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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Mansur, C. G., Fregni, F., Boggio, P. S., Riberto, M., Neto, J. G., dos Santos, C. M., Wagner, T., Rigonatti, S. P., Marcolin, M. A., & Pascual‐Leone, Á. (2005) · Neurology · doi:10.1212/01.wnl.0000161839.38079.92 · Cited by 544 · see citing works
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“…threshold for evoked muscle twitches produces a refractory state in which the electromyographic response to stimulation, the motor-evoked potential (MEP), is reduced in size (Wassermann et al., 1996b; Chen et al., 1997a; Touge et al., 2001), and its threshold is elevated (Fitzgerald et al., 2002).”
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“Reflecting findings in MDD (41, 42), repetitive TMS increased cortical inhibition (55) and lengthened CSP (56) in healthy individuals, suggesting enhanced GABA neurotransmission.”
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“Experimental LTD depends on prolonged weak synaptic activation, and this is achieved with low intensity and frequency TMS given over periods of 10– 15 min or even repeated over consecutive days (Chen et al. 1997; Maeda et al. 2000b; Fitzgerald et al. 2006).”
BackgroundLazzaro, V. D., Profice, P., Ranieri, F., Capone, F., Dileone, M., Oliviero, A., & Pilato, F. (2011) · Brain stimulation · doi:10.1016/j.brs.2011.07.008 · Cited by 326 · see citing works
Touge, T., Gerschlager, W., Brown, P., & Rothwell, J. C. (2001) · Clinical Neurophysiology · doi:10.1016/s1388-2457(01)00651-4 · Cited by 325 · see citing works
“…Maeda et al., 2000; Berardelli et al., 1998; Peinemann et al., 2000; Romeo et al., 2000), whereas low-frequency rTMS (i.e. rTMS at a frequency of 1 Hz) causes a short-term decrease in corticomotor excitability (Chen et al., 1997; Siebner et al., 1999a; Muellbacher et al., 2000; Maeda et al., 2000).”
BackgroundSauseng, P., Klimesch, W., Gerloff, C. P., & Hummel, F. C. (2008) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2008.07.021 · Cited by 315 · see citing works
Self-citationFettes, P., Schulze, L., & Downar, J. (2017) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2017.00025 · Cited by 299 · see citing works
“Inhibitory forms of rTMS, thought to act via long-term depression, include low frequency (1 Hz) stimulation (Chen et al., 1997) and continuous theta burst stimulation (cTBS; Huang et al., 2009).”
BackgroundPeinemann, A., Reimer, B., Löer, C., Quartarone, A., Münchau, A. M., Conrad, B., & Siebner, H. R. (2004) · Clinical Neurophysiology · doi:10.1016/j.clinph.2004.02.005 · Cited by 317 · see citing works
“Conversely, low-frequency rTMS (at frequencies of around 1 Hz) causes a short-term decrease in corticospinal excitability (Chen et al., 1997; Muellbacher et al., 2000).”
BackgroundInfluentialLow-frequency repetitive transcranial magnetic stimulation improves intractable epilepsy
Tergau, F., Naumann, U., Paulus, W., & Steinhoff, B. J. (1999) · The Lancet · doi:10.1016/s0140-6736(99)01301-x · Cited by 317 · see citing works
Chou, Y.-H., Ton That, V., & Sundman, M. (2020) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2019.08.020 · Cited by 319 · see citing works
Brief bursts of pulse stimulation terminate afterdischarges caused by cortical stimulation
Lesser, R. P., Kim, S. H., Beyderman, L., et al. (1999) · Neurology · doi:10.1212/wnl.53.9.2073 · Cited by 309 · see citing works
Di Lazzaro, V., Dileone, M., Pilato, F., Capone, F., Musumeci, G., Ranieri, F., Ricci, V., Bria, P., Di Iorio, R., de Waure, C., et al. (2011) · Journal of Neurophysiology · doi:10.1152/jn.00781.2010 · Cited by 303 · see citing works
“Low-frequency rTMS (stimulus rates of 1 Hz or less) produces a lasting decrease in motor cortex excitability (Chen et al. 1997), whereas high-frequency rTMS (stimulus rates of 5 Hz or higher) (Berardelli et al.”
