Clinical neurophysiology of migraine with aura

Gianluca Coppola, Cherubino Di Lorenzo, Vincenzo Parisi, Marco Lisicki, Mariano Serrao, Francesco Pierelli, Gianluca Coppola, Cherubino Di Lorenzo, Vincenzo Parisi, Marco Lisicki, Mariano Serrao, Francesco Pierelli

Abstract

Background: The purpose of this review is to provide a comprehensive overview of the findings of clinical electrophysiology studies aimed to investigate changes in information processing of migraine with aura patients.

Main body: Abnormalities in alpha rhythm power and symmetry, the presence of slowing, and increased information flow in a wide range of frequency bands often characterize the spontaneous EEG activity of MA. Higher grand-average cortical response amplitudes, an increased interhemispheric response asymmetry, and lack of amplitude habituation were less consistently demonstrated in response to any kind of sensory stimulation in MA patients. Studies with single-pulse and repetitive transcranial magnetic stimulation (TMS) have reported abnormal cortical responsivity manifesting as greater motor evoked potential (MEP) amplitude, lower threshold for phosphenes production, and paradoxical effects in response to both depressing or enhancing repetitive TMS methodologies. Studies of the trigeminal system in MA are sparse and the few available showed lack of blink reflex habituation and abnormal findings on SFEMG reflecting subclinical, probably inherited, dysfunctions of neuromuscular transmission. The limited studies that were able to investigate patients during the aura revealed suppression of evoked potentials, desynchronization in extrastriate areas and in the temporal lobe, and large variations in direct current potentials with magnetoelectroencephalography. Contrary to what has been observed in the most common forms of migraine, patients with familial hemiplegic migraine show greater habituation in response to visual and trigeminal stimuli, as well as a higher motor threshold and a lower MEP amplitude than healthy subjects.

Conclusion: Since most of the electrophysiological abnormalities mentioned above were more frequently present and had a greater amplitude in migraine with aura than in migraine without aura, neurophysiological techniques have been shown to be of great help in the search for the pathophysiological basis of migraine aura.

Keywords: Cortical excitability; Habituation; Interhemispheric asymmetry; Neuromodulation; Paradoxical responses; Slow rhythms.

Conflict of interest statement

The authors declare that they have no competing interests.

References

    1. Russell M, Olesen J. A nosographic analysis of the migraine aura in a general population. Brain. 1996;119:355–361. doi: 10.1093/brain/119.2.355.
    1. Eriksen M, Thomsen LL, Andersen I, et al. Clinical characteristics of 362 patients with familial migraine with aura. Cephalalgia. 2004;24:564–575. doi: 10.1111/j.1468-2982.2003.00718.x.
    1. Headache Classification Committee of the International Headache Society (IHS) The International Classification of Headache Disorders, 3rd edition. Cephalalgia. 2018;38:1–211. doi: 10.1177/0333102417738202.
    1. Charles A, Baca SM. Cortical spreading depression and migraine. Nat Rev. 2013;9:637–644.
    1. Leão AAP. Spreading depression of activity in the cerebral cortex. J Neurophysiol. 1944;7:359–390. doi: 10.1152/jn.1944.7.6.359.
    1. Olesen J, Friberg L, Olsen TS, et al. Timing and topography of cerebral blood flow, aura, and headache during migraine attacks. Ann Neurol. 1990;28:791–798. doi: 10.1002/ana.410280610.
    1. Cao Y, Welch KM, Aurora S, Vikingstad EM. Functional MRI-BOLD of visually triggered headache in patients with migraine. Arch Neurol. 1999;56:548–554. doi: 10.1001/archneur.56.5.548.
    1. 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. 2001;98:4687–4692. doi: 10.1073/pnas.071582498.
    1. Bowyer SM, Aurora KS, Moran JE, et al. Magnetoencephalographic fields from patients with spontaneous and induced migraine aura. Ann Neurol. 2001;50:582–587. doi: 10.1002/ana.1293.
    1. Hall SD, Barnes GR, Hillebrand A, et al. Spatio-temporal imaging of cortical desynchronization in migraine visual aura: a magnetoencephalography case study. Headache. 2004;44:204–208. doi: 10.1111/j.1526-4610.2004.04048.x.
    1. Ferrari MD, Klever RR, Terwindt GM, et al. Migraine pathophysiology: lessons from mouse models and human genetics. Lancet Neurol. 2015;14:65–80. doi: 10.1016/S1474-4422(14)70220-0.
    1. Golla FL, Winter AL. Analysis of cerebral responses to flicker in patients complaining of episodic headache. Electroencephalogr Clin Neurophysiol. 1959;11:539–549. doi: 10.1016/0013-4694(59)90052-5.
