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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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Sabbagh, M. N., Sadowsky, C., Tousi, B., Agronin, M., Alva, G., Armon, C., Bernick, C. B., Keegan, A. P., Karantzoulis, S., Baror, E., et al. (2019) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2019.08.197 · Cited by 175
Transcranial magnetic stimulation: Neurophysiological applications and safety
Anand, S., & Hotson, J. R. (2002) · Brain and Cognition · doi:10.1016/s0278-2626(02)00512-2 · Cited by 168
Shafi, M. M., Westover, M. B., Fox, M., & Pascual‐Leone, Á. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08035.x · Cited by 172
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Avenanti, A., Minio-Paluello, I., Bufalari, I., & Aglioti, S. M. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.08.001 · Cited by 164
“1 Hz frequency did not induce any change of excitability (Chen et al., 1997).”
InfluentialBrighina, F., Piazza, A., Daniele, O., & Fierro, B. (2002) · Experimental Brain Research · doi:10.1007/s00221-002-1096-7 · Cited by 164
“This observation could explain the inefficient potentiation of GABA-mediated circuits by low frequency rTMS found in migraine patients, which is different from the findings observed in normal ( Chen et al. 1997; Boroojerdi et al. 2000) and other pathological conditions (Siebner et al. 1999).”
BackgroundResultInfluentialMarra, H., Myczkowski, M. L., Memória, C. M., Arnaut, D., Ribeiro, P. L., Mansur, C. G., Alberto, R. L., Bellini, B. B., da Silva, A. A. F., Tortella, G., et al. (2015) · Behavioural Neurology · doi:10.1155/2015/287843 · Cited by 166
Schambra, H. M., Sawaki, L. A., & Cohen, L. G. (2002) · Clinical Neurophysiology · doi:10.1016/s1388-2457(02)00342-5 · Cited by 163
“Previous studies demonstrated that low frequency TMS for 15–30 min over M1 decreases the excitability of the stimulated motor cortex (Chen et al., 1997; Muellbacher et al., 2000).”
BackgroundSelf-citationMottaghy, F. M., Keller, C. E., Gangitano, M., Ly, J. D., Thall, M., Parker, J. A., & Pascual‐Leone, Á. (2002) · Psychiatry Research Neuroimaging · doi:10.1016/s0925-4927(02)00032-x · Cited by 161
“Low frequency rTMS (1 Hz) tends to suppress cortical excitability (Chen et al., 1997; Muellbacher et al., 2000), while higher frequency rTMS (5–20 Hz) increases it in most subjects (Maeda et al.”
BackgroundAbnormal plasticity in dystonia: Disruption of synaptic homeostasis
Quartarone, A., & Pisani, A. (2010) · Neurobiology of Disease · doi:10.1016/j.nbd.2010.12.011 · Cited by 167
Camus, M., Halelamien, N. S., Plaßmann, H., Shimojo, S., O’Doherty, J. P., Camerer, C. F., & Rangel, A. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06991.x · Cited by 167
“…of this issue in the motor system found that the decrease in corticospinal excitability lasted for up to half the stimulation time in one study (Chen et al., 1997) and for twice that time in another (Muellbacher et al., 2000), studies in the visual cortex found that cortical excitability was…”
BackgroundEichhammer, P., Langguth, B., Marienhagen, J., Kleinjung, T., & Hajak, G. (2003) · Biological Psychiatry · doi:10.1016/s0006-3223(02)01896-6 · Cited by 162
Understanding and enhancing motor recovery after stroke using transcranial magnetic stimulation
Hoyer, E. H., & Celnik, P. A. (2011) · Restorative Neurology and Neuroscience · doi:10.3233/rnn-2011-0611 · Cited by 160
“For instance, many rTMS studies targeting the contralesional hemisphere used intensities near or at resting motor threshold at 1 Hz frequency because these parameters lead to reductions in cortical excitability (Chen et al., 1997).”
InfluentialSelf-citationKarabanov, A. N., Ziemann, U., Hamada, M., George, M. S., Quartarone, A., Claßen, J., Massimini, M., Rothwell, J. C., & Siebner, H. R. (2015) · Brain stimulation · doi:10.1016/j.brs.2015.06.017 · Cited by 166
Self-citationQuartarone, A., Bagnato, S., Rizzo, V., Morgante, F., Sant'Angelo, A., Battaglia, F., Messina, C., Siebner, H. R., & Girlanda, P. (2004) · Experimental Brain Research · doi:10.1007/s00221-004-2052-5 · Cited by 169
“…of rTMS have been mainly studied in the primary motor hand area (M1HAND) because overall changes in corticomotor excitability can be readily assessed with TMS by measuring the size of the motor evoked response (MEP) in the contralateral upper limb (Chen et al. 1997; Pascual-Leone et al. 1994).”
