Migraine: A disorder of brain excitatory-inhibitory balance?

Trends in Neurosciences

Volumn 35, Issue 8, 2012, Pages 507-520

  Vecchia, Dania ^a   Pietrobon, Daniela ^a,b  

^a UNIVERSITY OF PADOVA   (Italy)

^b CNR   (Italy)

Author keywords

Channelopathy.; Excitatory inhibitory balance; Migraine; Spreading depression; Trigeminovascular pain

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE;

BRAIN DYSFUNCTION; CENTRAL NERVOUS SYSTEM SENSITIZATION; DEPRESSION; FAMILIAL HEMIPLEGIC MIGRAINE; FRAMESHIFT MUTATION; GENETICS; HUMAN; LOSS OF FUNCTION MUTATION; MENINGITIS; MIGRAINE; MIGRAINE WITH AURA; MIGRAINE WITHOUT AURA; NONHUMAN; PHOTOPHOBIA; PRIORITY JOURNAL; REVIEW; VASODILATATION;

ANIMALS; BRAIN; HUMANS; MIGRAINE DISORDERS; PAIN; TRIGEMINAL NERVE;

EID: 84864055317     PISSN: 01662236     EISSN: 1878108X     Source Type: Journal    
DOI: 10.1016/j.tins.2012.04.007     Document Type: Review

References (147)

