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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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Gritsenko, V., Kalaska, J. F., & Cisek, P. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.0132-11.2011 · Cited by 52
“This was done to ensure that the frequency of transcranial magnetic stimulation (TMS), which was applied in almost every trial (see below, TMS procedure), was well below 1 Hz and did not induce long-term changes in cortical excitability (Chen et al., 1997).”
rTMS Induced Tinnitus Relief Is Related to an Increase in Auditory Cortical Alpha Activity
Müller, N., Lorenz, I., Langguth, B., & Weisz, N. (2013) · PLoS ONE · doi:10.1371/journal.pone.0055557 · Cited by 51
“Particularly in its repetitive form (rTMS; [28,29]), it has been shown (mostly in the motor system) that stimulation-induced changes of excitability and plasticity outlast the period of stimulation.”
Tinnitus: current understanding and contemporary management
Seidman, M. D., Standring, R. T., & Dornhoffer, J. L. (2010) · Current Opinion in Otolaryngology & Head & Neck Surgery · doi:10.1097/moo.0b013e32833c718d · Cited by 51
Brasil-Neto, J. P., de Araújo, D. P., Teixeira, W. A., et al. (2004) · Arquivos de Neuro-Psiquiatria · doi:10.1590/s0004-282x2004000100004 · Cited by 52
Variable changes in PET activity before and after rTMS treatment for tinnitus
Mennemeier, M., Chelette, K. C., Allen, S. D., Bartel, T. B., Triggs, W. J., Kimbrell, T. A., Crew, J., Munn, T., Brown, G. J., & Dornhoffer, J. L. (2011) · The Laryngoscope · doi:10.1002/lary.21425 · Cited by 51
Costantini, M., Ambrosini, E., Cardellicchio, P., & Sinigaglia, C. (2013) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nst037 · Cited by 52
“Indeed, with this rTMS protocol it is possible to induce transient ‘virtual lesions’ in neurologically intact participants by suppressing excitability to motor and non-motor cortical areas (Chen, 1997; Hilgetag et al., 2001; Avenanti et al., 2007; Ziemann, 2010; Sandrini et al., 2011).”
MethodBassolino, M., Franza, M., Bello‐Ruiz, J., Pinardi, M., Schmidlin, T., Stephan, M. A., Solcà, M., Serino, A., & Blanke, O. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.13871 · Cited by 52
“The intertrial interval between two consecutive TMS pulses was randomly varying from 9.8 to 12.2 s to ensure no change in cortical excitability (Chen et al. , 1997) and to avoid expectancy.”
BackgroundMethodInfluentialReorganisation of cerebral circuits in human ischemic brain disease
Seitz, R. J., Bütefisch, C. M., Kleiser, R., & Hömberg, V. (2004) · Restorative Neurology and Neuroscience · doi:10.3233/rnn-2004-00265 · Cited by 52
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“Repetitive TMS was applied in one continuous train of 15 min duration (similar duration as the study of (Chen et al., 1997a)) at 1 Hz over left M1 using an intensity that was set at 90% of the participant's MT (similar intensity as the study of (Gangitano et al., 2002)).”
BackgroundMethodTherapies for Parkinson’s diseases: alternatives to current pharmacological interventions
Li, S., Dong, J., Cheng, C., & Le, W. (2016) · Journal of Neural Transmission · doi:10.1007/s00702-016-1603-9 · Cited by 50
“1994a, b), low-frequency rTMS causes a depressed cortical activity (Chen et al. 1997).”
BackgroundHuman Mind Control of Rat Cyborg’s Continuous Locomotion with Wireless Brain-to-Brain Interface
Zhang, S., Yuan, S., Huang, L., Zheng, X., Wu, Z., Xu, K., & Pan, G. (2019) · Scientific Reports · doi:10.1038/s41598-018-36885-0 · Cited by 55
Stimulation-Induced Within-Representation and Across-Representation Plasticity in Human Motor Cortex
Ziemann, U., Wittenberg, G. F., & Cohen, L. G. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-13-05563.2002 · Cited by 50
“These rTMS parameters were shown previously not to produce any significant change in MEP amplitude in the absence of INB (Chen et al., 1997; Ziemann et al., 1998a).”
BackgroundSelf-citationDammekens, E., Vanneste, S., Ost, J., et al. (2012) · Neurocase · doi:10.1080/13554794.2012.713493 · Cited by 51
“Several studies have found that low frequency rTMS (<1 Hz) decreases cortical excitability, while high frequency rTMS (> 1 Hz) increases cortical excitability (Chen et al., 1997; Wassermann, 1998; Wu, Sommer, Tergau, & Paulus, 2000).”