BackgroundBrain Effects of TMS Delivered Over Prefrontal Cortex in Depressed Adults
Nahas, Z. H., Tenebäck, C. C., Kozel, A., Speer, A. M., DeBrux, C., Molloy, M. A., Stallings, L. E., SPICER, K. M., Arana, G. W., Bohning, D. E., et al. (2001) · Journal of Neuropsychiatry · doi:10.1176/jnp.13.4.459 · Cited by 162
Urgesi, C., Candidi, M., Fabbro, F., Romani, M., & Aglioti, S. M. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04772.x · Cited by 160
“The choice of the interstimulus interval was based on research by Chen et al. (1997) that demonstrated no change in corticospinal excitability with repetitive TMS at 0.1 Hz for 1 h.”
MethodInfluentialLee, S., Kim, W. B., Chung, Y.-C., Jung, K.-H., Bahk, W., Jun, T.-Y., Kim, K., George, M. S., & Chae, J. (2004) · Neuroscience Letters · doi:10.1016/j.neulet.2004.11.048 · Cited by 157
Thickbroom, G. W., Byrnes, M. L., Edwards, D. J., & Mastaglia, F. L. (2005) · Clinical Neurophysiology · doi:10.1016/j.clinph.2005.09.010 · Cited by 159
“Repetitive single-pulse transcranial magnetic stimulation (rTMS) at low (w1 Hz) or high (w10 Hz) frequencies can have inhibitory or facilitatory effects respectively (Chen et al., 1997; Huang and Rothwell, 2004; Maeda et al., 2000; Pascual-Leone et al., 1994; Wu et al., 2000).”
BackgroundRepeated premotor rTMS leads to cumulative plastic changes of motor cortex excitability in humans
Bäumer, T., Lange, R., Liepert, J., et al. (2003) · NeuroImage · doi:10.1016/s1053-8119(03)00310-0 · Cited by 157
Methods of therapeutic cortical stimulation
Lefaucheur, J. P. (2008) · Neurophysiologie Clinique · doi:10.1016/j.neucli.2008.11.001 · Cited by 155
“[19] Chen R, Classen J, Gerloff C, Celnik P, Wassermann EM, Hallett M, et al.”
Mueller, J. K., Grigsby, E. M., Prevosto, V., Petraglia, F. W., Rao, H. M., Deng, Z., Peterchev, A. V., Sommer, M. A., Egner, T., Platt, M. L., et al. (2014) · Nature Neuroscience · doi:10.1038/nn.3751 · Cited by 148
Steeves, T. D. L., Mckinlay, B. D., Gorman, D. A., Billinghurst, L. L., Day, L., Carroll, A. M., Dion, Y., Doja, A., Luscombe, S., Sandor, P., et al. (2012) · The Canadian Journal of Psychiatry · doi:10.1177/070674371205700303 · Cited by 155
Prefrontal Cortex Stimulation Enhances Fear Extinction Memory in Humans
Raij, T., Nummenmaa, A., Marin, M.-F., Porter, D., Furtak, S., Setsompop, K., & Milad, M. R. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.10.022 · Cited by 156
“facilitatory effects on the primary target, respectively (41, 42).”
BackgroundTranscranial magnetic stimulation: its current role in epilepsy research
Ziemann, U., Steinhoff, B. J., Tergau, F., & Paulus, W. (1998) · Epilepsy Research · doi:10.1016/s0920-1211(97)00079-x · Cited by 153
Graff-Guerrero, A., González-Olvera, J., Fresán, A., Gómez-Martín, D., Carlos Méndez-Núñez, J., & Pellicer, F. (2005) · Cognitive Brain Research · doi:10.1016/j.cogbrainres.2005.05.002 · Cited by 154
Brain Stimulation in Addiction
Salling, M. C., & Martínez, D. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2016.80 · Cited by 160
“For instance, LF rTMS (~1 Hz) of the human motor cortex can decrease the MEP for over an hour following cessation (Chen et al, 1997; Iyer et al, 2003).”
