Cortical spreading depression and migraine

Nature Reviews Neurology

Volumn 9, Issue 11, 2013, Pages 637-644

  Charles, Andrew C ^a   Baca, Serapio M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMITRIPTYLINE; CARBAMAZEPINE; DEXPROPRANOLOL; LAMOTRIGINE; METHYSERGIDE; OXCARBAZEPINE; PROPRANOLOL; RIBOFLAVIN; TOPIRAMATE; VALPROIC ACID;

ACUTE DRUG ADMINISTRATION; ASTROCYTE; BLOOD VESSEL PARAMETERS; BRAIN MAPPING; BRAIN REGION; CELL ACTIVATION; CELL FUNCTION; CHRONIC DRUG ADMINISTRATION; CLINICAL FEATURE; DISEASE ACTIVITY; DISEASE ASSOCIATION; DRUG EFFECT; ELECTROENCEPHALOGRAM; FUNCTIONAL ASSESSMENT; GENE; GENE FUNCTION; GENE IDENTIFICATION; HEADACHE; HUMAN; IMAGE ANALYSIS; MIGRAINE; MIGRAINE ASSOCIATED GENE; MOLECULAR DYNAMICS; MOLECULAR PATHOLOGY; NERVE CELL NETWORK; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OUTCOME ASSESSMENT; PRIORITY JOURNAL; REVIEW; SEX DIFFERENCE; SIGNAL DETECTION; SIGNAL TRANSDUCTION; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; SPREADING CORTICAL DEPRESSION; VASCULAR CHANGE;

ANIMALS; BRAIN; CORTICAL SPREADING DEPRESSION; HUMANS; MIGRAINE DISORDERS; MIGRAINE WITH AURA;

EID: 84887239328     PISSN: 17594758     EISSN: 17594766     Source Type: Journal    
DOI: 10.1038/nrneurol.2013.192     Document Type: Review

References (89)

