Transcranial magnetic stimulation and synaptic plasticity: Experimental framework and human models
Abstract
Interest in the therapeutic potential of non-invasive human brain stimulation has been boosted by an improved understanding of the mechanisms of synaptic plasticity and the stimulus protocols that can induce plasticity in experimental preparations. A range of transcranial magnetic stimulation (TMS) protocols are available that have the potential to mimic these experimental protocols in the human. Repetitive TMS emulates aspects of activity-dependent plasticity, and theta-burst refinements may be able to take into account excitatory and inhibitory networks, paired associative stimulation can extend network considerations to incorporate sensorimotor integration, inhibitory networks may be targeted with short-interval paired stimulation and finally even the precision of spike-timing dependent plasticity may be accessible through I-(indirect)wave dynamics. This review will provide a synthesis of current concepts of activity- and time-dependent plasticity and their homeostatic regulation based on experimental studies, and relate these concepts to the promising range of TMS interventions that are available to target human brain plasticity.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Modulation of GABA receptors and glutamate receptors has been proposed as a possible mechanism explaining excitability changes following TBS.
“Modulation of GABA receptors (Thickbroom, 2007) and glutamate receptors (Glu-r) (Huang et al., 2007) has also been proposed as a possible mechanism explaining excitability changes following TBS.”
From Theta burst stimulation to characterize changes in brain plasticity following mild traumatic brain injury: A proof-of-principle study (2015) · cites this paper as Thickbroom, 2007
Cites
Hebb, D. O. (2005) · doi:10.4324/9781410612403 · Cited by 9,825 · see citing works
Bliss, T. V. P., & Gardner-Medwin, A. R. (1973) · The Journal of Physiology · doi:10.1113/jphysiol.1973.sp010274 · Cited by 7,460 · see citing works
indicated, N. A. (1950) · Journal of Consulting Psychology · doi:10.1037/h0049612 · Cited by 6,984 · see citing works
Bi, G.-Q., & Poo, M.-M. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-24-10464.1998 · Cited by 4,744 · see citing works
Theta Burst Stimulation of the Human Motor Cortex
Huang, Y.-Z., Edwards, M. J., Rounis, E., Bhatia, K. P., & Rothwell, J. C. (2005) · Neuron · doi:10.1016/j.neuron.2004.12.033 · Cited by 4,158 · see citing works
Malenka, R. C., & Bear, M. F. (2004) · Neuron · doi:10.1016/j.neuron.2004.09.012 · Cited by 3,968 · see citing works
The molecular biology of memory storage: a dialogue between genes and synapses
Kandel, E. R. (2001) · Science · doi:10.1126/science.1067020 · Cited by 3,917 · see citing works
Corticocortical inhibition in human motor cortex.
Kujirai, T., Caramia, M. D., Rothwell, J. C., Day, B. L., Thompson, P. D., Ferbert, A., Wroe, S. J., Asselman, P., & MARSDEN, C. D. (1993) · The Journal of Physiology · doi:10.1113/jphysiol.1993.sp019912 · Cited by 3,132 · see citing works
Bienenstock, E., Cooper, L., & Munro, P. (1982) · The Journal of Neuroscience · doi:10.1523/jneurosci.02-01-00032.1982 · Cited by 2,896 · see citing works
Long-Term Potentiation--A Decade of Progress?
Malenka, R. C., & Nicoll, A. R. A. (1999) · Science · doi:10.1126/science.285.5435.1870 · Cited by 2,729 · see citing works
Structural basis of long-term potentiation in single dendritic spines
Matsuzaki, M., Honkura, N., Ellis-Davies, G. C. R., & Kasai, H. (2004) · Nature · doi:10.1038/nature02617 · Cited by 2,500 · see citing works
Homeostatic plasticity in the developing nervous system
Turrigiano, G. G., & Nelson, S. B. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1327 · Cited by 2,485 · see citing works
Wassermann, E. M. (1998) · Electroencephalography and Clinical Neurophysiology/Evoked Potentials Section · doi:10.1016/s0168-5597(97)00096-8 · Cited by 2,298 · see citing works
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 · Cited by 2,128 · cited 2× · see citing works
“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).”