1. Lipton R.B., et al. Classification of primary headaches. Neurology 2004, 63:427-435.
2. Leonardi M., et al. The global burden of migraine: measuring disability in headache disorders with WHO's Classification of Functioning, Disability and Health (ICF). J. Headache Pain 2005, 6:429-440.
3. Stovner L.J., Hagen K. Prevalence, burden, and cost of headache disorders. Curr. Opin. Neurol. 2006, 19:281-285.
4. Olesen J., et al. The economic cost of brain disorders in Europe. Eur. J. Neurol. 2012, 19:155-162.
5. Pietrobon D., Striessnig J. Neurobiology of migraine. Nat. Rev. Neurosci. 2003, 4:386-398.
6. Olesen J., et al. Origin of pain in migraine: evidence for peripheral sensitisation. Lancet Neurol. 2009, 8:679-690.
7. Levy D. Migraine pain and nociceptor activation - where do we stand?. Headache 2010, 50:909-916.
8. Ayata C. Cortical spreading depression triggers migraine attack: pro. Headache 2010, 50:725-730.
9. Charles A. Does cortical spreading depression initiate a migraine attack? Maybe not. Headache 2010, 50:731-733.
10. Charles A., Brennan K. Cortical spreading depression - new insights and persistent questions. Cephalalgia 2009, 29:1115-1124.
11. Somjen G.G. Mechanisms of spreading depression and hypoxic spreading depression-like depolarization. Physiol. Rev. 2001, 81:1065-1096.
12. Giffin N.J., et al. Premonitory symptoms in migraine: an electronic diary study. Neurology 2003, 60:935-940.
13. Hauge A.W., et al. Characterization of consistent triggers of migraine with aura. Cephalalgia 2011, 31:416-438.
14. Coppola G., et al. Is the cerebral cortex hyperexcitable or hyperresponsive in migraine?. Cephalalgia 2007, 27:1427-1439.
15. Aurora S.K., Wilkinson F. The brain is hyperexcitable in migraine. Cephalalgia 2007, 27:1442-1453.
16. de Vries B., et al. Molecular genetics of migraine. Hum. Genet. 2009, 126:115-132.
17. Russell M.B., Ducros A. Sporadic and familial hemiplegic migraine: pathophysiological mechanisms, clinical characteristics, diagnosis, and management. Lancet Neurol. 2011, 10:457-470.
18. 2+ channel gene CACNL1A4. Cell 1996, 87:543-552.
19. + pump α2 subunit associated with familial hemiplegic migraine type 2. Nat. Genet. 2003, 33:192-196.
20. Dichgans M., et al. Mutation in the neuronal voltage-gated sodium channel SCN1A in familial hemiplegic migraine. Lancet 2005, 366:371-377.
21. Pietrobon D. Familial hemiplegic migraine. Neurotherapeutics 2007, 4:274-284.
22. Thomsen L.L., et al. The genetic spectrum of a population-based sample of familial hemiplegic migraine. Brain 2007, 130:346-356.
23. V2.1 channelopathies. Pflugers Arch. 2010, 460:375-393.
24. Pietrobon D. Function and dysfunction of synaptic calcium channels: insights from mouse models. Curr. Opin. Neurobiol. 2005, 15:257-265.
25. V2.1 current density in neurons. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:13284-13289.
26. V2.1 knockin migraine mice. Neuron 2009, 61:762-773.
27. van den Maagdenberg A.M., et al. A Cacna1a knockin migraine mouse model with increased susceptibility to cortical spreading depression. Neuron 2004, 41:701-710.
28. V2.1 S218L mice. Ann. Neurol. 2010, 67:85-98.
29. V2.1 knock-in mice is related to the shape of the action potential. J. Neurophysiol. 2010, 104:291-299.
30. Adams P.J., et al. Contribution of calcium-dependent facilitation to synaptic plasticity revealed by migraine mutations in the P/Q-type calcium channel. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:18694-18699.
31. V2.1 calcium current and excitability in a Cacna1a mouse model of migraine. J. Physiol. 2011, 589:5879-5895.
32. 2+ channel gating: evidence for β-subunit isoform-specific effects. J. Biol. Chem. 2004, 279:51844-51850.
33. V2.1 P/Q-type calcium channel alternative splicing affects the functional impact of familial hemiplegic migraine mutations: implications for calcium channelopathies. Channels (Austin) 2009, 3:110-121.
34. 2 subunit and the glutamate transporters GLAST and GLT-1 in the rat somatosensory cortex. Cereb. Cortex 2002, 12:515-525.
35. +-ATPase activity in astrocytes via activation of a distinct subunit highly sensitive to ouabain. J. Neurochem. 1997, 69:2132-2137.
