Innervation of cerebral arteries by nerves containing 5-hydroxytryptamine and noradrenaline

https://doi.org/10.1016/0163-7258(95)02017-9Get rights and content

Abstract

Noradrenaline (NA)-containing nerves, mainly originating in the sympathetic superior cervical ganglia, supply large and small cerebral arteries. In large cerebral arteries, nerves containing serotonin (5-hydroxytryptamine, 5-HT) may represent neuronal uptake of circulating 5-HT by sympathetic nerves. 5-HT-containing nerves supplying small pial vessels probably have a central origin in the dorsal raphe nucleus. In most species, NA is a weak vasoconstrictor (α1- or α2-adrenoceptors), while 5-HT is a potent vasoconstrictor (5-HT2 or 5-HT1-like receptors) of large cerebral arteries. In contrast, both NA and 5-HT tend to cause vasodilatation in small pial vessels and arterioles. Adrenergic and serotonergic transmission can be modulated by pH, a range of putative neurotransmitters and neuromodulators, and by the endothelium. Sumatriptan, a 5-HT1-like receptor agonist, has been shown to be effective in the treatment of migraine. Changes in NA- or 5-HT-containing nerves and/or in the responses of cerebral vessels to NA and 5-HT have been observed in a variety of vascular disorders, including cerebral vasospasm following subarachnoid haemorrhage, hypertension, and atherosclerosis.

References (256)

  • J.-Y. Chang et al.

    Evidence for coexistence of serotonin and noradrenaline in sympathetic nerves supplying brain vessels of guinea pig

    Brain Res.

    (1988)
  • J.-Y. Chang et al.

    Serotonin uptake into cerebrovascular nerve fibers of rat, visualization by immunohistochemistry, disappearance following sympathectomy, and release during electrical stimulation

    Brain Res.

    (1989)
  • A. Chedotal et al.

    Serotonin-synthesizing nerve fibers in rat and cat cerebral arteries and arterioles: immunohistochemistry of tryptophan-5-hydroxylase

    Neurosci. Lett.

    (1990)
  • A.H. Clark et al.

    Ca2+ channel antagonists and inhibition of protein kinase C each block contraction but not depolarization to 5-hydroxytryptamine in the rabbit basilar artery

    Eur. J. Pharmacol.

    (1993)
  • Z. Cohen et al.

    Cerebrovascular nerve fibers immunoreactive for tryptophan-5-hydroxylase in the rat: distribution, putative origin and comparison with sympathetic noradrenergic nerves

    Brain Res.

    (1992)
  • T. Cowen et al.

    5-HT-containing nerves to major cerebral arteries of the gerbil originate in the superior cervical ganglia

    Brain Res.

    (1986)
  • T. Cowen et al.

    Origin and postnatal development of nerves showing 5-hydroxytryptamine-like immunoreactivity supplying major cerebral arteries of the rat

    Neurosci. Lett.

    (1987)
  • V. Deckert et al.

    Evidence that 5-HT2 receptors predominantly mediate the contraction of the rat basilar artery to 5-hydroxytryptamine

    Eur. J. Pharmacol.

    (1992)
  • J. De Keyser et al.

    Subtypes of adrenergic and dopaminergic receptors in bovine cerebral blood vessels

    Neurosci. Lett.

    (1988)
  • J. De Keyser et al.

    What intracranial tissues in humans contain sumatriptan-sensitive serotonin 5-HT1-type receptors?

    Neurosci. Lett.

    (1993)
  • J.J. Descombes et al.

    Endothelial thromboxane production plays a role in the contraction caused by 5-hydroxytryptamine in rat basilar arteries

    Eur. J. Pharmacol.

    (1993)
  • U. Dhall et al.

    Eifect of oestrogen and progesterone on noradrenergic nerves and on nerves showing serotonin-like immunoreactivity in the basilar artery of the rabbit

    Brain Res.

    (1988)
  • K.K. Dhital et al.

    Increased density of perivascular nerves to the major cerebral vessels of the spontaneously hypertensive rat: differential changes in noradrenaline and neuropeptide Y during development

    Brain Res.

    (1988)
  • G. Diéguez et al.

