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Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation
Abstract
We studied the effects of low-frequency transcranial magnetic stimulation (TMS) on motor cortex excitability in humans. TMS at 0.1 Hz for 1 hour did not change cortical excitability. Stimulation at 0.9 Hz for 15 minutes (810 pulses), similar to the parameters used to induce long-term depression (LTD) in cortical slice preparations and in vivo animal studies, led to a mean decrease in motor evoked potential (MEP) amplitude of 19.5%. The decrease in cortical excitability lasted for at least 15 minutes after the end of the 0.9 Hz stimulation. The mechanism underlying this decrease in excitability may be similar to LTD. TMS-induced reduction of cortical excitability has potential clinical applications in diseases such as epilepsy and myoclonus. Spread of excitation, which may be a warning sign for seizures, occurred in one subject and was not accompanied by increased MEP amplitude, suggesting that spread of excitation and amplitude changes are different phenomena and also indicating the need for adequate monitoring even with stimulations at low frequencies.
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“These data build upon studies in patients with depression [39,50] and provide a biological mechanism through which DLPFC may be effective at attenuating craving.”
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Ragert, P., Franzkowiak, S., Schwenkreis, P., Tegenthoff, M., & Dinse, H. R. (2007) · Experimental Brain Research · doi:10.1007/s00221-007-1073-2 · Cited by 97
“For example, low-frequency repetitive TMS (rTMS) (<5 Hz) usually results in suppression of cortical excitability (Chen et al. 1997; Muellbacher et al. 2000; Romero et al. 2002), whereas high-frequency rTMS ( ̧5 Hz) is known to facilitate cortical excitability within the stimulated cortical area (Peinemann et al.”
BackgroundStereotaxic rTMS for the treatment of auditory hallucinations in schizophrenia
Schönfeldt‐Lecuona, C., Grön, G., Walter, H., Büchler, N., Wunderlich, A. P., Spitzer, M., & Herwig, U. (2004) · Neuroreport · doi:10.1097/01.wnr.0000126504.89983.ec · Cited by 97
“The observation that a low frequency stimulation (r1Hz) may decrease excitability of cortical neurons [5,6] suggests a therapeutic value against pathological hyperactivity of cortical areas [7].”
BackgroundFumal, A., Coppola, G., Bohotin, V., Gérardy, P.-Y., Seidel, L., Donneau, A., Vandenheede, M., de Noordhout, A. D., & Schoenen, J. (2006) · Cephalalgia · doi:10.1111/j.1468-2982.2005.01013.x · Cited by 104
“According to International Headache Society criteria ( 15 ), six patients had migraine without aura (MoA, code 1.1) and two migraine with typical aura (MA, code 1.2.1).”
BackgroundInfluentialTöpper, R., Foltys, H., Meister, I., Sparing, R., & Boroojerdi, B. (2003) · Clinical Neurophysiology · doi:10.1016/s1388-2457(03)00117-2 · Cited by 98
“In a number of studies it has been shown that applying trains of repetitive TMS (rTMS) can have effects on the brain which outlast the actual stimulation (Chen et al., 1997; Mottaghy et al., 1999; Boroojerdi et al., 2000).”
BackgroundRole of the Posterior Parietal Cortex in Spatial Hearing
Lewald, J., Foltys, H., & Töpper, R. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-03-j0005.2002 · Cited by 102
“Transient alterations of the activity of the stimulated area have been shown to persist for several minutes after application of rTMS (Pascual-Leone et al., 1994; Chen et al., 1997; Mottaghy et al., 1999; Töpper et al., 1999).”
MethodInfluentialKakuda, W., Abo, M., Kobayashi, K., et al. (2011) · Brain Injury · doi:10.3109/02699052.2011.559610 · Cited by 96
“Since both suppressive 1 Hz rTMS over the nonlesional hemisphere and facilitatory 5 Hz rTMS over the lesional hemisphere can increase the neural activity in the lesional hemisphere [25, 26], it can be speculated that neural activation in the lesional hemisphere might lead to a reduction of spasticity in the affected l…”
BackgroundPharmacological Modulation of Plasticity in the Human Motor Cortex
Ziemann, U., Meintzschel, F., Korchounov, A., & Ilić, T. (2006) · Neurorehabilitation and Neural Repair · doi:10.1177/1545968306287154 · Cited by 88
Hamidi, M. (2009) · Frontiers in Integrative Neuroscience · doi:10.3389/neuro.07.014.2009 · Cited by 96
Zafar, N., Paulus, W., & Sommer, M. (2008) · Clinical Neurophysiology · doi:10.1016/j.clinph.2008.02.006 · Cited by 96
“Two types of conventional rTMS The inhibitory 1 Hz rTMS protocol applied over 15 min (900 pulses) with an intensity of 90% resting motor threshold (RMT) reduces motor cortex excitability over a period of 30 min up to 1 h (Chen et al., 1997).”
