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Published in: The Journal of Headache and Pain 1/2013

Open Access 01-12-2013 | Review article

Cortical spreading depression as a target for anti-migraine agents

Published in: The Journal of Headache and Pain | Issue 1/2013

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Abstract

Spreading depression (SD) is a slowly propagating wave of neuronal and glial depolarization lasting a few minutes, that can develop within the cerebral cortex or other brain areas after electrical, mechanical or chemical depolarizing stimulations. Cortical SD (CSD) is considered the neurophysiological correlate of migraine aura. It is characterized by massive increases in both extracellular K+ and glutamate, as well as rises in intracellular Na+ and Ca2+. These ionic shifts produce slow direct current (DC) potential shifts that can be recorded extracellularly. Moreover, CSD is associated with changes in cortical parenchymal blood flow.
CSD has been shown to be a common therapeutic target for currently prescribed migraine prophylactic drugs. Yet, no effects have been observed for the antiepileptic drugs carbamazepine and oxcarbazepine, consistent with their lack of efficacy on migraine. Some molecules of interest for migraine have been tested for their effect on CSD. Specifically, blocking CSD may play an enabling role for novel benzopyran derivative tonabersat in preventing migraine with aura. Additionally, calcitonin gene-related peptide (CGRP) antagonists have been recently reported to inhibit CSD, suggesting the contribution of CGRP receptor activation to the initiation and maintenance of CSD not only at the classic vascular sites, but also at a central neuronal level. Understanding what may be lying behind this contribution, would add further insights into the mechanisms of actions for “gepants”, which may be pivotal for the effectiveness of these drugs as anti-migraine agents.
CSD models are useful tools for testing current and novel prophylactic drugs, providing knowledge on mechanisms of action relevant for migraine.
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Literature
1.
go back to reference Somjen GG: Aristides Leão's discovery of cortical spreading depression. J Neurophysiol 2005, 94: 2–4. 10.1152/classicessays.00031.2005 Somjen GG: Aristides Leão's discovery of cortical spreading depression. J Neurophysiol 2005, 94: 2–4. 10.1152/classicessays.00031.2005
2.
go back to reference Fabricius M, Fuhr S, Bhatia R, Boutelle M, Hashemi P, Strong AJ, Lauritzen M: Cortical spreading depression and peri-infarct depolarization in acutely injured human cerebral cortex. Brain 2006, 129: 778–790. 10.1093/brain/awh716 Fabricius M, Fuhr S, Bhatia R, Boutelle M, Hashemi P, Strong AJ, Lauritzen M: Cortical spreading depression and peri-infarct depolarization in acutely injured human cerebral cortex. Brain 2006, 129: 778–790. 10.1093/brain/awh716
3.
go back to reference Lauritzen M, Dreier JP, Fabricius M, Hartings JA, Graf R, Strong AJ: Clinical relevance of cortical spreading depression in neurological disorders: migraine, malignant stroke, subarachnoid and intracranial hemorrhage, and traumatic brain injury. J Cereb Blood Flow Metab 2011, 31: 17–35. 10.1038/jcbfm.2010.191PubMedCentral Lauritzen M, Dreier JP, Fabricius M, Hartings JA, Graf R, Strong AJ: Clinical relevance of cortical spreading depression in neurological disorders: migraine, malignant stroke, subarachnoid and intracranial hemorrhage, and traumatic brain injury. J Cereb Blood Flow Metab 2011, 31: 17–35. 10.1038/jcbfm.2010.191PubMedCentral
4.
go back to reference Dreier JP: The role of spreading depression, spreading depolarization and spreading ischemia in neurological disease. Nat Med 2011, 17: 439–447. 10.1038/nm.2333 Dreier JP: The role of spreading depression, spreading depolarization and spreading ischemia in neurological disease. Nat Med 2011, 17: 439–447. 10.1038/nm.2333
5.
go back to reference Somjen GG: Mechanisms of spreading depression and hypoxic spreading depression-like depolarization. Physiol Rev 2001, 81: 1065–1096. Somjen GG: Mechanisms of spreading depression and hypoxic spreading depression-like depolarization. Physiol Rev 2001, 81: 1065–1096.
6.
go back to reference Strong AJ, Dardis R: Depolarisation phenomena in traumatic and ischaemic brain injury. Austria vol. In Advances and Technical Standards in Neurosurgery, Springer, Wien, vol 30 Edited by: Pickard JD. 2005, 3–49. Strong AJ, Dardis R: Depolarisation phenomena in traumatic and ischaemic brain injury. Austria vol. In Advances and Technical Standards in Neurosurgery, Springer, Wien, vol 30 Edited by: Pickard JD. 2005, 3–49.
7.
go back to reference Diener HC: Positron emission tomography studies in headache. Headache 1997, 37: 622–625. 10.1046/j.1526-4610.1997.3710622.x Diener HC: Positron emission tomography studies in headache. Headache 1997, 37: 622–625. 10.1046/j.1526-4610.1997.3710622.x
8.
go back to reference Tfelt-Hansen PC: History of migraine with aura and cortical spreading depression from 1941 and onwards. Cephalalgia 2010, 30: 780–792. Tfelt-Hansen PC: History of migraine with aura and cortical spreading depression from 1941 and onwards. Cephalalgia 2010, 30: 780–792.
9.
go back to reference Sánchez del Rio M, Alvarez Linera J: Functional neuroimaging of headaches. Lancet Neurol 2004, 3: 645–651. 10.1016/S1474-4422(04)00904-4 Sánchez del Rio M, Alvarez Linera J: Functional neuroimaging of headaches. Lancet Neurol 2004, 3: 645–651. 10.1016/S1474-4422(04)00904-4
10.
go back to reference Smith JM, Bradley DP, James MF, Huang CL: Physiological studies of cortical spreading depression. Biol Rev Camb Philos Soc 2006, 81: 457–481. 10.1017/S1464793106007081 Smith JM, Bradley DP, James MF, Huang CL: Physiological studies of cortical spreading depression. Biol Rev Camb Philos Soc 2006, 81: 457–481. 10.1017/S1464793106007081
11.
go back to reference Smith JM, James MF, Fraser JA, Huang CL: Translational imaging studies of cortical spreading depression in experimental models for migraine aura. Expert Rev Neurother 2008, 8: 759–768. 10.1586/14737175.8.5.759 Smith JM, James MF, Fraser JA, Huang CL: Translational imaging studies of cortical spreading depression in experimental models for migraine aura. Expert Rev Neurother 2008, 8: 759–768. 10.1586/14737175.8.5.759
12.
go back to reference Zhang X, Levy D, Noseda R, Kainz V, Jakubowski M, Burstein R: Activation of meningeal nociceptors by cortical spreading depression: implications for migraine with aura. J Neurosci 2010, 30: 8807–8814. 10.1523/JNEUROSCI.0511-10.2010PubMedCentral Zhang X, Levy D, Noseda R, Kainz V, Jakubowski M, Burstein R: Activation of meningeal nociceptors by cortical spreading depression: implications for migraine with aura. J Neurosci 2010, 30: 8807–8814. 10.1523/JNEUROSCI.0511-10.2010PubMedCentral
13.
go back to reference Hansen JM: Familial hemiplegic migraine. Dan Med Bull 2010, 57: B4183. Hansen JM: Familial hemiplegic migraine. Dan Med Bull 2010, 57: B4183.
14.
go back to reference Bolay H, Berman NE, Akcali D: Sex-related differences in animal models of migraine headache. Headache 2011, 51: 891–904. 10.1111/j.1526-4610.2011.01903.x Bolay H, Berman NE, Akcali D: Sex-related differences in animal models of migraine headache. Headache 2011, 51: 891–904. 10.1111/j.1526-4610.2011.01903.x
15.
go back to reference Eikermann-Haerter K, Kudo C, Moskowitz MA: Cortical spreading depression and estrogen. Headache 2007,47(Suppl 2):S79-S85. Eikermann-Haerter K, Kudo C, Moskowitz MA: Cortical spreading depression and estrogen. Headache 2007,47(Suppl 2):S79-S85.
16.
go back to reference Eikermann-Haerter K, Ayata C: Cortical spreading depression and migraine. Curr Neurol Neurosci Rep 2010, 10: 167–173. 10.1007/s11910-010-0099-1 Eikermann-Haerter K, Ayata C: Cortical spreading depression and migraine. Curr Neurol Neurosci Rep 2010, 10: 167–173. 10.1007/s11910-010-0099-1
17.
go back to reference Eikermann-Haerter K, Can A, Ayata C: Pharmacological targeting of spreading depression in migraine. Expert Rev Neurother 2012, 12: 297–306. 10.1586/ern.12.13PubMedCentral Eikermann-Haerter K, Can A, Ayata C: Pharmacological targeting of spreading depression in migraine. Expert Rev Neurother 2012, 12: 297–306. 10.1586/ern.12.13PubMedCentral
18.
go back to reference Merikangas KR: Contributions of epidemiology to our understanding of migraine. Headache 2013, 53: 230–246. 10.1111/head.12038 Merikangas KR: Contributions of epidemiology to our understanding of migraine. Headache 2013, 53: 230–246. 10.1111/head.12038
19.
go back to reference Headache Classification Committee of The International Headache Society: The International Classification of Headache Disorders: 2nd edition. Cephalalgia 2004,24(1):1–160. 10.1111/j.1468-2982.2004.00711.x Headache Classification Committee of The International Headache Society: The International Classification of Headache Disorders: 2nd edition. Cephalalgia 2004,24(1):1–160. 10.1111/j.1468-2982.2004.00711.x
20.
go back to reference Montagna P: Migraine genetics. Expert Rev Neurother 2008, 8: 1321–1330. 10.1586/14737175.8.9.1321 Montagna P: Migraine genetics. Expert Rev Neurother 2008, 8: 1321–1330. 10.1586/14737175.8.9.1321
21.
go back to reference Pietrobon D: Familial hemiplegic migraine. Neurotherapeutics 2007, 4: 274–284. 10.1016/j.nurt.2007.01.008 Pietrobon D: Familial hemiplegic migraine. Neurotherapeutics 2007, 4: 274–284. 10.1016/j.nurt.2007.01.008
22.
go back to reference Lashley KS: Patterns of cerebral integration indicated by the scotomas of migraine. Arch Neurol Psychiatry 1941, 46: 331–339. 10.1001/archneurpsyc.1941.02280200137007 Lashley KS: Patterns of cerebral integration indicated by the scotomas of migraine. Arch Neurol Psychiatry 1941, 46: 331–339. 10.1001/archneurpsyc.1941.02280200137007
23.
go back to reference Leão AAP: Spreading depression of activity in the cerebral cortex. J Neurophysiol 1944, 7: 359–390. Leão AAP: Spreading depression of activity in the cerebral cortex. J Neurophysiol 1944, 7: 359–390.
24.
go back to reference Leão AAP: Pial circulation and spreading depression of activity in the cerebral cortex. J Neurophysiol 1944, 7: 391–396. Leão AAP: Pial circulation and spreading depression of activity in the cerebral cortex. J Neurophysiol 1944, 7: 391–396.
25.
go back to reference Leão AAP: Further observations on the spreading depression of activity in the cerebral cortex. J Neurophysiol 1947, 10: 409–414. Leão AAP: Further observations on the spreading depression of activity in the cerebral cortex. J Neurophysiol 1947, 10: 409–414.
26.
go back to reference Wolff HG: Headache mechanisms. Bull U S Army Med Dep 1948, 8: 641–653. Wolff HG: Headache mechanisms. Bull U S Army Med Dep 1948, 8: 641–653.
27.
go back to reference Olesen J, Larsen B, Lauritzen M: Focal hyperemia followed by spreading oligemia and impaired activation of rCBF in classic migraine. Ann Neurol 1981, 9: 344–352. 10.1002/ana.410090406 Olesen J, Larsen B, Lauritzen M: Focal hyperemia followed by spreading oligemia and impaired activation of rCBF in classic migraine. Ann Neurol 1981, 9: 344–352. 10.1002/ana.410090406
28.
go back to reference Lauritzen M: Pathophysiology of the migraine aura. The spreading depression theory. Brain 1994, 117: 199–210. 10.1093/brain/117.1.199 Lauritzen M: Pathophysiology of the migraine aura. The spreading depression theory. Brain 1994, 117: 199–210. 10.1093/brain/117.1.199
29.
go back to reference Olesen J, Friberg L, Olsen TS, Iversen HK, Lassen NA, Andersen AR, Karle A: Timing and topography of cerebral blood flow, aura, and headache during migraine attacks. Ann Neurol 1990, 28: 791–798. 10.1002/ana.410280610 Olesen J, Friberg L, Olsen TS, Iversen HK, Lassen NA, Andersen AR, Karle A: Timing and topography of cerebral blood flow, aura, and headache during migraine attacks. Ann Neurol 1990, 28: 791–798. 10.1002/ana.410280610
30.
go back to reference Cutrer FM, Sorensen AG, Weisskoff RM, Ostergaard L, Sanchez del Rio M, Lee EJ, Rosen BR, Moskowitz MA: Perfusion-weighted imaging defects during spontaneous migrainous aura. Ann Neurol 1998, 43: 25–31. 10.1002/ana.410430108 Cutrer FM, Sorensen AG, Weisskoff RM, Ostergaard L, Sanchez del Rio M, Lee EJ, Rosen BR, Moskowitz MA: Perfusion-weighted imaging defects during spontaneous migrainous aura. Ann Neurol 1998, 43: 25–31. 10.1002/ana.410430108
31.
go back to reference Cutrer FM, O'Donnell A, Sanchez del Rio M: Functional neuroimaging: enhanced understanding of migraine pathophysiology. Neurology 2000,55(Suppl 2):S36-S45. Cutrer FM, O'Donnell A, Sanchez del Rio M: Functional neuroimaging: enhanced understanding of migraine pathophysiology. Neurology 2000,55(Suppl 2):S36-S45.
