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Current Medicinal Chemistry

Author(s): Erica Marucco, Marco Lisicki and Delphine Magis*

DOI: 10.2174/0929867325666180627130811

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Electrophysiological Characteristics of the Migraine Brain: Current Knowledge and Perspectives

Page: [6222 - 6235] Pages: 14

  • * (Excluding Mailing and Handling)

Abstract

Background: Despite pain being its most prominent feature, migraine is primarily a disorder of sensory processing. Electrophysiology-based research in the field has consistently developed over the last fifty years.

Objective: To summarize the current knowledge on the electrophysiological characteristics of the migraine brain, and discuss perspectives.

Methods: We critically reviewed the literature on the topic to present and discuss articles selected on the basis of their significance and/or novelty.

Results: Physiologic fluctuations within time, between-subject differences, and methodological issues account as major limitations of electrophysiological research in migraine. Nonetheless, several abnormalities revealed through different approaches have been described in the literature. Altogether, these results are compatible with an abnormal state of sensory processing.

Perspectives: The greatest contribution of electrophysiological testing in the future will most probably be the characterization of sub-groups of migraine patients sharing specific electrophysiological traits. This should serve as strategy towards personalized migraine treatment. Incorporation of novel methods of analysis would be worthwhile.

Keywords: Migraine, electrophysiology, electroencephalography, magnetoencephalography, evoked potentials, blink reflex.

[1]
Goadsby, P.J.; Holland, P.R.; Martins-Oliveira, M.; Hoffmann, J.; Schankin, C.; Akerman, S. Pathophysiology of migraine: a disorder of sensory processing. Physiol. Rev., 2017, 97(2), 553-622.
[http://dx.doi.org/10.1152/physrev.00034.2015] [PMID: 28179394]
[2]
Schulte, L.H.; May, A. The migraine generator revisited: continuous scanning of the migraine cycle over 30 days and three spontaneous attacks. Brain, 2016, 139(Pt 7), 1987-1993.
[http://dx.doi.org/10.1093/brain/aww097] [PMID: 27190019]
[3]
Judit, A.; Sándor, P.S.; Schoenen, J. Habituation of visual and intensity dependence of auditory evoked cortical potentials tends to normalize just before and during the migraine attack. Cephalalgia, 2000, 20(8), 714-719.
[http://dx.doi.org/10.1111/j.1468-2982.2000.00122.x] [PMID: 11167900]
[4]
Coppola, G.; Iacovelli, E.; Bracaglia, M.; Serrao, M.; Di Lorenzo, C.; Pierelli, F. Electrophysiological correlates of episodic migraine chronification: evidence for thalamic involvement. J. Headache Pain, 2013, 14, 76.
[http://dx.doi.org/10.1186/1129-2377-14-76] [PMID: 24016158]
[5]
Home-Pubmed-NCBI. Available at: www.ncbi.nlm.nih. gov/pubmed/(Accessed at: October 11, 2017.
[6]
Eising, E.; Huisman, S.M.H.; Mahfouz, A.; Vijfhuizen, L.S.; Anttila, V.; Winsvold, B.S.; Kurth, T.; Ikram, M.A.; Freilinger, T.; Kaprio, J.; Boomsma, D.I.; van Duijn, C.M.; Järvelin, M.R.; Zwart, J.A.; Quaye, L.; Strachan, D.P.; Kubisch, C.; Dichgans, M.; Davey Smith, G.; Stefansson, K.; Palotie, A.; Chasman, D.I.; Ferrari, M.D.; Terwindt, G.M.; de Vries, B.; Nyholt, D.R.; Lelieveldt, B.P.F.; van den Maagdenberg, A.M.J.M.; Reinders, M.J.T. Gene co-expression analysis identifies brain regions and cell types involved in migraine pathophysiology: a GWAS-based study using the allen human brain atlas. Hum. Genet., 2016, 135(4), 425-439.
[http://dx.doi.org/10.1007/s00439-016-1638-x] [PMID: 26899160]
[7]
Hougaard, A.; Amin, F.M.; Ashina, M. Migraine and structural abnormalities in the brain. Curr. Opin. Neurol., 2014, 27(3), 309-314.
[http://dx.doi.org/10.1097/WCO.0000000000000086] [PMID: 24751961]
[8]
Magis, D.; Lisicki, M.; Coppola, G. Highlights in migraine electrophysiology: are controversies just reflecting disease heterogeneity? Curr. Opin. Neurol., 2016, 29(3), 320-330.
[http://dx.doi.org/10.1097/WCO.0000000000000335] [PMID: 27120104]
[9]
Lisicki, M.; Ruiz-Romagnoli, E.; Piedrabuena, R. Migraine triggers and habituation of visual evoked potentials. Cephalalgia, 2018, 38(5), 988-992.
[http://dx.doi.org/10.1177/0333102417720217] [PMID: 28691517]
[10]
Zameel Cader, M. The molecular pathogenesis of migraine: new developments and opportunities. Hum. Mol. Genet., 2013, 22(R1), R39-R44.
