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The Journal of Headache and Pain
Published in: The Journal of Headache and Pain 2/2009

Open Access 01-04-2009 | Review Article

Cortical inhibition and habituation to evoked potentials: relevance for pathophysiology of migraine

Authors: Filippo Brighina, Antonio Palermo, Brigida Fierro

Published in: The Journal of Headache and Pain | Issue 2/2009

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Abstract

Dysfunction of neuronal cortical excitability has been supposed to play an important role in etiopathogenesis of migraine. Neurophysiological techniques like evoked potentials (EP) and in the last years non-invasive brain stimulation techniques like transcranial magnetic stimulation (TMS) and transcranial direct current stimulation gave important contribution to understanding of such issue highlighting possible mechanisms of cortical dysfunctions in migraine. EP studies showed impaired habituation to repeated sensorial stimulation and this abnormality was confirmed across all sensorial modalities, making defective habituation a neurophysiological hallmark of the disease. TMS was employed to test more directly cortical excitability in visual cortex and then also in motor cortex. Contradictory results have been reported pointing towards hyperexcitability or on the contrary to reduced preactivation of sensory cortex in migraine. Other experimental evidence speaks in favour of impairment of inhibitory circuits and analogies have been proposed between migraine and conditions of sensory deafferentation in which down-regulation of GABA circuits is considered the more relevant pathophysiological mechanism. Whatever the mechanism involved, it has been found that repeated sessions of high-frequency rTMS trains that have been shown to up-regulate inhibitory circuits could persistently normalize habituation in migraine. This could give interesting insight into pathophysiology establishing a link between cortical inhibition and habituation and opening also new treatment strategies in migraine.
Literature
1.
2.
Olesen J, Larsen B, Lauritzen M (1981) Focal hyperemia followed by spreading oligemia and impaired activation of rCBF in classic migraine. Ann Neurol 9:344–352CrossRefPubMed
3.
Hadjikhani N, Sanchez Del Rio M, Wu O et al (2001) Mechanisms of migraine aura revealed by functional MRI in human visual cortex. Proc Natl Acad Sci USA 98:4687–4692PubMedCentralCrossRefPubMed
4.
5.
Bolay H, Reuter U, Dunn AK et al (2002) Intrinsic brain activity triggers trigeminal meningeal afferents in a migraine model. Nat Med 8:136–142CrossRefPubMed
6.
Schoenen J, Ambrosini A, Sándor PS, Maertens de Noordhout A (2003) Evoked potentials and transcranial magnetic stimulation in migraine: published data and viewpoint on their pathophysiologic significance. Clin Neurophysiol 114:955–972CrossRefPubMed
7.
Schoenen J (2006) Neurophysiological features of the migrainous brain. Neurol Sci 27(suppl 2):S77–S81CrossRefPubMed
8.
Coppola G, Pierelli F, Schoenen J (2008) Habituation and migraine. Neurobiol Learn Mem [Epub ahead of print]
9.
10.
11.
Coppola G, Pierelli F, Schoenen J (2007) Is the cerebral cortex hyperexcitable or hyperresponsive in migraine? Cephalalgia 27:1427–1439CrossRefPubMed
12.
Aurora SK, Barrodale P, Chronicle EP, Mulleners WM (2005) Cortical inhibition is reduced in chronic and episodic migraine and demonstrates a spectrum of illness. Headache 45:546–552CrossRefPubMed
13.
Brighina F, Fierro B (2007) Cortical hypoactivity or reduced efficiency of cortical inhibition in migraine? Cephalalgia 27:187–188 (author reply 188–189)CrossRefPubMed
14.
Valeriani M, Fierro B, Brighina F (2007) Brain excitability in migraine: hyperexcitability or inhibited inhibition? Pain 132:219–220CrossRefPubMed
15.
Schoenen J, Wang W, Albert A, Delwaide PJ (1995) Potentiation instead of habituation characterizes visual evoked potentials in migraine patients between attacks. Eur J Neurol 2:115–122CrossRefPubMed
16.
de Tommaso M (2008) Laser-evoked potentials in primary headaches and cranial neuralgias. Expert Rev Neurother 8:1339–1345CrossRefPubMed
17.
De Marinis M, Pujia A, Natale L, D’arcangelo E, Accornero N (2003) Decreased habituation of the R2 component of the blink reflex in migraine patients. Clin Neurophysiol 114:889–893CrossRefPubMed
18.