    Rete mirabile of goat: in vitro effects of adrenergic stimulation

    Brain Res.

    (1983)
  • G. Diéguez et al.

    In vitro studies of the carotid rete mirabile of Artiodactyla

    Microvasc. Res.

    (1987)
  • L. Edvinsson

    Sympathetic control of cerebral circulation

    Trends Neurosci.

    (1982)
  • L. Edvinsson et al.

    Autonomic nerves, mast cells, and amine receptors in human brain vessels. A histochemical and pharmacological study

    Brain Res.

    (1976)
  • L. Edvinsson et al.

    Reduced noradrenaline uptake and retention in cerebrovascular nerves associated with angiographically visible vasoconstriction following experimental subarachnoid hemorrhage in rabbits

    Brain Res. Bull.

    (1982)
  • M. Ferrer et al.

    Comparison of the vasoconstrictor responses induced by endothelin and phorbol 12,13-dibutyrate in bovine cerebral arteries

    Brain Res.

    (1992)
  • P.W. Abel et al.

    Effects of neuropeptide Y on contraction, relaxation, and membrane potential of rabbit cerebral arteries

    J. Cardiovasc. Pharmacol.

    (1989)
  • I. Akiguchi et al.

    Sympathetic nerve terminals in the tunica media of human superficial temporal and middle cerebral arteries: wet histofluorescence

    Stroke

    (1983)
  • C. Alafaci et al.

    Perivascular nerve types supplying cerebral blood vessels of the gerbil

    Acta Physiol. Scand.

    (1986)
  • C. Alafaci et al.

    Noradrenergic innervation of gerbil large cerebral arteries

    Blood Vessels

    (1986)
  • C. Alafaci et al.

    Histochemical and immunohistochemical study of noradrenergic, serotonergic and peptidergic innervation of the cerebral circulation

    Funct. Neurol.

    (1987)
  • E. Alexander et al.

    The identification of adrenergic receptors in human pial membranes

    Neurosurgery

    (1990)
  • H. Araki et al.

    Effect of superior cervical ganglionectomy on the sensitivity of rabbit ear artery and cerebral arteries of rabbit and cat to vasoactive agents

    J. Pharmacol. Exp. Ther.

    (1982)
  • S. Arribas et al.

    Characterization of the subtype of presynaptic α2-adrenoceptors modulating noradrenaline release in cat and bovine cerebral arteries

    J. Pharm. Pharmacol.

    (1991)
  • L.M. Auer et al.

    Effect of sympathetic nerve stimulation and adrenoceptor blockade on pial arterial and venous calibre and on intracranial pressure in the cat

    Acta Physiol. Scand.

    (1983)
  • L.M. Auer et al.

    Effect of serotonin and its antagonist ketanserin on pial vessels

    J. Cereb. Blood Flow Metab.

    (1985)
  • K. Ayajiki et al.

    Regional difference in the response mediated by β1-adrenoceptor subtype in bovine cerebral arteries

    J. Cereb. Blood Flow Metab.

    (1992)
  • D.G. Baramidze et al.

    Pattern and innervation of pial microvascular effectors which control blood supply to cerebral cortex

    Blood Vessels

    (1982)
  • M.T. Barrús et al.

    Receptors involved in the modulation of 5-hydroxytryptamine release in bovine cerebral arteries

    J. Pharm. Pharmacol.

    (1992)
  • D.I. Barry

    Cerebral blood flow in hypertension

    J. Cardiovasc. Pharmacol.

    (1985)
  • G.C.J. Bauknight et al.

    Endothelium-derived relaxing factor modulates noradrenergic constriction of cerebral arterioles in rabbits

    Stroke

    (1992)
  • G.L. Baumbach et al.

    Effects of sympathetic stimulation and changes in arterial pressure on segmental resistance of cerebral vessels in rabbits and cats

    Circ. Res.

    (1983)
  • J.A. Bevan et al.

    Sympathetic control of cerebral arteries: specialization in receptor type, reserve, affinity, and distribution

    FASEB J.

    (1987)
  • G. Bonvento et al.

