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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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BackgroundCombination rapid transcranial magnetic stimulation in treatment refractory depression
McDonald, W. M., Easley, K. A., Byrd, E. H., Holtzheimer, P. E., Tuohy, S., Woodard, J. L., Beyer, K., & Epstein, C. M. (2006) · Neuropsychiatric Disease and Treatment · doi:10.2147/ndt.a816 · Cited by 37
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Transcranial magnetic stimulation as a therapeutic tool in psychiatry
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New advances in the rehabilitation of CNS diseases applying rTMS
Málly, J., & Stone, T. W. (2007) · Expert Review of Neurotherapeutics · doi:10.1586/14737175.7.2.165 · Cited by 35
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Nasios, G., Messinis, L., Dardiotis, E., & Papathanasopoulos, P. (2018) · Behavioural Neurology · doi:10.1155/2018/8584653 · Cited by 37
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BackgroundTranscranial magnetic stimulation therapeutic applications on sleep and insomnia: a review
Oroz, R., Kung, S., Croarkin, P. E., & Cheung, J. (2021) · Sleep Science and Practice · doi:10.1186/s41606-020-00057-9 · Cited by 37
“LF rTMS, when used continuously, is thought to be inhibitory (Valero-cabré et al. 2017; Chen et al. 1997; Romero et al. 2002).”
BackgroundBörnke, C., Schulte, T., Przuntek, H., & Müller, T. (2004) · Journal of neural transmission. Supplementum · doi:10.1007/978-3-7091-0579-5_7 · Cited by 35
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Lazzaro, V. D., Dileone, M., Pilato, F., Profice, P., Cioni, B., Meglio, M., Papacci, F., Sabatelli, M., Musumeci, G., Ranieri, F., et al. (2009) · Brain stimulation · doi:10.1016/j.brs.2009.04.004 · Cited by 36
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Transcranial Magnetic Stimulation for Chronic Pain
Young, N. A., Sharma, M., & Deogaonkar, M. S. (2014) · Neurosurgery Clinics of North America · doi:10.1016/j.nec.2014.07.007 · Cited by 35
“Lowfrequency rTMS ( 1 Hz) produces an inhibitory effect on neural tissue via a long-term depression (LTD)–like mechanism.(42) However, the excitatory and inhibitory effects of high-frequency and lowfrequency rTMS respectively depend on the target and the state of the polarization of the neural tissues being stimulated.”
BackgroundA case of post-traumatic complex auditory hallucinosis treated with rTMS
Cosentino, G., Giglia, G., Palermo, A., Panetta, M., Baido, R. L., Brighina, F., & Fierro, B. (2010) · Neurocase · doi:10.1080/13554790903456191 · Cited by 35
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BackgroundCognitive style, cortical stimulation, and the conversion hypothesis
Kraemer, D. J. M., Hamilton, R. H., Messing, S. B., DeSantis, J. H., & Thompson‐Schill, S. L. (2014) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2014.00015 · Cited by 34
“…2014 | Volume 8 | Article 15 | 3 “fnhum-08-00015” — 2014/1/28 — 20:57 — page 4 — #4 shown to be effective at depressing cortex excitability for periods lasting at least 15 m post-stimulation (Chen et al., 1997), we applied low frequency (1 Hz) offline rTMS for a period of 15 m (900 pulses) at a…”
MethodIs 1 Hz rTMS Always Inhibitory in Healthy Individuals?
Caparelli, E. C., Backus, W. W., Telang, F., Wang, G.-J., Maloney, T., Goldstein, R. Z., & Henn, F. A. (2012) · The Open Neuroimaging Journal · doi:10.2174/1874440001206010069 · Cited by 35
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BackgroundMyoclonus and transcranial magnetic stimulation
Lefaucheur, J. P. (2006) · Neurophysiologie Clinique · doi:10.1016/j.neucli.2006.12.008 · Cited by 35
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“In normal subjects, low-frequency rTMS (1 Hz) decreases (Chen et al. 1997a), whereas high-frequency rTMS (5– 20 Hz) enhances motor cortex excitability (Pascual-Leone A. Fumal and V. Bohotin contributed equally to this study A. Fumal · V. Bohotin · M. Vandenheede · V. De Pasqua · A. M. de Noordhout…”
BackgroundInfluentialLamy, J., Russmann, H., Shamim, E. A., et al. (2010) · Journal of Neurophysiology · doi:10.1152/jn.00761.2009 · Cited by 34
Self-citationAn Ethics Perspective on Transcranial Magnetic Stimulation (TMS) and Human Neuromodulation
Illes, J., Gallo, M., & Kirschen, M. P. (2006) · Behavioural Neurology · doi:10.1155/2006/791072 · Cited by 34
Non-invasive brain stimulation and language processing in the healthy brain
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“High-frequency rTMS and anodal tDCS may increase motor-cortical excitability, while low-frequency rTMS and cathodal tDCS may decrease excitability (Chen et al., 1997; Hallett, 2007; Nitsche & Paulus, 2000, 2001).”
