Skip to main content
PMC home page
The Journal of Headache and Pain logoLink to The Journal of Headache and Pain
. 2009 Feb 10;10(2):77–84. doi: 10.1007/s10194-008-0095-x

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

Filippo Brighina 1,✉, Antonio Palermo 1, Brigida Fierro 1
PMCID: PMC3451650  PMID: 19209386

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.

Keywords: Cortical inhibition, Habituation, Migraine, Evoked potentials, TMS, rTMS, tDCS

Full Text

The Full Text of this article is available as a PDF (220.0 KB).

Conflict of interest

None.

Contributor Information

Filippo Brighina, Email: fbrighina@unipa.it.

Brigida Fierro, FAX: +39-00916555102.

References

  • 1.Pietrobon D. Migraine: new molecular mechanisms. Neuroscientist. 2005;11:373–386. doi: 10.1177/1073858405275554. [DOI] [PubMed] [Google Scholar]
  • 2.Olesen J, Larsen B, Lauritzen M. Focal hyperemia followed by spreading oligemia and impaired activation of rCBF in classic migraine. Ann Neurol. 1981;9:344–352. doi: 10.1002/ana.410090406. [DOI] [PubMed] [Google Scholar]
  • 3.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 USA. 2001;98:4687–4692. doi: 10.1073/pnas.071582498. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4.Pietrobon D. Familial hemiplegic migraine. Neurotherapeutics. 2007;4:274–284. doi: 10.1016/j.nurt.2007.01.008. [DOI] [PubMed] [Google Scholar]
  • 5.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. [DOI] [PubMed] [Google Scholar]
  • 6.Schoenen J, Ambrosini A, Sándor PS, Maertens de Noordhout A. Evoked potentials and transcranial magnetic stimulation in migraine: published data and viewpoint on their pathophysiologic significance. Clin Neurophysiol. 2003;114:955–972. doi: 10.1016/S1388-2457(03)00024-5. [DOI] [PubMed] [Google Scholar]
  • 7.Schoenen J. Neurophysiological features of the migrainous brain. Neurol Sci. 2006;27(suppl 2):S77–S81. doi: 10.1007/s10072-006-0575-1. [DOI] [PubMed] [Google Scholar]
  • 8.Coppola G, Pierelli F, Schoenen J (2008) Habituation and migraine. Neurobiol Learn Mem [Epub ahead of print] [DOI] [PubMed]
  • 9.Stankewitz A, May A. Cortical excitability and migraine. Cephalalgia. 2007;27:1454–1456. doi: 10.1111/j.1468-2982.2007.01503.x. [DOI] [PubMed] [Google Scholar]
  • 10.Sandor PS. Migraine excitability. Cephalalgia. 2007;27(12):1440–1441. doi: 10.1111/j.1468-2982.2007.01501.x. [DOI] [PubMed] [Google Scholar]
  • 11.Coppola G, Pierelli F, Schoenen J. Is the cerebral cortex hyperexcitable or hyperresponsive in migraine? Cephalalgia. 2007;27:1427–1439. doi: 10.1111/j.1468-2982.2007.01500.x. [DOI] [PubMed] [Google Scholar]
  • 12.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. [DOI] [PubMed] [Google Scholar]
  • 13.Brighina F, Fierro B. Cortical hypoactivity or reduced efficiency of cortical inhibition in migraine? Cephalalgia. 2007;27:187–188. doi: 10.1111/j.1468-2982.2007.01276_1.x. [DOI] [PubMed] [Google Scholar]
  • 14.Valeriani M, Fierro B, Brighina F. Brain excitability in migraine: hyperexcitability or inhibited inhibition? Pain. 2007;132:219–220. doi: 10.1016/j.pain.2007.08.016. [DOI] [PubMed] [Google Scholar]
  • 15.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: 10.1159/000096880. [DOI] [PubMed] [Google Scholar]
  • 16.Tommaso M. Laser-evoked potentials in primary headaches and cranial neuralgias. Expert Rev Neurother. 2008;8:1339–1345. doi: 10.1586/14737175.8.9.1339. [DOI] [PubMed] [Google Scholar]
