Cited by 1,603Transcranial Magnetic Stimulation StudiesUltrasound and Hyperthermia ApplicationsAdvanced MRI Techniques and Applications

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Transcranial magnetic stimulation and the human brain

Hallett, Mark·2000·Nature

DOI 10.1038/35018000

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Abstract

Transcranial magnetic stimulation (TMS) is rapidly developing as a powerful, non-invasive tool for studying the human brain. A pulsed magnetic field creates current flow in the brain and can temporarily excite or inhibit specific areas. TMS of motor cortex can produce a muscle twitch or block movement; TMS of occipital cortex can produce visual phosphenes or scotomas. TMS can also alter the functioning of the brain beyond the time of stimulation, offering potential for therapy.

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Miniussi, C., Cappa, S., Cohen, L., Flöel, A., Fregni, F., Nitsche, M., Oliveri, M., Pascual-Leone, Á., Paulus, W., Priori, A., et al. (2008) · Brain Stimulation · doi:10.1016/j.brs.2008.07.002 · Cited by 265
Unilateral left prefrontal transcranial magnetic stimulation (TMS) produces intensity-dependent bilateral effects as measured by interleaved BOLD fMRI.
Nahas, Z., Lomarev, M., Roberts, D., Shastri, A., Lorberbaum, J., Teneback, C. C., McConnell, K. A., Vincent, D., Li, X.-B., George, M., et al. (2001) · Biological Psychiatry · doi:10.1016/s0006-3223(01)01199-4 · Cited by 264
“As a research tool, TMS has been applied in studies of brain mapping, motor cortex neurophysiology (Ziemann and Hallett 2000), and to understand language (Epstein et al 1996) and vision (Amassian et al 1989).”
BackgroundMethod
Human brain connectivity during single and paired pulse transcranial magnetic stimulation
Ferreri, F., Pasqualetti, P., Määttä, S., Ponzo, D., Ferrarelli, F., Tononi, G., Mervaala, E., Miniussi, C., & Rossini, P. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2010.07.056 · Cited by 260
“…electromyographic (EMG) responses, termed motor evoked potentials (MEPs), in the target muscles contra-lateral to the side of the stimulation (Hallett, 2000), thus providing a reliable, but indirect, measure of pyramidal tract excitability as well as its cortico-cortical and…”
Treating Working Memory Deficits in Schizophrenia: A Review of the Neurobiology
Lett, T. A., Voineskos, A. N., Kennedy, J. L., Levine, B., & Daskalakis, Z. J. (2014) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.07.026 · Cited by 257
“Transcranial magnetic stimulation is an investigational tool to examine physiological brain processes in relation to cognition and psychiatric illness (91).”
Rethinking the role of sham TMS
Duecker, F., & Sack, A. T. (2015) · Frontiers in Psychology · doi:10.3389/fpsyg.2015.00210 · Cited by 289
“PERSPECTIVE ARTICLE published: 26 February 2015 doi: 10.3389/fpsyg.2015.00210”
BackgroundInfluential
Characteristics of the athletes' brain: Evidence from neurophysiology and neuroimaging
Nakata, H., Yoshie, M., Miura, A., & Kudo, K. (2009) · Brain Research Reviews · doi:10.1016/j.brainresrev.2009.11.006 · Cited by 250
Frequency-Dependent Tuning of the Human Motor System Induced by Transcranial Oscillatory Potentials
Feurra, M., Bianco, G., Santarnecchi, E., Testa, M. D., Rossi, A., & Rossi, S. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.0978-11.2011 · Cited by 262
“…axons (Zarola et al., 1989; Di Lazzaro et al., 2003), and therefore mostly reflects the physiological properties of human motor pathways (Hallett, 2000; Rossini and Rossi, 2007). tACS instead is supposed to entrain regional brain oscillations in a frequency-dependent manner, thereby…”
Background
Effects of brain polarization on reaction times and pinch force in chronic stroke
Hummel, F., Voller, B., Celnik, P., Flöel, A., Giraux, P., Gerloff, C., & Cohen, L. (2006) · BMC Neuroscience · doi:10.1186/1471-2202-7-73 · Cited by 248
“In 4 patients in whom MRI was not available at the time of testing, the anode was centered on the optimal scalp position for activation of the paretic First Dorsal Interosseus (FDI) muscle using an 8-shaped TMS Magstim coil, a procedure that matches the projection of the anatomical hand knob [52].”
Method
Segregating two inhibitory circuits in human motor cortex at the level of GABAA receptor subtypes: A TMS study
Di Lazzaro, V., Pilato, F., Dileone, M., Profice, P., Ranieri, F., Ricci, V., Bria, P., Tonali, P. A., & Ziemann, U. (2007) · Clinical Neurophysiology · doi:10.1016/j.clinph.2007.07.005 · Cited by 240
“Transcranial magnetic stimulation (TMS) techniques provide a non-invasive opportunity of testing integrity and function of the intact human brain (Hallett, 2000).”
Background
Top‐Down Modulation and Normal Aging
Gazzaley, A. H., & D’Esposito, M. (2007) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1379.010 · Cited by 238