36. Rose E.M., et al. Glutamate transporter coupling to Na,K-ATPase. J. Neurosci. 2009, 29:8143-8155.
37. 2-subunit causing familial hemiplegic migraine type 2. J. Biol. Chem. 2008, 283:31097-31106.
38. Tavraz N.N., et al. Impaired plasma membrane targeting or protein stability by certain ATP1A2 mutations identified in sporadic or familial hemiplegic migraine. Channels (Austin) 2009, 3:82-87.
39. Leo L., et al. Increased susceptibility to cortical spreading depression in the mouse model of familial hemiplegic migraine type 2. PLoS Genet. 2011, 7:e1002129.
40. V1.1 channels and epilepsy. J. Physiol. 2010, 588:1849-1859.
41. + channel. J. Neurosci. 2008, 28:7273-7283.
42. Kahlig K.M., et al. Divergent sodium channel defects in familial hemiplegic migraine. Proc. Nat. Acad. Sci. U.S.A. 2008, 105:9799-9804.
43. - cotransporter NBCe1 is associated with familial migraine. Proc. Nat. Acad. Sci. U.S.A. 2010, 107:15963-15968.
44. Lafreniere R.G., et al. A dominant-negative mutation in the TRESK potassium channel is linked to familial migraine with aura. Nat. Med. 2010, 16:1157-1160.
45. + channel. Sci. Rep. 2012, 2:237.
46. Anttila V., et al. Genome-wide association study of migraine implicates a common susceptibility variant on 8q22.1. Nat. Genet. 2010, 42:869-873.
47. Tzingounis A.V., Wadiche J.I. Glutamate transporters: confining runaway excitation by shaping synaptic transmission. Nat. Rev. Neurosci. 2007, 8:935-947.
48. Chasman D.I., et al. Genome-wide association study reveals three susceptibility loci for common migraine in the general population. Nat. Genet. 2011, 43:695-698.
49. Madrid R., et al. Contribution of TRPM8 channels to cold transduction in primary sensory neurons and peripheral nerve terminals. J. Neurosci. 2006, 26:12512-12525.
50. Strassman A.M., Levy D. Response properties of dural nociceptors in relation to headache. J. Neurophysiol. 2006, 95:1298-1306.
51. Schytz H.W., et al. What have we learnt from triggering migraine?. Curr. Opin. Neurol. 2010, 23:259-265.
52. Brennan K.C., Charles A. An update on the blood vessel in migraine. Curr. Opin. Neurol. 2010, 23:266-274.
53. Schoonman G.G., et al. Migraine headache is not associated with cerebral or meningeal vasodilatation - a 3T magnetic resonance angiography study. Brain 2008, 131:2192-2200.
54. Asghar M.S., et al. Evidence for a vascular factor in migraine. Ann. Neurol. 2011, 69:635-645.
55. Waeber C., Moskowitz M.A. Migraine as an inflammatory disorder. Neurology 2005, 64:S9-S15.
56. Levy D. Migraine pain, meningeal inflammation, and mast cells. Curr. Pain Headache Rep. 2009, 13:237-240.
57. Vaughn A.H., Gold M.S. Ionic mechanisms underlying inflammatory mediator-induced sensitization of dural afferents. J. Neurosci. 2010, 30:7878-7888.
58. Yan J., et al. Dural afferents express acid-sensing ion channels: a role for decreased meningeal pH in migraine headache. Pain 2011, 152:106-113.
59. Strassman A.M., et al. Sensitization of meningeal sensory neurons and the origin of headaches. Nature 1996, 384:560-564.
60. Edelmayer R.M., et al. Medullary pain facilitating neurons mediate allodynia in headache-related pain. Ann. Neurol. 2009, 65:184-193.
61. Burstein R., et al. The development of cutaneous allodynia during a migraine attack clinical evidence for the sequential recruitment of spinal and supraspinal nociceptive neurons in migraine. Brain 2000, 123:1703-1709.
62. Levy D., et al. Mast cell degranulation activates a pain pathway underlying migraine headache. Pain 2007, 130:166-176.
63. 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.
64. Villalon C.M., Olesen J. The role of CGRP in the pathophysiology of migraine and efficacy of CGRP receptor antagonists as acute antimigraine drugs. Pharmacol. Ther. 2009, 124:309-323.
65. Recober A., Russo A.F. Calcitonin gene-related peptide: an update on the biology. Curr. Opin. Neurol. 2009, 22:241-246.
66. Ho T.W., et al. CGRP and its receptors provide new insights into migraine pathophysiology. Nat. Rev. Neurol. 2010, 6:573-582.