BackgroundFacilitation of picture naming after repetitive transcranial magnetic stimulation
Mottaghy, F. M., Hungs, M., Brügmann, M., Sparing, R., Boroojerdi, B., Foltys, H., Huber, W., & Töpper, R. (1999) · Neurology · doi:10.1212/wnl.53.8.1806 · Cited by 155
Speer, A. M., Willis, M. W., Herscovitch, P., Daube-Witherspoon, M. E., Shelton, J. R., Benson, B. E., Post, R. M., & Wassermann, E. M. (2003) · Biological Psychiatry · doi:10.1016/s0006-3223(03)00002-7 · Cited by 152
Self-citationSegregation of Areas Related to Visual Working Memory in the Prefrontal Cortex Revealed by rTMS
Mottaghy, F. M. (2002) · Cerebral Cortex · doi:10.1093/cercor/12.4.369 · Cited by 154
“Furthermore, in the saccade studies there was an effect on speed rather than on accuracy, and our results did not show any significant reaction time delay after the DMPFC stimulation.”
BackgroundMethodResultInfluentialRepetitive TMS over the human oculomotor cortex: Comparison of 1-Hz and theta burst stimulation
Nyffeler, T., Wurtz, P., Lüscher, H.-R., Hess, C. W., Senn, W., Pflugshaupt, T., von Wartburg, R., Lüthi, M., & Müri, R. M. (2006) · Neuroscience Letters · doi:10.1016/j.neulet.2006.09.011 · Cited by 151
“How rTMS interferes with physiological mechanisms in he human brain is far from clear: The effect of low frequency TMS has been related to long-term depression (LTD) of cortical ynapses [3,16].”
BackgroundAn Overview of Noninvasive Brain Stimulation: Basic Principles and Clinical Applications
Bhattacharya, A., Kambhampati, M., Sreepada, S. S. S., Sathyaprabha, T. N., Pal, P. K., Chen, R. E., & Udupa, K. (2021) · Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques · doi:10.1017/cjn.2021.158 · Cited by 180
“29,30 These changes are likely caused by synaptic long-term potentiation and depression (LTP/LTD) since effects of rTMS are blocked by administration of drugs that interfere with N-methyl-D-aspartate (NMDA) receptors, which are known to be involved in LTP/LTD processes.”
BackgroundSelf-citationHallett, M. (2002) · Neurology · doi:10.1212/01.wnl.0000027361.73814.0e · Cited by 153
Self-citationSchambra, H. M., Abe, M., Luckenbaugh, D., Reis, J., Krakauer, J., & Cohen, L. (2011) · Journal of Neurophysiology · doi:10.1152/jn.00210.2011 · Cited by 156
Self-citationSparing, R., & Mottaghy, F. M. (2008) · Methods · doi:10.1016/j.ymeth.2007.02.001 · Cited by 162
Evidence for GABAergic inhibitory deficits in major depressive disorder
Croarkin, P. E., LEVINSON, A. J., & Daskalakis, Z. J. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.10.002 · Cited by 160
Huber, R., Treyer, V., Schuderer, J., et al. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.03929.x · Cited by 150
“…rCBF. Stimulation frequency-dependent effects on brain activity were observed with transcranial magnetic stimulation (TMS) such that low-frequency stimulation (1 Hz) induced inhibition (Chen et al., 1997), whereas stimulation with higher frequencies induced activation (Pascual-Leone et al., 1994).”
BackgroundSiebner, H. R., Roßmeier, C., Mentschel, C., et al. (2000) · Journal of the Neurological Sciences · doi:10.1016/s0022-510x(00)00370-1 · Cited by 150
Zhao, H., Qiao, L., Fan, D., Zhang, S., Turel, O., Li, Y., Li, J., Xue, G., Chen, A., & He, Q. (2017) · Frontiers in Psychology · doi:10.3389/fpsyg.2017.00685 · Cited by 154
“…stimulation (tDCS), transcranial alternating current stimulation (tACS), transcranial random noise stimulation (tRNS), transcranial pulsed current stimulation (tPCS), and transcranial ultrasound stimulation (TUS) (Chen et al., 1997; Paulus, 2011; Tufail et al., 2011; Jaberzadeh et al., 2014).”
MethodInduction of Human Motor Cortex Plasticity by Theta Burst Transcranial Ultrasound Stimulation
Zeng, K., Darmani, G., Fomenko, A., Xia, X., Tran, S., Nankoo, J., Oghli, Y. S., Wang, Y., Lozano, A. M., & Chen, R. (2021) · Annals of Neurology · doi:10.1002/ana.26294 · Cited by 152
“For example, rTMS at 5Hz or higher increases cortical excitability,(1) whereas rTMS at 1Hz or lower decreases cortical excitability.(2) Recently, repetitive TUS protocols with pulse duration from 0.”
