Cortical spreading depression and migraine

Current Neurology and Neuroscience Reports

Volumn 10, Issue 3, 2010, Pages 167-173

  Eikermann Haerter, Katharina ^a   Ayata, Cenk ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Aura; Cortical spreading depression (CSD); Familial hemiplegic migraine (FHM); Hormones; Migraine; Trigger

Indexed keywords

BRAIN ELECTROPHYSIOLOGY; DEPOLARIZATION; DISEASE PREDISPOSITION; EXCITABILITY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GENE MUTATION; GLIA; HEADACHE; HEMODYNAMICS; HUMAN; INCIDENCE; MICROEMBOLISM; MIGRAINE; MIGRAINE WITH AURA; NONHUMAN; PATHOPHYSIOLOGY; REVIEW; RISK ASSESSMENT; SPREADING CORTICAL DEPRESSION; STROKE; BIOLOGICAL MODEL; BRAIN CORTEX; GENETICS; NERVE CELL; PATHOLOGY; PHYSIOLOGY;

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ATP1A1 PROTEIN, HUMAN; CACNA1A PROTEIN, HUMAN; CALCIUM CHANNEL; NERVE PROTEIN; SODIUM CHANNEL; SODIUM CHANNEL, VOLTAGE GATED, TYPE I, ALPHA PROTEIN; SODIUM CHANNEL, VOLTAGE-GATED, TYPE I, ALPHA PROTEIN;

CALCIUM CHANNELS; CEREBRAL CORTEX; CORTICAL SPREADING DEPRESSION; DISEASE SUSCEPTIBILITY; HUMANS; MIGRAINE DISORDERS; MODELS, NEUROLOGICAL; NERVE TISSUE PROTEINS; NEURONS; SODIUM CHANNELS; SODIUM-POTASSIUM-EXCHANGING ATPASE;

EID: 77954945261     PISSN: 15284042     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11910-010-0099-1     Document Type: Review

References (76)

1. Lauritzen M: Pathophysiology of the migraine aura. The spreading depression theory. Brain 1994, 117(Pt 1):199-210.
2. 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.
3. 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.
4. 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. Welch KM: Brain hyperexcitability: the basis for antiepileptic drugs in migraine prevention. Headache 2005, 45(Suppl 1):S25-S32.
6. Haut SR, Bigal ME, Lipton RB: Chronic disorders with episodic manifestations: focus on epilepsy and migraine. Lancet Neurol 2006, 5(2):148-157.
7. • 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. Ayata C: Spreading depression: from serendipity to targeted therapy in migraine prophylaxis. Cephalalgia 2009, 29(10):1095-1114.
9. 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.
10. •• 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. Leão AAP: Spreading depression of activity in cerebral cortex. J Neurophysiol 1944, 7:359-390.
12. Somjen GG: Mechanisms of spreading depression and hypoxic spreading depression-like depolarization. Physiol Rev 2001, 81 (3):1065-1096.
13. 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.
14. 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.
15. 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.
16. 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.
17. • 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. Gorelova NA, Koroleva VI, Amemori T, et al.: Ketamine blockade of cortical spreading depression in rats. Electroencephalogr Clin Neurophysiol 1987, 66(4):440-447.
19. Gorji A, Scheller D, Straub H, et al.: Spreading depression in human neocortical slices. Brain Res 2001, 906(1-2):74-83.
20. 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.
21. Takano T, Tian GF, Peng W, et al.: Cortical spreading depression causes and coincides with tissue hypoxia. Nat Neurosci 2007, 10 (6):754-762.
22. Kunkler PE, Kraig RP: Calcium waves precede electrophysiological changes of spreading depression in hippocampal organ cultures. J Neurosci 1998, 18(9):3416-3425.
23. 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.
24. Bures J, Buresova O, Krivanek J: The mechanism and applications of Leao's spreading depression of electroencephalographic activity. New York: Academic Press; 1974.
25. 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.
26. 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.
27. 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.
28. 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.
29. 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.
30. Strong AJ: Detecting and characterizing spreading depression in the injured human brain. J Cereb Blood Flow Metab 2003, 23 (1):748.
31. 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.
32. 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.
33. Leão AAP, Morison RS: Propagation of spreading cortical depression. J Neurophysiol 1945, 8:33-45.
34. 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.
35. Lashley K: Patterns of cerebral integration indicated by the scotomas of migraine. Arch Neurol Psychiat 1941, 46:331-339.
36. 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.
37. 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.
38. 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.
39. 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.
40. 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.
41. 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.
42. 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.
43. 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.
44. 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.
45. 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.
46. •• 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. Pietrobon D: Function and dysfunction of synaptic calcium channels: insights from mouse models. Curr Opin Neurobiol 2005, 15(3):257-265.
48. Pietrobon D, Striessnig J: Neurobiology of migraine. Nat Rev Neurosci 2003, 4(5):386-398.
49. 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.
50. 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.
51. 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.
52. 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.
53. Johnston D, Magee JC, Colbert CM, Cristie BR: Active properties of neuronal dendrites. Annu Rev Neurosci 1996, 19:165-186.
54. Moskowitz MA, Bolay H, Dalkara T: Deciphering migraine mechanisms: clues from familial hemiplegic migraine genotypes. Ann Neurol 2004, 55(2):276-280.
55. 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.
56. 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.
57. 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.
58. 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.
59. 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.
60. 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. 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.
62. 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.
63. Eriksen MK, Thomsen LL, Olesen J: Implications of clinical subtypes of migraine with aura. Headache 2006, 46(2):286-297.
64. 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.
65. Smith SS: Female sex steroid hormones: from receptors to networks to performance-actions on the sensorimotor system. Prog Neurobiol 1994, 44(1):55-86.
66. SmithMJ, Adams LF, Schmidt PJ, et al.: Effects of ovarian hormones on human cortical excitability. Ann Neurol 2002, 51(5):599-603.
67. Bousser MG, Welch KM: Relation between migraine and stroke. Lancet Neurol 2005, 4(9):533-542.
68. KruitMC, van BuchemMA, Hofman PAM, et al.: Migraine as a risk factor for subclinical brain lesions. JAMA 2004, 291:427-434.
69. Kruit MC, Launer LJ, van Buchem MA, et al.: MRI findings in migraine. Rev Neurol (Paris) 2005, 161(6-7):661-665.
70. Schwedt TJ, Dodick DW: Patent foramen ovale and migraine- bringing closure to the subject. Headache 2006, 46(4):663-671.
71. Post MC, Letteboer TG, Mager JJ, et al.: A pulmonary right-toleft shunt in patients with hereditary hemorrhagic telangiectasia is associated with an increased prevalence of migraine. Chest 2005, 128(4):2485-2489.
72. Spies C, Schrader R: Transcatheter closure of patent foramen ovale in patients with migraine headache. J Interv Cardiol 2006, 19(6):552-557.
73. 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.
74. Moskowitz MA: The neurobiology of vascular head pain. Ann Neurol 1984, 16(2):157-168.
75. Kunkler PE, Kraig RP: Hippocampal spreading depression bilaterally activates the caudal trigeminal nucleus in rodents. Hippocampus 2003, 13(7):835-844.
76. 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.