32.
go back to reference Cao Y, Welch KM, Aurora S, Vikingstad EM: Functional MRI-BOLD of visually triggered headache in patients with migraine. Arch Neurol 1999, 56: 548–554. 10.1001/archneur.56.5.548 Cao Y, Welch KM, Aurora S, Vikingstad EM: Functional MRI-BOLD of visually triggered headache in patients with migraine. Arch Neurol 1999, 56: 548–554. 10.1001/archneur.56.5.548
33.
go back to reference Hadjikhani N, Sanchez Del Rio M, Wu O, Schwartz D, Bakker D, Fischl B, Kwong KK, Cutrer FM, Rosen BR, Tootell RB, Sorensen AG, Moskowitz MA: Mechanisms of migraine aura revealed by functional MRI in human visual cortex. Proc Natl Acad Sci USA 2001, 98: 4687–4692. 10.1073/pnas.071582498PubMedCentral Hadjikhani N, Sanchez Del Rio M, Wu O, Schwartz D, Bakker D, Fischl B, Kwong KK, Cutrer FM, Rosen BR, Tootell RB, Sorensen AG, Moskowitz MA: Mechanisms of migraine aura revealed by functional MRI in human visual cortex. Proc Natl Acad Sci USA 2001, 98: 4687–4692. 10.1073/pnas.071582498PubMedCentral
34.
go back to reference Oberndorfer S, Wöber C, Nasel C, Asenbaum S, Lahrmann H, Fueger B, Grisold W: Familial hemiplegic migraine: follow-up findings of diffusion-weighted magnetic resonance imaging (MRI), perfusion-MRI and [99mTc] HMPAO-SPECT in a patient with prolonged hemiplegic aura. Cephalalgia 2004, 24: 533–539. 10.1111/j.1468-2982.2003.00706.x Oberndorfer S, Wöber C, Nasel C, Asenbaum S, Lahrmann H, Fueger B, Grisold W: Familial hemiplegic migraine: follow-up findings of diffusion-weighted magnetic resonance imaging (MRI), perfusion-MRI and [99mTc] HMPAO-SPECT in a patient with prolonged hemiplegic aura. Cephalalgia 2004, 24: 533–539. 10.1111/j.1468-2982.2003.00706.x
35.
go back to reference Jäger HR, Giffin NJ, Goadsby PJ: Diffusion- and perfusion-weighted MR imaging in persistent migrainous visual disturbances. Cephalalgia 2005, 25: 323–332. 10.1111/j.1468-2982.2004.00858.x Jäger HR, Giffin NJ, Goadsby PJ: Diffusion- and perfusion-weighted MR imaging in persistent migrainous visual disturbances. Cephalalgia 2005, 25: 323–332. 10.1111/j.1468-2982.2004.00858.x
36.
go back to reference Belvís R, Ramos R, Villa C, Segura C, Pagonabarraga J, Ormazabal I, Kulisevsky J: Brain apparent water diffusion coefficient magnetic resonance image during a prolonged visual aura. Headache 2010, 50: 1045–1049. 10.1111/j.1526-4610.2010.01672.x Belvís R, Ramos R, Villa C, Segura C, Pagonabarraga J, Ormazabal I, Kulisevsky J: Brain apparent water diffusion coefficient magnetic resonance image during a prolonged visual aura. Headache 2010, 50: 1045–1049. 10.1111/j.1526-4610.2010.01672.x
37.
go back to reference Mourand I, Menjot de Champfleur N, Carra-Dallière C, Le Bars E, Roubertie A, Bonafé A, Thouvenot E: Perfusion-weighted MR imaging in persistent hemiplegic migraine. Neuroradiology 2012, 54: 255–260. 10.1007/s00234-011-0946-z Mourand I, Menjot de Champfleur N, Carra-Dallière C, Le Bars E, Roubertie A, Bonafé A, Thouvenot E: Perfusion-weighted MR imaging in persistent hemiplegic migraine. Neuroradiology 2012, 54: 255–260. 10.1007/s00234-011-0946-z
38.
go back to reference Bereczki D, Kollár J, Kozák N, Viszokay K, Barta Z, Sikula J, Magyar MT: Cortical spreading edema in persistent visual migraine aura. Headache 2008, 48: 1226–1229. 10.1111/j.1526-4610.2008.01183.x Bereczki D, Kollár J, Kozák N, Viszokay K, Barta Z, Sikula J, Magyar MT: Cortical spreading edema in persistent visual migraine aura. Headache 2008, 48: 1226–1229. 10.1111/j.1526-4610.2008.01183.x
39.
go back to reference Smith M, Cros D, Sheen V: Hyperperfusion with vasogenic leakage by fMRI in migraine with prolonged aura. Neurology 2002, 58: 1308–1310. Smith M, Cros D, Sheen V: Hyperperfusion with vasogenic leakage by fMRI in migraine with prolonged aura. Neurology 2002, 58: 1308–1310.
40.
go back to reference Arnold G, Reuter U, Kinze S, Wolf T, Einhäupl KM: MWA shows gadolinium enhancement which is reversed following prophylactic treatment. Cephalalgia 1998, 18: 644–646. 10.1046/j.1468-2982.1998.1809644.x Arnold G, Reuter U, Kinze S, Wolf T, Einhäupl KM: MWA shows gadolinium enhancement which is reversed following prophylactic treatment. Cephalalgia 1998, 18: 644–646. 10.1046/j.1468-2982.1998.1809644.x
41.
go back to reference Bowyer SM, Aurora KS, Moran JE, Tepley N, Welch KM: Magnetoencephalographic fields from patients with spontaneous and induced migraine aura. Ann Neurol 2001, 50: 582–587. 10.1002/ana.1293 Bowyer SM, Aurora KS, Moran JE, Tepley N, Welch KM: Magnetoencephalographic fields from patients with spontaneous and induced migraine aura. Ann Neurol 2001, 50: 582–587. 10.1002/ana.1293
42.
go back to reference Hall SD, Barnes GR, Hillebrand A, Furlong PL, Singh KD, Holliday IE: Spatio-temporal imaging of cortical desynchronization in migraine visual aura: a magnetoencephalography case study. Headache 2004, 44: 204–208. 10.1111/j.1526-4610.2004.04048.x Hall SD, Barnes GR, Hillebrand A, Furlong PL, Singh KD, Holliday IE: Spatio-temporal imaging of cortical desynchronization in migraine visual aura: a magnetoencephalography case study. Headache 2004, 44: 204–208. 10.1111/j.1526-4610.2004.04048.x
43.
go back to reference Grafstein B: Mechanism of spreading cortical depression. J Neurophysiol 1956, 19: 154–171. Grafstein B: Mechanism of spreading cortical depression. J Neurophysiol 1956, 19: 154–171.
44.
go back to reference Strong AJ: Dr. Bernice Grafstein's paper on the mechanism of spreading depression. J Neurophysiol 2005, 94: 5–7. 10.1152/classicessays.00032.2005 Strong AJ: Dr. Bernice Grafstein's paper on the mechanism of spreading depression. J Neurophysiol 2005, 94: 5–7. 10.1152/classicessays.00032.2005
45.
go back to reference Martins-Ferreira H, Nedergaard M, Nicholson C: Perspectives on spreading depression. Brain Res Brain Res Rev 2000, 32: 215–234. 10.1016/S0165-0173(99)00083-1 Martins-Ferreira H, Nedergaard M, Nicholson C: Perspectives on spreading depression. Brain Res Brain Res Rev 2000, 32: 215–234. 10.1016/S0165-0173(99)00083-1
46.
go back to reference de Azeredo FA: Transient changes in energy metabolites and intracellular pH during spreading depression in the chick retina. Metab Brain Dis 1991, 6: 75–82. 10.1007/BF00999905 de Azeredo FA: Transient changes in energy metabolites and intracellular pH during spreading depression in the chick retina. Metab Brain Dis 1991, 6: 75–82. 10.1007/BF00999905
47.
go back to reference Gault LM, Lin CW, LaManna JC, Lust WD: Changes in energy metabolites, cGMP and intracellular pH during cortical spreading depression. Brain Res 1994, 641: 176–180. 10.1016/0006-8993(94)91835-X Gault LM, Lin CW, LaManna JC, Lust WD: Changes in energy metabolites, cGMP and intracellular pH during cortical spreading depression. Brain Res 1994, 641: 176–180. 10.1016/0006-8993(94)91835-X
48.
go back to reference Footitt DR, Newberry NR: Cortical spreading depression induces an LTP-like effect in rat neocortex in vitro. Brain Res 1998, 781: 339–342. 10.1016/S0006-8993(97)01359-0 Footitt DR, Newberry NR: Cortical spreading depression induces an LTP-like effect in rat neocortex in vitro. Brain Res 1998, 781: 339–342. 10.1016/S0006-8993(97)01359-0
49.
go back to reference Világi I, Klapka N, Luhmann HJ: Optical recording of spreading depression in rat neocortical slices. Brain Res 2001, 898: 288–296. 10.1016/S0006-8993(01)02196-5 Világi I, Klapka N, Luhmann HJ: Optical recording of spreading depression in rat neocortical slices. Brain Res 2001, 898: 288–296. 10.1016/S0006-8993(01)02196-5
50.
go back to reference Peeters M, Gunthorpe MJ, Strijbos PJ, Goldsmith P, Upton N, James MF: Effects of pan- and subtype-selective N-methyl-D-aspartate receptor antagonists on cortical spreading depression in the rat: therapeutic potential for migraine. J Pharmacol Exp Ther 2007, 321: 564–572. 10.1124/jpet.106.117101 Peeters M, Gunthorpe MJ, Strijbos PJ, Goldsmith P, Upton N, James MF: Effects of pan- and subtype-selective N-methyl-D-aspartate receptor antagonists on cortical spreading depression in the rat: therapeutic potential for migraine. J Pharmacol Exp Ther 2007, 321: 564–572. 10.1124/jpet.106.117101
51.
go back to reference Petzold GC, Haack S, von Bohlen Und Halbach O, Priller J, Lehmann TN, Heinemann U, Dirnagl U, Dreier JP: Nitric oxide modulates spreading depolarization threshold in the human and rodent cortex. Stroke 2008, 39: 1292–1299. 10.1161/STROKEAHA.107.500710 Petzold GC, Haack S, von Bohlen Und Halbach O, Priller J, Lehmann TN, Heinemann U, Dirnagl U, Dreier JP: Nitric oxide modulates spreading depolarization threshold in the human and rodent cortex. Stroke 2008, 39: 1292–1299. 10.1161/STROKEAHA.107.500710
52.
go back to reference McLachlan RS: Suppression of spreading depression of Leao in neocortex by an N-methyl-D-aspartate receptor antagonist. Can J Neurol Sci 1992, 19: 487–491. McLachlan RS: Suppression of spreading depression of Leao in neocortex by an N-methyl-D-aspartate receptor antagonist. Can J Neurol Sci 1992, 19: 487–491.