Katsarava Z, Giffin N, Diener H, Kaube H (2003) Abnormal habituation of ‘nociceptive’ blink reflex in migraine—evidence for increased excitability of trigeminal nociception. Cephalalgia 23:814–819CrossRefPubMed
19.
Di Clemente L, Coppola G, Magis D, Fumal A, De Pasqua V, Schoenen J (2005) Nociceptive blink reflex and visual evoked potential habituations are correlated in migraine. Headache 45:1388–1393CrossRefPubMed
20.
Di Clemente L, Coppola G, Magis D, Fumal A, De Pasqua V, Di Piero V, Schoenen J (2007) Interictal habituation deficit of the nociceptive blink reflex: an endophenotypic marker for presymptomatic migraine? Brain 130:765–770CrossRefPubMed
21.
Schoenen J (1996) Deficient habituation of evoked cortical potentials in migraine: a link between brain biology, behavior and trigeminovascular activation? Biomed Pharmacother 50:71–78CrossRefPubMed
22.
Afra J, Proietti Cecchini A, De Pasqua V, Albert A, Schoenen J (1998) Visual evoked potentials during long periods of pattern-reversal stimulation in migraine. Brain 121:233–241CrossRefPubMed
23.
Ambrosini A, Rossi P, De Pasqua V, Pierelli F, Schoenen J (2003) Lack of habituation causes high intensity dependence of auditory evoked cortical potentials in migraine. Brain 126(Pt 9):2009–2015CrossRefPubMed
24.
Ozkul Y, Uckardes A (2002) Median nerve somatosensory evoked potentials in migraine. Eur J Neurol 9:227–232CrossRefPubMed
25.
Coppola G, Vandenheede M, Di Clemente L, Ambrosini A, Fumal A, De Pasqua V et al (2005) Somatosensory evoked high-frequency oscillations reflecting thalamo-cortical activity are decreased in migraine patients between attacks. Brain 128:98–103CrossRefPubMed
26.
Coppola G, Ambrosini A, Di Clemente L, Magis D, Fumal A, Gérard P et al (2007) Interictal abnormalities of gamma band activity in visual evoked responses in migraine: an indication of thalamocortical dysrhythmia? Cephalalgia 27:1323–1330CrossRef
27.
Fregni F, Pascual-Leone A (2007) Technology insight: non-invasive brain stimulation in neurology-perspectives on the therapeutic potential of rTMS and tDCS. Nat Clin Pract Neurol 3:383–393CrossRefPubMed
28.
Aurora SK, Ahmad BK, Welch KM, Bhardhwaj P, Ramadan NM (1998) Transcranial magnetic stimulation confirms hyperexcitability of occipital cortex in migraine. Neurology 50:1111–1114CrossRefPubMed
29.
Mulleners WM, Chronicle EP, Palmer JE, Koehler PJ, Vredeveld JW (2001) Visual cortex excitability in migraine with and without aura. Headache 41:565–572CrossRefPubMed
30.
Mulleners WM, Chronicle EP, Palmer JE, Koehler PJ, Vredeveld JW (2001) Suppression of perception in migraine: evidence for reduced inhibition in the visual cortex. Neurology 56:178–183CrossRefPubMed
31.
32.
Battelli L, Black KR, Wray SH (2002) Transcranial magnetic stimulation of visual areaV5 in migraine. Neurology 58:1066–1069CrossRefPubMed
33.
Antal A, Arlt S, Nitsche MA, Chadaide Z, Paulus W (2006) Higher variability of phosphene thresholds in migraineurs than in controls: a consecutive transcranial magnetic stimulation study. Cephalalgia 26:865–870CrossRefPubMed
34.
Afra J, Mascia A, Gerard P, Maertens de Noordhout A, Schoenen J (1998) Interictal cortical excitability in migraine: a study using transcranial magnetic stimulation of motor and visual cortices. Ann Neurol 44:209–215CrossRefPubMed
35.
Bohotin V, Fumal A, Vandenheede M, Bohotin C, Schoenen J (2003) Excitability of visual V1–V2 and motor cortices to single transcranial magnetic stimuli in migraine: a reappraisal using a figure-of-eight coil. Cephalalgia 23:264–270CrossRefPubMed
36.
Lo YL, Lum SY, Fook-Chong S, Cui SL, Siow HC (2008) Clinical correlates of phosphene perception in migraine without aura: an Asian study. J Neurol Sci 15(264):93–96CrossRef
37.