    1. Puca FM, de Tommaso M, Savarese MA, et al. Topographic analysis of steady-state visual evoked potentials (SVEPs) in the medium frequency range in migraine with and without aura. Cephalalgia. 1992;12:244–246. doi: 10.1046/j.1468-2982.1992.1204244.x.
    1. Genco S, de Tommaso M, Prudenzano AM, et al. EEG features in juvenile migraine: topographic analysis of spontaneous and visual evoked brain electrical activity: a comparison with adult migraine. Cephalalgia. 1994;14:41–46. doi: 10.1046/j.1468-2982.1994.1401041.x.
    1. Chorlton P, Kane N. Investigation of the cerebral response to flicker stimulation in patients with headache. Clin Electroencephalogr. 2000;31:83–87. doi: 10.1177/155005940003100206.
    1. de Tommaso M, Stramaglia S, Marinazzo D, et al. Functional and effective connectivity in EEG alpha and beta bands during intermittent flash stimulation in migraine with and without aura. Cephalalgia. 2013;33:938–947. doi: 10.1177/0333102413477741.
    1. Bjørk M, Hagen K, Stovner L, Sand T. Photic EEG-driving responses related to ictal phases and trigger sensitivity in migraine: a longitudinal, controlled study. Cephalalgia. 2011;31:444–455. doi: 10.1177/0333102410385582.
    1. Shiina Tomohiko, Takashima Ryotaro, Pascual-Marqui Roberto D., Suzuki Keisuke, Watanabe Yuka, Hirata Koichi. Evaluation of Electroencephalogram Using Exact Low-Resolution Electromagnetic Tomography During Photic Driving Response in Patients with Migraine. Neuropsychobiology. 2018;77(4):186–191. doi: 10.1159/000489715.
    1. Facchetti D, Marsile C, Faggi L, et al. Cerebral mapping in subjects suffering from migraine with aura. Cephalalgia. 1990;10:279–284. doi: 10.1046/j.1468-2982.1990.1006279.x.
    1. Neufeld MY, Treves TA, Korczyn AD. EEG and topographic frequency analysis in common and classic migraine. Headache. 1991;31:232–236. doi: 10.1111/j.1526-4610.1991.hed3104232.x.
    1. Schoenen J, Jamart B, Delwaide PJ. Electroencephalographic mapping in migraine during the critical and intercritical periods. Rev Electroencephalogr Neurophysiol Clin. 1987;17:289–299. doi: 10.1016/S0370-4475(87)80066-7.
    1. Bjørk MH, Stovner LJ, Engstrøm M, et al. Interictal quantitative EEG in migraine: a blinded controlled study. J Headache Pain. 2009;10:331–339. doi: 10.1007/s10194-009-0140-4.
    1. de Tommaso M, Trotta G, Vecchio E, et al. Brain networking analysis in migraine with and without aura. J Headache Pain. 2017;18:98. doi: 10.1186/s10194-017-0803-5.
    1. Wu D, Zhou Y, Xiang J, et al. Multi-frequency analysis of brain connectivity networks in migraineurs: a magnetoencephalography study. J Headache Pain. 2016;17:38. doi: 10.1186/s10194-016-0636-7.
    1. Russo A, Tessitore A, Giordano A, et al. Executive resting-state network connectivity in migraine without aura. Cephalalgia. 2012;32:1041–1048. doi: 10.1177/0333102412457089.
    1. Tessitore A, Russo A, Conte F, et al. Abnormal connectivity within executive resting-state network in migraine with Aura. Headache J Head Face Pain. 2015;55:794–805. doi: 10.1111/head.12587.
    1. Tedeschi G, Russo A, Conte F, et al. Increased interictal visual network connectivity in patients with migraine with aura. Cephalalgia. 2016;36:139–147. doi: 10.1177/0333102415584360.
    1. Shibata K, Osawa M, Iwata M. Pattern reversal visual evoked potentials in classic and common migraine. J Neurol Sci. 1997;145:177–181. doi: 10.1016/S0022-510X(96)00258-4.
    1. Shibata K, Osawa M, Iwata M. Pattern reversal visual evoked potentials in migraine with aura and migraine aura without headache. Cephalalgia. 1998;18:319–323. doi: 10.1046/j.1468-2982.1998.1806319.x.
    1. Oelkers R, Grosser K, Lang E, et al. Visual evoked potentials in migraine patients: alterations depend on pattern spatial frequency. Brain. 1999;122:1147–1155. doi: 10.1093/brain/122.6.1147.
    1. Coutin-Churchman P, de Freytez A. Vector analysis of visual evoked potentials in migraineurs with visual aura. Clin Neurophysiol. 2003;114:2132–2137. doi: 10.1016/S1388-2457(03)00229-3.
    1. Zaletel M, Strucl M, Bajrović FF, Pogacnik T. Coupling between visual evoked cerebral blood flow velocity responses and visual evoked potentials in migraneurs. Cephalalgia. 2005;25:567–574. doi: 10.1111/j.1468-2982.2005.00918.x.
