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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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Münchau, A. M., Bloem, B. R., Irlbacher, K., Trimble, M., & Rothwell, J. C. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-02-00554.2002 · Cited by 257
“When applied to the motor cortex, rTMS at the same frequency and duration reduces resting cortical excitability for 15 min (Chen et al., 1997; Maeda et al., 2000).”
BackgroundMethodInfluentialTreating Working Memory Deficits in Schizophrenia: A Review of the Neurobiology
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“Through these mechanisms, low-frequency rTMS will cause a decrease in brain excitability (116); in contrast, high-frequency rTMS causes”
Reduction of human visual cortex excitability using 1-Hz transcranial magnetic stimulation
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Self-citationStimulus-driven modulation of motor-evoked potentials during observation of others' pain
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“1-Hz frequency did not induce any change in excitability (Chen et al., 1997).”
InfluentialTHETA-BURST STIMULATION: A NEW FORM OF TMS TREATMENT FOR DEPRESSION?
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“[16] Low-frequency rTMS (1 Hz) has been shown to reduce cortical excitability when applied for 15 min,[17] whereas high-frequency rTMS (5–20 Hz) has been observed to increase excitability.”
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“Chen and colleagues reported the shorter silent period in writer’s cramp when stimulated with the intensity of 110% above the rMT (Chen et al., 1997).”
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Self-citationSomatic and motor components of action simulation
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“This effect was accounted for by the lower MEP amplitude recorded in the in-win session (w75% of the MEP amplitude in the out-win session, see Figure S1), in keeping with previous reports of reduced motor excitability after 1 Hz rTMS [21, 28, 35].”
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“Relationship to rTMS rTMS with repetition rates equal to or less than 1 s have been reported to yield a long-lasting (up to hours) reduction of cortical excitability (Chen et al. 1997), while higher repetition rates (5–30 Hz) raise cortical excitability (Pascual-Leone et al.”
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“When applying regular trains of repetitive TMS (rTMS), highfrequency rTMS using frequencies of 5 Hz or higher [52] increase excitability in the stimulated M1 [7,53,54], while low-frequency rTMS at a frequency of around 1 Hz [55] decrease corticomotor”
Self-citationLasting cortical activation after repetitive TMS of the motor cortex
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“rTMS at frequencies of 5 Hz and higher can enhance motor cortex excitability,(2,3) whereas lower frequencies rTMS (1 Hz and lower) can transiently depress cortical excitability.(4)”
BackgroundSelf-citationDepression and the hyperactive right-hemisphere
Hecht, D. (2010) · Neuroscience Research · doi:10.1016/j.neures.2010.06.013 · Cited by 230
Top‐Down Modulation and Normal Aging
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TMS Induced Plasticity in Human Cortex
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Repetitive TMS of cerebellum interferes with millisecond time processing
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“A 1 Hz frequency rTMS paradigm, shown to induce an inhibition of the stimulated cortical area lasting beyond the duration of the train (Chen et al. 1997; Oliveri et al. 2005) was used.”
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Rehabilitating the addicted brain with transcranial magnetic stimulation
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Reliability of motor cortex transcranial magnetic stimulation in four muscle representations.
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BackgroundSimulating the Future of Actions in the Human Corticospinal System
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Self-citationTranscranial magnetic stimulation
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“In this regard, stimulation of M1 at a subthreshold intensity and at a frequency of 1 Hz for about 25 minutes (1500 total stimuli) reduced the size of the motor evoked potentials (MEPs) evoked in finger muscles for the next 30 minutes.(124) Stimulation at frequencies higher than 1 Hz tends to increase rather than decr…”
Self-citationChouinard, P. A., van der Werf, Y. D., Leonard, G. T., & Paus, T. (2003) · Journal of Neurophysiology · doi:10.1152/jn.01105.2002 · Cited by 218
“Typically, low-stimulation frequencies of 1 to 2 Hz induce inhibitory effects (e.g., Chen et al. 1997; Gerschlager et al. 2001; Maeda et al. 2000; Muellbacher et al. 2000) and high-stimulation frequencies between 5 and 20 Hz induce facilitory effects (e.g., Maeda et al. 2000; Pascual-Leone et al.…”
BackgroundAltered plasticity of the human motor cortex in Parkinson's disease
Ueki, Y., Mima, T., Kotb, M. A., Sawada, H., Saiki, H., Ikeda, A., Begum, T., Reza, F., Nagamine, T., & Fukuyama, H. (2005) · Annals of Neurology · doi:10.1002/ana.20692 · Cited by 215
“1Hz.(45,46) At least one study showed that the repetitive TMS at 0.”