BackgroundSelf-citationPasley, B. N., Allen, E. A., & Freeman, R. D. (2009) · Neuron · doi:10.1016/j.neuron.2009.03.012 · Cited by 152
“Each of these variables has been found previously to alter the outcome of TMS application (Berardelli et al., 1998; Chen et al., 1997; Pascual-Leone et al., 1998).”
Stroke recovery can be enhanced by using repetitive transcranial magnetic stimulation (rTMS)
Lefaucheur, J. P. (2006) · Neurophysiologie Clinique · doi:10.1016/j.neucli.2006.08.011 · Cited by 146
Ceceli, A. O., Bradberry, C. W., & Goldstein, R. Z. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-021-01153-9 · Cited by 150
“TMS capitalizes on magnetic-field driven cortical depolarization, with high-frequency stimulation largely resulting in excitatory, and low-frequency applications resulting in inhibitory, effects [237, 238].”
BackgroundRole of the primary somatosensory cortex in motor learning: An rTMS study
Vidoni, E. D., Acerra, N., Dao, E. A., et al. (2010) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2010.01.011 · Cited by 147
“Tracking was completed within 15 min from the end of rTMS so that the protocol ended while the effects of rTMS were still present (Chen et al., 1997).”
Phasic Voluntary Movements Reverse the Aftereffects of Subsequent Theta-Burst Stimulation in Humans
Iezzi, E., Conte, A., Suppa, A., Agostino, R., Dinapoli, L., Scontrini, A., & Berardelli, A. (2008) · Journal of Neurophysiology · doi:10.1152/jn.90521.2008 · Cited by 146
“For example, Siebner et al. (2004) showed that the normally induced inhibitory aftereffects elicited by 1-Hz rTMS (Chen et al. 1997) could be reversed to facilitation when preceded by another inhibitory protocol such as cathodal transcranial DC stimulation (Nitsche et al. 2003).”
BackgroundMethodArai, N., Okabe, S., Furubayashi, T., Terao, Y., Yuasa, K., & Ugawa, Y. (2004) · Clinical Neurophysiology · doi:10.1016/j.clinph.2004.09.020 · Cited by 161
Houdayer, E., Degardin, A., Cassim, F., Bocquillon, P., Derambure, P., & Devanne, H. (2008) · Experimental Brain Research · doi:10.1007/s00221-008-1294-z · Cited by 145
“In the literature, the inhibitory effect of low-frequency rTMS is generally considered to be substantiated by a decrease in MEP amplitude (Chen et al. 1997; Gerschlager et al. 2001; Romero et al. 2002) and an increase in MT (Muellbacher et al. 2000; Fitzgerald et al. 2002), whereas high-frequency…”
BackgroundMethodInfluentialClinical and Research Methods for Evaluating Cortical Excitability
Abbruzzese, G., & Trompetto, C. (2002) · Journal of Clinical Neurophysiology · doi:10.1097/00004691-200208000-00005 · Cited by 147
“9 to 1 Hz can produce a transient depression of MEP excitability that outlasts the train for several minutes (Chen et al., 1997; Maeda et al., 2000; Muellbacher et al., 2000; Siebner et al., 1999a; Touge et al., 2001).”
BackgroundInfluentialUnderstanding and Modulating Motor Learning with Cerebellar Stimulation
Celnik, P. A. (2014) · The Cerebellum · doi:10.1007/s12311-014-0607-y · Cited by 144
“For instance, applications of repetitive TMS can elicit reduction or facilitation of cortical excitability that last beyond the period of stimulation [13, 14].”
BackgroundSelf-citationZhang, L., Xing, G., Fan, Y., Guo, Z., Chen, H., & Mu, Q. (2017) · Clinical Rehabilitation · doi:10.1177/0269215517692386 · Cited by 143
Rose, J. E., McClernon, F. J., Froeliger, B., Behm, F. M., Preudʼhomme, X., & Krystal, A. D. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.05.031 · Cited by 144
Noninvasive Associative Plasticity Induction in a Corticocortical Pathway of the Human Brain
Buch, E. R., Johnen, V. M., Nelissen, N., O’Shea, J., & Rushworth, M. F. S. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.1513-11.2011 · Cited by 142
“Some approaches entail repetitive stimulation of M1 itself (Chen et al., 1997), while others involve stimulation of premotor regions projecting to M1 (Munchau et al., 2002).”