[http://dx.doi.org/10.1093/hmg/ddt364] [PMID: 23922230]
[11]
Lisicki, M.; D’Ostilio, K.; Erpicum, M.; Schoenen, J.; Magis, D. Sunlight irradiance and habituation of visual evoked potentials in migraine: The environment makes its mark. Cephalalgia, 2018, 38(7), 1351-1360.
[http://dx.doi.org/ 10.1177/0333102417730128] [PMID: 28856911]
[12]
Lisicki, M.; Ruiz-Romagnoli, E.; D’Ostilio, K.; Piedrabuena, R.; Giobellina, R.; Schoenen, J.; Magis, D. Familial history of migraine influences habituation of visual evoked potentials. Cephalalgia, 2017, 37(11), 1082-1087.
[http://dx.doi.org/10.1177/0333102416673207] [PMID: 27821640]
[13]
Di Clemente, L.; Coppola, G.; Magis, D.; Fumal, A.; De Pasqua, V.; Di Piero, V.; Schoenen, J. Interictal habituation deficit of the nociceptive blink reflex: an endophenotypic marker for presymptomatic migraine? Brain, 2007, 130(Pt 3), 765-770.
[http://dx.doi.org/10.1093/brain/awl351] [PMID: 17251239]
[14]
Siniatchkin, M.; Kropp, P.; Neumann, M.; Gerber, W.; Stephani, U. Intensity dependence of auditory evoked cortical potentials in migraine families. Pain, 2000, 85(1-2), 247-254.
[http://dx.doi.org/10.1016/S0304-3959(99)00271-7] [PMID: 10692625]
[15]
Buonfiglio, M.; Toscano, M.; Puledda, F.; Avanzini, G.; Di Clemente, L.; Di Sabato, F.; Di Piero, V. Lack of habituation of evoked visual potentials in analytic information processing style: evidence in healthy subjects. Neurol. Sci., 2015, 36(3), 391-395.
[http://dx.doi.org/10.1007/s10072-014-1962-7] [PMID: 25260654]
[16]
Sand, T. We were blind, so now we can see: the EP/ERP story in migraine. Clin. Neurophysiol., 2014, 125(3), 433-434.
[http://dx.doi.org/10.1016/j.clinph.2013.10.006] [PMID: 24210998]
[17]
Porcaro, C.; Ostwald, D.; Hadjipapas, A.; Barnes, G.R.; Bagshaw, A.P. The relationship between the visual evoked potential and the gamma band investigated by blind and semi-blind methods. Neuroimage, 2011, 56(3), 1059-1071.
[http://dx.doi.org/10.1016/j.neuroimage.2011.03.008] [PMID: 21396460]
[18]
Makeig, S.; Debener, S.; Onton, J.; Delorme, A. Mining event-related brain dynamics. Trends Cogn. Sci. (Regul. Ed.),, 2004, 8(5), 204-210.
[http://dx.doi.org/10.1016/j.tics.2004.03.008] [PMID: 15120678]
[19]
Sandrini, G.; Friberg, L.; Coppola, G.; Jänig, W.; Jensen, R.; Kruit, M.; Rossi, P.; Russell, D.; Sanchez del Rìo, M.; Sand, T.; Schoenen, J. European Federation of Neurological Sciences In: Neurophysiological tests and neuroimaging procedures in non-acute headache (2nd edition). Eur J Neurol,; , 2011; 18, pp. (3)373-381.
[http://dx.doi.org/10.1111/j.1468-1331.2010.03212.x] [PMID: 20868464]
[20]
Viticchi, G.; Falsetti, L.; Silvestrini, M.; Luzzi, S.; Provinciali, L.; Bartolini, M. The real usefulness and indication for migraine diagnosis of neurophysiologic evaluation. Neurol. Sci., 2012, 33(Suppl. 1), S161-S163.
[http://dx.doi.org/10.1007/s10072-012-1074-1] [PMID: 22644194]
[21]
Sand, T. EEG in migraine: a review of the literature. Funct. Neurol., 1991, 6(1), 7-22.
[PMID: 2055554]
[22]
Bjørk, M.H.; Stovner, L.J.; Nilsen, B.M.; Stjern, M.; Hagen, K.; Sand, T. The occipital alpha rhythm related to the “migraine cycle” and headache burden: a blinded, controlled longitudinal study. Clin. Neurophysiol., 2009, 120(3), 464-471.
[http://dx.doi.org/10.1016/j.clinph.2008.11.018] [PMID: 19157973]
[23]
Bjørk, M.H.; Stovner, L.J.; Engstrøm, M.; Stjern, M.; Hagen, K.; Sand, T. Interictal quantitative EEG in migraine: a blinded controlled study. J. Headache Pain, 2009, 10(5), 331-339.
[http://dx.doi.org/10.1007/s10194-009-0140-4] [PMID: 19705061]
[24]
Bjørk, M.; Sand, T. Quantitative EEG power and asymmetry increase 36 h before a migraine attack. Cephalalgia, 2008, 28(9), 960-968.
[http://dx.doi.org/10.1111/j.1468-2982.2008.01638.x] [PMID: 18624805]
[25]
Clemens, B.; Bánk, J.; Piros, P.; Bessenyei, M.; Veto, S.; Tóth, M.; Kondákor, I. Three-dimensional localization of abnormal EEG activity in migraine: a low resolution electromagnetic tomography (LORETA) study of migraine patients in the pain-free interval. Brain Topogr., 2008, 21(1), 36-42.
