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
A Fumal, G Coppola, V Bohotin, P-Y Gérardy, L Seidel,
A-F Donneau,
M Vandenheede, A Maertens de Noordhout, J Schoenen,
L Seidel
Biostatistics–Medical Informatics, University of Liège, Liège, Belgium
Search for more papers by this authorA-F Donneau
Biostatistics–Medical Informatics, University of Liège, Liège, Belgium
Search for more papers by this authorCorresponding Author
J Schoenen
Departments of Neurology
Neuroanatomy
Prof. Dr J. Schoenen, Headache Research Unit, University Department of Neurology, CHR Citadelle, B-4000 Liege, Belgium. Tel. + 32 4225 6111, fax + 32 4225 6451, e-mail [email protected]Search for more papers by this authorA Fumal, G Coppola, V Bohotin, P-Y Gérardy, L Seidel,
A-F Donneau,
M Vandenheede, A Maertens de Noordhout, J Schoenen,
L Seidel
Biostatistics–Medical Informatics, University of Liège, Liège, Belgium
Search for more papers by this authorA-F Donneau
Biostatistics–Medical Informatics, University of Liège, Liège, Belgium
Search for more papers by this authorCorresponding Author
J Schoenen
Departments of Neurology
Neuroanatomy
Prof. Dr J. Schoenen, Headache Research Unit, University Department of Neurology, CHR Citadelle, B-4000 Liege, Belgium. Tel. + 32 4225 6111, fax + 32 4225 6451, e-mail [email protected]Search for more papers by this authorAbstract
We have shown that in healthy volunteers (HV) one session of 1 Hz repetitive transcranial magnetic stimulation (rTMS) over the visual cortex induces dishabituation of visual evoked potentials (VEPs) on average for 30 min, while in migraineurs one session of 10 Hz rTMS replaces the abnormal VEP potentiation by a normal habituation for 9 min. In the present study, we investigated whether repeated rTMS sessions (1 Hz in eight HV; 10 Hz in eight migraineurs) on 5 consecutive days can modify VEPs for longer periods. In all eight HV, the 1 Hz rTMS-induced dishabituation increased in duration over consecutive sessions and persisted between several hours (n = 4) and several weeks (n = 4) after the fifth session. In six out eight migraineurs, the normalization of VEP habituation by 10 Hz rTMS lasted longer after each daily stimulation but did not exceed several hours after the last session, except in two patients, where it persisted for 2 days and 1 week. Daily rTMS can thus induce long-lasting changes in cortical excitability and VEP habituation pattern. Whether this effect may be useful in preventative migraine therapy remains to be determined.
References
- 1 Hallett M. Transcranial magnetic stimulation and the human brain. Nature 2000; 406: 147–50.
- 2 Kobayashi M, Pascual-Leone A. Transcranial magnetic stimulation in neurology. Lancet Neurol 2003; 2: 145–56.
- 3 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: 912–22.
- 4 Fumal A, Bohotin V, Vandenheede M, Seidel L, De Pasqua V, Maertens de Noordhout A, Schoenen J. Effects of repetitive transcranial magnetic stimulation on visual evoked potentials: new insights in healthy subjects. Exp Br Res 2003; 150: 332–40.
- 5 Schoenen J, Ambrosini A, Sandor 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: 955–72.
- 6 Schoenen J. Pathogenesis of migraine: the biobehavioural and hypoxia theories reconciled. Acta Neurologica Belgica 1994; 94: 79–86.
- 7 Sappey-Marinier D, Calabrese G, Fein G, Hugg JW, Biggins C, Weiner MW. Effect of photic stimulation on human visual cortex lactate and phosphates using 1H and 31P magnetic resonance spectroscopy. J Cereb Blood Flow Metab 1992; 12: 584–92.
- 8 Judit A, Sandor PS, 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: 714–9.
- 9 Siniatchkin M, Gerber WD, Kropp P, Vein A. How the brain anticipates an attack: a study of neurophysiological periodicity in migraine. Funct Neurol 1999; 14: 69–77.
- 10 Kropp P, Gerber WD. Contingent negative variation during migraine attack and interval: evidence for normalization of slow cortical potentials during the attack. Cephalalgia 1995; 15: 123–8.
- 11 McKay DR, Ridding MC, Thompson PD, Miles MS. Induction of persistent changes in the organisation of the motor cortex. Exp Br Res 2002; 143: 342–9.
- 12 Mottaghy FM, Keller CE, Gangitano M, Ly J, Thall M, Parker JA, Pascual-Leone A. Correlation of cerebral blood flow and treatments effects of repetitive transcranial magnetic stimulation in depressed patients. Psychiatry Res Neuroimaging 2002; 115: 1–14.
- 13 Baumer T, Lange R, Liepert J, Weiller C, Siebner HR, Rothwell JC, Munchau A. Repeated premotor rTMS leads to cumulative plastic changes of motor cortex excitability in humans. Neuroimage 2003; 20: 550–60.