1. Leão, A. A. Spreading depression of activity in the cerebral cortex. J. Neurophysiol. 7, 359-390 (1944).
2. Leão, A. A. Further observervations on the spreading depression of activity in the cerebral cortex. J. Neurophysiol. 10, 409-414 (1947).
3. Leão, A. A. Pial circulation and spreading depression of activity in the cerebral cortex. J. Neurophysiol. 7, 391-396 (1944).
4. Leão, A. A. & Morison, R. S. Propagation of spreading cortical depression. J. Neurophysiol. 8, 33-45 (1945).
5. Hansen, A. J. & Zeuthen, T. Extracellular ion concentrations during spreading depression and ischemia in the rat brain cortex. Acta Physiol. Scand. 113, 437-445 (1981).
6. Mutch, W. A. & Hansen, A. J. Extracellular pH changes during spreading depression and cerebral ischemia: mechanisms of brain pH regulation. J. Cereb. Blood Flow Metab. 4, 17-27 (1984).
7. Dietz, R. M., Weiss, J. H. & Shuttleworth, C. W. Zn2+ influx is critical for some forms of spreading depression in brain slices. J. Neurosci. 28, 8014-8024 (2008).
8. Hansen, A. J. & Olsen, C. E. Brain extracellular space during spreading depression and ischemia. Acta Physiol. Scand. 108, 355-365 (1980).
9. Sugaya, E., Takato, M. & Noda, Y. Neuronal and glial activity during spreading depression in cerebral cortex of cat. J. Neurophysiol. 38, 822-841 (1975).
10. Sheardown, M. J. The triggering of spreading depression in the chicken retina: A pharmacological study. Brain Res. 607, 189-194 (1993).
11. Tobiasz, C. & Nicholson, C. Tetrodotoxin resistant propagation and extracellular sodium changes during spreading depression in rat cerebellum. Brain Res. 241, 329-333 (1982).
12. Herreras, O., Largo, C., Ibarz, J. M., Somjen, G. G. & Martin del Rio, R. Role of neuronal synchronizing mechanisms in the propagation of spreading depres sion in the in vivo hippocampus. J. Neurosci. 14, 7087-7098 (1994).
13. Canals, S. et al. Longitudinal depolarization gradients along the somatodendritic axis of CA1 pyramidal cells: A novel feature of sprea ding depression. J. Neurophysiol. 94, 943-951 (2005).
14. Charles, A. Intercellular calcium waves in glia. Glia 24, 39-49 (1998).
15. Busija, D. W., Bari, F. , Domoki, F., Horiguchi, T. & Shimizu, K. Mechanisms involved in the cerebrovascular dilator effects of cortical spreading depression. Prog. Neurobiol. 86, 417-433 (2008).
16. Smith, J. M., B radley, D. P., James, M. F. & Huang, C. L. Physiological studies of cortical spreading depression. Biol. Rev. Camb. Philos. Soc. 81, 457-481 (2006).
17. Akcali, D., Sayin, A., Sara, Y. & Bolay, H. Does single cortical spreading depression elicit pain behaviour in freely moving rats Cephalalgia 30, 1195-1206 (2010).
18. Peeters, M. et al. 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. 321, 564-572 (2007).
19. Petzold, G. C. et al. Increased ex tracellular K+ concentration reduces the efficacy of N-methyl-d-aspartate receptor antagonists to block spreading depression-like depolarizations and spreading ischemia. Stroke 36, 1270-1277 (2005).
20. Lauritze n, M. & Hansen, A. The effect of glutamate receptor blockade on anoxic depolarization and cortical spreading depression. J. Cereb. Blood Flow Metab. 12, 223-229 (1992).
21. Faria, L. C. & Mody, I. Protective effect of ifenprodil against spreading depression in the mouse entorhinal cortex. J. Neurophysiol. 92, 2610-2614 (2004).
22. Nozari, A. et al. Microemboli may link spreading depression, migraine aura, and patent foramen ovale. Ann. Neurol. 67, 221-229 (2010).
23. van den Maagdenberg, A. M. et al. A Cacna1a knockin migraine mouse model with increased susceptibility to cort ical spreading depression. Neuron 41, 701-710 (2004).
24. Leo, L. et al. Increased susceptibility to cortical spreading depression in the mouse model of familial hemiplegic migraine type 2. PLoS Ge net. 7, e1002129 (2011).
25. Dreier, J. P. et al. Cortical spreading ischaemia is a novel process involved in ischaemic damage in patients with aneurysmal subarachnoid haemorrhage. Brain 132, 1866-1881 (2009).
26. Hartings, J. A. et al. Spreading depolarizations have prolonged direct current shifts and are associated with poor outcome in brain trauma. Brain 134, 1529-1540 (2011).
27. Woitzik, J. et al. Propagation of cortical spreading depolarization in the human cortex after malignant stroke. Neurology 80, 1095-1102 (2013).
28. Lashley, K. S. Patterns of cerebral integration indicated by the scotomas of migraine. Arch. Neurol. Psychiatry 46, 331-339 (1941).
29. Tfelt-Hansen, P. C. History of migraine with aura and cortical spreading depression from 1941 and onwards. Cephalalgia 30, 780-792 (2010).
30. Bowyer, S. M., A urora, S. K., Moran, J. E., Tepley, N. & Welch, K. M. Magnetoencephalographic fields from patients with spontaneous and induced migraine aura. Ann. Neurol. 50, 582-587 (2001).
