Abstract
There is an accumulating body of evidence suggesting that the periaqueductal grey (PAG) is involved in the pathophysiology of migraine. Positron emission tomography (PET) studies in humans have shown that the caudal ventrolateral midbrain, encompassing the ventrolateral PAG, has activations during migraine attacks. The PAG may well be involved not only through the descending modulation of nociceptive afferent information, but also by its ascending projections to the pain processing centres of the thalamus. In this study the intranuclear oncogene protein Fos was used to mark cell activation in the PAG following stimulation of the trigeminally-innervated superior sagittal sinus (SSS) in both cats and in nonhuman primates (Macaca nemestrina). Fos expression in the PAG increased following stimulation to a median of 242 cells (interquartile range 236–272) in the cat and 155 cells (range 104–203) in the monkey, compared with control levels of 35 cells (21–50) and 26 cells (18–33), respectively. Activation was predominantly in the ventrolateral area of the caudal PAG suggesting that the PAG is involved following trigeminally-evoked craniovascular pain.
Keywords: Sagittal sinus, craniofacial pain, migraine
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- Bandler R., Keay K. A. Columnar organization in the midbrain periaqueductal gray and the integration of emotional expression. Prog Brain Res. 1996;107:285–300. doi: 10.1016/s0079-6123(08)61871-3. [DOI] [PubMed] [Google Scholar]
- Bandler R., Shipley M. T. Columnar organization in the midbrain periaqueductal gray: modules for emotional expression? Trends Neurosci. 1994 Sep;17(9):379–389. doi: 10.1016/0166-2236(94)90047-7. [DOI] [PubMed] [Google Scholar]
- Basbaum A. I., Marley N. J., O'Keefe J., Clanton C. H. Reversal of morphine and stimulus-produced analgesia by subtotal spinal cord lesions. Pain. 1977 Feb;3(1):43–56. doi: 10.1016/0304-3959(77)90034-3. [DOI] [PubMed] [Google Scholar]
- Baskin D. S., Mehler W. R., Hosobuchi Y., Richardson D. E., Adams J. E., Flitter M. A. Autopsy analysis of the safety, efficacy and cartography of electrical stimulation of the central gray in humans. Brain Res. 1986 Apr 23;371(2):231–236. doi: 10.1016/0006-8993(86)90358-6. [DOI] [PubMed] [Google Scholar]
- Drummond P. D., Lance J. W. Neurovascular disturbances in headache patients. Clin Exp Neurol. 1984;20:93–99. [PubMed] [Google Scholar]
- Ferrari M. D. Migraine. Lancet. 1998 Apr 4;351(9108):1043–1051. doi: 10.1016/S0140-6736(97)11370-8. [DOI] [PubMed] [Google Scholar]
- Goadsby P. J., Hoskin K. L. The distribution of trigeminovascular afferents in the nonhuman primate brain Macaca nemestrina: a c-fos immunocytochemical study. J Anat. 1997 Apr;190(Pt 3):367–375. doi: 10.1046/j.1469-7580.1997.19030367.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Goadsby P. J., Zagami A. S., Lambert G. A. Neural processing of craniovascular pain: a synthesis of the central structures involved in migraine. Headache. 1991 Jun;31(6):365–371. doi: 10.1111/j.1526-4610.1991.hed3106365.x. [DOI] [PubMed] [Google Scholar]
- Haas D. C., Kent P. F., Friedman D. I. Headache caused by a single lesion of multiple sclerosis in the periaqueductal gray area. Headache. 1993 Sep;33(8):452–455. doi: 10.1111/j.1526-4610.1993.hed3308452.x. [DOI] [PubMed] [Google Scholar]
- Hammond D. L., Presley R., Gogas K. R., Basbaum A. I. Morphine or U-50,488 suppresses Fos protein-like immunoreactivity in the spinal cord and nucleus tractus solitarii evoked by a noxious visceral stimulus in the rat. J Comp Neurol. 1992 Jan 8;315(2):244–253. doi: 10.1002/cne.903150210. [DOI] [PubMed] [Google Scholar]
- Hoskin K. L., Goadsby P. J. Exposure and isolation of the superior sagittal sinus elicits Fos in the trigeminal nucleus caudalis and dorsal horn of the cervical spinal cord: how long should you wait? Brain Res. 1999 Apr 3;824(1):133–135. doi: 10.1016/s0006-8993(99)01135-x. [DOI] [PubMed] [Google Scholar]
- Hoskin K. L., Kaube H., Goadsby P. J. Central activation of the trigeminovascular pathway in the cat is inhibited by dihydroergotamine. A c-Fos and electrophysiological study. Brain. 1996 Feb;119(Pt 1):249–256. doi: 10.1093/brain/119.1.249. [DOI] [PubMed] [Google Scholar]
- Hoskin K. L., Kaube H., Goadsby P. J. Sumatriptan can inhibit trigeminal afferents by an exclusively neural mechanism. Brain. 1996 Oct;119(Pt 5):1419–1428. doi: 10.1093/brain/119.5.1419. [DOI] [PubMed] [Google Scholar]
- Jones S. L., Gebhart G. F. Inhibition of spinal nociceptive transmission from the midbrain, pons and medulla in the rat: activation of descending inhibition by morphine, glutamate and electrical stimulation. Brain Res. 1988 Sep 20;460(2):281–296. doi: 10.1016/0006-8993(88)90373-3. [DOI] [PubMed] [Google Scholar]
