[en] Background: In previous studies we found that high-frequency somatosensory oscillations (HFOs) reflecting thalamo-cortical activation were decreased in migraineurs between attacks and that high-frequency repetitive transcranial magnetic stimulation (rTMS) was able to normalize the habituation deficit of visual evoked potentials (VEPs). Here we study the effects of activating (10 Hz) or inhibiting (1 Hz) rTMS on conventional low-frequency (LF) and high-frequency somatosensory evoked potentials (SSEPs). Subjects and methods: rTMS was applied on the motor cortex of 13 healthy volunteers (HVs) and 13 migraine without aura (MO) patients. We measured N20-P25 LF-SSEP amplitude and habituation, and maximal peak-to-peak amplitude of early and late HFOs before and after rTMS. Results: In HVs, 1 Hz rTMS significantly reduced the amplitude of the first LF-SSEP block and its habituation. In MO patients, 10 Hz rTMS increased the amplitude of the first block and induced habituation. Ten Hz rTMS produced an increase of late HFO in both groups, but more interestingly, in MO patients also significantly increased the early HFOs, which are reduced at baseline compared to those of HVs. Conclusions: These data confirm for SSEP that excitatory rTMS can normalize habituation in migraine patients and show that this is accompanied by early an HFO increase, which is thought to reflect thalamo-cortical activity. Taken together with similar effects we observed for VEPs, this finding supports the hypothesis that dysfunctioning thalamo-cortical loops may be responsible for the interictal habituation deficit in migraine.
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 (Pubitemid 26116392)
Coppola G, Pierelli F, Schoenen J. Habituation and migraine. Neurobiol Learn Mem. 2009 ; 92: 249-259
Aurora SK, Wilkinson F. The brain is hyperexcitable in migraine. Cephalalgia. 2007 ; 27: 1442-1453 (Pubitemid 350150807)
Mulleners WM, Chronicle EP, Palmer JE, et al. Visual cortex excitability in migraine with and without aura. Headache. 2001 ; 41: 565-572 (Pubitemid 32619260)
Brighina F, Palermo A, Fierro B. Cortical inhibition and habituation to evoked potentials: relevance for pathophysiology of migraine. J Headache Pain. 2009 ; 10: 77-84
Mesulam MM. Large-scale neurocognitive networks and distributed processing for attention, language, and memory. Ann Neurol. 1990 ; 28: 597-613
Hegerl U, Juckel G. Intensity dependence of auditory evoked potentials as an indicator of central serotonergic neurotransmission: a new hypothesis. Biol Psychiatry. 1993 ; 33: 173-187 (Pubitemid 23089966)
Gobbelé R, Buchner H, Curio G. High-frequency (600 Hz) SEP activities originating in the subcortical and cortical human somatosensory system. Electroencephalogr Clin Neurophysiol. 1998 ; 108: 182-189
Restuccia D, Della Marca G, Valeriani M, et al. Influence of cholinergic circuitries in generation of high-frequency somatosensory evoked potentials. Clin Neurophysiol. 2003 ; 114: 1538-1548 (Pubitemid 36897791)
Mochizuki H, Machii K, Terao Y, et al. Recovery function of and effects of hyperventilation on somatosensory evoked high-frequency oscillation in Parkinson's disease and myoclonus epilepsy. Neurosci Res. 2003 ; 46: 485-492 (Pubitemid 36842799)
Gobbelé R, Waberski TD, Thyerlei D, et al. Functional dissociation of a subcortical and cortical component of high-frequency oscillations in human somatosensory evoked potentials by motor interference. Neurosci Lett. 2003 ; 350: 97-100 (Pubitemid 37101422)
Gobbelé R, Waberski TD, Kuelkens S, et al. Thalamic and cortical high-frequency (600-Hz) somatosensory-evoked potential (SEP) components are modulated by slight arousal changes in awake subjects. Exp Brain Res. 2000 ; 133: 506-513 (Pubitemid 30609376)