[http://dx.doi.org/10.1007/s10548-008-0061-6] [PMID: 18679787]
[26]
Mo, J.; Maizels, M.; Ding, M.; Ahn, A.H. Does throbbing pain have a brain signature? Pain, 2013, 154(7), 1150-1155.
[http://dx.doi.org/10.1016/j.pain.2013.02.013] [PMID: 23557747]
[27]
Walker, J.E. QEEG-guided neurofeedback for recurrent migraine headaches. Clin. EEG Neurosci., 2011, 42(1), 59-61.
[http://dx.doi.org/10.1177/155005941104200112] [PMID: 21309444]
[28]
Norcia, A.M.; Appelbaum, L.G.; Ales, J.M.; Cottereau, B.R.; Rossion, B. The steady-state visual evoked potential in vision research: A review. J. Vis., 2015, 15(6), 4.
[http://dx.doi.org/10.1167/15.6.4] [PMID: 26024451]
[29]
Golla, F.L.; Winter, A.L. Analysis of cerebral responses to flicker in patients complaining of episodic headache. Electroencephalogr. Clin. Neurophysiol., 1959, 11(3), 539-549.
[http://dx.doi.org/10.1016/0013-4694(59)90052-5] [PMID: 13663826]
[30]
Bjørk, M.; Hagen, K.; Stovner, Lj.; Sand, T. Photic EEG-driving responses related to ictal phases and trigger sensitivity in migraine: a longitudinal, controlled study. Cephalalgia, 2011, 31(4), 444-455.
[http://dx.doi.org/10.1177/0333102410385582] [PMID: 21098109]
[31]
Chorlton, P.; Kane, N. Investigation of the cerebral response to flicker stimulation in patients with headache. Clin. Electroencephalogr., 2000, 31(2), 83-87.
[http://dx.doi.org/10.1177/155005940003100206] [PMID: 10840630]
[32]
Fogang, Y.; Gérard, P.; De Pasqua, V.; Pepin, J.L.; Ndiaye, M.; Magis, D.; Schoenen, J. Analysis and clinical correlates of 20 Hz photic driving on routine EEG in migraine. Acta Neurol. Belg., 2015, 115(1), 39-45.
[http://dx.doi.org/10.1007/s13760-014-0309-8] [PMID: 24858629]
[33]
Gantenbein, A.R.; Sandor, P.S.; Goadsby, P.J.; Kaube, H. Chirp stimulation: H-response short and dynamic. Cephalalgia, 2014, 34(7), 554-558.
[http://dx.doi.org/10.1177/0333102413517777] [PMID: 24391117]
[34]
de Tommaso, M.; Stramaglia, S.; Marinazzo, D.; Trotta, G.; Pellicoro, M. Functional and effective connectivity in EEG alpha and beta bands during intermittent flash stimulation in migraine with and without aura. Cephalalgia, 2013, 33(11), 938-947.
[http://dx.doi.org/10.1177/0333102413477741] [PMID: 23439574]
[35]
Drummond, P.D. A quantitative assessment of photophobia in migraine and tension headache. Headache, 1986, 26(9), 465-469.
[http://dx.doi.org/10.1111/j.1526-4610.1986.hed2609465.x] [PMID: 3781834]
[36]
Magis, D.; Ambrosini, A.; Bendtsen, L.; Ertas, M.; Kaube, H.; Schoenen, J. Evaluation and proposal for optimalization of neurophysiological tests in migraine: part 1--electrophysiological tests. Cephalalgia, 2007, 27(12), 1323-1338.
[http://dx.doi.org/10.1111/j.1468-2982.2007.01440.x] [PMID: 17970766]
[37]
Schoenen, J.; Wang, W.; Albert, A.; Delwaide, P.J. Potentiation instead of habituation characterizes visual evoked potentials in migraine patients between attacks. Eur. J. Neurol., 1995, 2(2), 115-122.
[http://dx.doi.org/10.1111/j.1468-1331.1995.tb00103.x] [PMID: 24283611]
[38]
Omland, P.M.; Uglem, M.; Hagen, K.; Linde, M.; Tronvik, E.; Sand, T. Visual evoked potentials in migraine: Is the “neurophysiological hallmark” concept still valid? Clin. Neurophysiol., 2016, 127(1), 810-816.
[http://dx.doi.org/10.1016/j.clinph.2014.12.035] [PMID: 26093935]
[39]
Omland, P.M.; Nilsen, K.B.; Uglem, M.; Gravdahl, G.; Linde, M.; Hagen, K.; Sand, T. Visual evoked potentials in interictal migraine: no confirmation of abnormal habituation. Headache, 2013, 53(7), 1071-1086.
[http://dx.doi.org/10.1111/head.12006] [PMID: 23298223]
[40]
Sand, T.; Zhitniy, N.; White, L.R.; Stovner, L.J. Visual evoked potential latency, amplitude and habituation in migraine: a longitudinal study. Clin. Neurophysiol., 2008, 119(5), 1020-1027.