BackgroundMetaplasticity: the plasticity of synaptic plasticity
Abraham, W. C., & Bear, M. F. (1996) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)80018-x · Cited by 1,783 · see citing works
Induction of plasticity in the human motor cortex by paired associative stimulation
Stefan, K. (2000) · Brain · doi:10.1093/brain/123.3.572 · Cited by 1,484 · see citing works
Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex
Pascual‐Leone, Á., Valls‐Solé, J., Wassermann, E. M., & Hallett, M. (1994) · Brain · doi:10.1093/brain/117.4.847 · Cited by 1,457 · see citing works
A Synaptically Controlled, Associative Signal for Hebbian Plasticity in Hippocampal Neurons
Magee, J. C., & Johnston, D. (1997) · Science · doi:10.1126/science.275.5297.209 · Cited by 1,303 · see citing works
Variability, compensation and homeostasis in neuron and network function
Marder, E., & Goaillard, J.-M. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn1949 · Cited by 1,212 · see citing works
Plasticity in the human central nervous system
Cooke, S. F. (2006) · Brain · doi:10.1093/brain/awl082 · Cited by 1,195 · see citing works
Rate, Timing, and Cooperativity Jointly Determine Cortical Synaptic Plasticity
Sjöström, P. J., Turrigiano, G. G., & Nelson, S. B. (2001) · Neuron · doi:10.1016/s0896-6273(01)00542-6 · Cited by 1,174 · see citing works
Spike Timing-Dependent Plasticity of Neural Circuits
Dan, Y., & Poo, M. (2004) · Neuron · doi:10.1016/j.neuron.2004.09.007 · Cited by 1,029 · see citing works
A comprehensive review of the effects of rTMS on motor cortical excitability and inhibition
Fitzgerald, P. B., FOUNTAIN, S., & Daskalakis, Z. J. (2006) · Clinical Neurophysiology · doi:10.1016/j.clinph.2006.06.712 · Cited by 1,026 · see citing works
Day, B. L., Dressler, D. W., de Noordhout, A. M., MARSDEN, C. D., Nakashima, K., Rothwell, J. C., & Thompson, P. D. (1989) · The Journal of Physiology · doi:10.1113/jphysiol.1989.sp017626 · Cited by 932 · see citing works
Temporal structure in spatially organized neuronal ensembles: a role for interneuronal networks
Buzsáki, G., & Chrobak, J. J. (1995) · Current Opinion in Neurobiology · doi:10.1016/0959-4388(95)80012-3 · Cited by 878 · see citing works
Homeostatic plasticity in neuronal networks: the more things change, the more they stay the same
Turrigiano, G. G. (1999) · Trends in Neurosciences · doi:10.1016/s0166-2236(98)01341-1 · Cited by 823 · see citing works
Plasticity in the intrinsic excitability of cortical pyramidal neurons
Desai, N. S., Rutherford, L. C., & Turrigiano, G. G. (1999) · Nature Neuroscience · doi:10.1038/9165 · Cited by 806 · see citing works
Silent period evoked by transcranial stimulation of the human cortex and cervicomedullary junction.
Inghilleri, M., Berardelli, A., Cruccu, G., & Manfredi, M. (1993) · The Journal of Physiology · doi:10.1113/jphysiol.1993.sp019732 · Cited by 785 · see citing works
ELECTRICAL SYNAPSES IN THE MAMMALIAN BRAIN
Connors, B. W., & Long, M. A. (2004) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.26.041002.131128 · Cited by 784 · see citing works
Diversity and Dynamics of Dendritic Signaling
Häusser, M., Spruston, N., & Stuart, G. J. (2000) · Science · doi:10.1126/science.290.5492.739 · Cited by 783 · see citing works
Action potential initiation and backpropagation in neurons of the mammalian CNS
Stuart, G., Spruston, N., Sakmann, B., & Häusser, M. (1997) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)10075-8 · Cited by 768 · see citing works
Modulation of corticospinal excitability by repetitive transcranial magnetic stimulation
Maeda, F., Keenan, J. P., Tormos, J. M., Topka, H. R., & Pascual‐Leone, Á. (2000) · Clinical Neurophysiology · doi:10.1016/s1388-2457(99)00323-5 · Cited by 734 · see citing works
Hebb and homeostasis in neuronal plasticity
Turrigiano, G. G., & Nelson, S. B. (2000) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(00)00091-x · Cited by 687 · see citing works
Maeda, F., Keenan, J. P., Tormos, J. M., Topka, H., & Pascual-Leone, A. (2000) · Experimental Brain Research · doi:10.1007/s002210000432 · Cited by 651 · see citing works
Stefan, K., Kunesch, E., Benecke, R., Cohen, L. G., & Claßen, J. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2002.023317 · Cited by 643 · see citing works
A temporally asymmetric Hebbian rule governing plasticity in the human motor cortex.
