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Published in: Current Neurology and Neuroscience Reports 3/2010

01-05-2010

Cortical Spreading Depression and Migraine

Authors: Katharina Eikermann-Haerter, Cenk Ayata

Published in: Current Neurology and Neuroscience Reports | Issue 3/2010

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Abstract

Cortical spreading depression, a slowly propagating wave of transient neuronal and glial depolarization, is widely accepted as the electrophysiologic substrate of migraine aura and a trigger for headache. Recent clinical and experimental evidence reinforces the putative role of cortical spreading depression in migraine pathophysiology. Imaging studies in migraineurs demonstrated hemodynamic changes consistent with cortical spreading depression during aura, whereas recent animal studies helped unravel pathophysiologic aspects such as the triggering mechanisms, genetic and hormonal modulation, and potential therapeutic targets. Here, we provide an overview of recent advances in our understanding of migraine pathophysiology and treatment.
Literature
1.
go back to reference Lauritzen M: Pathophysiology of the migraine aura. The spreading depression theory. Brain 1994, 117(Pt 1):199–210.CrossRefPubMed Lauritzen M: Pathophysiology of the migraine aura. The spreading depression theory. Brain 1994, 117(Pt 1):199–210.CrossRefPubMed
2.
go back to reference Bolay H, Reuter U, Dunn AK, et al.: Intrinsic brain activity triggers trigeminal meningeal afferents in a migraine model. Nat Med 2002, 8(2):136–142.CrossRefPubMed Bolay H, Reuter U, Dunn AK, et al.: Intrinsic brain activity triggers trigeminal meningeal afferents in a migraine model. Nat Med 2002, 8(2):136–142.CrossRefPubMed
3.
go back to reference Moskowitz MA, Nozaki K, Kraig RP: Neocortical spreading depression provokes the expression of c-fos protein-like immunoreactivity within trigeminal nucleus caudalis via trigeminovascular mechanisms. J Neurosci 1993, 13(3):1167–1177.PubMed Moskowitz MA, Nozaki K, Kraig RP: Neocortical spreading depression provokes the expression of c-fos protein-like immunoreactivity within trigeminal nucleus caudalis via trigeminovascular mechanisms. J Neurosci 1993, 13(3):1167–1177.PubMed
4.
go back to reference Nozari A, Dilekoz E, Sukhotinsky I, et al.: Microemboli may link spreading depression migraine aura and patent foramen ovale (p NA). Ann Neurol 2009 (In press). Nozari A, Dilekoz E, Sukhotinsky I, et al.: Microemboli may link spreading depression migraine aura and patent foramen ovale (p NA). Ann Neurol 2009 (In press).
5.
go back to reference Welch KM: Brain hyperexcitability: the basis for antiepileptic drugs in migraine prevention. Headache 2005, 45(Suppl 1):S25–S32.CrossRefPubMed Welch KM: Brain hyperexcitability: the basis for antiepileptic drugs in migraine prevention. Headache 2005, 45(Suppl 1):S25–S32.CrossRefPubMed
6.
go back to reference Haut SR, Bigal ME, Lipton RB: Chronic disorders with episodic manifestations: focus on epilepsy and migraine. Lancet Neurol 2006, 5(2):148–157.CrossRefPubMed Haut SR, Bigal ME, Lipton RB: Chronic disorders with episodic manifestations: focus on epilepsy and migraine. Lancet Neurol 2006, 5(2):148–157.CrossRefPubMed
7.
go back to reference • Eikermann-Haerter K, Dilekoz E, Kudo C, et al.: Genetic and hormonal factors modulate spreading depression and transient hemiparesis in mouse models of familial hemiplegic migraine type 1. J Clin Invest 2009, 119(1):99–109. The authors provide experimental evidence showing enhanced CSD susceptibility and post-CSD neurologic deficits in mutant mice expressing FHM1 mutations, as well as their modulation by gene-dosage and female hormones. • Eikermann-Haerter K, Dilekoz E, Kudo C, et al.: Genetic and hormonal factors modulate spreading depression and transient hemiparesis in mouse models of familial hemiplegic migraine type 1. J Clin Invest 2009, 119(1):99–109. The authors provide experimental evidence showing enhanced CSD susceptibility and post-CSD neurologic deficits in mutant mice expressing FHM1 mutations, as well as their modulation by gene-dosage and female hormones.