BackgroundMethodNi, Z., & Chen, R. (2015) · Translational Neurodegeneration · doi:10.1186/s40035-015-0045-x · Cited by 93
“One Hz rTMS, which produced MEP inhibition in healthy controls [47], had no effect in AD patients [69].”
BackgroundMethodSelf-citationGoetz, S. M., Luber, B. M., Lisanby, S. H., Murphy, D. L. K., Kozyrkov, I. C., Grill, W. M., & Peterchev, A. V. (2015) · Brain stimulation · doi:10.1016/j.brs.2015.08.013 · Cited by 93
“0% (20%) for SB rTMS, compared to 3 (2) for RU-N, 2 (1) for RU-R, and 4 (2) for RB.”
BackgroundFierro, B., Brighina, F., Vitello, G., Piazza, A., Scalia, S., Giglia, G., Daniele, O., & Pascual‐Leone, Á. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2004.080184 · Cited by 94
“In healthy subjects, low-frequency rTMS (1 Hz) has been demonstrated to generally induce a lasting decrease in motor (Chen et al. 1997) and visual (Boroojerdi et al.”
BackgroundThirugnanasambandam, N., Sparing, R., Dafotakis, M., Meister, I. G., Paulus, W., Nitsche, M. A., & Fink, G. R. (2011) · Restorative Neurology and Neuroscience · doi:10.3233/rnn-2011-0601 · Cited by 104
“…of tDCS on these two parameters of intracortical inhibition might be caused by the fact that CSP is solely mediated by the GABAergic system (Ziemann et al., 1996a), while NMDA receptors seem to be additionally involved in SICI (Chen et al., 1997; Liepert et al., 1997; Ziemann et al., 1996a, 1998).”
Transcranial Magnetic Stimulation in Clinical Psychiatry
Belmaker, R. H. (2006) · American Psychiatric Association Publishing eBooks · doi:10.1176/appi.books.9781615377510 · Cited by 96
Kauffmann, C. D., Cheema, M. A., & Miller, B. E. (2004) · Depression and Anxiety · doi:10.1002/da.10144 · Cited by 95
“Depending on stimulation parameters (frequency, rate, and duration), repetitive stimuli to specific cortical regions can either decrease or enhance the excitability of the affected brain structures [Chen et al., 1997; Pascual-Leone et al., 1994, 1996a].”
BackgroundArai, N., Okabe, S., Furubayashi, T., Mochizuki, H., Iwata, N. K., Hanajima, R., Terao, Y., & Ugawa, Y. (2007) · Clinical Neurophysiology · doi:10.1016/j.clinph.2007.07.006 · Cited by 94
“Low-frequency rTMS Chen et al. (1997) 0.”
BackgroundBütefisch, C. M., Kleiser, R., & Seitz, R. J. (2006) · Journal of Physiology-Paris · doi:10.1016/j.jphysparis.2006.03.001 · Cited by 95
Santiago-Rodríguez, E., Cárdenas-Morales, L., Harmony, T., Fernandez-bouzas, A., Porras-Kattz, E., & Hernandez, A. (2008) · Seizure · doi:10.1016/j.seizure.2008.04.005 · Cited by 94
“Longterm depression-like mechanisms have been also postulated as responsible for a diminution in the number of seizures.(1,3) The permanence of the effect for 3 weeks after the end of rTMS together with the slow return to baseline frequency supports this concept.”
BackgroundSummers, J. J., Johnson, S., PRIDMORE, S. A., & Oberoi, G. (2004) · Neuroscience Letters · doi:10.1016/j.neulet.2004.07.008 · Cited by 94
Yang, Y., Tseng, C.-Y., Chiou, S., Liao, K., Cheng, S., Lai, K., & Wang, R. (2012) · Neurorehabilitation and neural repair · doi:10.1177/1545968312451915 · Cited by 96
“Low-frequency stimulation induced depression of cortical excitability, whereas high-frequency stimulation induced facilitation.(11,12) These changes in cortical excitability are transient, lasting 10 to 30 minutes.”
BackgroundLasting effects of repeated rTMS application in focal hand dystonia
Borich, M. R., Arora, S., & Kimberley, T. J. (2009) · Restorative Neurology and Neuroscience · doi:10.3233/rnn-2009-0461 · Cited by 94
“Low frequency rTMS (≤ 1 Hz) has been shown to produce inhibitory effects on neuronal excitability (Chen et al., 1997) and rTMS to PMC led to a reduction in regional neural activity for at least one hour after the end of stimulation.”
Inhibition of return and the human frontal eye fields
Ro, T., Farnè, A., & Chang, E. C. (2003) · Experimental Brain Research · doi:10.1007/s00221-003-1470-0 · Cited by 98
“2002), and that this along with the intermittent TMS pulses delivered to the FEF in this condition may have produced disruption of visual processing beyond the immediate effects of the TMS pulse, as has been shown with 1 Hz stimulation (Chen et al. 1997; Kosslyn et al. 1999).”
