[en] Between attacks, migraine patients are characterized by potentiation instead of habituation of stimulation-evoked cortical responses. It is debated whether this is due to increased or decreased cortical excitability. We have studied the changes in visual cortex excitability by recording pattern-reversal visual evoked potentials (PR-VEP) after low- and high-frequency repetitive transcranial magnetic stimulation (rTMS), known respectively for their inhibitory and excitatory effect on the cortex. In 30 patients (20 migraine without, 10 with aura) and 24 healthy volunteers, rTMS of the occipital cortex was performed with a focal figure-of-eight magnetic coil (Magstim). Nine hundred pulses were delivered randomly at 1 or 10 Hz in two separate sessions. Stimulus intensity was set to the phosphene threshold or to 110% of the motor threshold if no phosphenes were elicited. Before and after rTMS, PR-VEP were averaged sequentially in six blocks of 100zztieresponses during uninterrupted 3.1 Hz stimulation. In healthy volunteers, PR-VEP amplitude was significantly decreased in the first block after 1 Hz rTMS and the habituation normally found in successive blocks after sustained stimulation was significantly attenuated. In migraine patients, 10 Hz rTMS was followed by a significant increase of first block PR-VEP amplitude and by a reversal to normal habituation of the potentiation (or dishabituation) characteristic of the disorder. This effect was similar in both forms of migraine and lasted for at least 9 min. There were no significant changes of PR-VEP amplitudes after 1 Hz rTMS in migraineurs and after 10 Hz rTMS in healthy volunteers, nor after sham stimulation. The recovery of a normal PR-VEP habituation pattern after high-frequency rTMS is probably due to activation of the visual cortex and the dishabituation in healthy volunteers to cortical inhibition. We conclude, therefore, that the deficient interictal PR-VEP habituation in migraine is due to a reduced, and not to an increased, pre-activation excitability level of the visual cortex.
Disciplines :
Neurology Neurosciences & behavior
Author, co-author :
Bohotin, V.
Fumal, Arnaud ; Centre Hospitalier Universitaire de Liège - CHU > Neurologie CHR
Vandenheede, M.
Gerard, Pascale ; Centre Hospitalier Universitaire de Liège - CHU > Neurologie CHR
Áfra J., Cecchini A.P., De Pasqua V., Albert A., Schoenen J. (1998) Visual evoked potentials during long periods of pattern-reversal stimulation in migraine. Brain 121:233-241.
Áfra 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 44:209-215.
Áfra J., Sandor P.S., Schoenen J. (2000) Habituation of visual and intensity dependence of auditory evoked cortical potentials tend to normalize just before and during the migraine attack. Cephalalgia 20:714-719.
Aurora S.K., Ahmad B.K., Welch K.M., Bhardhwaj P., Ramadan N.M. (1998) Transcranial magnetic stimulation confirms hyperexcitability of occipital cortex in migraine. Neurology 50:1111-1114.
Bahra A., Matharu M.S., Buchel C., Frackowiak R.S., Goadsby P.J. (2001) Brainstem activation specific to migraine headache. Lancet 357:1016-1017.
Ben-Shachar D., Gazawi H., Riboyad Levin J., Klein E. (1999) Chronic repetitive transcranial magnetic stimulation alters beta-adrenergic and 5-HT2 receptor characteristics in rat brain. Brain Res 816:78-83.
Berardelli A., Inghilleri M., Gillio E., Romeo S., Pedace F., Curra A. (1999) Effects of repetitive cortical stimulation on the silent period evoked by magnetic stimulation. Exp Brain Res 125:82-86.
Bettucci D., Cantello R., Gianelli M., Naldi P., Mutani R. (1992) Menstrual migraine without aura: Cortical excitability to magnetic stimulation. Headache 32:345-347.
Bohning D.E., Shastri A., McConnell K.A., Nahas Z., Lorberbaum J.P., Roberts D.R. (1999) A combined TMS/fMRI study of intensity-dependent TMS over motor cortex. Biol Psychiatry 45:385-394.