[http://dx.doi.org/10.1016/j.clinph.2008.01.009] [PMID: 18308628]
[41]
Coppola, G.; Bracaglia, M.; Di Lenola, D.; Di Lorenzo, C.; Serrao, M.; Parisi, V.; Di Renzo, A.; Martelli, F.; Fadda, A.; Schoenen, J.; Pierelli, F. Visual evoked potentials in subgroups of migraine with aura patients. J. Headache Pain, 2015, 16, 92.
[http://dx.doi.org/10.1186/s10194-015-0577-6] [PMID: 26527348]
[42]
Schoenen, J. Is chronic migraine a never-ending migraine attack? Pain, 2011, 152(2), 239-240.
[http://dx.doi.org/10.1016/j.pain.2010.12.002] [PMID: 21168270]
[43]
Bohotin, V.; Fumal, A.; Vandenheede, M.; Gérard, P.; Bohotin, C.; Maertens de Noordhout, A.; Schoenen, J. Effects of repetitive transcranial magnetic stimulation on visual evoked potentials in migraine. Brain, 2002, 125(Pt 4), 912-922.
[http://dx.doi.org/10.1093/brain/awf081] [PMID: 11912123]
[44]
Viganò, A.; D’Elia, T.S.; Sava, S.L.; Auvé, M.; De Pasqua, V.; Colosimo, A.; Di Piero, V.; Schoenen, J.; Magis, D. Transcranial Direct Current Stimulation (tDCS) of the visual cortex: a proof-of-concept study based on interictal electrophysiological abnormalities in migraine. J. Headache Pain, 2013, 14, 23.
[http://dx.doi.org/10.1186/1129-2377-14-23] [PMID: 23566101]
[45]
Sannita, W.G.; Lopez, L.; Piras, C.; Di Bon, G. Scalp-recorded oscillatory potentials evoked by transient pattern-reversal visual stimulation in man. Electroencephalogr. Clin. Neurophysiol., 1995, 96(3), 206-218.
[http://dx.doi.org/10.1016/0168-5597(94)00285-M] [PMID: 7750446]
[46]
Coppola, G.; Ambrosini, A.; Di Clemente, L.; Magis, D.; Fumal, A.; Gérard, P.; Pierelli, F.; Schoenen, J. Interictal abnormalities of gamma band activity in visual evoked responses in migraine: an indication of thalamocortical dysrhythmia? Cephalalgia, 2007, 27(12), 1360-1367.
[http://dx.doi.org/10.1111/j.1468-2982.2007.01466.x] [PMID: 17986271]
[47]
Llinás, R.R.; Ribary, U.; Jeanmonod, D.; Kronberg, E.; Mitra, P.P. Thalamocortical dysrhythmia: A neurological and neuropsychiatric syndrome characterized by magnetoencephalography. Proc. Natl. Acad. Sci. USA, 1999, 96(26), 15222-15227.
[http://dx.doi.org/10.1073/pnas.96.26.15222] [PMID: 10611366]
[48]
Gantenbein, A.R.; Sandor, P.S.; Fritschy, J.; Turner, R.; Goadsby, P.J.; Kaube, H. Sensory information processing may be neuroenergetically more demanding in migraine patients. Neuroreport, 2013, 24(4), 202-205.
[http://dx.doi.org/10.1097/WNR.0b013e32835eba81] [PMID: 23381352]
[49]
Vanagaite Vmgen, J.; Pareja, J.; White, L.R.; Støren, O.; Stovner, L.J. Phonophobia in migraine. Cephalalgia, 1998, 18(5), 243-249.
[http://dx.doi.org/ 10.1111/j.1468-2982.1998.1805243.x] [PMID: 9673802]
[50]
Ashkenazi, A.; Mushtaq, A.; Yang, I.; Oshinsky, M.L. Ictal and interictal phonophobia in migraine-a quantitative controlled study. Cephalalgia, 2009, 29(10), 1042-1048.
[http://dx.doi.org/10.1111/j.1468-2982.2008.01834.x] [PMID: 19735532]
[51]
Headache Classification Committee of the International Headache Society (IHS). The International Classification of Headache Disorders, 3rd edition (beta version). Cephalalgia, 2013, 33(9), 629-808.
[http://dx.doi.org/10.1177/0333102413485658] [PMID: 23771276]
[52]
Sand, T.; Zhitniy, N.; White, L.R.; Stovner, L.J. Brainstem auditory-evoked potential habituation and intensity-dependence related to serotonin metabolism in migraine: a longitudinal study. Clin. Neurophysiol., 2008, 119(5), 1190-1200.
[http://dx.doi.org/10.1016/j.clinph.2008.01.007] [PMID: 18316245]
[53]
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(5), 1404-1409.
[http://dx.doi.org/10.1212/WNL.46.5.1404] [PMID: 8628490]
[54]
Ambrosini, A.; Rossi, P.; De Pasqua, V.; Pierelli, F.; Schoenen, J. Lack of habituation causes high intensity dependence of auditory evoked cortical potentials in migraine. Brain, 2003, 126(Pt 9), 2009-2015.