BackgroundLow frequency rTMS of the SMA transiently ameliorates peak-dose LID in Parkinson’s disease
Brusa, L., Versace, V., Koch, G., Iani, C., Stanzione, P., Bernardi, G., & Centonze, D. (2006) · Clinical Neurophysiology · doi:10.1016/j.clinph.2006.03.033 · Cited by 97
“This finding is in agreement with previous studies demonstrating that the reduction of cortical excitability induced by 1 Hz rTMS outlast the period of stimulation in a range from minutes to hours, depending on the duration of the trains (Chen et al., 1997; Munchau et al., 2002).”
ResultTheta-burst stimulation: Remote physiological and local behavioral after-effects
Stefan, K., Gentner, R., Zeller, D., Dang, S., & Claßen, J. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.11.037 · Cited by 94
“037 slow uniform repetition frequencies around 1 Hz, rTMS leads to a sustained reversible decrease of corticospinal excitability (Chen et al., 1997).”
BackgroundInfluentialSelf-citationTranscranial magnetic stimulation in cognitive rehabilitation
Miniussi, C., & Rossini, P. M. (2011) · Neuropsychological Rehabilitation · doi:10.1080/09602011.2011.562689 · Cited by 94
“Namely, high-frequency stimulation has been shown to produce an increase in the MEP amplitude (Maeda, Keenan, Tormos, Topka, & Pascual-Leone, 2000), whereas low-frequency stimulation produced a decrease in the MEP amplitude (Chen et al., 1997; Maeda et al., 2000).”
Transcranial Magnetic Stimulation and Aphasia Rehabilitation
Naeser, M. A., Martin, P. I., Ho, M. D., Treglia, E., Kaplan, E., Bashir, S., & Pascual‐Leone, Á. (2011) · Archives of Physical Medicine and Rehabilitation · doi:10.1016/j.apmr.2011.04.026 · Cited by 92
“Slow rTMS, where magnetic pulse is applied every second (1Hz), delivered to he motor cortex can give rise to a lasting decrease in corticopinal excitability.(7,8) Conversely, fast rTMS (5, 10, or 20Hz) an induce a transient increase in cortical excitability.”
BackgroundConcerto, C., Lanza, G., Cantone, M., Ferri, R., Pennisi, G., Bella, R., & Aguglia, E. (2015) · International Journal of Psychiatry in Clinical Practice · doi:10.3109/13651501.2015.1084329 · Cited by 99
“When a constant interstimulus interval is used, low-frequency rTMS ( 1 Hz) produces a decrease in the excitability of the motor cortex (Chen et al. 1997), whereas higher frequencies (5 Hz or more) determine an increase in excitation (Pascual-Leone et al. 1994; Berardelli et al. 1998; Maeda et al.…”
MethodJulkunen, P., Säïsänen, L., Hukkanen, T., Danner, N., & Könönen, M. (2011) · Brain stimulation · doi:10.1016/j.brs.2011.07.006 · Cited by 93
Breaks during 5 Hz rTMS are essential for facilitatory after effects
Rothkegel, H., Sommer, M., & Paulus, W. (2009) · Clinical Neurophysiology · doi:10.1016/j.clinph.2009.11.016 · Cited by 93
“Prolonged continuous stimulation has been applied mainly to inhibitory 1 Hz paradigms (Chen et al., 1997), but to our knowledge there are only few studies using prolonged high frequency continuous stimulation and none of these exam-”
MethodTranscranial magnetic stimulation: a new investigational and treatment tool in psychiatry.
Daskalakis, Z., Christensen, B., Fitzgerald, P., & Chen, R. (2002) · The Journal of Neuropsychiatry and Clinical Neurosciences · doi:10.1176/jnp.14.4.406 · Cited by 387
“The mechanisms behind such inhibition are unclear, although there are similarities to long-term depresssion.(38) In contrast, stimulation at frequencies above 1 Hz has been shown to induce increased cortical activation.”
BackgroundSelf-citationHanlon, C. A., Dowdle, L. T., & Henderson, J. (2018) · Pharmacological Reviews · doi:10.1124/pr.116.013649 · Cited by 101
Auditory cortex stimulation for tinnitus
Ridder, D. A., Mulder, G. D., Verstraeten, E., Seidman, M. D., Elisevich, K. V., Sunaert, S. G., Kovacs, S., der Kelen, K. V., de Heyning, P. V., & Møller, A. R. (2007) · Springer eBooks · doi:10.1007/978-3-211-33081-4_52 · Cited by 93
“1 Hz, on the other hand, reduces cortical excitability [10, 35] for periods of up to 30 minutes [9]; this correlates with the longer suppression of tinnitus seen at 1Hz stimulation [27, 61, 62].”