    1. Shibata K, Yamane K, Iwata M, Ohkawa S. Evaluating the effects of spatial frequency on migraines by using pattern-reversal visual evoked potentials. Clin Neurophysiol. 2005;116:2220–2227. doi: 10.1016/j.clinph.2005.05.015.
    1. Sand T, Zhitniy N, White LR, Stovner LJ. Visual evoked potential latency, amplitude and habituation in migraine a longitudinal study. Clin Neurophysiol. 2008;119:1020–1027. doi: 10.1016/j.clinph.2008.01.009.
    1. Sand T, White LR, Hagen K, Stovner LJ. Visual evoked potential and spatial frequency in migraine: a longitudinal study. Acta Neurol Scand. 2009;189:33–37. doi: 10.1111/j.1600-0404.2009.01211.x.
    1. Shibata K, Yamane K, Otuka K, Iwata M. Abnormal visual processing in migraine with aura: a study of steady-state visual evoked potentials. J Neurol Sci. 2008;271:119–126. doi: 10.1016/j.jns.2008.04.004.
    1. Nguyen B, McKendrick AM, Vingrys AJ. Simultaneous retinal and cortical visually evoked electrophysiological responses in between migraine attacks. Cephalalgia. 2012;32:896–907. doi: 10.1177/0333102412453953.
    1. Khalil NM, Legg NJ, Anderson DJ. Long term decline of P100 amplitude in migraine with aura. J Neurol Neurosurg Psychiatry. 2000;69:507–511. doi: 10.1136/jnnp.69.4.507.
    1. Afra J, Cecchini AP, De Pasqua V, et al. Visual evoked potentials during long periods of pattern-reversal stimulation in migraine. Brain. 1998;121(Pt 2):233–241. doi: 10.1093/brain/121.2.233.
    1. Coppola G, Ambrosini A, Di Clemente L, et al. Interictal abnormalities of gamma band activity in visual evoked responses in migraine: an indication of thalamocortical dysrhythmia? Cephalalgia. 2007;27:1360–1367. doi: 10.1111/j.1468-2982.2007.01466.x.
    1. Coppola G, Parisi V, Di Lorenzo C, et al. Lateral inhibition in visual cortex of migraine patients between attacks. J Headache Pain. 2013;14:20. doi: 10.1186/1129-2377-14-20.
    1. Schoenen J, Wang W, Albert A, Delwaide PJ. Potentiation instead of habituation characterizes visual evoked potentials in migraine patients between attacks. Eur J Neurol. 1995;2:115–122. doi: 10.1111/j.1468-1331.1995.tb00103.x.
    1. Afra J, Ambrosini a GR, et al. Influence of colors on habituation of visual evoked potentials in patients with migraine with aura and in healthy volunteers. Headache. 2000;40:36–40. doi: 10.1046/j.1526-4610.2000.00006.x.
    1. Afra J, Cecchini a P, Sándor PS, Schoenen J. Comparison of visual and auditory evoked cortical potentials in migraine patients between attacks. Clin Neurophysiol. 2000;111:1124–1129. doi: 10.1016/S1388-2457(00)00271-6.
    1. Ozkul Y, Bozlar S. Effects of fluoxetine on habituation of pattern reversal visually evoked potentials in migraine prophylaxis. Headache. 2002;42:582–587. doi: 10.1046/j.1526-4610.2002.02144.x.
    1. De Tommaso M, Sciruicchio V, Tota P, et al. Somatosensory evoked potentials in migraine. Funct Neurol. 1997;12:77–82.
    1. Sakuma K, Takeshima T, Ishizaki K, Nakashima K. Somatosensory evoked high-frequency oscillations in migraine patients. Clin Neurophysiol. 2004;115:1857–1862. doi: 10.1016/j.clinph.2004.03.011.
    1. Coppola G, Vandenheede M, Di Clemente L, et al. Somatosensory evoked high-frequency oscillations reflecting thalamo-cortical activity are decreased in migraine patients between attacks. Brain. 2005;128:98–103. doi: 10.1093/brain/awh334.
    1. Boćkowski L, Smigielska Kuzia J, Sobaniec W, Sendrowski K. Somatosensory evoked potentials in children with migraine with aura and without aura. Przegl Lek. 2010;67:688–691.
    1. Sand T, Zhitniy N, White LR, Stovner LJ. Brainstem auditory-evoked potential habituation and intensity-dependence related to serotonin metabolism in migraine: a longitudinal study. Clin Neurophysiol. 2008;119:1190–1200. doi: 10.1016/j.clinph.2008.01.007.
    1. Evers S, Bauer B, Suhr B, et al. Cognitive processing in primary headache: a study on event-related potentials. Neurology. 1997;48:108–113. doi: 10.1212/WNL.48.1.108.