    Differential effects of electrical stimulation of the dorsal raphe nucleus and of cervical sympathectomy on serotonin and noradrenaline concentrations in major cerebral arteries and pial vessels in the rat

    J. Cereb. Blood Flow Metab.

    (1990)
  • G. Bonvento et al.

    Evidence for differing origins of the serotonergic innervation of major cerebral arteries and small pial vessels in the rat

    J. Neurochem.

    (1991)
  • P.B. Bradley et al.

    Evidence for the existence of 5-hydroxytryptamine receptors, which are not of the 5-HT2 type, mediating contraction of rabbit isolated basilar artery

    Br. J. Pharmacol.

    (1986)
  • L. Brandt et al.

    Effects of extracellular calcium and of calcium antagonists on the contractile responses of isolated human pial and mesenteric arteries

    J. Cereb. Blood Flow Metab.

    (1981)
  • Cited by (61)

    • Reorganizations of latency structures within the white matter from wakefulness to sleep

      2022, Magnetic Resonance Imaging
      Citation Excerpt :

      However, there were lingering concerns about the physiological sources underlying the latency structure in WM. The most mentioned potential source relates to a recent finding of sympathetic responses giving rise to large changes in BOLD signals in the WM (and GM) with a significant time delay [25]. The delay is consistent with the perfusion time between brain regions, and thus, the pial artery contractions caused by extrinsic sympathetic innervation [26,27] have been modeled as the source driving such fMRI changes [25], which were presumed to further yield latency structures. Notably, the progression from NREM sleep into deeper stages was accompanied by a shift in autonomic balance from sympathetic to parasympathetic dominance [28], based on which nonspecific regions that show significant variations in latencies between paired stages are expected to be activated due to changes in systematic sympathetic tone over upper stream extracranial arteries.

    • Hemodynamics in acute stroke: Cerebral and cardiac complications

      2021, Handbook of Clinical Neurology
      Citation Excerpt :

      Such segmental discrepancies in autonomic innervation lead to a heterogeneous segmental vascular response to neural mediators. Norepinephrine (in the presence of alpha-adrenoreceptors) and serotonin are shown to cause vasoconstriction in pial arteries, but due to an abundance of beta-adrenoreceptors in parenchymal vessels (Lincoln, 1995) norepinephrine may cause vasodilation (Cipolla et al., 2004). In addition to a segmental heterogeneity, there are regional differences in autonomic innervation: sympathetic nerves have a denser presence on the anterior circulation compared with vertebrobasilar arteries and their branches (Edvinsson et al., 1976), which has led to a differential response to hypertension: Cerebral autoregulatory response to hypertension is generally shown to be more effective in the posterior circulation through mounting a vasoconstrictive response and moderating CBF (Faraci et al., 1987).

    • Preeclampsia postpartum: Impairment of cerebral autoregulation and reversible cerebral hyperperfusion

      2019, Pregnancy Hypertension
      Citation Excerpt :

      This could be explained by the better preserved DCA in the PCA as compared to the MCA. The susceptibility to edema formation during preeclampsia especially in posterior areas of the brain indicates that additional factors like reduced sympathetic innervation of the PCA might play a role [27–29]. Regional differences in cerebral autoregulation and vascular sympathetic innervation were also observed in pregnant rats [27].

    • Partial pharmacologic blockade shows sympathetic connection between blood pressure and cerebral blood flow velocity fluctuations

      2016, Journal of the Neurological Sciences
      Citation Excerpt :

      While Cencetti et al. presume that PA-shortening upon sympathetic activation is due to “stiffening” of distal cerebral vessels [29], we assume that there are opposing sympathetic effects on proximal, cerebral artery segments and on the distal cerebral arterioles. Sympathetic innervation is denser and primarily alpha-adrenergic at the proximal cerebral arteries than at the distal, primarily beta2-adrenergic cerebral arterioles [1,9,57–60]. Thus, the CPS associated CBFV increase and PA-shortening are likely to result from sympathetically mediated alpha-adrenergic vasoconstriction at the proximal MCA, i.e. at the site of our TCD-insonation, and from beta-adrenergic vasodilatation at distal cerebral resistance vessels [1,10].

    View all citing articles on Scopus
    View full text