BackgroundMisawa, S., Kuwabara, S., Shibuya, K., Mamada, K., & Hattori, T. (2005) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2005.03.035 · Cited by 91
Jefferson, S., Mistry, S., Michou, E., Singh, S., Rothwell, J. C., & Hamdy, S. (2009) · Gastroenterology · doi:10.1053/j.gastro.2009.04.056 · Cited by 92
Ozaki, I., & Hashimoto, I. (2011) · Clinical Neurophysiology · doi:10.1016/j.clinph.2011.05.023 · Cited by 94
“Effects of repetitive TMS (rTMS) on motor cortex activity are inhibitory when a stimulus frequency is lower than 1 Hz (Chen et al., 1997; Gerschlager et al., 2001) or excitatory when it is higher than 1 Hz (high-frequency rTMS) (Di Lazzaro et al., 2002; Matsunaga et al., 2005).”
Loo, C. K. A., Katalinic, N., Mitchell, P. B., & Greenberg, B. D. (2010) · Journal of Affective Disorders · doi:10.1016/j.jad.2010.08.017 · Cited by 92
Temporal dynamics of motor cortex excitability during perception of natural emotional scenes
Borgomaneri, S., Gazzola, V., & Avenanti, A. (2013) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nst139 · Cited by 101
“This way the interpulse interval was >10 s, thereby avoiding changes in motor excitability due to TMS per se (Chen et al., 1997).”
BackgroundPleger, B., Blankenburg, F., Bestmann, S., Ruff, C. C., Wiech, K., Stephan, K. E., Friston, K. J., & Dolan, R. J. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4097-05.2006 · Cited by 94
“, 1999) or inhibit excitability (Chen et al., 1997) and produce controllable, consistent, long-lasting effects on cortex physiology (Huang et al.”
BackgroundRepetitive Transcranial Magnetic Stimulation Treatment for Chronic Tinnitus
Folmer, R. L., Theodoroff, S. M., Casiana, L., Shi, Y., Griest, S. E., & Vachhani, J. J. (2015) · JAMA Otolaryngology–Head & Neck Surgery · doi:10.1001/jamaoto.2015.1219 · Cited by 91
Levodopa increases memory encoding and dopamine release in the striatum in the elderly.
Flöel, A., Garraux, G., Xu, B., Breitenstein, C., Knecht, S., Herscovitch, P., & Cohen, L. G. (2008) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2006.10.009 · Cited by 95
“1 Hertz (Hz), a rate that does not affect cortical excitability [13].”
BackgroundSelf-citationSachdev, P. S., McBride, R., Loo, C. K. A., Mitchell, P. M., Malhi, G. S., & Croker, V. (2002) · Biological Psychiatry · doi:10.1016/s0006-3223(01)01298-7 · Cited by 88
On the role of the SMA in the discrete sequence production task: a TMS study
Verwey, W. B., Lammens, R., & van Honk, J. (2002) · Neuropsychologia · doi:10.1016/s0028-3932(01)00221-4 · Cited by 96
“Slow rTMS depresses cortical excitability [5,24], thus if the SMA is involved in selecting elements of familiar sequences from cortical sequence representations, the inhibitory effects of rTMS should slow execution of all response elements to an equal degree.”
BackgroundKirton, A. (2013) · Pediatric Neurology · doi:10.1016/j.pediatrneurol.2012.08.001 · Cited by 102
Neuromodulation of delay discounting, the reflection effect, and cigarette consumption
Sheffer, C. E., Mennemeier, M., Landes, R. D., Bickel, W. K., Brackman, S. L., Dornhoffer, J. L., Kimbrell, T. A., & Brown, G. J. (2013) · Journal of Substance Abuse Treatment · doi:10.1016/j.jsat.2013.01.012 · Cited by 96
Seeing fearful body language rapidly freezes the observer's motor cortex
Borgomaneri, S., Vitale, F., Gazzola, V., & Avenanti, A. (2015) · Cortex · doi:10.1016/j.cortex.2015.01.014 · Cited by 88
Kinoshita, M., Ikeda, A., Begum, T., Yamamoto, J., Hitomi, T., & Shibasaki, H. (2005) · Seizure · doi:10.1016/j.seizure.2005.05.002 · Cited by 91
Waldowski, K., Seniów, J. B., Leśniak, M., Iwański, S., & Członkowska, A. (2012) · The Scientific World JOURNAL · doi:10.1100/2012/518568 · Cited by 90
Effects of repetitive cortical stimulation on the silent period evoked by magnetic stimulation
Berardelli, A., Inghilleri, M., Gilio, F., Romeo, S., Pedace, F., Currà, A., & Manfredi, M. (1999) · Experimental Brain Research · doi:10.1007/s002210050661 · Cited by 90
A Physiological Signal That Prevents Motor Skill Improvements during Consolidation
Tunovic, S., Press, D. Z., & Robertson, E. M. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.3497-13.2014 · Cited by 96
“…replicating this signal may explain how applying 1 Hz TMS immediately after learning, which decreases corticospinal excitability, prevents off-line improvements over wakefulness, but these improvements still occurred over sleep (Chen et al., 1997; Robertson et al., 2005; Kantak et al., 2010).”