Prefontal cortex in long-term memory: an “interference” approach using magnetic stimulation
Rossi, S., Cappa, S., Babiloni, C., Pasqualetti, P., Miniussi, C., Carducci, F., Babiloni, F., & Rossini, P. (2001) · Nature Neuroscience · doi:10.1038/nn0901-948 · Cited by 232
“This can be achieved with transcranial magnetic stimulation, a widely used technique for motor control research and clinical testin”
Method
Neurophysiology of unimanual motor control and mirror movements.
Cincotta, M., & Ziemann, U. (2008) · Clinical Neurophysiology · doi:10.1016/j.clinph.2007.11.047 · Cited by 231
Efficacy of neurostimulation across mental disorders: systematic review and meta-analysis of 208 randomized controlled trials
Hyde, J., Carr, H., Kelley, N. J., Seneviratne, R., Reed, C., Parlatini, V., Garner, M. J., Solmi, M., Rosson, S., Cortese, S., et al. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01524-8 · Cited by 270
“During TMS, a brief electrical current flows through a wire coil, creating a magnet field that passes through the skull and induces a current on the surface of the cortex, depolarizing neurons or their axons [6].”
Enhancing Encoding of a Motor Memory in the Primary Motor Cortex By Cortical Stimulation
Bütefisch, C. M., Khurana, V., Kopylev, L., & Cohen, L. G. (2004) · Journal of Neurophysiology · doi:10.1152/jn.01038.2003 · Cited by 211
“Transcranial magnetic stimulation (TMS) is a technique that allows noninvasive focal stimulation of the human brain (Hallett 2000) and that, in particular settings, can enhance cortical reorganization (Ziemann et al. 1998a) and information processing (Boroojerdi et al. 2001; Flitmann et al. 1998).”
Method
Reliability of motor cortex transcranial magnetic stimulation in four muscle representations.
Malcolm, M., Triggs, W., Light, K., Shechtman, O., Khandekar, G., & Rothi, L. G. G. (2006) · Clinical Neurophysiology · doi:10.1016/j.clinph.2006.02.005 · Cited by 228
“The threshold for these neurons is higher either because they are less excitable or because they are further from the site of stimulation (Hallett, 2000).”
Background
Role of the Contralesional vs. Ipsilesional Hemisphere in Stroke Recovery
Dodd, K., Nair, V. A., & Prabhakaran, V. (2017) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2017.00469 · Cited by 225
“TMS therapy can inhibit or excite targeted brain regions, and applications of this technique may encourage stroke rehabilitation (Hallett, 2000; Fregni et al., 2006) without deteriorating motor performance in the non-affected hand (Fregni et al., 2006; Vines et al., 2008; Hoyer and Celnik, 2011).”
Background
Transcranial magnetic stimulation and Parkinson's disease.
Cantello, R., Tarletti, R., & Civardi, C. (2002) · Brain research. Brain research reviews · doi:10.1016/s0165-0173(01)00158-8 · Cited by 225
Transcranial Magnetic Stimulation for Tinnitus: Influence of Tinnitus Duration on Stimulation Parameter Choice and Maximal Tinnitus Suppression
Ridder, D. D., Verstraeten, E., van der Kelen, K., Mulder, G. D., Sunaert, S., Verlooy, J., van de Heyning, P., & Møller, A. (2005) · Otology and Neurotology · doi:10.1097/01.mao.0000178146.91139.3c · Cited by 222
“A strong magnetic field induces electrical current intracranially that can excite or inhibit neuronal activity depending on the stimulation parameters (15).”
Background
Imaging the Brain Activity Changes Underlying Impaired Visuospatial Judgments: Simultaneous fMRI, TMS, and Behavioral Studies
Sack, A. T., Kohler, A., Bestmann, S., Linden, D. E. J., Dechent, P., Goebel, R., & Baudewig, J. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhm013 · Cited by 220
“The technique of transcranial magnetic stimulation (TMS) is a well-established tool for inducing transient disruptions of neural activity (''virtual lesions'') noninvasively in human volunteers (Hallett 2000; Pascual-Leone et al. 2000; Walsh and Cowey 2000; George et al. 2002; Sack 2006).”
Method
The electric field induced in the brain by magnetic stimulation: a 3-D finite-element analysis of the effect of tissue heterogeneity and anisotropy
Miranda, P. C., Hallett, M., & Basser, P. (2003) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.2003.816079 · Cited by 221
Self-citation
Non-invasive Brain Stimulation: A Paradigm Shift in Understanding Brain Oscillations
Vosskuhl, J., Strüber, D., & Herrmann, C. S. (2018) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2018.00211 · Cited by 249
“This fast change in magnetic field strength induces a current in cortical neurons which is oriented in parallel to the magnetic coil (Hallett, 2000, 2007).”
Background
Investigating human motor control by transcranial magnetic stimulation
Petersen, N. T., Pyndt, H., & Nielsen, J. (2003) · Experimental Brain Research · doi:10.1007/s00221-003-1537-y · Cited by 220