BackgroundBrain Neuromodulation Techniques
Lewis, P., Thomson, R. H., Rosenfeld, J. V., & Fitzgerald, P. B. (2016) · The Neuroscientist · doi:10.1177/1073858416646707 · Cited by 147
Repetitive Transcranial Magnetic Stimulation for Major Depressive Disorder: A Review
Daskalakis, Z. J., LEVINSON, A. J., & Fitzgerald, P. B. (2008) · The Canadian Journal of Psychiatry · doi:10.1177/070674370805300902 · Cited by 142
Lang, N., Harms, J., Weyh, T., Lemon, R., Paulus, W., Rothwell, J. C., & Siebner, H. R. (2006) · Clinical Neurophysiology · doi:10.1016/j.clinph.2006.05.030 · Cited by 147
“Suprathreshold stimulation with 1 Hz can produce sustained inhibition of motor cortex excitability (Chen et al., 1997; Muellbacher et al., 2000).”
BackgroundResultMistry, S., Vérin, É., Singh, S., Jefferson, S., Rothwell, J. C., Thompson, D. G., & Hamdy, S. (2007) · The Journal of Physiology · doi:10.1113/jphysiol.2007.144592 · Cited by 141
“…since it can cause immediate and lasting changes in the excitability of focal cortical areas at the site of stimulation (Pascual-Leone et al. 1994; Chen et al. 1997; Berardelli et al. 1998; Maeda et al. 2000; Siebner et al. 2000; Gerschlager et al. 2001; Modugno et al. 2001; Touge et al. 2001).”
BackgroundMotor cortex excitability following short trains of repetitive magnetic stimuli
Modugno, N., Nakamura, Y., MacKinnon, C. D., et al. (2001) · Experimental Brain Research · doi:10.1007/s002210100843 · Cited by 142
Cerebellar rTMS disrupts predictive language processing
Lesage, E., Morgan, B. E., Olson, A. C., Meyer, A. S., & Miall, R. C. (2012) · Current Biology · doi:10.1016/j.cub.2012.07.006 · Cited by 141
Serino, A., Canzoneri, E., & Avenanti, A. (2011) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_00006 · Cited by 145
“Studies suggest that this low-frequency rTMS protocol disrupts functions related to the targeted area for at least half the stimulation time (Pascual-Leone et al., 2000; Chen et al., 1997).”
Romani, M., Cesari, P., Urgesi, C., Facchini, S., & Aglioti, S. M. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2005.02.027 · Cited by 144
“While TMS delivered for 15 min with a 0.9-Hz frequency may induce a clear decrease of MEP amplitude, TMS delivered for 1 h at 0.1 Hz frequency did not induce any change of excitability ( Chen et al., 1997 ).”
MethodInfluentialHadley, D., Anderson, B., Borckardt, J., Arana, A., Li, X.-B., Nahas, Z., & George, M. (2011) · Journal of ECT · doi:10.1097/yct.0b013e3181ce1a8c · Cited by 148
Influence of imagined posture and imagery modality on corticospinal excitability
Fourkas, A. D., Ionta, S., & Aglioti, S. M. (2005) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.10.015 · Cited by 140
“[5] Chen R, Classen J, Gerloff C, Celnik P, Wassermann EM, Hallet M al.”
Backgroundvan der Werf, Y. D., & Paus, T. (2006) · Experimental Brain Research · doi:10.1007/s00221-006-0551-2 · Cited by 139
“We determined this value as the lowest intensity of stimulation that resulted in at least 5 MEPs of 50 V or larger in a series of 10 consecutive single-pulse stimulations applied over the left primary motor cortex.”
BackgroundResultInfluentialLefaucheur, J. P., André‐Obadia, N., Poulet, E., Devanne, H., Haffen, É., Londero, A., Cretin, B., Leroi, A., Radtchenko, A., Saba, G., et al. (2011) · Neurophysiologie Clinique · doi:10.1016/j.neucli.2011.10.062 · Cited by 138
“[64].”