  • 17.Marinis M, Pujia A, Natale L, D’arcangelo E, Accornero N. Decreased habituation of the R2 component of the blink reflex in migraine patients. Clin Neurophysiol. 2003;114:889–893. doi: 10.1016/S1388-2457(03)00010-5. [DOI] [PubMed] [Google Scholar]
  • 18.Katsarava Z, Giffin N, Diener H, 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. [DOI] [PubMed] [Google Scholar]
  • 19.Di Clemente L, Coppola G, Magis D, Fumal A, Pasqua V, Schoenen J. 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. [DOI] [PubMed] [Google Scholar]
  • 20.Di Clemente L, Coppola G, Magis D, Fumal A, Pasqua V, Di Piero V, Schoenen J. Interictal habituation deficit of the nociceptive blink reflex: an endophenotypic marker for presymptomatic migraine? Brain. 2007;130:765–770. doi: 10.1093/brain/awl351. [DOI] [PubMed] [Google Scholar]
  • 21.Schoenen J. Deficient habituation of evoked cortical potentials in migraine: a link between brain biology, behavior and trigeminovascular activation? Biomed Pharmacother. 1996;50:71–78. doi: 10.1016/0753-3322(96)84716-0. [DOI] [PubMed] [Google Scholar]
  • 22.Afra J, Proietti Cecchini A, Pasqua V, Albert A, Schoenen J. Visual evoked potentials during long periods of pattern-reversal stimulation in migraine. Brain. 1998;121:233–241. doi: 10.1093/brain/121.2.233. [DOI] [PubMed] [Google Scholar]
  • 23.Ambrosini A, Rossi P, 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. doi: 10.1093/brain/awg206. [DOI] [PubMed] [Google Scholar]
  • 24.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. [DOI] [PubMed] [Google Scholar]
  • 25.Coppola G, Vandenheede M, Di Clemente L, Ambrosini A, Fumal A, Pasqua V, 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. [DOI] [PubMed] [Google Scholar]
  • 26.Coppola G, Ambrosini A, Di Clemente L, Magis D, Fumal A, Gérard P, et al. Interictal abnormalities of gamma band activity in visual evoked responses in migraine: an indication of thalamocortical dysrhythmia? Cephalalgia. 2007;27:1323–1330. doi: 10.1111/j.1468-2982.2007.01440.x. [DOI] [PubMed] [Google Scholar]
  • 27.Fregni F, Pascual-Leone A. Technology insight: non-invasive brain stimulation in neurology-perspectives on the therapeutic potential of rTMS and tDCS. Nat Clin Pract Neurol. 2007;3:383–393. doi: 10.1038/ncpneuro0530. [DOI] [PubMed] [Google Scholar]
  • 28.Aurora SK, Ahmad BK, Welch KM, Bhardhwaj P, Ramadan NM. Transcranial magnetic stimulation confirms hyperexcitability of occipital cortex in migraine. Neurology. 1998;50:1111–1114. doi: 10.1212/wnl.50.4.1111. [DOI] [PubMed] [Google Scholar]
  • 29.Mulleners WM, Chronicle EP, Palmer JE, Koehler PJ, Vredeveld JW. Visual cortex excitability in migraine with and without aura. Headache. 2001;41:565–572. doi: 10.1046/j.1526-4610.2001.041006565.x. [DOI] [PubMed] [Google Scholar]
  • 30.Mulleners WM, Chronicle EP, Palmer JE, Koehler PJ, Vredeveld JW. Suppression of perception in migraine: evidence for reduced inhibition in the visual cortex. Neurology. 2001;56:178–183. doi: 10.1212/wnl.56.2.178. [DOI] [PubMed] [Google Scholar]
  • 31.Aurora SK, Chronicle EP. Migraine’s magnetic attraction. Lancet Neurol. 2002;1:211. doi: 10.1016/S1474-4422(02)00097-2. [DOI] [PubMed] [Google Scholar]
  • 32.Battelli L, Black KR, Wray SH. Transcranial magnetic stimulation of visual areaV5 in migraine. Neurology. 2002;58:1066–1069. doi: 10.1212/wnl.58.7.1066. [DOI] [PubMed] [Google Scholar]