    1. Evers S, Bauer B, Grotemeyer KH, et al. Event-related potentials (P300) in primary headache in childhood and adolescence. J Child Neurol. 1998;13:322–326. doi: 10.1177/088307389801300703.
    1. Kam JW, Mickleborough MJ, Eades C, Handy TC. Migraine and attention to visual events during mind wandering. Exp Brain Res. 2015;233:1503–1510. doi: 10.1007/s00221-015-4224-x.
    1. Tagliati M, Sabbadini M, Bernardi G, Silvestrini M. Multichannel visual evoked potentials in migraine. Electroencephalogr Clin Neurophysiol. 1995;96:1–5. doi: 10.1016/0013-4694(94)00211-3.
    1. Shibata K, Osawa M, Iwata M. Simultaneous recording of pattern reversal electroretinograms and visual evoked potentials in migraine. Cephalalgia. 1997;17:742–747. doi: 10.1046/j.1468-2982.1997.1707742.x.
    1. Nyrke T, Kangasniemi P, Lang AH. Transient asymmetries of steady-state visual evoked potentials in classic migraine. Headache. 1990;30:133–137. doi: 10.1111/j.1526-4610.1990.hed3003133.x.
    1. Logi F, Bonfiglio L, Orlandi G, et al. Asymmetric scalp distribution of pattern visual evoked potentials during interictal phases in migraine. Acta Neurol Scand. 2001;104:301–307. doi: 10.1034/j.1600-0404.2001.00329.x.
    1. Coppola G, Parisi V, Fiermonte G, et al. Asymmetric distribution of visual evoked potentials in patients with migraine with aura during the interictal phase. Eur J Ophthalmol. 2007;17:828–835. doi: 10.1177/112067210701700523.
    1. Schlake HP, Grotemeyer KH, Hofferberth B, et al. Brainstem auditory evoked potentials in migraine--evidence of increased side differences during the pain-free interval. Headache. 1990;30:129–132. doi: 10.1111/j.1526-4610.1990.hed3003129.x.
    1. Hamed SA, Youssef AH, Elattar AM. Assessment of cochlear and auditory pathways in patients with migraine. Am J Otolaryngol. 2012;33:385–394. doi: 10.1016/j.amjoto.2011.10.008.
    1. Bohotin V, Fumal A, Vandenheede M, et al. Effects of repetitive transcranial magnetic stimulation on visual evoked potentials in migraine. Brain. 2002;125:912–922. doi: 10.1093/brain/awf081.
    1. Chen WT, Lin YY, Fuh JL, et al. Sustained visual cortex hyperexcitability in migraine with persistent visual aura. Brain. 2011;134:2387–2395. doi: 10.1093/brain/awr157.
    1. Bednář M, Kubová Z, Kremláček J. Lack of visual evoked potentials amplitude decrement during prolonged reversal and motion stimulation in migraineurs. Clin Neurophysiol. 2014;125:1223–1230. doi: 10.1016/j.clinph.2013.10.050.
    1. Omland PM, Nilsen KB, Uglem M, et al. Visual evoked potentials in Interictal migraine: no confirmation of abnormal habituation. Headache. 2013;53:1071–1086. doi: 10.1111/head.12006.
    1. Omland Petter M., Uglem Martin, Hagen Knut, Linde Mattias, Tronvik Erling, Sand Trond. Visual evoked potentials in migraine: Is the “neurophysiological hallmark” concept still valid? Clinical Neurophysiology. 2016;127(1):810–816. doi: 10.1016/j.clinph.2014.12.035.
    1. Strigaro G, Cerino A, Falletta L, et al. Impaired visual inhibition in migraine with aura. Clin Neurophysiol. 2015;126:1988–1993. doi: 10.1016/j.clinph.2014.12.013.
    1. Coppola G, Bracaglia M, Di Lenola D et al (2015) Visual evoked potentials in subgroups of migraine with aura patients. J Headache Pain. 10.1186/s10194-015-0577-6
    1. Siniatchkin M, Sendacki M, Moeller F, et al. Abnormal changes of synaptic excitability in migraine with aura. Cereb cortex (New York) NY. 2012;1991(22):2207–2216.
    1. Ozkul Y, Uckardes A. Median nerve somatosensory evoked potentials in migraine. Eur J Neurol. 2002;9:227–232. doi: 10.1046/j.1468-1331.2002.00387.x.
    1. Wang W, Timsit-Berthier M, Schoenen J. Intensity dependence of auditory evoked potentials is pronounced in migraine: an indication of cortical potentiation and low serotonergic neurotransmission? Neurology. 1996;46:1404–1409. doi: 10.1212/WNL.46.5.1404.
    1. Aurora SK, Ahmad BK, Welch KM, et al. Transcranial magnetic stimulation confirms hyperexcitability of occipital cortex in migraine. Neurology. 1998;50:1111–1114. doi: 10.1212/WNL.50.4.1111.