Wolters, A., Sandbrink, F., Schlottmann, A., Kunesch, E., Stefan, K., Cohen, L., Benecke, R., & Classen, J. (2003) · Journal of Neurophysiology · doi:10.1152/jn.00900.2002 · Cited by 633 · see citing works
The after-effect of human theta burst stimulation is NMDA receptor dependent
Huang, Y.-Z., Chen, R.-S., Rothwell, J. C., & Wen, H.-Y. (2007) · Clinical Neurophysiology · doi:10.1016/j.clinph.2007.01.021 · Cited by 618 · see citing works
GABAB autoreceptors regulate the induction of LTP
Davies, C. H., Starkey, S. J., Pozza, M. F., & Collingridge, G. L. (1991) · Nature · doi:10.1038/349609a0 · Cited by 615 · see citing works
Long-Term Depression in Hippocampus
Bear, M. F., & Abraham, W. C. (1996) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.19.030196.002253 · Cited by 601 · see citing works
Induction of synaptic potentiation in hippocampus by patterned stimulation involves two events
Larson, J., & Lynch, G. (1986) · Science · doi:10.1126/science.3704635 · Cited by 597 · cited 2× · see citing works
“One early experimental approach that took into account network function was to deliver bursts of high-frequency LTP-inducing stimuli at naturally occurring network rhythms with a view to harnessing normal patterns of activity, such as the theta (5 Hz) rhythm of the hippocampus (Larson and Lynch 1986).”
BackgroundThe role of GABAB receptors in intracortical inhibition in the human motor cortex
McDonnell, M. N., Orekhov, Y., & Ziemann, U. (2006) · Experimental Brain Research · doi:10.1007/s00221-006-0365-2 · Cited by 558 · see citing works
Hebbian synapses in hippocampus.
Kelso, S. R., Ganong, A. H., & Brown, T. H. (1986) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.83.14.5326 · Cited by 555 · see citing works
Ziemann, U., Tergau, F., Wassermann, E. M., Wischer, S., Hildebrandt, J., & Paulus, W. (1998) · The Journal of Physiology · doi:10.1111/j.1469-7793.1998.181bi.x · Cited by 464 · see citing works
Woodin, M. A., Ganguly, K., & Poo, M. (2003) · Neuron · doi:10.1016/s0896-6273(03)00507-5 · Cited by 411 · see citing works
Dendritic coincidence detection of EPSPs and action potentials
Stuart, G. J., & Häusser, M. (2001) · Nature Neuroscience · doi:10.1038/82910 · Cited by 354 · see citing works
Barrionuevo, G., Schottler, F., & Lynch, G. (1980) · Life Sciences · doi:10.1016/0024-3205(80)90509-3 · Cited by 321 · see citing works
Short latency facilitation between pairs of threshold magnetic stimuli applied to human motor cortex
Tokimura, H., Ridding, M. C., Tokimura, Y., Amassian, V. E., & Rothwell, J. C. (1996) · Electroencephalography and Clinical Neurophysiology/Electromyography and Motor Control · doi:10.1016/0924-980x(96)95664-7 · Cited by 287 · see citing works
Plasticity of perisynaptic astroglia during synaptogenesis in the mature rat hippocampus
Witcher, M. R., Kirov, S. A., & Harris, K. M. (2006) · Glia · doi:10.1002/glia.20415 · Cited by 281 · see citing works
Task-specific hand dystonia: can too much plasticity be bad for you?
Quartarone, A., Siebner, H. R., & Rothwell, J. C. (2006) · Trends in Neurosciences · doi:10.1016/j.tins.2006.02.007 · Cited by 275 · see citing works
Plasticity in single neuron and circuit computations
Alain Destexhe, A., & Marder, E. E. (2004) · Nature · doi:10.1038/nature03011 · Cited by 271 · see citing works
Induction of sharp wave–ripple complexes in vitro and reorganization of hippocampal networks
Behrens, C. J., van den Boom, L. P., de Hoz, L., Friedman, A., & Heinemann, U. (2005) · Nature Neuroscience · doi:10.1038/nn1571 · Cited by 262 · see citing works
Bidirectional synaptic plasticity: from theory to reality
Bear, M. F. (2003) · Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rstb.2002.1255 · Cited by 260 · see citing works
The muscle silent period following transcranial magnetic cortical stimulation
Wilson, S. A., Lockwood, R. J., Thickbroom, G. W., & Mastaglia, F. L. (1993) · Journal of the Neurological Sciences · doi:10.1016/0022-510x(93)90301-e · Cited by 249 · see citing works
Self-citationSynaptic integration in dendritic trees
Gulledge, A. T., Kampa, B. M., & Stuart, G. J. (2005) · Journal of Neurobiology · doi:10.1002/neu.20144 · Cited by 248 · see citing works
Active dendrites, potassium channels and synaptic plasticity
Johnston, D., Christie, B. R., Frick, A., Gray, R. G. F., Hoffman, D. A., Schexnayder, L. K., Watanabe, S., & Yuan, L. (2003) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2002.1248 · Cited by 246 · see citing works