BackgroundThe Transcranial Magnetic Stimulation (TMS) Device and Foundational Techniques
Rotenberg, A., Horvath, J., & Pascual-Leone, Á. (2014) · Neuromethods · doi:10.1007/978-1-4939-0879-0_1 · Cited by 31
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Neurostimulation for depression in epilepsy
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Sundby, K. K., Jana, S., & Aron, A. R. (2020) · Journal of Neurophysiology · doi:10.1152/jn.00459.2020 · Cited by 32
Electrical brain stimulation and continuous behavioral state tracking in ambulatory humans
Mívalt, F., Křemen, V., Sladky, V., Balzekas, I., Nejedlý, P., Gregg, N. M., Lundstrom, B. N., Lepkova, K., Pridalova, T., Brinkmann, B. H., et al. (2022) · Journal of Neural Engineering · doi:10.1088/1741-2552/ac4bfd · Cited by 32
Zuur, A. T., Christensen, M. S., Sinkjær, T., et al. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2009.169367 · Cited by 34
“In the hand, corticospinal excitability is reduced with 1 Hz repetitive transcranial magnetic stimulation (rTMS) applied over the motor cortex (Chen et al. 1997; Muellbacher et al. 2000; Touge et al. 2001; Sommer et al. 2002; for review see Fitzgerald et al. 2006).”
BackgroundResultInfluentialMeeus, O., Blaivie, C., Ost, J., et al. (2009) · Otology & Neurotology · doi:10.1097/mao.0b013e3181b05023 · Cited by 34
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“From motor cortex stimulation, it is known that repetitive TMS (rTMS) with long trains at frequencies of 1 Hz or lower results in a decrease of corticospinal excitability lasting for several minutes after the stimulation has stopped [4].”
BackgroundTranscranial magnetic stimulation for the treatment of depression in neurologic disorders
Fregni, F., & Pascual‐Leone, Á. (2005) · Current Psychiatry Reports · doi:10.1007/s11920-005-0041-4 · Cited by 33
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Imaging causal interactions during sensorimotor processing
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Repetitive TMS temporarily alters brain diffusion
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“interval, needed to avoid any interference between 2 successive pulses.(39) In patients who began prophylactic treatment with LEV, I–O curves were reassessed 2 months after the beginning of the treatment.”
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“The interval between videos was of at least 7 s to avoid cumulative effects of TMS (Chen et al. 1997).”
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Self-citationSykes, M., Matheson, N. A., Brownjohn, P. W., Tang, A. D., Rodger, J., Shemmell, J. B. H., & Reynolds, J. N. J. (2016) · Frontiers in Neural Circuits · doi:10.3389/fncir.2016.00080 · Cited by 33
“In the relatively short history of rTMS, it has broadly been understood that low frequency rTMS (around 1 Hz) is inhibitory (Chen et al., 1997) and higher frequencies appear to be facilitatory (Fitzgerald et al., 2006; Ziemann et al., 2008), although significant variation is reported.”
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Cerebellar rTMS and PAS effectively induce cerebellar plasticity
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“Analysis of cerebello-M1 interaction revealed a main effect of TIME (F(1,37) = 5.”
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“This may be avoided by utilizing specified stimulation frequencies and a combination of parameters, as reported by Chen et al. (1997b) and Wassermann (1998).”
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“Indeed, it is well known that the effects of TMS on outcome variables like cortical excitability (72, 73), functional connectivity (53, 59), and behavior (74, 75) are dependent on the stimulation parameters used (60, 76).”
