The pathophysiology of migraine. Reflections on the glutamatergic hypothesis;Fisiopatología de la migraña. Reflexiones sobre la hipótesis glutamatérgica

Revista de Neurologia

Volumn 43, Issue 8, 2006, Pages 481-488

  González De La Aleja Tejera, Jesús ^a   Porta Etessam, J ^b   Sepulveda Sanchez J M ^a   Rodriguez Pena Marin M ^a  

^a HOSPITAL UNIVERSITARIO 12 DE OCTUBRE   (Spain)

^b HOSPITAL CENTRAL DE LA CRUZ ROJA   (Spain)

Author keywords

Glutamatergic hypothesis; Memantine; Migraine; Pathophysiology; Pregabalin

Indexed keywords

ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; GLUTAMIC ACID; KAINIC ACID RECEPTOR; MEMANTINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PREGABALIN;

BRAIN CORTEX; DEPRESSION; DISEASE ACTIVITY; EXCITATORY POSTSYNAPTIC POTENTIAL; HUMAN; MELAS SYNDROME; MIGRAINE; NEUROPATHOLOGY; NEUROTRANSMISSION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PATHOPHYSIOLOGY; REVIEW; PHYSIOLOGY; SPREADING CORTICAL DEPRESSION; TRIGEMINAL NERVE; VASCULARIZATION;

GLUTAMIC ACID; HUMANS; MIGRAINE DISORDERS; SPREADING CORTICAL DEPRESSION; TRIGEMINAL NERVE;

EID: 35348813842     PISSN: 02100010     EISSN: None     Source Type: Journal    
DOI: 10.33588/rn.4308.2005657     Document Type: Review

References (106)