53.
go back to reference Obrenovitch TP, Zilkha E: Inhibition of cortical spreading depression by L-701,324, a novel antagonist at the glycine site of the N-methyl-D-aspartate receptor complex. Br J Pharmacol 1996, 117: 931–937. 10.1111/j.1476-5381.1996.tb15283.xPubMedCentral Obrenovitch TP, Zilkha E: Inhibition of cortical spreading depression by L-701,324, a novel antagonist at the glycine site of the N-methyl-D-aspartate receptor complex. Br J Pharmacol 1996, 117: 931–937. 10.1111/j.1476-5381.1996.tb15283.xPubMedCentral
54.
go back to reference Jing APG, Somjen GG: Role of calcium channels in spreading depression in rat hippocampal slices. Brain Res 1993, 604: 251–259. 10.1016/0006-8993(93)90376-X Jing APG, Somjen GG: Role of calcium channels in spreading depression in rat hippocampal slices. Brain Res 1993, 604: 251–259. 10.1016/0006-8993(93)90376-X
55.
go back to reference Footitt DR, Newberry NR: Cortical spreading depression induces an LTP-like effect in rat neocortex in vitro. Brain 1998, 781: 339–342. 10.1016/S0006-8993(97)01359-0 Footitt DR, Newberry NR: Cortical spreading depression induces an LTP-like effect in rat neocortex in vitro. Brain 1998, 781: 339–342. 10.1016/S0006-8993(97)01359-0
56.
go back to reference Hernándéz-Cáceres J, Macias-González R, Brozek G, Bures J: Systemic ketamine blocks cortical spreading depression but does not delay the onset of terminal anoxic depolarization in rats. Brain Res 1987, 437: 360–364. 10.1016/0006-8993(87)91652-0 Hernándéz-Cáceres J, Macias-González R, Brozek G, Bures J: Systemic ketamine blocks cortical spreading depression but does not delay the onset of terminal anoxic depolarization in rats. Brain Res 1987, 437: 360–364. 10.1016/0006-8993(87)91652-0
57.
go back to reference Marrannes R, Willems R, De Prins E, Wauquier A: Evidence for a role of the N-methyl-D-aspartate (NMDA) receptor in cortical spreading depression in the rat. Brain Res 1988, 457: 226–240. 10.1016/0006-8993(88)90690-7 Marrannes R, Willems R, De Prins E, Wauquier A: Evidence for a role of the N-methyl-D-aspartate (NMDA) receptor in cortical spreading depression in the rat. Brain Res 1988, 457: 226–240. 10.1016/0006-8993(88)90690-7
58.
go back to reference Lauritzen M, Hansen AJ: The effect of glutamate receptor blockade on anoxic depolarization and cortical spreading depression. J Cereb Blood Flow Metab 1992, 12: 223–229. 10.1038/jcbfm.1992.32 Lauritzen M, Hansen AJ: The effect of glutamate receptor blockade on anoxic depolarization and cortical spreading depression. J Cereb Blood Flow Metab 1992, 12: 223–229. 10.1038/jcbfm.1992.32
59.
go back to reference Nellgård B, Wieloch T: NMDA-receptor blockers but not NBQX, an AMPA-receptor antagonist, inhibit spreading depression in the rat brain. Acta Physiol Scand 1992, 146: 497–503. 10.1111/j.1748-1716.1992.tb09451.x Nellgård B, Wieloch T: NMDA-receptor blockers but not NBQX, an AMPA-receptor antagonist, inhibit spreading depression in the rat brain. Acta Physiol Scand 1992, 146: 497–503. 10.1111/j.1748-1716.1992.tb09451.x
60.
go back to reference Gorji A, Scheller D, Straub H, Tegtmeier F, Köhling R, Höhling JM, Tuxhorn I, Ebner A, Wolf P, Werner Panneck H, Oppel F, Speckmann EJ: Spreading depression in human neocortical slices. Brain Res 2001, 906: 74–83. 10.1016/S0006-8993(01)02557-4 Gorji A, Scheller D, Straub H, Tegtmeier F, Köhling R, Höhling JM, Tuxhorn I, Ebner A, Wolf P, Werner Panneck H, Oppel F, Speckmann EJ: Spreading depression in human neocortical slices. Brain Res 2001, 906: 74–83. 10.1016/S0006-8993(01)02557-4
61.
go back to reference Berger M, Speckmann EJ, Pape HC, Gorji A: Spreading depression enhances human neocortical excitability in vitro. Cephalalgia 2008, 28: 558–562. 10.1111/j.1468-2982.2008.01556.x Berger M, Speckmann EJ, Pape HC, Gorji A: Spreading depression enhances human neocortical excitability in vitro. Cephalalgia 2008, 28: 558–562. 10.1111/j.1468-2982.2008.01556.x
62.
go back to reference Tottene A, Urbani A, Pietrobon D: Role of different voltage-gated Ca2+ channels in cortical spreading depression: specific requirement of P/Q-type Ca2+ channels. Channels (Austin) 2011, 5: 110–114. 10.4161/chan.5.2.14149 Tottene A, Urbani A, Pietrobon D: Role of different voltage-gated Ca2+ channels in cortical spreading depression: specific requirement of P/Q-type Ca2+ channels. Channels (Austin) 2011, 5: 110–114. 10.4161/chan.5.2.14149
63.
go back to reference Petzold GC, Scheibe F, Braun JS, Freyer D, Priller J, Dirnagl U, Dreier JP: Nitric oxide modulates calcium entry through P/Q-type calcium channels and N-methyl-d-aspartate receptors in rat cortical neurons. Brain Res 2005, 1063: 9–14. 10.1016/j.brainres.2005.09.048 Petzold GC, Scheibe F, Braun JS, Freyer D, Priller J, Dirnagl U, Dreier JP: Nitric oxide modulates calcium entry through P/Q-type calcium channels and N-methyl-d-aspartate receptors in rat cortical neurons. Brain Res 2005, 1063: 9–14. 10.1016/j.brainres.2005.09.048
64.
go back to reference Zhou N, Gordon GR, Feighan D, MacVicar BA: Transient swelling, acidification, and mitochondrial depolarization occurs in neurons but not astrocytes during spreading depression. Cereb Cortex 2010, 20: 2614–2624. 10.1093/cercor/bhq018 Zhou N, Gordon GR, Feighan D, MacVicar BA: Transient swelling, acidification, and mitochondrial depolarization occurs in neurons but not astrocytes during spreading depression. Cereb Cortex 2010, 20: 2614–2624. 10.1093/cercor/bhq018
65.
go back to reference Herreras O, Somjen GG: Analysis of potential shifts associated with recurrent spreading depression and prolonged unstable SD induced by microdyalisis of elevated K+ in hippocampus of anesthetized rats. Brain Res 1993, 610: 283–294. 10.1016/0006-8993(93)91412-L Herreras O, Somjen GG: Analysis of potential shifts associated with recurrent spreading depression and prolonged unstable SD induced by microdyalisis of elevated K+ in hippocampus of anesthetized rats. Brain Res 1993, 610: 283–294. 10.1016/0006-8993(93)91412-L
66.
go back to reference Richter F, Ebersberger A, Schaible HG: Blockade of voltage-gated calcium channels in rat inhibits repetitive cortical spreading depression. Neurosci Lett 2002, 334: 123–126. 10.1016/S0304-3940(02)01120-5 Richter F, Ebersberger A, Schaible HG: Blockade of voltage-gated calcium channels in rat inhibits repetitive cortical spreading depression. Neurosci Lett 2002, 334: 123–126. 10.1016/S0304-3940(02)01120-5
67.
go back to reference Sugaya E, Takato M, Noda Y: Neuronal and glial activity during spreading depression in cerebral cortex of cat. J Neurophysiol 1975,38(4):822–841. Sugaya E, Takato M, Noda Y: Neuronal and glial activity during spreading depression in cerebral cortex of cat. J Neurophysiol 1975,38(4):822–841.
68.
go back to reference Tuckwell HC, Hermansen CL: Ion and transmitter movements during spreading cortical depression. Int J Neurosci 1981, 12: 109–135. 10.3109/00207458108985795 Tuckwell HC, Hermansen CL: Ion and transmitter movements during spreading cortical depression. Int J Neurosci 1981, 12: 109–135. 10.3109/00207458108985795
69.
go back to reference Somjen GG, Aitken PG: The ionic and metabolic responses associated with neuronal depression of Leão's type in cerebral cortex and in hippocampal formation. An Acad Bras Cienc 1984,56(4):495–504. Somjen GG, Aitken PG: The ionic and metabolic responses associated with neuronal depression of Leão's type in cerebral cortex and in hippocampal formation. An Acad Bras Cienc 1984,56(4):495–504.
70.
go back to reference Tozzi A, de Iure A, Di Filippo M, Costa C, Caproni S, Pisani A, Bonsi P, Picconi B, Cupini LM, Materazzi S, Geppetti P, Sarchielli P, Calabresi P: Critical role of calcitonin gene-related peptide receptors in cortical spreading depression. Proc Natl Acad Sci USA 2012, 109: 18985–18990. 10.1073/pnas.1215435109PubMedCentral Tozzi A, de Iure A, Di Filippo M, Costa C, Caproni S, Pisani A, Bonsi P, Picconi B, Cupini LM, Materazzi S, Geppetti P, Sarchielli P, Calabresi P: Critical role of calcitonin gene-related peptide receptors in cortical spreading depression. Proc Natl Acad Sci USA 2012, 109: 18985–18990. 10.1073/pnas.1215435109PubMedCentral
71.
go back to reference Akerman S, Holland PR, Goadsby PJ: Mechanically-induced cortical spreading depression associated regional cerebral blood flow changes are blocked by Na+ ion channel blockade. Brain Res 2008, 1229: 27–36. Akerman S, Holland PR, Goadsby PJ: Mechanically-induced cortical spreading depression associated regional cerebral blood flow changes are blocked by Na+ ion channel blockade. Brain Res 2008, 1229: 27–36.
72.
go back to reference Addae JI, Evans SM, Ali N, Stone TW: NMDA-induced changes in a cortical network in vivo are prevented by AMPA. Brain Res 2000, 869: 211–215. 10.1016/S0006-8993(00)02233-2 Addae JI, Evans SM, Ali N, Stone TW: NMDA-induced changes in a cortical network in vivo are prevented by AMPA. Brain Res 2000, 869: 211–215. 10.1016/S0006-8993(00)02233-2
73.
go back to reference Anderson TR, Andrew RD: Spreading depression: imaging and blockade in the rat neocortical brain slice. J Neurophysiol 2002, 88: 2713–2725. 10.1152/jn.00321.2002 Anderson TR, Andrew RD: Spreading depression: imaging and blockade in the rat neocortical brain slice. J Neurophysiol 2002, 88: 2713–2725. 10.1152/jn.00321.2002
74.
go back to reference Addae JI, Ali N, Stone TW: Effects of AMPA and clomethiazole on spreading depression cycles in the rat neocortex in vivo. Eur J Pharmacol 2011, 653: 41–46. 10.1016/j.ejphar.2010.11.021 Addae JI, Ali N, Stone TW: Effects of AMPA and clomethiazole on spreading depression cycles in the rat neocortex in vivo. Eur J Pharmacol 2011, 653: 41–46. 10.1016/j.ejphar.2010.11.021
75.
go back to reference Holland PR, Akerman S, Goadsby PJ: Cortical spreading depression-associated cerebral blood flow changes induced by mechanical stimulation are modulated by AMPA and GABA receptors. Cephalalgia 2010, 30: 519–527. Holland PR, Akerman S, Goadsby PJ: Cortical spreading depression-associated cerebral blood flow changes induced by mechanical stimulation are modulated by AMPA and GABA receptors. Cephalalgia 2010, 30: 519–527.
76.
go back to reference Haghir H, Kovac S, Speckmann EJ, Zilles K, Gorji A: Patterns of neurotransmitter receptor distributions following cortical spreading depression. Neuroscience 2009, 163: 1340–1352. 10.1016/j.neuroscience.2009.07.067 Haghir H, Kovac S, Speckmann EJ, Zilles K, Gorji A: Patterns of neurotransmitter receptor distributions following cortical spreading depression. Neuroscience 2009, 163: 1340–1352. 10.1016/j.neuroscience.2009.07.067
77.
go back to reference Van Harreveld A, Ochs S: Electrical and vascular concomitants of spreading depression. Am J Physiol 1957, 189: 159–166. Van Harreveld A, Ochs S: Electrical and vascular concomitants of spreading depression. Am J Physiol 1957, 189: 159–166.
78.
go back to reference Wahl M, Lauritzen M, Schilling L: Change of cerebrovascular reactivity after cortical spreading depression in cats and rats. Brain Res 1987, 411: 72–80. 10.1016/0006-8993(87)90682-2 Wahl M, Lauritzen M, Schilling L: Change of cerebrovascular reactivity after cortical spreading depression in cats and rats. Brain Res 1987, 411: 72–80. 10.1016/0006-8993(87)90682-2
79.
go back to reference Fabricius M, Akgoren N, Lauritzen M: Arginine-nitric oxide pathway and cerebrovascular regulation in cortical spreading depression. Am J Physiol 1995, 269: H23-H29. Fabricius M, Akgoren N, Lauritzen M: Arginine-nitric oxide pathway and cerebrovascular regulation in cortical spreading depression. Am J Physiol 1995, 269: H23-H29.
80.
go back to reference Duckrow RB: Regional cerebral blood flow during spreading cortical depression in conscious rats. J Cereb Blood Flow Metab 1991, 11: 150–154. 10.1038/jcbfm.1991.18 Duckrow RB: Regional cerebral blood flow during spreading cortical depression in conscious rats. J Cereb Blood Flow Metab 1991, 11: 150–154. 10.1038/jcbfm.1991.18
81.
go back to reference Duckrow RB: A brief hypoperfusion precedes spreading depression if nitric oxide synthesis is inhibited. Brain Res 1993, 618: 190–195. 10.1016/0006-8993(93)91265-T Duckrow RB: A brief hypoperfusion precedes spreading depression if nitric oxide synthesis is inhibited. Brain Res 1993, 618: 190–195. 10.1016/0006-8993(93)91265-T
82.
go back to reference Piper RD, Lambert GA, Duckworth JW: Cortical blood flow changes during spreading depression in cats. Am J Physiol 1991, 261: H96-H102. Piper RD, Lambert GA, Duckworth JW: Cortical blood flow changes during spreading depression in cats. Am J Physiol 1991, 261: H96-H102.
