[en] The migraine headache involves activation and central sensitization of the trigeminovascular pain path- way. The migraine aura is likely due to cortical spreading depression (CSD), a propagating wave of brief neuronal depolarization followed by prolonged inhibition. The precise link between CSD and headache remains controversial. Our objectives were to study the effect of CSD on neuronal activation in the peri- aqueductal grey matter (PAG), an area known to control pain and autonomic functions, and to be involved in migraine pathogenesis. Fos-immunoreactive nuclei were counted in rostral PAG and Edinger–Westphal nuclei (PAG–EWn bregma −6.5 mm), and caudal PAG (bregma −8 mm) of 17 adult male Sprague–Dawley rats after KCl-induced CSD under chloral hydrate anesthesia. Being part of a pharmacological study, six animals had received, for the preceding 4 weeks daily, intraperitoneal injections of lamotrigine (15 mg/kg), six others had been treated with saline, while five sham-operated animals served as controls. We found that the number of Fos-immunoreactive nuclei in the PAG decreased after CSD provocation. There was no difference between lamotrigine- and saline-treated animals. The number of CSDs correlated negatively with Fos-immunoreactive counts. CSD-linked inhibition of neuronal activity in the PAG might play a role in central sensitization during migraine attacks and contribute to a better understanding of the link between the aura and the headache.
Research Center/Unit :
Giga-Neurosciences - ULiège
Disciplines :
Neurology
Author, co-author :
Borysovych Bogdanov, V.; Giga-Neurosciences, Headache Research Unit, University of Liege, Liege, Belgium, Taras Shevchenko National University of Kyiv, Volodymyrska Str. 64, Kyiv, Ukraine, INRA, Nutrition et Neurobiologie Intégrée and University Bordeaux, Nutrition et Neurobiologie Intégrée, UMR 1286, 146 Rue Léo-Saignat, Bordeaux Cedex, France
Bogdanova, O. V.; Taras Shevchenko National University of Kyiv, Volodymyrska Str. 64, Kyiv, Ukraine
LOMBARD, Arnaud ; Centre Hospitalier Universitaire de Liège - CHU > Neurologie Sart Tilman
Chauvel, V.; Giga-Neurosciences, Headache Research Unit, University of Liege, Liege, Belgium
Multon, Sylvie ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Histologie
Kot, L. I.; Taras Shevchenko National University of Kyiv, Volodymyrska Str. 64, Kyiv, Ukraine
Makarchuk, MY
Schoenen, Jean ; Université de Liège > Département des sciences biomédicales et précliniques > Département des sciences biomédicales et précliniques
Language :
English
Title :
Cortical spreading depression decreases Fos expression in rat periaqueductal gray matter.
Publication date :
2015
Journal title :
Neuroscience Letters
ISSN :
0304-3940
eISSN :
1872-7972
Publisher :
Elsevier, Limerick, Ireland
Volume :
585
Pages :
138-143
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
F.R.S.-FNRS - Fonds de la Recherche Scientifique Fonds Léon Fredericq
Afridi S.K., Giffin N.J., Kaube H., Friston K.J., Ward N.S., Frackowiak R.S., Goadsby P.J. A positron emission tomographic study in spontaneous migraine. Arch. Neurol. 2005, 62:1270-1275.
Akcali D., Sayin A., Sara Y., Bolay H. Does single cortical spreading depression elicit pain behaviour in freely moving rats?. Cephalalgia 2010, 30:1195-1206.
Bandler R., Shipley M.T. Columnar organization in the midbrain periaqueductal gray: modules for emotional expression?. Trends Neurosci. 1994, 17:379-389.
Bartsch T., Knight Y.E., Goadsby P.J. Activation of 5-HT (1B/1D) receptor in the periaqueductal gray inhibits nociception. Ann. Neurol. 2004, 56:371-381.
Behbehani M.M. Functional characteristics of the midbrain periaqueductal gray. Prog. Neurobiol. 1995, 46:575-605.
Bogdanov V.B., Multon S., Chauvel V., Bogdanova O.V., Prodanov D., Makarchuk M.Y., Schoenen J. Migraine preventive drugs differentially affect cortical spreading depression in rat. Neurobiol. Dis. 2010, 41:430-435.
