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The Journal of Headache and Pain
Published in: The Journal of Headache and Pain 1/2012

Open Access 01-01-2012 | Original

Increased variability of motor cortical excitability to transcranial magnetic stimulation in migraine: a new clue to an old enigma

Authors: Adriana B. Conforto, Mariana S. Moraes, Edson Amaro Jr., William B. Young, Lais A. Lois, André L. Gonçalves, Mario F. P. Peres

Published in: The Journal of Headache and Pain | Issue 1/2012

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Abstract

Increased, decreased or normal excitability to transcranial magnetic stimulation (TMS) has been reported in the motor (M1) and visual cortices of patients with migraine. Light deprivation (LD) has been reported to modulate M1 excitability in control subjects (CS). Still, effects of LD on M1 excitability compared to exposure to environmental light exposure (EL) had not been previously described in patients with migraine (MP). To further our knowledge about differences between CS and MP, regarding M1 excitability and effects of LD on M1 excitability, we opted for a novel approach by extending measurement conditions. We measured motor thresholds (MTs) to TMS, short-interval intracortical inhibition, and ratios between motor-evoked potential amplitudes and supramaximal M responses in MP and CS on two different days, before and after LD or EL. Motor thresholds significantly increased in MP in LD and EL sessions, and remained stable in CS. There were no significant between-group differences in other measures of TMS. Short-term variation of MTs was greater in MP compared to CS. Fluctuation in excitability over hours or days in MP is an issue that, until now, has been relatively neglected. The results presented here will help to reconcile conflicting observations.
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Literature
1.
Aurora SK, Wilkinson F (2007) The brain is hyperexcitable in migraine. Cephalalgia 27:1442–1453, 18034688, 10.1111/j.1468-2982.2007.01502.x, 1:STN:280:DC%2BD2snpslSktw%3D%3DCrossRefPubMed
2.
Ambrosini A, Magis D, Schoenen J (2010) Migraine—clinical neurophysiology. Handb Clin Neurol 97:275–293, 20816429, 10.1016/S0072-9752(10)97023-1CrossRefPubMed
3.
Coppola G, Pierelli F, Schoenen J (2007) Is the cerebral cortex hyperexcitable or hyperresponsive in migraine? Cephalalgia 27:1427–1439, 18034686, 10.1111/j.1468-2982.2007.01500.x, 1:STN:280:DC%2BD2snpslSksQ%3D%3DCrossRefPubMed
4.
Schoenen J (2006) Neurophysiological features of the migrainous brain. Neurol Sci 27(Suppl 2):S77–S81, 16688634, 10.1007/s10072-006-0575-1CrossRefPubMed
5.
Reis J, Swayne OB, Vandermeeren Y, Camus M, Dimyan MA, Harris-Love M et al (2008) Contribution of transcranial magnetic stimulation to the understanding of cortical mechanisms involved in motor control. J Physiol 586:325–351, 17974592, 10.1113/jphysiol.2007.144824, 1:CAS:528:DC%2BD1cXhsFSis7g%3DPubMedCentralCrossRefPubMed
6.
Siniatchkin M, Reich AL, Shepherd AJ, van Baalen A, Siebner HR, Stephani U (2009) Peri-ictal changes of cortical excitability in children suffering from migraine without aura. Pain 147:132–140, 19796876, 10.1016/j.pain.2009.08.028CrossRefPubMed
7.
Young WB, Oshinsky ML, Shechter AL, Gebeline-Myers C, Bradley KC, Wassermann EM (2004) Consecutive transcranial magnetic stimulation: phosphene thresholds in migraineurs and controls. Headache 44:131–135, 14756850, 10.1111/j.1526-4610.2004.04028.xCrossRefPubMed
8.
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 26:865–870, 16776703, 10.1111/j.1468-2982.2006.01132.x, 1:STN:280:DC%2BD28zmtlejug%3D%3DCrossRefPubMed
9.
Main A, Dowson A, Gross M (1997) Photophobia and phonophobia in migraineurs between attacks. Headache 37:492–495, 9329231, 10.1046/j.1526-4610.1997.3708492.x, 1:STN:280:DyaK2svmvFyitg%3D%3DCrossRefPubMed
