory non-adrenergic non-cholinergic neurotransmitter

    Nature

    (1990)
  • DawsonT.M. et al.

    Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues

  • EdvinssonL. et al.

    Nerve fibers containing neuropeptide Y in the cerebrovascular bed: immunocytochemistry, radioimmunoassay, and vasomotor effects

    J. cerebr. Blood Flow Metab.

    (1987)
  • EdvinssonL. et al.

    Calcitonin gene-related peptide and cerebral blood vessels: distribution and vasomotor effects

    J. cerebr. Blood Flow Metab.

    (1987)
  • EdvinssonL. et al.

    Retrograde tracing of nerve fibers to the rat middle cerebral artery with true blue; colocalization with different peptides

    J. cerebr. Blood Flow Metab.

    (1989)
  • Cited by (65)

    • Distribution of vasoactive intestinal peptide, pituitary adenylate cyclase-activating peptide, nitric oxide synthase, and their receptors in human and rat sphenopalatine ganglion

      2012, Neuroscience
      Citation Excerpt :

      The cranial parasympathetic outflow is mediated in part through the SPG and in part via the otic ganglion. Cerebral and dural blood vessels are innervated by parasympathetic fibers (from SPG and otic ganglion) and by unmyelinated sensory nerve fibers (from trigeminal ganglion) (Edvinsson and Uddman, 1981, 2005; Nozaki et al., 1993; Minami et al., 1994). The activation of parasympathetic fibers can alter the status of the perivascular sensory pain fibers (Delépine and Aubineau, 1997).

    • Nitric oxide neurons and neurotransmission

      2010, Progress in Neurobiology
    • Roles of dorsal column pathway and transient receptor potential vanilloid type 1 in augmentation of cerebral blood flow by upper cervical spinal cord stimulation in rats

      2008, Neuroscience
      Citation Excerpt :

      Electrical stimulation of sphenopalatine ganglion or postganglionic fibers significantly increased CBF in the ipsilateral and contralateral parietal cortex independent of cerebral metabolism in rats (Seylaz et al., 1988; Suzuki et al., 1990), and cats (Goadsby, 1990). Nitric oxide and vasoactive intestinal polypeptide often co-exist in these postganglionic fiber terminals perivascularly innervating the cerebral arteries in rats (Iadecola et al., 1993; Minami et al., 1994). Thus, it was reasonable to suggest that a potential pathway, i.e. dorsal column nuclei, rostral ventrolateral medulla, sphenopalatine ganglion, and cortical vascular beds, could be activated by cSCS and produce an augmentation of CBF observed in the present study.

    • Peripheral Autonomic Pathways

      2003, The Human Nervous System: Second Edition
    • Neurogenic cerebral vasodilation mediated by nitric oxide

      2002, Japanese Journal of Pharmacology
    View all citing articles on Scopus
    View full text