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. 1999 May;127(2):457-67.
doi: 10.1038/sj.bjp.0702561.

Capsaicin-insensitive sensory-efferent meningeal vasodilatation evoked by electrical stimulation of trigeminal nerve fibres in the rat

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Capsaicin-insensitive sensory-efferent meningeal vasodilatation evoked by electrical stimulation of trigeminal nerve fibres in the rat

B Peitl et al. Br J Pharmacol. 1999 May.

Abstract

1. Antidromic vasodilatation and plasma extravasation to stimulation of the trigeminal ganglion or its perivascular meningeal fibres was investigated by laser-Doppler flowmetry and 125I-labelled bovin serum albumin in the dura mater and in exteroceptive areas (nasal mucosa, upper eyelid) of anaesthetized rats pretreated with guanethidine and pipecuronium. 2 Trigeminal stimulation at 5 Hz for 20 s elicited unilateral phasic vasodilatation in the dura and lasting response in the nasal mucosa. Resiniferatoxin (1-3 microg kg(-1) i.v.), topical (1%) or systemic capsaicin pretreatment (300 mg kg(-1) s.c. plus 1 mg kg(-1) i.v.) did not inhibit the meningeal responses but abolished or strongly inhibited the nasal responses. Administration of vinpocetine (3 mg kg(-1) i.v.) increased both basal blood flow and the dural vasodilatation to perivascular nerve stimulation. 3. Dural vasodilatation to trigeminal stimulation was not inhibited by the calcitonin gene-related peptide-1 receptor (CGRP-1) antagonist hCGRP8-37 (15 or 50 microg kg(-1) i.v), or the neurokinin-1 receptor antagonist RP 67580 (0.1 mg kg(-1) i.v.) although both antagonists inhibited the nasal response. Neither mucosal nor meningeal responses were inhibited by atropine (5 mg kg(-1) i.v.), hexamethonium (10 mg kg(-1) i.v.) or the vasoactive intestinal polypeptide (VIP) antagonist (p-chloro-D-Phe6-Leul7)VIP (20 microg kg(-1) i.v.). 4. Plasma extravasation in the dura and upper eyelid elicited by electrical stimulation of the trigeminal ganglion was almost completely abolished in rats pretreated with resiniferatoxin (3 microg kg(-1) i.v.). 5. It is concluded that in the rat meningeal vasodilatation evoked by stimulation of trigeminal fibres is mediated by capsaicin-insensitive primary afferents, while plasma extravasation in the dura and upper eyelid and the vasodilatation in the nasal mucosa are mediated by capsaicin-sensitive trigeminal fibres.