10.
Boroojerdi B, Bushara KO, Corwell B, Immisch I, Battaglia F, Muellbacher W et al (2000) Enhanced excitability of the human visual cortex induced by short-term light deprivation. Cereb Cortex 10:529–534, 10847602, 10.1093/cercor/10.5.529, 1:STN:280:DC%2BD3cvhsl2gtg%3D%3DCrossRefPubMed
11.
Fierro B, Brighina F, Vitello G, Piazza A, Scalia S, Giglia G et al (2005) Modulatory effects of low- and high-frequency repetitive transcranial magnetic stimulation on visual cortex of healthy subjects undergoing light deprivation. J Physiol 565:659–665, 15760946, 10.1113/jphysiol.2004.080184, 1:CAS:528:DC%2BD2MXlsV2gsrw%3DPubMedCentralCrossRefPubMed
12.
Leon-Sarmiento FE, Bara-Jimenez W, Wassermann EM (2005) Visual deprivation effects on human motor cortex excitability. Neurosci Lett 389:17–20, 16040193, 10.1016/j.neulet.2005.06.061, 1:CAS:528:DC%2BD2MXpslCgu7o%3DCrossRefPubMed
13.
Headache Classification Subcommittee of the International Headache Society (2004) The International Classification of Headache Disorders, 2nd edn. Cephalalgia 24(Suppl 1):9–160
14.
Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh Inventory. Neuropsychologia 9:97–113, 5146491, 10.1016/0028-3932(71)90067-4, 1:STN:280:DyaE387msVSqsQ%3D%3DCrossRefPubMed
15.
Rossi S, Hallett M, Rossini PM, Safety of TMS Consensus Group (2009) Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol 120:2008–2039, 19833552, 10.1016/j.clinph.2009.08.016PubMedCentralCrossRefPubMed
16.
17.
Stovner L, Hagen K, Jensen R, Katsaraya Z, Lipton R, Scher A et al (2007) The global burden of headache: a documentation of headache prevalence and disability worldwide. Cephalalgia 27:193–210, 17381554, 10.1111/j.1468-2982.2007.01288.xCrossRefPubMed
18.
Stewart WF, Lipton RB, Dowson AJ, Sawyer J (2001) Development and testing of the Migraine Disability Assessment (MIDAS) Questionnaire to assess headache-related disability. Neurology 56:S20–S28, 11294956, 1:STN:280:DC%2BD3M3ivVGntA%3D%3DCrossRefPubMed
19.
Lefebvre R, Pepin A, Louis PF, Boucher JP (2004) Reliability of the motor evoked potentials elicited through magnetic stimulation at three sites. J Manipulative Physiol Ther 27:97–102, 14970810, 10.1016/j.jmpt.2003.12.004CrossRefPubMed
20.
Kaelin-Lang A, Cohen LG (2000) Enhancing the quality of studies using transcranial magnetic and electrical stimulation with a new computer-controlled system. J Neurosci Methods 102:81–89, 11000414, 10.1016/S0165-0270(00)00284-3, 1:STN:280:DC%2BD3M%2FivVGktg%3D%3DCrossRefPubMed
21.
Herwig U, Kolbel K, Wunderlich AP, Thielscher A, von Tiesenhausen C, Spitzer M et al (2002) Spatial congruence of neuronavigated transcranial magnetic stimulation and functional neuroimaging. Clin Neurophysiol 113:462–468, 11955990, 10.1016/S1388-2457(02)00026-3CrossRefPubMed
22.
Conforto AB, Z′Graggen WJ, Kohl AS, Rösler KM, Kaelin-Lang A (2004) Impact of coil position and electrophysiological monitoring on determination of motor thresholds to transcranial magnetic stimulation. Clin Neurophysiol 115:812–819, 15003761, 10.1016/j.clinph.2003.11.010CrossRefPubMed
23.
Kujirai T, Caramia MD, Rothwell JC, Day BL, Thompson PD, Ferbert A et al (2003) Corticortical inhibition in human motor cortex. J Physiol 471:501–519CrossRef
24.
Boros K, Poreisz C, Paulus W, Antal A (2009) Does the menstrual cycle influence the motor and phosphene thresholds in migraine? Eur J Neurol 16:367–374, 19490072, 10.1111/j.1468-1331.2008.02500.x, 1:STN:280:DC%2BD1MzpvV2isg%3D%3DCrossRefPubMed
25.
Smith MJ, Adams LF, Schmidt PJ, Rubinow DR, Wassermann EM (2002) Effects of ovarian hormones on human cortical excitability. Ann Neurol 51:599–603, 12112106, 10.1002/ana.10180, 1:CAS:528:DC%2BD38XjvFGhsrg%3DCrossRefPubMed
26.
