Cited by 2,128Transcranial Magnetic Stimulation StudiesNeuroscience and Neuropharmacology ResearchDeep Brain Stimulation and Movement Disorders

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Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation

Chen, R., Classen, J., Gerloff, C., Celnik, P., Wassermann, E. M., Hallett, M., Cohen, L. G.·1997·Neurology

DOI 10.1212/wnl.48.5.1398

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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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Background
Effects of low frequency rTMS treatment on brain networks for inner speech in patients with schizophrenia and auditory verbal hallucinations
Bais, L., Liemburg, E. J., Vercammen, A., Bruggeman, R., Knegtering, H., & Aleman, A. (2017) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.04.017 · Cited by 57
“Decreases in brain metabolism were observed in the left superior temporal gyrus, the left inferior temporal gyrus and the left insula after low frequency rTMS treatment, which could be explained by the immediate inhibitory effect of 1 Hz rTMS on brain function (Chen et al., 1997; Mottaghy et al., 2003).”
Comparative study of ipsilesional and contralesional repetitive transcranial magnetic stimulations for acute infarction
Watanabe, K., Kudo, Y., Sugawara, E., Nakamizo, T., Amari, K., Koji, T., Tanaka, O., Endo, M., Hayakawa, Y., & Johkura, K. (2017) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2017.11.001 · Cited by 57
Impaired short-term plasticity in restless legs syndrome: a pilot rTMS study
Lanza, G., Lanuzza, B., Aricò, D., et al. (2018) · Sleep Medicine · doi:10.1016/j.sleep.2018.02.008 · Cited by 56
Smoking Cessation With 20 Hz Repetitive Transcranial Magnetic Stimulation (rTMS) Applied to Two Brain Regions: A Pilot Study
Chang, D., Zhang, J., Peng, W., Shen, Z., Gao, X., Du, Y., Ge, Q., Song, D., Shang, Y., & Wang, Z. (2018) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2018.00344 · Cited by 54
Neuromodulation Strategies for the Treatment of Depression
Conroy, S. K., & Holtzheimer, P. E. (2021) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2021.21101034 · Cited by 55
Molecular Mechanisms and Therapeutic Strategies for Levodopa-Induced Dyskinesia in Parkinson’s Disease: A Perspective Through Preclinical and Clinical Evidence
Bandopadhyay, R., Mishra, N., Rana, R., Kaur, G., Ghoneim, M. M., Alshehri, S., Mustafa, G., Ahmad, J., Alhakamy, N. A., & Mishra, A. (2022) · Frontiers in Pharmacology · doi:10.3389/fphar.2022.805388 · Cited by 58
“It has been observed that the excitability in the cortical region gets increased after application of high-frequency stimulation, and it gets decreased by the application of low-frequency stimulation, but in the case of theta-burst stimulation (TBS), intermittent stimulation increases cortical excitability, whereas co…”
Background
Therapeutic effect of repetitive magnetic stimulation combined with speech and language therapy in post-stroke non-fluent aphasia
Yoon, T. H., Han, S. J., Yoon, T. S., Kim, J. S., & Yi, T. I. (2015) · Neurorehabilitation · doi:10.3233/nre-141198 · Cited by 57
“In contrast, low-frequency rTMS (≤1 Hz) suppresses or inhibits neural activity, and has the advantage of modulating the excitability of a given cortical area beyond the duration of the rTMS session itself (Chen et al., 1997; Kobayashi & Pascual-Leone, 2003; Pascual-Leone et al., 1998; Sparing et al., 2001).”
Background
High frequency repetitive transcranial magnetic stimulation (rTMS) is effective in migraine prophylaxis: an open labeled study
Misra, U. K., Kalita, J., & Bhoi, S. K. (2012) · Neurological Research · doi:10.1179/1743132812y.0000000045 · Cited by 54
Transcranial Magnetic Stimulation for the treatment of tinnitus: Effects on cortical excitability
Langguth, B., Kleinjung, T., Marienhagen, J., Binder, H., Sand, P. G., Hajak, G., & Eichhammer, P. (2007) · BMC Neuroscience · doi:10.1186/1471-2202-8-45 · Cited by 56
“When used in the low-frequency range, rTMS modulates brain activity both in directly stimulated regions and in functionally connected brain areas [18,19].”
Background
Variability of behavioural responses to transcranial magnetic stimulation: Origins and predictors
Nicolo, P., Ptak, R., & Guggisberg, A. G. (2015) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2015.01.033 · Cited by 56