8.
go back to reference Ayata C: Spreading depression: from serendipity to targeted therapy in migraine prophylaxis. Cephalalgia 2009, 29(10):1095–1114.CrossRefPubMed Ayata C: Spreading depression: from serendipity to targeted therapy in migraine prophylaxis. Cephalalgia 2009, 29(10):1095–1114.CrossRefPubMed
9.
go back to reference Eikermann-Haerter K, Baum MJ, Ferrari MD, et al.: Androgenic suppression of spreading depression in familial hemiplegic migraine type 1 mutant mice. Ann Neurol 2009, 66(4):564–568.CrossRefPubMed Eikermann-Haerter K, Baum MJ, Ferrari MD, et al.: Androgenic suppression of spreading depression in familial hemiplegic migraine type 1 mutant mice. Ann Neurol 2009, 66(4):564–568.CrossRefPubMed
10.
go back to reference •• Ayata C, Jin H, Kudo C, et al.: Suppression of cortical spreading depression in migraine prophylaxis. Ann Neurol 2006, 59(4):652–661. This was the first demonstration of CSD suppression by chronic treatment with migraine prophylactic drugs as a probable shared mechanism of action. •• Ayata C, Jin H, Kudo C, et al.: Suppression of cortical spreading depression in migraine prophylaxis. Ann Neurol 2006, 59(4):652–661. This was the first demonstration of CSD suppression by chronic treatment with migraine prophylactic drugs as a probable shared mechanism of action.
11.
go back to reference Leão AAP: Spreading depression of activity in cerebral cortex. J Neurophysiol 1944, 7:359–390. Leão AAP: Spreading depression of activity in cerebral cortex. J Neurophysiol 1944, 7:359–390.
12.
go back to reference Somjen GG: Mechanisms of spreading depression and hypoxic spreading depression-like depolarization. Physiol Rev 2001, 81(3):1065–1096.PubMed Somjen GG: Mechanisms of spreading depression and hypoxic spreading depression-like depolarization. Physiol Rev 2001, 81(3):1065–1096.PubMed
13.
go back to reference Van Harreveld A: Compounds in brain extracts causing spreading depression of cerebral cortical activity and contraction of crustacean muscle. J Neurochem 1959, 3:300–315.CrossRef Van Harreveld A: Compounds in brain extracts causing spreading depression of cerebral cortical activity and contraction of crustacean muscle. J Neurochem 1959, 3:300–315.CrossRef
14.
go back to reference James MF, Smith MI, Bockhorst KH, et al.: Cortical spreading depression in the gyrencephalic feline brain studied by magnetic resonance imaging. J Physiol 1999, 519(Pt 2):415–425.CrossRefPubMed James MF, Smith MI, Bockhorst KH, et al.: Cortical spreading depression in the gyrencephalic feline brain studied by magnetic resonance imaging. J Physiol 1999, 519(Pt 2):415–425.CrossRefPubMed
15.
go back to reference Hartings J, Strong AJ, Fabricius M, et al.: Spreading depolarizations and late secondary insults after traumatic brain injury. J Neurotrauma 2009, 26(11):1857–1866.CrossRefPubMed Hartings J, Strong AJ, Fabricius M, et al.: Spreading depolarizations and late secondary insults after traumatic brain injury. J Neurotrauma 2009, 26(11):1857–1866.CrossRefPubMed
16.
go back to reference Dohmen C, Sakowitz OW, Fabricius M, et al.: Spreading depolarizations occur in human ischemic stroke with high incidence. Ann Neurol 2008, 63(6):720–728.CrossRefPubMed Dohmen C, Sakowitz OW, Fabricius M, et al.: Spreading depolarizations occur in human ischemic stroke with high incidence. Ann Neurol 2008, 63(6):720–728.CrossRefPubMed
17.
go back to reference • Dreier JP, Woitzik J, Fabricius M, et al.: Delayed ischaemic neurological deficits after subarachnoid haemorrhage are associated with clusters of spreading depolarizations. Brain 2006, 129(Pt 12):3224–3237. This prospective multicenter study demonstrated that ischemic depolarizations occur after subarachnoid hemorrhage and ischemic stroke in humans and may be an early indicator of delayed ischemic brain damage. • Dreier JP, Woitzik J, Fabricius M, et al.: Delayed ischaemic neurological deficits after subarachnoid haemorrhage are associated with clusters of spreading depolarizations. Brain 2006, 129(Pt 12):3224–3237. This prospective multicenter study demonstrated that ischemic depolarizations occur after subarachnoid hemorrhage and ischemic stroke in humans and may be an early indicator of delayed ischemic brain damage.