Bohotin C., Scholsem M., Multon S., Martin D., Bohotin V., Schoenen J. Vagus nerve stimulation in awake rats reduces formalin-induced nociceptive behaviour and Fos-immunoreactivity in trigeminal nucleus caudalis. Pain 2003, 101:3-12.
Carrive P. The periaqueductal gray and defensive behavior: functional representation and neuronal organization. Behav. Brain Res. 1993, 58:27-47.
Chiou R.J., Chang C.W., Kuo C.C. Involvement of the periaqueductal gray in the effect of motor cortex stimulation. Brain Res. 2013, 1500:28-35.
da Costa Gomez T.M., Behbehani M.M. An electrophysiological characterization of the projection from the central nucleus of the amygdala to the periaqueductal gray of the rat: the role of opioid receptors. Brain Res. 1995, 689:21-31.
De Marinis M., Assenza S., Carletto F. Oculosympathetic alterations in migraine patients. Cephalalgia 1998, 18:77-84.
Dehbandi S., Speckmann E.J., Pape H.C., Gorji A. Cortical spreading depression modulates synaptic transmission of the rat lateral amygdala. Eur. J. Neurosci. 2008, 27:2057-2065.
Douglass J., Daoud S. Characterization of the human cDNA and genomic DNA encoding CART: a cocaine- and amphetamine-regulated transcript. Gene 1996, 169:241-245.
Floyd N.S., Price J.L., Ferry A.T., Keay K.A., Bandler R. Orbitomedial prefrontal cortical projections to distinct longitudinal columns of the periaqueductal gray in the rat. J. Comp. Neurol. 2000, 422:556-578.
Gamlin P.D., Reiner A. The Edinger-Westphal nucleus: sources of input influencing accommodation, pupilloconstriction, and choroidal blood flow. J. Comp. Neurol. 1991, 306:425-438.
Gee J.R., Chang J., Dublin A.B., Vijayan N. The association of brainstem lesions with migraine-like headache: an imaging study of multiple sclerosis. Headache 2005, 45:670-677.
Goadsby P.J. Migraine, aura, and cortical spreading depression: why are we still talking about it?. Ann. Neurol. 2001, 49:4-6.
Hadjikhani N., Sanchez Del Rio M., Wu O., Schwartz D., Bakker D., Fischl B., Kwong K.K., Cutrer F.M., Rosen B.R., Tootell R.B., Sorensen A.G., Moskowitz M.A. Mechanisms of migraine aura revealed by functional MRI in human visual cortex. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:4687-4692.
Harle D.E., Wolffsohn J.S., Evans B.J. The pupillary light reflex in migraine ophthalmic. Physiol. Opt. 2005, 25:240-245.
Harrison N.A., Singer T., Rotshtein P., Dolan R.J., Critchley H.D. Pupillary contagion: central mechanisms engaged in sadness processing. Social Cognit. Affective Neurosci. 2006, 1:5-17.
Hoskin K.L., Bulmer D.C., Lasalandra M., Jonkman A., Goadsby P.J. Fos expression in the midbrain periaqueductal grey after trigeminovascular stimulation. J. Anat. 2001, 198:29-35.
Ingvardsen B.K., Laursen H., Olsen U.B., Hansen A.J. Possible mechanism of c-Fos expression in trigeminal nucleus caudalis following cortical spreading depression. Pain 1997, 72:407-415.
Iqbal Chowdhury G.M., Liu Y., Tanaka M., Fujioka T., Ishikawa A., Nakamura S. Cortical spreading depression affects Fos expression in the hypothalamic paraventricular nucleus and the cerebral cortex of both hemispheres. Neurosci. Res. 2003, 45:149-155.
Jansen A.S., Farkas E., Mac Sams J., Loewy A.D. Local connections between the columns of the periaqueductal gray matter: a case for intrinsic neuromodulation. Brain Res. 1998, 784:329-336.
Klooster J., Vrensen G.F. New indirect pathways subserving the pupillary light reflex: projections of the accessory oculomotor nuclei and the periaqueductal gray to the Edinger-Westphal nucleus and the thoracic spinal cord in rats. Anat. Embryol. 1998, 198:123-132.
Kong J., Tu P.C., Zyloney C., Su T.P. Intrinsic functional connectivity of the periaqueductal gray, a resting fMRI study. Behav. Brain Res. 2010, 211:215-219.