BackgroundPallanti, S., Rollo, A. D., Antonini, S., Cauli, G., Hollander, E., & Quercioli, L. (2012) · Neuropsychobiology · doi:10.1159/000336999 · Cited by 51
Zanette, G., Forgione, A., Manganotti, P., et al. (2008) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2008.01.011 · Cited by 51
Loporto, M., Holmes, P. S., Wright, D. J., & McAllister, C. J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0064911 · Cited by 50
“For example, the application of 1 Hz repetitive TMS over the PMv, a ‘virtual lesion’ approach which can transiently inhibit the excitability of the underlying cortex [31], abolished motor resonance effects during the subsequent observation of index-finger abductions [13].”
MethodPilato, F., Profice, P., Ranieri, F., Capone, F., Iorio, R. D., Florio, L., & Lazzaro, V. D. (2012) · Molecular Neurobiology · doi:10.1007/s12035-012-8302-9 · Cited by 53
“9 Hz for 15 min reduced motor-evoked potential (MEP) amplitudes for 15 min after the period of stimulation [42].”
High-frequency rTMS using a double cone coil for gait disturbance
Kakuda, W., Abo, M., Nakayama, Y., et al. (2013) · Acta Neurologica Scandinavica · doi:10.1111/ane.12085 · Cited by 51
“The following inclusion criteria were applied: (1) Clinical confirmation of gait disturbance (unable to walk as before the onset of stroke).”
MethodBarr, M. S., Fitzgerald, P. B., Farzan, F., George, T. P., & Daskalakis, Z. (2008) · Current Drug Abuse Reviews · doi:10.2174/1874473710801030328 · Cited by 49
“To this end, drugs that block voltage-gated sodium channels [5-7], such as an antagonist of NMDA, an amino acid that normally mimics excitatory neurotransmitter GLU, elevates MT [8].”
BackgroundHosono, Y., Urushihara, R., Harada, M., Morita, N., Murase, N., Kunikane, Y., Shimazu, H., Asanuma, K., Uguisu, H., & Kaji, R. (2008) · Clinical Neurophysiology · doi:10.1016/j.clinph.2008.07.279 · Cited by 51
“High-frequency stimulation (P5 Hz) increases the cortical excitability, whereas low-frequency rTMS (61 Hz) decreases it for an extended period of time (Chen et al., 1997; Chen, 2000).”
BackgroundKnikou, M., Dixon, L., Santora, D., et al. (2015) · Journal of Neurophysiology · doi:10.1152/jn.00449.2015 · Cited by 51
Interfering with working memory in humans
Mottaghy, F. M. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.05.037 · Cited by 51
Frequency-dependent, bi-directional plasticity in motor cortex of human adults
Pitcher, J. B., Ridding, M. C., & Miles, T. S. (2003) · Clinical Neurophysiology · doi:10.1016/s1388-2457(03)00092-0 · Cited by 51
“9–1 Hz) rTMS induces MEP depression (Chen et al., 1997; Tergau et al., 1997; Maeda et al., 2000a,b; Muellbacher et al., 2000) while rTMS at higher frequencies (approximately 5–25 Hz) facilitates MEPs (Pascual-Leone et al.”
BackgroundMethodInfluentialAaronson, S. T., Carpenter, L. L., Hutton, T. M., Kraus, S., Mina, M., Pages, K., Shi, L., West, W. S., & Sackeim, H. A. (2022) · Brain Stimulation · doi:10.1016/j.brs.2022.01.006 · Cited by 50
“effectiveness was understandable, especially given the targeting of homologous lateralized regions with stimulation protocols that differ in their modulation of excitatory and inhibitory neural transmission [18-21].”
BackgroundModifying somatosensory processing with non-invasive brain stimulation
Song, S., Sandrini, M., & Cohen, L. G. (2011) · Restorative Neurology and Neuroscience · doi:10.3233/rnn-2011-0614 · Cited by 50
“The term ‘low-frequency’ rTMS refers to stimulus rates of 1 Hz or less (Chen et al., 1997) and ‘high-frequency’ rTMS refers to stimulus rates of more than 5 Hz.”