BackgroundMcLoughlin, D., Mogg, A., Eranti, S., Pluck, G., Purvis, R., Edwards, D., Landau, S., Brown, R. G., Rabe-Heskith, S., Howard, R., et al. (2007) · Health Technology Assessment · doi:10.3310/hta11240 · Cited by 93
Pellicciari, M. C., Miniussi, C., Ferrari, C., Koch, G., & Bortoletto, M. (2015) · Clinical Neurophysiology · doi:10.1016/j.clinph.2015.03.002 · Cited by 89
“By applying this protocol we found an effect that it is not in line with the motor cortex excitability inhibition, usually observed after low frequency rTMS (Chen et al., 1997).”
BackgroundResultInfluentialChung, C. L. H., & Mak, K. Y. (2016) · Brain stimulation · doi:10.1016/j.brs.2016.03.017 · Cited by 88
“Cortical excitability can be enhanced by high-frequency rTMS [9] whereas low-frequency rTMS induces the depression of cortical activity [10].”
BackgroundChen, W., Mima, T., Siebner, H. R., Oga, T., Hara, H., Satow, T., Begum, T., Nagamine, T., & Shibasaki, H. (2003) · Clinical Neurophysiology · doi:10.1016/s1388-2457(03)00063-4 · Cited by 86
“The motor cortex excitability was often measured by TMS (Chen et al., 1997; Siebner et al., 1999; Muellbacher et al., 2000; Maeda et al., 2000; Touge et al., 2001), which applied artificial external stimulation and, therefore, might not reflect the physiological changes that occur during natural…”
BackgroundInfluentialCorrelation between motor and phosphene thresholds: A transcranial magnetic stimulation study
Deblieck, C., Thompson, B. S., Iacoboni, M., & Wu, A. D. (2007) · Human Brain Mapping · doi:10.1002/hbm.20427 · Cited by 85
Beaulieu, L., Flamand, V. H., Massé‐Alarie, H., & Schneider, C. (2016) · Brain stimulation · doi:10.1016/j.brs.2016.12.008 · Cited by 84
Barwood, C., Murdoch, B., Whelan, B., Lloyd, D., Riek, S., O'Sullivan, J., Coulthard, A., Wong, A., Aitken, P., & Hall, G. (2011) · NeuroRehabilitation (Reading, MA) · doi:10.3233/nre-2011-0640 · Cited by 92
“Previous studies have verified the inhibitory effects of 1 Hz frequency rTMS on cortical brain tissue in humans [8,31] and the inhibitory effect on event related brain potentials after stimulation of at least 15 minutes [18].”
Pennisi, G., Ferri, R., Lanza, G., Cantone, M., Pennisi, M., Puglisi, V., Malaguarnera, G., & Bella, R. (2011) · Journal of Neural Transmission · doi:10.1007/s00702-010-0554-9 · Cited by 85
“…frequency (C5 Hz) transiently enhances motor excitability (Pascual-Leone et al. 1994), whereas slow rTMS (1 Hz) transiently depresses excitability (Chen et al. 1997), although both frequencies of stimulation may have similar positive effects in some pathological conditions, depending on the site…”
Interhemispheric effects of high and low frequency rTMS in healthy humans
Gorsler, A., Bäumer, T., Weiller, C., Münchau, A. M., & Liepert, J. (2003) · Clinical Neurophysiology · doi:10.1016/s1388-2457(03)00157-3 · Cited by 91
“1 Hz or less) inhibitory (Chen et al., 1997).”
BackgroundDyskinesia in Parkinson's disease: mechanisms and current non‐pharmacological interventions
Heumann, R., Moratalla, R., Herrero, M. T., Chakrabarty, K., Drucker-Colı́n, R., García-Montes, J. R., Simola, N., & Morelli, M. (2014) · Journal of Neurochemistry · doi:10.1111/jnc.12751 · Cited by 94
“Previous studies have used rTMS to reduce motor impairment in PD. rTMS at frequencies of 5 Hz and higher can enhance motor cortex excitability (Pascual-Leone et al. 1994), whereas lower frequencies rTMS (1 Hz and lower) can transiently depress cortical excitability (Chen et al. 1997).”
BackgroundMechanisms and the Current State of Transcranial Magnetic Stimulation
George, M. S., Nahas, Z. H., Kozel, F. A., Li, X., Yamanaka, K., Mishory, A., & Bohning, D. E. (2003) · CNS Spectrums · doi:10.1017/s1092852900018976 · Cited by 86
Turi, Z., Lenz, M., Paulus, W., Mittner, M., & Vlachos, A. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.15195 · Cited by 84
“, 1 Hz) [12], whereas patterned protocols combine 181 at least two stimulation frequencies (e.”