Kozicz T., Korosi A., Korsman C., Tilburg-Ouwens D., Groenink L., Veening J., van Der Gugten J., Roubos E., Olivier B. Urocortin expression in the Edinger-Westphal nucleus is down-regulated in transgenic mice over-expressing neuronal corticotropin-releasing factor. Neuroscience 2004, 123:589-594.
Lambert G.A., Zagami A.S. The mode of action of migraine triggers: a hypothesis. Headache 2008, 49:253-275.
Louter M.A., Bosker J.E., van Oosterhout W.P., van Zwet E.W., Zitman F.G., Ferrari M.D., Terwindt G.M. Cutaneous allodynia as a predictor of migraine chronification. Brain 2013, 136:3489-3496.
Mainero C., Boshyan J., Hadjikhani N. Altered functional magnetic resonance imaging resting-state connectivity in periaqueductal gray networks in migraine. Ann. Neurol. 2011, 70:838-845.
Maniyar F.H., Sprenger T., Monteith T., Schankin C., Goadsby P.J. Brain activations in the premonitory phase of nitroglycerin-triggered migraine attacks. Brain 2014, 137:232-241.
Martella G., Costa C., Pisani A., Cupini L.M., Bernardi G., Calabresi P. Antiepileptic drugs on calcium currents recorded from cortical and PAG neurons: therapeutic implications for migraine. Cephalalgia 2008, 28:1315-1326.
Moskowitz M.A. Neurogenic inflammation in the pathophysiology and treatment of migraine. Neurology 1993, 43:S16-S20.
Niehaus L., Guldin B., Meyer B. Influence of transcranial magnetic stimulation on pupil size. J. Neurol. Sci. 2001, 182:123-128.
Pagano R.L., Fonoff E.T., Dale C.S., Ballester G., Teixeira M.J., Britto L.R. Motor cortex stimulation inhibits thalamic sensory neurons and enhances activity of PAG neurons: possible pathways for antinociception. Pain 2012, 153:2359-2369.
Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates/George Paxinos 2007, 1. Charles Watson, Amsterdam.
Raskin N.H., Hosobuchi Y., Lamb S. Headache may arise from perturbation of brain. Headache 1987, 27:416-420.
Rocca M.A., Ceccarelli A., Falini A., Colombo B., Tortorella P., Bernasconi L., Comi G., Scotti G., Filippi M. Brain gray matter changes in migraine patients with T2-visible lesions: a 3-T MRI study. Stroke 2006, 37:1765-1770.
Russell M.B., Olesen J. Migrainous disorder and its relation to migraine without aura and migraine with aura. A genetic epidemiological study. Cephalalgia 1996, 16:431-435.
Spina M., Merlo-Pich E., Chan R.K., Basso A.M., Rivier J., Vale W., Koob G.F. Appetite-suppressing effects of urocortin, a CRF-related neuropeptide. Science 1996, 273:1561-1564.
Strassman A., Mason P., Eckenstein F., Baughman R.W., Maciewicz R. Choline acetyltransferase immunocytochemistry of Edinger-Westphal and ciliary ganglion afferent neurons in the cat. Brain Res. 1987, 423:293-304.
Vaughan J., Donaldson C., Bittencourt J., Perrin M.H., Lewis K., Sutton S., Chan R., Turnbull A.V., Lovejoy D., Rivier C., et al. Urocortin, a mammalian neuropeptide related to fish urotensin I and to corticotropin-releasing factor. Nature 1995, 378:287-292.
Vianna D.M., Brandao M.L. Anatomical connections of the periaqueductal gray: specific neural substrates for different kinds of fear. Braz. J. Med. Biol. Res. 2003, 36:557-566. Epub 2003 Apr 2022.
Welch K.M., Nagesh V., Aurora S.K., Gelman N. Periaqueductal gray matter dysfunction in migraine: cause or the burden of illness?. Headache 2001, 41:629-637.
Weninger S.C., Peters L.L., Majzoub J.A. Urocortin expression in the Edinger-Westphal nucleus is up-regulated by stress and corticotropin-releasing hormone deficiency. Endocrinology 2000, 141:256-263.
Woods R.P., Iacoboni M., Mazziotta J.C. Brief report: bilateral spreading cerebral hypoperfusion during spontaneous migraine headache. N. Engl. J. Med. 1994, 331:1689-1692.