18.
go back to reference Gorelova NA, Koroleva VI, Amemori T, et al.: Ketamine blockade of cortical spreading depression in rats. Electroencephalogr Clin Neurophysiol 1987, 66(4):440–447.CrossRefPubMed Gorelova NA, Koroleva VI, Amemori T, et al.: Ketamine blockade of cortical spreading depression in rats. Electroencephalogr Clin Neurophysiol 1987, 66(4):440–447.CrossRefPubMed
19.
go back to reference Gorji A, Scheller D, Straub H, et al.: Spreading depression in human neocortical slices. Brain Res 2001, 906(1–2):74–83.CrossRefPubMed Gorji A, Scheller D, Straub H, et al.: Spreading depression in human neocortical slices. Brain Res 2001, 906(1–2):74–83.CrossRefPubMed
20.
go back to reference Piilgaard H, Lauritzen M: Persistent increase in oxygen consumption and impaired neurovascular coupling after spreading depression in rat neocortex. J Cereb Blood Flow Metab 2009, 29(9):1517–1527.CrossRefPubMed Piilgaard H, Lauritzen M: Persistent increase in oxygen consumption and impaired neurovascular coupling after spreading depression in rat neocortex. J Cereb Blood Flow Metab 2009, 29(9):1517–1527.CrossRefPubMed
21.
go back to reference Takano T, Tian GF, Peng W, et al.: Cortical spreading depression causes and coincides with tissue hypoxia. Nat Neurosci 2007, 10(6):754–762.CrossRefPubMed Takano T, Tian GF, Peng W, et al.: Cortical spreading depression causes and coincides with tissue hypoxia. Nat Neurosci 2007, 10(6):754–762.CrossRefPubMed
22.
go back to reference Kunkler PE, Kraig RP: Calcium waves precede electrophysiological changes of spreading depression in hippocampal organ cultures. J Neurosci 1998, 18(9):3416–3425.PubMed Kunkler PE, Kraig RP: Calcium waves precede electrophysiological changes of spreading depression in hippocampal organ cultures. J Neurosci 1998, 18(9):3416–3425.PubMed
23.
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(1–2):69–77.CrossRefPubMed 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(1–2):69–77.CrossRefPubMed
24.
go back to reference Bures J, Buresova O, Krivanek J: The mechanism and applications of Leao’s spreading depression of electroencephalographic activity. New York: Academic Press; 1974. Bures J, Buresova O, Krivanek J: The mechanism and applications of Leao’s spreading depression of electroencephalographic activity. New York: Academic Press; 1974.
25.
go back to reference Kruger H, Heinemann U, Luhmann HJ: Effects of ionotropic glutamate receptor blockade and 5-HT1A receptor activation on spreading depression in rat neocortical slices. Neuroreport 1999, 10(12):2651–2656.PubMedCrossRef Kruger H, Heinemann U, Luhmann HJ: Effects of ionotropic glutamate receptor blockade and 5-HT1A receptor activation on spreading depression in rat neocortical slices. Neuroreport 1999, 10(12):2651–2656.PubMedCrossRef
26.
go back to reference Avoli M, Drapeau C, Louvel J, et al.: Epileptiform activity induced by low extracellular magnesium in the human cortex maintained in vitro. Ann Neurol 1991, 30(4):589–596.CrossRefPubMed Avoli M, Drapeau C, Louvel J, et al.: Epileptiform activity induced by low extracellular magnesium in the human cortex maintained in vitro. Ann Neurol 1991, 30(4):589–596.CrossRefPubMed
27.
go back to reference Sramka M, Brozek G, Bures J, Nadvornik P: Functional ablation by spreading depression: possible use in human stereotactic neurosurgery. Appl Neurophysiol 1977, 40(1):48–61.PubMed Sramka M, Brozek G, Bures J, Nadvornik P: Functional ablation by spreading depression: possible use in human stereotactic neurosurgery. Appl Neurophysiol 1977, 40(1):48–61.PubMed
28.