Boroojerdi B., Prager A., Muellbacher W., Cohen L.G. (2000) Reduction of human visual cortex excitability using 1-Hz transcranial magnetic stimulation. Neurology 54:1529-1531.
Boroojerdi B., Bushara K.O., Corwell B., Immisch I., Battaglia F., Muellbacher W. (2000) Enhanced excitability of the human visual cortex induced by short-term light deprivation. Cereb Cortex 10:529-534.
Boroojerdi B., Phipps M., Kopylev L., Wharton C.M., Cohen L.G., Grafman J. (2001) Enhancing analogic reasoning with rTMS over the left prefrontal cortex. Neurology 56:526-528.
Cao Y., Welch K.M., Aurora S., Vikingstad E.M. (1999) Functional MRI-BOLD of visually triggered headache in patients with migraine. Arch Neurol 56:548-554.
Chen R., Gerloff C., Classen J., Wassermann E.M., Hallett M., Cohen L.G. (1997) Safety of different inter-train intervals for repetitive transcranial magnetic stimulation and recommendations for safe ranges of stimulation parameters. Electroencephalogr Clin Neurophysiol 105:415-421.
Chen R., Classen J., Gerloff C., Celnik P., Wassermann E.M., Hallett M. (1997) Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology 48:1398-1403.
Cutrer F.M., Sorensen A.G., Weisskoff R.M., Ostergaard L., Sanchez del Rio M., Lee E.J. (1998) Perfusion-weighted imaging defects during spontaneous migrainous aura. Ann Neurol 43:25-31.
Dudek S.M., Bear M.F. (1992) Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade. Proc Natl Acad Sci USA 89:4363-4367.
Eschweiler G.W., Wegerer C., Schlotter W., Spandl C., Stevens A., Bartels M. (2000) Left prefrontal activation predicts therapeutic effects of repetitive transcranial magnetic stimulation (rTMS) in major depression. Psychiatry Res 99:161-172.
Evers S., Quibeldey F., Grotemeyer K.H., Suhr B., Husstedt I.W. (1999) Dynamic changes of cognitive habituation and serotonin metabolism during the migraine interval. Cephalalgia 19:485-491.
Fierro B., Piazza A., Brighina F., La Bua V., Buffa D., Oliveri M. (2001) Modulation of intracortical inhibition induced by low- and high-frequency repetitive transcranial magnetic stimulation. Exp Brain Res 138:452-457.
Gawel M., Connolly J.F., Rose F.C. (1983) Migraine patients exhibit abnormalities in the visual evoked potential. Headache 23:49-52.
Golla F.L., Winter A.L. (1959) Analysis of cerebral responses to flicker in patients complaining of episodic headache. Electroencephalogr Clin Neurophysiol 11:539-549.
Gur E., Lerer B., Dremencov E., Newman M.E. (2000) Chronic repetitive transcranial magnetic stimulation induces subsensitivity of presynaptic serotonergic autoreceptor activity in rat brain. Neuroreport 11:2925-2929.
Hadjikhani N., Sanchez Del Rio M., Wu O., Schwartz D., Bakker D., Fischl B. (2001) Mechanisms of migraine aura revealed by functional MRI in human visual cortex. Proc Natl Acad Sci USA 98:4687-4692.
Hallett M. (2000) Transcranial magnetic stimulation and the human brain. Nature 406:147-150.
Hess G., Donoghue J.P. (1996) Long-term depression of horizontal connections in rat motor cortex. Eur J Neurosci 8:658-665.
Ji R.R., Schlaepfer T.E., Aizenman C.D., Epstein C.M., Qiu D., Huang J.C. (1998) Repetitive transcranial magnetic stimulation activates specific regions in rat brain. Proc Natl Acad Sci USA 95:15635-15640.
Kennard C., Gawel M., Rudolph N.D., Rose F.C. (1978) Visual evoked potentials in migraine subjects. Res Clin Stud Headache 6:73-80.
