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Development of the sympathetic innervation to the cerebral arterial system in neonatal rats as revealed by anterograde labeling with wheatgerm agglutinin-horseradish peroxidase

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Abstract

In order to clarify the developmental pattern in the sympathetic nerve fibers innervating the cerebral arterial system during the postnatal period in rats, we labeled the postganglionic nerve fibers originating in the superior cervical ganglion (SCG) and directly observed their extension and plexus formation by means of anterograde labeling with wheat germ agglutinin-horseradish peroxidase (WGA-HRP). The WGA-HRP solution was injected into the right SCG 1–7 days after birth. The rats were killed 48 h after trace injection, and the cerebral arteries were reacted with tetramethylbenzidine, then observed as a whole mount preparation. The labeled nerve fibers appeared as a few relatively straight bundles with branching fibers running longitudinally to the long axis of the artery in the ipsilateral right side of the circle of Willis and proximal portion of their main branching arteries at 3 days after birth. The nerve fibers started to form a circular pattern of nerve plexus only on the wall of the circle of Willis as early as 1 week after birth. At the beginning of postnatal week 2, labeled nerve fibers extended the collateral projections into the collateral side of the circle of Willis, and these expanding projections could not be observed at postnatal week 3. We observed a route of the sympathetic nerve fibers advancing into the cerebral arterial system which has not been described in previous studies; bundle of labeled nerve fibers entered into the wall of the middle portion of the basilar artery in half of the animals, in any postnatal period. We were able to confirm, by using an anterograde labeling technique with WGA-HRP, how the sympathetic nerve fibers advance into the cerebral arterial system, when they start to form nerve plexus during the postnatal period in rats, and clarified that the sympathetic nerve fibers showed overabundant collateral projection in the cerebral arterial system during the early postnatal period.

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References

  • Arbab MAR, Wiklund L, Delgado T, Svendgaard NA (1988) Stellate ganglion innervation of the vertebro-basilar arterial system demonstrated in the rat with anterograde and retrograde WGA-HRP tracing. Brain Res 445:175–180

    Google Scholar 

  • Allen JM, Schon F, Todd N, Yeates JC, Crockard HA, Bloom SR (1984) Presence of neuropeptide Y (NPY) in human circle of Willis and its possible role in cerebral vasospasm. Lancet 2:550–552

    Google Scholar 

  • Bennett MR, Lavidis NA (1984) Development of the topographical projection of motor neurons to a rat muscle accompanies loss of polyneuronal innervation. J Neurosci 4:2204–2212

    Google Scholar 

  • Bevan RD (1984) Trophic effects of peripheral a vascular structure. Hypertension [Suppl III] pp 19–26

  • Brown MC, Jansen JKS, Van Essen D (1976) Polyneuronal innervation of skeletal muscle in new-born rats and its elimination during maturation. J Physiol 261:387–422

    Google Scholar 

  • Cowan WM, Fawcett JW, O'Leary DDM, Stanfield BB (1984) Regressive events in neurogenesis. Science 225:1258–1265

    Google Scholar 

  • Edvinsson L, Emson P, McCulloch J, Tatemoto K, Uddman R (1984) Neuropeptide Y: immunocytochemical localization to and effect upon feline pial arteries and veins in vitro and in situ. Acta Physiol Scand 122:155–163

    Google Scholar 

  • Falck B, Mchedlishvili GI, Owman C (1965) Histochemical demonstration of adrenergic nerves in cortex-pia of rabbit. Acta Pharmacol Toxicol 23:133–142

    Google Scholar 

  • Handa Y, Caner H, Hayashi M, Tamamaki N, Nojyo Y (1990) The distribution pattern of the sympathetic nerve fibers to the cerebral arterial system in rats as revealed by anterograde labeling with WGA-HRP. Exp Brain Res 82:493–498

    Google Scholar 

  • Handa Y, Nojyo Y, Hayashi M (1991) Patterns of reinnervation of denervated cerebral arteries by sympathetic nerve fibers after unilateral ganglionectomy in rats. Exp Brain Res 86:82–89

    Google Scholar 

  • Handa Y, Nojyo Y, Ishiguro H, Nagatsu I (1992) Plasticity of the sympathetic nervous system innervating the cerebral arteries in rats. Exp Neurol 118:324–331