67. Nicoletti P., et al. Ethanol causes neurogenic vasodilation by TRPV1 activation and CGRP release in the trigeminovascular system of the guinea pig. Cephalalgia 2008, 28:9-17.
68. Nassini R., et al. The 'headache tree' via umbellulone and TRPA1 activates the trigeminovascular system. Brain 2012, 135:376-390.
69. Baun M., et al. Dural mast cell degranulation is a putative mechanism for headache induced by PACAP-38. Cephalalgia 2012, 32:337-345.
70. Burstein R., et al. An association between migraine and cutaneous allodynia. Ann. Neurol. 2000, 47:614-624.
71. Lipton R.B., et al. Cutaneous allodynia in the migraine population. Ann. Neurol. 2008, 63:148-158.
72. Burstein R., et al. Chemical stimulation of the intracranial dura induces enhanced responses to facial stimulation in brain stem trigeminal neurons. J. Neurophysiol. 1998, 79:964-982.
73. Burstein R., et al. Thalamic sensitization transforms localized pain into widespread allodynia. Ann. Neurol. 2010, 68:81-91.
74. Lee M.C., et al. Identifying brain activity specifically related to the maintenance and perceptual consequence of central sensitization in humans. J. Neurosci. 2008, 28:11642-11649.
75. Moulton E.A., et al. Interictal dysfunction of a brainstem descending modulatory center in migraine patients. PLoS ONE 2008, 3:e3799.
76. Weiller C., et al. Brain stem activation in spontaneous human migraine attacks. Nat. Med. 1995, 1:658-660.
77. Olesen J., et al. Calcitonin gene-related peptide receptor antagonist BIBN 4096 BS for the acute treatment of migraine. N. Engl. J. Med. 2004, 350:1104-1110.
78. Ho T.W., et al. Efficacy and tolerability of MK-0974 (telcagepant), a new oral antagonist of calcitonin gene-related peptide receptor, compared with zolmitriptan for acute migraine: a randomised, placebo-controlled, parallel-treatment trial. Lancet 2008, 372:2115-2123.
79. Lassen L.H., et al. CGRP may play a causative role in migraine. Cephalalgia 2002, 22:54-61.
80. Lennerz J.K., et al. Calcitonin receptor-like receptor (CLR), receptor activity-modifying protein 1 (RAMP1), and calcitonin gene-related peptide (CGRP) immunoreactivity in the rat trigeminovascular system: differences between peripheral and central CGRP receptor distribution. J. Comp. Neurol. 2008, 507:1277-1299.
81. Eftekhari S., et al. Differential distribution of calcitonin gene-related peptide and its receptor components in the human trigeminal ganglion. Neuroscience 2010, 169:683-696.
82. Levy D., et al. Calcitonin gene-related peptide does not excite or sensitize meningeal nociceptors: implications for the pathophysiology of migraine. Ann. Neurol. 2005, 58:698-705.
83. Zhang X.C., et al. Sensitization and activation of intracranial meningeal nociceptors by mast cell mediators. J. Pharmacol. Exp. Ther. 2007, 322:806-812.
84. Dux M., et al. Involvement of capsaicin-sensitive afferent nerves in the proteinase-activated receptor 2-mediated vasodilatation in the rat dura mater. Neuroscience 2009, 161:887-894.
85. 3 receptors of trigeminal sensory neurons by calcitonin gene-related peptide. J. Neurosci. 2006, 26:6163-6171.
86. Zhang Z., et al. Sensitization of calcitonin gene-related peptide receptors by receptor activity-modifying protein-1 in the trigeminal ganglion. J. Neurosci. 2007, 27:2693-2703.
87. Li J., et al. Calcitonin gene-related peptide stimulation of nitric oxide synthesis and release from trigeminal ganglion glial cells. Brain Res. 2008, 1196:22-32.
88. Vause C.V., Durham P.L. Calcitonin gene-related peptide differentially regulates gene and protein expression in trigeminal glia cells: findings from array analysis. Neurosci. Lett. 2010, 473:163-167.
89. Capuano A., et al. Proinflammatory-activated trigeminal satellite cells promote neuronal sensitization: relevance for migraine pathology. Mol. Pain 2009, 5:43.
90. V2.1 knock-in mice: implications for basic mechanisms of migraine pain. J. Neurosci. 2011, 31:3638-3649.
91. 3 receptor activity of mouse sensory ganglion neurons mediating trigeminal pain. Mol. Pain 2010, 6:48.
92. Summ O., et al. Modulation of nocioceptive transmission with calcitonin gene-related peptide receptor antagonists in the thalamus. Brain 2010, 133:2540-2548.