“The popularity of the technique is also reflected in a large number of recent reviews (Weber and Eisen 2002; Walsh and Cowey 2000; Cantello et al. 2002; Lisanby et al. 2000; Hallett 2000; Bailey et al. 2001; Siebner and Rothwell 2003).”
Method
Impairment of bidirectional synaptic plasticity in the striatum of a mouse model of DYT1 dystonia: role of endogenous acetylcholine
Martella, G., Tassone, A., Sciamanna, G., Platania, P., Cuomo, D., Viscomi, M. T., Bonsi, P., Cacci, E., Biagioni, S., Usiello, A., et al. (2009) · Brain · doi:10.1093/brain/awp194 · Cited by 222
“Similar results were observed in patients with focal dystonia by using transcranial magnetic stimulation, a non-invasive tool to assess excitability of the motor system (Hallett, 2000).”
Transcranial magnetic stimulation and epilepsy
Tassinari, C. A., Cincotta, M., Zaccara, G., & Michelucci, R. (2003) · Clinical Neurophysiology · doi:10.1016/s1388-2457(03)00004-x · Cited by 193
“However, it became more and more evident that TMS also provided a noninvasive evaluation of distinct excitatory and inhibitory functions of the human cerebral cortex (for review, see Hallett, 1996, 2000; Rossini and Rossi, 1998; Chen, 2000).”
Background
Image-Guided Focused Ultrasound-Mediated Regional Brain Stimulation in Sheep
Lee, W., Lee, S. D., Park, M. Y., Foley, L., Purcell-Estabrook, E., Kim, H., Fischer, K., Maeng, L.-S., & Yoo, S. (2015) · Ultrasound in Medicine & Biology · doi:10.1016/j.ultrasmedbio.2015.10.001 · Cited by 223
Repetitive Transcranial Magnetic Stimulation Enhances BDNF-TrkB Signaling in Both Brain and Lymphocyte
Wang, H.-Y., Crupi, D., Liu, J., Stucky, A., Cruciata, G., Rocco, A. D., Friedman, E., Quartarone, A., & Ghilardi, M. F. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.2125-11.2011 · Cited by 229
“As it can be influenced by drugs affecting sodium and calcium channels, RMT value must indicate membrane excitability (Hallett, 2000) and, thus, could probably reflect mechanisms other than synaptic changes.”
Background
Modulation of input-output curves by low and high frequency repetitive transcranial magnetic stimulation of the motor cortex.
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
“…modulate cortical excitability by using repetitive transcranial magnetic stimulation (rTMS) has been used in a growing number of neurophysiological (Hallett, 2000; Pascual-Leone et al., 1998), cognitive (Pascual-Leone et al., 1999, 2000; Walsh and Cowey, 2000) and clinical applications (George et…”
Method
Motor cortex excitability in Alzheimer's disease: A transcranial magnetic stimulation study
Ferreri, F., Pauri, F., Pasqualetti, P., Fini, R., Forno, G. D., & Rossini, P. M. (2002) · Annals of Neurology · doi:10.1002/ana.10416 · Cited by 223
Linking Physics with Physiology in TMS: A Sphere Field Model to Determine the Cortical Stimulation Site in TMS
Thielscher, A., & Kammer, T. (2002) · NeuroImage · doi:10.1006/nimg.2002.1282 · Cited by 211
“Transcranial magnetic stimulation (TMS) is a widely used research tool in the neurosciences (Hallett, 2000; Walsh and Cowey, 2000).”
Method
Transcranial magnetic stimulation as a therapeutic tool in psychiatry: what do we know about the neurobiological mechanisms?
Keck, M., Welt, T., Müller, M., Post, A., Sillaber, I., & Holsboer, F. (2001) · European psychiatry · doi:10.1016/s0924-9338(02)80193-6 · Cited by 211
A Direct Brain-to-Brain Interface in Humans
Rao, R. P. N., Stocco, A., Bryan, M., Sarma, D., Youngquist, T. M., Wu, J., & Prat, C. S. (2014) · PLoS ONE · doi:10.1371/journal.pone.0111332 · Cited by 210
“A variety of stimulation techniques also exist that permit users to encode digital information into neural activity using implanted electrodes [15,16], transcranial magnetic stimulation, (TMS, [17]) and focused ultrasound (FUS, [18]).”
Background
Evoked potentials and transcranial magnetic stimulation in migraine: published data and viewpoint on their pathophysiologic significance
Schoenen, J. E., Ambrosini, A., Sándor, P. S., & de Noordhout, A. M. (2003) · Clinical Neurophysiology · doi:10.1016/s1388-2457(03)00024-5 · Cited by 208
Closed-Loop Neuroscience and Non-Invasive Brain Stimulation: A Tale of Two Loops
Zrenner, C., Belardinelli, P., Müller‐Dahlhaus, F., & Ziemann, U. (2016) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2016.00092 · Cited by 214
“…Health, USA Reviewed by: Gregor Thut, University of Glasgow, UK Giuseppe Sciamanna, University of Rome Torvergata, Italy *Correspondence: Christoph Zrenner christoph.zrenner@uni-tuebingen.de Received: 22 July 2015 Accepted: 23 March 2016 Published: 07 April 2016 Citation: Zrenner C, Belardinelli…”
BackgroundMethod
Parietal cortex and spatial cognition
Sack, A. T. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.03.012 · Cited by 215
Studying spontaneous EEG activity with fMRI