Ikeda H, Leyba L, Bartolo A, et al. Synchronized spikes of thalamocortical axonal terminals and cortical neurons are detectable outside the pig brain with MEG. J Neurophysiol. 2002 ; 87: 626-630 (Pubitemid 34669977)
Porcaro C, Coppola G, Di Lorenzo G, et al. Hand somatosensory subcortical and cortical sources assessed by functional source separation: an EEG study. Hum Brain Mapp. 2009 ; 30: 660-674
Coppola G, Vandenheede M, Di Clemente L, et al. Somatosensory evoked high-frequency oscillations reflecting thalamo-cortical activity are decreased in migraine patients between attacks. Brain. 2005 ; 128: 98-103 (Pubitemid 40070524)
Lai K, Liao K, Fuh J, et al. Subcortical hyperexcitability in migraineurs: a high-frequency oscillation study. Can J Neurol Sci. 2011 ; 38: 309-316
Bohotin V, Fumal A, Vandenheede M, et al. Effects of repetitive transcranial magnetic stimulation on visual evoked potentials in migraine. Brain. 2002 ; 125: 912-922 (Pubitemid 34279785)
Fumal A, Coppola G, Bohotin V, et al. 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
Smith MJ, Keel JC, Greenberg BD, et al. Menstrual cycle effects on cortical excitability. Neurology. 1999 ; 53: 2069-2072
Maertens D, Pepin J, Schoenen J, et al. Percutaneous magnetic stimulation of the motor cortex in migraine. Electroencephalogr Clin Neurophysiol. 1992 ; 85: 110-115
Ozkul Y, Uckardes A. Median nerve somatosensory evoked potentials in migraine. Eur J Neurol. 2002 ; 9: 227-232 (Pubitemid 35013908)
Coppola G, Currà A, Di Lorenzo C, et al. Abnormal cortical responses to somatosensory stimulation in medication-overuse headache. BMC Neurol. 2010 ; 10: 126-126
Restuccia D, Ulivelli M, De Capua A, et al. Modulation of high-frequency (600-Hz) somatosensory-evoked potentials after rTMS of the primary sensory cortex. Eur J Neurosci. 2007 ; 26: 2349-2358 (Pubitemid 47620479)
Enomoto H, Ugawa Y, Hanajima R, et al. Decreased sensory cortical excitability after 1-Hz-rTMS over the ipsilateral primary motor cortex. Clin Neurophysiol. 2001 ; 112: 2154-2158 (Pubitemid 32995984)
Satow T, Mima T, Yamamoto J, et al. Short-lasting impairment of tactile perception by 0.9-Hz-rTMS of the sensorimotor cortex. Neurology. 2003 ; 60: 1045-1047 (Pubitemid 36348948)
Urushihara R, Murase N, Rothwell JC, et al. Effect of repetitive transcranial magnetic stimulation applied over the premotor cortex on somatosensory-evoked potentials and regional cerebral blood flow. Neuroimage. 2006 ; 31: 699-709 (Pubitemid 43776666)
Ragert P, Becker M, Tegenthoff M, et al. Sustained increase of somatosensory cortex excitability by 5 Hz repetitive transcranial magnetic stimulation studied by paired median nerve stimulation in humans. Neurosci Lett. 2004 ; 356: 91-94 (Pubitemid 38121476)
Siebner HR, Hartwigsen G, Kassuba T, et al. How does transcranial magnetic stimulation modify neuronal activity in the brain? Implications for studies of cognition. Cortex. 2009 ; 45: 1035-1042
Brighina F, Giglia G, Scalia S, et al. Facilitatory effects of 1-Hz-rTMS in motor cortex of patients affected by migraine with aura. Exp Brain Res. 2005 ; 161: 34-38 (Pubitemid 40238867)
Werhahn KJ, Wiseman K, Herzog J, et al. Motor cortex excitability in patients with migraine with aura and hemiplegic migraine. Cephalalgia. 2000 ; 20: 45-50 (Pubitemid 32250293)
Bohotin V, Fumal A, Vandenheede M, et al. 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 (Pubitemid 36577943)
Gunaydin S, Soysal A, Atay T, et al. Motor and occipital cortex excitability in migraine patients. Can J Neurol Sci. 2006 ; 33: 63-67
Ogawa A, Ukai S, Shinosaki K, et al. Slow repetitive transcranial magnetic stimulation increases somatosensory high-frequency oscillations in humans. Neurosci Lett. 2004 ; 358: 193-196 (Pubitemid 38368202)
Huang YZ, Edwards MJ, Rounis E, et al. Theta burst stimulation of the human motor cortex. Neuron. 2005 ; 45: 201-206 (Pubitemid 40128115)