    1. Mulleners WM, Chronicle EP, Palmer JE, et al. Visual cortex excitability in migraine with and without aura. Headache. 2001;41:565–572. doi: 10.1046/j.1526-4610.2001.041006565.x.
    1. Aurora SK, Cao Y, Bowyer SM, Welch KM. The occipital cortex is hyperexcitable in migraine: experimental evidence. Headache. 1999;39:469–476. doi: 10.1046/j.1526-4610.1999.3907469.x.
    1. Battelli L, Black KR, Wray SH. Transcranial magnetic stimulation of visual area V5 in migraine. Neurology. 2002;58:1066–1069. doi: 10.1212/WNL.58.7.1066.
    1. Aurora SK, KM a W, Al-Sayed F. The threshold for phosphenes is lower in migraine. Cephalalgia. 2003;23:258–263. doi: 10.1046/j.1468-2982.2003.00471.x.
    1. Young WB, Oshinsky ML, Shechter AL, et al. Consecutive transcranial magnetic stimulation: phosphene thresholds in migraineurs and controls. Headache. 2004;44:131–135. doi: 10.1111/j.1526-4610.2004.04028.x.
    1. 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;45:546–552. doi: 10.1111/j.1526-4610.2005.05108.x.
    1. Bohotin V, Fumal A, Vandenheede M, et al. Excitability of visual V1-V2 and motor cortices to single transcranial magnetic stimuli in migraine: a reappraisal using a figure-of-eight coil. Cephalalgia. 2003;23:264–270. doi: 10.1046/j.1468-2982.2003.00475.x.
    1. Afra J, Mascia A, Gérard P, et al. Interictal cortical excitability in migraine: a study using transcranial magnetic stimulation of motor and visual cortices. Ann Neurol. 1998;44:209–215. doi: 10.1002/ana.410440211.
    1. Brighina F, Piazza A, Daniele O, Fierro B. Modulation of visual cortical excitability in migraine with aura: effects of 1 Hz repetitive transcranial magnetic stimulation. Exp Brain Res. 2002;145:177–181. doi: 10.1007/s00221-002-1096-7.
    1. Gerwig M, Niehaus L, Kastrup O, et al. Visual cortex excitability in migraine evaluated by single and paired magnetic stimuli. Headache. 2005;45:1394–1399. doi: 10.1111/j.1526-4610.2005.00272.x.
    1. Chadaide Z, Arlt S, Antal A, et al. Transcranial direct current stimulation reveals inhibitory deficiency in migraine. Cephalalgia. 2007;27:833–839. doi: 10.1111/j.1468-2982.2007.01337.x.
    1. Naeije G, Fogang Y, Ligot N, Mavroudakis N. Occipital transcranial magnetic stimulation discriminates transient neurological symptoms of vascular origin from migraine aura without headache. Neurophysiol Clin Neurophysiol. 2017;47:269–274. doi: 10.1016/j.neucli.2017.05.093.
    1. Cosentino G, Fierro B, Vigneri S, et al. Impaired glutamatergic neurotransmission in migraine with aura? Evidence by an input-output curves transcranial magnetic stimulation study. Headache. 2011;51:726–733. doi: 10.1111/j.1526-4610.2011.01893.x.
    1. Brighina F, Giglia G, Scalia S, et al. Facilitatory effects of 1 Hz rTMS in motor cortex of patients affected by migraine with aura. Exp Brain Res. 2005;161:34–38. doi: 10.1007/s00221-004-2042-7.
    1. Palermo A, Fierro B, Giglia G, et al. Modulation of visual cortex excitability in migraine with aura: effects of valproate therapy. Neurosci Lett. 2009;467:26–29. doi: 10.1016/j.neulet.2009.09.054.
    1. Brighina F, Cosentino G, Vigneri S, et al. Abnormal facilitatory mechanisms in motor cortex of migraine with aura. Eur J Pain. 2011;15:928–935. doi: 10.1016/j.ejpain.2011.03.012.
    1. Conte A, Barbanti P, Frasca V, 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. doi: 10.1016/j.pain.2009.09.031.
    1. Pierelli Francesco, Iacovelli Elisa, Bracaglia Martina, Serrao Mariano, Coppola Gianluca. Abnormal sensorimotor plasticity in migraine without aura patients. Pain. 2013;154(9):1738–1742. doi: 10.1016/j.pain.2013.05.023.
    1. Schulte LH, May A. The migraine generator revisited: continuous scanning of the migraine cycle over 30 days and three spontaneous attacks. Brain. 2016;139:1987–1993. doi: 10.1093/brain/aww097.