Self-citationBurger, J., Frank, E., Kreuzer, P. M., Kleinjung, T., Vielsmeier, V., Landgrebe, M., Hajak, G., & Langguth, B. (2011) · Brain Stimulation · doi:10.1016/j.brs.2010.11.003 · Cited by 53
Piccirillo, J. F., Kallogjeri, D., Nicklaus, J. E., Wineland, A., Spitznagel, E. L., Vlassenko, A. G., Benzinger, T. L. S., Mathews, J., & Garcia, K. S. (2013) · JAMA Otolaryngology–Head & Neck Surgery · doi:10.1001/jamaoto.2013.233 · Cited by 50
Vascular Cognitive Impairment through the Looking Glass of Transcranial Magnetic Stimulation
Lanza, G., Bramanti, P., Cantone, M., Pennisi, M., Pennisi, G., & Bella, R. (2017) · Behavioural Neurology · doi:10.1155/2017/1421326 · Cited by 50
“Single TMS pulses delivered in trains are the principle of repetitive TMS (rTMS), an approach that can transiently modulate the functioning of stimulated and connected brain areas mainly depending on the frequency of stimulation [36, 64, 65].”
BackgroundRepetitive Deep TMS for Parkinson Disease: A 3-Month Double-Blind, Randomized Sham-Controlled Study
Cohen, O. S., Rigbi, A., Yahalom, G., Warman-Alaluf, N., Nitsan, Z., Zangen, A., & Hassin‐Baer, S. (2018) · Journal of Clinical Neurophysiology · doi:10.1097/wnp.0000000000000455 · Cited by 51
Perera, M. P. N., Mallawaarachchi, S., Miljevic, A., Bailey, N. W., Herring, S. E., & Fitzgerald, P. B. (2021) · Biological Psychiatry: Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2021.03.010 · Cited by 51
Repetitive transcranial magnetic stimulation and chronic tinnitus
Langguth, B., Hajak, G., Kleinjung, T., PRIDMORE, S. A., Sand, P. G., & Eichhammer, P. (2006) · Acta Oto-Laryngologica · doi:10.1080/03655230600895457 · Cited by 50
“Low-frequency (5/1 Hz) rTMS results in a decrease in cortical excitability [13,14], while highfrequency (generally considered to be 5 20 Hz) TMS results in an increase in excitability [15].”
BackgroundDobkin, B. H. (2003) · PubMed · doi:10.1097/01.wco.0000102622.38669.ac · Cited by 50
Valero-Cabré, A., Rushmore, R. J., & Payne, B. R. (2006) · Experimental Brain Research · doi:10.1007/s00221-005-0307-4 · Cited by 48
“We then applied trains of low frequency rTMS stimulation, which have proved to induce limited but long lasting decreases of cortical excitability (Chen et al. 1997; Gangitano et al. 2002) and metabolic activity (ValeroCabré et al. 2005b), thus likely interfering with normal visual spatial…”
BackgroundMethodInfluentialYan, Y., Tian, M., Wang, T., Wang, X., Wang, Y., & Shi, J. (2023) · Frontiers in Neurology · doi:10.3389/fneur.2023.1209205 · Cited by 50
“Previous studies have demonstrated that high-frequency (HF) rTMS (>1Hz) or intermittent theta-burst stimulation induce an enhanced effect, whereas low-frequency (LF) rTMS (≤ 1Hz) or continuous theta-burst stimulation suppress neural activity (9, 10).”
BackgroundHarvey, R. L., & Nudo, R. J. (2007) · Topics in Stroke Rehabilitation · doi:10.1310/tsr1406-54 · Cited by 49
Klírová, M., Horáček, J., Novák, T., Cermak, J. K., Španiel, F., Skrdlantová, L., Mohr, P., & Höschl, C. (2012) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/s00406-012-0368-x · Cited by 49
“Our approach to target rTMS according to the local maxima of (18)FDG uptake is in accordance with the supposed long-term depression phenomenon induced by LF-rTMS responsible for the inhibitory effect [50, 51] and our previous finding of decreased metabolism in the cortex underlying the coil in LF-rTMS treatment [12].”
MethodGentilucci, M., Volta, R. D., & Gianelli, C. (2008) · Journal of Physiology-Paris · doi:10.1016/j.jphysparis.2008.03.002 · Cited by 57
Yamada, N., Kakuda, W., Senoo, A., et al. (2013) · International Journal of Stroke · doi:10.1111/ijs.12056 · Cited by 49
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“Furthermore, to assess the neurons membrane excitability in dystonia, the MT, and the RC (Ziemann et al., 1996a; Chen et al., 1997; Werhahn et al., 1999; Ziemann et al., 2004; Murase et al., 2005) were assessed and were consistently normal in both primary and non-primary dystonia (Quartarone et…”
BackgroundMethodHordacre, B. G., Comacchio, K., Williams, L. J., & Hillier, S. (2020) · Journal of Neurology · doi:10.1007/s00415-020-10315-6 · Cited by 52
CSF Tau Levels Influence Cortical Plasticity in Alzheimer's Disease Patients
Koch, G., Esposito, Z., Kusayanagi, H., Monteleone, F., Codecà, C., Lorenzo, F. D., Caltagirone, C., Bernardi, G., & Martorana, A. (2011) · Journal of Alzheimer s Disease · doi:10.3233/jad-2011-110116 · Cited by 50
“In 20 AD patients, CSF samples were collected in a polypropylene tube and directly transported the local laboratory for centrifugation at 2000 × +4 ◦ C for 10 min.”