Bohotin V, Fumal A, Vandenheede M, Gerard P, Bohotin C, Maertens de Noordhout A, Schoenen J (2002) Effects of repetitive transcranial magnetic stimulation on visual evoked potentials in migraine. Brain 125:912–922CrossRefPubMed
38.
Brighina F, Piazza A, Daniele O, Fierro B (2002) Modulation of visual cortical excitability in migraine with aura: effects of 1 Hz repetitive transcranial magnetic stimulation. Exp Brain Res 145:177–181CrossRefPubMed
39.
Fierro B, Ricci R, Piazza A, Scalia S, Giglia G, Vitello G, Brighina F (2003) 1 Hz rTMS enhances extrastriate cortex activity in migraine: evidence of a reduced inhibition? Neurology 61:1446–1448CrossRefPubMed
40.
Boroojerdi B, Bushara KO, Corwell B, Immisch I, Battaglia F, Muellbacher W, Cohen LG (2000) Enhanced excitability of the human visual cortex induced by short-term light deprivation. Cereb Cortex 10:529–534CrossRefPubMed
41.
Bolla M, Coppola G, De Pasqua V, Gerardy PY, Kazadi EK, Magis D, Schoenen J (2007) Conditioning by high frequency visual stimuli of the visual evoked potential in healthy volunteers and migraineurs. Cephalalgia 27:715
42.
Mulleners WM, Chronicle EP, Vredeveld JW, Koehler PJ (2002) Visual cortex excitability in migraine before and after valproate prophylaxis: a pilot study using TMS. Eur J Neurol 9(1):35–40CrossRefPubMed
43.
Palmer JE, Chronicle EP, Rolan P, Mulleners WM (2000) Cortical hyperexcitability is cortical under-inhibition: evidence from a novel functional test of migraine patients. Cephalalgia 20:525–532CrossRefPubMed
44.
Shepherd AJ (2001) Increased visual after-effects following pattern adaptation in migraine: a lack of intracortical excitation? Brain 124:2310–2318CrossRefPubMed
45.
Shepherd AJ (2006) Local and global motion after-effects are both enhanced in migraine, and the underlying mechanisms differ across cortical areas. Brain 129:1833–1843CrossRefPubMed
46.
Brighina F, Giglia G, Scalia S, Francolini M, Palermo A, Fierro B (2005) Facilitatory effects of 1 Hz rTMS in motor cortex of patients affected by migraine with aura. Exp Brain Res 161:34–38CrossRefPubMed
47.
Werhahn KJ, Wiseman K, Herzog J, Förderreuther S, Dichgans M, Straube A (2000) Motor cortex excitability in patients with migraine with aura and hemiplegic migraine. Cephalalgia 20:45–50CrossRefPubMed
48.
Aurora SK, al-Sayeed F, Welch KM (1999) The cortical silent period is shortened in migraine with aura. Cephalalgia 19:708–712CrossRefPubMed
49.
Curra A, Pierelli F, Coppola G, Barbanti P, Buzzi MG, Galeotti F, Serrao M, Truini A, Casal C, Pauri F, Cruccu G (2007) Shortened cortical silent period in facial muscles of patients with migraine. Pain 132:124–131CrossRefPubMed
50.
Chadaide Z, Arlt S, Antal A, Nitsche MA, Lang N, Paulus W (2007) Transcranial direct current stimulation reveals inhibitory deficiency in migraine. Cephalalgia 27:833–839CrossRefPubMed
51.
Chen FP, Evinger C (2006) Cerebellar modulation of trigeminal reflex blinks: interpositus neurons. J Neurosci 26:10569–10576CrossRefPubMed
52.
De Vito A, Gastaldo E, Tugnoli V, Eleopra R, Casula A, Tola MR, Granieri E, Quatrale R (2009) Effect of slow rTMS of motor cortex on the excitability of the blink reflex: a study in healthy humans. Clin Neurophysiol 120:174–180
53.
Lambert GA, Zagami AS (2008) The mode of action of migraine triggers: a hypothesis. Headache [Epub ahead of print]
54.
Lambert GA, Hoskin KL, Zagami AS (2008) Cortico-NRM influences on trigeminal neuronal sensation. Cephalalgia 28:640–652CrossRefPubMed
55.
Sanes JN, Donoghue JP (1997) Static and dynamic organization of motor cortex. Adv Neurol 73:277–296PubMed
56.
