Dural Headache and Innervation of the Dura Mater

Penfield, Wilder; McNaughton, Francis L.

doi:10.1097/00005053-194112000-00023

Cited by 76 publications

(134 citation statements)

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“…Both neurogenic plasma extravasation and headache can be blocked by aspirin and in selected cases, by indomethacin pretreatment (Buzzi et al, 1989). A central role in migraine pathogenesis has been proposed for dural vessels (Penfield & McNaughton, 1940). Dural vessels are among the few pain-sensitive intracranial tissues (Ray & Wolff, 1940); they contain structures important to the development of neurogenic inflammation, namely fenestrated capillary venules surrounded by a network of neuropeptide-containing unmyelinated C-fibres and mast cells (McNaughton, 1938;Andres et al, 1987).…”

Section: Receptor Localizationmentioning

confidence: 99%

Further characterization of the putative 5‐HT receptor which mediates blockade of neurogenic plasma extravasation in rat dura mater

Buzzi

Moskowitz

Peroutka

et al. 1991

British J Pharmacology

102

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1 We describe the effects of pretreatment with 5-hydroxytryptamine (5-HT) receptor agonists and antagonists on neurogenically-mediated plasma protein extravasation (["25I]-albumin) in rat dura mater and in extracranial tissues (temporalis muscle fascia, conjunctiva, eyelid and lip) induced by electrical stimulation of the right trigeminal ganglion. 2 Leakage of [25I]-bovine serum albumin from blood vessels in dura mater following high intensity stimulation (1.2 mA, Sims, 5Hz for 5min) was significantly reduced by the intravenous administration of drugs active at 5-HT receptors with some selectivity for the 5-HT1 receptor subtypes: 5-carboxamidotryptamine (5-CT) (threshold dose, 1ngkg-1); 5-benzyloxytryptamine (5-BT) (10, 30 or 100augkg-1); 8-hydroxydipropylaminotetralin (8-OH-DPAT) (300pigkg-1); and as previously reported, sumatriptan (lOOpugkg -), dihydroergotamine (DHE) (SOugkg 1), ergotamine tartrate (lOO1ugkg 1) and chronically administered methysergide (1 mgkg-1).3 The putative 5-HT receptor antagonist, metergoline lOOpgkg-1, inhibited partially the effect of sumatriptan in dura mater providing additional evidence for a 5-HT1 receptor subtype-mediated mechanism, although it was not effective against 5-CT (1 ng kg-1). Methiothepin (300,ug kg-1) did not affect the response to sumatriptan. When administered at high concentrations (1 mg kg 1) methiothepin and metergoline decreased plasma protein extravasation in rat dura mater. 4 Pretreatment with the 5-HT2 receptor antagonists pizotifen, 300pugkg 1, or ketanserin, 300,ugkg ', or the 5-HT3 receptor antagonists MDL 72222, 300,ugkg-1, or ICS 205-930, 300pgkg-1, did not affect plasma protein leakage following electrical trigeminal stimulation. Blockade by sumatriptan of plasma protein extravasation was not inhibited by pizotifen (300,ug kg-1) or MDL 72222 (300pg kg-').5 The 5-HT receptor(s) mediating this response were present only on intracranial tissues innervated by the trigeminal nerve; plasma protein extravasation in extracranial tissues was not blocked by pretreatment with the equivalent or higher concentrations of the above drugs following low intensity trigeminal stimulation (0.1 mA, 5 ms, 5 Hz). 6 The putative 5-HT receptor(s) mediating this response were not present on sympathetic fibres innervating dura mater since unilateral removal of the superior cervical ganglion did not prevent the development of plasma protein extravasation nor did it affect the blockade by sumatriptan IOOpug kg-'. 7 The above pharmacological data suggest that intracranial vessels possess 5-HT receptor(s) which are coupled to inhibition of neurogenically-mediated plasma protein extravasation. These receptors cannot be detected on extracranial cephalic blood vessels innervated by the trigeminal nerve, although available evidence strongly suggests that the 5-HT receptors reside on perivascular trigeminal nerve fibres. The rank order of effective doses (threshold concentrations; 5-CT < 5-BT < DHE < sumatriptan < 8-OHDPAT) is most consistent with a 5-HTlB-or 5-HTlD-mediated response, ...