[http://dx.doi.org/10.1093/brain/awg206] [PMID: 12821515]
[55]
Sand, T.; Vingen, J.V. Visual, long-latency auditory and brainstem auditory evoked potentials in migraine: relation to pattern size, stimulus intensity, sound and light discomfort thresholds and pre-attack state. Cephalalgia, 2000, 20(9), 804-820.
[http://dx.doi.org/10.1046/j.1468-2982.2000.00098.x] [PMID: 11167910]
[56]
Ambrosini, A.; Kisialiou, A.; Schoenen, J. Visual and auditory cortical evoked potentials in interictal episodic migraine: An audit on 624 patients from three centres. Response to the letter by Omland et al. Cephalalgia, 2017, 37(12), 1209-1210.
[http://dx.doi.org/10.1177/0333102416680616] [PMID: 27872339]
[57]
Stolte, B.; Holle, D.; Naegel, S.; Diener, H.C.; Obermann, M. Vestibular migraine. Cephalalgia, 2015, 35(3), 262-270.
[http://dx.doi.org/10.1177/0333102414535113] [PMID: 24847169]
[58]
Allena, M.; Magis, D.; De Pasqua, V.; Schoenen, J.; Bisdorff, A.R. The vestibulo-collic reflex is abnormal in migraine. Cephalalgia, 2007, 27(10), 1150-1155.
[http://dx.doi.org/10.1111/j.1468-2982.2007.01414.x] [PMID: 17784856]
[59]
Zaleski, A.; Bogle, J.; Starling, A.; Zapala, D.A.; Davis, L.; Wester, M.; Cevette, M. Vestibular evoked myogenic potentials in patients with vestibular migraine. Otol. Neurotol., 2015, 36(2), 295-302.
[http://dx.doi.org/10.1097/MAO.0000000000000665] [PMID: 25415464]
[60]
Kim, C-H.; Jang, M-U.; Choi, H-C.; Sohn, J.H. Subclinical vestibular dysfunction in migraine patients: a preliminary study of ocular and rectified cervical vestibular evoked myogenic potentials. J. Headache Pain, 2015, 16, 93.
[http://dx.doi.org/10.1186/s10194-015-0578-5] [PMID: 26527349]
[61]
Zanchin, G.; Dainese, F.; Mainardi, F.; Mampreso, E.; Perin, C.; Maggioni, F. Osmophobia in primary headaches. J. Headache Pain, 2005, 6(4), 213-215.
[http://dx.doi.org/10.1007/s10194-005-0188-8] [PMID: 16362667]
[62]
Fornazieri, M.A.; Neto, A.R.; de Rezende Pinna, F.; Gobbi Porto, F.H.; de Lima Navarro, P.; Voegels, R.L.; Doty, R.L. Olfactory symptoms reported by migraineurs with and without auras. Headache, 2016, 56(10), 1608-1616.
[http://dx.doi.org/10.1111/head.12973] [PMID: 27779326]
[63]
Demarquay, G.; Royet, J.P.; Mick, G.; Ryvlin, P. Olfactory hypersensitivity in migraineurs: a H(2)(15)O-PET study. Cephalalgia, 2008, 28(10), 1069-1080.
[http://dx.doi.org/10.1111/j.1468-2982.2008.01672.x] [PMID: 18727640]
[64]
Stankewitz, A.; Schulz, E.; May, A. Neuronal correlates of impaired habituation in response to repeated trigemino-nociceptive but not to olfactory input in migraineurs: an fMRI study. Cephalalgia, 2013, 33(4), 256-265.
[http://dx.doi.org/10.1177/0333102412470215] [PMID: 23230239]
[65]
Grosser, K.; Oelkers, R.; Hummel, T.; Geisslinger, G.; Brune, K.; Kobal, G.; Lötsch, J. Olfactory and trigeminal event-related potentials in migraine. Cephalalgia, 2000, 20(7), 621-631.
[http://dx.doi.org/10.1111/j.1468-2982.2000.00094.x] [PMID: 11128819]
[66]
Ozkul, Y.; Uckardes, A. Median nerve somatosensory evoked potentials in migraine. Eur. J. Neurol., 2002, 9(3), 227-232.
[http://dx.doi.org/10.1046/j.1468-1331.2002.00387.x] [PMID: 11985630]
[67]
Coppola, G.; Currà, A.; Di Lorenzo, C.; Parisi, V.; Gorini, M.; Sava, S.L.; Schoenen, J.; Pierelli, F. Abnormal cortical responses to somatosensory stimulation in medication-overuse headache. BMC Neurol., 2010, 10, 126.
[http://dx.doi.org/10.1186/1471-2377-10-126] [PMID: 21192822]
[68]
Coppola, G.; Vandenheede, M.; Di Clemente, L.; Ambrosini, A.; Fumal, A.; De Pasqua, V.; Schoenen, J. Somatosensory evoked high-frequency oscillations reflecting thalamo-cortical activity are decreased in migraine patients between attacks. Brain, 2005, 128(Pt 1), 98-103.
[http://dx.doi.org/10.1093/brain/awh334] [PMID: 15563513]
[69]
Sakuma, K.; Takeshima, T.; Ishizaki, K. Somatosensory evoked high-frequency oscillations in migraine patients. Clin. Neurophysiol., 2004, 115(8), 1857-1862.