  • 33.Antal A, Arlt S, Nitsche MA, Chadaide Z, Paulus W. Higher variability of phosphene thresholds in migraineurs than in controls: a consecutive transcranial magnetic stimulation study. Cephalalgia. 2006;26:865–870. doi: 10.1111/j.1468-2982.2006.01132.x. [DOI] [PubMed] [Google Scholar]
  • 34.Afra J, Mascia A, Gerard P, Maertens de Noordhout A, Schoenen J. 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. [DOI] [PubMed] [Google Scholar]
  • 35.Bohotin V, Fumal A, Vandenheede M, Bohotin C, Schoenen J. 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. [DOI] [PubMed] [Google Scholar]
  • 36.Lo YL, Lum SY, Fook-Chong S, Cui SL, Siow HC. Clinical correlates of phosphene perception in migraine without aura: an Asian study. J Neurol Sci. 2008;15(264):93–96. doi: 10.1016/j.jns.2007.07.026. [DOI] [PubMed] [Google Scholar]
  • 37.Bohotin V, Fumal A, Vandenheede M, Gerard P, Bohotin C, Maertens de Noordhout A, Schoenen J. Effects of repetitive transcranial magnetic stimulation on visual evoked potentials in migraine. Brain. 2002;125:912–922. doi: 10.1093/brain/awf081. [DOI] [PubMed] [Google Scholar]
  • 38.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. [DOI] [PubMed] [Google Scholar]
  • 39.Fierro B, Ricci R, Piazza A, Scalia S, Giglia G, Vitello G, Brighina F. 1 Hz rTMS enhances extrastriate cortex activity in migraine: evidence of a reduced inhibition? Neurology. 2003;61:1446–1448. doi: 10.1212/01.wnl.0000094823.74175.92. [DOI] [PubMed] [Google Scholar]
  • 40.Boroojerdi B, Bushara KO, Corwell B, Immisch I, Battaglia F, Muellbacher W, Cohen LG. Enhanced excitability of the human visual cortex induced by short-term light deprivation. Cereb Cortex. 2000;10:529–534. doi: 10.1093/cercor/10.5.529. [DOI] [PubMed] [Google Scholar]
  • 41.Bolla M, Coppola G, Pasqua V, Gerardy PY, Kazadi EK, Magis D, Schoenen J. Conditioning by high frequency visual stimuli of the visual evoked potential in healthy volunteers and migraineurs. Cephalalgia. 2007;27:715. [Google Scholar]
  • 42.Mulleners WM, Chronicle EP, Vredeveld JW, Koehler PJ. Visual cortex excitability in migraine before and after valproate prophylaxis: a pilot study using TMS. Eur J Neurol. 2002;9(1):35–40. doi: 10.1046/j.1468-1331.2002.00334.x. [DOI] [PubMed] [Google Scholar]
  • 43.Palmer JE, Chronicle EP, Rolan P, Mulleners WM. Cortical hyperexcitability is cortical under-inhibition: evidence from a novel functional test of migraine patients. Cephalalgia. 2000;20:525–532. doi: 10.1046/j.1468-2982.2000.00075.x. [DOI] [PubMed] [Google Scholar]
  • 44.Shepherd AJ. Increased visual after-effects following pattern adaptation in migraine: a lack of intracortical excitation? Brain. 2001;124:2310–2318. doi: 10.1093/brain/124.11.2310. [DOI] [PubMed] [Google Scholar]
  • 45.Shepherd AJ. Local and global motion after-effects are both enhanced in migraine, and the underlying mechanisms differ across cortical areas. Brain. 2006;129:1833–1843. doi: 10.1093/brain/awl124. [DOI] [PubMed] [Google Scholar]
  • 46.Brighina F, Giglia G, Scalia S, Francolini M, Palermo A, Fierro B. 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. [DOI] [PubMed] [Google Scholar]
  • 47.Werhahn KJ, Wiseman K, Herzog J, Förderreuther S, Dichgans M, Straube A. Motor cortex excitability in patients with migraine with aura and hemiplegic migraine. Cephalalgia. 2000;20:45–50. doi: 10.1046/j.1468-2982.2000.00011.x. [DOI] [PubMed] [Google Scholar]