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“The facilitatory effect on cortical excitatory interneurons was seen by using TMS trains of high frequency and intensity (Pascual-Leone et al. 1994); whereas it has been demonstrated that low-frequency rTMS trains decrease excitability of the motor ( Chen et al. 1997 ) and visual cortices (Boroojerdi et al. 2000) in n…”
InfluentialBenwell, N. M., Mastaglia, F. L., & Thickbroom, G. W. (2006) · Experimental Brain Research · doi:10.1007/s00221-006-0579-3 · Cited by 33
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“RMT was used to scale intensity for 1 Hz rTMS (Chen et al., 1997), AMT scaled intensity for cTBS (Huang et al.”
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“For example, low-frequency rTMS (1- Hz) to motor cortex has been shown to induce a lasting reduction in cortical excitability that persists for 15 min or more (Chen et al., 1997).”
BackgroundTranscranial magnetic stimulation and its applications in children.
Lin, K.-L., & Pascual‐Leone, Á. (2002) · PubMed · Cited by 33
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Genetics and pathogenesis of malignant hyperthermia
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“Conversely, low-frequency stimulation results in a small influx of intracellular calcium due to incomplete magnesium block of the NMDA receptor, activating protein phosphatases and the endocytosis of AMPA receptors to produce LTD. 12 As such, the induction of LTD rather than LTP occurs, with smaller increases in intra…”
BackgroundInfluentialChapter 74 LTP-like plasticity in human motor cortex
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“20 Exclusion criteria were: (1) any neurologic condition other than FHD, (2) medication 20 for dystonia, (3) botulinum toxin injection within the past four months, (4) seizure history, (5) 21 pregnancy, (6) metal in head, or (7) implanted medical devices.”
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“The first rTMS studies demonstrated that 10 Hz rTMS over the motor cortex increased cortical excitability (Pascual-Leone et al., 1994), whereas 1 Hz rTMS decreased cortical excitability (Chen et al., 1997).”
BackgroundNeuromodulation in migraine: state of the art and perspectives
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“, 1 Hz) are thought to have an inhibitory effect [38], whereas high frequencies (‡10 Hz) are considered as excitatory [39].”
BackgroundGulli, G., Tarperi, C., Cevese, A., Acler, M., Bongiovanni, G., & Manganotti, P. (2013) · Experimental Brain Research · doi:10.1007/s00221-013-3431-6 · Cited by 33
“The application of a train of high-frequency or low-frequency magnetic pulses on a brain area allows, respectively, the increase (Berardelli et al. 1998; Siebner et al. 1998) or the decrease (Chen et al. 1997) in cortical excitability even beyond the duration of the train of stimuli.”
BackgroundRepetitive transcranial magnetic stimulation of the supplementary motor area induces echophenomena
Finis, J., Enticott, P. G., Pollok, B., et al. (2012) · Cortex · doi:10.1016/j.cortex.2012.08.019 · Cited by 32
TMS modulation of visual and auditory processing in the posterior parietal cortex
Bolognini, N., Miniussi, C., Savazzi, S., Bricolo, E., & Maravita, A. (2009) · Experimental Brain Research · doi:10.1007/s00221-009-1820-7 · Cited by 32
“Generally, from a physiological point of view, low frequency (·1 Hz) results in inhibition in the stimulated area (Chen et al. 1997).”
BackgroundInfluentialTamashiro, H., Kinoshita, S., Okamoto, T., et al. (2018) · International Journal of Neuroscience · doi:10.1080/00207454.2018.1536053 · Cited by 32
Mylius, V., Reis, J., Knaack, A., Haag, A., Oertel, W. H., Rosenow, F., & Schepelmann, K. (2006) · Neuroscience Letters · doi:10.1016/j.neulet.2006.12.042 · Cited by 32
Plasticity in the Human Nervous System
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Adu, M. K., Shalaby, R., Chue, P., & Agyapong, V. I. O. (2022) · Behavioral Sciences · doi:10.3390/bs12060195 · Cited by 31
“While high-frequency rTMS is deemed to produce a stimulating effect on the cerebral cortex, low-frequency rTMS is believed to have an inhibitory effect [26].”
BackgroundHanlon, C. A., Kearney-Ramos, T., Dowdle, L. T., Hamilton, S., DeVries, W., Mithoefer, O., Austelle, C., Lench, D. H., Correia, B., Canterberry, M., et al. (2017) · Current Behavioral Neuroscience Reports · doi:10.1007/s40473-017-0135-4 · Cited by 31
“TMS is a non-invasive brain stimulation technique which, through electromagnetic induction, can induce long-term potentiation (LTP)-like [3] or longterm depression (LTD)-like [4] changes in cortical activity in a frequency-dependent manner (reviews: [5–8]).”