go back to reference Hadjikhani N, Sanchez Del Rio M, Wu O, et al.: Mechanisms of migraine aura revealed by functional MRI in human visual cortex. Proc Natl Acad Sci U S A 2001, 98(8):4687–4692.CrossRefPubMed Hadjikhani N, Sanchez Del Rio M, Wu O, et al.: Mechanisms of migraine aura revealed by functional MRI in human visual cortex. Proc Natl Acad Sci U S A 2001, 98(8):4687–4692.CrossRefPubMed
29.
go back to reference Mayevsky A, Doron A, Manor T, et al.: Cortical spreading depression recorded from the human brain using a multiparametric monitoring system. Brain Res 1996, 740(1–2):268–274.CrossRefPubMed Mayevsky A, Doron A, Manor T, et al.: Cortical spreading depression recorded from the human brain using a multiparametric monitoring system. Brain Res 1996, 740(1–2):268–274.CrossRefPubMed
30.
go back to reference Strong AJ: Detecting and characterizing spreading depression in the injured human brain. J Cereb Blood Flow Metab 2003, 23(1):748. Strong AJ: Detecting and characterizing spreading depression in the injured human brain. J Cereb Blood Flow Metab 2003, 23(1):748.
31.
go back to reference Strong AJ, Fabricius M, Boutelle MG, et al.: Spreading and synchronous depressions of cortical activity in acutely injured human brain. Stroke 2002, 33(12):2738–2743.CrossRefPubMed Strong AJ, Fabricius M, Boutelle MG, et al.: Spreading and synchronous depressions of cortical activity in acutely injured human brain. Stroke 2002, 33(12):2738–2743.CrossRefPubMed
32.
go back to reference Fabricius M, Fuhr S, Bhatia R, et al.: Cortical spreading depression and peri-infarct depolarization in acutely injured human cerebral cortex. Brain 2006, 129(Pt 3):778–790.CrossRefPubMed Fabricius M, Fuhr S, Bhatia R, et al.: Cortical spreading depression and peri-infarct depolarization in acutely injured human cerebral cortex. Brain 2006, 129(Pt 3):778–790.CrossRefPubMed
33.
go back to reference Leão AAP, Morison RS: Propagation of spreading cortical depression. J Neurophysiol 1945, 8:33–45. Leão AAP, Morison RS: Propagation of spreading cortical depression. J Neurophysiol 1945, 8:33–45.
34.
go back to reference Milner PM: Note on a possible correspondence between the scotomas of migraine and spreading depression of Leao. Electroencephalogr Clin Neurophysiol Suppl 1958, 10(4):705.CrossRef Milner PM: Note on a possible correspondence between the scotomas of migraine and spreading depression of Leao. Electroencephalogr Clin Neurophysiol Suppl 1958, 10(4):705.CrossRef
35.
go back to reference Lashley K: Patterns of cerebral integration indicated by the scotomas of migraine. Arch Neurol Psychiat 1941, 46:331–339. Lashley K: Patterns of cerebral integration indicated by the scotomas of migraine. Arch Neurol Psychiat 1941, 46:331–339.
36.
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(4):344–352.CrossRefPubMed Olesen J, Larsen B, Lauritzen M: Focal hyperemia followed by spreading oligemia and impaired activation of rCBF in classic migraine. Ann Neurol 1981, 9(4):344–352.CrossRefPubMed
37.
go back to reference Lauritzen M, Skyhoj Olsen T, Lassen NA, Paulson OB: Changes in regional cerebral blood flow during the course of classic migraine attacks. Ann Neurol 1983, 13(6):633–641.CrossRefPubMed Lauritzen M, Skyhoj Olsen T, Lassen NA, Paulson OB: Changes in regional cerebral blood flow during the course of classic migraine attacks. Ann Neurol 1983, 13(6):633–641.CrossRefPubMed
38.
go back to reference Woods RP, Iacoboni M, Mazziotta JC: Brief report: bilateral spreading cerebral hypoperfusion during spontaneous migraine headache. N Engl J Med 1994, 331(25):1689–1692.CrossRefPubMed Woods RP, Iacoboni M, Mazziotta JC: Brief report: bilateral spreading cerebral hypoperfusion during spontaneous migraine headache. N Engl J Med 1994, 331(25):1689–1692.CrossRefPubMed
39.