- 14 Wassermann EM, Lisanby SH. Therapeutic application of repetitive transcranial magnetic stimulation: a review. Clin Neurophysiol 2001; 112: 1367–77.
- 15 International Headache Society. The international classification of headache disorders, 2nd edition. Cephalalgia 2004; 24 (Suppl. 1): 1–160.
- 16 Chen R, Gerloff C, Classen J, Wassermann EM, Hallett M, Cohen LG. Safety of different inter-train intervals for repetitive transcranial magnetic stimulation and recommendations for safe ranges of stimulation parameters. Electroencephalogr Clin Neurophysiol 1997; 105: 415–21.
- 17 Smith MJ, Keel JC, Greenberg BD, Adams LF, Schmidt PJ, Rubinow DA, Wasserman EM. Menstrual cycle effects on cortical excitability. Neurology 1999; 53: 2069–72.
- 18 Bohotin V, Bohotin C, Fumal A, Schoenen J. Cortical excitability changes during the ovarian cycle: a comparative study between healthy volunteers and migraine patients. Cephalalgia 2003; 23: 684.
- 19 Fumal A, Bohotin V, Vandenheede M, Seidel L, Maertens de Noordhout A, Schoenen J. Motor and phosphene thresholds to transcranial magnetic stimuli: a reproducibility study. Acta Neurologica Belgica 2002; 102: 171–5.
- 20 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: 264–70.
- 21 Boroojerdi B, Prager A, Muellbacher W, Cohen LG. Reduction of human visual cortex excitability using 1-Hz transcranial magnetic stimulation. Neurology 2000; 54: 1529–31.
- 22 Brighina F, Piazza A, Daniele O, Fierro B. Modulation of visual cortex excitability in migraine with aura: effects of 1 Hz repetitive transcranial magnetic stimulation. Exp Brain Res 2002; 145: 177–81.
- 23 Young WB, Oshinsky ML, Shechter AL, Gebeline-Myers C, Bradley KC, Wassermann EM. Consecutive transcranial magnetic stimulation: phosphene thresholds in migraineurs and controls. Headache 2004; 44: 131–5.
- 24 Chen R, Classen J, Gerloff C, Celnik P, Wassermann EM, Hallet M, Cohen LG. Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology 1997; 48: 1398–403.
- 25 Wu T, Sommer M, Tergau F, Paulus W. Lasting influence of repetitive transcranial magnetic stimulation on intracortical excitability in human subjects. Neurosci Lett 2000; 287: 37–40.
- 26 Gerschlager W, Siebner HR, Rothwell JC. Decreased corticospinal excitability after subthreshold 1 Hz rTMS over lateral premotor cortex. Neurology 2001; 57: 449–55.
- 27 Munchau A, Bloem BR, Irlbacher K, Trimble MR, Rothwell JC. Functional connectivity of human premotor and motor cortex explored with repetitive transcranial magnetic stimulation. J Neurosci 2002; 22: 554–61.
- 28 Knott JR, Irwin DA. Anxiety, stress and the contingent negative variation. Arch General Psychiatry 1973; 29: 538–41.
- 29 Schoenen J. Deficient habituation of evoked cortical potentials in migraine: a link between brain biology, behavior and trigeminovascular activation? Biomed Pharmacother 1996; 50: 71–8.
- 30 Sandor PS, Dydak U, Schoenen J, Kollias S, Hess K, Boesiger P, Agosti RM. Multi-voxel magnetic resonance spectroscopy during prolonged visual stimulation in subgroups of migraine with aura. Cephalalgia 2005 (in press).
- 31 Montagna P, Cortelli P, Monari L, Pierangeli G, Parchi P, Lodi R, et al. 31P-magnetic resonance spectroscopy in migraine without aura. Neurology 1994; 44: 666–9.
- 32 Kropp P, Siniatchkin M, Gerber WD. Contingent negative variation as indicator of duration of migraine disease. Funct Neurol 2000; 15 (Suppl. 3): 78–81.
- 33 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; 227: 67–71.
- 34 Evers S, Quibeldey F, Grotemeyer KH, Suhr B, Husstedt IW. Dynamic changes of cognitive habituation and serotonin metabolism during the migraine interval. Cephalalgia 1999; 19: 485–91.
- 35 Hegerl U, Juckel G. Intensity dependence of auditory evoked potentials as an indicator of central serotonergic neurotransmission: a new hypothesis. Biol Psychiatry 1993; 33: 173–87.
- 36 Bohotin V, Bohotin C, Fumal A, Vandenheede M, Schoenen J. Evidence from repetitive transcranial magnetic stimulation for increased excitability of visual cortex just before and during migraine attacks. Cephalalgia 2002; 22: 577.