83.
go back to reference Lauritzen M, Jørgensen MB, Diemer NH, Gjedde A, Hansen AJ: Persistent oligemia of rat cerebral cortex in the wake of spreading depression. Ann Neurol 1982, 12: 469–474. 10.1002/ana.410120510 Lauritzen M, Jørgensen MB, Diemer NH, Gjedde A, Hansen AJ: Persistent oligemia of rat cerebral cortex in the wake of spreading depression. Ann Neurol 1982, 12: 469–474. 10.1002/ana.410120510
84.
go back to reference Goadsby PJ: The oligemic phase of cortical spreading depression is not blocked by tirilazad mesylate (U-74006F). Brain Res 1992, 588: 140–143. 10.1016/0006-8993(92)91353-G Goadsby PJ: The oligemic phase of cortical spreading depression is not blocked by tirilazad mesylate (U-74006F). Brain Res 1992, 588: 140–143. 10.1016/0006-8993(92)91353-G
85.
go back to reference Ba AM, Guiou M, Pouratian N, Muthialu A, Rex DE, Cannestra AF, Chen JW, Toga AW: Multiwavelength optical intrinsic signal imaging of cortical spreading depression. J Neurophysiol 2002, 88: 2726–2735. 10.1152/jn.00729.2001 Ba AM, Guiou M, Pouratian N, Muthialu A, Rex DE, Cannestra AF, Chen JW, Toga AW: Multiwavelength optical intrinsic signal imaging of cortical spreading depression. J Neurophysiol 2002, 88: 2726–2735. 10.1152/jn.00729.2001
86.
go back to reference Guiou M, Sheth S, Nemoto M, Walker M, Pouratian N, Ba A, Toga AW: Cortical spreading depression produces long-term disruption of activity-related changes in cerebral blood volume and neurovascular coupling. J Biomed Opt 2005,10(1):11004. 10.1117/1.1852556 Guiou M, Sheth S, Nemoto M, Walker M, Pouratian N, Ba A, Toga AW: Cortical spreading depression produces long-term disruption of activity-related changes in cerebral blood volume and neurovascular coupling. J Biomed Opt 2005,10(1):11004. 10.1117/1.1852556
87.
go back to reference O'Farrell AM, Rex DE, Muthialu A, Pouratian N, Wong GK, Cannestra AF, Chen JW, Toga AW: Characterization of optical intrinsic signals and blood volume during cortical spreading depression. Neuroreport 2000, 11: 2121–2125. 10.1097/00001756-200007140-00013 O'Farrell AM, Rex DE, Muthialu A, Pouratian N, Wong GK, Cannestra AF, Chen JW, Toga AW: Characterization of optical intrinsic signals and blood volume during cortical spreading depression. Neuroreport 2000, 11: 2121–2125. 10.1097/00001756-200007140-00013
88.
go back to reference Ayata C, Shin HK, Salomone S, Ozdemir-Gursoy Y, Boas DA, Dunn AK, Moskowitz MA: Pronounced hypoperfusion during spreading depression in mouse cortex. J Cereb Blood Flow Metab 2004, 24: 1172–1182. Ayata C, Shin HK, Salomone S, Ozdemir-Gursoy Y, Boas DA, Dunn AK, Moskowitz MA: Pronounced hypoperfusion during spreading depression in mouse cortex. J Cereb Blood Flow Metab 2004, 24: 1172–1182.
89.
go back to reference Brennan KC, Beltrán-Parrazal L, López-Valdés HE, Theriot J, Toga AW, Charles AC: Distinct vascular conduction with cortical spreading depression. J Neurophysiol 2007, 97: 4143–4151. 10.1152/jn.00028.2007 Brennan KC, Beltrán-Parrazal L, López-Valdés HE, Theriot J, Toga AW, Charles AC: Distinct vascular conduction with cortical spreading depression. J Neurophysiol 2007, 97: 4143–4151. 10.1152/jn.00028.2007
90.
go back to reference Chang JC, Shook LL, Biag J, Nguyen EN, Toga AW, Charles AC, Brennan KC: Biphasic direct current shift, haemoglobin desaturation and neurovascular uncoupling in cortical spreading depression. Brain 2010, 133: 996–1012. 10.1093/brain/awp338PubMedCentral Chang JC, Shook LL, Biag J, Nguyen EN, Toga AW, Charles AC, Brennan KC: Biphasic direct current shift, haemoglobin desaturation and neurovascular uncoupling in cortical spreading depression. Brain 2010, 133: 996–1012. 10.1093/brain/awp338PubMedCentral
91.
go back to reference Wang M, Obrenovich TP, Ureniak J: Effects of the nitric oxide donor, DEA/NO on cortical spreading depression. Neuropharmacology 2003, 44: 949–957. 10.1016/S0028-3908(03)00082-0 Wang M, Obrenovich TP, Ureniak J: Effects of the nitric oxide donor, DEA/NO on cortical spreading depression. Neuropharmacology 2003, 44: 949–957. 10.1016/S0028-3908(03)00082-0
92.
go back to reference Kleeberg J, Petzold GC, Major S, Dirnagl U, Dreier JP: ET-1 induces cortical spreading depression via activation of the ETA receptor/phospholipase C pathway in vivo. Am J Physiol Heart Circ Physiol 2004, 286: H1339-H1346. Kleeberg J, Petzold GC, Major S, Dirnagl U, Dreier JP: ET-1 induces cortical spreading depression via activation of the ETA receptor/phospholipase C pathway in vivo. Am J Physiol Heart Circ Physiol 2004, 286: H1339-H1346.
93.
go back to reference Dreier JP, Kleeberg J, Alam M, Major S, Kohl-Bareis M, Petzold GC, Victorov I, Dirnagl U, Obrenovitch TP, Priller J: Endothelin-1-induced spreading depression in rats is associated with a microarea of selective neuronal necrosis. Exp Biol Med (Maywood) 2007, 232: 204–213. Dreier JP, Kleeberg J, Alam M, Major S, Kohl-Bareis M, Petzold GC, Victorov I, Dirnagl U, Obrenovitch TP, Priller J: Endothelin-1-induced spreading depression in rats is associated with a microarea of selective neuronal necrosis. Exp Biol Med (Maywood) 2007, 232: 204–213.
94.
go back to reference Ophoff RA, Terwindt GM, Vergouwe MN, van Eijk R, Oefner PJ, Hoffman SM, Lamerdin JE, Mohrenweiser HW, Bulman DE, Ferrari M, Haan J, Lindhout D, van Ommen GJ, Hofker MH, Ferrari MD, Frants RR: Familial hemiplegic migraine and episodic ataxia type-2 are caused by mutations in the Ca2+ channel gene CACNL1A4. Cell 1996, 87: 543–552. 10.1016/S0092-8674(00)81373-2 Ophoff RA, Terwindt GM, Vergouwe MN, van Eijk R, Oefner PJ, Hoffman SM, Lamerdin JE, Mohrenweiser HW, Bulman DE, Ferrari M, Haan J, Lindhout D, van Ommen GJ, Hofker MH, Ferrari MD, Frants RR: Familial hemiplegic migraine and episodic ataxia type-2 are caused by mutations in the Ca2+ channel gene CACNL1A4. Cell 1996, 87: 543–552. 10.1016/S0092-8674(00)81373-2
95.
go back to reference van den Maagdenberg AM, Pietrobon D, Pizzorusso T, Kaja S, Broos LA, Cesetti T, van de Ven RC, Tottene A, van der Kaa J, Plomp JJ, Frants RR, Ferrari MD: A Cacna1a knockin migraine mouse model with increased susceptibility to cortical spreading depression. Neuron 2004, 41: 701–710. 10.1016/S0896-6273(04)00085-6 van den Maagdenberg AM, Pietrobon D, Pizzorusso T, Kaja S, Broos LA, Cesetti T, van de Ven RC, Tottene A, van der Kaa J, Plomp JJ, Frants RR, Ferrari MD: A Cacna1a knockin migraine mouse model with increased susceptibility to cortical spreading depression. Neuron 2004, 41: 701–710. 10.1016/S0896-6273(04)00085-6
96.
go back to reference Pietrobon D: Function and dysfunction of synaptic calcium channels: insights from mouse models. Curr Opin Neurobiol 2005, 15: 257–265. 10.1016/j.conb.2005.05.010 Pietrobon D: Function and dysfunction of synaptic calcium channels: insights from mouse models. Curr Opin Neurobiol 2005, 15: 257–265. 10.1016/j.conb.2005.05.010
97.
go back to reference Stam AH, Haan J, van den Maagdenberg AM, Ferrari MD, Terwindt GM: Migraine and genetic and acquired vasculopathies. Cephalalgia 2009, 29: 1006–1017. 10.1111/j.1468-2982.2009.01940.x Stam AH, Haan J, van den Maagdenberg AM, Ferrari MD, Terwindt GM: Migraine and genetic and acquired vasculopathies. Cephalalgia 2009, 29: 1006–1017. 10.1111/j.1468-2982.2009.01940.x
98.
go back to reference Uchitel OD, Inchauspe CG, Urbano FJ, Di Guilmi MN: CaV2.1 voltage activated calcium channels and synaptic transmission in familial hemiplegic migraine pathogenesis. J Physiol Paris 2012, 106: 12–22. 10.1016/j.jphysparis.2011.10.004 Uchitel OD, Inchauspe CG, Urbano FJ, Di Guilmi MN: CaV2.1 voltage activated calcium channels and synaptic transmission in familial hemiplegic migraine pathogenesis. J Physiol Paris 2012, 106: 12–22. 10.1016/j.jphysparis.2011.10.004
99.
go back to reference Inchauspe CG, Urbano FJ, Di Guilmi MN, Forsythe ID, Ferrari MD, van den Maagdenberg AM, Uchitel OD: Gain of function in FHM-1 Cav 2.1 knock-in mice is related to the shape of the action potential. J Neurophysiol 2010, 104: 291–299. 10.1152/jn.00034.2010PubMedCentral Inchauspe CG, Urbano FJ, Di Guilmi MN, Forsythe ID, Ferrari MD, van den Maagdenberg AM, Uchitel OD: Gain of function in FHM-1 Cav 2.1 knock-in mice is related to the shape of the action potential. J Neurophysiol 2010, 104: 291–299. 10.1152/jn.00034.2010PubMedCentral
100.
go back to reference Pietrobon D: Cav2.1 channelopathies. Pflugers Arch 2010, 460: 375–393. 10.1007/s00424-010-0802-8 Pietrobon D: Cav2.1 channelopathies. Pflugers Arch 2010, 460: 375–393. 10.1007/s00424-010-0802-8
101.
go back to reference Pietrobon D: Insights into migraine mechanisms and CaV2.1 calcium channel function from mouse models of familial hemiplegic migraine. J Physiol 2010, 588: 1871–1878. 10.1113/jphysiol.2010.188003PubMedCentral Pietrobon D: Insights into migraine mechanisms and CaV2.1 calcium channel function from mouse models of familial hemiplegic migraine. J Physiol 2010, 588: 1871–1878. 10.1113/jphysiol.2010.188003PubMedCentral
102.
go back to reference Tottene A, Fellin T, Pagnutti S, Luvisetto S, Striessnig J, Fletcher C, Pietrobon D: Familial hemiplegic migraine mutations increase Ca2+ influx through single human Cav2.1 channels and decrease maximal Cav2.1 current density in neurons. Proc Natl Acad Sci USA 2002, 99: 13284–13289. 10.1073/pnas.192242399PubMedCentral Tottene A, Fellin T, Pagnutti S, Luvisetto S, Striessnig J, Fletcher C, Pietrobon D: Familial hemiplegic migraine mutations increase Ca2+ influx through single human Cav2.1 channels and decrease maximal Cav2.1 current density in neurons. Proc Natl Acad Sci USA 2002, 99: 13284–13289. 10.1073/pnas.192242399PubMedCentral
103.
go back to reference Tottene A, Conti R, Fabbro A, Vecchia D, Shapovalova M, Santello M, van den Maagdenberg AM, Ferrari MD, Pietrobon D: Enhanced excitatory transmission at cortical synapses as the basis for facilitated spreading depression in Ca(v)2.1 knockin migraine mice. Neuron 2009,61(5):762–773. 10.1016/j.neuron.2009.01.027 Tottene A, Conti R, Fabbro A, Vecchia D, Shapovalova M, Santello M, van den Maagdenberg AM, Ferrari MD, Pietrobon D: Enhanced excitatory transmission at cortical synapses as the basis for facilitated spreading depression in Ca(v)2.1 knockin migraine mice. Neuron 2009,61(5):762–773. 10.1016/j.neuron.2009.01.027
104.
go back to reference van den Maagdenberg AM, Pizzorusso T, Kaja S, Terpolilli N, Shapovalova M, Hoebeek FE, Barrett CF, Gherardini L, van de Ven RC, Todorov B, Broos LA, Tottene A, Gao Z, Fodor M, De Zeeuw CI, Frants RR, Plesnila N, Plomp JJ, Pietrobon D, Ferrari MD: High cortical spreading depression susceptibility and migraine-associated symptoms in Cav2.1 S218L mice. Ann Neurol 2010, 67: 85–98. 10.1002/ana.21815 van den Maagdenberg AM, Pizzorusso T, Kaja S, Terpolilli N, Shapovalova M, Hoebeek FE, Barrett CF, Gherardini L, van de Ven RC, Todorov B, Broos LA, Tottene A, Gao Z, Fodor M, De Zeeuw CI, Frants RR, Plesnila N, Plomp JJ, Pietrobon D, Ferrari MD: High cortical spreading depression susceptibility and migraine-associated symptoms in Cav2.1 S218L mice. Ann Neurol 2010, 67: 85–98. 10.1002/ana.21815
105.
go back to reference Ayata C, Shimizu-Sasamata M, Lo EH, Noebels JL, Moskowitz MA: Impaired neurotransmitter release and elevated threshold for cortical spreading depression in mice with mutations in the α1A subunit of P/Q type calcium channels. Neuroscience 2000, 95: 639–645. Ayata C, Shimizu-Sasamata M, Lo EH, Noebels JL, Moskowitz MA: Impaired neurotransmitter release and elevated threshold for cortical spreading depression in mice with mutations in the α1A subunit of P/Q type calcium channels. Neuroscience 2000, 95: 639–645.