Salek‐Haddadi, A., Friston, K. J., Lemieux, L., & Fish, D. R. (2003) · Brain Research Reviews · doi:10.1016/s0165-0173(03)00193-0 · Cited by 205
Examination of neural systems sub-serving facebook addiction
Turel, O., He, Q., Xue, G., Xiao, L., & Bechara, A. (2014) · Psychological Reports · doi:10.2466/18.pr0.115c31z8 · Cited by 206
“Lastly, this study points to the possibility that some interventions, such as CBT or trans-cranial magnetic stimulation (Hallett, 2000), may be efficacious in treating Facebook “addiction.””
Background
Activity-dependent neural plasticity from bench to bedside
Ganguly, K., & Poo, M.-M. (2013) · Neuron · doi:10.1016/j.neuron.2013.10.028 · Cited by 202
Brain 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
Effects of repetitive transcranial magnetic stimulation on visual evoked potentials in migraine
Bohotin, V., Fumal, A., Vandenheede, M., Gérard, P., Bohotin, C. R., de Noordhout, A. M., & Schoenen, J. E. (2002) · Brain · doi:10.1093/brain/awf081 · Cited by 201
“In the last decade, numerous studies on the effects of rTMS on cortical excitability have been performed (Berardelli et al., 1999; Klein et al., 1999b; Hallett, 2000; Maeda et al., 2000).”
Background
Increased variability of paced finger tapping accuracy following repetitive magnetic stimulation of the cerebellum in humans
Théoret, H., Haque, J., & Pascual‐Leone, Á. (2001) · Neuroscience Letters · doi:10.1016/s0304-3940(01)01860-2 · Cited by 190
Cortical and spinal abnormalities in psychogenic dystonia
Espay, A., Morgante, F., Purzner, J., Gunraj, C., Lang, A. E., & Chen, R. (2006) · Annals of Neurology · doi:10.1002/ana.20837 · Cited by 197
“Transcranial magnetic stimulation (TMS) is a noninvasive way to stimulate the brain in human subjects.(20,21) With weak (subthreshold) conditioning pulse followed by a suprathreshold test pulse at short interstimulus intervals (ISIs; approximately 2 milliseconds) there occurs reduction of the size of the motor-evoked…”
Background
Transitions between dynamical states of differing stability in the human brain
Meyer‐Lindenberg, A., Ziemann, U., Hajak, G., Cohen, L. G., & Berman, K. F. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.162114799 · Cited by 186
Upper alpha ERD and absolute power: their meaning for memory performance.
Klimesch, W., Doppelmayr, M., & Hanslmayr, S. (2006) · Progress in Brain Research · doi:10.1016/s0079-6123(06)59010-7 · Cited by 196
Transcranial magnetic stimulation in the treatment of substance addiction
Gorelick, D. A., Zangen, A., & George, M. S. (2014) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.12479 · Cited by 195
Influence of the pressure field distribution in transcranial ultrasonic neurostimulation.
Younan, Y., Deffieux, T., Larrat, B., Fink, M., Tanter, M., & Aubry, J. (2013) · Medical Physics (Lancaster) · doi:10.1118/1.4812423 · Cited by 193
Human Motor Plasticity Induced by Mirror Visual Feedback
Nojima, I., Mima, T., Koganemaru, S., Thabit, M., Fukuyama, H., & Kawamata, T. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.5364-11.2012 · Cited by 193
“Although the aMT, reflecting the neuronal membrane excitability levels in the M1 (Mavroudakis et al., 1994; Ziemann et al., 1996a; Hallett, 2000), was significantly decreased after mirror therapy, the change in the rMT failed to reach statistical significance.”
Background
Brain Plasticity in the Adult: Modulation of Function in Amblyopia with rTMS
Thompson, B. S., Mansouri, B., Koski, L. M., & Hess, R. F. (2008) · Current Biology · doi:10.1016/j.cub.2008.06.052 · Cited by 182
“This method of measurement was used because it provided the best tradeoff between accuracy and speed of measurement as necessitated by the transient nature of rTMS effects [21].”
TMS 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
Functional brain reorganization after spinal cord injury: Systematic review of animal and human studies
Nardone, R., Höller, Y., Brigo, F., Seidl, M., Christova, M., Bergmann, J., Golaszewski, S. M., & Trinka, E. (2013) · Brain Research · doi:10.1016/j.brainres.2012.12.034 · Cited by 182
Transcranial magnetic stimulation techniques in clinical investigation
Currá, A., Modugno, N., Inghilleri, M., Manfredi, M., Hallett, M., & Berardelli, A. (2002) · Neurology · doi:10.1212/01.wnl.0000038744.30298.d4 · Cited by 182
Self-citation
Brain 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
Neural effects of transcranial magnetic stimulation at the single-cell level
Romero, M. C., Davare, M., Armendáriz, M., & Janssen, P. (2019) · Nature Communications · doi:10.1038/s41467-019-10638-7 · Cited by 179
Stanford Accelerated Intelligent Neuromodulation Therapy for Treatment-Resistant Depression (SAINT-TRD)Preprint
Cole, E., Stimpson, K., Bentzley, B. S., Gulser, M., Cherian, K., Tischler, C., Nejad, R., Pankow, H., Choi, E., Aaron, H., et al. (2019) · bioRxiv · doi:10.1101/581280 · Cited by 179