  • 48.Aurora SK, al-Sayeed F, Welch KM. The cortical silent period is shortened in migraine with aura. Cephalalgia. 1999;19:708–712. doi: 10.1046/j.1468-2982.1999.019008708.x. [DOI] [PubMed] [Google Scholar]
  • 49.Curra A, Pierelli F, Coppola G, Barbanti P, Buzzi MG, Galeotti F, Serrao M, Truini A, Casal C, Pauri F, Cruccu G. Shortened cortical silent period in facial muscles of patients with migraine. Pain. 2007;132:124–131. doi: 10.1016/j.pain.2007.05.009. [DOI] [PubMed] [Google Scholar]
  • 50.Chadaide Z, Arlt S, Antal A, Nitsche MA, Lang N, Paulus W. Transcranial direct current stimulation reveals inhibitory deficiency in migraine. Cephalalgia. 2007;27:833–839. doi: 10.1111/j.1468-2982.2007.01337.x. [DOI] [PubMed] [Google Scholar]
  • 51.Chen FP, Evinger C. Cerebellar modulation of trigeminal reflex blinks: interpositus neurons. J Neurosci. 2006;26:10569–10576. doi: 10.1523/JNEUROSCI.0079-06.2006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 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 [DOI] [PubMed]
  • 53.Lambert GA, Zagami AS (2008) The mode of action of migraine triggers: a hypothesis. Headache [Epub ahead of print] [DOI] [PubMed]
  • 54.Lambert GA, Hoskin KL, Zagami AS. Cortico-NRM influences on trigeminal neuronal sensation. Cephalalgia. 2008;28:640–652. doi: 10.1111/j.1468-2982.2008.01572.x. [DOI] [PubMed] [Google Scholar]
  • 55.Sanes JN, Donoghue JP. Static and dynamic organization of motor cortex. Adv Neurol. 1997;73:277–296. [PubMed] [Google Scholar]
  • 56.Jacobs KM, Donoghue JP. Reshaping the cortical motor map by unmasking latent intracortical connections. Science. 1991;251:944–947. doi: 10.1126/science.2000496. [DOI] [PubMed] [Google Scholar]
  • 57.Kirkwood A, Bear MF. Hebbian synapses in visual cortex. J Neurosci. 1994;14:1634–1645. doi: 10.1523/JNEUROSCI.14-03-01634.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 58.Ziemann U, Corwell B, Cohen LG. Modulation of plasticity in human motor cortex after forearm ischemic nerve block. J Neurosci. 1998;18:1115–1123. doi: 10.1523/JNEUROSCI.18-03-01115.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 59.Ziemann U, Hallett M, Cohen LG. Mechanisms of deafferentation-induced plasticity in human motor cortex. J Neurosci. 1998;18:7000–7007. doi: 10.1523/JNEUROSCI.18-17-07000.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 60.Fierro B, Brighina F, Vitello G, Piazza A, Scalia S, Giglia G, Daniele O, Pascual-Leone A. Modulatory effects of low- and high-frequency repetitive transcranial magnetic stimulation on visual cortex of healthy subjects undergoing light deprivation. J Physiol. 2005;565(2):659–665. doi: 10.1113/jphysiol.2004.080184. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 61.Hendry SH, Fuchs J, deBlas AL, Jones EG. Distribution and plasticity of immunocytochemically localized GABAA receptors in adult monkey visual cortex. J Neurosci. 1990;10:2438–2450. doi: 10.1523/JNEUROSCI.10-07-02438.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 62.Jones EG. GABAergic neurons and their role in cortical plasticity in primates. Cereb Cortex. 1993;3:361–372. doi: 10.1093/cercor/3.5.361-a. [DOI] [PubMed] [Google Scholar]
  • 63.Rosier AM, Arckens L, Demeulemeester H, Orban GA, Eysel UT, Wu YJ, Vandesande F. Effect of sensory deafferentation on immunoreactivity of GABAergic cells and on GABA receptors in the adult cat visual cortex. J Comp Neurol. 1995;359:476–489. doi: 10.1002/cne.903590309. [DOI] [PubMed] [Google Scholar]