106.
go back to reference Leo L, Gherardini L, Barone V, De Fusco M, Pietrobon D, Pizzorusso T, Casari G: Increased susceptibility to cortical spreading depression in the mouse model of familial hemiplegic migraine type 2. PLoS Genet 2011,7(6):e1002129. 10.1371/journal.pgen.1002129PubMedCentral Leo L, Gherardini L, Barone V, De Fusco M, Pietrobon D, Pizzorusso T, Casari G: Increased susceptibility to cortical spreading depression in the mouse model of familial hemiplegic migraine type 2. PLoS Genet 2011,7(6):e1002129. 10.1371/journal.pgen.1002129PubMedCentral
107.
go back to reference Eikermann-Haerter K, Yuzawa I, Dilekoz E, Joutel A, Moskowitz MA, Ayata C: Cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy syndrome mutations increase susceptibility to spreading depression. Ann Neurol 2011, 69: 413–418. 10.1002/ana.22281PubMedCentral Eikermann-Haerter K, Yuzawa I, Dilekoz E, Joutel A, Moskowitz MA, Ayata C: Cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy syndrome mutations increase susceptibility to spreading depression. Ann Neurol 2011, 69: 413–418. 10.1002/ana.22281PubMedCentral
108.
go back to reference Nagel-Leiby S, Welch KM, Grunfeld S, D’Andrea G: Ovarian steroid levels in migraine with and without aura. Cephalalgia 1990, 10: 147–152. 10.1046/j.1468-2982.1990.1003147.x Nagel-Leiby S, Welch KM, Grunfeld S, D’Andrea G: Ovarian steroid levels in migraine with and without aura. Cephalalgia 1990, 10: 147–152. 10.1046/j.1468-2982.1990.1003147.x
109.
go back to reference MacGregor EA: Oestrogen and attacks of migraine with and without aura. Lancet Neurol 2004, 3: 354–361. 10.1016/S1474-4422(04)00768-9 MacGregor EA: Oestrogen and attacks of migraine with and without aura. Lancet Neurol 2004, 3: 354–361. 10.1016/S1474-4422(04)00768-9
110.
go back to reference Ertresvag JM, Zwart JA, Helde G, Johnsen HJ, Bovim G: Headache and transient focal neurological symptoms during pregnancy, a prospective cohort. Acta Neurol Scand 2005, 111: 233–237. 10.1111/j.1600-0404.2005.00350.x Ertresvag JM, Zwart JA, Helde G, Johnsen HJ, Bovim G: Headache and transient focal neurological symptoms during pregnancy, a prospective cohort. Acta Neurol Scand 2005, 111: 233–237. 10.1111/j.1600-0404.2005.00350.x
111.
go back to reference Granella F, Sances G, Zanferrari C, Costa A, Martignoni E, Manzoni GC: Migraine without aura and reproductive life events: a clinical epidemiological study in 1300 women. Headache 1993, 33: 385–389. 10.1111/j.1526-4610.1993.hed3307385.x Granella F, Sances G, Zanferrari C, Costa A, Martignoni E, Manzoni GC: Migraine without aura and reproductive life events: a clinical epidemiological study in 1300 women. Headache 1993, 33: 385–389. 10.1111/j.1526-4610.1993.hed3307385.x
112.
go back to reference Calton GJ, Burnett JW: Danazol and migraine. N Engl J Med 1984, 310: 721–722. Calton GJ, Burnett JW: Danazol and migraine. N Engl J Med 1984, 310: 721–722.
113.
go back to reference Jonsson B, Von Reis G, Sahlgren E: Testosterone therapy of headache. Acta Psychiatr Neurol Scand 1951, 74: 102–105. Jonsson B, Von Reis G, Sahlgren E: Testosterone therapy of headache. Acta Psychiatr Neurol Scand 1951, 74: 102–105.
114.
go back to reference Moehlig RC: Methyl testosterone for migraine of women; report of sixty cases. J Mich State Med Soc 1955, 54: 577–579. Moehlig RC: Methyl testosterone for migraine of women; report of sixty cases. J Mich State Med Soc 1955, 54: 577–579.
115.
go back to reference Vincent FM: Migraine responsive to danazol. Neurology 1985, 35: 618. Vincent FM: Migraine responsive to danazol. Neurology 1985, 35: 618.
116.
go back to reference Lichten EM, Bennett RS, Whitty AJ, Daoud Y: Efficacy of danazol in the control of hormonal migraine. J Reprod Med 1991,36(6):419–424. Lichten EM, Bennett RS, Whitty AJ, Daoud Y: Efficacy of danazol in the control of hormonal migraine. J Reprod Med 1991,36(6):419–424.
117.
go back to reference Arango O, Bielsa O, Pascual-Calvet J, Herrero M, Gelabert-Mas A: Disappearance of migraine crises in two patients with male infertility treated with human chorionic gonadotropin/human menopausal gonadotrophin. Rev Neurol 1996, 24: 977–979. Arango O, Bielsa O, Pascual-Calvet J, Herrero M, Gelabert-Mas A: Disappearance of migraine crises in two patients with male infertility treated with human chorionic gonadotropin/human menopausal gonadotrophin. Rev Neurol 1996, 24: 977–979.
118.
go back to reference Pringsheim T, Gooren L: Migraine prevalence in male to female transsexuals on hormone therapy. Neurology 2004, 63: 593–594. Pringsheim T, Gooren L: Migraine prevalence in male to female transsexuals on hormone therapy. Neurology 2004, 63: 593–594.
119.
go back to reference Eikermann-Haerter K, Dileköz E, Kudo C, Savitz SI, Waeber C, Baum MJ, Ferrari MD, van den Maagdenberg AM, Moskowitz MA, Ayata C: Genetic and hormonal factors modulate spreading depression and transient hemiparesis in mouse models of familial hemiplegic migraine type 1. J Clin Invest 2009, 119: 99–109.PubMedCentral Eikermann-Haerter K, Dileköz E, Kudo C, Savitz SI, Waeber C, Baum MJ, Ferrari MD, van den Maagdenberg AM, Moskowitz MA, Ayata C: Genetic and hormonal factors modulate spreading depression and transient hemiparesis in mouse models of familial hemiplegic migraine type 1. J Clin Invest 2009, 119: 99–109.PubMedCentral
120.
go back to reference Eikermann-Haerter K, Baum MJ, Ferrari MD, van den Maagdenberg AM, Moskowitz MA, Ayata C: Androgenic suppression of spreading depression in familial hemiplegic migraine type 1 mutant mice. Ann Neurol 2009, 66: 564–568. 10.1002/ana.21779PubMedCentral Eikermann-Haerter K, Baum MJ, Ferrari MD, van den Maagdenberg AM, Moskowitz MA, Ayata C: Androgenic suppression of spreading depression in familial hemiplegic migraine type 1 mutant mice. Ann Neurol 2009, 66: 564–568. 10.1002/ana.21779PubMedCentral
121.
go back to reference Benarroch EE: Neuron-astrocyte interactions: partnership for normal function and disease in the central nervous system. Mayo Clin Proc 2005, 80: 1326–1338. 10.4065/80.10.1326 Benarroch EE: Neuron-astrocyte interactions: partnership for normal function and disease in the central nervous system. Mayo Clin Proc 2005, 80: 1326–1338. 10.4065/80.10.1326
122.
go back to reference Lian XY, Stringer JL: Energy failure in astrocytes increases the vulnerability of neurons to spreading depression. Eur J Neurosci 2004, 19: 2446–2454. 10.1111/j.0953-816X.2004.03289.x Lian XY, Stringer JL: Energy failure in astrocytes increases the vulnerability of neurons to spreading depression. Eur J Neurosci 2004, 19: 2446–2454. 10.1111/j.0953-816X.2004.03289.x
123.
go back to reference Lian XY, Stringer JL: Astrocytes contribute to regulation of extracellular calcium and potassium in the rat cerebral cortex during spreading depression. J Pharmacol Exp Ther 2007, 321: 564–572. 10.1124/jpet.106.117101 Lian XY, Stringer JL: Astrocytes contribute to regulation of extracellular calcium and potassium in the rat cerebral cortex during spreading depression. J Pharmacol Exp Ther 2007, 321: 564–572. 10.1124/jpet.106.117101
124.
go back to reference Giaume C, McCarthy KD: Control of gap-junctional communication in astrocytic networks. Trends Neurosci 1996, 19: 319–325. 10.1016/0166-2236(96)10046-1 Giaume C, McCarthy KD: Control of gap-junctional communication in astrocytic networks. Trends Neurosci 1996, 19: 319–325. 10.1016/0166-2236(96)10046-1
125.
go back to reference Bennett MVL, Contreras JE, Bukauskas FF, Sáez JC: New roles for astrocytes: gap junction hemichannels have something to communicate. Trends Neurosci 2003, 26: 610–617. 10.1016/j.tins.2003.09.008PubMedCentral Bennett MVL, Contreras JE, Bukauskas FF, Sáez JC: New roles for astrocytes: gap junction hemichannels have something to communicate. Trends Neurosci 2003, 26: 610–617. 10.1016/j.tins.2003.09.008PubMedCentral
126.
go back to reference Nagy JI, Dudek FE, Rash JE: Update on connexins and gap junctions in neurons and glia in the mammalian nervous system. Brain Res Rev 2004, 47: 191–215. 10.1016/j.brainresrev.2004.05.005 Nagy JI, Dudek FE, Rash JE: Update on connexins and gap junctions in neurons and glia in the mammalian nervous system. Brain Res Rev 2004, 47: 191–215. 10.1016/j.brainresrev.2004.05.005
127.
go back to reference Ye Z-C, Wyeth MS, Baltan-Tekkok S, Ransom BR: Functional hemichannels in astrocytes: a novel mechanism of glutamate release. J Neurosci 2003, 23: 3588–3596. Ye Z-C, Wyeth MS, Baltan-Tekkok S, Ransom BR: Functional hemichannels in astrocytes: a novel mechanism of glutamate release. J Neurosci 2003, 23: 3588–3596.
128.
go back to reference Peters O, Schipke CG, Hashimoto Y, Kettenmann H: Different mechanisms promote astrocyte Ca 2+ waves and spreading depression in the mouse neocortex. J Neurosci 2003,23(30):9888–9896. Peters O, Schipke CG, Hashimoto Y, Kettenmann H: Different mechanisms promote astrocyte Ca 2+ waves and spreading depression in the mouse neocortex. J Neurosci 2003,23(30):9888–9896.
129.
go back to reference Stout CE, Costantin JL, Naus CCG, Charles AC: Intercellular calcium signaling in astrocytes via ATP release through connexin hemichannels. J Biol Chem 2002, 277: 10482–10488. 10.1074/jbc.M109902200 Stout CE, Costantin JL, Naus CCG, Charles AC: Intercellular calcium signaling in astrocytes via ATP release through connexin hemichannels. J Biol Chem 2002, 277: 10482–10488. 10.1074/jbc.M109902200
130.
go back to reference Grafstein B, Liu S, Cotrina ML, Goldman SA, Nedergaard M: Meningeal cells can communicate with astrocytes by calcium signaling. Ann Neurol 2000, 47: 18–25. 10.1002/1531-8249(200001)47:1<18::AID-ANA6>3.0.CO;2-N Grafstein B, Liu S, Cotrina ML, Goldman SA, Nedergaard M: Meningeal cells can communicate with astrocytes by calcium signaling. Ann Neurol 2000, 47: 18–25. 10.1002/1531-8249(200001)47:1<18::AID-ANA6>3.0.CO;2-N
131.
go back to reference Gursoy-Ozdemir Y, Qiu J, Matsuoka N, Bolay H, Bermpohl D, Jin H, Wang X, Rosenberg GA, Lo EH, Moskowitz MA: Cortical spreading depression activates and upregulates MMP-9. J Clin Invest 2004, 113: 1447–1455.PubMedCentral Gursoy-Ozdemir Y, Qiu J, Matsuoka N, Bolay H, Bermpohl D, Jin H, Wang X, Rosenberg GA, Lo EH, Moskowitz MA: Cortical spreading depression activates and upregulates MMP-9. J Clin Invest 2004, 113: 1447–1455.PubMedCentral
132.
go back to reference Martins-Oliveira A, Speciali JG, Dach F, Marcaccini AM, Gonçalves FM, Gerlach RF, Tanus-Santos JE: Different circulating metalloproteinases profiles in women with migraine with and without aura. Clin Chim Acta 2009, 408: 60–64. 10.1016/j.cca.2009.07.008 Martins-Oliveira A, Speciali JG, Dach F, Marcaccini AM, Gonçalves FM, Gerlach RF, Tanus-Santos JE: Different circulating metalloproteinases profiles in women with migraine with and without aura. Clin Chim Acta 2009, 408: 60–64. 10.1016/j.cca.2009.07.008
133.
go back to reference Gao HM, Li L, Zhang KL, Chen XH, Tian SQ, Zhang ZL: Impact of migraine attacks on the blood–brain barrier. Chin Med J (Engl) 2010, 123: 2559–2561. Gao HM, Li L, Zhang KL, Chen XH, Tian SQ, Zhang ZL: Impact of migraine attacks on the blood–brain barrier. Chin Med J (Engl) 2010, 123: 2559–2561.
