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
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Background
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Background
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Background
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Background
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BackgroundSelf-citation
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BackgroundMethodInfluential
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Background
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Background
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BackgroundResult
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Background
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Background
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Self-citation
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Background
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“In the current study, we used low-frequency TMS to achieve a noninvasive and temporary disruption of insula activity, as such frequency is known to consistently inhibit motor cortical excitability (34), with the aim to replicate the findings from lesion studies and to explore whether urge processing could be modulated.”
MethodSelf-citation
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Method
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Background
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Background
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BackgroundMethod
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Rajji, T. K., Rogasch, N. C., Daskalakis, Z. J., & Fitzgerald, P. B. (2013) · The Canadian Journal of Psychiatry · doi:10.1177/070674371305800206 · Cited by 37
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Reti, I. M., Schwarz, N. R., Bower, A., Tibbs, M., & Rao, V. (2015) · Brain Injury · doi:10.3109/02699052.2015.1009168 · Cited by 40
“The only serious adverse effect of rTMS is seizure, which is very rare nowadays following the publication of safety guidelines [39, 41, 42].”
Background
Cross-modal Processing in the Occipito-temporal Cortex: A TMS Study of the Müller-Lyer Illusion
Mancini, F., Bolognini, N., Bricolo, E., & Vallar, G. (2010) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2010.21561 · Cited by 38
“From a physiological point of view, low-frequency rTMS (1 Hz) generally results in inhibition of the stimulated area (Chen et al., 1997).”
Background
Characterization of Visual Percepts Evoked by Noninvasive Stimulation of the Human Posterior Parietal Cortex
Fried, P. J., Elkin-Frankston, S., Rushmore, J., Hilgetag, C. C., & Valero‐Cabré, A. (2011) · PLoS ONE · doi:10.1371/journal.pone.0027204 · Cited by 37
“In the second experiment, we examined the interdependence of parietal and occipital phosphenes using low frequency (1 Hz) repetitive TMS (rTMS) to temporarily deactivate each site in separate sessions [50,51].”
BackgroundMethod
Voluntary movement and repetitive transcranial magnetic stimulation over human motor cortex
Todd, G., Rogasch, N. C., Flavel, S. C., & Ridding, M. C. (2009) · Journal of Applied Physiology · doi:10.1152/japplphysiol.91364.2008 · Cited by 39
Low-frequency rTMS with language therapy over a 3-month period for sensory-dominant aphasia: Case series of two post-stroke Japanese patients
Kakuda, W., Abo, M., Uruma, G., et al. (2010) · Brain Injury · doi:10.3109/02699052.2010.494587 · Cited by 38
Treating Chronic Migraine With Neuromodulation: The Role of Neurophysiological Abnormalities and Maladaptive Plasticity
Viganò, A., Toscano, M., Puledda, F., & Piero, V. D. (2019) · Frontiers in Pharmacology · doi:10.3389/fphar.2019.00032 · Cited by 42
“By contrast, LTD occurs if postsynaptic neuron fires before the presynaptic one (Markram et al., 1997; Song et al., 2000; D’amour and Froemke, 2015).”
MethodInfluential
Advances in repetitive transcranial magnetic stimulation for posttraumatic stress disorder: A systematic review
Belsher, B. E., Beech, E. H., Reddy, M. K., Smolenski, D. J., Rauch, S. A. M., Kelber, M. S., Issa, F., Lewis, C., & Bisson, J. I. (2021) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2021.05.011 · Cited by 40
Non-invasive brain stimulation as therapy: systematic review and recommendations with a focus on the treatment of Tourette syndrome
Dyke, K., Jackson, G. M., & Jackson, S. R. (2021) · Experimental Brain Research · doi:10.1007/s00221-021-06229-y · Cited by 35
A study of the effects of lorazepam and dextromethorphan on the response to cortical 1 Hz repetitive transcranial magnetic stimulation
Fitzgerald, P. B., Mendieta, J. B., Oxley, T., Daskalakis, J. Z., de Castella, A. R., & Kulkarni, J. (2005) · Neuroreport · doi:10.1097/01.wnr.0000177005.14108.f1 · Cited by 38
Role of the right dorsal premotor cortex in “physiological” mirror EMG activity
Giovannelli, F., Borgheresi, A., Balestrieri, F., et al. (2006) · Experimental Brain Research · doi:10.1007/s00221-006-0581-9 · Cited by 38
“This rTMS protocol has been shown to produce a depression of the excitability of the stimulated cortical area lasting for about 15 min (Chen et al. 1997).”
Influential
Chronic low-frequency rTMS of primary motor cortex diminishes exercise training-induced gains in maximal voluntary force in humans.
Hortobágyi, T., Richardson, S., Lomarev, M., Shamim, E., Meunier, S., Russman, H., Dang, N., & Hallett, M. (2009) · Journal of applied physiology · doi:10.1152/japplphysiol.90701.2008 · Cited by 45
“While several studies reported that low-rate rTMS does not interfere with simple motor skills such as paced fist clenching (43), finger tapping (11, 58), and finger acceleration during pinching (40), a few studies did report impairments in motor output, including reaction time and finger tracking performance (7, 51).”