Oliveri, M., Koch, G., Torriero, S., & Caltagirone, C. (2004) · Neuroscience Letters · doi:10.1016/j.neulet.2004.11.053 · Cited by 135
Decreased sensory cortical excitability after 1 Hz rTMS over the ipsilateral primary motor cortex
Enomoto, H., Ugawa, Y., Hanajima, R., Yuasa, K., Mochizuki, H., Terao, Y., Shiio, Y., Furubayashi, T., Iwata, N., & Kanazawa, I. (2001) · Clinical Neurophysiology · doi:10.1016/s1388-2457(01)00667-8 · Cited by 138
“…into how these treatments might work, lasting effects of rTMS after the cessation of stimulation have been studied (Pascual-Leone et al., 1994b; Chen et al., 1997; Berardelli et al., 1998; Maeda et al., 2000; Wu et al., 2000; Peinemann et al., 2000; Boroojerdi et al., 2000), mostly after rTMS…”
BackgroundPrinciples of therapeutic use of transcranial and epidural cortical stimulation
Lefaucheur, J. (2008) · Clinical Neurophysiology · doi:10.1016/j.clinph.2008.07.007 · Cited by 140
“2–1 Hz) consists of a single continuous train and is thought to depress synaptic transmission, whereas high-frequency rTMS (5–20 Hz) consists of intermittent bursts and is thought to potentiate synaptic transmission (Chen et al., 1997; Pascual-Leone et al., 1998; Post et al., 1999).”
BackgroundInfluentialRosenberg, P. B., Mehndiratta, R. B., Mehndiratta, Y. P., Wamer, A., Rosse, R. B., & Balish, M. (2002) · Journal of Neuropsychiatry · doi:10.1176/jnp.14.3.270 · Cited by 145
“Fast rTMS (defined as 5 Hz) increases motor cortex excitability, and slow rTMS (1 Hz) decreases it.(43,44) Because left frontal cortical metabolism has often been found to be decreased in major depression, one might expect fast left frontal rTMS to “normalize” metabolism and thus be more effective than slow left front…”
Valero-Cabré, A., Payne, B. R., & Pascual-Leone, A. (2007) · Experimental Brain Research · doi:10.1007/s00221-006-0639-8 · Cited by 137
“…agreement with the observation that slow rTMS on the human primary motor cortex leads to a decrease of intracortical and corticospinal excitability (Chen et al. 1997; Romero et al. 2002), whereas rapid rTMS tends to induce the opposite eVect (Pascual-Leone et al. 1994; Maeda et al. 2000; Gangitano…”
BackgroundThe effects of motor cortex rTMS on corticospinal descending activity
Lazzaro, V. D., Profice, P., Pilato, F., Dileone, M., Oliviero, A., & Ziemann, U. (2010) · Clinical Neurophysiology · doi:10.1016/j.clinph.2009.11.007 · Cited by 137
“Low frequency rTMS (stimulus rates of 1 Hz or less) produces a lasting decrease in motor cortex excitability (Chen et al., 1997) while high frequency rTMS (stimulus rates of 5 Hz or more) (Berardelli et al., 1998; Maeda et al., 2000; Pascual-Leone et al., 1994; Peinemann et al., 2000) promotes a…”
BackgroundMethodInfluentialNeuromodulation techniques – From non-invasive brain stimulation to deep brain stimulation
Davidson, B., Bhattacharya, A., Sarica, C., Darmani, G., Raies, N., Chen, R. E., & Lozano, A. M. (2024) · Neurotherapeutics · doi:10.1016/j.neurot.2024.e00330 · Cited by 166
“High-frequency ( > 5 Hz) rTMS increases cortical excitability, whereas low frequency (1 Hz or lower) rTMS decreases cortical excitability [10,11].”
BackgroundSelf-citationMagnetic stimulation of the central and peripheral nervous systems
Weber, M., Eisen, A., & AAEM (2002) · Muscle & Nerve · doi:10.1002/mus.10038 · Cited by 140
“The effects, ranging from inhibition to facilitation, depend on the stimulation parameters (stimulus intensity, interstimulus interval, number of stimuli, and interval between successive trains) and may last beyond the duration of the rTMS itself.(26,103) Lasting effects of highfrequency rTMS (greater than 1 HZ) on cl…”
BackgroundMethodNeggers, S. F. W., Langerak, T., Schutter, D. J. L. G., Mandl, R. C. W., Ramsey, N. F., Lemmens, P. J. J., & Postma, A. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2003.12.006 · Cited by 136
A new device and protocol for combining TMS and online recordings of EEG and evoked potentials
Thut, G., Ives, J. R., Kampmann, F., Pastor, M. A., & Pascual‐Leone, Á. (2004) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2004.06.016 · Cited by 134
Charlton, C. S. (2003) · Journal of the Neurological Sciences · doi:10.1016/s0022-510x(02)00443-4 · Cited by 135
Transcranial Magnetic Stimulation: Disrupting Neural Activity to Alter and Assess Brain Function
Bolognini, N., & Ro, T. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.1990-10.2010 · Cited by 140
“Applied in earlier studies to investigate motor cortex excitability (Chen et al., 1997) and visual imagery (Kosslyn et al., 1999), this technique has been used across a variety of other cognitive tasks.”