Kimbrell T.A., Little J.T., Dunn R.T., Frye M.A., Greenberg B.D., Wassermann E.M. (1999) Frequency dependence of antidepressant response to left prefrontal repetitive transcranial magnetic stimulation (rTMS) as a function of baseline cerebral glucose metabolism. Biol Psychiatry 46:1603-1613.
Klein E., Kolsky Y., Puyerovsky M., Koren D., Chistyakov A., Feinsod M. (1999) Right prefrontal slow repetitive transcranial magnetic stimulation in schizophrenia: A double-blind sham-controlled pilot study. Biol Psychiatry 46:1451-1454.
Klein E., Kreinin I., Chistyakov A., Koren D., Mecz L., Marmur S. (1999) Therapeutic efficacy of right prefrontal slow repetitive transcranial magnetic stimulation in major depression: A double-blind controlled study. Arch Gen Psychiatry 56:315-320.
Knott J.R., Irwin D.A. (1973) Anxiety, stress, and the contingent negative variation. Arch Gen Psychiatry 29:538-541.
Kropp P., Gerber W.D. (1993) Is increased amplitude of contingent negative variation in migraine due to cortical hyperactivity or to reduced habituation?. Cephalalgia 13:37-41.
Kropp P., Gerber W.D. (1995) Contingent negative variation during migraine attack and interval: Evidence for normalization of slow cortical potentials during the attack. Cephalalgia 15:123-128.
Lẽo A.A. (1944) Spreading depression of activity in cerebral cortex. J Neurophysiol 7:359-390.
Maeda F., Keenan J.P., Tormos J.M., Topka H., Pascual-Leone A. (2000) Modulation of corticospinal excitability by repetitive transcranial magnetic stimulation. Clin Neurophysiol 111:800-805.
MaertensdeNoordhout A., Schoenen J. (1999) Transcranial magnetic stimulation in migraine. Electroencephalogr Clin Neurophysiol Suppl 51:260-264.
MaertensdeNoordhout A., Timsit-Berthier M., Timsit M., Schoenen J. (1986) Contingent negative variation in headache. Ann Neurol 19:78-80.
MaertensdeNoordhout A., Pepin J.L., Schoenen J., Delwaide P.J. (1992) Percutaneous magnetic stimulation of the motor cortex in migraine. Electroencephalogr Clin Neurophysiol 85:110-115.
Megela A.L., Teyler T.J. (1979) Habituation and the human evoked potential. J Comp Physiol Psychol 93:1154-1170.
Mesulam M.M. (1990) Large-scale neurocognitive networks and distributed processing for attention, language, and memory. Ann Neurol 28:597-613.
Mizuno T., Kanazawa I., Sakurai M. (2001) Differential induction of LTP and LTD is not determined solely by instantaneous calcium concentration: An essential involvement of a temporal factor. Eur J Neurosci 14:701-708.
Modugno N., Nakamura Y., MacKinnon C.D., Filipovic S.R., Bestmann S., Berardelli A. (2001) Motor cortex excitability following short trains of repetitive magnetic stimuli. Exp Brain Res 140:453-459.
Montagna P. (2000) Molecular genetics of migraine headaches: A review. Cephalalgia 20:3-14.
Muellbacher W., Ziemann U., Boroojerdi B., Hallett M. (2000) Effects of low-frequency transcranial magnetic stimulation on motor excitability and basic motor behavior. Clin Neurophysiol 111:1002-1007.
Mulleners W.M., Chronicle E.P., Palmer J.E., Koehler P.J., Vredeveld J.W. (2001) Visual cortex excitability in migraine with and without aura. Headache 41:565-572.
Mulleners W.M., Aurora S.K., Chronicle E.P., Stewart R., Gopal S., Koehler P.J. (2001) Self-reported photophobic symptoms in migraineurs and controls are reliable and predict diagnostic category accurately. Headache 41:31-39.
Oelkers R., Grosser K., Lang E., Geisslinger G., Kobal G., Brune K. (1999) Visual evoked potentials in migraine patients: Alterations depend on pattern spatial frequency. Brain 122:1147-1155.