go back to reference Bowyer SM, Aurora KS, Moran JE, et al.: Magnetoencephalographic fields from patients with spontaneous and induced migraine aura. Ann Neurol 2001, 50(5):582–587.CrossRefPubMed Bowyer SM, Aurora KS, Moran JE, et al.: Magnetoencephalographic fields from patients with spontaneous and induced migraine aura. Ann Neurol 2001, 50(5):582–587.CrossRefPubMed
40.
go back to reference D’Esposito M, Deouell LY, Gazzaley A: Alterations in the BOLD fMRI signal with ageing and disease: a challenge for neuroimaging. Nat Rev Neurosci 2003, 4(11):863–872.CrossRefPubMed D’Esposito M, Deouell LY, Gazzaley A: Alterations in the BOLD fMRI signal with ageing and disease: a challenge for neuroimaging. Nat Rev Neurosci 2003, 4(11):863–872.CrossRefPubMed
41.
go back to reference Kim YR, van Meer MP, Mandeville JB, et al.: fMRI of delayed albumin treatment during stroke recovery in rats: implication for fast neuronal habituation in recovering brains. J Cereb Blood Flow Metab 2007, 27(1):142–153.CrossRefPubMed Kim YR, van Meer MP, Mandeville JB, et al.: fMRI of delayed albumin treatment during stroke recovery in rats: implication for fast neuronal habituation in recovering brains. J Cereb Blood Flow Metab 2007, 27(1):142–153.CrossRefPubMed
42.
go back to reference Aurora SK, Barrodale P, Chronicle EP, Mulleners WM: Cortical inhibition is reduced in chronic and episodic migraine and demonstrates a spectrum of illness. Headache 2005, 45(5):546–552.CrossRefPubMed Aurora SK, Barrodale P, Chronicle EP, Mulleners WM: Cortical inhibition is reduced in chronic and episodic migraine and demonstrates a spectrum of illness. Headache 2005, 45(5):546–552.CrossRefPubMed
43.
go back to reference Tottene A, Fellin T, Pagnutti S, et al.: Familial hemiplegic migraine mutations increase Ca(2+) influx through single human CaV2.1 channels and decrease maximal CaV2.1 current density in neurons. Proc Natl Acad Sci U S A 2002, 99(20):13284–13289.CrossRefPubMed Tottene A, Fellin T, Pagnutti S, et al.: Familial hemiplegic migraine mutations increase Ca(2+) influx through single human CaV2.1 channels and decrease maximal CaV2.1 current density in neurons. Proc Natl Acad Sci U S A 2002, 99(20):13284–13289.CrossRefPubMed
44.
go back to reference Ayata C, Shimizu-Sasamata M, Lo EH, et al.: Impaired neurotransmitter release and elevated threshold for cortical spreading depression in mice with mutations in the alpha1A subunit of P/Q type calcium channels. Neuroscience 2000, 95(3):639–645.CrossRefPubMed Ayata C, Shimizu-Sasamata M, Lo EH, et al.: Impaired neurotransmitter release and elevated threshold for cortical spreading depression in mice with mutations in the alpha1A subunit of P/Q type calcium channels. Neuroscience 2000, 95(3):639–645.CrossRefPubMed
45.
go back to reference Caddick SJ, Wang C, Fletcher CF, et al.: Excitatory but not inhibitory synaptic transmission is reduced in lethargic (Cacnb4(lh)) and tottering (Cacna1atg) mouse thalami. J Neurophysiol 1999, 81(5):2066–2074.PubMed Caddick SJ, Wang C, Fletcher CF, et al.: Excitatory but not inhibitory synaptic transmission is reduced in lethargic (Cacnb4(lh)) and tottering (Cacna1atg) mouse thalami. J Neurophysiol 1999, 81(5):2066–2074.PubMed
46.
go back to reference •• Tottene A, Conti R, Fabbro A, et al.: 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. This in vitro study provided strong evidence for enhanced excitatory neurotransmission linked to increased glutamate release in FHM1 mutant mouse brain slices, supporting the notion that migraine is associated with increased cerebral excitability. •• Tottene A, Conti R, Fabbro A, et al.: 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. This in vitro study provided strong evidence for enhanced excitatory neurotransmission linked to increased glutamate release in FHM1 mutant mouse brain slices, supporting the notion that migraine is associated with increased cerebral excitability.