31. Lauritzen, M., Trojaborg, W. & Olesen, J. EEG during attacks of common and classical migraine. Cephalalgia 1, 63-66 (1981).
32. Drenckhahn, C. et al. Correlates of spreading depolarization in human scalp electroencephalography. Brain 135, 853-868 (2012).
33. Eikermann-Haerter, K. et al. Genetic and hormonal factors modulate spreading depression and transient hemiparesis in mouse models of fam ilial hemiplegic migraine type 1. J. Clin. Invest. 119, 99-109 (2009).
34. Hansen, J. M., Thomsen, L. L., Olesen, J. & Ashina, M. Coexisting typical migraine in familial hemiplegic migraine. Neurology 74, 594-600 (2010).
35. Brennan, K. C. et al. Casein kinase I mutations in familial migraine and advanced sleep phase. Sci. Transl. Med. 5, 183ra56 (2013).
36. Brennan, K. C., Romero-Reyes, M., López Valdés, H. E., Arnold, A. P. & Charles, A. C. Reduced threshold for cortical spreading depression in female mice. Ann. Neurol. 61, 603-606 (2 007).
37. Eikermann-Haerter, K. et al. Androgenic suppression of spreading depression in familial hemiplegic migraine type 1 mutant mice. Ann. Neurol. 66, 564-568 (2009).
38. Ayata, C., Jin, H., Kudo, C., Dalkara, T. & Moskowitz, M. A. Suppression of cortical spreading depression in migraine prophylaxis. Ann. Neurol. 59, 652-661 (2006).
39. Akerman, S. & Goadsby, P. J. Topiramate inhibits cortical spreading depression in rat and cat: impact in migraine aura. Neuroreport 16, 1383-1387 (2005).
40. Holland, P. R. et al. Acid-sensing ion channel 1: A novel therapeutic target for migraine with aura. Ann. Neurol. 72, 559-563 (2012).
41. Bogdanov, V. B. et al. Migraine preventive drugs differentially affect cortical spreading depression in rat. Neurobiol. Dis. 41, 430-435 (2011).
42. Hoffmann, U., Dileköz, E., Kudo, C. & Ayata, C. Oxcarbazepine does not suppress cortical spreading depression. Cephalalgia 31, 537-542 (2011).
43. Tozzi, A. et al. Critical role of calcitonin gene-related peptide receptors in cortical spreading depression. Proc. Natl Acad. Sci. USA 109, 18985-18990 (2012).
44. Ayata, C. et al. Pronounced hypoperfusion during spreading depression in mouse cortex. J. Cereb. Blood Flow Metab. 24, 1172-1182 (2004).
45. Brennan, K. C. et al. Distinct vascular conduction with cortical spreading depression. J. Neurophysiol. 97, 4143-4151 (2007).
46. Chang, J. C. et al. Biphasic direct current shift, haemoglobin desaturat ion and neurovascular uncoupling in cortical spreading depression. Brain 133, 996-1012 (2010).
47. Piilgaard, H. & Lauritzen, M. Persistent increase in oxygen consumption and impaired neurova scular coupling after spreading depression in rat neocortex. J. Cereb. Blood Flow Metab. 29, 1517-1527 (2009).
48. Iizuka, T. et al. Neurovascular changes in prolonged migraine aura in FHM with a novel ATP1A2 gene mutation. J. Neurol. Neurosurg. Psychiatry 83, 205-212 (2012).
49. Bereczki, D. et al. Cortical spreading edema in persistent visual migraine aura. Headache 48, 1226-1229 (2008).
50. Guedj, E. et al. Partially reversible cortical metabolic dysfunction in familial hemiplegic migraine with prolonged aura. Headache 50, 872-877 (2010).
51. Gutsc halk, A. et al. Multimodal functional imaging of prolonged neurological deficits in a patient suffering from familial hemiplegic migraine. Neurosci. Lett. 332, 115-118 (2002).
52. Wolf, M. E., Jager, T. Bazner, H. & Hennerici, M. Changes in functional vasomotor reactivity in migraine with aura. Cephalalgia 29, 1156-1164 (2009).
53. Zhang, X. et al. Activation of central trigeminovascular neurons by cortical spreading depression. Ann. Neurol. 69, 855-865 (2011).
54. Zhang, X. et al. Activation of meningeal nociceptors by cortical spreading depression: implications for migraine with aura. J. Neurosci. 30, 8807-8814 (2010).
55. Charles, A. C., Merrill, J. E., Dirksen, E. R. & Sanderson, M. J. Intercellular signaling in glial cells: calcium waves and oscillations in response to mechanical stimulation and glutamate. Neuron 6, 983-992 (1991).
56. Cornell-Bell, A. H., Finkbeiner, S. M., Cooper, M. S. & Smith, S. J. Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling. Science 247, 470-473 (1990).
57. Basarsky, T. A., Duffy, S. N., Andrew, R. D. & MacVicar, B. A. Imaging spreading depression and associated intracellular calcium waves in brain slices. J. Neurosci. 18, 7189-7199 (1998).
58. Peters, O., Schipke, C. G., Hashimoto, Y. & K ettenmann, H. Different mechanisms promote astrocyte Ca2+ waves and spreading depression in the mouse neocortex. J. Neurosci. 23, 9888-9896 (2003).
59. Chuquet, J., Hollender, L. & Nimchinsky, E. High-resolution in vivo imaging of the neurovascular unit during spreading depression. J. Neurosci. 27, 4036-4044 (2007).
60. Largo, C., Tombaugh, G. C., Aitken, P. G., Herreras, O. & Somjen, G. G. Heptanol but not fluoroacetate prevents the propagation of spreading depression in rat hippocampal slices. J. Neurophysiol. 77, 9-16 (1997).