Parente AC, Garcia-Leal C, Del-Ben CM, Guimarães FS, Graeff FG (2005) Subjective and neurovegetative changes in healthy volunteers and panic patients performing simulated public speaking. Eur Neuropsychopharmacol 15:663–671, 15961294, 10.1016/j.euroneuro.2005.05.002, 1:CAS:528:DC%2BD2MXht1Sks7nLCrossRefPubMed
27.
Koski L, Schrader LM, Wu AD, Stern JM (2005) Normative data on changes in transcranial magnetic stimulation measures over a ten hour period. Clin Neurophysiol 116:2099–2109, 16043397, 10.1016/j.clinph.2005.06.006CrossRefPubMed
28.
Wassermann EM (2002) Variation in the response to transcranial magnetic brain stimulation in the general population. Clin Neurophysiol 113:1165–1171, 12088713, 10.1016/S1388-2457(02)00144-XCrossRefPubMed
29.
Wolf SL, Butler AJ, Campana GI, Parris TA, Struys DM, Weinstein SR et al (2004) Intra-subject reliability of parameters contributing to maps generated by transcranial magnetic stimulation. Clin Neurophysiol 115:1740–1747, 15261852, 10.1016/j.clinph.2004.02.027CrossRefPubMed
30.
Antal A, Nitsche MA, Kincses TZ, Lampe C, Paulus W (2003) No correlation between moving phosphene and motor thresholds: a transcranial magnetic stimulation study. Neuroreport 15:297–302, 10.1097/00001756-200402090-00017CrossRef
31.
Boroojerdi B, Battaglia F, Muellbacher W, Cohen LG (2001) Mechanisms underlying rapid experience-dependent plasticity in the human visual cortex. Proc Natl Acad Sci USA 98:14698–14701, 11734655, 10.1073/pnas.251357198, 1:CAS:528:DC%2BD3MXptFCksbc%3DPubMedCentralCrossRefPubMed
32.
Gerwig M, Kastrup O, Meyer B-U, Niehaus L (2003) Evaluation of cortical excitability by motor and phosphene thresholds in transcranial magnetic stimulation. J Neurol Sci 215:75–78, 14568132, 10.1016/S0022-510X(03)00228-4, 1:CAS:528:DC%2BD3sXotVylur8%3DCrossRefPubMed
33.
Stewart LM, Walsh V, Rothwell JC (2001) Motor and phosphene thresholds: a transcranial magnetic stimulation correlation study. Neuropsychologia 39:415–419, 11164880, 10.1016/S0028-3932(00)00130-5, 1:STN:280:DC%2BD3M7ptl2jsQ%3D%3DCrossRefPubMed
34.
Deblieck C, Thompson B, Iacoboni M, Wu A (2008) Correlation between motor and phosphene thresholds: a transcranial magnetic stimulation study. Human Brain Mapp 29:662–670, 10.1002/hbm.20427CrossRef
35.
Vucic S, Kiernan MC (2006) Novel threshold tracking techniques suggest that cortical hyperexcitability is an early feature of motor neuron disease. Brain 129:2436–2446, 16835248, 10.1093/brain/awl172CrossRefPubMed
36.
Traversa R, Cicinelli P, Oliveri M, Palmieri MG, Filippi MM, Pasqualetti P et al (2000) Neurophysiological follow-up of motor cortical output in stroke patients. Clin Neurophysiol 111:1695–1703, 10964084, 10.1016/S1388-2457(00)00373-4, 1:STN:280:DC%2BD3M%2Fhs1OqtA%3D%3DCrossRefPubMed
37.
Paulus W, Classen J, Cohen LG, Large CH, Lazzaro Di, Nitsche M et al (2008) State of the art: pharmacologic effects on cortical excitability measures tested by transcranial magnetic stimulation. Brain Stimul 1:151–163, 20633382, 10.1016/j.brs.2008.06.002CrossRefPubMed
38.
Chen R, Samii A, Canos M, Wassermann EM, Hallett M (1997) Effects of phenytoin on cortical excitability in humans. Neurology 49:881–883, 9305361, 1:CAS:528:DyaK2sXmtlOltrk%3DCrossRefPubMed
39.
Mavroudakis N, Caroyer JM, Brunko E, de Beyl DZ (1994) Effects of diphenylhydantoin on motor potentials evoked with magnetic stimulation. Electroencephalogr Clin Neurophysiol 93:428–433, 7529692, 10.1016/0168-5597(94)90149-X, 1:CAS:528:DyaK2MXktlWgsrk%3DCrossRefPubMed
40.
Boroojerdi B, Battaglia F, Muellbacher W, Cohen LG (2001) Mechanisms influencing stimulus–response properties of the human corticospinal system. Clin Neurophysiol 112:931–937, 11336911, 10.1016/S1388-2457(01)00523-5, 1:STN:280:DC%2BD3MzntFSruw%3D%3DCrossRefPubMed
41.