Tamura, Y., Hoshiyama, M., Nakata, H., Hiroe, N., Inui, K., Kaneoke, Y., Inoue, K., & Kakigi, R. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04096.x · Cited by 53
“, 2000), finger tapping (Chen et al., 1997; Wassermann et al., 1998; Lee et al., 2003), peak force and acceleration during finger pinch (Muellbacher et al.”
BackgroundInfluentialrTMS for adolescents: Safety and efficacy considerations
D’Agati, D., Bloch, Y., Levkovitz, Y., & Reti, I. M. (2010) · Psychiatry Research · doi:10.1016/j.psychres.2010.03.004 · Cited by 49
Lazzaro, V. D., Thickbroom, G. W., Pilato, F., Profice, P., Dileone, M., Mazzone, P., Insola, A., Ranieri, F., Tonali, P., & Rothwell, J. C. (2007) · Clinical Neurophysiology · doi:10.1016/j.clinph.2007.02.020 · Cited by 48
“Thus 30 min of 1 Hz rTMS decreases the amplitude of the MEP evoked by single pulse stimulation for the next 30 min (Chen et al., 1997), whereas higher frequencies may either increase (Berardelli et al.”
BackgroundModulation of motor cortical excitability following rapid-rate transcranial magnetic stimulation
Khedr, E. M., Rothwell, J. C., Ahmed, M. A., Shawky, O. A., & Farouk, M. (2006) · Clinical Neurophysiology · doi:10.1016/j.clinph.2006.09.006 · Cited by 49
“…(>5 Hz) stimulation is likely to yield excitation whereas lower frequencies or irregular patterns of stimulation can lead to inhibition (Pascual-Leone et al., 1994; Chen et al., 1997; Daskalakis et al., 2006; Gangitano et al., 2002; Huang and Rothwell, 2004; Maeda et al., 2000; Wu et al., 2000).”
BackgroundAltered dopamine modulation of LTD-like plasticity in Alzheimer's disease patients.
Koch, G., Esposito, Z., Codecà, C., Mori, F., Kusayanagi, H., Monteleone, F., Lorenzo, F. D., Bernardi, G., & Martorana, A. (2011) · Clinical Neurophysiology · doi:10.1016/j.clinph.2010.10.033 · Cited by 51
“Nevertheless, when rTMS is given at low frequencies of stimulation over the primary motor cortex (M1), in the range of 1 Hz, can induce LTD-like inhibition of cortical excitability (Chen et al., 1997), whereas frequencies >5 Hz can induce LTP-like facilitation.”
A unifying conceptual framework of factors associated to cardiac vagal control
Laborde, S., Mosley, E., & Mertgen, A. (2018) · Heliyon · doi:10.1016/j.heliyon.2018.e01002 · Cited by 49
“, 1998) or the decrease (Chen et al., 1997) in cortical excitability even beyond the duration of the train of stimuli.”
BackgroundPrecise Modulation Strategies for Transcranial Magnetic Stimulation: Advances and Future Directions
Zhong, G., Yang, Z., & Jiang, T. (2021) · Neuroscience Bulletin · doi:10.1007/s12264-021-00781-x · Cited by 52
Treatment of hemispatial neglect by means of rTMS – a review
Cazzoli, D., Müri, R. M., Hess, C. W., & Nyffeler, T. (2010) · Restorative Neurology and Neuroscience · doi:10.3233/rnn-2010-0560 · Cited by 49
“However, the question about a possible therapeutic application remained unclear, since similar rTMS protocols have been shown to have an effect lasting only about 15 minutes in healthy subjects (Chen et al., 1997).”
Mesquita, R. C., Faseyitan, O. K., Turkeltaub, P. E., Buckley, E. M., Thomas, A. L., Kim, M. N., Durduran, T., Greenberg, J. H., Detre, J. A., Yodh, A. G., et al. (2013) · Journal of Biomedical Optics · doi:10.1117/1.jbo.18.6.067006 · Cited by 48
“physiology and on behaviors that persist after discontinuation of stimulation.(6,7)”
BackgroundSuppa, A., Biasiotta, A., Belvisi, D., Marsili, L., Cesa, S. L., Truini, A., Cruccu, G., & Berardelli, A. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhs182 · Cited by 51
“Our data also agree with previous studies showing that 0.1 Hz-rTMS elicits no changes in MEP amplitudes (Chen et al. 1997; Cincotta et al. 2003; Fitzgerald et al. 2006).”