[http://dx.doi.org/10.1016/j.clinph.2004.03.011] [PMID: 15261864]
[70]
Kalita, J.; Bhoi, S.K.; Misra, U.K. Is lack of habituation of evoked potential a biological marker of migraine? Clin. J. Pain, 2014, 30(8), 724-729.
[http://dx.doi.org/10.1097/AJP.0000000000000034] [PMID: 24281284]
[71]
Restuccia, D.; Vollono, C.; Virdis, D.; del Piero, I.; Martucci, L.; Zanini, S. Patterns of habituation and clinical fluctuations in migraine. Cephalalgia, 2014, 34(3), 201-210.
[http://dx.doi.org/10.1177/0333102413508241] [PMID: 24121287]
[72]
Coppola, G.; Bracaglia, M.; Di Lenola, D. Lateral inhibition in the somatosensory cortex during and between migraine without aura attacks: Correlations with thalamocortical activity and clinical features. Cephalalgia, 2016, 36(6), 568-578.
[http://dx.doi.org/10.1177/0333102415610873] [PMID: 26442930]
[73]
Di Lorenzo, C.; Coppola, G.; Currà, A.; Grieco, G.; San-torelli, F.M.; Lepre, C.; Porretta, E.; Pascale, E.; Pierelli, F. Cortical response to somatosensory stimulation in medica-tion overuse headache patients is influenced by angiotensin converting enzyme (ACE) I/D genetic polymorphism. Cephalalgia, 2012, 32(16), 1189-1197.
[http://dx.doi.org/10.1177/0333102412461890] [PMID: 23053304]
[74]
Zhu, B.; Gianluca, C.; Shoaran, M. Migraine classification using somatosensory evoked potentials. Cephalalgia, 2019, 39(9), 1143-1155.
[http://dx.doi.org/10.1177/0333102419839975] [PMID: 30913908]
[75]
Rhudy, J.L.; France, C.R. Defining the nociceptive flexion reflex (NFR) threshold in human participants: A comparison of different scoring. Pain, 2007, 128(3), 244-253.Available at:. www.ncbi.nlm.nih.gov/pmc/articles/PMC1993909/pdf/nihms21227.pdf (accessed 16 November 2017)
[http://dx.doi.org/ 10.1016/j.pain.2006.09.024] [PMID: 17070999]
[76]
Filatova, E.; Latysheva, N.; Kurenkov, A. Evidence of persistent central sensitization in chronic headaches: a multi-method study. J. Headache Pain, 2008, 9(5), 295-300.
[http://dx.doi.org/10.1007/s10194-008-0061-7] [PMID: 18690491]
[77]
De Icco, R.; Cucinella, L.; De Paoli, I.; Martella, S.; Sances, G.; Bitetto, V.; Sandrini, G.; Nappi, G.; Tassorelli, C.; Nappi, R.E. Modulation of nociceptive threshold by combined hormonal contraceptives in women with oestrogen-withdrawal migraine attacks: a pilot study. J. Headache Pain, 2016, 17(1), 70.
[http://dx.doi.org/10.1186/s10194-016-0661-6] [PMID: 27488685]
[78]
Katsarava, Z.; Ellrich, J.; Diener, H.C.; Kaube, H. Optimized stimulation and recording parameters of human ‘nociception specific’ blink reflex recordings. Clin. Neurophysiol., 2002, 113(12), 1932-1936.Available at:. ac.els-cdn.com/S1388245702003073/1-s2.0-S1388245702003073-main.pdf?_tid=094ce8ca-c485-11e7-bba9-00000aacb360&acdnat=1510146314_00e09e79ee6c10fd5475f320a2ed2743 (Accessed 8 November 2017).
[http://dx.doi.org/10.1016/s1388-2457(02)00307-3] [PMID: 12464330]
[79]
Perrotta, A.; Anastasio, M.G.; De Icco, R.; Coppola, G.; Ambrosini, A.; Serrao, M.; Sandrini, G.; Pierelli, F. Frequency-dependent habituation deficit of the nociceptive blink reflex in aura with migraine headache. can migraine aura modulate trigeminal excitability? Headache, 2017, 57(6), 887-898.
[http://dx.doi.org/10.1111/head.13111] [PMID: 28488755]
[80]
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(8), 814-819.
[http://dx.doi.org/10.1046/j.1468-2982.2003.00591.x] [PMID: 14510928]
[81]
Di Clemente, L.; Coppola, G.; Magis, D.; Fumal, A.; De Pasqua, V.; Schoenen, J. Nociceptive blink reflex and visual evoked potential habituations are correlated in migraine. Headache, 2005, 45(10), 1388-1393.
[http://dx.doi.org/10.1111/j.1526-4610.2005.00271.x] [PMID: 16324171]
[82]
Marin, J.C.A.; Gantenbein, A.R.; Paemeleire, K.; Kaube, H.; Goadsby, P.J. Nociception-specific blink reflex: pharmacology in healthy volunteers. J. Headache Pain, 2015, 16, 87.