    1. Perrotta Armando, Anastasio Maria Grazia, De Icco Roberto, Coppola Gianluca, Ambrosini Anna, Serrao Mariano, Sandrini Giorgio, Pierelli Francesco. Frequency-Dependent Habituation Deficit of the Nociceptive Blink Reflex in Aura With Migraine Headache. Can Migraine Aura Modulate Trigeminal Excitability? Headache: The Journal of Head and Face Pain. 2017;57(6):887–898. doi: 10.1111/head.13111.
    1. Di Clemente L, Coppola G, Magis D, et al. Nociceptive blink reflex and visual evoked potential habituations are correlated in migraine. Headache. 2005;45:1388–1393. doi: 10.1111/j.1526-4610.2005.00271.x.
    1. Katsarava Z, Giffin N, Diener H-C, Kaube H. Abnormal habituation of “nociceptive” blink reflex in migraine--evidence for increased excitability of trigeminal nociception. Cephalalgia. 2003;23:814–819. doi: 10.1046/j.1468-2982.2003.00591.x.
    1. Domitrz I, Kostera-Pruszczyk A, Kwieciñski H. A single-fibre EMG study of neuromuscular transmission in migraine patients. Cephalalgia. 2005;25:817–821. doi: 10.1111/j.1468-2982.2005.00961.x.
    1. Ambrosini A, de Noordhout AM, Alagona G, et al. Impairment of neuromuscular transmission in a subgroup of migraine patients. Neurosci Lett. 1999;276:201–203. doi: 10.1016/S0304-3940(99)00820-4.
    1. Ambrosini A, de Noordhout AM, Schoenen J. Neuromuscular transmission in migraine patients with prolonged aura. Acta Neurol Belg. 2001;101:166–170.
    1. Ambrosini A, Maertens de Noordhout A, Schoenen J. Neuromuscular transmission in migraine: a single-fiber EMG study in clinical subgroups. Neurology. 2001;56:1038–1043. doi: 10.1212/WNL.56.8.1038.
    1. Ambrosini A, Pierelli F, Schoenen J. Acetazolamide acts on neuromuscular transmission abnormalities found in some migraineurs. Cephalalgia. 2003;23:75–78. doi: 10.1046/j.1468-2982.2003.00409.x.
    1. Engel G, Ferris E, Romano J. Focal electroencephalographic changes during the scotomas of migraine. Am J Med Sci. 1945;209:650–657. doi: 10.1097/00000441-194505000-00013.
    1. Dow DJ, Whitty CW. Electroencephalographic changes in migraine; review of 51 cases. Lancet. 1947;2:52–54. doi: 10.1016/S0140-6736(47)90054-8.
    1. Lauritzen M, Trojaborg W, Olesen J. EEG during attacks of common and classical migraine. Cephalalgia. 1981;1:63–66. doi: 10.1111/j.1468-2982.1981.tb00010.x.
    1. Bowyer SM, Okada YC, Papuashvili N, et al. Analysis of MEG signals of spreading cortical depression with propagation constrained to a rectangular cortical strip. I Lissencephalic rabbit model Brain Res. 1999;843:71–78.
    1. MacLean C, Appenzeller O, Cordaro JT, Rhodes J. Flash evoked potentials in migraine. Headache. 1975;14:193–198. doi: 10.1111/j.1526-4610.1975.hed1404193.x.
    1. Chayasirisobhon S. Somatosensory evoked potentials in acute migraine with sensory aura. Clin Electroencephalogr. 1995;26:65–69. doi: 10.1177/155005949502600109.
    1. Chastan N, Lebas A, Legoff F, et al. Clinical and electroencephalographic abnormalities during the full duration of a sporadic hemiplegic migraine attack. Neurophysiol Clin Neurophysiol. 2016;46:307–311. doi: 10.1016/j.neucli.2016.03.004.
    1. WA CAMP, HG WOLFF. Studies on headache. Electroenceph-alographic abnormalities in patients with vascular headache of the migraine type. Arch Neurol. 1961;4:475–485. doi: 10.1001/archneur.1961.00450110005002.
    1. Gastaut H, Navarranne P, Simon y Canton L. EEG characteristics of migranous cerebral attacks of a deficitory type (hemiplegic migrane) Electroencephalogr. Clin Neurophysiol. 1967;23:381.
    1. Heyck H. Varieties of hemiplegic migraine. Headache. 1973;12:135–142. doi: 10.1111/j.1526-4610.1973.hed1204135.x.
    1. Marchioni E, Galimberti CA, Soragna D, et al. Familial hemiplegic migraine versus migraine with prolonged aura: an uncertain diagnosis in a family report. Neurology. 1995;45:33–37. doi: 10.1212/WNL.45.1.33.
    1. Kramer U, Lerman-Sagi T, Margalith D, Harel S. A family with hemiplegic migraine and focal seizures. Eur J Paediatr Neurol. 1997;1:35–38. doi: 10.1016/S1090-3798(97)80008-6.