61. Zhou, N., Gordon, G. R., Feighan, D. & MacVicar, B. A. Transient swelling, acidification, and mitochondrial depolarization occurs in neurons but not astrocytes during spreading depression. Cereb. Cortex 20, 2614-2624 (2010).
62. C olonna, D. M., Meng, W., Deal, D. D., Gowda, M. & Busija, D. W. Neuronal NO promotes cerebral cortical hyperemia during cortical spreading depression in rabbits. Am. J. Physiol. 272, H1315-H1322 (1997).
63. Obrenovitch, T. P., 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. 22, 680-688 (2002).
64. Schock, S. C. et al. Cortical spreading depression releases ATP into the extracellular space and purinergic receptor activation contributes to the induction of ischemic tolerance. Brain Res. 1168, 129-138 (2007).
65. Colonna, D. M., Meng, W., Deal, D. D. & Busija, D. W. Calcitonin gene-related peptide promotes cerebrovascular dilation during cortical spreading depression in rabbits. Am. J. Physiol. 266, H1095-H1102 (1994).
66. Reuter, U. et al. Perivascular nerves contribute to cortical spreading depression-associated hyperemia in rats. Am. J. Physiol. Heart Circ. Physiol. 274, H1979-H1987 (1998).
67. Wahl, M., Schilling, L., Parsons, A. A. & Kaumann, A. Involvement of calcitonin gene-related peptide (CGRP) and nitric oxide (NO) in the pial artery dilatation elicited by cortical spreading depression. Brain R es. 637, 204-210 (1994).
68. Karatas, H. et al. Spreading depression triggers headache by activating neuronal Panx1 channels. Science 339, 1092-1095 (2013).
69. Bolay, H. et al. Intrinsic brain activity triggers trigeminal meningeal afferents in a migraine model. Nat. Med. 8, 136-142 (2002).
70. Fioravanti, B. et al. Evaluation of cutane ous allodynia following induction of cortical spreading depression in freely moving rats. Cephalalgia 31, 1090-1100 (2011).
71. Amin, F. M. et al. Magnetic resonance angiography of intracranial a nd extracranial arteries in patients with spontaneous migraine without aura: A cross-sectional study. Lancet Neurol. 12, 454-461 (2013).
72. Charles, A. Vasodilation out of the picture as a cause of migraine headache. Lancet Neurol. 12, 419-420 (2013).
73. Lambert, G. A., Truong, L. & Zagami, A. S. Effect of cortical spreading depression on basal and evoked traffic in the trigeminova scular sensory system. Cephalalgia 31, 1439-1451 (2011).
74. Eikermann-Haerter, K. et al. Enhanced subcortical spreading depression in familial hemiplegic migraine type 1 mutant mice. J. Neurosci. 31, 5755-5763 (2011).
75. Burstein, R., Strassman, A. & Moskowitz, M. Can cortical spreading depression activate central trigeminovascular neurons without peripheral input Pitfalls of a new concept. Cephalalgia 32, 509-511 (2012).
76. Goadsby, P. J. & 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 32, 3-5 (2012).
77. Olesen, J. et al. Timing and topography of cerebral blood flow, aura, and headache during migraine attacks. Ann. Neurol. 28, 791-798 (1990).
78. Woods, R. P., Iacoboni, M. & Mazziotta, J. C. Bilateral spreading cerebral hypoperfusio n during spontaneous migraine headache. N. Engl. J. Med. 331, 1689-1692 (1994).
79. Hadjikhani, N. et al. Mechanisms of migraine aura revealed by functional MRI in human visual cortex. Proc. Natl Acad. Sci. USA 98, 4687-4692 (2001).
80. Cao, Y., Welch, K. M., Aurora, S. & Vikingstad, E. M. Functional MRI-BOLD of visually triggered headache in patients with migraine. Arch. Neurol. 56, 548-554 (1999).
81. Schott, G. D. Exploring the visual hallucinations of migraine aura: the tacit contribution of illustration. Brain 130, 1690-1703 (2007).
82. Queiroz, L. P., Friedman, D. I., Rapoport, A. M. & Purdy, R. A. Characteristics of migraine visual aura in Southern Brazil and Northern USA. Cephalalgia 31, 1652-1658 (2011).
83. Queiroz, L. P. et al. Characteristics of migraine visual aura. Headache 37, 137-141 (1997).
84. Headache Classification Committee of the International Headache Society (IHS). The International Classification of Headache Disorders, 3rd edition (beta version). Cephalalgia 33, 629-808 (2013).
85. Jensen, K., Tfelt-Hansen, P., Lauritzen, M. & Olesen, J. Classic migrain e. A prospective recording of symptoms. Acta Neurol. Scand. 73, 359-362 (1986).
86. Hansen, J. M. et al. Migraine headache is present in the aura phase: A prospective study. Neurology 79, 2044-2049 (2012).
87. Charles, A. Migraine: A brain state. Curr. Opin. Neurol. 26, 235-239 (2013).
88. Dahlem, M. A. & Hadjikhani, N. Migraine aura: retracting particle-like waves in weakly susceptible cortex. PLoS ONE 4, e5007 (2009).
89. Fabricius, M. et al. Association of seizures with cortical spreading depression and peri-infarct depolarisations in the acutely injured human brain. Clin. Neurophysiol. 119, 1973-1984 (2008).