InfluentialInfluence of inter-train interval on the plastic effects of rTMS
Cash, R. F. H., Dar, A., Hui, J., Ruiter, L. D., Baarbé, J. K., Fettes, P., Peters, S., Fitzgerald, P. B., Downar, J. H., & Chen, R. E. (2017) · Brain stimulation · doi:10.1016/j.brs.2017.02.012 · Cited by 50
“For example, rTMS delivered at high frequencies induces long-term potentiation (LTP) -like increases in cortical excitability while low frequency rTMS elicits long-term depression (LTD) -like decreases in cortical excitability [1,2].”
BackgroundSelf-citationBorgomaneri, S., Vitale, F., & Avenanti, A. (2017) · Brain Structure and Function · doi:10.1007/s00429-017-1403-5 · Cited by 48
Losing my hand. Body ownership attenuation after virtual lesion of the primary motor cortex
Fossataro, C., Bruno, V., Giurgola, S., Bolognini, N., & Garbarini, F. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.14116 · Cited by 49
“According to our predictions, we found that the inhibitory effect of rTMS over M1 (Chen et al., 1997; Maeda, Keenan, Tormos, Topka, & Pascual- Leone, 2000; Siebner & Rothwell, 2003) strengthens the RHI susceptibility in our subjects, as proved by the significant increase, in rTMS compared to Sham,…”
BackgroundShift in sound localization induced by rTMS of the posterior parietal lobe.
Lewald, J., Wienemann, M., & Boroojerdi, B. (2004) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2004.04.012 · Cited by 54
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“, 2000), or last several minutes after the end of the train (long-term) (Chen et al., 1997).”
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“Flat coil can induce an electric current circumscribed to cortical structures (superficial) and be more focal vertically than the double cone coil (Cohen et al., 1990).”
BackgroundContribution of noninvasive cortical stimulation to the study of memory functions
Flöel, A., & Cohen, L. G. (2006) · Brain Research Reviews · doi:10.1016/j.brainresrev.2006.08.006 · Cited by 48
Self-citationThe neurobiology of misophonia and implications for novel, neuroscience-driven interventions
Neacsiu, A. D., Szymkiewicz, V., Galla, J. T., Li, B., Kulkarni, Y., & Spector, C. W. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.893903 · Cited by 53
“High-frequency (HF; up to 20 Hz) rTMS has been associated with more excitability resulting in enhanced activity, and low frequency (≤1 Hz) with less excitability, and inhibited activity (Pascual-Leone et al., 1994; Chen et al., 1997; Neacsiu and Lisanby, 2015).”
BackgroundAdvances in the Application of Technology to Epilepsy: The CIMIT/NIO Epilepsy Innovation Summit
Schachter, S. C., Guttag, J. V., Schiff, S. J., & Schomer, D. L. (2009) · Epilepsy & Behavior · doi:10.1016/j.yebeh.2009.06.028 · Cited by 46
Pollok, B., Rothkegel, H., Schnitzler, A., Paulus, W., & Lang, N. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06044.x · Cited by 46
“, 2006) without changes of basic motor behaviour, as determined by maximum tapping speed (Chen et al., 1997) or muscle force and movement acceleration of the thumb (Muellbacher et al.”
BackgroundInfluentialInterference in Ballistic Motor Learning: Specificity and Role of Sensory Error Signals
Lundbye‐Jensen, J., Petersen, T. H., Rothwell, J. C., & Nielsen, J. B. (2011) · PLoS ONE · doi:10.1371/journal.pone.0017451 · Cited by 46
“Several studies have documented that low frequency rTMS can reduce cortical excitability transiently [5,14,15,16,26] for review see [17].”
Paes, F., Machado, S., Arias-Carrión, Ó., Velasques, B., Teixeira, S., Budde, H., Cagy, M., Piedade, R., Ribeiro, P., Huston, J., et al. (2011) · CNS and Neurological Disorders - Drug Targets · doi:10.2174/187152711796234943 · Cited by 43
“[27], showed that rTMS administered at 0.”