    1. Varkey B, Varkey L. EEG in hemiplegic migraine. Neurol India. 2004;52:134.
    1. Chan Y-C, Burgunder J-M, Wilder-Smith E, et al. Electroencephalographic changes and seizures in familial hemiplegic migraine patients with the CACNA1A gene S218L mutation. J Clin Neurosci. 2008;15:891–894. doi: 10.1016/j.jocn.2007.01.013.
    1. Merwick A, Fernandez D, McNamara B, Harrington H. Case reports 2013:bcr2013009750-bcr2013009750. 2013. Acute encephalopathy in familial hemiplegic migraine with ATP1A2 mutation.
    1. Schwarz G, Anzalone N, Baldoli C, et al. Pediatric sporadic hemiplegic migraine (ATP1A2 gene): a case report and brief literature review. Neurol Sci. 2018;39:69–71. doi: 10.1007/s10072-018-3405-3.
    1. Murphy OC, Merwick A, OʼMahony O, et al. Familial hemiplegic migraine with asymmetric encephalopathy secondary to ATP1A2 mutation. J Clin Neurophysiol. 2018;35:e3–e7. doi: 10.1097/WNP.0000000000000387.
    1. Indelicato E, Nachbauer W, Eigentler A, et al. Ten years of follow-up in a large family with familial hemiplegic migraine type 1: clinical course and implications for treatment. Cephalalgia. 2018;38:1167–1176. doi: 10.1177/0333102417715229.
    1. Bickerstaff ER. Impairment of consciousness in migraine. Lancet (London, England) 1961;2:1057–1059. doi: 10.1016/S0140-6736(61)92538-7.
    1. Lee CH, Lance JW. Migraine stupor. Headache. 1977;17:32–38. doi: 10.1111/j.1526-4610.1977.hed1701032.x.
    1. Swanson JW, Vick NA. Basilar artery migraine 12 patients, with an attack recorded electroencephalographically. Neurology. 1978;28:782–786. doi: 10.1212/WNL.28.8.782.
    1. Camfield PR, Metrakos K, Andermann F. Basilar migraine, seizures, and severe epileptiform EEG abnormalities. Neurology. 1978;28:584–588. doi: 10.1212/WNL.28.6.584.
    1. Walser H, Isler H. Frontal intermittent rhythmic delta activity. Impairment of consciousness and migraine. Headache. 1982;22:74–80. doi: 10.1111/j.1526-4610.1982.hed2202074.x.
    1. Parrino L, Pietrini V, Spaggiari MC, Terzano MG. Acute confusional migraine attacks resolved by sleep: lack of significant abnormalities in post-ictal polysomnograms. Cephalalgia. 1986;6:95–100. doi: 10.1046/j.1468-2982.1986.0602095.x.
    1. Ganji S. Basilar artery migraine: EEG and evoked potential patterns during acute stage. Headache. 1986;26:220–223. doi: 10.1111/j.1526-4610.1986.hed2605220.x.
    1. Pietrini V, Terzano MG, D’Andrea G, et al. Acute confusional migraine: clinical and electroencephalographic aspects. Cephalalgia. 1987;7:29–37. doi: 10.1046/j.1468-2982.1987.0701029.x.
    1. Haan J, Ferrari MD, Brouwer OF Acute confusional migraine. Case report and review of literature. Clin Neurol Neurosurg. 1988;90:275–278. doi: 10.1016/0303-8467(88)90037-6.
    1. Muellbacher W, Mamoli B. Prolonged impaired consciousness in basilar artery migraine. Headache. 1994;34:282–285. doi: 10.1111/j.1526-4610.1994.hed3405282.x.
    1. Ramelli GP, Sturzenegger M, Donati F, Karbowski K. EEG findings during basilar migraine attacks in children. Electroencephalogr Clin Neurophysiol. 1998;107:374–378. doi: 10.1016/S0013-4694(98)00094-7.
    1. Hansen JM, Bolla M, Magis D, et al. Habituation of evoked responses is greater in patients with familial hemiplegic migraine than in controls: a contrast with the common forms of migraine. Eur J Neurol. 2011;18:478–485. doi: 10.1111/j.1468-1331.2010.03190.x.
    1. van der Kamp W, MaassenVanDenBrink A, Ferrari MD, van Dijk JG. Interictal cortical excitability to magnetic stimulation in familial hemiplegic migraine. Neurology. 1997;48:1462–1464. doi: 10.1212/WNL.48.5.1462.
    1. Bolay H, Reuter U, Dunn AK, et al. Intrinsic brain activity triggers trigeminal meningeal afferents in a migraine model. Nat Med. 2002;8:136–142. doi: 10.1038/nm0202-136.
    1. Lambert GA, Truong L, Zagami AS. Effect of cortical spreading depression on basal and evoked traffic in the trigeminovascular sensory system. Cephalalgia. 2011;31:1439–1451. doi: 10.1177/0333102411422383.