134.
go back to reference Martins-Oliveira A, Gonçalves FM, Speciali JG, Fontana V, Izidoro-Toledo TC, Belo VA, Dach F, Tanus-Santos JE: Specific matrix metalloproteinase 9 (MMP-9) haplotype affect the circulating MMP-9 levels in women with migraine. J Neuroimmunol 2012, 252: 89–94. 10.1016/j.jneuroim.2012.07.016 Martins-Oliveira A, Gonçalves FM, Speciali JG, Fontana V, Izidoro-Toledo TC, Belo VA, Dach F, Tanus-Santos JE: Specific matrix metalloproteinase 9 (MMP-9) haplotype affect the circulating MMP-9 levels in women with migraine. J Neuroimmunol 2012, 252: 89–94. 10.1016/j.jneuroim.2012.07.016
135.
go back to reference Gonçalves FM, Martins-Oliveira A, Lacchini R, Belo VA, Speciali JG, Dach F, Tanus-Santos JE: Matrix metalloproteinase (MMP)-2 gene polymorphisms affect circulating MMP-2 levels in patients with migraine with aura. Gene 2013, 512: 35–40. 10.1016/j.gene.2012.09.109 Gonçalves FM, Martins-Oliveira A, Lacchini R, Belo VA, Speciali JG, Dach F, Tanus-Santos JE: Matrix metalloproteinase (MMP)-2 gene polymorphisms affect circulating MMP-2 levels in patients with migraine with aura. Gene 2013, 512: 35–40. 10.1016/j.gene.2012.09.109
136.
go back to reference Gupta VK: CSD, BBB and MMP-9 elevations: animal experiments versus clinical phenomena in migraine. Expert Rev Neurother 2009, 9: 1595–1614. 10.1586/ern.09.103 Gupta VK: CSD, BBB and MMP-9 elevations: animal experiments versus clinical phenomena in migraine. Expert Rev Neurother 2009, 9: 1595–1614. 10.1586/ern.09.103
137.
go back to reference Levy D: Endogenous mechanisms underlying the activation and sensitization of meningeal nociceptors: the role of immuno-vascular interactions and cortical spreading depression. Curr Pain Headache Rep 2012, 16: 270–277. 10.1007/s11916-012-0255-1 Levy D: Endogenous mechanisms underlying the activation and sensitization of meningeal nociceptors: the role of immuno-vascular interactions and cortical spreading depression. Curr Pain Headache Rep 2012, 16: 270–277. 10.1007/s11916-012-0255-1
138.
go back to reference Lambert GA, Truong L, Zagami AS: Effect of cortical spreading depression on basal and evoked traffic in the trigeminovascular sensory system. Cephalalgia 2011,31(14):1439–1451. 10.1177/0333102411422383 Lambert GA, Truong L, Zagami AS: Effect of cortical spreading depression on basal and evoked traffic in the trigeminovascular sensory system. Cephalalgia 2011,31(14):1439–1451. 10.1177/0333102411422383
139.
go back to reference Ji R-R, Kohno T, Moore KA, Woolf CJ: Central sensitization and LTP: do pain and memory share similar mechanisms? Trends Neurosci 2003, 26: 696–705. 10.1016/j.tins.2003.09.017 Ji R-R, Kohno T, Moore KA, Woolf CJ: Central sensitization and LTP: do pain and memory share similar mechanisms? Trends Neurosci 2003, 26: 696–705. 10.1016/j.tins.2003.09.017
140.
go back to reference Goadsby PJ, Akerman S: The trigeminovascular system does not require a peripheral sensory input to be activated–migraine is a central disorder. Focus on 'Effect of cortical spreading depression on basal and evoked traffic in the trigeminovascular sensory system'. Cephalalgia 2012, 32: 3–5. 10.1177/0333102411430267 Goadsby PJ, Akerman S: The trigeminovascular system does not require a peripheral sensory input to be activated–migraine is a central disorder. Focus on 'Effect of cortical spreading depression on basal and evoked traffic in the trigeminovascular sensory system'. Cephalalgia 2012, 32: 3–5. 10.1177/0333102411430267
141.
go back to reference Strassman AM, Raimond SA, Burstein R: Sensitization of meningeal sensory neurons and the origin of headache. Nature 1996, 384: 560–564. 10.1038/384560a0 Strassman AM, Raimond SA, Burstein R: Sensitization of meningeal sensory neurons and the origin of headache. Nature 1996, 384: 560–564. 10.1038/384560a0
142.
go back to reference Karatas H, Erdener SE, Gursoy-Ozdemir Y, Lule S, Eren-Koçak E, Sen ZD, Dalkara T: Spreading depression triggers headache by activating neuronal Panx1 channels. Science 2013, 339: 1092–1095. 10.1126/science.1231897 Karatas H, Erdener SE, Gursoy-Ozdemir Y, Lule S, Eren-Koçak E, Sen ZD, Dalkara T: Spreading depression triggers headache by activating neuronal Panx1 channels. Science 2013, 339: 1092–1095. 10.1126/science.1231897
143.
go back to reference Silverman WR, de Rivero Vaccari JP, Locovei S, Qiu F, Carlsson SK, Scemes E, Keane RW, Dahl G: The pannexin 1 channel activates the inflammasome in neurons and astrocytes. J Biol Chem 2009, 284: 18143–18151. 10.1074/jbc.M109.004804PubMedCentral Silverman WR, de Rivero Vaccari JP, Locovei S, Qiu F, Carlsson SK, Scemes E, Keane RW, Dahl G: The pannexin 1 channel activates the inflammasome in neurons and astrocytes. J Biol Chem 2009, 284: 18143–18151. 10.1074/jbc.M109.004804PubMedCentral
144.
go back to reference Müller S, Ronfani L, Bianchi ME: Regulated expression and subcellular localization of HMGB1, a chromatin protein with a cytokine function. J Intern Med 2004, 255: 332–343. 10.1111/j.1365-2796.2003.01296.x Müller S, Ronfani L, Bianchi ME: Regulated expression and subcellular localization of HMGB1, a chromatin protein with a cytokine function. J Intern Med 2004, 255: 332–343. 10.1111/j.1365-2796.2003.01296.x
145.
go back to reference Faraco G, Fossati S, Bianchi ME, Patrone M, Pedrazzi M, Sparatore B, Moroni F, Chiarugi A: High mobility group box 1 protein is released by neural cells upon different stresses and worsens ischemic neurodegeneration in vitro and in vivo. J Neurochem 2007, 103: 590–603. 10.1111/j.1471-4159.2007.04788.x Faraco G, Fossati S, Bianchi ME, Patrone M, Pedrazzi M, Sparatore B, Moroni F, Chiarugi A: High mobility group box 1 protein is released by neural cells upon different stresses and worsens ischemic neurodegeneration in vitro and in vivo. J Neurochem 2007, 103: 590–603. 10.1111/j.1471-4159.2007.04788.x
146.
go back to reference Pontremoli S, Melloni E: Selective proinflammatory activation of astrocytes by high-mobility group box 1 protein signaling. J Immunol 2007, 179: 8525–8532. Pontremoli S, Melloni E: Selective proinflammatory activation of astrocytes by high-mobility group box 1 protein signaling. J Immunol 2007, 179: 8525–8532.
147.
go back to reference Read SJ, Parsons AA: Sumatriptan modifies cortical free radical release during cortical spreading depression. A novel antimigraine action for sumatriptan? Brain Res 2000, 870: 44–53. 10.1016/S0006-8993(00)02400-8 Read SJ, Parsons AA: Sumatriptan modifies cortical free radical release during cortical spreading depression. A novel antimigraine action for sumatriptan? Brain Res 2000, 870: 44–53. 10.1016/S0006-8993(00)02400-8
148.
go back to reference Read SJ, Hirst WD, Upton N, Parsons AA: Cortical spreading depression produces increased cGMP levels in cortex and brain stem that is inhibited by tonabersat (SB-220453) but not sumatriptan. Brain Res 2001, 891: 69–77. 10.1016/S0006-8993(00)03191-7 Read SJ, Hirst WD, Upton N, Parsons AA: Cortical spreading depression produces increased cGMP levels in cortex and brain stem that is inhibited by tonabersat (SB-220453) but not sumatriptan. Brain Res 2001, 891: 69–77. 10.1016/S0006-8993(00)03191-7
149.
go back to reference Ayata C: Spreading depression: from serendipity to targeted therapy in migraine prophylaxis. Cephalalgia 2009, 29: 1095–1114. 10.1111/j.1468-2982.2009.01982.x Ayata C: Spreading depression: from serendipity to targeted therapy in migraine prophylaxis. Cephalalgia 2009, 29: 1095–1114. 10.1111/j.1468-2982.2009.01982.x
150.
go back to reference Kaube H, Goadsby PJ: Anti-migraine compounds fail to modulate the propagation of cortical spreading depression in the cat. Eur Neurol 1994, 34: 30–35. 10.1159/000117004 Kaube H, Goadsby PJ: Anti-migraine compounds fail to modulate the propagation of cortical spreading depression in the cat. Eur Neurol 1994, 34: 30–35. 10.1159/000117004
151.
go back to reference Ayata C, Jin H, Kudo C, Dalkara T, Moskowitz MA: Suppression of cortical spreading depression in migraine prophylaxis. Ann Neurol 2006, 59: 652–661. 10.1002/ana.20778 Ayata C, Jin H, Kudo C, Dalkara T, Moskowitz MA: Suppression of cortical spreading depression in migraine prophylaxis. Ann Neurol 2006, 59: 652–661. 10.1002/ana.20778
152.
go back to reference Unekawa M, Tomita Y, Toriumi H, Suzuki N: Suppressive effect of chronic peroral topiramate on potassium-induced cortical spreading depression in rats. Cephalalgia 2012, 32: 518–527. 10.1177/0333102412444015 Unekawa M, Tomita Y, Toriumi H, Suzuki N: Suppressive effect of chronic peroral topiramate on potassium-induced cortical spreading depression in rats. Cephalalgia 2012, 32: 518–527. 10.1177/0333102412444015
153.
go back to reference Akerman S, Goadsby PJ: Topiramate inhibits cortical spreading depression in rat and cat: impact in migraine aura. Neuroreport 2005, 16: 1383–1387. 10.1097/01.wnr.0000175250.33159.a9 Akerman S, Goadsby PJ: Topiramate inhibits cortical spreading depression in rat and cat: impact in migraine aura. Neuroreport 2005, 16: 1383–1387. 10.1097/01.wnr.0000175250.33159.a9
154.
go back to reference Hoffmann U, Dileköz E, Kudo C, Ayata C: Gabapentin suppresses cortical spreading depression susceptibility. J Cereb Blood Flow Metab 2010, 30: 1588–1592. 10.1038/jcbfm.2010.92PubMedCentral Hoffmann U, Dileköz E, Kudo C, Ayata C: Gabapentin suppresses cortical spreading depression susceptibility. J Cereb Blood Flow Metab 2010, 30: 1588–1592. 10.1038/jcbfm.2010.92PubMedCentral
155.
go back to reference D'Andrea G, Granella F, Cadaldini M, Manzoni GC: Effectiveness of lamotrigine in the prophylaxis of migraine with aura: an open pilot study. Cephalalgia 1999, 19: 64–66. 10.1111/j.1468-2982.1999.1901064.x D'Andrea G, Granella F, Cadaldini M, Manzoni GC: Effectiveness of lamotrigine in the prophylaxis of migraine with aura: an open pilot study. Cephalalgia 1999, 19: 64–66. 10.1111/j.1468-2982.1999.1901064.x
156.
go back to reference Lampl C, Buzath A, Klinger D, Neumann K: Lamotrigine in the prophylactic treatment of migraine aura–a pilot study. Cephalalgia 1999, 19: 58–63. 10.1111/j.1468-2982.1999.1901058.x Lampl C, Buzath A, Klinger D, Neumann K: Lamotrigine in the prophylactic treatment of migraine aura–a pilot study. Cephalalgia 1999, 19: 58–63. 10.1111/j.1468-2982.1999.1901058.x
157.
go back to reference Lampl C, Katsarava Z, Diener HC, Limmroth V: Lamotrigine reduces migraine aura and migraine attacks in patients with migraine with aura. J Neurol Neurosurg Psychiatry 2005, 76: 1730–1732. 10.1136/jnnp.2005.063750PubMedCentral Lampl C, Katsarava Z, Diener HC, Limmroth V: Lamotrigine reduces migraine aura and migraine attacks in patients with migraine with aura. J Neurol Neurosurg Psychiatry 2005, 76: 1730–1732. 10.1136/jnnp.2005.063750PubMedCentral
158.
go back to reference Steiner TJ, Findley LJ, Yuen AW: Lamotrigine versus placebo in the prophylaxis of migraine with and without aura. Cephalalgia 1997, 17: 109–112. 10.1046/j.1468-2982.1997.1702109.x Steiner TJ, Findley LJ, Yuen AW: Lamotrigine versus placebo in the prophylaxis of migraine with and without aura. Cephalalgia 1997, 17: 109–112. 10.1046/j.1468-2982.1997.1702109.x
159.
go back to reference Gupta P, Singh S, Goyal V, Shukla G, Behari M: Low-dose topiramate versus lamotrigine in migraine prophylaxis (the Lotolamp study). Headache 2007, 47: 402–412. Gupta P, Singh S, Goyal V, Shukla G, Behari M: Low-dose topiramate versus lamotrigine in migraine prophylaxis (the Lotolamp study). Headache 2007, 47: 402–412.