[http://dx.doi.org/10.1186/s10194-015-0568-7] [PMID: 26449227]
[83]
Sohn, J-H.; Kim, C-H.; Choi, H-C. Differences in central facilitation between episodic and chronic migraineurs in nociceptive-specific trigeminal pathways. J. Headache Pain, 2016, 17, 35.
[http://dx.doi.org/10.1186/s10194-016-0637-6] [PMID: 27084694]
[84]
de Tommaso, M. Laser-evoked potentials in primary headaches and cranial neuralgias. Expert Rev. Neurother., 2008, 8(9), 1339-1345.
[http://dx.doi.org/10.1586/14737175.8.9.1339] [PMID: 18759546]
[85]
Uglem, M.; Omland, P.M.; Stjern, M.; Gravdahl, G.B.; Sand, T. Habituation of laser-evoked potentials by migraine phase: a blinded longitudinal study. J. Headache Pain, 2017, 18(1), 100.
[http://dx.doi.org/10.1186/s10194-017-0810-6] [PMID: 28971336]
[86]
de Tommaso, M.; Guido, M.; Libro, G.; Losito, L.; Difruscolo, O.; Puca, F.; Specchio, L.M.; Carella, A. Topographic and dipolar analysis of laser-evoked potentials during migraine attack. Headache, 2004, 44(10), 947-960.
[http://dx.doi.org/10.1111/j.1526-4610.2004.04188.x] [PMID: 15546257]
[87]
Vecchio, E.; Ricci, K.; Montemurno, A.; Delussi, M.; Invitto, S.; de Tommaso, M. Effects of left primary motor and dorsolateral prefrontal cortex transcranial direct current stimulation on laser-evoked potentials in migraine patients and normal subjects. Neurosci. Lett., 2016, 626, 149-157.
[http://dx.doi.org/10.1016/j.neulet.2016.05.034] [PMID: 27208831]
[88]
Walter, W.G.; Cooper, R.; Aldridge, V.J.; McCallum, W.C.; Winter, A.L. Contingent Negative Variation : An Electric Sign of Sensori-Motor Association and Expectancy in the Human Brain. Nature, 1964, 203, 380-384.
[http://dx.doi.org/10.1038/203380a0] [PMID: 14197376]
[89]
Schoenen, J.; Maertens, A.; Timsit-Berthier, M. Contingent Negative Variation (CNV) as a Diagnostic and Physiopathologic Tool in Headache Patients; Migraine, 1985, pp. 17-25.
[http://dx.doi.org/10.1159/000411482]
[90]
Kropp, P.; Gerber, W-D. Contingent negative variation during migraine attack and interval: evidence for normalization of slow cortical potentials during the attack. Cephalalgia, 1995, 15(2), 123-128.
[http://dx.doi.org/10.1046/j.1468-2982.1995.015002123.x] [PMID: 7641246]
[91]
de Tommaso, M.; Difruscolo, O.; Sardaro, M.; Losito, L.; Serpino, C.; Pietrapertosa, A.; Santeramo, M.T.; Dicuonzo, F.; Carella, A.; Lamberti, P.; Livrea, P. Influence of MTHFR genotype on contingent negative variation and MRI abnormalities in migraine. Headache, 2007, 47(2), 253-265.
[http://dx.doi.org/10.1111/j.1526-4610.2006.00690.x] [PMID: 17300365]
[92]
Siniatchkin, M.; Jonas, A.; Baki, H.; van Baalen, A.; Gerber, W.D.; Stephani, U. Developmental changes of the contingent negative variation in migraine and healthy children. J. Headache Pain, 2010, 11(2), 105-113.
[http://dx.doi.org/10.1007/s10194-009-0180-9] [PMID: 20013021]
[93]
Schoenen, J.; Maertens de Noordhout, A.; Timsit-Berthier, M.; Timsit, M. Contingent negative variation and efficacy of beta-blocking agents in migraine. Cephalalgia, 1986, 6(4), 229-233.
[http://dx.doi.org/10.1046/j.1468-2982.1986.0604229.x] [PMID: 2879628]
[94]
Overath, C.H.; Darabaneanu, S.; Evers, M.C.; Gerber, W.D.; Graf, M.; Keller, A.; Niederberger, U.; Schäl, H.; Siniatchkin, M.; Weisser, B. Does an aerobic endurance programme have an influence on information processing in migraineurs? J. Headache Pain, 2014, 15, 11.
[http://dx.doi.org/10.1186/1129-2377-15-11] [PMID: 24528557]
[95]
Knott, J.R.; Irwin, D.A. Anxiety, stress, and the contingent negative variation. Arch. Gen. Psychiatry, 1973, 29(4), 538-541.
[http://dx.doi.org/10.1001/archpsyc.1973.04200040080013] [PMID: 4748314]
[96]
Titlic, M.; Mise, N.I.; Pintaric, I.; Rogosic, V.; Vanjaka-Rogosic, L.; Mihalj, M.; Jurinovic, P.; Katic, A.C.; Andjelinovic, M. The event-related potential P300 in patients with migraine. Acta Inform. Med., 2015, 23(6), 339-342.