InfluentialMálly, J., & Dinya, E. (2008) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2007.11.019 · Cited by 130
Repetitive transcranial magnetic stimulation for Tourette syndrome
Münchau, A. M., Bloem, B. R., Thilo, K. V., Trimble, M., Rothwell, J. C., & Robertson, M. M. (2002) · Neurology · doi:10.1212/01.wnl.0000036615.25044.50 · Cited by 132
Gow, D. L., Rothwell, J. C., Hobson, A. R., et al. (2004) · Clinical Neurophysiology · doi:10.1016/j.clinph.2003.12.001 · Cited by 133
“9 and 1 Hz) decreasing, excitability (Pascual-Leone et al., 1994; Chen et al., 1997; Berardelli et al., 1998; Siebner et al., 2000; Modugno et al., 2001; Touge et al., 2001).”
Electrical stimulation of cranial nerves in cognition and disease
Adair, D., Truong, D. Q., Esmaeilpour, Z., Gebodh, N., Borges, H., Ho, L., Bremner, J. D., Badran, B. W., Napadow, V., Clark, V. P., et al. (2020) · Brain stimulation · doi:10.1016/j.brs.2020.02.019 · Cited by 136
Rounis, E., Lee, L., Siebner, H. R., Rowe, J. B., Friston, K. J., Rothwell, J. C., & Frackowiak, R. S. J. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2005.01.037 · Cited by 137
Yamamoto, J., Ikeda, A., Satow, T., et al. (2002) · Epilepsia · doi:10.1046/j.1528-1157.2002.29001.x · Cited by 132
“Low-frequency rTMS at 1 Hz applied to the human motor and visual cortices for 15 min has been shown to produce inhibitory effects lasting 15 and 10 min, respectively (6,7).”
BackgroundNoninvasive Brain Stimulation for Parkinson’s Disease and Dystonia
Wu, A. D., Fregni, F., Simon, D. K., Deblieck, C., & Pascual‐Leone, Á. (2008) · Neurotherapeutics · doi:10.1016/j.nurt.2008.02.002 · Cited by 132
“Different rTMS frequencies produce bidirectional changes in healthy subjects, with low frequencies ( 1 Hz) suppressing cortical excitability and high frequencies ( 5 Hz) facilitating it.(14,15) These excitability changes are transient, lasting 10 min to 30 min, with effects of longer duration generally linked to a hig…”
BackgroundCensor, N., Dimyan, M. A., & Cohen, L. G. (2010) · Current Biology · doi:10.1016/j.cub.2010.07.047 · Cited by 130
“In a series of experiments we show here that when an existing human motor memory is reactivated during recall, modification of the memory is blocked by virtual lesion [5] of the related primary cortical human brain area.”
BackgroundSelf-citationMotor System Reorganization After Stroke: Stimulating and Training Toward Perfection
Jones, T. A., & Adkins, D. L. (2015) · Physiology · doi:10.1152/physiol.00014.2015 · Cited by 142
“The size of TMS coils makes it challenging to deliver during rehabilitation regimens, but it alters cortical excitation for a period after stimulation to facilitate learning “off-line” (39, 65, 84).”
BackgroundUnderestimation of time perception after repetitive transcranial magnetic stimulation
Koch, G., Oliveri, M., Torriero, S., & Caltagirone, C. (2003) · Neurology · doi:10.1212/wnl.60.11.1844 · Cited by 129
Okabe, S., Ugawa, Y., & Kanazawa, I. (2002) · Movement Disorders · doi:10.1002/mds.10370 · Cited by 131
Loo, C. K. A., Mitchell, P. B., Croker, V., Malhi, G. S., WEN, W., Gandevia, S. C., & Sachdev, P. S. (2002) · Psychological Medicine · doi:10.1017/s0033291702006839 · Cited by 130
“There is some evidence from studies on the motor cortex that low (Chen et al. 1997) and high (Pascual-Leone et al.”
BackgroundDisinhibition of the contralateral motor cortex by low-frequency rTMS
Plewnia, C., Lotze, M., & Gerloff, C. P. (2003) · Neuroreport · doi:10.1097/00001756-200303240-00017 · Cited by 130
Self-citationModality-Specific Cognitive Function of Medial and Lateral Human Brodmann Area 6
Tanaka, S., Honda, M., & Sadato, N. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.4324-04.2005 · Cited by 128
“It is known that low-frequency rTMS inhibits cortical excitability for several minutes and temporarily impairs task performance (Chen et al., 1997; Maeda et al., 2000; Robertson et al., 2003).”