“In early studies low-frequency rTMS (1 Hz or less) has been found to inhibit the underlying cortex (Chen et al., 1997), while facilitatory effects were observed after high-frequency stimulation (5 Hz or more) (Pascual-Leone et al., 1994). However, as shown by a study of Gangitano et al. (2002) it would be an oversimpl…”
Background
Facilitation of Aδ-fiber-mediated acute pain by repetitive transcranial magnetic stimulation
Tamura, Y., Hoshiyama, M., Inui, K., Nakata, H., Qiu, Y.-H., Ugawa, Y., Inoue, K., & Kakigi, R. (2004) · Neurology · doi:10.1212/01.wnl.0000130081.96533.85 · Cited by 52
Dopaminergic potentiation of rTMS-induced motor cortex inhibition.
Lang, N., Speck, S., Harms, J., Rothkegel, H., Paulus, W., & Sommer, M. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.04.033 · Cited by 53
Transcranial Magnetic Stimulation
Pape, T., Rosenow, J. M., & Lewis, G. N. (2006) · Journal of Head Trauma Rehabilitation · doi:10.1097/00001199-200609000-00063 · Cited by 55
Effect of electroconvulsive therapy on cortical excitability in patients with major depression: a transcranial magnetic stimulation study
Chistyakov, A. V., Kaplan, B., Rubichek, O., Kreinin, I., Koren, D., Hafner, H., D, M. F. M., & Klein, E. (2004) · Clinical Neurophysiology · doi:10.1016/j.clinph.2004.09.008 · Cited by 54
“It has been also established that this kind of rTMS, in contrast to high frequency rTMS, produces a suppression of the stimulated cortex excitability which outlasts the duration of the stimulus train by at least several minutes (Boroojerdi et al., 2000; Chen et al., 1997).”
BackgroundMethod
Improved Discrimination of Visual Stimuli Following Repetitive Transcranial Magnetic Stimulation
Waterston, M. L., & Pack, C. C. (2010) · PLoS ONE · doi:10.1371/journal.pone.0010354 · Cited by 55
Theta‐burst stimulation over primary motor cortex degrades early motor learning
Iezzi, E., Suppa, A., Conte, A., Agostino, R., Nardella, A., & Berardelli, A. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07090.x · Cited by 54
“Although at least some of the inhibitory effects of 1-Hz rTMS (Chen et al., 1997) are known to take place at the cortical level (Di Lazzaro et al.”
Background
Modulation of EEG Functional Connectivity Networks in Subjects Undergoing Repetitive Transcranial Magnetic Stimulation
Shafi, M. M., Westover, M. B., Oberman, L. M., Cash, S. S., & Pascual‐Leone, Á. (2013) · Brain Topography · doi:10.1007/s10548-013-0277-y · Cited by 55
“When a train of TMS stimuli is applied (repetitive TMS, or rTMS), changes in cortical activity can persist long after the end of stimulation (Chen et al. 1997; Pascual-Leone et al. 1994; Thut and Pascual-Leone 2010).”
Advancing non-invasive neuromodulation clinical trials in children: Lessons from perinatal stroke
Kirton, A. (2016) · European Journal of Paediatric Neurology · doi:10.1016/j.ejpn.2016.07.002 · Cited by 60
New perspectives for the study of lucid dreaming: From brain stimulation to philosophical theories of self-consciousness
Noreika, V., Windt, J., Lenggenhager, B., & Karim, A. A. (2010) · International journal of dream research · doi:10.11588/ijodr.2010.1.586 · Cited by 55
“could be also tested by applying low-frequency rTMS over the DLPFC, which has been shown to inhibit cortical excitability (Karim et al., 2003; Chen et al., 1997).”
BackgroundMethodInfluential
Intermittent Theta Burst Stimulation of the Prefrontal Cortex in Cocaine Use Disorder: A Pilot Study
Sanna, A., Fattore, L., Badas, P., Corona, G., Cocco, V., & Diana, M. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00765 · Cited by 58
The role of transcranial magnetic stimulation in the study of cerebellar cognitive function
Oliveri, M., Torriero, S., Koch, G., et al. (2007) · The Cerebellum · doi:10.1080/14734220701213421 · Cited by 54
“These data suggest that low-frequency rTMS trains can provide a useful tool to produce plastic changes in the cerebellar cortex, similar to those reported for many cerebral areas, including motor, prefrontal and premotor cortex (6,17,8,24).”
Result
Changes in Visual Responses in the Feline dLGN: Selective Thalamic Suppression Induced by Transcranial Magnetic Stimulation of V1
de Labra, C., Rivadulla, C., Grieve, K. L., Marino, J., Espinosa, N., & Cudeiro, J. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhl048 · Cited by 54
Bilateral Low-Frequency Repetitive Transcranial Magnetic Stimulation of the Auditory Cortex in Tinnitus Patients Is Not Effective: A Randomised Controlled Trial