    Google Scholar 

  • Heisted DD, Marcus ML, Abbound FM (1978) Experimental attempts to unmask effects of neural stimuli on cerebral blood flow. In: Purves MJ (eds) Cerebral vascular smooth muscle and its control. Elsevier, Amsterdam, pp 97–111

    Google Scholar 

  • Hill CE, Vidovic M (1989) The role of competition in the refinement of the projections of sympathetic neurons to the rat eye during development. Int J Dev Neurosci 7:539–551

    Google Scholar 

  • Hubel DH, Wiesel TN, LeVay S (1977) Plasticity of ocular dominance columns in monkey striate cortex. Philos Trans R Soc Lond [Biol] 278:377–409

    Google Scholar 

  • Jackson H, Parks TN (1982) Functional synapse elimination in the developing avian cochlear nucleus with simultaneous reduction in cochlear nerve axon branching. J Neurosci 2:1736–1743

    Google Scholar 

  • Jackson PC (1983) Reduced activity during development delays the normal rearrangement of synapses in the rabbit ciliary ganglion. J Physiol 345:319–327

    Google Scholar 

  • Johnson DA, Purves D (1981) Post-natal reduction of neural unit size in the rabbit ciliary ganglion. J Physiol 318:143–159

    Google Scholar 

  • Kajikawa H (1969) Mode of the sympathetic innervation of the cerebral vessels demonstrated by the fluorescent histochemical technique in rats and cats. Arch Jpn Chir 38:227–235

    Google Scholar 

  • Lichtman JW (1977) The reorganization of synaptic connexions in the rat submandibular ganglion during post-natal development. J Physiol 273:155–177

    Google Scholar 

  • Lichtman JW, Purves D (1980) The elimination of redundant preganglionic innervation to hamster sympathetic ganglion cells in early post-natal life. J Physiol 301:213–228

    Google Scholar 

  • Mesulam MM (1978) Tetramethylbenzidine for horseradish peroxidase neurohistochemistry: a non-carcinogenic blue reaction-product with superior sensitivity for visualizing neural afferents and efferents. J Histochem Cytochem 26:106–117

    CAS  PubMed  Google Scholar 

  • Nielsen KC, Owman C (1967) Adrenergic innervation of pial arteries related to the circle of Willis in the cat. Brain Res 6:773–776

    Google Scholar 

  • Nojyo Y, Tamamaki N, Matsuura T, Sano Y (1988) Histochemical and electron microscopical demonstration of the sympathetic nerve fibers joining to the fourth and the sixth cranial nerves in rats. Histochemistry 88:557–561

    Google Scholar 

  • Purves D, Lichtman JW (1980) Elimination of synapses in the developing nervous system. Science 210:153–157

    Google Scholar 

  • Redfern PA (1970) Neuromuscular transmission in new-born rats. J Physiol 209:701–709

    Google Scholar 

  • Tamamaki N, Nojyo Y (1987) Intracranial trajectories of sympathetic nerve fibers originating in the superior cervical ganglion in the rat: WGH-HRP anterograde labeling study. Brain Res 437:387–392

    Google Scholar 

  • Thompson W (1983) Synapse elimination in neonatal rat muscle in sensitive to pattern of muscle use. Nature 302:614–616

    Google Scholar 

  • Tolbert DL (1987) Intrinsically directed pruning as a mechanism regulating the elimination of transient collateral pathway. Brain Res Dev Brain Res 33:11–21

    Google Scholar 

  • Tsai SH, Tew JM, Shipley MT (1989) Cerebral arterial innervation II. Development of calcitonin-gene-related peptide and norepinephrine in the rat. J Comp Neurol 279:1–12

    Google Scholar 

  • Vidovic M, Hill C (1988) Withdrawal of collaterals of sympathetic axons to the rat eye during postnatal development: the role of function. J Auton Nerv Syst 22:57–65

    Google Scholar 

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Handa, Y., Nojyo, Y., Tamamaki, N. et al. Development of the sympathetic innervation to the cerebral arterial system in neonatal rats as revealed by anterograde labeling with wheatgerm agglutinin-horseradish peroxidase. Exp Brain Res 94, 216–224 (1993). https://doi.org/10.1007/BF00230289

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  • DOI: https://doi.org/10.1007/BF00230289

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