1. Headache Classification Subcommittee of the International Headache Society. The international classification of headache disorders. Cephalalgia 2004; 24 (Suppl): S1-152.
2. Wolff HG. Headache and other head pain. 2 ed. New York: Oxford University Press; 1963.
3. Graham JR, Wolff HG. Mechanism of migraine headache and action of ergotamine tartrate. Arch Neurol Psychiatry 1938; 39: 737-63.
4. Martínez F, Castillo J, Noya M. Basic mechanisms of the migraine physiopathology. Rev Neurol 1995; 23: 800-18.
5. SD Silberstein. Migraine pathophysiology and its clinical implications. Cephalalgia. 2004; 24 (Suppl 2): S2-7.
6. Welch KM. Contemporary concepts of migraine pathogenesis. Neurology 2003; 61 (Suppl 4): S2-8.
7. Sánchez-Del Río M, Reuter U. Migraine aura: new information on underlying mechanisms. Curr Opin Neurol 2004; 17: 289-93.
8. Welch KM, D'Andrea G, Tepley N, Barkley G, Ramadan NM. The concept of migraine as a state of central neuronal hyperexcitability. Neurol Clin 1990; 8: 817-28.
9. Silberstein SD. Migraine. Lancet 2004; 31: 381-91.
10. Aurora SK, Welch KM, Al-Sayed F. The threshold for phosphene is lower in migraine. Cephalalgia 2003; 23: 258-63.
11. Aurora SK, Ahmad BK, Welch KM, Bhardhwaj P, Ramadan N. Transcranial magnetic stimulation confirms hyperexcitability of occipital cortex in migraine. Neurology 1998; 50: 1111-4.
12. Young WB, Oshinsky ML, Shechter AL, Gebeline-Myers C, Bradley KC, Wassermann EM. Consecutive transcranial magnetic stimulation: phosphene thresholds in migraineurs and controls. Headache 2004; 44: 131-5.
13. Battelli L, Black KR, Wray SH. Transcranial magnetic stimulation of visual area V5 in migraine. Neurology; 2002; 58: 1066-9.
14. Schoenen J, Ambrosini A, Sandor PS, Maertens de Noordhout A. Evoked potentials and transcranial magnetic stimulation in migraine: published data and viewpoint on their pathophysiologic significance. Clin Neurophysiol 2003; 114: 955-72.
15. Van der Kamp W, Maassen VanDenBrink A, Ferrari MD, Van Dijk JG. Interictal cortical hyperexcitability in migraine patients demonstrated with transcranial magnetic stimulation. J Neurol Sci 1996; 139: 106-10.
16. Ambrosini A, Schoenen J. The electrophysiology of migraine. Curr Opin Neurol 2003; 16: 327-31.
17. Ozturk V, Cakmur R, Donmez B, Yener GG, Kursad F, Idiman F. Comparison of cortical excitability in chronic migraine (transformed migraine) and migraine without aura. A transcranial magnetic stimulation study. J Neurol 2002; 249: 1268-71.
18. Chronicle EP, Wilkins AJ, Coleston DM. Thresholds for detection of a target against a background grating suggest visual dysfunction in migraine with aura but not migraine without aura. Cephalalgia 1995; 15: 117-22.
19. Wray SH, Mijovic-Prelec D, Kosslyn SM. Visual processing in migraineurs. Brain 1995; 118: 25-35.
20. Shepherd AJ. Increased visual after-effects following pattern adaptation in migraine: a lack of intracortical excitation? Brain 2001; 124: 2310-8.
21. McKendrick AM, Badcock DR. Motion processing deficits in migraine. Cephalalgia 2004; 24: 363-72.
22. Afra J, Cecchini AP, De Pasqua V, Albert A, Schoenen J. Visual evoked potentials during long periods of pattern-reversal stimulation in migraine. Brain 1998; 121: 233-41.
23. Ambrosini A, De Pasqua V, Afra J, Sandor PS, Schoenen J. Reduced gating of middle-latency auditory evoked potentials (P50) in migraine patients: another indication of abnormal sensory processing? Neurosci Lett 2001; 22; 306: 132-4.
24. Ozkul Y, Uckardes A. Median nerve somatosensory evoked potentials in migraine. Eur J Neurol 2002; 9: 227-32.