Olesen J., Friberg L., Olsen T.S., Iversen H.K., Lassen N.A., Andersen A.R. (1990) Timing and topography of cerebral blood flow, aura, and headache during migraine attacks. Ann Neurol 28:791-798.
Pascual-Leone A., Valls-Sole J., Wassermann E.M., Hallett M. (1994) Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex. Brain 117:847-858.
Reuter U., Sanchez del Rio M., Moskowitz M.A. (2000) Experimental models of migraine. Funct Neurol 15(SUPPL. 3):9-18.
Sand T., Vingen J.V. (2000) 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 20:804-820.
Sándor P.S., Áfra J., Proietti Cecchini A.P., Albert A., Schoenen J. (2000) From neurophysiology to genetics: Cortical information processing in migraine underlies familial influences - A novel approach. Funct Neurol 15(SUPPL. 3):68-72.
Sappey-Marinier D., Calabrese G., Fein G., Hugg J.W., Biggins C., Weiner M.W. (1992) Effect of photic stimulation on human visual cortex lactate and phosphates using 1H and 31P magnetic resonance spectroscopy. J Cereb Blood Flow Metab 12:584-592.
Schoenen J. (1996) Deficient habituation of evoked cortical potentials in migraine: A link between brain biology, behavior and trigeminovascular activation?. Biomed Pharmacother 50:71-78.
Schoenen J. (1998) Cortical electrophysiology in migraine and possible pathogenetic implications. Clin Neurosci 5:10-17.
Schoenen J., Timsit-Berthier M. (1993) Contingent negative variation: Methods and potential interest in headache. Cephalalgia 13:28-32.
Schoenen J., Jamart B., Delwaide P.J. (1987) Electroencephalographic mapping in migraine during the critical and intercritical periods. Rev Electroencephalogr Neurophysiol Clin 17:289-299.
Schoenen J., Wang W., Albert A., Delwaide P.J. (1995) Potentiation instead of habituation characterizes visual evoked potentials in migraine patients between attacks. Eur J Neurol 2:115-122.
Siniatchkin M., Gerber W.D., Kropp P., Vein A. (1999) How the brain anticipates an attack: A study of neurophysiological periodicity in migraine. Funct Neurol 14:69-77.
Smith M.J., Keel J.C., Greenberg B.D., Adams L.F., Schmidt P.J., Rubinow D.A. (1999) Menstrual cycle effects on cortical excitability. Neurology 53:2069-2072.
Speer A.M., Kimbrell T.A., Wassermann E.M., Repella J., Willis M.W., Herscovitch P. (2000) Opposite effects of high and low frequency rTMS on regional brain activity in depressed patients. Biol Psychiatry 48:1133-1141.
Van der Kamp W., MaassenVanDenBrink A., Ferrari M.D., Van Dijk J.G. (1997) Interictal cortical excitability to magnetic stimulation in familial hemiplegic migraine. Neurology 48:1462-1464.
Wang W., Timsit-Berthier M., Schoenen J. (1996) Intensity dependence of auditory evoked potentials is pronounced in migraine: An indication of cortical potentiation and low serotonergic neurotransmission?. Neurology 46:1404-1409.
Wassermann E.M., Wedegaertner F.R., Ziemann U., George M.S., Chen R. (1998) Crossed reduction of human motor cortex excitability by 1-Hz transcranial magnetic stimulation. Neurosci Lett 250:141-144.
Weiller C., May A., Limmroth V., Juptner M., Kaube H., Schayck R.V. (1995) Brain stem activation in spontaneous human migraine attacks. Nat Med 1:658-660.
Welch K.M., Levine S.R., D'Andrea G., Schultz L.R., Helpern J.A. (1989) Preliminary observations on brain energy metabolism in migraine studied by in vivo phosphorus 31 NMR spectroscopy. Neurology 39:538-541.
Wu T., Sommer M., Tergau F., Paulus W. (2000) Lasting influence of repetitive transcranial magnetic stimulation on intracortical excitability in human subjects. Neurosci Lett 287:37-40.