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Section: Receptor Localizationmentioning

confidence: 99%

Further characterization of the putative 5‐HT receptor which mediates blockade of neurogenic plasma extravasation in rat dura mater

Buzzi

Moskowitz

Peroutka

et al. 1991

British J Pharmacology

102

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“…The pathophysiology underlying the pulsating quality of the migraine pain is not yet fully understood; however, activation of the dense plexus of trigeminal afferents that innervate the cranial blood vessels may have some role . It has been recognized for some time that most of the intracranial structures, including the dura mater and blood vessels, are painproducing, especially when electrical stimulation is used (Penfield, 1932(Penfield, , 1934Penfield and McNaughton, 1940;Wolff, 1948;Feindel et al, 1960).…”

mentioning

confidence: 99%

Orexin 1 Receptor Activation Attenuates Neurogenic Dural Vasodilation in an Animal Model of Trigeminovascular Nociception

Holland¹,

Akerman²,

Goadsby³

2005

J Pharmacol Exp Ther

120

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The pathophysiology underlying the pulsating quality of the pain of a migraine attack is not fully understood, although trigeminal vascular afferents containing the sensory neuropeptide calcitonin gene-related peptide (CGRP) must have a role. Antimigraine drugs, such as triptans, serotonin 5-hydroxytryptamine 1B/1D receptor agonists, reproducibly block neurogenic vasodilation associated with CGRP release. We examined the effects of the hypothalamic neuropeptides orexin A and orexin B on neurogenic dural vasodilation, dissecting out the receptor pharmacology with the novel orexin 1 (OX 1 ) receptor antagonist N-(2-methyl-6-benzoxazolyl)-NЉ-1,5-naphthyridin-4-yl urea (SB-334867). Electrical stimulation of dural afferents (50 -300 A) resulted in reproducible dural vasodilation of 136 Ϯ 9%. Orexin A 30 g kg Ϫ1 , but not 3 and 10 g kg Ϫ1 ,inhibited the dilation brought about by electrical stimulation over 60 min and maximally after 15 min by 60% (t 7 ϭ 7.138; P Ͻ 0.001; n ϭ 8). This response was reversed by pretreatment with the OX 1 receptor antagonist SB-334867. Addition of CGRP at the point of maximal effect of orexin A produced a further significant decrease in neurogenic dural vasodilation compared with orexin A only. CGRP administration (1 g kg Ϫ1 ) produced a reproducible dural blood vessel dilation of 145 Ϯ 7% that was not inhibited by intravenous administration of orexin A (30 g kg Ϫ1 ). Orexin B had no significant effect even at the highest dose. The current study demonstrates that orexin A is able to inhibit neurogenic dural vasodilation via activation of the OX 1 receptor, resulting in inhibition of prejunctional release of CGRP from trigeminal neurons.

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“…Anatomical studies have shown that the trigeminal nerve gives rise to a sensory innervation of the major blood vessels of the intracranial meninges (Penfield and McNaughton, 1940;Feindel et al, 1960;Fang, 1961;Mayberg et al, 1984;Keller et al, 1985;O'Connor and van der Kooy, 1986;Andres et al, 1987;Ruskell and Simons, 1987;Ruskell, 1988). This intracranial trigeminal sensory innervation supplies both the major pial arteries that branch from the Circle of Willis, as well as the meningeal arteries and venous sinuses of the dura mater.…”

mentioning

confidence: 99%

Axon diameters and intradural trajectories of the dural innervation in the rat

Strassman

Weissner

Williams

et al. 2004

J of Comparative Neurology

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Neurophysiological studies have characterized the sensory responses of primary afferent nociceptors that innervate the intracranial dura. The present study used anatomical methods to examine in greater detail the axonal trajectories within the dura, as well as the axonal size distribution of the dural innervation. Immunostaining for CGRP in dural wholemounts revealed a network of fibers extending across the entire dura, with an especially dense plexus running along the borders of the transverse and superior sagittal sinuses. The plexus along the caudal border of the transverse sinus partially overlapped the dural area that shows the greatest density of mast cells. Visualization of axon bundles by DiI application in formalin-fixed tissue revealed two separate systems of fibers in the dura that could be distinguished by the orientation of their trajectories: one that runs parallel to the middle meningeal artery (MMA), and another with a more or less orthogonal orientation that runs rostromedially from the transverse sinus across the MMA. Axons traversed large distances across the dura, but the majority of the branching and arborization was usually concentrated in the distal part of the trajectory. In separate animals, measurement of myelinated axon diameters with electron microscopy showed that approximately one-third of the myelinated axons in the nerves supplying the dura (nervus spinosus and tentorial nerves) could be classified as A-beta, since they were comparable in size to the majority of axons in the trochlear nerve and the upper end of the size range in the trigeminal nerve (i.e., > 5 microm).

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Dural Headache and Innervation of the Dura Mater

Cited by 76 publications

References 0 publications

Further characterization of the putative 5‐HT receptor which mediates blockade of neurogenic plasma extravasation in rat dura mater

Further characterization of the putative 5‐HT receptor which mediates blockade of neurogenic plasma extravasation in rat dura mater

Orexin 1 Receptor Activation Attenuates Neurogenic Dural Vasodilation in an Animal Model of Trigeminovascular Nociception

Axon diameters and intradural trajectories of the dural innervation in the rat

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