25. Coelho-Miranda L, Playan A, Artuch R, Vilaseca MA, Colomer J, Briones P, et al. Encefalomiopatía mitocondrial, acidosis láctica y accidentes cerebrovasculares (MELAS) en edad pediátrica con la mutación A3243G en el gen del ARNtLeu(UUR) del ADN mitocondrial. Rev Neurol 2000; 31: 804-11.
26. Sacconi S, Salviati L, Gooch C, Bonilla E, Shanske S, DiMauro S. Complex neurologic syndrome associated with the G1606A mutation of mitochondrial DNA. Arch Neurol 2002; 59: 1013-5.
27. Cupini LM, Massa R, Floris R, Manenti G, Martini B, Tessa A, et al. Migraine-like disorder segregating with mtDNA 14484 Leber hereditary optic neuropathy mutation. Neurology 2003; 25; 60: 717-9.
28. Haan J, Terwindt GM, Maassen JA, Hart LM, Frants RR, Ferrari MD. Search for mitochondrial DNA mutations in migraine subgroups. Cephalalgia 1999; 19: 20-2.
29. Barbiroli B, Montagna P, Cortelli P, Funicello R, Iotti S, Monari L, et al. Abnormal brain and muscle energy metabolism shown by 31P magnetic resonance spectroscopy in patients affected by migraine with aura. Neurology 1992; 42: 1209-14.
30. Montagna P, Cortelli P, Monari L, Pierangeli G, Parchi P, Lodi R, et al. 31P-magnetic resonance spectroscopy in migraine without aura. Neurology 1994; 44: 666-9.
31. Schoenen J, Jacquy J, Lenaerts M. Effectiveness of high-dose riboflavin in migraine prophylaxis. A randomized controlled trial. Neurology 1998; 50: 466-70.
32. Welch KM, Ramadan NM. Mitochondria, magnesium and migraine. J Neurol Sci 1995; 134: 9-14.
33. Welch KM. Current opinions in headache pathogenesis: introduction and synthesis. Curr Opin Neurol 1998; 11: 193-7.
34. 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: 345-53.
35. Demirkaya S, Vural O, Dora B, Topcuoglu MA. Efficacy of intravenous magnesium sulfate in the treatment of acute migraine attacks. Headache 2001; 41: 171-7.
36. Cete Y, Dora B, Ertan C, Ozdemir C, Oktay C. A randomized prospective placebo-controlled study of intravenous magnesium sulphate vs. metoclopramide in the management of acute migraine attacks in the Emergency Department. Cephalalgia 2005; 25: 199-204.
37. Pfaffenrath V, Wessely P, Meyer C, Isler HR, Evers S, Grotemeyer KH, et al. Magnesium in the prophylaxis of migraine -a double-blind placebo-controlled study. Cephalalgia 1996; 16: 436-40.
38. Peikert A, Wilimzig C, Kohne-Volland R. Prophylaxis of migraine with oral magnesium: results from a prospective, multi-center, placebo-controlled and double-blind randomized study. Cephalalgia 1996; 16: 257-63.
39. Boska MD, Welch KM, Barker PB, Nelson JA, Schultz L. Contrasts in cortical magnesium, phospholipid and energy metabolism between migraine syndromes. Neurology 2002; 58: 1227-33.
40. Ptacek LJ. The place of migraine as a channelopathy. Curr Opin Neurol 1998; 11: 217-26.
41. Gardner K, Hoffman EP. Current status of genetic discoveries in migraine: familial hemiplegic migraine and beyond. Curr Opin Neurol 1998; 11: 211-6.
42. Tottene A, Fellin T, Pagnutti S, Luvisetto S, Striessnig J, Fletcher C, 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: 13284-9.
43. Turner TJ, Adams ME, Dunlap K. Calcium channels coupled to glutamate release identified by omega-Aga-IVA. Science 1992; 258: 310-3.
44. Van den Maagdenberg AM, Pietrobon D, Pizzorusso T, Kaja S, Broos LA, Cesetti T, et al. A CACNA1A knockin migraine mouse model with increased susceptibility to cortical spreading depression. Neuron 2004; 41: 701-10.
45. 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 alpha1A subunit of P/Q type calcium channels. Neuroscience 2000; 95: 639-45.