Gobbelé R, Waberski TD, Simon H, et al. Different origins of low- and high-frequency components (600-Hz) of human somatosensory evoked potentials. Clin Neurophysiol. 2004 ; 115: 927-937 (Pubitemid 38293491)
Restuccia D, Micoli B, Cazzagon M, et al. Dissociated effects of quiet stance on standard and high-frequency (600-Hz) lower limb somatosensory evoked potentials. Clin Neurophysiol. 2008 ; 119: 1408-1418
Murakami T, Sakuma K, Nomura T, et al. Changes in somatosensory-evoked potentials and high-frequency oscillations after paired-associative stimulation. Exp Brain Res. 2008 ; 184: 339-347 (Pubitemid 350275881)
Thickbroom GW. Transcranial magnetic stimulation and synaptic plasticity: experimental framework and human models. Exp Brain Res. 2007 ; 180: 583-593 (Pubitemid 46988122)
Shin HC, Chapin JK. Movement induced modulation of afferent transmission to single neurons in the ventroposterior thalamus and somatosensory cortex in rat. Exp Brain Res. 1990 ; 81: 515-522 (Pubitemid 20258532)
Shin HC, Chapin JK. Mapping the effects of motor cortex stimulation on single neurons in the dorsal column nuclei in the rat: direct responses and afferent modulation. Brain Res Bull. 1989 ; 22: 245-252 (Pubitemid 19165306)
Fanselow EE, Nicolelis MA. Behavioral modulation of tactile responses in the rat somatosensory system. J Neurosci. 1999 ; 19: 7603-7616 (Pubitemid 29404616)
Strafella AP, Vanderwerf Y, Sadikot AF. Transcranial magnetic stimulation of the human motor cortex influences the neuronal activity of subthalamic nucleus. Eur J Neurosci. 2004 ; 20: 2245-2249 (Pubitemid 39331146)
Van D, Sadikot A, Strafella A, et al. The neural response to transcranial magnetic stimulation of the human motor cortex. II. Thalamocortical contributions. Exp Brain Res. 2006 ; 175: 246-255 (Pubitemid 44624483)
Wang H, Wang X, Scheich H. LTD and LTP induced by transcranial magnetic stimulation in auditory cortex. Neuroreport. 1996 ; 7: 521-525 (Pubitemid 26105032)
Chen R, Classen J, Gerloff C, et al. Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology. 1997 ; 48: 1398-1403 (Pubitemid 27240571)
Fitzgerald P, Fountain S, Daskalakis Z. A comprehensive review of the effects of rTMS on motor cortical excitability and inhibition. Clin Neurophysiol. 2006 ; 117: 2584-2596 (Pubitemid 44781313)
Heide G, Witte O, Ziemann U. Physiology of modulation of motor cortex excitability by low-frequency suprathreshold repetitive transcranial magnetic stimulation. Exp Brain Res. 2006 ; 171: 26-34
Hashimoto I, Mashiko T, Imada T. Somatic evoked high-frequency magnetic oscillations reflect activity of inhibitory interneurons in the human somatosensory cortex. Electroencephalogr Clin Neurophysiol. 1996 ; 100: 189-203
Coppola G, Crémers J, Gérard P, et al. Effects of light deprivation on visual evoked potentials in migraine without aura. BMC Neurol. 2011 ; 11: 91-91
Andin J, Enz A, Gentsch C, et al. Rivastigmine as a modulator of the neuronal glutamate transporter rEAAC1 mRNA expression. Dement Geriatr Cogn Disord. 2005 ; 19: 18-23 (Pubitemid 39664184)
Brighina F, Cosentino G, Vigneri S, et al. Abnormal facilitatory mechanisms in motor cortex of migraine with aura. Eur J Pain. 2011 ; 15: 928-935
Siebner H, Lang N, Rizzo V, et al. Preconditioning of low-frequency repetitive transcranial magnetic stimulation with transcranial direct current stimulation: evidence for homeostatic plasticity in the human motor cortex. J Neurosci. 2004 ; 24: 3379-3385 (Pubitemid 38451903)
Lang N, Siebner H, Ernst D, et al. Preconditioning with transcranial direct current stimulation sensitizes the motor cortex to rapid-rate transcranial magnetic stimulation and controls the direction of after-effects. Biol Psychiatry. 2004 ; 56: 634-639 (Pubitemid 39446844)