160.
go back to reference Bogdanov VB, Multon S, Chauvel V, Bogdanova OV, Prodanov D, Makarchuk MY, Schoenen J: Migraine preventive drugs differentially affect cortical spreading depression in rat. Neurobiol Dis 2011, 41: 430–435. 10.1016/j.nbd.2010.10.014 Bogdanov VB, Multon S, Chauvel V, Bogdanova OV, Prodanov D, Makarchuk MY, Schoenen J: Migraine preventive drugs differentially affect cortical spreading depression in rat. Neurobiol Dis 2011, 41: 430–435. 10.1016/j.nbd.2010.10.014
161.
go back to reference Marrannes R, Wauquier A, Reid K, De Prins E: The Prelude to The Migraine Attack. UK: Effects of drugs on cortical spreading depression. Baillière Tindal Oxford; 1986:158–173. Marrannes R, Wauquier A, Reid K, De Prins E: The Prelude to The Migraine Attack. UK: Effects of drugs on cortical spreading depression. Baillière Tindal Oxford; 1986:158–173.
162.
go back to reference Hansen A, Lauritzen M, Tfelt-Hansen P: Spreading cortical depression and antimigraine drugs. In The Pharmacological Basis of Migraine Therapy. Edited by: Amery WK, Nueten JM, Waquier A. London, UK: Putman; 1984:161–170. Hansen A, Lauritzen M, Tfelt-Hansen P: Spreading cortical depression and antimigraine drugs. In The Pharmacological Basis of Migraine Therapy. Edited by: Amery WK, Nueten JM, Waquier A. London, UK: Putman; 1984:161–170.
163.
go back to reference Reid KH, Marrannes R, Wauquier A: Effects of flunarizine on rat cerebral cortex. Drug Dev Res 1987, 10: 107–116. 10.1002/ddr.430100210 Reid KH, Marrannes R, Wauquier A: Effects of flunarizine on rat cerebral cortex. Drug Dev Res 1987, 10: 107–116. 10.1002/ddr.430100210
164.
go back to reference Wauquier A, Ashton D, Marrannes R: The effects of flunarizine in experimental models related to the pathogenesis of migraine. Cephalalgia 1985,5(2):119–123. Wauquier A, Ashton D, Marrannes R: The effects of flunarizine in experimental models related to the pathogenesis of migraine. Cephalalgia 1985,5(2):119–123.
165.
go back to reference Marrannes R, De Prins E, Fransen J, Clincke G: Neuropharmacology of spreading depression. In Migraine: Basic Mechanisms and Treatment. Edited by: Lehmenkuhler A, Grotemeyer KH, Tegtmeier F. Urban & Schwarzenberg: MD, USA; 1993:431–443. Marrannes R, De Prins E, Fransen J, Clincke G: Neuropharmacology of spreading depression. In Migraine: Basic Mechanisms and Treatment. Edited by: Lehmenkuhler A, Grotemeyer KH, Tegtmeier F. Urban & Schwarzenberg: MD, USA; 1993:431–443.
166.
go back to reference Shimazawa M, Hara H, Watano T, Sukamoto T: Effects of Ca 2+ channel blockers on cortical hypoperfusion and expression of c-Fos-like immunoreactivity after cortical spreading depression in rats. Br J Pharmacol 1995, 115: 1359–1368. 10.1111/j.1476-5381.1995.tb16624.xPubMedCentral Shimazawa M, Hara H, Watano T, Sukamoto T: Effects of Ca 2+ channel blockers on cortical hypoperfusion and expression of c-Fos-like immunoreactivity after cortical spreading depression in rats. Br J Pharmacol 1995, 115: 1359–1368. 10.1111/j.1476-5381.1995.tb16624.xPubMedCentral
167.
go back to reference Sarchielli P, Coata G, Firenze C, Morucci P, Abbritti G, Gallai V: Serum and salivary magnesium levels in migraine and tension-type headache. Results in a group of adult patients. Cephalalgia 1992, 12: 21–27. 10.1046/j.1468-2982.1992.1201021.x Sarchielli P, Coata G, Firenze C, Morucci P, Abbritti G, Gallai V: Serum and salivary magnesium levels in migraine and tension-type headache. Results in a group of adult patients. Cephalalgia 1992, 12: 21–27. 10.1046/j.1468-2982.1992.1201021.x
168.
go back to reference Gallai V, Sarchielli P, Morucci P, Abbritti G: Magnesium content of mononuclear blood cells in migraine patients. Headache 1994, 34: 160–165. 10.1111/j.1526-4610.1994.hed3403160.x Gallai V, Sarchielli P, Morucci P, Abbritti G: Magnesium content of mononuclear blood cells in migraine patients. Headache 1994, 34: 160–165. 10.1111/j.1526-4610.1994.hed3403160.x
169.
go back to reference Gallai V, Sarchielli P, Morucci P, Abbritti G: Red blood cell magnesium levels in migraine patients. Cephalalgia 1993, 13: 94–101. 10.1046/j.1468-2982.1993.1302094.x Gallai V, Sarchielli P, Morucci P, Abbritti G: Red blood cell magnesium levels in migraine patients. Cephalalgia 1993, 13: 94–101. 10.1046/j.1468-2982.1993.1302094.x
170.
go back to reference Mauskop A, Altura BM: Role of magnesium in the pathogenesis and treatment of migraines. Clin Neurosci 1998, 5: 24–27. Mauskop A, Altura BM: Role of magnesium in the pathogenesis and treatment of migraines. Clin Neurosci 1998, 5: 24–27.
171.
go back to reference Ramadan NM, Halvorson H, Vande-Linde A, Levine SR, Helpern JA, Welch KM: Low brain magnesium in migraine. Headache 1989, 29: 590–593. 10.1111/j.1526-4610.1989.hed2909590.x Ramadan NM, Halvorson H, Vande-Linde A, Levine SR, Helpern JA, Welch KM: Low brain magnesium in migraine. Headache 1989, 29: 590–593. 10.1111/j.1526-4610.1989.hed2909590.x
172.
go back to reference Bigal ME, Bordini CA, Tepper SJ, Speciali JG: Intravenous magnesium sulphate in the acute treatment of migraine without aura and migraine with aura. A randomized, double-blind, placebo-controlled study. Cephalalgia 2002, 22: 345–353. 10.1046/j.1468-2982.2002.00364.x Bigal ME, Bordini CA, Tepper SJ, Speciali JG: Intravenous magnesium sulphate in the acute treatment of migraine without aura and migraine with aura. A randomized, double-blind, placebo-controlled study. Cephalalgia 2002, 22: 345–353. 10.1046/j.1468-2982.2002.00364.x
173.
go back to reference van der Hel WS, van den Bergh WM, Nicolay K, Tulleken KA, Dijkhuizen RM: Suppression of cortical spreading depressions after magnesium treatment in the rat. Neuroreport 1998, 9: 2179–2182. 10.1097/00001756-199807130-00006 van der Hel WS, van den Bergh WM, Nicolay K, Tulleken KA, Dijkhuizen RM: Suppression of cortical spreading depressions after magnesium treatment in the rat. Neuroreport 1998, 9: 2179–2182. 10.1097/00001756-199807130-00006
174.
go back to reference Silberstein S, Saper J, Berenson F, Somogyi M, McCague K, D’Souza J: Oxcarbazepine in migraine headache: a double-blind, randomized, placebo-controlled study. Neurology 2008, 70: 548–555. 10.1212/01.wnl.0000297551.27191.70 Silberstein S, Saper J, Berenson F, Somogyi M, McCague K, D’Souza J: Oxcarbazepine in migraine headache: a double-blind, randomized, placebo-controlled study. Neurology 2008, 70: 548–555. 10.1212/01.wnl.0000297551.27191.70
175.
go back to reference Durham PL, Garrett FG: Neurological mechanisms of migraine: potential of the gap-junction modulator tonabersat in prevention of migraine. Cephalalgia 2009,29(Suppl 2):1–6.PubMedCentral Durham PL, Garrett FG: Neurological mechanisms of migraine: potential of the gap-junction modulator tonabersat in prevention of migraine. Cephalalgia 2009,29(Suppl 2):1–6.PubMedCentral
176.
go back to reference Silberstein SD, Schoenen J, Göbel H, Diener HC, Elkind AH, Klapper JA, Howard RA: Tonabersat, a gap-junction modulator: efficacy and safety in two randomized, placebo-controlled, dose-ranging studies of acute migraine. Cephalalgia 2009,29(Suppl 2):17–27. Silberstein SD, Schoenen J, Göbel H, Diener HC, Elkind AH, Klapper JA, Howard RA: Tonabersat, a gap-junction modulator: efficacy and safety in two randomized, placebo-controlled, dose-ranging studies of acute migraine. Cephalalgia 2009,29(Suppl 2):17–27.
177.
go back to reference Goadsby PJ, Ferrari MD, Csanyi A, Olesen J, Mills JG: Tonabersat TON-01–05 Study Group. Randomized, double-blind, placebo-controlled, proof-of-concept study of the cortical spreading depression inhibiting agent tonabersat in migraine prophylaxis. Cephalalgia 2009, 29: 742–750. 10.1111/j.1468-2982.2008.01804.x Goadsby PJ, Ferrari MD, Csanyi A, Olesen J, Mills JG: Tonabersat TON-01–05 Study Group. Randomized, double-blind, placebo-controlled, proof-of-concept study of the cortical spreading depression inhibiting agent tonabersat in migraine prophylaxis. Cephalalgia 2009, 29: 742–750. 10.1111/j.1468-2982.2008.01804.x
178.
go back to reference Dahlöf CG, Hauge AW, Olesen J: Efficacy and safety of tonabersat, a gap-junction modulator, in the acute treatment of migraine: a double-blind, parallel-group, randomized study. Cephalalgia 2009,29(Suppl 2):7–16. Dahlöf CG, Hauge AW, Olesen J: Efficacy and safety of tonabersat, a gap-junction modulator, in the acute treatment of migraine: a double-blind, parallel-group, randomized study. Cephalalgia 2009,29(Suppl 2):7–16.