93. Storer R.J., et al. Calcitonin gene-related peptide (CGRP) modulates nociceptive trigeminovascular transmission in the cat. Br. J. Pharmacol. 2004, 142:1171-1181.
94. Meng J., et al. Activation of TRPV1 mediates calcitonin gene-related peptide release, which excites trigeminal sensory neurons and is attenuated by a retargeted botulinum toxin with anti-nociceptive potential. J. Neurosci. 2009, 29:4981-4992.
95. Fischer M.J., et al. The nonpeptide calcitonin gene-related peptide receptor antagonist BIBN4096BS lowers the activity of neurons with meningeal input in the rat spinal trigeminal nucleus. J. Neurosci. 2005, 25:5877-5883.
96. Sixt M.L., et al. Calcitonin gene-related peptide receptor antagonist olcegepant acts in the spinal trigeminal nucleus. Brain 2009, 132:3134-3141.
97. Edvinsson L., et al. Inhibitory effect of BIBN4096BS, CGRP(8-37), a CGRP antibody and an RNA-Spiegelmer on CGRP induced vasodilatation in the perfused and non-perfused rat middle cerebral artery. Br. J. Pharmacol. 2007, 150:633-640.
98. Asghar M.S., et al. Effect of CGRP and sumatriptan on the BOLD response in visual cortex. J. Headache Pain 2012, 13:159-166.
99. Akerman S., et al. Diencephalic and brainstem mechanisms in migraine. Nat. Rev. Neurosci. 2011, 12:570-584.
100. Lambert G.A., Zagami A.S. The mode of action of migraine triggers: a hypothesis. Headache 2009, 49:253-275.
101. Denuelle M., et al. Hypothalamic activation in spontaneous migraine attacks. Headache 2007, 47:1418-1426.
102. Mainero C., et al. Mapping the spinal and supraspinal pathways of dynamic mechanical allodynia in the human trigeminal system using cardiac-gated fMRI. Neuroimage 2007, 35:1201-1210.
103. Stankewitz A., et al. Trigeminal nociceptive transmission in migraineurs predicts migraine attacks. J. Neurosci. 2011, 31:1937-1943.
104. Mainero C., et al. Altered functional magnetic resonance imaging resting-state connectivity in periaqueductal gray networks in migraine. Ann. Neurol. 2011, 70:838-845.
105. Noseda R., et al. A neural mechanism for exacerbation of headache by light. Nat. Neurosci. 2010, 13:239-245.
106. Zhang X., et al. Activation of meningeal nociceptors by cortical spreading depression: implications for migraine with aura. J. Neurosci. 2010, 30:8807-8814.
107. Zhang X., et al. Activation of central trigeminovascular neurons by cortical spreading depression. Ann. Neurol. 2011, 69:855-865.
108. Busija D.W., et al. Mechanisms involved in the cerebrovascular dilator effects of cortical spreading depression. Prog. Neurobiol. 2008, 86:379-395.
109. Bolay H., et al. Intrinsic brain activity triggers trigeminal meningeal afferents in a migraine model. Nat. Med. 2002, 8:136-142.
110. Ebersberger A., et al. Is there a correlation between spreading depression, neurogenic inflammation, and nociception that might cause migraine headache?. Ann. Neurol. 2001, 49:7-13.
111. Noseda R., et al. Changes of meningeal excitability mediated by corticotrigeminal networks: a link for the endogenous modulation of migraine pain. J. Neurosci. 2010, 30:14420-14429.
112. Koroleva V.I., Bures J. Rats do not experience cortical or hippocampal spreading depression as aversive. Neurosci. Lett. 1993, 149:153-156.
113. Akcali D., et al. Does single cortical spreading depression elicit pain behaviour in freely moving rats?. Cephalalgia 2010, 30:1195-1206.
114. Fioravanti B., et al. Evaluation of cutaneous allodynia following induction of cortical spreading depression in freely moving rats. Cephalalgia 2010, 31:1090-1100.
115. Levy D., et al. Activation of the migraine pain pathway by cortical spreading depression: Do we need more evidence?. Cephalalgia 2012, 32:581-582.
116. Ayata C., et al. Suppression of cortical spreading depression in migraine prophylaxis. Ann. Neurol. 2006, 59:652-661.
117. Hoffmann U., et al. Oxcarbazepine does not suppress cortical spreading depression. Cephalalgia 2011, 31:537-542.
118. Hauge A.W., et al. Effects of tonabersat on migraine with aura: a randomised, double-blind, placebo-controlled crossover study. Lancet Neurol. 2009, 8:718-723.