    1. Goadsby PJ, 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. 2012;32:3–5. doi: 10.1177/0333102411430267.
    1. Hougaard A, Amin FM, Christensen CE, et al. Increased brainstem perfusion, but no blood-brain barrier disruption, during attacks of migraine with aura. Brain. 2017;140:1633–1642. doi: 10.1093/brain/awx089.
    1. Weiller C, May A, Limmroth V, et al. Brain stem activation in spontaneous human migraine attacks. Nat Med. 1995;1:658–660. doi: 10.1038/nm0795-658.
    1. Bahra A, Matharu MS, Buchel C, et al. Brainstem activation specific to migraine headache. Lancet. 2001;357:1016–1017. doi: 10.1016/S0140-6736(00)04250-1.
    1. Afridi SK, Giffin NJ, Kaube H, et al. A positron emission tomographic study in spontaneous migraine. Arch Neurol. 2005;62:1270–1275. doi: 10.1001/archneur.62.8.1270.
    1. Marciszewski KK, Meylakh N, Di Pietro F, et al. Altered brainstem anatomy in migraine. Cephalalgia. 2018;38:476–486. doi: 10.1177/0333102417694884.
    1. Hadjikhani N, Ward N, Boshyan J, et al. The missing link: enhanced functional connectivity between amygdala and visceroceptive cortex in migraine. Cephalalgia. 2013;33:1264–1268. doi: 10.1177/0333102413490344.
    1. DaSilva AFM, Granziera C, Tuch DS, et al. Interictal alterations of the trigeminal somatosensory pathway and periaqueductal gray matter in migraine. Neuroreport. 2007;18:301–305. doi: 10.1097/WNR.0b013e32801776bb.
    1. Granziera C, Daducci A, Romascano D, et al. Structural abnormalities in the thalamus of migraineurs with aura: a multiparametric study at 3 T. Hum Brain Mapp. 2014;35:1461–1468. doi: 10.1002/hbm.22266.
    1. Granziera C, DaSilva AFM, Snyder J, et al. Anatomical alterations of the visual motion processing network in migraine with and without aura. PLoS Med. 2006;3:e402. doi: 10.1371/journal.pmed.0030402.
    1. Hougaard A, Amin FM, Larsson HBW, et al. Increased intrinsic brain connectivity between pons and somatosensory cortex during attacks of migraine with aura. Hum Brain Mapp. 2017;38:2635–2642. doi: 10.1002/hbm.23548.
    1. Arngrim N, Hougaard A, Ahmadi K, et al. Heterogenous migraine aura symptoms correlate with visual cortex functional magnetic resonance imaging responses. Ann Neurol. 2017;82:925–939. doi: 10.1002/ana.25096.
    1. Llinás R, Urbano FJ, Leznik E, et al. Rhythmic and dysrhythmic thalamocortical dynamics: GABA systems and the edge effect. Trends Neurosci. 2005;28:325–333. doi: 10.1016/j.tins.2005.04.006.
    1. Walton KD, Llinás RR (2010) In: Kruger L, Light AR (eds) Translational pain research: from mouse to man. CRC Press Chapter 13
    1. Datta R, Aguirre GK, Hu S, et al. Interictal cortical hyperresponsiveness in migraine is directly related to the presence of aura. Cephalalgia. 2013;33:365–374. doi: 10.1177/0333102412474503.
    1. Coppola G, Tinelli E, Lepre C, et al. Dynamic changes in thalamic microstructure of migraine without aura patients: a diffusion tensor magnetic resonance imaging study. Eur J Neurol. 2014;21:287–e13. doi: 10.1111/ene.12296.
    1. Hauge AW, Asghar MS, Schytz HW, et al. Effects of tonabersat on migraine with aura: a randomised, double-blind, placebo-controlled crossover study. Lancet Neurol. 2009;8:718–723. doi: 10.1016/S1474-4422(09)70135-8.
    1. Pellacani S, Sicca F, Di Lorenzo C, et al. The revolution in migraine genetics: from aching channels disorders to a next-generation medicine. Front Cell Neurosci. 2016;10:156. doi: 10.3389/fncel.2016.00156.
    1. Woods R, Iacoboni M, Mazziotta JC. Brief report: bilateral spreading cerebral hypoperfusion during spontaneous migraine headache. N Engl J Med. 1994;331:1689–1692. doi: 10.1056/NEJM199412223312505.
    1. Maniyar F, Sprenger T, Monteith T, et al. Brain activations in the premonitory phase of nitroglycerin-triggered migraine attacks. Brain. 2014;137:232–241. doi: 10.1093/brain/awt320.
    1. Tepe N, Filiz A, Dilekoz E, et al. The thalamic reticular nucleus is activated by cortical spreading depression in freely moving rats: prevention by acute valproate administration. Eur J Neurosci. 2015;41:120–128. doi: 10.1111/ejn.12753.

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