BackgroundFregni, F., Thomé-Souza, S., Bermpohl, F., Marcolin, M. A., Herzog, A. G., Pascual‐Leone, Á., & Valente, K. D. R. (2005) · Stereotactic and Functional Neurosurgery · doi:10.1159/000086674 · Cited by 84
“While these previous studies focused only on the clinical effect of rTMS in epilepsy patients, the present study extends this investigation. In addition to clinical outcome measures, we used EEG to address the question of whether rTMS might cause electrophysiological changes in patients with MCD and refractory epileps…”
ResultMechanisms underlying human motor system plasticity
Boroojerdi, B., Ziemann, U., Chen, R. E., Bütefisch, C. M., & Cohen, L. G. (2001) · Muscle & Nerve · doi:10.1002/mus.1045 · Cited by 85
“This rate has been shown not to modify motor cortical excitability in the absence of ischemia.(28) Under ischemic nerve block, rTMS of the contralateral (‘plastic‘) motor cortex led to enhancement of ischemia-induced increase in MEP size.”
BackgroundSelf-citationVeniero, D., Brignani, D., Thut, G., & Miniussi, C. (2011) · Psychophysiology · doi:10.1111/j.1469-8986.2011.01218.x · Cited by 85
Sauseng, P., Feldheim, J. F., Freunberger, R., & Hummel, F. C. (2011) · Frontiers in Psychology · doi:10.3389/fpsyg.2011.00241 · Cited by 84
“However, their behavioral data was used in the current analysis.”
BackgroundMethodLanza, G., Cantone, M., Aricò, D., Lanuzza, B., Cosentino, F., Paci, D., Papotto, M., Pennisi, M., Bella, R., Pennisi, G., et al. (2018) · Therapeutic Advances in Neurological Disorders · doi:10.1177/1756286418759973 · Cited by 82
Soleimani, R., Jalali, M., & Hasandokht, T. (2016) · European Archives of Oto-Rhino-Laryngology · doi:10.1007/s00405-015-3642-5 · Cited by 106
The Effects of Transcranial Stimulation on Paretic Lower Limb Motor Excitability During Walking
Jayaram, G., & Stinear, J. W. (2009) · Journal of Clinical Neurophysiology · doi:10.1097/wnp.0b013e3181af1d41 · Cited by 84
“Although the mechanisms underlying this effect are still unclear, the frequency-specific effects of iRTMS have been likened to long-term depression (Chen et al., 1997).”
BackgroundBrunoni, A. R., Teng, C. T., Correa, C. F., Imamura, M., Brasil-Neto, J. P., Boëchat‐Barros, R., Rosa, M. A., Caramelli, P., Cohen, R. B., Porto, J. A. D., et al. (2010) · Arquivos de Neuro-Psiquiatria · doi:10.1590/s0004-282x2010000300021 · Cited by 86
Transcranial magnetic brain stimulation modulates blepharospasm
Kranz, G., Shamim, E. A., Lin, P. T., Kranz, G. S., & Hallett, M. (2010) · Neurology · doi:10.1212/wnl.0b013e3181f8814d · Cited by 84
Self-citationChistyakov, A. V. (2001) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.70.5.580 · Cited by 84
“confirms this conclusion. The authors demonstrated a reduced intracortical inhibition in the affected hemisphere in patients after acute stroke using a paired pulse paradigm. On the other hand, an enhanced cortical inhibition as evidenced by the unilateral prolongation of the SPD was found in the same patients. In tha…”
BackgroundTranscranial magnetic stimulation: applications in basic neuroscience and neuropsychopharmacology
Lisanby, S. H., Luber, B. M., Perera, T. D., & Sackeïm, H. A. (2000) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145700002005 · Cited by 84
“These effects last beyond the duration of the rTMS trains themselves (Chen et al., 1997).”
BackgroundTranscranial magnetic stimulation (TMS) for schizophrenia
Dougall, N. J., Maayan, N., Soares‐Weiser, K., McDermott, L. M., & McIntosh, A. M. (2015) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd006081.pub2 · Cited by 86
An animal model of attention deficit hyperactivity disorder
Gainetdinov, R. R., & Caron, M. G. (2000) · Molecular Medicine Today · doi:10.1016/s1357-4310(99)01616-0 · Cited by 84
Bottom-Up and Top-Down Visuomotor Responses to Action Observation
Ubaldi, S., Barchiesi, G., & Cattaneo, L. (2013) · Cerebral Cortex · doi:10.1093/cercor/bht295 · Cited by 81
“The aftereffects of 1-Hz rTMS are expected to be about as long as the duration of the train of stimulation itself (Chen et al. 1997, 2003).”
BackgroundBaur, D., Galevska, D., Hussain, S. J., Cohen, L. G., Ziemann, U., & Zrenner, C. (2020) · Brain stimulation · doi:10.1016/j.brs.2020.09.005 · Cited by 86
“[20], it was one of the first rTMS plasticity protocols to be characterized, and influential for the development of other rTMS protocols [21].”