InfluentialStudies of human motor physiology with transcranial magnetic stimulation
Chen, R. E. (2000) · Muscle & Nerve · doi:10.1002/1097-4598(2000)999:9 · Cited by 304 · see citing works
Self-citationThe theoretical model of theta burst form of repetitive transcranial magnetic stimulation
Huang, Y., Rothwell, J. C., Chen, R., Lu, C., & Chuang, W. (2010) · Clinical Neurophysiology · doi:10.1016/j.clinph.2010.08.016 · Cited by 300 · see citing works
“For example10 minutes or more 1Hz rTMS conditioning usually leads to LTD-like effects (Chen et al., 1997; Touge et al., 2001) whereas rTMS at 5 Hz leads to LTP-like changes.”
BackgroundSelf-citationLoo, C. K. A., & Mitchell, P. B. (2005) · Journal of Affective Disorders · doi:10.1016/j.jad.2005.08.001 · Cited by 292 · see citing works
“Motor cortex studies suggest that high and low frequency rTMS have opposite effects on the excitability of neurons in brain cortex (Chen et al., 1997; PascualLeone et al., 1994).”
BackgroundNeurochemical Effects of Theta Burst Stimulation as Assessed by Magnetic Resonance Spectroscopy
Stagg, C. J., Wylezinska, M., Matthews, P. M., Johansen‐Berg, H., Jezzard, P., Rothwell, J. C., & Bestmann, S. (2009) · Journal of Neurophysiology · doi:10.1152/jn.91060.2008 · Cited by 292 · see citing works
Lee, L., Siebner, H. R., Rowe, J. B., Rizzo, V., Rothwell, J. C., Frackowiak, R. S. J., & Friston, K. J. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-12-05308.2003 · Cited by 289 · see citing works
“This is in agreement with previous work investigating the effects of rTMS on simple motor behavior (Wassermann et al., 1996; Chen et al., 1997; Pascual Leone et al., 1998; Muellbacher et al., 2000; Rossi et al., 2000).”
BackgroundResultInfluentialPadberg, F., Zwanzger, P., Thoma, H., Kathmann, N., Haag, C., Greenberg, B. D., Hampel, H. J., & Möller, H. (1999) · Psychiatry Research · doi:10.1016/s0165-1781(99)00092-x · Cited by 286 · see citing works
Assessing the mechanisms of brain plasticity by transcranial magnetic stimulation
Jannati, A., Oberman, L. M., Rotenberg, A., & Pascual‐Leone, Á. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-022-01453-8 · Cited by 303 · see citing works
“In contrast, low-frequency (≤1 Hz) rTMS often decreases cortical excitability as measured by the post-rTMS decrease in MEP size [38, 39].”
Hoffman, R. E., & Çavuş, I. (2002) · American Journal of Psychiatry · doi:10.1176/appi.ajp.159.7.1093 · Cited by 286 · see citing works
“(8) have been replicated by other groups, and suppressive effects on the size of motor evoked potentials have lasted up to 30 minutes after stimulation (12, 14).”
BackgroundLazzaro, V. D., & Rothwell, J. C. (2014) · The Journal of Physiology · doi:10.1113/jphysiol.2014.274316 · Cited by 283 · see citing works
“The 1 Hz protocol involves applying one thousand or more pulses at a rate of one per second with a suprathreshold stimulus pulse (Chen et al. 1997).”
MethodTerraneo, A., Leggio, L., Saladini, M., Ermani, M., Bonci, A., & Gallimberti, L. (2016) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2015.11.011 · Cited by 281 · see citing works
“Specifically, repetitive TMS (rTMS) at a low frequency (about 1 Hz) is typically considered to have inhibitory effects, (Chen et al., 1997) while high-frequency rTMS (Z5 Hz) is excitatory (Pascual-Leone et al., 1994).”
BackgroundMantovani, A., Simpson, H. B., Fallon, B. A., Rossi, S., & Lisanby, S. H. (2010) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145709990435 · Cited by 281 · see citing works
“Given the evidence for deficient inhibition in OCD, the use of low-frequency rTMS, which has been reported to be inhibitory on motor cortex excitability (Chen et al. 1997), may be a fruitful avenue to explore as a putative treatment.”