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Figures

Figure 1
Figure 1
Meningeal blood flow enhancements evoked by electrical stimulation (15 V, 5 Hz, 0.5 ms, 20 s) of the dura mater before and after resiniferatoxin (RTX, 3 μg kg−1 i.v.) application (A). Meningeal and nasal blood flow enhancements evoked by electrical stimulation (15 V, 5 Hz, 0.5 ms, 20 s) of the ipsilateral trigeminal ganglion (B). Blood flow records of the ipsilateral and contralateral sides of the dura mater during electrical stimulation of the left trigeminal ganglion (C). BP: blood pressure, AU: arbitrary unit, MBF: meningeal blood flow, NBF: nasal blood flow, arrowheads: electrical stimulations, arrow: resiniferatoxin injection.
Figure 2
Figure 2
Left: Effect of vinpocetine infusion (3 mg kg−1 i.v. at a rate of 0.1 mg kg−1 min−1 for 30 min) on meningeal blood flow responses evoked by electrical stimulation (15 V, 5 Hz, 0.5 ms, 20 s) of the dura mater. The terminal part of a similar infusion of the solvent is also shown. Right: Per cent increase in blood flow values at the end of vinpocetine infusion [area under the curve (AUC); n=6; mean±s.e.mean *P<0.05]. BP: blood pressure, AU: arbitrary unit, MBF: meningeal blood flow, arrowheads: electrical stimulations.
Figure 3
Figure 3
Frequency-response curves of meningeal and nasal blood flow enhancements (means±s.e.mean) evoked by electrical stimulation (15 V, 0.5 ms, 100 impulses) of the ipsilateral trigeminal ganglion (n=6; max: response maximum; AUC: area under the curve).
Figure 4
Figure 4
Effect of guanethidine (8 mg kg−1 i.v.) and capsaicin (cumulative dose of 1 mg kg−1 i.v.) on blood pressure and on meningeal and nasal blood flow enhancements evoked by electrical stimulation (15 V, 5 Hz, 0.5 ms, 20 s) of the ipsilateral trigeminal ganglion in a capsaicin pretreated (total dose: 300 mg kg−1) rat. BP: blood pressure, AU: arbitrary unit, MBF: meningeal blood flow, NBF: nasal blood flow, arrowheads: electrical stimulations, arrows: injection of drugs.
Figure 5
Figure 5
Quantitative evaluation of the effect of resiniferatoxin (RTX, 3 μg kg−1 i.v.; n=15), local (1%; n=6) or systemic application of capsaicin (cumulative dose of 1 mg kg−1 i.v. in capsaicin pretreated rats with a total dose of 300 mg kg−1; n=6) on dural and nasal blood flow enhancement evoked by electrical stimulation (15 V, 5 Hz, 0.5 ms, 20 s) of the ipsilateral trigeminal ganglion. Responses are expressed as percentage deviation from control values (means±s.e.m). *P<0.05, **P<0.01. N.S., non significant.
Figure 6
Figure 6
Effect of hCGRP8–37 (15+35 μg kg−1 i.v.) on blood flow enhancement in the dura and nasal mucosa evoked by electrical stimulation (15 V, 5 Hz, 0.5 ms, 20 s) of the ipsilateral trigeminal ganglion. BP: blood pressure, AU: arbitrary unit, MBF: meningeal blood flow, NBF: nasal blood flow, arrowheads: electrical stimulations, arrows: injection of drug.
Figure 7
Figure 7
(A) Quantitative evaluation of the effect of hCGRP8–37 (15 μg kg−1 i.v.; n=6), atropine (5 mg kg−1 i.v.; n=6), hexamethonium (10 mg kg−1 i.v.; n=6), p-chloro-D-Phe6-Leu17-VIP (20 μg kg−1 i.v.; n=6) and RP 67580 (0.1 mg kg−1 i.v.; n=18) on the blood flow increase in the dura mater evoked by electrical stimulation (15 V, 5 Hz, 0.5 ms, 20 s) of the ipsilateral trigeminal ganglion. (B) Quantitative evaluation of the effect of hCGRP8–37 (15 μg kg−1 i.v.; n=6), atropine (5 mg kg−1 i.v.; n=6), p-chloro-D-Phe6-Leu17-VIP (20 μg kg−1 i.v.; n=6) and RP 67580 (0.1 mg kg−1 i.v. n=12) on the blood flow increase in the nasal mucosa evoked by electrical stimulation (15 V, 5 Hz, 0.5 ms, 20 s) of the ipsilateral trigeminal ganglion. Responses are expressed as percentage deviation from control values (means±s.e.mean). *P<0.05, N.S., non significant.
Figure 7
Figure 7
(A) Quantitative evaluation of the effect of hCGRP8–37 (15 μg kg−1 i.v.; n=6), atropine (5 mg kg−1 i.v.; n=6), hexamethonium (10 mg kg−1 i.v.; n=6), p-chloro-D-Phe6-Leu17-VIP (20 μg kg−1 i.v.; n=6) and RP 67580 (0.1 mg kg−1 i.v.; n=18) on the blood flow increase in the dura mater evoked by electrical stimulation (15 V, 5 Hz, 0.5 ms, 20 s) of the ipsilateral trigeminal ganglion. (B) Quantitative evaluation of the effect of hCGRP8–37 (15 μg kg−1 i.v.; n=6), atropine (5 mg kg−1 i.v.; n=6), p-chloro-D-Phe6-Leu17-VIP (20 μg kg−1 i.v.; n=6) and RP 67580 (0.1 mg kg−1 i.v. n=12) on the blood flow increase in the nasal mucosa evoked by electrical stimulation (15 V, 5 Hz, 0.5 ms, 20 s) of the ipsilateral trigeminal ganglion. Responses are expressed as percentage deviation from control values (means±s.e.mean). *P<0.05, N.S., non significant.
Figure 8
Figure 8
Effect of resiniferatoxin (RTX, 3 μg kg−1 i.v. 10 min. before electrical stimulation; n=6) on plasma extravasation in the dura mater and in the upper eyelid evoked by electrical stimulation (25 V, 5 Hz, 0.5 ms, 5 min) of the ipsilateral trigeminal ganglion (means±s.e.mean; c.p.m.: count per minute; *P<0.01; N.S., non significant).

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