Competing Mechanisms for Mapping Action-Related Categorical Knowledge and Observed Actions
Candidi, M., Vicario, C. M., Abreu, A. M., & Aglioti, S. M. (2010) · Cerebral Cortex · doi:10.1093/cercor/bhq033 · Cited by 47
Singh, A., Erwin-Grabner, T., Sutcliffe, G., Antal, A., Paulus, W., & Goya‐Maldonado, R. (2019) · Scientific Reports · doi:10.1038/s41598-019-42067-3 · Cited by 47
Functional Imaging of Stroke Recovery: What Have We Learnt and Where Do We Go from Here?
Johansen‐Berg, H. (2007) · International Journal of Stroke · doi:10.1111/j.1747-4949.2007.00093.x · Cited by 46
Bohning, D. E., Shastri, A., Lomarev, M. P., Lorberbaum, J. P., Nahas, Z. H., & George, M. S. (2003) · Journal of Magnetic Resonance Imaging · doi:10.1002/jmri.10271 · Cited by 47
“Typically applied in trains, electrophysiologic studies with TMS have reported inhibition when applied at frequencies of 1 Hz (32) and facilitation when applied at frequencies 1 Hz (33).”
BackgroundResultImpaired Interhemispheric Interactions in Patients With Major Depression
Bajwa, S., Bermpohl, F., Rigonatti, S. P., Pascual‐Leone, Á., Boggio, P. S., & Fregni, F. (2008) · The Journal of Nervous and Mental Disease · doi:10.1097/nmd.0b013e318183f86f · Cited by 46
“Repetitive TMS was applied in 1 continuous train of 15 minutes duration similar duration as the study of Chen et al. (1997) at 1 Hz over left M1 using an intensity that was set at 90% of the participant’s MT similar intensity as the study of Gangitano et al. (2002) .”
MethodLorenzano, C., Dinapoli, L., Gilio, F., et al. (2006) · Clinical Neurophysiology · doi:10.1016/j.clinph.2006.04.012 · Cited by 47
“Trains at low frequency (1 Hz or less) produce inhibitory effects (Chen et al., 1997) whereas those at high frequency (5–20 Hz) produce facilitatory effects (Berardelli et al.”
BackgroundApproach to tinnitus management.
Wu, V., Cooke, B., Eitutis, S. T., Simpson, M. T. W., & Beyea, J. A. (2018) · Europe PMC (PubMed Central) · Cited by 50
Motor Cortical Network Excitability in Parkinson's Disease
Leodori, G., Bartolo, M. I. D., Guerra, A., Fabbrini, A., Rocchi, L., Latorre, A., Paparella, G., Belvisi, D., Conte, A., Bhatia, K. P., et al. (2022) · Movement Disorders · doi:10.1002/mds.28914 · Cited by 47
“61 However, we found that TEP amplitude obtained by averaging the fi rst third of TMS epochs did not signi fi - cantly differ from TEP amplitude observed in the second and last third of trials for HCs or OFF patients.”
ResultThe effects of 1 Hz rTMS preconditioned by tDCS on gait kinematics in Parkinson’s disease
von Papen, M., Fisse, M., Sarfeld, A., et al. (2014) · Journal of Neural Transmission · doi:10.1007/s00702-014-1178-2 · Cited by 46
“Depending on stimulation parameters, rTMS over the primary motor cortex (M1) induces either an increase (high frequency stimulation) or a decrease (low frequency stimulation) of cortico-spinal excitability that outlasts the stimulation period (Pascual-Leone et al. 1994; Chen et al. 1997).”
BackgroundAndoh, J., Eric Artiges, A., Pallier, C., Rivière, D., Mangin, J., Martinot, M. P., & Martinot, J. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhm047 · Cited by 46
“To date, the modulatory effects of TMS on cortical excitability have been shown to depend on the frequency, intensity, duration, and intertrain interval (Chen et al. 1997; Berardelli et al. 1998; Pascual-Leone et al. 1998).”
BackgroundPark, H.-J., Furmaga, H., Cooperrider, J., et al. (2015) · Brain stimulation · doi:10.1016/j.brs.2015.06.020 · Cited by 46
“Cortical excitability was assessed by motor evoked potentials [19,20], and changes in cortical excitability related to the stroke, as well as frequency of stimulation, are reported.”
MethodRemue, J., Baeken, C., & Raedt, R. D. (2016) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2016.03.012 · Cited by 50
Pisapia, N. D., Barchiesi, G., Jovicich, J., & Cattaneo, L. (2018) · Brain Imaging and Behavior · doi:10.1007/s11682-018-9867-3 · Cited by 44
“The effects of 1 Hz rTMS have been shown to last for a period equivalent to the duration of the stimulation train (R. Chen et al. 1997; W. H. Chen et al. 2003).”