47.
go back to reference Pietrobon D: Function and dysfunction of synaptic calcium channels: insights from mouse models. Curr Opin Neurobiol 2005, 15(3):257–265.CrossRefPubMed Pietrobon D: Function and dysfunction of synaptic calcium channels: insights from mouse models. Curr Opin Neurobiol 2005, 15(3):257–265.CrossRefPubMed
48.
49.
go back to reference Ophoff RA, Terwindt GM, Vergouwe MN, et al.: Familial hemiplegic migraine and episodic ataxia type-2 are caused by mutations in the Ca2+ channel gene CACNL1A4. Cell 1996, 87(3):543–552.CrossRefPubMed Ophoff RA, Terwindt GM, Vergouwe MN, et al.: Familial hemiplegic migraine and episodic ataxia type-2 are caused by mutations in the Ca2+ channel gene CACNL1A4. Cell 1996, 87(3):543–552.CrossRefPubMed
50.
go back to reference Jorgensen PL, Hakansson KO, Karlish SJ: Structure and mechanism of Na,K-ATPase: functional sites and their interactions. Annu Rev Physiol 2003, 65:817–849.CrossRefPubMed Jorgensen PL, Hakansson KO, Karlish SJ: Structure and mechanism of Na,K-ATPase: functional sites and their interactions. Annu Rev Physiol 2003, 65:817–849.CrossRefPubMed
51.
go back to reference D’Ambrosio R, Gordon DS, Winn HR: Differential role of KIR channel and Na(+)/K(+)-pump in the regulation of extracellular K(+) in rat hippocampus. J Neurophysiol 2002, 87(1):87–102.PubMed D’Ambrosio R, Gordon DS, Winn HR: Differential role of KIR channel and Na(+)/K(+)-pump in the regulation of extracellular K(+) in rat hippocampus. J Neurophysiol 2002, 87(1):87–102.PubMed
52.
go back to reference Dichgans M, Freilinger T, Eckstein G, et al.: Mutation in the neuronal voltage-gated sodium channel SCN1A in familial hemiplegic migraine. Lancet 2005, 366(9483):371–377.CrossRefPubMed Dichgans M, Freilinger T, Eckstein G, et al.: Mutation in the neuronal voltage-gated sodium channel SCN1A in familial hemiplegic migraine. Lancet 2005, 366(9483):371–377.CrossRefPubMed
53.
go back to reference Johnston D, Magee JC, Colbert CM, Cristie BR: Active properties of neuronal dendrites. Annu Rev Neurosci 1996, 19:165–186.CrossRefPubMed Johnston D, Magee JC, Colbert CM, Cristie BR: Active properties of neuronal dendrites. Annu Rev Neurosci 1996, 19:165–186.CrossRefPubMed
54.
go back to reference Moskowitz MA, Bolay H, Dalkara T: Deciphering migraine mechanisms: clues from familial hemiplegic migraine genotypes. Ann Neurol 2004, 55(2):276–280.CrossRefPubMed Moskowitz MA, Bolay H, Dalkara T: Deciphering migraine mechanisms: clues from familial hemiplegic migraine genotypes. Ann Neurol 2004, 55(2):276–280.CrossRefPubMed
55.
go back to reference Qian J, Noebels JL: Presynaptic Ca(2+) influx at a mouse central synapse with Ca(2+) channel subunit mutations. J Neurosci 2000, 20(1):163–170.PubMed Qian J, Noebels JL: Presynaptic Ca(2+) influx at a mouse central synapse with Ca(2+) channel subunit mutations. J Neurosci 2000, 20(1):163–170.PubMed
56.
go back to reference Fletcher CF, Lutz CM, O’Sullivan TN, et al.: Absence epilepsy in tottering mutant mice is associated with calcium channel defects. Cell 1996, 87(4):607–617.CrossRefPubMed Fletcher CF, Lutz CM, O’Sullivan TN, et al.: Absence epilepsy in tottering mutant mice is associated with calcium channel defects. Cell 1996, 87(4):607–617.CrossRefPubMed
57.