BackgroundResultInfluentialSelf-citation
A preliminary fMRI study of the effects on cortical activation of the treatment of refractory auditory hallucinations with rTMS
Fitzgerald, P. B., Sritharan, A., Mendieta, J. B., Daskalakis, Z. J., Jackson, G. D., Kulkarni, J., & Egan, G. F. (2007) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2006.12.011 · Cited by 38
“It is known that 1 Hz rTMS can reduce cortical excitability (e.g., Chen et al., 1997).”
Background
Haptic Working Memory for Grasping: the Role of the Parietal Operculum
Maule, F., Barchiesi, G., Brochier, T. G., & Cattaneo, L. (2013) · Cerebral Cortex · doi:10.1093/cercor/bht252 · Cited by 39
Chapter 21 Exploring paradoxical functional facilitation with TMS
Théoret, H., Kobayashi, M., Valero‐Cabré, A., & Pascual‐Leone, Á. (2003) · Supplements to Clinical neurophysiology · doi:10.1016/s1567-424x(09)70224-7 · Cited by 38
Modulation of frequency and duration of repetitive magnetic stimulation affects catecholamine levels and tyrosine hydroxylase activity in human neuroblastoma cells: implication for the antidepressant effect of rTMS.
Shaul, U., Ben-Shachar, D., Karry, R., & Klein, E. (2003) · International Journal of Neuropsychopharmacology · doi:10.1017/s1461145703003493 · Cited by 41
“…magnetic fields such as those produced by rTMS are believed to have inhibitory effects at low frequencies (f1 Hz) whereas higher frequencies facilitate neuronal activity of the primary motor cortex (Chen et al., 1997 ; Kimbrell et al., 1999 ; Pascual-Leone et al., 1994 ; Speer et al., 2000).”
Background
Reduction of cortical myoclonus-related epileptic activity following slow-frequency rTMS. A case study
Rossi, S., Ulivelli, M., Bartalini, S., Galli, R., Passero, S. G., Battistini, N., & Vatti, G. (2004) · Neuroreport · doi:10.1097/00001756-200402090-00016 · Cited by 38
Evaluation of rTMS in patients with poststroke aphasia: a systematic review and focused meta-analysis
Gholami, M., Pourbaghi, N., & Taghvatalab, S. (2022) · Neurological Sciences · doi:10.1007/s10072-022-06092-x · Cited by 37
“Slow rTMS, where 1 magnetic pulse is applied every second (1 Hz), delivered to the motor cortex, can give rise to a lasting decrease in corticospinal excitability [22, 23].”
Method
Left dorsolateral prefrontal transcranial magnetic stimulation (TMS): Sleep factor changes during treatment in patients with pharmacoresistant major depressive disorder
Rosenquist, P. B., Krystal, A. D., Heart, K. L., Demitrack, M. A., & McCall, W. V. (2012) · Psychiatry Research · doi:10.1016/j.psychres.2012.09.011 · Cited by 38
“The accumulated evidence suggests that high frequency TMS stimulation has been observed to exert excitatory effects on neuronal function, while low frequency stimulation conversely is inhibitory to neuronal function (Boroojerdi et al., 2000; Chen et al., 1997; Knecht et al., 2003; Wassermann, 1998).”
Background
High frequency repetitive transcranial magnetic stimulation to the left dorsolateral prefrontal cortex modulates sensorimotor cortex function in the transition to sustained muscle pain
Martino, E. D., Seminowicz, D. A., Schabrun, S. M., Petrini, L., & Graven‐Nielsen, T. (2018) · NeuroImage · doi:10.1016/j.neuroimage.2018.10.076 · Cited by 37
“For instance, low-frequency rTMS (1 Hz) to M1 has been demonstrated to generally induce a lasting decrease in motor cortical excitability (Chen et al., 1997), while high-frequency stimulation has been observed to generally increase excitability of the motor cortex (Pascual-Leone et ., 1994).”
Background
Neuronal tuning: Selective targeting of neuronal populations via manipulation of pulse width and directionality.
Halawa, I., Shirota, Y., Neef, A., Sommer, M., & Paulus, W. (2019) · Brain Stimulation · doi:10.1016/j.brs.2019.04.012 · Cited by 37
Influence of Repetitive Transcranial Magnetic Stimulation on Human Neurochemistry and Functional Connectivity: A Pilot MRI/MRS Study at 7 T
Gröhn, H. I., Gillick, B. T., Tkáč, I., Bednařík, P., Mascali, D., Deelchand, D. K., Michaeli, S., Meekins, G. D., Leffler-McCabe, M. J., MacKinnon, C. D., et al. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.01260 · Cited by 37
Transcranial Magnetic Stimulation: From Neurophysiology to Pharmacology, Molecular Biology and Genomics
Cheeran, B., Koch, G., Stagg, C. J., Baig, F., & Teo, J. (2010) · The Neuroscientist · doi:10.1177/1073858409349901 · Cited by 39
The effects of 1 Hz rTMS over the hand area of M1 on movement kinematics of the ipsilateral hand
Dafotakis, M., Grefkes, C., Wang, L. E., Fink, G. R., & Nowak, D. A. (2008) · Journal of Neural Transmission · doi:10.1007/s00702-008-0064-1 · Cited by 38
“This stimulation protocol has been shown to reduce cortical excitability at least for 10 min (Maeda et al. 2000; Chen et al. 1997).”