BackgroundTakeuchi, N., Tada, T., Toshima, M., Chuma, T., Matsuo, Y., & Ikoma, K. (2008) · Journal of Rehabilitation Medicine · doi:10.2340/16501977-0181 · Cited by 218
Enhancing Encoding of a Motor Memory in the Primary Motor Cortex By Cortical Stimulation
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“Initially, we determined the direction of TMS-evoked thumb movements by stimulating the optimal scalp position overlying the contralateral motor cortex (total of 60 stimuli) at 0.1 Hz, a rate that does not affect cortical excitability (Chen et al. 1997).”
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“…of inhibitory circuits in many areas of the motor system from cortico-cortical inhibition in motor cortex (Ridding et al., 1995; Ikoma et al., 1996; Chen et al., 1997b; Filipovic et al., 1997; Siebner et al., 1999b; Abbruzzese et al., 2001) to reciprocal inhibition in the spinal cord (Nakashima et…”
BackgroundLow-frequency rTMS promotes use-dependent motor plasticity in chronic stroke
Avenanti, A., Coccia, M., Làdavas, E., Provinciali, L., & Ceravolo, M. G. (2012) · Neurology · doi:10.1212/wnl.0b013e3182436558 · Cited by 212
Mechanisms and applications of theta-burst rTMS on the human motor cortex
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Gangitano, M., Valero-Cabré, A., Tormos, J., Mottaghy, F., Romero, J. R., & Pascual-Leone, Á. (2002) · Clinical Neurophysiology · doi:10.1016/s1388-2457(02)00109-8 · Cited by 213
“Facilitatory or inhibitory effects of rTMS appear to depend mainly on the frequency of stimulation (Berardelli et al., 1998; Chen et al., 1997; Muellbacher et al., 2000; Pascual-Leone et al., 1994; Wassermann et al., 1998).”
BackgroundNon-invasive brain stimulation in neurorehabilitation: local and distant effects for motor recovery
Liew, S., Santarnecchi, E., Buch, E. R., & Cohen, L. G. (2014) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2014.00378 · Cited by 219
“…non-invasive method available for demonstrating the causal influence of a given cortical region or its interconnected network on specific behaviors (Chen et al., 1997; Cohen et al., 1997; Walsh and Cowey, 2000). rTMS induces frequency- and intensity-specific after-effects, with low-frequency…”
BackgroundInfluentialSelf-citationRole of Corticospinal Suppression during Motor Preparation
Duqué, J., & Ivry, R. B. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhn230 · Cited by 217
Upper alpha ERD and absolute power: their meaning for memory performance.
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“Going beyond the very short-lasting “virtual lesion” effects of high-frequency rTMS, low-frequency rTMS ( 1 Hz) can be used for the induction of longer-lasting reductions (up to 30 min) of focal cortical excitability [Chen et al., 1997; Plewnia et al., 2003b] and activity [Lee et al.”
MethodInfluentialSelf-citationAbsence of Embodied Empathy During Pain Observation in Asperger Syndrome
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Transcranial magnetic stimulation, synaptic plasticity and network oscillations
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“Repetitive transcranial magnetic stimulation (rTMS) is a noninvasive technique for altering cortical excitability (Chen et al., 1997; Boroojerdi et al., 2000; Rotenberg et al., 2008).”
MethodEffects of repetitive transcranial magnetic stimulation on visual evoked potentials in migraine
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“Low-frequency rTMS (<1 Hz) decreases (Chen et al., 1997b; Wassermann et al., 1998; Boroojerdi et al., 2000a), whereas high-frequency rTMS (5±20 Hz) enhances cortical excitability (PascualLeone et al., 1994).”