Authors: Hallett, M.
Affiliations: National Institutes of Health (US)
Corresponding author: Hallett, Mark
ORCID: Hallett, Mark
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2000-07
Volume: 406
Issue: 6792
Pages: 147-150
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/35018000
OpenAlex: W2129291496
Cited by: 1,603
References: 42
Citations by year: 2026: 44 · 2025: 61 · 2024: 66 · 2023: 70 · 2022: 84 · 2021: 87 · 2020: 103 · 2019: 73 · 2018: 81 · 2017: 46 · 2016: 80 · 2015: 85 · 2014: 75 · 2013: 72 · 2012: 71
FWCI: 4.67
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Topics: Life Sciences › Neuroscience › Neurology › Transcranial Magnetic Stimulation Studies
Physical Sciences › Engineering › Biomedical Engineering › Ultrasound and Hyperthermia Applications
Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced MRI Techniques and Applications
Keywords: transcranial magnetic stimulation, non-invasive brain stimulation, motor cortex, occipital cortex, muscle twitch, scotoma, brain therapy
MeSH terms: Brain, Brain Mapping, Cerebral Cortex, Forecasting, Humans, Nervous System Diseases, Neuronal Plasticity, Evoked Potentials, Motor, Transcranial Magnetic Stimulation

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Transcranial magnetic stimulation and the human brain

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