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Low-frequency electrical stimulation reduces cortical excitability in the human brain
Manzouri, F., Meisel, C., Kunz, L., Dümpelmann, M., Stieglitz, T., & Schulze‐Bonhage, A. (2021) · NeuroImage Clinical · doi:10.1016/j.nicl.2021.102778 · Cited by 31
“This reduction in cortical excitability lasted for at least 15 min after the stimulation period ended (Chen et al., 1997).”
BackgroundMethodCentral nervous system physiology
Rothwell, J. C., Antal, A., Burke, D. J., Carlsen, A. N., Georgiev, D., Jahanshahi, M., Sternad, D., Valls‐Solé, J., & Ziemann, U. (2021) · Clinical Neurophysiology · doi:10.1016/j.clinph.2021.09.013 · Cited by 34
“…of 1000 stimuli at 1 Hz can reduce the excitability of motor cortex for up to 30 min (i.e. single pulse MEPs are smaller than before rTMS) (Chen et al., 1997) whereas higher frequencies such as 5 Hz or more can increase excitability for about the same length of time (Huang et al., 2017;…”
Parameterization of transcranial magnetic stimulation
Rubens, M. T., & Zanto, T. P. (2011) · Journal of Neurophysiology · doi:10.1152/jn.00716.2011 · Cited by 31
“Application of highfrequency rTMS (5 Hz or greater) induces increased excitability (Maeda et al. 2000), whereas low-frequency rTMS (1 Hz or less) produces decreased cortical excitability (Chen et al. 1997).”
BackgroundDumas, R., Richieri, R. M., Guedj, É., Auquier, P., Lançon, C., & Boyer, L. (2012) · Health and Quality of Life Outcomes · doi:10.1186/1477-7525-10-87 · Cited by 30
“The choice of distinct frequency comes from electrophysiological data of the motor cortex, showing that high-frequencies may have an excitatory effect while lowfrequencies tend to suppress cortical excitability [6,7].”
BackgroundGersner, R., Oberman, L. M., Sanchez, M. J., Chiriboga, N., Kaye, H. L., Pascual‐Leone, Á., Libenson, M. H., Roth, Y., Zangen, A., & Rotenberg, A. (2016) · Epilepsy & Behavior Case Reports · doi:10.1016/j.ebcr.2016.03.001 · Cited by 31
“Repetitive TMS (rTMS) stimulates the brain with a series of magnetic pulses and has an inhibitory effect on the neuronal activity when applied at a low (≤1 Hz) frequency [3].”
BackgroundRodríguez‐Herreros, B., Amengual, J. L., Gurtubay-Antolín, A., Richter, L., Jauer, P., Erdmann, C., Schweikard, A., López‐Moliner, J., Rodríguez‐Fornells, A., & Münte, T. F. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2015.06.070 · Cited by 32
“This approach has been empirically proven in many prior TMS studies (Chen et al., 1997; Muellbacher et al., 2000; Siebner et al., 1999).”
Lee, L., Siebner, H. R., & Bestmann, S. (2006) · Behavioural Neurology · doi:10.1155/2006/287276 · Cited by 32
“, paced fist clench [60], finger tapping [13,41,90], generation of freely selected movement sequences [41], maintenance of tonic contraction [84] peak force and acceleration during finger pinch [53].”
BackgroundIllusory contours and specific regions of human extrastriate cortex: evidence from rTMS
Brighina, F., Ricci, R., Piazza, A., et al. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02679.x · Cited by 31
O'Malley, M., Ro, T., & Levin, H. (2006) · Archives of Physical Medicine and Rehabilitation · doi:10.1016/j.apmr.2006.08.332 · Cited by 32
Neurophysiological insights in dystonia and its response to deep brain stimulation treatment
Tisch, S. H., & Limousin, P. D. (2020) · Experimental Brain Research · doi:10.1007/s00221-020-05833-8 · Cited by 31
Koch, G. (2010) · Restorative Neurology and Neuroscience · doi:10.3233/rnn-2010-0556 · Cited by 30
“Low-frequency ( ∼ 1Hz) stimulation reduces neural activity (Chen et al., 1997), whereas stimulation at higher frequency – usually over 5Hz—increases cortical excitability (Pacual-Leone et al., 1994).”