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Transcranial Magnetic Stimulation as a Complementary Treatment for Aphasia
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“Since TMS-evokedMEP amplitudes have been described to be affected to varying degrees when using an inter-trials b 10 s (Chen et al., 1997; Julkunen et al., 2012; Pascual-Leone et al., 1994), we cannot exclude the possibility that short-term plasticity may have influenced some of our observations.”
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“Low-frequency stimulation, usually in the range of 1 Hz, has been shown to induce inhibition [9,49,50], while so-called ‘‘high-frequency’’ stimulation (around 5 Hz or higher) leads to increased excitability [8,51–54].”
BackgroundDegree of language lateralization determines susceptibility to unilateral brain lesions
Knecht, S., Flöel, A., Dräger, B., Breitenstein, C., Sommer, J. B., Henningsen, H., Ringelstein, E. B., & Pascual‐Leone, Á. (2002) · Nature Neuroscience · doi:10.1038/nn868 · Cited by 196
“TMS was applied at 1 Hz for 600 s at 110% intensity of the motor threshol”
MethodRobertson, E. M., Tormos, J. M., Maeda, F., & Pascual‐Leone, Á. (2001) · Cerebral Cortex · doi:10.1093/cercor/11.7.628 · Cited by 195
Advances and challenges in neurostimulation for headaches
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Cortical plasticity associated with Braille learning
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“While many studies have reported significant reductions in MEP amplitude (Chen et al. 1997a; Muellbacher et al. 2000b; Siebner & Rothwell, 2003; Fitzgerald et al. 2006), some have found no effect (Siebner et al. 1999; Gilio et al. 2003), and others have highlighted large inter-individual…”
MethodResultA Role for the Left Angular Gyrus in Episodic Simulation and Memory
Thakral, P. P., Madore, K. P., & Schacter, D. L. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.1319-17.2017 · Cited by 187
“This TMS protocol constitutes a standard inhibitory protocol (for other uses of this protocol see, Kosslyn, et al., 1999; Slotnick and Thakral, 2011; Thakral and Slotnick, 2011; see also, Chen et al., 1997).”
MethodTranscranial magnetic stimulation and epilepsy
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“Moreover, it is well known that the excitability of cortical networks can be modulated by trains of regularly repeated magnetic stimuli (Pascual-Leone et al., 1994; Chen et al., 1997a; Wassermann and Lisanby, 2001).”
BackgroundDopaminergic influences on formation of a motor memory
Flöel, A., Breitenstein, C., Hummel, F. C., Celnik, P. A., Gingert, C., Sawaki, L. A., Knecht, S., & Cohen, L. G. (2005) · Annals of Neurology · doi:10.1002/ana.20536 · Cited by 187
“1Hz, a rate that does not affect cortical excitability.(29) Subjects occasionally realized that the thumb had moved but could not determine its direction.”
BackgroundSelf-citationShaping the excitability of human motor cortex with premotor rTMS
Rizzo, V., Siebner, H. R., Modugno, N., Pesenti, A., Münchau, A. M., Gerschlager, W., Webb, R. M., & Rothwell, J. C. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.048777 · Cited by 186
“Stimulation for periods of up to 30 min at a frequency of around 1 Hz (referred to as low-frequency rTMS) results in a decrease in excitability that outlasts the stimulation by 30 min or so (Chen et al. 1997; Muellbacher et al. 2000; Fitzgerald et al. 2002; Touge et al. 2001).”
BackgroundThéoret, H., Haque, J., & Pascual‐Leone, Á. (2001) · Neuroscience Letters · doi:10.1016/s0304-3940(01)01860-2 · Cited by 190
Non-invasive brain stimulation in neurological diseases
Schulz, R., Gerloff, C. P., & Hummel, F. C. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.05.016 · Cited by 195
“…TMS (rTMS) can either enhance (5e20 Hz, highfrequency stimulation) or suppress (approximately 0.2e1 Hz, low-frequency stimulation) cortical activity and modulate excitability beyond the duration of the applied trains (Chen et al., 1997; Fregni and Pascual-Leone, 2007; Hummel and Cohen, 2005).”