go back to reference Doyle J, Ren X, Lennon G, Stubbs L: Mutations in the Cacnl1a4 calcium channel gene are associated with seizures, cerebellar degeneration, and ataxia in tottering and leaner mutant mice. Mamm Genome 1997, 8(2):113–120.CrossRefPubMed Doyle J, Ren X, Lennon G, Stubbs L: Mutations in the Cacnl1a4 calcium channel gene are associated with seizures, cerebellar degeneration, and ataxia in tottering and leaner mutant mice. Mamm Genome 1997, 8(2):113–120.CrossRefPubMed
58.
go back to reference Plomp JJ, Vergouwe MN, Van den Maagdenberg AM, et al.: Abnormal transmitter release at neuromuscular junctions of mice carrying the tottering alpha(1A) Ca(2+) channel mutation. Brain 2000, 123(Pt 3):463–471.CrossRefPubMed Plomp JJ, Vergouwe MN, Van den Maagdenberg AM, et al.: Abnormal transmitter release at neuromuscular junctions of mice carrying the tottering alpha(1A) Ca(2+) channel mutation. Brain 2000, 123(Pt 3):463–471.CrossRefPubMed
59.
go back to reference van den Maagdenberg AM, Pietrobon D, Pizzorusso T, et al.: A Cacna1a knockin migraine mouse model with increased susceptibility to cortical spreading depression. Neuron 2004, 41(5):701–710.CrossRefPubMed van den Maagdenberg AM, Pietrobon D, Pizzorusso T, et al.: A Cacna1a knockin migraine mouse model with increased susceptibility to cortical spreading depression. Neuron 2004, 41(5):701–710.CrossRefPubMed
60.
go back to reference van den Maagdenberg AMP, Kaja T, Terpolilli S, et al.: High CSD susceptibility and migraine-associated symptoms in Cav2.1 S218L mice (n NA). Neuron 2009 (In press). van den Maagdenberg AMP, Kaja T, Terpolilli S, et al.: High CSD susceptibility and migraine-associated symptoms in Cav2.1 S218L mice (n NA). Neuron 2009 (In press).
61.
go back to reference Kors EE, Terwindt GM, Vermeulen FL, et al.: Delayed cerebral edema and fatal coma after minor head trauma: role of the CACNA1A calcium channel subunit gene and relationship with familial hemiplegic migraine. Ann Neurol 2001, 49(6):753–760.CrossRefPubMed Kors EE, Terwindt GM, Vermeulen FL, et al.: Delayed cerebral edema and fatal coma after minor head trauma: role of the CACNA1A calcium channel subunit gene and relationship with familial hemiplegic migraine. Ann Neurol 2001, 49(6):753–760.CrossRefPubMed
62.
go back to reference Stam AH, Luijckx GJ, Poll-The BT, et al.: Early seizures and cerebral oedema after trivial head trauma associated with the CACNA1A S218L mutation. J Neurol Neurosurg Psychiatry 2009, 80(10):1125–1129.CrossRefPubMed Stam AH, Luijckx GJ, Poll-The BT, et al.: Early seizures and cerebral oedema after trivial head trauma associated with the CACNA1A S218L mutation. J Neurol Neurosurg Psychiatry 2009, 80(10):1125–1129.CrossRefPubMed
63.
go back to reference Eriksen MK, Thomsen LL, Olesen J: Implications of clinical subtypes of migraine with aura. Headache 2006, 46(2):286–297.CrossRefPubMed Eriksen MK, Thomsen LL, Olesen J: Implications of clinical subtypes of migraine with aura. Headache 2006, 46(2):286–297.CrossRefPubMed
64.
go back to reference Thomsen LL, Eriksen MK, Roemer SF, et al.: A population-based study of familial hemiplegic migraine suggests revised diagnostic criteria. Brain 2002, 125(Pt 6):1379–1391.CrossRefPubMed Thomsen LL, Eriksen MK, Roemer SF, et al.: A population-based study of familial hemiplegic migraine suggests revised diagnostic criteria. Brain 2002, 125(Pt 6):1379–1391.CrossRefPubMed
65.
go back to reference Smith SS: Female sex steroid hormones: from receptors to networks to performance—actions on the sensorimotor system. Prog Neurobiol 1994, 44(1):55–86.CrossRefPubMed Smith SS: Female sex steroid hormones: from receptors to networks to performance—actions on the sensorimotor system. Prog Neurobiol 1994, 44(1):55–86.CrossRefPubMed
66.
go back to reference Smith MJ, Adams LF, Schmidt PJ, et al.: Effects of ovarian hormones on human cortical excitability. Ann Neurol 2002, 51(5):599–603.CrossRefPubMed Smith MJ, Adams LF, Schmidt PJ, et al.: Effects of ovarian hormones on human cortical excitability. Ann Neurol 2002, 51(5):599–603.CrossRefPubMed
67.