Self-citationThe value of neuronavigated rTMS for the treatment of depression
Schönfeldt‐Lecuona, C., Lefaucheur, J. P., Cárdenas‐Morales, L., Wolf, R. C., Kammer, T., & Herwig, U. (2009) · Neurophysiologie Clinique · doi:10.1016/j.neucli.2009.06.004 · Cited by 84
“Pioneering studies on motor cortex (M1) showed that rTMS delivered at low frequencies (≤ 1 Hz) for several minutes was able to transiently reduce the amplitude of motor evoked potentials (MEP), thus reflecting a transitory decrease in cortical excitability [7], whereas short trains at high frequencies (≥ 5 Hz) increas…”
BackgroundZwanzger, P., Steinberg, C., Rehbein, M. A., Bröckelmann, A., Dobel, C., Zavorotnyy, M., Domschke, K., & Junghöfer, M. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2014.07.003 · Cited by 83
“In contrast to the rule of thumb that inhibitory TMS effects on motor cortex excitability last for as long as TMS was applied (e.g. Chen et al., 1997), there is some evidence that rTMS effects of inhibitory dlPFC stimulations might last for a shorter duration.”
ResultLi, X., Malcolm, R. J., Huebner, K., Hanlon, C. A., Taylor, J. J., Brady, K. T., George, M. S., & See, R. E. (2013) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2013.08.012 · Cited by 85
“Depending on the frequency of the pulsed magnetic fields, rTMS can be used to either stimulate (high frequency) or suppress (low frequency) neural activity in a particular cortical region (Chen et al., 1997; Pascual-Leone et al., 1994).”
BackgroundMethodMantovani, A., Lisanby, S. H., Pieraccini, F., Ulivelli, M., Castrogiovanni, P., & Rossi, S. (2007) · Journal of Affective Disorders · doi:10.1016/j.jad.2006.11.027 · Cited by 82
“A few groups have examined whether PD could be treated by targeting right DLPFC overactivity with low-frequency repetitive Transcranial Magnetic Stimulation (rTMS), reported to have inhibitory action on cortical excitability (Chen et al., 1997).”
BackgroundThe right parietal cortex and time perception: back to Critchley and the Zeitraffer phenomenon
Alexander, I. H., Cowey, A., & Walsh, V. (2005) · Cognitive Neuropsychology · doi:10.1080/02643290442000356 · Cited by 82
Brain Stimulation in Poststroke Rehabilitation
Alonso‐Alonso, M., Fregni, F., & Pascual‐Leone, Á. (2007) · Cerebrovascular Diseases · doi:10.1159/000107392 · Cited by 85
“When TMS is applied in the form of trains of stimuli (rTMS), it can facilitate or suppress activity in the targeted brain region depending on the stimulation parameters. With frequencies in the range of 1 Hz or lower, a decrease in excitability is induced in the underlying cortex, whereas higher frequencies lead to in…”
Takano, B., Drzezga, A. E., Peller, M., Sax, I., Schwaiger, M., Lee, L., & Siebner, H. R. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2004.06.032 · Cited by 80
Cortical mechanisms for trans-saccadic memory and integration of multiple object features
Prime, S. L., Vesia, M., & Crawford, J. D. (2011) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2010.0184 · Cited by 89
Manganotti, P., Formaggio, E., Storti, S., Fiaschi, A., Battistin, L., Tonin, P., Piccione, F., & Cavinato, M. (2013) · Brain Stimulation · doi:10.1016/j.brs.2013.06.006 · Cited by 83
“The isolated increase in MEP amplitude without changes in EEG activity after rTMS might be related to short-range connectivity, perhaps reflecting a functional correlate of strictly local activity over the motor cortex [14,15,17].”
BackgroundTranscranial Magnetic Stimulation in the investigation and treatment of schizophrenia: a review.
Haraldsson, H. M., Ferrarelli, F., Kalin, N., & Tononi, G. (2004) · Schizophrenia Research · doi:10.1016/j.schres.2003.10.006 · Cited by 92
“Several studies have found that after high frequency TMS (>1 Hz) there is increased excitability in various brain areas, while after low frequency stimulation ( Chen et al., 1997; Wassermann et al., 1998).”
BackgroundGu, S. Y., & Chang, M. C. (2016) · Brain stimulation · doi:10.1016/j.brs.2016.10.010 · Cited by 82
Electric Stimulation on Human Cortex Suppresses Fast Cortical Activity and Epileptic Spikes
Kinoshita, M., Ikeda, A., Matsumoto, R., Begum, T., Usui, K., Yamamoto, J., Matsuhashi, M., Takayama, M., Mikuni, N., Takahashi, J., et al. (2004) · Epilepsia · doi:10.1111/j.0013-9580.2004.60203.x · Cited by 81
“9 Hz, bipolar) of the epileptic area was performed with 7 mA for 15 min, emulating a previous study of low-frequency transcranial magnetic stimulation, which demonstrated the depression of motor cortex excitability (8).”