- Kaube H., Keay K. A., Hoskin K. L., Bandler R., Goadsby P. J. Expression of c-Fos-like immunoreactivity in the caudal medulla and upper cervical spinal cord following stimulation of the superior sagittal sinus in the cat. Brain Res. 1993 Nov 26;629(1):95–102. doi: 10.1016/0006-8993(93)90486-7. [DOI] [PubMed] [Google Scholar]
- Keay K. A., Bandler R. Anatomical evidence for segregated input from the upper cervical spinal cord to functionally distinct regions of the periaqueductal gray region of the cat. Neurosci Lett. 1992 May 25;139(2):143–148. doi: 10.1016/0304-3940(92)90538-i. [DOI] [PubMed] [Google Scholar]
- Keay K. A., Bandler R. Deep and superficial noxious stimulation increases Fos-like immunoreactivity in different regions of the midbrain periaqueductal grey of the rat. Neurosci Lett. 1993 May 14;154(1-2):23–26. doi: 10.1016/0304-3940(93)90162-e. [DOI] [PubMed] [Google Scholar]
- Levine R., Morgan M. M., Cannon J. T., Liebeskind J. C. Stimulation of the periaqueductal gray matter of the rat produces a preferential ipsilateral antinociception. Brain Res. 1991 Dec 13;567(1):140–144. doi: 10.1016/0006-8993(91)91446-8. [DOI] [PubMed] [Google Scholar]
- Li Y. Q., Takada M., Shinonaga Y., Mizuno N. Direct projections from the midbrain periaqueductal gray and the dorsal raphe nucleus to the trigeminal sensory complex in the rat. Neuroscience. 1993 May;54(2):431–443. doi: 10.1016/0306-4522(93)90264-g. [DOI] [PubMed] [Google Scholar]
- Marek P., Yirmiya R., Liebeskind J. C. Stimulation-produced analgesia in the mouse: evidence for laterality of opioid mediation. Brain Res. 1991 Feb 8;541(1):154–156. doi: 10.1016/0006-8993(91)91090-n. [DOI] [PubMed] [Google Scholar]
- Mayer D. J., Liebeskind J. C. Pain reduction by focal electrical stimulation of the brain: an anatomical and behavioral analysis. Brain Res. 1974 Mar 15;68(1):73–93. doi: 10.1016/0006-8993(74)90534-4. [DOI] [PubMed] [Google Scholar]
- Mayer D. J., Wolfle T. L., Akil H., Carder B., Liebeskind J. C. Analgesia from electrical stimulation in the brainstem of the rat. Science. 1971 Dec 24;174(4016):1351–1354. doi: 10.1126/science.174.4016.1351. [DOI] [PubMed] [Google Scholar]
- Menétrey D., Chaouch A., Binder D., Besson J. M. The origin of the spinomesencephalic tract in the rat: an anatomical study using the retrograde transport of horseradish peroxidase. J Comp Neurol. 1982 Apr 1;206(2):193–207. doi: 10.1002/cne.902060208. [DOI] [PubMed] [Google Scholar]
- Raskin N. H., Hosobuchi Y., Lamb S. Headache may arise from perturbation of brain. Headache. 1987 Sep;27(8):416–420. doi: 10.1111/j.1526-4610.1987.hed2708416.x. [DOI] [PubMed] [Google Scholar]
- Rasmussen B. K., Olesen J. Migraine with aura and migraine without aura: an epidemiological study. Cephalalgia. 1992 Aug;12(4):221–186. doi: 10.1046/j.1468-2982.1992.1204221.x. [DOI] [PubMed] [Google Scholar]
- Reynolds D. V. Surgery in the rat during electrical analgesia induced by focal brain stimulation. Science. 1969 Apr 25;164(3878):444–445. doi: 10.1126/science.164.3878.444. [DOI] [PubMed] [Google Scholar]
- Sandkühler J., Helmchen C., Fu Q. G., Zimmermann M. Inhibition of spinal nociceptive neurons by excitation of cell bodies or fibers of passage at various brainstem sites in the cat. Neurosci Lett. 1988 Oct 31;93(1):67–72. doi: 10.1016/0304-3940(88)90014-6. [DOI] [PubMed] [Google Scholar]
- Sandkühler J., Willmann E., Fu Q. G. Characteristics of midbrain control of spinal nociceptive neurons and nonsomatosensory parameters in the pentobarbital-anesthetized rat. J Neurophysiol. 1991 Jan;65(1):33–48. doi: 10.1152/jn.1991.65.1.33. [DOI] [PubMed] [Google Scholar]
- Storer R. J., Butler P., Hoskin K. L., Goadsby P. J. A simple method, using 2-hydroxypropyl-beta-cyclodextrin, of administering alpha-chloralose at room temperature. J Neurosci Methods. 1997 Nov 7;77(1):49–53. doi: 10.1016/s0165-0270(97)00110-6. [DOI] [PubMed] [Google Scholar]
- Strassman A. M., Vos B. P., Mineta Y., Naderi S., Borsook D., Burstein R. Fos-like immunoreactivity in the superficial medullary dorsal horn induced by noxious and innocuous thermal stimulation of facial skin in the rat. J Neurophysiol. 1993 Nov;70(5):1811–1821. doi: 10.1152/jn.1993.70.5.1811. [DOI] [PubMed] [Google Scholar]
- Veloso F., Kumar K., Toth C. Headache secondary to deep brain implantation. Headache. 1998 Jul-Aug;38(7):507–515. doi: 10.1046/j.1526-4610.1998.3807507.x. [DOI] [PubMed] [Google Scholar]
- Weiller C., May A., Limmroth V., Jüptner M., Kaube H., Schayck R. V., Coenen H. H., Diener H. C. Brain stem activation in spontaneous human migraine attacks. Nat Med. 1995 Jul;1(7):658–660. doi: 10.1038/nm0795-658. [DOI] [PubMed] [Google Scholar]