Jacobs KM, Donoghue JP (1991) Reshaping the cortical motor map by unmasking latent intracortical connections. Science 251:944–947CrossRefPubMed
57.
Kirkwood A, Bear MF (1994) Hebbian synapses in visual cortex. J Neurosci 14:1634–1645PubMed
58.
Ziemann U, Corwell B, Cohen LG (1998) Modulation of plasticity in human motor cortex after forearm ischemic nerve block. J Neurosci 18:1115–1123PubMed
59.
Ziemann U, Hallett M, Cohen LG (1998) Mechanisms of deafferentation-induced plasticity in human motor cortex. J Neurosci 18:7000–7007PubMed
60.
Fierro B, Brighina F, Vitello G, Piazza A, Scalia S, Giglia G, Daniele O, Pascual-Leone A (2005) Modulatory effects of low- and high-frequency repetitive transcranial magnetic stimulation on visual cortex of healthy subjects undergoing light deprivation. J Physiol 565(2):659–665PubMedCentralCrossRefPubMed
61.
Hendry SH, Fuchs J, deBlas AL, Jones EG (1990) Distribution and plasticity of immunocytochemically localized GABAA receptors in adult monkey visual cortex. J Neurosci 10:2438–2450PubMed
62.
Jones EG (1993) GABAergic neurons and their role in cortical plasticity in primates. Cereb Cortex 3:361–372CrossRefPubMed
63.
Rosier AM, Arckens L, Demeulemeester H, Orban GA, Eysel UT, Wu YJ, Vandesande F (1995) Effect of sensory deafferentation on immunoreactivity of GABAergic cells and on GABA receptors in the adult cat visual cortex. J Comp Neurol 359:476–489CrossRefPubMed
64.
Vidyasagar TR (1990) Pattern adaptation in cat visual cortex is a co-operative phenomenon. Neuroscience 36:175–179CrossRefPubMed
65.
McLean J, Palmer LA (1996) Contrast adaptation and excitatory amino acid receptors in cat striate cortex. Visual Neurosci 13:1069–1087CrossRef
66.
Gilbert CD (1998) Adult Cortical Dynamics Physiol. Rev 78:467–485
67.
Le Roux N, Amar M, Moreau A, Baux G, Fossier P (2008) Impaired GABAergic transmission disrupts normal homeostatic plasticity in rat cortical networks. Eur J Neurosci 27:3244–3256PubMedCentralCrossRefPubMed
68.
Fierro B, Brighina F, D’Amelio M, Daniele O, Lupo I, Ragonese P, Palermo A, Savettieri G (2008) Motor intracortical inhibition in PD: L-DOPA modulation of high-frequency rTMS effects. Exp Brain Res 184:521–528CrossRefPubMed
69.
Lefaucheur JP, Drouot X, Ménard-Lefaucheur I, Keravel Y, Nguyen JP (2006) Motor cortex rTMS restores defective intracortical inhibition in chronic neuropathic pain. Neurology 67:1568–1574CrossRefPubMed
70.
Quartarone A, Rizzo V, Bagnato S, Morgante F, Sant’Angelo A, Romano M, Crupi D, Girlanda P, Rothwell JC, Siebner HR (2005) Homeostatic-like plasticity of the primary motor hand area is impaired in focal hand dystonia. Brain 128:1943–1950CrossRefPubMed
71.
Antal A, Lang N, Boros K, Nitsche M, Siebner HR, Paulus W (2008) Homeostatic metaplasticity of the motor cortex is altered during headache-free intervals in migraine with Aura. Cereb Cortex 18:2701–2705CrossRefPubMed
72.
73.
Palermo A, Brighina F, Giglia G, Puma AR, Panetta ML, Fierro B (2008) Cortical inhibition affects habituation to visual evoked potentials combined effects of light deprivation and repetitive transcranial magnetic stimulation in healthy subjects. Europ J Neurol 15(suppl 3):410
74.
Fumal A, Coppola G, Bohotin V, Gerardy PY, Seidel L, Donneau AF, Vandenheede M, Maertens de Noordhout A, Schonen J (2006) Induction of long-lasting changes of visual cortex excitability by five daily sessions of repetitive transcranial magnetic stimulation (rTMS) in healthy volunteers and migraine patients. Cephalalgia 26:143–149CrossRefPubMed
75.