Noninvasive Brain Stimulation in Epilepsy
VanHaerents, S. A., Chang, B. S., Rotenberg, A., Pascual‐Leone, Á., & Shafi, M. M. (2020) · Journal of Clinical Neurophysiology · doi:10.1097/wnp.0000000000000573 · Cited by 45
Ziemann, U., Tam, A., Bütefisch, C., & Cohen, L. (2002) · Clinical Neurophysiology · doi:10.1016/s1388-2457(02)00171-2 · Cited by 46
“This low-frequency rTMS does not produce any measurable change in motor cortex excitability when given in the absence of INB, although subtle changes cannot be ruled out (Chen et al., 1997; Ziemann et al., 1998a,b).”
BackgroundSelf-citationMagnuson, J. R., Ozdemir, M. A., Mathieson, E., Kirkman, S., Passera, B., Rampersad, S. M., Dufour, A. B., Brooks, D. H., Pascual‐Leone, Á., Fried, P. J., et al. (2023) · PLoS ONE · doi:10.1371/journal.pone.0286465 · Cited by 47
Mechanisms and therapeutic applications of electromagnetic therapy in Parkinson’s disease
Vadalà, M., Vallelunga, A., Palmieri, L., Palmieri, B., Morales‐Medina, J. C., & Iannitti, T. (2015) · Behavioral and Brain Functions · doi:10.1186/s12993-015-0070-z · Cited by 45
Priming the Brain to Capitalize on Metaplasticity in Stroke Rehabilitation
Cassidy, J. M., Gillick, B. T., & Carey, J. R. (2013) · Physical Therapy · doi:10.2522/ptj.20130027 · Cited by 46
Villalta, J. I., Landi, S. M., Fló, A., & Della‐Maggiore, V. (2013) · Cerebral Cortex · doi:10.1093/cercor/bht346 · Cited by 43
“Transcranial Magnetic Stimulation It is now well established that low-frequency rTMS applied during 15 min over the SM increases the motor threshold and depresses corticospinal excitability (Chen et al. 1997; Romero et al. 2002).”
BackgroundTargeting Neural Endophenotypes of Eating Disorders with Non-invasive Brain Stimulation
Dunlop, K., Woodside, D. B., & Downar, J. H. (2016) · Frontiers in Neuroscience · doi:10.3389/fnins.2016.00030 · Cited by 44
“Higher frequency stimulation (5–20Hz) is usually considered to be excitatory, while low frequency (<1Hz) stimulation is considered inhibitory (Pascual-Leone et al., 1994; Chen et al., 1997).”
BackgroundDosSantos, M. F. H., Oliveira, A. T., Ferreira, N. R., Carvalho, A. C. P., & Rosado-de-Castro, P. H. (2018) · Pain Research and Management · doi:10.1155/2018/2368386 · Cited by 44
“*erefore, LTP and LTD, well-known mechanisms of synaptic plasticity would constitute the neuroanatomical basis of TMS mechanisms.”
BackgroundGoldsworthy, M., Vallence, A., Hodyl, N., Semmler, J., Pitcher, J. B., & Ridding, M. (2016) · Clinical Neurophysiology · doi:10.1016/j.clinph.2015.06.014 · Cited by 44
“Conventional rTMS approaches involve a constant rate of stimulation, with low frequencies (61 Hz) reducing cortical excitability (Chen et al., 1997) and high frequencies (P5 Hz) increasing cortical excitability (Berardelli et al.”
BackgroundVerplaetse, J., Schrijver, J. D., Vanneste, S., & Braeckman, J. (2009) · Springer eBooks · doi:10.1007/978-1-4020-6287-2 · Cited by 49
Transcranial Magnetic Stimulation
Kobayashi, M., & Pascual‐Leone, Á. (2007) · Humana Press eBooks · doi:10.1007/978-1-59745-271-7_28 · Cited by 47
Safety of 6-Hz Primed Low-Frequency rTMS in Stroke
Carey, J. R., Evans, C. D., Anderson, D. C., Bhatt, E., Nagpal, A., Kimberley, T. J., & Pascual‐Leone, Á. (2007) · Neurorehabilitation and neural repair · doi:10.1177/1545968307305458 · Cited by 45
The nature of corticospinal paths driving human motoneurones during voluntary contractions
Butler, J. E., Larsen, T. S., Gandevia, S. C., et al. (2007) · The Journal of Physiology · doi:10.1113/jphysiol.2007.134205 · Cited by 45
“It has been reported that TMS at an interstimulus interval of about 1 Hz may produce effects on cortical excitability in hand muscles (Chen et al. 1997) although this does not occur for elbow flexor muscles (Martin et al.”