Ziemann U, Lönnecker S, Steinhoff BJ, Paulus W (1996) Effects of antiepileptic drugs on motor cortex excitability in humans: a transcranial magnetic stimulation study. Ann Neurol 40:367–378, 8797526, 10.1002/ana.410400306, 1:CAS:528:DyaK28XmtVSgtb4%3DCrossRefPubMed
42.
Di Lazzaro V, Oliviero A, Profice P, Pennisi MA, Pilato F, Zito G et al (2003) Ketamine increases motor cortex excitability to transcranial magnetic stimulation. J Physiol 547:485–496, 12562932, 10.1113/jphysiol.2002.030486, 1:CAS:528:DC%2BD3sXivFSrtLg%3DCrossRefPubMed
43.
Kors EE, Vanmolkot KR, Haan J, Frants RR, van den Maagdenberg AM, Ferrari MD (2004) Recent findings in headache genetics. Curr Opin Neurol 17:283–288, 15167062, 10.1097/00019052-200406000-00008CrossRefPubMed
44.
Pietrobon D, Striessnig J (2003) Neurobiology of migraine. Nat Rev Neurosci 4:386–398, 12728266, 10.1038/nrn1102, 1:CAS:528:DC%2BD3sXjtlalsbw%3DCrossRefPubMed
45.
Vanmolkot KR, Babini E, de Vries B, Stam AH, Freilinger T, Terwindt GM, et al. (2007) The novel p.L1649Q mutation in the SCN1A epilepsy gene is associated with familial hemiplegic migraine: genetic and functional studies. Hum Mutat 28:522
46.
Cestele S, Scalmani P, Rusconi R, Terragni B, Franceschetti S, Mantegazza M (2008) Self-limited hyperexcitability: functional effect of a familial hemiplegic migraine mutation of the Nav1.1 (SCN1A) Na+ channel. J Neurosci 28:7273–7283, 18632931, 10.1523/JNEUROSCI.4453-07.2008, 1:CAS:528:DC%2BD1cXovFWmt74%3DPubMedCentralCrossRefPubMed
47.
Julkunen P, Saisanen L, Danner N, Niskanen E, Hukkanen T, Mervaala E et al (2009) Comparison of navigated and non-navigated transcranial magnetic stimulation for motor cortex mapping, motor threshold and motor evoked potentials. Neuroimage 44:790–795, 18976714, 10.1016/j.neuroimage.2008.09.040CrossRefPubMed
48.
Fujisawa R, Kimura J, Taniguchi S, Ichikawa H, Hara M, Shimizu H et al (2011) Effect of volitional relaxation and motor imagery on F wave and MEP: do these tasks affect excitability of the spinal or cortical motor neurons? Clin Neurophysiol 122:1405–1410, 21256796, 10.1016/j.clinph.2010.12.041, 1:STN:280:DC%2BC3MrlvFWlsw%3D%3DCrossRefPubMed
49.
Livingston SC, Ingersoll CD (2008) Intra-rater reliability of a transcranial magnetic stimulation technique to obtain motor evoked potentials. Int J Neurosci 118:239–256, 18205080, 10.1080/00207450701668020CrossRefPubMed
50.
Badawy R, Macdonell RAL, Berkovic SF, Newton MR, Jackson G (2010) Predicting seizure control: cortical excitability and antiepileptic medication. Ann Neurol 67:64–73, 20186859, 10.1002/ana.21806CrossRefPubMed
51.
Lipton RB, Dodick DW, Silberstein SD, Saper JR, Aurora SK, Pearlman SH et al (2010) Single-pulse transcranial magnetic stimulation for acute treatment of migraine with aura: a randomised, double-blind, parallel-group, sham-controlled trial. Lancet Neurol 9:373–380, 20206581, 10.1016/S1474-4422(10)70054-5CrossRefPubMed
52.
Lo YL (2010) Migraine, magnetic stimulation and cortical excitability. Nat Rev Neurol 6:425–427, 20689566, 10.1038/nrneurol.2010.109CrossRefPubMed
53.
Bucher D (2009) Neuronal homeostasis: does form follow function or vice versa? Curr Biol 19:R64–R67, 19174140, 10.1016/j.cub.2008.11.042, 1:CAS:528:DC%2BD1MXhtFequro%3DCrossRefPubMed
Metadata
Title
Increased variability of motor cortical excitability to transcranial magnetic stimulation in migraine: a new clue to an old enigma
Authors
Adriana B. Conforto
Mariana S. Moraes
Edson Amaro Jr.
William B. Young
Lais A. Lois
André L. Gonçalves
Mario F. P. Peres
Publication date
01-01-2012
Publisher
Springer Milan
Published in
The Journal of Headache and Pain / Issue 1/2012
Print ISSN: 1129-2369
Electronic ISSN: 1129-2377
DOI
https://doi.org/10.1007/s10194-011-0379-4

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