Brighina F, Piazza A, Vitello G, Aloisio A, Palermo A, Daniele O, Fierro B (2004) rTMS of the prefrontal cortex in the treatment of chronic migraine: a pilot study. J Neurol Sci 15(227):67–71CrossRef
76.
Siniatchkin M, Kröner-Herwig B, Kocabiyik E, Rothenberger A (2007) Intracortical inhibition and facilitation in migraine–a transcranial magnetic stimulation study. Headache 47:364–370CrossRefPubMed
77.
Jones EG (2002) Thalamic circuitry and thalamocortical synchrony. Philos Trans R Soc Lond B 357:1659–1673CrossRef
78.
Murakami T, Sakuma K, Nomura T, Uemura Y, Hashimoto I, Nakashima K (2008) Changes in somatosensory-evoked potentials and high-frequency oscillations after paired-associative stimulation. Exp Brain Res 184:339–347CrossRefPubMed
79.
Murakami T, Sakuma K, Nomura T, Nakashima K, Hashimoto I (2008) High-frequency oscillations change in parallel with short-interval intracortical inhibition after theta burst magnetic stimulation. Clin Neurophysiol 119:301–308CrossRefPubMed
80.
Walpurger V, Hebing-Lennartz G, Denecke H, Pietrowsky R (2003) Habituation deficit in auditory event-related potentials in tinnitus complainers. Hear Res 181(1–2):57–64CrossRefPubMed
81.
Shepherd AJ (2004) Colour vision in migraine: selective deficits for S-cone discriminations. Cephalalgia 25:412–423CrossRef
82.
Grosser K, Oelkers R, Hummel T, Geisslinger G, Brune K, Kobal G, Lötsch J (2000) Olfactory and trigeminal event-related potentials in migraine. Cephalalgia 20:621–631CrossRefPubMed
83.
Bolay H, Bayazit YA, Gündüz B, Ugur AK, Akçali D, Altunyay S, Ilica S, Babacan A (2008) Subclinical dysfunction of cochlea and cochlear efferents in migraine: an otoacoustic emission study. Cephalalgia 28:309–317CrossRefPubMed
84.
Allena M, Magis D, De Pasqua V, Schoenen J, Bisdorff AR (2007) The vestibulo-collic reflex is abnormal in migraine. Cephalalgia 27:1150–1155CrossRefPubMed
85.
Roceanu A, Allena M, De Pasqua V, Bisdorff A, Schoenen J (2008) Abnormalities of the vestibulo-collic reflex are similar in migraineurs with and without vertigo. Cephalalgia 28:988–990CrossRefPubMed
86.
Baseler HA, Brewer AA, Sharpe LT, Morland AB, Jägle H, Wandell BA (2002) Reorganization of human cortical maps caused by inherited photoreceptor abnormalities. Nat Neurosci 5:364–370CrossRefPubMed
87.
Eggermont JJ (2006) Cortical tonotopic map reorganization and its implications for treatment of tinnitus. Acta Otolaryngol Suppl (556):9–12
88.
De Ridder D, De Mulder G, Verstraeten E, Seidman M, Elisevich K, Sunaert S, Kovacs S, Van der Kelen K, Van de Heyning P, Moller A (2007) Auditory cortex stimulation for tinnitus. Acta Neurochir Suppl 97:451–462CrossRefPubMed
89.
Brozoski TJ, Spires TJ, Bauer CA (2007) Vigabatrin, a GABA transaminase inhibitor, reversibly eliminates tinnitus in an animal model. J Assoc Res Otolaryngol 8:105–118PubMedCentralCrossRefPubMed
90.
Alkhatib A, Biebel UW, Smolders JW (2006) Reduction of inhibition in the inferior colliculus after inner hair cell loss. Neuroreport 17:1493–1497CrossRefPubMed
91.
Jones EG (2000) Cortical and subcortical contributions to activity-dependent plasticity in primate somatosensory cortex. Annu Rev Neurosci 23:1–37CrossRefPubMed
Metadata
Title
Cortical inhibition and habituation to evoked potentials: relevance for pathophysiology of migraine
Authors
Filippo Brighina
Antonio Palermo
Brigida Fierro
Publication date
01-04-2009
Publisher
Springer Milan
Published in
The Journal of Headache and Pain / Issue 2/2009
Print ISSN: 1129-2369
Electronic ISSN: 1129-2377
DOI
https://doi.org/10.1007/s10194-008-0095-x

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