Method
Role of the Dorsal Premotor Cortex in Rhythmic Auditory-Motor Entrainment: A Perturbational Approach by rTMS
Giovannelli, F., Innocenti, I., Rossi, S., Borgheresi, A., Ragazzoni, A., Zaccara, G., Viggiano, M. P., & Cincotta, M. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhs386 · Cited by 36
Origin of facilitation in repetitive, 1.5 ms interval, paired pulse transcranial magnetic stimulation (rPPS) of the human motor cortex
Hamada, M., Hanajima, R., Terao, Y., Arai, N., Furubayashi, T., Inomata‐Terada, S., Yugeta, A., Matsumoto, H., Shirota, Y., & Ugawa, Y. (2007) · Clinical Neurophysiology · doi:10.1016/j.clinph.2007.03.009 · Cited by 37
“used biphasic rTMS (Berardelli et al., 1998, 1999; Chen et al., 1997; Di Lazzaro et al., 2002; Huang et al., 2005; Maeda et al., 2000a,b; Pascual-Leone et al., 1994; Romeo et al., 2000).”
BackgroundMethod
Paired-pulse repetitive transcranial magnetic stimulation of the human motor cortex
Sommer, M., Tergau, F., Wischer, S., & Paulus, W. (2001) · Experimental Brain Research · doi:10.1007/s002210100791 · Cited by 40
“This is well in accordance with the literature, where longer trains of rTMS were necessary to produce a lasting inhibition of cortical excitability ( Chen et al. 1997; Siebner et al. 1999b; Muellbacher et al. 2000).”
BackgroundResultInfluential
Motor-evoked potential amplitudes elicited by transcranial magnetic stimulation do not differentiate between patients and normal controls
Grunhaus, L. J., Polak, D., Amiaz, R., & Dannon, P. N. (2003) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145703003705 · Cited by 37
“Stimulation with low-frequency rTMS leads to inhibition of cortical excitability and hence to a decrease in MEP amplitude (Chen et al., 1997), whereas high-frequency rTMS leads to increases in cortical excitability, and hence to increases in MEP amplitude (Jennum et al.”
Background
Modifying the Cortical Processing for Motor Preparation by Repetitive Transcranial Magnetic Stimulation
Terao, Y., Furubayashi, T., Okabe, S., et al. (2007) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2007.19.9.1556 · Cited by 37
“( Jäncke, Steinmetz, Benilow, & Ziemann, 2004), whereas others have failed to produce any significant effect (Kim, Park, Ko, Jang, & Lee, 2004; Muellbacher, Ziemann, Boroojerdi, & Hallett, 2000; Chen et al., 1997).”
BackgroundInfluential
Slow repetitive transcranial magnetic stimulation increases somatosensory high-frequency oscillations in humans
Ogawa, A., Ukai, S., Shinosaki, K., Yamamoto, M., Kawaguchi, S., Ishii, R., & Takeda, M. (2004) · Neuroscience Letters · doi:10.1016/j.neulet.2004.01.038 · Cited by 37
“Slow rTMS delivered to the motor cortex decreased motor evoked potentials (MEPs) [2] and cortical glucose metabolism [10].”
Background
Inhibition of the primary motor cortex can alter one's “sense of effort”: Effects of low-frequency rTMS
Takarada, Y., Mima, T., Abe, M., et al. (2014) · Neuroscience Research · doi:10.1016/j.neures.2014.09.005 · Cited by 36
Test-retest assessment of cortical activation induced by repetitive transcranial magnetic stimulation with brain atlas-guided optical topography
Tian, F., Kozel, F. A., Yennu, A. S., Croarkin, P. E., McClintock, S. M., Mapes, K. S., Husain, M. M., & Liu, H. (2012) · Journal of Biomedical Optics · doi:10.1117/1.jbo.17.11.116020 · Cited by 36
“For example, several previous studies have suggested that stimulation at a higher frequency than 1 Hz tends to increase cortical excitability, whereas stimulation at a lower frequency (≤1 Hz) tends to decrease cortical excitability.(47,48) In this study, cortical deactivations associated with 1-Hz rTMS were identified…”
Background
Noninvasive Brain Stimulation Techniques Can Modulate Cognitive Processing
Veniero, D., Strüber, D., Thut, G., & Herrmann, C. S. (2016) · Organizational Research Methods · doi:10.1177/1094428116658960 · Cited by 39
Interrogating cortical function with transcranial magnetic stimulation: insights from neurodegenerative disease and stroke
Agarwal, S., Koch, G., Hillis, A. E., Huynh, W., Ward, N., Vucic, S., & Kiernan, M. C. (2018) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp-2017-317371 · Cited by 36

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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