119. Bogdanov V.B., et al. Migraine preventive drugs differentially affect cortical spreading depression in rat. Neurobiol. Dis. 2011, 41:430-435.
120. V2.1 calcium channels produced by mutation S218L causing familial hemiplegic migraine and delayed cerebral edema and coma after minor head trauma. J. Biol. Chem. 2005, 280:17678-17686.
121. Eikermann-Haerter K., 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, 119:99-109.
122. Eikermann-Haerter K., et al. Enhanced subcortical spreading depression in familial hemiplegic migraine type 1 mutant mice. J. Neurosci. 2011, 31:5755-5763.
123. Eikermann-Haerter K., et al. Androgenic suppression of spreading depression in familial hemiplegic migraine type 1 mutant mice. Ann. Neurol. 2009, 66:564-568.
124. Vahedi K., et al. Elicited repetitive daily blindness: a new phenotype associated with hemiplegic migraine and SCN1A mutations. Neurology 2009, 72:1178-1183.
125. Eikermann-Haerter K., et al. Cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy syndrome mutations increase susceptibility to spreading depression. Ann. Neurol. 2011, 69:413-418.
126. Denuelle M., et al. Posterior cerebral hypoperfusion in migraine without aura. Cephalalgia 2008, 28:856-862.
127. Siniatchkin M., et al. Neurophysiological reactivity before a migraine attack. Neurosci. Lett. 2006, 400:121-124.
128. Siniatchkin M., et al. Peri-ictal changes of cortical excitability in children suffering from migraine without aura. Pain 2009, 147:132-140.
129. Wilkinson F., et al. Binocular rivalry in migraine. Cephalalgia 2008, 28:1327-1338.
130. Battista J., et al. Migraine increases centre-surround suppression for drifting visual stimuli. PLoS ONE 2011, 6:e18211.
131. McKendrick A.M., et al. Visual and auditory perceptual rivalry in migraine. Cephalalgia 2011, 31:1158-1169.
132. Siniatchkin M., et al. Intracortical inhibition and facilitation in migraine - a transcranial magnetic stimulation study. Headache 2007, 47:364-370.
133. Cosentino G., et al. Impaired glutamatergic neurotransmission in migraine with aura? Evidence by an input-output curves transcranial magnetic stimulation study. Headache 2011, 51:726-733.
134. Antal A., et al. Homeostatic metaplasticity of the motor cortex is altered during headache-free intervals in migraine with aura. Cereb. Cortex 2008, 18:2701-2705.
135. Conte A., et al. Differences in short-term primary motor cortex synaptic potentiation as assessed by repetitive transcranial magnetic stimulation in migraine patients with and without aura. Pain 2010, 148:43-48.
136. Siniatchkin M., et al. Abnormal changes of synaptic excitability in migraine with aura. Cereb. Cortex 2011, 10.1093/cercor/bhr248.
137. Moulton E.A., et al. Painful heat reveals hyperexcitability of the temporal pole in interictal and ictal migraine states. Cereb. Cortex 2011, 21:435-448.
138. Pietrobon D. Migraine: new molecular mechanisms. Neuroscientist 2005, 11:373-386.
139. 2+ channels. Channels (Austin) 2011, 5:110-114.
140. Shu Y., et al. Turning on and off recurrent balanced cortical activity. Nature 2003, 423:288-293.
141. Monier C., et al. Orientation and direction selectivity of synaptic inputs in visual cortical neurons: a diversity of combinations produces spike tuning. Neuron 2003, 37:663-680.
142. Prescot A., et al. Excitatory neurotransmitters in brain regions in interictal migraine patients. Mol. Pain 2009, 5:34.
143. Olesen J., Ashina M. Emerging migraine treatments and drug targets. Trends Pharmacol. Sci. 2011, 32:352-359.
144. Edvinsson L. Tracing neural connections to pain pathways with relevance to primary headaches. Cephalalgia 2011, 31:737-747.
145. Noseda R., et al. Cortical projections of functionally identified thalamic trigeminovascular neurons: implications for migraine headache and its associated symptoms. J. Neurosci. 2011, 31:14204-14217.
146. Freilinger T., et al. Genome-wide association analysis identifies susceptibility loci for migraine without aura. Nat. Genet. 2012, 44:777-782.
147. Flavell S.W., et al. Genome-wide analysis of MEF2 transcriptional program reveals synaptic target genes and neuronal activity-dependent polyadenylation site selection. Neuron 2008, 60:1022-1038.