46. De Fusco M, Marconi R, Silvestri L, Atorino L, Rampoldi L, Morgante L, et al. Haploinsufficiency of ATP1A2 encoding the Na+/K+ pump alpha2 subunit associated with familial hemiplegic migraine type 2. Nat Genet 2003; 33: 192-6.
47. Lashley KS. Patterns of cerebral integration indicated by scotomas of migraine. Arch Neurol Psychiatry 1941; 46: 331-9.
48. Leao AA. Spreading depression of activity in the cerebral cortex. J Neurophysiol 1944; 7: 359-90.
49. Milner PM. Note on a possible correspondence between the scotomas of migraine and spreading depression of Leao. Electroencephalogr Clin Neurophysiol Suppl 1958; 10: 705.
50. Lauritzen M. Pathophysiology of the migraine aura. The spreading depression theory. Brain 1994; 117: 199-210.
51. Lian XY, Stringer JL. Astrocytes contribute to regulation of extracellular calcium and potassium in the rat cerebral cortex during spreading depression. Brain Res 2004; 1012: 177-84.
52. Hadjikhani N, Sánchez-Del Rio M, Wu O, Schwartz D, Bakker D, Fischl B, et al. Mechanisms of migraine aura revealed by functional MRI in human visual cortex. Proc Natl Acad Sci U S A 2001; 98: 4687-92.
53. Sánchez-Del Río M, Álvarez-Linera J. Functional neuroimaging of headaches. Lancet Neurol 2004; 3: 645-51.
54. Cutrer FM, Sorensen AG, Weisskoff RM, Sánchez-Del Río M, Lee EJ. Perfusion-weighted imaging defects during spontaneous migrainous aura. Ann Neurol 1998; 43: 25-31.
55. Bowyer SM, Aurora KS, Moran JE, Tepley N, Welch KM. Magnetoencephalographic fields from patients with spontaneous and induced migraine aura. Ann Neurol 2001; 50: 582-7.
56. Read SJ, Smith MI, Hunter AJ, Parsons AA. The dynamics of nitric oxide release measured directly and in real time following repeated waves of cortical spreading depression in the anaesthetised cat. Neurosci Lett 1997; 232: 127-30.
57. Obrenovitch TP, Urenjak J, Wang M. Nitric oxide formation during cortical spreading depression is critical for rapid subsequent recovery of ionic homeostasis. J Cereb Blood Flow Metab 2002; 22: 680-8.
58. Wang M, Obrenovitch TP, Urenjak J. Effects of the nitric oxide donor, DEA/NO on cortical spreading depression. Neuropharmacology 2003; 44: 949-57.
59. Strecker T, Dux M, Messlinger K. Nitric oxide releases calcitoningene-related peptide from rat dura mater encephali promoting increases in meningeal blood flow. J Vasc Res 2002; 39: 489-96.
60. Goadsby PJ, Edvinsson L, Ekman R. Vasoactive peptide release in the extracerebral circulation of humans during migraine headache. Ann Neurol 1990; 28: 183-7.
61. Sarchielli P, Alberti A, Codini M, Floridi A, Gallai V. Nitric oxide metabolites, prostaglandins and trigeminal vasoactive peptides in internal jugular vein blood during spontaneous migraine attacks. Cephalalgia 2000; 20: 907-18.
62. Bolay H, Reuter U, Dunn AK, Huang Z, Boas DA, Moskowitz MA. Intrinsic brain activity triggers trigeminal meningeal afferents in a migraine model. Nat Med 2002; 8: 136-42.
63. Buzzi MG, Bonamini M, Moskowitz MA. Neurogenic model of migraine. Cephalalgia 1995; 15: 277-80.
64. Kiss C, Shepard PD, Bari F, Schwarcz R. Cortical spreading depression augments kynurenate levels and reduces malonate toxicity in the rat cortex. Brain Res 2004; 1002: 129-35.
65. García-Salman JD. Protección neuronal endógena: un enfoque alternativo. Rev Neurol 2004; 38: 150-5.
66. Wiggins AK, Shen PJ, Gundlach AL. Atrial natriuretic peptide expression is increased in rat cerebral cortex following spreading depression: possible contribution to SD-induced neuroprotection. Neuroscience 2003; 118: 715-26.
67. Shen PJ, Gundlach AL. Prolonged induction of neuronal NOS expression and activity following cortical spreading depression (SD): implications for SD- and NO-mediated neuroprotection. Exp Neurol 1999; 160: 317-32.