BackgroundWang, J., Deng, X., Wu, Y., Li, X., Feng, Z., Wang, H.-X., Jing, Y., Zhao, N., Zang, Y., & Zhang, J. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.00186 · Cited by 44
“Lowfrequency (≤1 Hz) and high-frequency (≥5 Hz) stimulation are two classic rTMS paradigms and cause inhibitory effects through long-term depression (LTD) of synaptic transmission, and excitatory effects through long-term potentiation (LTP), respectively (Chen et al., 1997; Pascual-Leone et al., 1998; Post et al., 199…”
BackgroundTranscranial magnetic stimulation and sleep disorders: pathophysiologic insights
Nardone, R., Höller, Y., Brigo, F., Tezzon, F., Golaszewski, S. M., & Trinka, E. (2013) · Sleep Medicine · doi:10.1016/j.sleep.2013.04.025 · Cited by 46
“Generally low-frequency rTMS (stimulus rates of 61 Hz) induces inhibitory effects on motor cortical excitability allowing creation of a reversible virtual lesion [32], while high-frequency rTMS (5–20 Hz) usually promotes an increase in cortical excitability [33,34].”
BackgroundMachado, S. E. D. C., Arias-Carrión, Ó., Paes, F., Vieira, R. T., Caixeta, L. F., Novaes, F. C., Pessoa, T. M., Almada, L. F., Silva, A. C., & Nardi, A. E. (2013) · Eurasian Journal of Medicine · doi:10.5152/eajm.2013.39 · Cited by 49
“Although the response to rTMS can vary across individuals [22], highfrequency rTMS seems to facilitate cortical excitability, whereas low-frequency rTMS can suppress this excitability on the motor cortex [23-24].”
BackgroundPictures of disgusting foods and disgusted facial expressions suppress the tongue motor cortex
Vicario, C. M., Rafal, R. D., Borgomaneri, S., Paracampo, R., Kritikos, A., & Avenanti, A. (2016) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsw129 · Cited by 46
“The inter-pulse interval was > 10 s to avoid changes in motor excitability due to TMS per se (Chen et al., 1997).”
BackgroundMethodSun, W., Fu, W., Mao, W., et al. (2011) · Clinical EEG and Neuroscience · doi:10.1177/155005941104200109 · Cited by 44
Non-invasive induction of plasticity in the human cortex: Uses and limitations
Vallence, A., & Ridding, M. C. (2013) · Cortex · doi:10.1016/j.cortex.2013.12.006 · Cited by 45
“Both conventional and patterned rTMS protocols induce changes in cortical excitability that outlast the stimulation period and are reversible (Berardelli et al., 1998; Chen et al., 1997; Huang et al., 2005).”
BackgroundHemispheric cerebellar rTMS to treat drug-resistant epilepsy: Case reports
Brighina, F., Daniele, O., Piazza, A., Giglia, G., & Fierro, B. (2006) · Neuroscience Letters · doi:10.1016/j.neulet.2005.12.050 · Cited by 45
Motor cortex stimulation for amyotrophic lateral sclerosis. Time for a therapeutic trial?
Lazzaro, V. D., Oliviero, A., Saturno, E., Pilato, F., Dileone, M., Sabatelli, M., & Tonali, P. A. (2004) · Clinical Neurophysiology · doi:10.1016/j.clinph.2004.01.027 · Cited by 43
“, 2003), and because the excitability of neural circuits in the cerebral cortex is not static, repetitive TMS (rTMS) can produce changes in neurotransmission that outlast the period of stimulation (Berardelli et al., 1998; Chen et al., 1997; Di Lazzaro et al., 2002; Maeda et al., 2000; Pascual-Leone et al., 1994a,b, 1…”
BackgroundEitan, R., & Lerer, B. (2006) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2006.8.2/reitan · Cited by 43
Grüner, U., Eggers, C., Ameli, M., Sarfeld, A., Fink, G. R., & Nowak, D. A. (2009) · Journal of Neural Transmission · doi:10.1007/s00702-009-0356-0 · Cited by 44
“1994) or a decrease (Chen et al. 1997) of cortico-spinal excitability that outlasts the stimulation period for several minutes.”
BackgroundRollnik, J. D., Schröder, C., Rodríguez‐Fornells, A., Kurzbuch, A. R., Däuper, J., Möller, J., & Münte, T. F. (2003) · Clinical Neurophysiology · doi:10.1016/j.clinph.2003.05.001 · Cited by 41
“For example, Chen and coworkers have used a 15 min 0.9 Hz rTMS train and found a decrease of motor cortex excitability lasting 15 min after the end of the stimulation (Chen et al., 1997).”
BackgroundMethodInfluential
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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