  • 64.Vidyasagar TR. Pattern adaptation in cat visual cortex is a co-operative phenomenon. Neuroscience. 1990;36:175–179. doi: 10.1016/0306-4522(90)90360-G. [DOI] [PubMed] [Google Scholar]
  • 65.McLean J, Palmer LA. Contrast adaptation and excitatory amino acid receptors in cat striate cortex. Visual Neurosci. 1996;13:1069–1087. doi: 10.1017/S0952523800007720. [DOI] [PubMed] [Google Scholar]
  • 66.Gilbert CD. Adult Cortical Dynamics Physiol. Rev. 1998;78:467–485. doi: 10.1152/physrev.1998.78.2.467. [DOI] [PubMed] [Google Scholar]
  • 67.Le Roux N, Amar M, Moreau A, Baux G, Fossier P. Impaired GABAergic transmission disrupts normal homeostatic plasticity in rat cortical networks. Eur J Neurosci. 2008;27:3244–3256. doi: 10.1111/j.1460-9568.2008.06288.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 68.Fierro B, Brighina F, D’Amelio M, Daniele O, Lupo I, Ragonese P, Palermo A, Savettieri G. Motor intracortical inhibition in PD: L-DOPA modulation of high-frequency rTMS effects. Exp Brain Res. 2008;184:521–528. doi: 10.1007/s00221-007-1121-y. [DOI] [PubMed] [Google Scholar]
  • 69.Lefaucheur JP, Drouot X, Ménard-Lefaucheur I, Keravel Y, Nguyen JP. Motor cortex rTMS restores defective intracortical inhibition in chronic neuropathic pain. Neurology. 2006;67:1568–1574. doi: 10.1212/01.wnl.0000242731.10074.3c. [DOI] [PubMed] [Google Scholar]
  • 70.Quartarone A, Rizzo V, Bagnato S, Morgante F, Sant’Angelo A, Romano M, Crupi D, Girlanda P, Rothwell JC, Siebner HR. Homeostatic-like plasticity of the primary motor hand area is impaired in focal hand dystonia. Brain. 2005;128:1943–1950. doi: 10.1093/brain/awh527. [DOI] [PubMed] [Google Scholar]
  • 71.Antal A, Lang N, Boros K, Nitsche M, Siebner HR, Paulus W. Homeostatic metaplasticity of the motor cortex is altered during headache-free intervals in migraine with Aura. Cereb Cortex. 2008;18:2701–2705. doi: 10.1093/cercor/bhn032. [DOI] [PubMed] [Google Scholar]
  • 72.Harsing LG. The pharmacology of the neurochemical transmission in the midbrain raphe nuclei of the rat. Curr Neuropharmacol. 2006;4:313–339. doi: 10.2174/157015906778520764. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 73.Palermo A, Brighina F, Giglia G, Puma AR, Panetta ML, Fierro B. Cortical inhibition affects habituation to visual evoked potentials combined effects of light deprivation and repetitive transcranial magnetic stimulation in healthy subjects. Europ J Neurol. 2008;15(suppl 3):410. [Google Scholar]
  • 74.Fumal A, Coppola G, Bohotin V, Gerardy PY, Seidel L, Donneau AF, Vandenheede M, Maertens de Noordhout A, Schonen J. 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. 2006;26:143–149. doi: 10.1111/j.1468-2982.2005.01013.x. [DOI] [PubMed] [Google Scholar]
  • 75.Brighina F, Piazza A, Vitello G, Aloisio A, Palermo A, Daniele O, Fierro B. rTMS of the prefrontal cortex in the treatment of chronic migraine: a pilot study. J Neurol Sci. 2004;15(227):67–71. doi: 10.1016/j.jns.2004.08.008. [DOI] [PubMed] [Google Scholar]
  • 76.Siniatchkin M, Kröner-Herwig B, Kocabiyik E, Rothenberger A. Intracortical inhibition and facilitation in migraine–a transcranial magnetic stimulation study. Headache. 2007;47:364–370. doi: 10.1111/j.1526-4610.2007.00727.x. [DOI] [PubMed] [Google Scholar]
  • 77.Jones EG. Thalamic circuitry and thalamocortical synchrony. Philos Trans R Soc Lond B. 2002;357:1659–1673. doi: 10.1098/rstb.2002.1168. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 78.Murakami T, Sakuma K, Nomura T, Uemura Y, Hashimoto I, Nakashima K. Changes in somatosensory-evoked potentials and high-frequency oscillations after paired-associative stimulation. Exp Brain Res. 2008;184:339–347. doi: 10.1007/s00221-007-1103-0. [DOI] [PubMed] [Google Scholar]