Hoekstra, C. E. L., Versnel, H., Neggers, S. F. W., Niesten, M. E. F., & van Zanten, G. A. (2013) · Audiology and Neurotology · doi:10.1159/000354977 · Cited by 53
“rTMS at low rates ( ≤ 1 Hz) is thought to suppress neural activity [Chen et al., 1997; Hallett, 2007].”
Background
Transcranial magnetic stimulation for post-traumatic stress disorder
Petrosino, N. J., Cosmo, C. S. A., Berlow, Y. A., Zandvakili, A., Wout‐Frank, M. V. ‘., & Philip, N. S. (2021) · Therapeutic Advances in Psychopharmacology · doi:10.1177/20451253211049921 · Cited by 55
Mechanisms of Action of TMS in the Treatment of Depression
Downar, J. H., Siddiqi, S., Mitra, A., Williams, N., & Liston, C. M. (2024) · Current topics in behavioral neurosciences · doi:10.1007/7854_2024_483 · Cited by 59
Assessment and treatment of pain with non-invasive cortical stimulation
Zaghi, S., Thiele, B., Pimentel, D., Pimentel, T., & Fregni, F. (2011) · Restorative Neurology and Neuroscience · doi:10.3233/rnn-2011-0615 · Cited by 61
Shifts in connectivity during procedural learning after motor cortex stimulation: A combined transcranial magnetic stimulation/functional magnetic resonance imaging study
Steel, A., Song, S., Bageac, D. V., Knutson, K. M., Keisler, A., Saad, Z. S., Gotts, S. J., Wassermann, E. M., & Wilkinson, L. (2015) · Cortex · doi:10.1016/j.cortex.2015.10.004 · Cited by 51
“This effect resembles longterm synaptic depression (R. Chen et al., 1997; Huang, Edwards, Rounis, Bhatia, & Rothwell, 2005; Iyer, Schleper, & Wassermann, 2003; Wassermann, Wedegaertner, Ziemann, George, & Chen, 1998; Wilkinson et al., 2015) and likely reflects a change in the efficacy of synapses…”
BackgroundSelf-citation
Moving sounds within the peripersonal space modulate the motor system
Finisguerra, A., Canzoneri, E., Serino, A., Pozzo, T., & Bassolino, M. (2014) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2014.09.043 · Cited by 54
“The inter-trial interval was controlled via software to ensure that it was always higher than 10 s (precisely, between 10 and 12 s) in order to avoid inducing a change in motor excitability (Chen et al., 1997).”
Repetitive transcranial magnetic stimulation for ALS
Lazzaro, V. D., Dileone, M., Pilato, F., Profice, P., Ranieri, F., Musumeci, G., Angelucci, F., Sabatelli, M., & Tonali, P. A. (2006) · Neuroscience Letters · doi:10.1016/j.neulet.2006.08.069 · Cited by 53
Therapeutic Efficacy of Neurostimulation for Depression: Techniques, Current Modalities, and Future Challenges
Akhtar, H., Bukhari, F., Nazir, M., Anwar, M. N., & Shahzad, A. (2016) · Neuroscience Bulletin · doi:10.1007/s12264-015-0009-2 · Cited by 64
Analgesic effect of repetitive transcranial magnetic stimulation (rTMS) in patients with chronic low back pain
Ambriz‐Tututi, M., Alvarado‐Reynoso, B., & Drucker-Colı́n, R. (2016) · Bioelectromagnetics · doi:10.1002/bem.22001 · Cited by 56
“rTMS has potential therapeutic use since it modulates the level of excitability of a given cortical area beyond the duration of the stimulation [Chen et al., 1997; Berardelli et al., 1998; Pascual-Leone et al., 1998].”
Background
Attending to local form while ignoring global aspects depends on handedness: evidence from TMS
Mevorach, C., Humphreys, G. W., & Shalev, L. (2005) · Nature Neuroscience · doi:10.1038/nn1400 · Cited by 56
Do electrically stimulated sensory inputs and movements lead to long-term plasticity and rehabilitation gains?
Dobkin, B. H. (2003) · Current Opinion in Neurology · doi:10.1097/00019052-200312000-00007 · Cited by 53
Short-lasting impairment of tactile perception by 0.9Hz-rTMS of the sensorimotor cortex
Satow, T., Mima, T., Yamamoto, J., Oga, T., Begum, T., Aso, T., Hashimoto, N., Rothwell, J. C., & Shibasaki, H. (2003) · Neurology · doi:10.1212/01.wnl.0000052821.99580.d3 · Cited by 53

Authors: Chen, R., Classen, J., Gerloff, C., Celnik, P., Wassermann, E. M., Hallett, M., & Cohen, L. G.
Affiliations: National Institutes of Health (US)
ORCID: Classen, J.
Gerloff, C.
Celnik, P.
Wassermann, E. M.
Hallett, M.
Venue: Neurology
Publisher: Ovid Technologies (Wolters Kluwer Health)
Published: 1997-05
Volume: 48
Issue: 5
Pages: 1398-1403
ISSN: 0028-3878 (ISSN-L)
1526-632X
DOI: 10.1212/wnl.48.5.1398
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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Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation

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