[http://dx.doi.org/10.5455/aim.2015.23.339-342] [PMID: 26862241]
[97]
Wang, R.; Dong, Z.; Chen, X. Gender differences of cognitive function in migraine patients: evidence from event-related potentials using the oddball paradigm J Headache Pain.,, 2014. 15, 6. Available at:. www.ncbi.nlm.nih.gov/pmc/articles/PMC3904684/pdf/1129-2377-15-6.pdf (accessed 8 November 2017).
[http://dx.doi.org/10.1186/1129-2377-15-6] [PMID: 24467625]
[98]
Nyholt, D.R.; Borsook, D.; Griffiths, L.R. Migrainomics - identifying brain and genetic markers of migraine. Nat. Rev. Neurol., 2017, 13(12), 725-741.
[http://dx.doi.org/10.1038/nrneurol.2017.151] [PMID: 29146952]
[99]
Akerman, S.; Holland, P.R.; Goadsby, P.J. Diencephalic and brainstem mechanisms in migraine. Nat. Rev. Neurosci., 2011, 12(10), 570-584.
[http://dx.doi.org/10.1038/nrn3057] [PMID: 21931334]
[100]
Magis, D.; Allena, M.; Coppola, G.; Di Clemente, L.; Gérard, P.; Schoenen, J. Search for correlations between genotypes and electrophysiological patterns in migraine: the MTHFR C677T polymorphism and visual evoked potentials. Cephalalgia, 2007, 27(10), 1142-1149.
[http://dx.doi.org/10.1111/j.1468-2982.2007.01412.x] [PMID: 17711493]
[101]
Hansen, J.M.; Bolla, M.; Magis, D.; de Pasqua, V.; Ashina, M.; Thomsen, L.L.; Olesen, J.; Schoenen, J. 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(3), 478-485.
[http://dx.doi.org/10.1111/j.1468-1331.2010.03190.x] [PMID: 20727009]
[102]
Russell, M.B. Genetics in primary headaches. J. Headache Pain, 2007, 8(3), 190-195.
[http://dx.doi.org/10.1007/s10194-007-0389-4] [PMID: 17563838]
[103]
Silberstein, S.D.; Dodick, D.W. Migraine genetics: Part II. Headache, 2013, 53(8), 1218-1229.
[http://dx.doi.org/10.1111/head.12169] [PMID: 23919895]
[104]
Montagna, P. The primary headaches: genetics, epigenetics and a behavioural genetic model. J. Headache Pain, 2008, 9(2), 57-69.
[http://dx.doi.org/10.1007/s10194-008-0026-x] [PMID: 18345478]
[105]
Eising, E.A.; Datson, N.; van den Maagdenberg, A.M.; Ferrari, M.D. Epigenetic mechanisms in migraine: a promising avenue? BMC Med., 2013, 11, 26.
[http://dx.doi.org/10.1186/1741-7015-11-26] [PMID: 23379668]
[106]
Chong, C.D.; Schwedt, T.J.; Hougaard, A. Brain functional connectivity in headache disorders: A narrative review of MRI investigations. J. Cereb. Blood Flow Metab., 2019, 39(4), 650-669.
[http://dx.doi.org/10.1177/0271678X17740794] [PMID: 29154684]
[107]
Bashir, A.; Lipton, R.B.; Ashina, S.; Ashina, M. Migraine and structural changes in the brain. Neurology, 2013, 81(14), 1260-1268.
[http://dx.doi.org/ 10.1212/WNL.0b013e3182a6cb32] [PMID: 23986301]
[108]
Younis, S.; Hougaard, A.; Vestergaard, M.B.; Larsson, H.B.W.; Ashina, M. Migraine and magnetic resonance spectroscopy: a systematic review. Curr. Opin. Neurol., 2017, 30(3), 246-262.
[http://dx.doi.org/10.1097/WCO.0000000000000436] [PMID: 28240609]
[109]
Paemeleire, K.; Schoenen, J. (31) P-MRS in migraine: fallen through the cracks. Headache, 2013, 53(4), 676-678.
[http://dx.doi.org/10.1111/head.12049] [PMID: 23557159]
[110]
Schytz, H.W.; Olesen, J. Laboratory tests of headache disorders - dawn of a new era? Cephalalgia, 2016, 36(13), 1268-1290.
[http://dx.doi.org/10.1177/0333102415612585] [PMID: 26763044]
[111]
Lisicki, M.; D’Ostilio, K.; Coppola, G.; Maertens de Noordhout, A.; Parisi, V.; Schoenen, J.; Magis, D. Brain correlates of single trial visual evoked potentials in migraine: more than meets the eye. Front. Neurol., 2018, 9, 393.
[http://dx.doi.org/10.3389/fneur.2018.00393] [PMID: 29899730]
[112]
Lisicki, M.; D’Ostilio, K.; Coppola, G.; Scholtes, F.; Maertens de Noordhout, A.; Parisi, V.; Schoenen, J.; Magis, D. Evidence of an increased neuronal activation-to-resting glucose uptake ratio in the visual cortex of migraine patients: a study comparing 18FDG-PET and visual evoked potentials. J. Headache Pain, 2018, 19(1), 49.
[http://dx.doi.org/10.1186/s10194-018-0877-8] [PMID: 29978429]