  • 79.Murakami T, Sakuma K, Nomura T, Nakashima K, Hashimoto I. High-frequency oscillations change in parallel with short-interval intracortical inhibition after theta burst magnetic stimulation. Clin Neurophysiol. 2008;119:301–308. doi: 10.1016/j.clinph.2007.10.012. [DOI] [PubMed] [Google Scholar]
  • 80.Walpurger V, Hebing-Lennartz G, Denecke H, Pietrowsky R. Habituation deficit in auditory event-related potentials in tinnitus complainers. Hear Res. 2003;181(1–2):57–64. doi: 10.1016/S0378-5955(03)00172-2. [DOI] [PubMed] [Google Scholar]
  • 81.Shepherd AJ. Colour vision in migraine: selective deficits for S-cone discriminations. Cephalalgia. 2004;25:412–423. doi: 10.1111/j.1468-2982.2004.00831.x. [DOI] [PubMed] [Google Scholar]
  • 82.Grosser K, Oelkers R, Hummel T, Geisslinger G, Brune K, Kobal G, Lötsch J. Olfactory and trigeminal event-related potentials in migraine. Cephalalgia. 2000;20:621–631. doi: 10.1046/j.1468-2982.2000.00094.x. [DOI] [PubMed] [Google Scholar]
  • 83.Bolay H, Bayazit YA, Gündüz B, Ugur AK, Akçali D, Altunyay S, Ilica S, Babacan A. Subclinical dysfunction of cochlea and cochlear efferents in migraine: an otoacoustic emission study. Cephalalgia. 2008;28:309–317. doi: 10.1111/j.1468-2982.2008.01534.x. [DOI] [PubMed] [Google Scholar]
  • 84.Allena M, Magis D, Pasqua V, Schoenen J, Bisdorff AR. The vestibulo-collic reflex is abnormal in migraine. Cephalalgia. 2007;27:1150–1155. doi: 10.1111/j.1468-2982.2007.01414.x. [DOI] [PubMed] [Google Scholar]
  • 85.Roceanu A, Allena M, Pasqua V, Bisdorff A, Schoenen J. Abnormalities of the vestibulo-collic reflex are similar in migraineurs with and without vertigo. Cephalalgia. 2008;28:988–990. doi: 10.1111/j.1468-2982.2008.01641.x. [DOI] [PubMed] [Google Scholar]
  • 86.Baseler HA, Brewer AA, Sharpe LT, Morland AB, Jägle H, Wandell BA. Reorganization of human cortical maps caused by inherited photoreceptor abnormalities. Nat Neurosci. 2002;5:364–370. doi: 10.1038/nn817. [DOI] [PubMed] [Google Scholar]
  • 87.Eggermont JJ (2006) Cortical tonotopic map reorganization and its implications for treatment of tinnitus. Acta Otolaryngol Suppl (556):9–12 [DOI] [PubMed]
  • 88.Ridder D, Mulder G, Verstraeten E, Seidman M, Elisevich K, Sunaert S, Kovacs S, Kelen K, Heyning P, Moller A. Auditory cortex stimulation for tinnitus. Acta Neurochir Suppl. 2007;97:451–462. doi: 10.1007/978-3-211-33081-4_52. [DOI] [PubMed] [Google Scholar]
  • 89.Brozoski TJ, Spires TJ, Bauer CA. Vigabatrin, a GABA transaminase inhibitor, reversibly eliminates tinnitus in an animal model. J Assoc Res Otolaryngol. 2007;8:105–118. doi: 10.1007/s10162-006-0067-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 90.Alkhatib A, Biebel UW, Smolders JW. Reduction of inhibition in the inferior colliculus after inner hair cell loss. Neuroreport. 2006;17:1493–1497. doi: 10.1097/01.wnr.0000234754.11431.ee. [DOI] [PubMed] [Google Scholar]
  • 91.Jones EG. Cortical and subcortical contributions to activity-dependent plasticity in primate somatosensory cortex. Annu Rev Neurosci. 2000;23:1–37. doi: 10.1146/annurev.neuro.23.1.1. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Headache and Pain are provided here courtesy of BMC

RESOURCES