MethodSchutter, D., & van Honk, J. (2005) · Journal of Psychiatry & Neuroscience · doi:10.1139/jpn.0515 · Cited by 95
Lusicic, A., Schruers, K. R., Pallanti, S., & Castle, D. J. (2018) · Neuropsychiatric Disease and Treatment · doi:10.2147/ndt.s121140 · Cited by 81
“Stimulation protocols include low-frequency (LF) rTMS ( , 5 Hz), inducing decreased neuronal activity in the cortex, 25 or high-frequency (HF) rTMS ( .”
Tergau, F., Neumann, D., Rosenow, F., Nitsche, M. A., Paulus, W., & Steinhoff, B. J. (2003) · Supplements to Clinical neurophysiology · doi:10.1016/s1567-424x(09)70244-2 · Cited by 81
Johnen, V. M., Neubert, F.-X., Buch, E. R., Verhagen, L., O’Reilly, J. X., Mars, R. B., & Rushworth, M. F. S. (2015) · eLife · doi:10.7554/elife.04585 · Cited by 82
“Several TMS protocols have been shown to induce changes in excitability in primary 76 motor cortex (M1) using repetitive stimulation of M1 itself (12) or stimulation of premotor regions 77 projecting to M1 (13).”
Zhou, W., Wang, J., Wang, K., Huang, B., Niu, L., Li, F., Cai, F., Chen, Y., Liu, X., Zhang, X., et al. (2017) · Lab on a Chip · doi:10.1039/c7lc00163k · Cited by 81
Zeng, K., Li, Z., Xia, X., Wang, Z., Darmani, G., Li, X., & Chen, R. E. (2024) · Brain stimulation · doi:10.1016/j.brs.2024.03.001 · Cited by 87
Self-citationOrth, M., Kirby, R., Richardson, M. P., Snijders, A. H., Rothwell, J. C., Trimble, M., Robertson, M. M., & Münchau, A. M. (2004) · Clinical Neurophysiology · doi:10.1016/j.clinph.2004.10.003 · Cited by 80
Linking Essential Tremor to the Cerebellum: Physiological Evidence
Filip, P., Lungu, O., Manto, M., & Bareš, M. (2015) · The Cerebellum · doi:10.1007/s12311-015-0740-2 · Cited by 81
Kukke, S. N., Paine, R. W., Chao, C., de Campos, A. C., & Hallett, M. (2014) · Journal of Clinical Neurophysiology · doi:10.1097/wnp.0000000000000057 · Cited by 81
“However, a previous study of 0.1 Hz TMS of the motor cortex at 5% MSO above resting CMT showed no change in cortical excitability (Chen et al., 1997).”
BackgroundInfluentialSelf-citationTrojak, B., Meille, V., Achab, S., Lalanne, L., Poquet, H., Ponavoy, E., Blaise, E., Bonin, B., & Chauvet‐Gélinier, J. (2015) · Brain stimulation · doi:10.1016/j.brs.2015.06.004 · Cited by 79
Ragert, P., Dinse, H. R., Pleger, B., Wilimzig, C., Frombach, E., Schwenkreis, P., & Tegenthoff, M. (2003) · Neuroscience Letters · doi:10.1016/s0304-3940(03)00745-6 · Cited by 81
Muller, P. A., Dhamne, S. C., Vahabzadeh‐Hagh, A. M., Pascual‐Leone, Á., Jensen, F. E., & Rotenberg, A. (2014) · PLoS ONE · doi:10.1371/journal.pone.0091065 · Cited by 80
“0 Hz stimulation has the most prominent effect on MEP size [35,41].”
BackgroundResult
Metadata
- Authors
- Chen, R., Classen, J., Gerloff, C., Celnik, P., Wassermann, E. M., Hallett, M., & Cohen, L. G.
- Affiliations
- National Institutes of Health (US)
- Venue
- Neurology
- Published
- 1997-05
- Volume
- 48
- Issue
- 5
- Pages
- 1398-1403
- ISSN
- 0028-3878 (ISSN-L)
- 1526-632X
- OpenAlex
- W2034753893
- Cited by
- 2,128
- References
- 0
- Citations by year
- 2026: 51 · 2025: 58 · 2024: 68 · 2023: 62 · 2022: 64 · 2021: 95 · 2020: 71 · 2019: 64 · 2018: 76 · 2017: 69 · 2016: 78 · 2015: 106 · 2014: 105 · 2013: 118 · 2012: 104
- FWCI
- 12.48
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neurology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Neurology › Transcranial Magnetic Stimulation Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Health Sciences › Medicine › Clinical Neurology › Deep Brain Stimulation and Movement Disorders
- Keywords
- motor cortex excitability, long-term depression, motor evoked potentials, cortical plasticity, epilepsy, myoclonus, excitation propagation
- MeSH terms
- Adult, Aged, Electric Stimulation, Female, Fingers, Humans, Male, Middle Aged, Motor Activity, Motor Cortex, Evoked Potentials, Motor, Transcranial Magnetic Stimulation
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