BackgroundSelf-citationBrain polarization enhances the formation and retention of motor memories.
Galea, J., & Celnik, P. (2009) · Journal of Neurophysiology · doi:10.1152/jn.00184.2009 · Cited by 202
Self-citationGilio, F., Rizzo, V., Siebner, H. R., & Rothwell, J. C. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.044313 · Cited by 183
“…here leads to after effects in the excitability of corticospinal and intracortical circuits that depend on the intensity, frequency and duration of stimulation (Pascual-Leone et al. 1994; Chen et al. 1997; Maeda et al. 2000a,b; Muellbacher et al. 2000; Touge et al. 2001; Tsuji & Rothwell, 2002).”
BackgroundBrain stimulation in the study and treatment of addiction
Feil, J., & Zangen, A. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.11.006 · Cited by 181
Modulation of use‐dependent plasticity by d‐amphetamine
Bütefisch, C. M., Davis, B. C., Sawaki, L., Waldvogel, D., Classen, J., Kopylev, L., & Cohen, L. G. (2002) · Annals of Neurology · doi:10.1002/ana.10056 · Cited by 182
“1Hz, a rate that does not affect motor cortical excitability.(31) Subjects occasionally realized that the thumb had moved but could not determine its direction.”
BackgroundSelf-citationChouinard, P. A., Leonard, G. T., & Paus, T. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.4649-04.2005 · Cited by 180
“Indeed, a number of TMS studies have reported a similar lack of effects on motor execution despite reductions in motor excitability after low-frequency repetitive stimulation over the primary motor cortex (Chen et al., 1997; Muellbacher et al., 2000, 2002).”
BackgroundImproved naming after TMS treatments in a chronic, global aphasia patient – case report
Naeser, M. A., Martin, P. I., Nicholas, M. L., Baker, E. H., Seekins, H., Helm‐Estabrooks, N., Cayer-Meade, C., Kobayashi, M., Théoret, H., Fregni, F., et al. (2005) · Neurocase · doi:10.1080/13554790590944663 · Cited by 180
Cantello, R., Rossi, S., Varrasi, C., Ulivelli, M., Civardi, C., Bartalini, S., Vatti, G., Cincotta, M., Borgheresi, A., Zaccara, G., et al. (2007) · Epilepsia · doi:10.1111/j.1528-1167.2006.00938.x · Cited by 179
“Particularly, low-frequency (<1 Hz) rTMS (slow rTMS) decreases the excitability of the primary motor and other cortical areas (Chen et al., 1997; Muellbacher et al., 2001; Modugno et al., 2003).”
BackgroundGrammatical Distinctions in the Left Frontal Cortex
Shapiro, K. A., Pascual‐Leone, Á., Mottaghy, F. M., Gangitano, M., & Caramazza, A. (2001) · Journal of Cognitive Neuroscience · doi:10.1162/08989290152541386 · Cited by 179
“For the purposes of the present experiment, however, functional resolution is the critical variable (Mottaghy et al., in press; Kosslyn et al., 1999; Siebner et al., 1998; Chen et al., 1997).”
BackgroundInfluentialCentonze, D., Koch, G., Versace, V., Mori, F., Rossi, S., Brusa, L., Grossi, K., Torelli, F., Prosperetti, C., Cervellino, A., et al. (2007) · Neurology · doi:10.1212/01.wnl.0000257818.16952.62 · Cited by 177
Fatigue of elbow flexor muscles in younger and older adults
Bilodeau, M., Erb, M., Nichols, J. M., Joiner, K. L., & Weeks, J. B. (2001) · Muscle & Nerve · doi:10.1002/1097-4598(200101)24:1 · Cited by 109
Noninvasive brain stimulation treatments for addiction and major depression
Dunlop, K., Hanlon, C. A., & Downar, J. (2017) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.12985 · Cited by 171
Plewnia, C., Reimold, M., Najib, A., Reischl, G., Plontke, S. K., & Gerloff, C. P. (2006) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.2006.095612 · Cited by 177
“Indeed, a short-lasting decrease in tinnitus was observed, providing evidence for the critical role of cortical auditory and association areas in tinnitus perception. In contrast with short trains of high-frequency rTMS, low-frequency rTMS is suited to induce a longer-lasting decrease in cortical activity in the stimu…”
BackgroundSelf-citationFeeling by Sight or Seeing by Touch?