179.
go back to reference Hauge AW, Asghar MS, Schytz HW, Christensen K, Olesen J: Effects of tonabersat on migraine with aura: a randomised, double-blind, placebo-controlled crossover study. Lancet Neurol 2009, 8: 718–723. 10.1016/S1474-4422(09)70135-8 Hauge AW, Asghar MS, Schytz HW, Christensen K, Olesen J: Effects of tonabersat on migraine with aura: a randomised, double-blind, placebo-controlled crossover study. Lancet Neurol 2009, 8: 718–723. 10.1016/S1474-4422(09)70135-8
180.
go back to reference Bradley DP, Smith MI, Netsiri C, Smith JM, Bockhorst KH, Hall LD, Huang CL, Leslie RA, Parsons AA, James MF: Diffusion-Weighted MRI Used to Detect in Vivo Modulation of Cortical Spreading Depression: Comparison of Sumatriptan and Tonabersat. Exp Neurol 2001, 172: 342–353. 10.1006/exnr.2001.7809 Bradley DP, Smith MI, Netsiri C, Smith JM, Bockhorst KH, Hall LD, Huang CL, Leslie RA, Parsons AA, James MF: Diffusion-Weighted MRI Used to Detect in Vivo Modulation of Cortical Spreading Depression: Comparison of Sumatriptan and Tonabersat. Exp Neurol 2001, 172: 342–353. 10.1006/exnr.2001.7809
181.
go back to reference Damodaram S, Thalakoti S, Freeman SE, Garrett FG, Durham PL: Tonabersat inhibits trigeminal ganglion neuronal-satellite glial cell signaling. Headache 2009, 49: 5–20. 10.1111/j.1526-4610.2008.01262.xPubMedCentral Damodaram S, Thalakoti S, Freeman SE, Garrett FG, Durham PL: Tonabersat inhibits trigeminal ganglion neuronal-satellite glial cell signaling. Headache 2009, 49: 5–20. 10.1111/j.1526-4610.2008.01262.xPubMedCentral
182.
go back to reference Holland PR, Akerman S, Andreou AP, Karsan N, Wemmie JA, Goadsby PJ: Acid-sensing ion channel 1: a novel therapeutic target for migraine with aura. Ann Neurol 2012, 72: 559–563. 10.1002/ana.23653 Holland PR, Akerman S, Andreou AP, Karsan N, Wemmie JA, Goadsby PJ: Acid-sensing ion channel 1: a novel therapeutic target for migraine with aura. Ann Neurol 2012, 72: 559–563. 10.1002/ana.23653
183.
go back to reference Durham PL, Masterson CG: Two mechanisms involved in trigeminal CGRP release: implications for migraine treatment. Headache 2013, 53: 67–80. 10.1111/j.1526-4610.2012.02262.xPubMedCentral Durham PL, Masterson CG: Two mechanisms involved in trigeminal CGRP release: implications for migraine treatment. Headache 2013, 53: 67–80. 10.1111/j.1526-4610.2012.02262.xPubMedCentral
184.
go back to reference Yan J, Edelmayer RM, Wei X, De Felice M, Porreca F, Dussor G: Dural afferents express acid-sensing ion channels: A role for decreased meningeal pH in migraine headache. Pain 2011, 152: 106–113. 10.1016/j.pain.2010.09.036PubMedCentral Yan J, Edelmayer RM, Wei X, De Felice M, Porreca F, Dussor G: Dural afferents express acid-sensing ion channels: A role for decreased meningeal pH in migraine headache. Pain 2011, 152: 106–113. 10.1016/j.pain.2010.09.036PubMedCentral
185.
go back to reference Raddant AC, Russo AF: Calcitonin gene-related peptide in migraine: intersection of peripheral inflammation and central modulation. Expert Rev Mol Med 2011, 13: e36.PubMedCentral Raddant AC, Russo AF: Calcitonin gene-related peptide in migraine: intersection of peripheral inflammation and central modulation. Expert Rev Mol Med 2011, 13: e36.PubMedCentral
186.
go back to reference Seybold VS: The role of peptides in central sensitization. Handb Exp Pharmacol 2009, 194: 451–491. 10.1007/978-3-540-79090-7_13 Seybold VS: The role of peptides in central sensitization. Handb Exp Pharmacol 2009, 194: 451–491. 10.1007/978-3-540-79090-7_13
187.
go back to reference Wahl M, Schilling L, Parsons AA, Kaumann A: Involvement of calcitonin gene-related peptide (CGRP) and nitric oxide (NO) in the pial artery dilatation elicited by cortical spreading depression. Brain Res 1994, 637: 2004–2010. Wahl M, Schilling L, Parsons AA, Kaumann A: Involvement of calcitonin gene-related peptide (CGRP) and nitric oxide (NO) in the pial artery dilatation elicited by cortical spreading depression. Brain Res 1994, 637: 2004–2010.
188.
go back to reference Colonna DM, Meng W, Deal DD, Busija DW: Calcitonin gene-related peptide promotes cerebrovascular dilation during cortical spreading depression in rabbits. Am J Physiol 1994, 266: H1095-H1102. Colonna DM, Meng W, Deal DD, Busija DW: Calcitonin gene-related peptide promotes cerebrovascular dilation during cortical spreading depression in rabbits. Am J Physiol 1994, 266: H1095-H1102.
189.
go back to reference De Corato A, Lisi L, Capuano A, Tringali G, Tramutola A, Navarra P, Dello Russo C: Trigeminal satellite cells express functional calcitonin gene-related peptide receptors, whose activation enhances interleukin-1β pro-inflammatory effects. J Neuroimmunol 2011, 237: 39–46. 10.1016/j.jneuroim.2011.05.013 De Corato A, Lisi L, Capuano A, Tringali G, Tramutola A, Navarra P, Dello Russo C: Trigeminal satellite cells express functional calcitonin gene-related peptide receptors, whose activation enhances interleukin-1β pro-inflammatory effects. J Neuroimmunol 2011, 237: 39–46. 10.1016/j.jneuroim.2011.05.013
190.
go back to reference Piper RD P, Edvinsson L, Ekman R, Lambert GA: Cortical spreading depression does not result in the release of calcitonin gene-related peptide into the external jugular vein of the cat: relevance to human migraine. Cephalalgia 1993, 13: 180–183. 10.1046/j.1468-2982.1993.1303180.x Piper RD P, Edvinsson L, Ekman R, Lambert GA: Cortical spreading depression does not result in the release of calcitonin gene-related peptide into the external jugular vein of the cat: relevance to human migraine. Cephalalgia 1993, 13: 180–183. 10.1046/j.1468-2982.1993.1303180.x
191.
go back to reference Hansen JM, Hauge AW, Olesen J, Ashina M: Calcitonin gene-related peptide triggers migraine-like attacks in patients with migraine with aura. Cephalalgia 2010, 30: 1179–1186. 10.1177/0333102410368444 Hansen JM, Hauge AW, Olesen J, Ashina M: Calcitonin gene-related peptide triggers migraine-like attacks in patients with migraine with aura. Cephalalgia 2010, 30: 1179–1186. 10.1177/0333102410368444
192.
go back to reference Negro A, Lionetto L, Simmaco M, Martelletti P: CGRP receptor antagonists: an expanding drug class for acute migraine? Expert Opin Investig Drugs 2012, 21: 807–818. 10.1517/13543784.2012.681044 Negro A, Lionetto L, Simmaco M, Martelletti P: CGRP receptor antagonists: an expanding drug class for acute migraine? Expert Opin Investig Drugs 2012, 21: 807–818. 10.1517/13543784.2012.681044
193.
go back to reference Hoffmann J, Goadsby PJ: New Agents for Acute Treatment of Migraine: CGRP Receptor Antagonists, iNOS Inhibitors. Curr Treat Options Neurol 2012, 14: 50–59. 10.1007/s11940-011-0155-4 Hoffmann J, Goadsby PJ: New Agents for Acute Treatment of Migraine: CGRP Receptor Antagonists, iNOS Inhibitors. Curr Treat Options Neurol 2012, 14: 50–59. 10.1007/s11940-011-0155-4
194.
go back to reference Diener HC, Barbanti P, Dahlöf C, Reuter U, Habeck J, Podhorna J: BI 44370 TA, an oral CGRP antagonist for the treatment of acute migraine attacks: results from a phase II study. Cephalalgia 2011, 31: 573–584. 10.1177/0333102410388435 Diener HC, Barbanti P, Dahlöf C, Reuter U, Habeck J, Podhorna J: BI 44370 TA, an oral CGRP antagonist for the treatment of acute migraine attacks: results from a phase II study. Cephalalgia 2011, 31: 573–584. 10.1177/0333102410388435
195.
go back to reference Chauvel V, Vamos E, Pardutz A, Vecsei L, Schoenen J, Multon S: Effect of systemic kynurenine on cortical spreading depression and its modulation by sex hormones in rat. Exp Neurol 2012, 236: 207–214. 10.1016/j.expneurol.2012.05.002 Chauvel V, Vamos E, Pardutz A, Vecsei L, Schoenen J, Multon S: Effect of systemic kynurenine on cortical spreading depression and its modulation by sex hormones in rat. Exp Neurol 2012, 236: 207–214. 10.1016/j.expneurol.2012.05.002
196.
go back to reference Hirota K, Sikand KS, Lambert DG: Interaction of ketamine with mu2 opioid receptors in SH-SY5Y human neuroblastoma cells. J Anesth 1999, 13: 107–109. 10.1007/s005400050035 Hirota K, Sikand KS, Lambert DG: Interaction of ketamine with mu2 opioid receptors in SH-SY5Y human neuroblastoma cells. J Anesth 1999, 13: 107–109. 10.1007/s005400050035
197.
go back to reference Narita M, Yoshizawa K, Aoki K, Takagi M, Miyatake M, Suzuki T: A putative sigma1 receptor antagonist NE-100 attenuates the discriminative stimulus effects of ketamine in rats. Addict Biol 2001, 6: 373–376. 10.1080/13556210020077091 Narita M, Yoshizawa K, Aoki K, Takagi M, Miyatake M, Suzuki T: A putative sigma1 receptor antagonist NE-100 attenuates the discriminative stimulus effects of ketamine in rats. Addict Biol 2001, 6: 373–376. 10.1080/13556210020077091
198.
go back to reference Gorelova NA, Koroleva VI, Amemori T, Pavlík V, Burĕs J: Ketamine blockade of cortical spreading depression in rats. Electroencephalogr Clin Neurophysiol 1987, 66: 440–447. 10.1016/0013-4694(87)90213-6 Gorelova NA, Koroleva VI, Amemori T, Pavlík V, Burĕs J: Ketamine blockade of cortical spreading depression in rats. Electroencephalogr Clin Neurophysiol 1987, 66: 440–447. 10.1016/0013-4694(87)90213-6
199.
go back to reference Rashidy-Pour A, Motaghed-Larijani Z, Bures J: Tolerance to ketamine-induced blockade of cortical spreading depression transfers to MK-801 but not to AP5 in rats. Brain Res 1995, 693: 64–69. 10.1016/0006-8993(95)00692-J Rashidy-Pour A, Motaghed-Larijani Z, Bures J: Tolerance to ketamine-induced blockade of cortical spreading depression transfers to MK-801 but not to AP5 in rats. Brain Res 1995, 693: 64–69. 10.1016/0006-8993(95)00692-J
200.
go back to reference Kaube H, Herzog J, Käufer T, Dichgans M, Diener HC: Aura in some patients with familial hemiplegic migraine can be stopped by intranasal ketamine. Neurology 2000, 55: 139–141. 10.1212/WNL.55.1.139 Kaube H, Herzog J, Käufer T, Dichgans M, Diener HC: Aura in some patients with familial hemiplegic migraine can be stopped by intranasal ketamine. Neurology 2000, 55: 139–141. 10.1212/WNL.55.1.139
201.
go back to reference Afridi SK, Giffin NJ, Kaube H, Goadsby PJ: A randomized controlled trial of intranasal ketamine in migraine with prolonged aura. Neurology 2013, 80: 642–647. 10.1212/WNL.0b013e3182824e66 Afridi SK, Giffin NJ, Kaube H, Goadsby PJ: A randomized controlled trial of intranasal ketamine in migraine with prolonged aura. Neurology 2013, 80: 642–647. 10.1212/WNL.0b013e3182824e66
202.
go back to reference Dhir A, Lossin C, Rogawski MA: Propofol hemisuccinate suppresses cortical spreading depression. Neurosci Lett 2012, 514: 67–70. 10.1016/j.neulet.2012.02.058 Dhir A, Lossin C, Rogawski MA: Propofol hemisuccinate suppresses cortical spreading depression. Neurosci Lett 2012, 514: 67–70. 10.1016/j.neulet.2012.02.058
203.
go back to reference Kudo C, Toyama M, Boku A, Hanamoto H, Morimoto Y, Sugimura M, Niwa H: Anesthetic effects on susceptibility to cortical spreading depression. Neuropharmacol 2013, 67: 32–36. Kudo C, Toyama M, Boku A, Hanamoto H, Morimoto Y, Sugimura M, Niwa H: Anesthetic effects on susceptibility to cortical spreading depression. Neuropharmacol 2013, 67: 32–36.
204.
go back to reference Kudo C, Nozari A, Moskowitz MA, Ayata C: The impact of anesthetics and hyperoxia on cortical spreading depression. Exp Neurol 2008, 212: 201–206. 10.1016/j.expneurol.2008.03.026PubMedCentral Kudo C, Nozari A, Moskowitz MA, Ayata C: The impact of anesthetics and hyperoxia on cortical spreading depression. Exp Neurol 2008, 212: 201–206. 10.1016/j.expneurol.2008.03.026PubMedCentral
205.
go back to reference Summ O, Holland PR, Akerman S, Goadsby PJ: TRPV1 receptor blockade is ineffective in different in vivo models of migraine. Cephalalgia 2011, 31: 172–180. 10.1177/0333102410375626 Summ O, Holland PR, Akerman S, Goadsby PJ: TRPV1 receptor blockade is ineffective in different in vivo models of migraine. Cephalalgia 2011, 31: 172–180. 10.1177/0333102410375626
206.
go back to reference Kazemi H, Rahgozar M, Speckmann EJ, Gorji A: Effect of cannabinoid receptor activation on spreading depression. Iran J Basic Med Sci 2012, 15: 926–936.PubMedCentral Kazemi H, Rahgozar M, Speckmann EJ, Gorji A: Effect of cannabinoid receptor activation on spreading depression. Iran J Basic Med Sci 2012, 15: 926–936.PubMedCentral
Metadata
Title
Cortical spreading depression as a target for anti-migraine agents
Publication date
01-12-2013
Published in
The Journal of Headache and Pain / Issue 1/2013
Print ISSN: 1129-2369
Electronic ISSN: 1129-2377
DOI
https://doi.org/10.1186/1129-2377-14-62

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