Measuring Brain Stimulation Induced Changes in Cortical Properties Using TMS-EEG
Chung, S. W., Rogasch, N. C., Hoy, K. E., & Fitzgerald, P. B. (2015) · Brain stimulation · doi:10.1016/j.brs.2015.07.029 · Cited by 129
Corticospinal facilitation during first and third person imagery
Fourkas, A. D., Avenanti, A., Urgesi, C., & Aglioti, S. M. (2006) · Experimental Brain Research · doi:10.1007/s00221-005-0076-0 · Cited by 127
“The choice of interstimulus interval was based on research by Chen et al. (1997) which demonstrated no change in corticospinal excitability with repetitive TMS at 0.1 Hz for 1 h using intervals of 10 s. Fifteen trials were performed in each condition, with approximately 3 min between conditions.”
BackgroundMethodInfluentialLangguth, B., Zowe, M., Landgrebe, M., Sand, P. G., Kleinjung, T., Binder, H., Hajak, G., & Eichhammer, P. (2006) · Brain Topography · doi:10.1007/s10548-006-0002-1 · Cited by 128
“Applied as low frequency rTMS (1 Hz) it is known to effectively reduce cortical activation (Chen et al. 1997), especially in areas of increased excitability (Speer et al. 2003; Siebner et al. 2003, 2004).”
BackgroundTMS Brain Mapping in Less Than Two Minutes
van de Ruit, M., Perenboom, M., & Grey, M. J. (2014) · Brain stimulation · doi:10.1016/j.brs.2014.10.020 · Cited by 128
“Whilst the use of a 1 s ISI has been associated with lasting depression of excitability of the cortex when administered to a single site repetitively for 4e15min [44,45], a number of recent observations suggest depression is unlikely to be a problem with the present method.”
The application of transcranial magnetic stimulation in psychiatry and neurosciences research
Fitzgerald, P. B., Brown, T. L., & Daskalakis, Z. J. (2002) · Acta Psychiatrica Scandinavica · doi:10.1034/j.1600-0447.2002.1r179.x · Cited by 128
Lazzaro, V. D., Oliviero, A., Mazzone, P., Pilato, F., Saturno, E., Dileone, M., Insola, A., Tonali, P., & Rothwell, J. C. (2002) · Experimental Brain Research · doi:10.1007/s00221-002-1223-5 · Cited by 128
“…shown that rTMS can produce changes in the resting excitability of corticospinal projections that outlast the period of stimulation for minutes and even hours (Pascual-Leone et al. 1994, 1998; Chen et al. 1997; Tergau et al. 1997; Berardelli et al. 1998; Maeda et al. 2000; Peinemann et al. 2000).”
BackgroundrTMS over the intraparietal sulcus disrupts numerosity processing
Cappelletti, M., Barth, H. C., Fregni, F., Spelke, E. S., & Pascual‐Leone, Á. (2007) · Experimental Brain Research · doi:10.1007/s00221-006-0820-0 · Cited by 135
“…at 1 Hz has been shown to reduce blood Xow and cortical excitability in the brain regions targeted by rTMS for several minutes after stimulation (Chen et al. 1997; Paus et al. 1997) and to impair performance on behavioral tasks depending on the regions stimulated (e.g., Romero et al. 2002;…”
BackgroundHordacre, B. G., Goldsworthy, M. R., Vallence, A., Darvishi, S., Moezzi, B., Hamada, M., Rothwell, J. C., & Ridding, M. C. (2016) · Brain stimulation · doi:10.1016/j.brs.2016.12.001 · Cited by 125
“directional based on pattern of stimulation [3-5], and is abolished following administration of NMDA antagonists [6].”
BackgroundEffect of low-frequency repetitive transcranial magnetic stimulation on interhemispheric inhibition.
Pal, P., Hanajima, R., Gunraj, C., Li, J., Wagle-Shukla, A., Morgante, F., & Chen, R. (2005) · Journal of Neurophysiology · doi:10.1152/jn.01306.2004 · Cited by 132
Self-citationCirillo, J., Todd, G., & Semmler, J. G. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07870.x · Cited by 124
“For instance, the number and frequency of TMS are too low to produce any changes in motor cortex excitability (Chen et al., 1997; see Hoogendam et al., 2010), and most studies have shown that TMS-induced motor cortex plasticity is”
Result
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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