Bates, K. A., & Rodger, J. (2015) · Restorative Neurology and Neuroscience · doi:10.3233/rnn-130359 · Cited by 28
“, 1994) 1 Hz Reduced MEP amplitude in humans (Chen et al., 1997) cTBS and iTBS NMDA receptor antagonists block the effects of TBS on MEP amplitude in humans (Huang et al.”
BackgroundNardone, R., Blasi, P. D., Höller, Y., Christova, M., Tezzon, F., Trinka, E., & Brigo, F. (2013) · Journal of Neural Transmission · doi:10.1007/s00702-013-1100-3 · Cited by 30
Navigated rTMS for the treatment of tinnitus: A pilot study with assessment by fMRI and AEPs
Lefaucheur, J. P., Brugières, P., Guimont, F., Iglesias, S., Franco-Rodrigues, A., Liégeois‐Chauvel, C., & Londero, A. (2012) · Neurophysiologie Clinique · doi:10.1016/j.neucli.2011.12.001 · Cited by 29
Motor-Evoked Potential Facilitation During Progressive Cortical Suppression by Propofol
Scheufler, K.-M., & Zentner, J. (2002) · Anesthesia & Analgesia · doi:10.1097/00000539-200204000-00025 · Cited by 30
Effects of Visual Cortex Activation on the Nociceptive Blink Reflex in Healthy Subjects
Sava, S. L., Pasqua, V. D., Magis, D., & Schoenen, J. E. (2014) · PLoS ONE · doi:10.1371/journal.pone.0100198 · Cited by 30
“To modulate the visual cortex, we used flash light stimulation or repetitive transcranial magnetic stimulation (rTMS) at high or low stimulation frequency [26,27].”
BackgroundMethodLewald, J., Staedtgen, M., Sparing, R., & Meister, I. G. (2010) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2010.11.038 · Cited by 30
Fang, J., Zhou, M., Yang, M., et al. (2013) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd008554.pub3 · Cited by 30
Noninvasive brain stimulation for addiction medicine
Yavari, F., Shahbabaie, A., Leite, J., Carvalho, S., Ekhtiari, H., & Fregni, F. (2015) · Progress in brain research · doi:10.1016/bs.pbr.2015.08.007 · Cited by 31
Finisguerra, A., Amoruso, L., Makris, S., & Urgesi, C. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhw346 · Cited by 30
Novel Therapeutic Approaches to the Treatment of Chronic Abdominal Visceral Pain
Patrizi, F., Freedman, S., Pascual-Leone, Á., & Fregni, F. (2006) · TheScientificWorldJournal · doi:10.1100/tsw.2006.98 · Cited by 27
“Several animal and human studies establish that rTMS can modulate brain cortex activity noninvasively[110,111,112,113,114,115].”
BackgroundEmerging treatments for depression
Holtzheimer, P. E., & Nemeroff, C. B. (2006) · Expert Opinion on Pharmacotherapy · doi:10.1517/14656566.7.17.2323 · Cited by 27
“High-frequency rTMS has been shown to increase cortical excitability when given to the motor cortex, and low-frequency rTMS is associated with decreased motor cortical excitability [136,137].”
BackgroundBattaglia, S., Nazzi, C., Fullana, M. A., di Pellegrino, G., & Borgomaneri, S. (2024) · Behaviour Research and Therapy · doi:10.1016/j.brat.2024.104548 · Cited by 31
Cognitive and neural foundations of discrete sequence skill: A TMS study
Ruitenberg, M. F. L., Verwey, W. B., Schutter, D. J. L. G., & Abrahamse, E. L. (2014) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2014.01.014 · Cited by 29
“, De Kleine and Verwey (2009a, 2009b), Ruitenberg, Abrahamse, and Verwey (2013), Verwey et al. (2009), Verwey and Eikelboom (2003)).”
Enhancing Motor Brain Activity Improves Memory for Action Language: A tDCS Study
Vitale, F., Padrón, I., Avenanti, A., & de Vega, M. (2020) · Cerebral Cortex · doi:10.1093/cercor/bhaa309 · Cited by 29
Desarkar, P., Rajji, T. K., Ameis, S. H., Blumberger, D. M., Lai, M., Lunsky, Y., & Daskalakis, Z. J. (2021) · Clinical Neurophysiology · doi:10.1016/j.clinph.2021.03.046 · Cited by 32
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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