BackgroundUnderstanding the role of the primary somatosensory cortex: Opportunities for rehabilitation
Borich, M., Brodie, S. M., Gray, W. A., Ionta, S., & Boyd, L. A. (2015) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2015.07.007 · Cited by 274 · see citing works
Non-invasive Human Brain Stimulation in Cognitive Neuroscience: A Primer
Parkin, B., Ekhtiari, H., & Walsh, V. (2015) · Neuron · doi:10.1016/j.neuron.2015.07.032 · Cited by 274 · see citing works
“Repetitive 1 Hz rTMS is widely used as an inhibitory intervention (Chen et al., 1997) and is classically associated with mimicking the effects of neuropsychological patients (e.g Guse et al., 2010).”
MethodMapping Implied Body Actions in the Human Motor System
Urgesi, C., Moro, V., Candidi, M., & Aglioti, S. M. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.1289-06.2006 · Cited by 273 · see citing works
“The coil was placed tangentially on the scalp, with the handle pointing backward and laterally 45° away from the midline, approximately perpendicular to the line of the central sulcus.”
MethodInfluentialrTMS of the prefrontal cortex in the treatment of chronic migraine: A pilot study
Brighina, F., Piazza, A., Vitello, G., Aloisio, A., Palermo, A., Daniele, O., & Fierro, B. (2004) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2004.08.008 · Cited by 269 · see citing works
“In particular, repetitive stimulation (rTMS) allows to modulate cortical activity: at low frequencies, it has an inhibitory effect [5], whereas at high frequencies, it is able to enhance cortical excitability [6].”
BackgroundHoffman, R. E., Gueorguieva, R., Hawkins, K. A., Varanko, M., Boutros, N. N., Wu, Y.-T., Carroll, K., & Krystal, J. H. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.03.041 · Cited by 272 · see citing works
Fregni, F., Otachi, P. T. M., Valle, A., Boggio, P. S., Thut, G., Rigonatti, S. P., Pascual‐Leone, Á., & Valente, K. D. R. (2006) · Annals of Neurology · doi:10.1002/ana.20950 · Cited by 272 · see citing works
Motor Representations of Articulators Contribute to Categorical Perception of Speech Sounds
Möttönen, R., & Watkins, K. E. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.6018-08.2009 · Cited by 268 · see citing works
“, to reduce MEP amplitudes) for a further 15 min after the end of rTMS (Chen et al., 1997).”
BackgroundModifying motor learning through gating and homeostatic metaplasticity
Ziemann, U., & Siebner, H. R. (2008) · Brain Stimulation · doi:10.1016/j.brs.2007.08.003 · Cited by 269 · see citing works
Transcranial magnetic stimulation for the treatment of seizures
Theodore, W. H., Hunter, K., Chen, R. E., Vega‐Bermudez, F., Boroojerdi, B., Reeves‐Tyer, P., Werhahn, K. J., Kelley, K., & Cohen, L. G. (2002) · Neurology · doi:10.1212/wnl.59.4.560 · Cited by 267 · see citing works
Self-citationContribution of the ipsilateral motor cortex to recovery after chronic stroke
Werhahn, K. J., Conforto, A. B., Kadom, N., Hallett, M., & Cohen, L. G. (2003) · Annals of Neurology · doi:10.1002/ana.10686 · Cited by 266 · see citing works
“Second, application of 1Hz TMS for 30 minutes at 50% above rMT, as implemented in experiment 3, leads to transient and reversible downregulation of cortical activity in the underlying cortical structures that outlasts the stimulation period for several minutes.(11) We took advantage of this property of the TMS paradig…”
BackgroundMethodSelf-citationReis, J., Robertson, E. M., Krakauer, J. W., Rothwell, J. C., Marshall, L., Gerloff, C. P., Wassermann, E. M., Pascual‐Leone, Á., Hummel, F. C., Celnik, P. A., et al. (2008) · Brain stimulation · doi:10.1016/j.brs.2008.08.001 · Cited by 267 · see citing works
Self-citationRepetitive TMS of the motor cortex improves ipsilateral sequential simple finger movements
Kobayashi, M., Hutchinson, S., Théoret, H., Gottfried Schlaug, A., & Pascual‐Leone, Á. (2004) · Neurology · doi:10.1212/wnl.62.1.91 · Cited by 268 · see citing works
- 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 › Neurology › Neurological disorders and treatments
- 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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