Merabet, L. B., Thut, G., Murray, B. J., Andrews‐Hanna, J. R., Hsiao, S. S., & Pascual‐Leone, Á. (2004) · Neuron · doi:10.1016/s0896-6273(04)00147-3 · Cited by 178
Motor Priming in Neurorehabilitation
Stoykov, M. E., & Madhavan, S. (2014) · Neurology Report · doi:10.1097/npt.0000000000000065 · Cited by 179
Hummel, F. C., & Cohen, L. G. (2005) · Current Opinion in Neurology · doi:10.1097/01.wco.0000189876.37475.42 · Cited by 173
Self-citationThe use of repetitive transcranial magnetic stimulation (rTMS) in chronic neuropathic pain
Lefaucheur, J. P. (2006) · Neurophysiologie Clinique · doi:10.1016/j.neucli.2006.08.002 · Cited by 174
Collignon, O., Lassonde, M. C., Leporé, F., Bastien, D., & Veraart, C. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhj162 · Cited by 184
Farzan, F., Vernet, M., Shafi, M. M. D., Rotenberg, A., Daskalakis, Z. J., & Pascual-Leone, A. (2016) · Frontiers in Neural Circuits · doi:10.3389/fncir.2016.00073 · Cited by 173
“Two types of EEG recordings are generally considered: continuous recording without a temporally-defined external or internal event; or event-related recordings over multiple repeated trials, relative to the presentation or processing of an internal or external event.”
BackgroundTMS in cognitive plasticity and the potential for rehabilitation.
Rossi, S., & Rossini, P. (2004) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2004.04.012 · Cited by 192
Martin, P. I., Naeser, M. A., Ho, M. D., Doron, K. W., Kurland, J., Kaplan, J., Wang, Y., Nicholas, M. L., Baker, E. H., Fregni, F., et al. (2009) · Brain and Language · doi:10.1016/j.bandl.2009.07.007 · Cited by 170
“When rTMS is delivered to the same cortical region at 1 Hz, it generally decreases cortical excitability , even beyond the duration of stimulation itself (Chen et al., 1997; Maeda, Keenan, Tormos, Topka, & Pascual-Leone, 2000).”
Disruption of Primary Motor Cortex before Learning Impairs Memory of Movement Dynamics
Richardson, A. G., Overduin, S. A., Valero‐Cabré, A., Padoa‐Schioppa, C., Pascual‐Leone, Á., Bizzi, E., & Press, D. Z. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.1139-06.2006 · Cited by 173
“The use of a 15 min train of subthreshold 1 Hz rTMS was specifically chosen to depress M1 excitability for the duration of the learning epoch (Chen et al., 1997; Gangitano et al., 2002; Romero et al., 2002).”
MethodHoffman, R. E., Hampson, M., Wu, K., Anderson, A. W., Gore, J. C., Buchanan, R. J., Constable, R. T., Hawkins, K. A., Sahay, N., & Krystal, J. H. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhl183 · Cited by 169
“…frequency of 1 Hz for 15--20 min duration can produce sustained reductions in excitability or reactivity of the cortical region directly stimulated (Chen et al. 1997; Boroojerdi et al. 2000), possibly via a mechanism analogous to long-term depression elicited by direct electrical stimulation of…”
BackgroundEncoding a motor memory in the older adult by action observation
Celnik, P. A., Stefan, K., Hummel, F. C., Duqué, J., Claßen, J., & Cohen, L. G. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2005.07.039 · Cited by 169
Self-citationSack, A. T., & Linden, D. E. J. (2003) · Brain Research Reviews · doi:10.1016/s0165-0173(03)00191-7 · Cited by 172
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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