68. Kiss C, Shepard PD, Bari F, Schwarcz R. Cortical spreading depression augments kynurenate levels and reduces malonate toxicity in the rat cortex. Brain Res 2004; 1002: 129-35.
69. Yanamoto H, Xue JH, Miyamoto S, Nagata I, Nakano Y, Murao K, et al. Spreading depression induces long-lasting brain protection against infarcted lesion development via BDNF gene-dependent mechanism. Brain Res 2004; 1019: 178-88.
70. Wiggins AK, Shen PJ, Gundlach AL. Delayed, but prolonged increases in astrocytic clusterin (ApoJ) mRNA expression following acute cortical spreading depression in the rat: evidence for a role of clustering in ischemic tolerance. Brain Res Mol Brain Res 2003; 114: 20-30.
71. Choudhuri R, Cui L, Yong C, Bowyer S, Klein RM, Welch KM, et al. Cortical spreading depression and gene regulation: relevance to migraine. Ann Neurol 2002; 51: 499-506.
72. Jander S, Schroeter M, Peters O, Witte OW, Stoll G. Cortical spreading depression induces proinflammatory cytokine gene expression in the rat brain. J Cereb Blood Flow Metab 2001; 21: 218-25.
73. Gursoy-Ozdemir Y, Qiu J, Matsuoka N, Bolay H, Bermpohl D, Jin H, Wang X. Cortical spreading depression activates and upregulates MMP-9. J Clin Invest 2004; 113: 1447-55.
74. Chazot PL, Godukhin OV, McDonald A, Obrenovitch TP. Spreading depression-induced preconditioning in the mouse cortex: differential changes in the protein expression of ionotropic nicotinic acetylcholine and glutamate receptors. J Neurochem 2002; 83: 1235-8.
75. Woods RP, Iacoboni M, Mazziotta JC. Brief report: bilateral spreading cerebral hypoperfusion during spontaneous migraine headache. N Engl J Med 1994; 331: 1689-92.
76. Weiller C, May A, Limmroth V, Juptner M, Kaube H, Schayck RV, et al. Brain stem activation in spontaneous human migraine attacks. Nat Med 1995; 1: 658-60.
77. Bahra A, Matharu MS, Buchel C, Frackowiak RS, Goadsby PJ. Brainstem activation specific to migraine headache. Lancet 2001; 357: 1016-7.
78. Juhasz G, Zsombok T, Modos EA, Olajos S, Jakab B, Nemeth J, et al. NO-induced migraine attack: strong increase in plasma calcitonin gene-related peptide (CGRP) concentration and negative correlation with platelet serotonin release. Pain 2003; 106: 461-70.
79. Dohovics R, Janaky R, Varga V, Hermann A, Saransaari P, Oja SS. Regulation of glutamatergic neurotransmission in the striatum by presynaptic adenylyl cyclase-dependent processes. Neurochem Int 2003; 42: 1-7.
80. Huang CC, Hsu KS, Gean PW. Isoproterenol potentiates synaptic transmission primarily by enhancing presynaptic calcium influx via P-and/or Q-type calcium channels in the rat amygdala. J Neurosci 1996; 16: 1026-33.
81. Lin YW, Min MY, Chiu TH, Yang HW. Enhancement of associative longterm potentiation by activation of beta-adrenergic receptors at CA1 synapses in rat hippocampal slices. Neuropharmacology 2003; 44: 462-72.
82. Croce A, Astier H, Recasens M, Vignes M. Opposite effects of alpha 1-and beta-adrenoceptor stimulation on both glutamate- and gammaaminobutyric acid-mediated spontaneous transmission in cultured rat hippocampal neurons. J Neurosci Res 2003; 71: 516-25.
83. Waugh J, Goa KL. Topiramate: as monotherapy in newly diagnosed epilepsy. CNS Drugs 2003; 17: 985-92.
84. Skradski S, White HS. Topiramate blocks kainate-evoked cobalt influx into cultured neurons. Epilepsia 2000; 41 (Suppl 1): S45-7.
85. Vajda FJ. Valproate and neuroprotection. J Clin Neurosci 2002; 9: 508-14.
86. Loscher W. Valproate: a reappraisal of its pharmacodynamic properties and mechanisms of action. Prog Neurobiol 1999; 58: 31-59.