68.
go back to reference Kruit MC, van Buchem MA, Hofman PAM, et al.: Migraine as a risk factor for subclinical brain lesions. JAMA 2004, 291:427–434.CrossRefPubMed Kruit MC, van Buchem MA, Hofman PAM, et al.: Migraine as a risk factor for subclinical brain lesions. JAMA 2004, 291:427–434.CrossRefPubMed
69.
go back to reference Kruit MC, Launer LJ, van Buchem MA, et al.: MRI findings in migraine. Rev Neurol (Paris) 2005, 161(6–7):661–665. Kruit MC, Launer LJ, van Buchem MA, et al.: MRI findings in migraine. Rev Neurol (Paris) 2005, 161(6–7):661–665.
70.
go back to reference Schwedt TJ, Dodick DW: Patent foramen ovale and migraine—bringing closure to the subject. Headache 2006, 46(4):663–671.CrossRefPubMed Schwedt TJ, Dodick DW: Patent foramen ovale and migraine—bringing closure to the subject. Headache 2006, 46(4):663–671.CrossRefPubMed
71.
go back to reference Post MC, Letteboer TG, Mager JJ, et al.: A pulmonary right-to-left shunt in patients with hereditary hemorrhagic telangiectasia is associated with an increased prevalence of migraine. Chest 2005, 128(4):2485–2489.CrossRefPubMed Post MC, Letteboer TG, Mager JJ, et al.: A pulmonary right-to-left shunt in patients with hereditary hemorrhagic telangiectasia is associated with an increased prevalence of migraine. Chest 2005, 128(4):2485–2489.CrossRefPubMed
72.
go back to reference Spies C, Schrader R: Transcatheter closure of patent foramen ovale in patients with migraine headache. J Interv Cardiol 2006, 19(6):552–557.CrossRefPubMed Spies C, Schrader R: Transcatheter closure of patent foramen ovale in patients with migraine headache. J Interv Cardiol 2006, 19(6):552–557.CrossRefPubMed
73.
go back to reference Azarbal B, Tobis J, Suh W, et al.: Association of interatrial shunts and migraine headaches: impact of transcatheter closure. J Am Coll Cardiol 2005, 45(4):489–492.CrossRefPubMed Azarbal B, Tobis J, Suh W, et al.: Association of interatrial shunts and migraine headaches: impact of transcatheter closure. J Am Coll Cardiol 2005, 45(4):489–492.CrossRefPubMed
74.
75.
go back to reference Kunkler PE, Kraig RP: Hippocampal spreading depression bilaterally activates the caudal trigeminal nucleus in rodents. Hippocampus 2003, 13(7):835–844.CrossRefPubMed Kunkler PE, Kraig RP: Hippocampal spreading depression bilaterally activates the caudal trigeminal nucleus in rodents. Hippocampus 2003, 13(7):835–844.CrossRefPubMed
76.
go back to reference Gursoy-Ozdemir Y, Qiu J, Matsuoka N, et al.: Cortical spreading depression activates and upregulates MMP-9. J Clin Invest 2004, 113(10):1447–1455.PubMed Gursoy-Ozdemir Y, Qiu J, Matsuoka N, et al.: Cortical spreading depression activates and upregulates MMP-9. J Clin Invest 2004, 113(10):1447–1455.PubMed
Metadata
Title
Cortical Spreading Depression and Migraine
Authors
Katharina Eikermann-Haerter
Cenk Ayata
Publication date
01-05-2010
Publisher
Current Science Inc.
Published in
Current Neurology and Neuroscience Reports / Issue 3/2010
Print ISSN: 1528-4042
Electronic ISSN: 1534-6293
DOI
https://doi.org/10.1007/s11910-010-0099-1

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