87. Cunningham MO, Woodhall GL, Thompson SE, Dooley DJ, Jones RS. Dual effects of gabapentin and pregabalin on glutamate release at rat entorhinal synapses in vitro. Eur J Neurosci 2004; 20: 1566-76.
88. McCaslin PP, Yu XZ, Ho IK, Smith TG. Amitriptyline prevents N-methyl-D-aspartate (NMDA)-induced toxicity, does not prevent NMDAinduced elevations of extracellular glutamate, but augments kainate-induced elevations of glutamate. J Neurochem 1992; 59: 401-5.
89. 2+ levels in neuronal culture. Eur J Pharmacol 1992; 219: 53-7.
90. Sills MA, Loo PS. Tricyclic antidepressants and dextromethorphan bind with higher affinity to the phencyclidine receptor in the absence of magnesium and L-glutamate. Mol Pharmacol 1989; 36: 160-5.
91. Cousin MA, Nicholls DG, Pocock JM. Flunarizine inhibits both calcium-dependent and -independent release of glutamate from synaptosomes and cultured neurones. Brain Res 1993; 606: 227-36.
92. Silberstein SD, Peres MF, Hopkins MM, Shechter AL, Young WB, Rozen TD. Olanzapine in the treatment of refractory migraine and chronic daily headache. Headache 2002; 42: 515-8.
93. Tarazi FI, Baldessarini RJ, Kula NS, Zhang K. Long-term effects of olanzapine, risperidone, and quetiapine on ionotropic glutamate receptor types: implications for antipsychotic drug treatment. J Pharmacol Exp Ther 2003; 306: 1145-51.
94. Ninan I, Jardemark KE, Wang RY. Olanzapine and clozapine but not haloperidol reverse subchronic phencyclidine-induced functional hyperactivity of N-methyl-D-aspartate receptors in pyramidal cells of the rat medial prefrontal cortex. Neuropharmacology 2003; 44: 462-72.
95. Smith MJ, Keel JC, Greenberg BD, Adams LF, Schmidt PJ, Rubinow DA, et al. Menstrual cycle effects on cortical excitability. Neurology 1999; 53: 2069-72.
96. Weaver CE Jr, Park-Chung M, Gibbs TT, Farb DH. 17beta-estradiol protects against NMDA-induced excitotoxicity by direct inhibition of NMDA receptors. Brain Res 1997; 761: 338-41.
97. Huang Y, Huang YL, Zhang S, Zhu YC, Yao T. Estradiol acutely attenuates glutamate-induced calcium overload in primarily cultured rat hippocampal neurons through a membrane receptor-dependent mechanism. Brain Res 2004; 1026: 254-60.
98. Xue B, Hay M. 17beta-estradiol inhibits excitatory amino acid-induced activity of neurons of the nucleus tractus solitarius. Brain Res 2003; 976: 41-52.
99. MacGregor EA. Oestrogen and attacks of migraine with and without aura. Lancet Neurol 2004; 3: 354-61.
100. Galiano L, Montiel I, Falip R, Asensio M, Matías-Guiu J. El estrés como factor precipitante de la migraña. Rev Neurol 1995; 23: 830-2.
101. Galiano L, Montiel I, Falip R, Asensio M, Matías-Guiu J. Los factores precipitantes de la migraña. Rev Neurol 1995; 23: 826-9.
102. Jen JC, Wan J, Palos TP, Howard BD, Baloh RW. Mutation in the glutamate transporter EAAT1 causes episodic ataxia, hemiplegia, and seizures. Neurology 2005; 23: 529-34.
103. Martínez F, Castillo J, Rodríguez JR, Leira R, Noya M. Neuroexcitatory amino acid levels in plasma and cerebrospinal fluid during migraine attacks. Cephalalgia 1993; 13: 89-93.
104. Ferrari MD, Odink J, Bos KD, Malessy MJ, Bruyn GW. Neuroexcitatory plasma amino acids are elevated in migraine. Neurology 1990; 40: 1582-6.
105. Parsons CG, Danysz W, Quack G. Memantine is a clinically well tolerated N-methyl-D-aspartate (NMDA) receptor antagonist -a review of preclinical data. Neuropharmacology 1999; 38: 735-67.
106. Fink K, Dooley DJ, Meder WP, Suman-Chauhan N, Duffy S, Clusmann H, et al. Inhibition of neuronal Ca2+ influx by gabapentin and pregabalin in the human neocortex. Neuropharmacology 2002; 42: 229-36.