Long-term potentiation: outstanding questions and attempted synthesis
Lisman, J. (2003) · Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rstb.2002.1242 · Cited by 240 · see citing works
The discovery of long-term potentiation
Lømo, T. (2003) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2002.1226 · Cited by 237 · see citing works
Spike timing, calcium signals and synaptic plasticity
Sjöström, P. (2002) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(02)00325-2 · Cited by 231 · see citing works
The long-term potential of LTP
Malenka, R. C. (2003) · Nature reviews. Neuroscience · doi:10.1038/nrn1258 · Cited by 229 · see citing works
TMS Induced Plasticity in Human Cortex
Ziemann, U. (2004) · Reviews in the Neurosciences · doi:10.1515/revneuro.2004.15.4.253 · Cited by 218 · see citing works
Hanajima, R., Ugawa, Y., Terao, Y., Enomoto, H., Shiio, Y., Mochizuki, H., Furubayashi, T., Uesugi, H., Iwata, N. K., & Kanazawa, I. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2001.013094 · Cited by 215 · see citing works
Characteristics of hippocampal primed burst potentiation in vitro and in the awake rat
Diamond, D. M., Dunwiddie, T., & Rose, G. (1988) · Journal of Neuroscience · doi:10.1523/jneurosci.08-11-04079.1988 · Cited by 214 · see citing works
Linden, D. J. (1999) · Neuron · doi:10.1016/s0896-6273(00)80726-6 · Cited by 194 · see citing works
Linking 600-Hz “Spikelike” EEG/MEG Wavelets (“ς-Bursts”) to Cellular Substrates
Curio, G. (2000) · Journal of Clinical Neurophysiology · doi:10.1097/00004691-200007000-00004 · Cited by 180 · see citing works
Structural changes at dendritic spine synapses during long-term potentiation
Harris, K. M., Fiala, J. C., & Ostroff, L. (2003) · Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rstb.2002.1254 · Cited by 180 · see citing works
Thickbroom, G. W., Byrnes, M. L., Edwards, D. J., & Mastaglia, F. L. (2005) · Clinical Neurophysiology · doi:10.1016/j.clinph.2005.09.010 · Cited by 159 · see citing works
Self-citationDiscrete synaptic states define a major mechanism of synapse plasticity
Montgomery, J. M., & Madison, D. V. (2004) · Trends in Neurosciences · doi:10.1016/j.tins.2004.10.006 · Cited by 158 · see citing works
Modeling the Effects of Transcranial Magnetic Stimulation on Cortical Circuits
Esser, S. K., Hill, S., & Tononi, G. (2005) · Journal of Neurophysiology · doi:10.1152/jn.01230.2004 · Cited by 157 · see citing works
EEG oscillations at 600 Hz are macroscopic markers for cortical spike bursts
Baker, S. N., Curio, G., & Lemon, R. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.045674 · Cited by 148 · see citing works
Ridding, M. C., & Taylor, J. L. (2001) · The Journal of Physiology · doi:10.1111/j.1469-7793.2001.00623.x · Cited by 141 · see citing works
Sensing and expressing homeostatic synaptic plasticity
Rich, M. M., & Wenner, P. (2007) · Trends in Neurosciences · doi:10.1016/j.tins.2007.01.004 · Cited by 118 · see citing works
Bliss, T., Collingridge, G. L., & Morris, R. (2003) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2003.1282 · Cited by 105 · see citing works
Timing in synaptic plasticity: from detection to integration
Bi, G., & Rubin, J. E. (2005) · Trends in Neurosciences · doi:10.1016/j.tins.2005.02.002 · Cited by 74 · see citing works
Heide, G., Witte, O. W., & Ziemann, U. (2005) · Experimental Brain Research · doi:10.1007/s00221-005-0262-0 · Cited by 71 · see citing works
Vargas‐Caballero, M., & Robinson, H. P. C. (2003) · Journal of Neurophysiology · doi:10.1152/jn.01038.2002 · Cited by 56 · see citing works
Khedr, E. M., Gilio, F., & Rothwell, J. C. (2004) · Clinical Neurophysiology · doi:10.1016/j.clinph.2003.08.025 · Cited by 50 · see citing works
Lazzaro, V. D., Thickbroom, G. W., Pilato, F., Profice, P., Dileone, M., Mazzone, P., Insola, A., Ranieri, F., Tonali, P., & Rothwell, J. C. (2007) · Clinical Neurophysiology · doi:10.1016/j.clinph.2007.02.020 · Cited by 48 · see citing works
Self-citationThe induction of N -methyl-D-aspartate receptor-dependent long-term potentiation
Collingridge, G. L. (2003) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2002.1241 · Cited by 46 · see citing works
Homeostasis or synaptic plasticity?
Frégnac, Y. (1998) · Nature · doi:10.1038/35996 · Cited by 41 · see citing works
Developing concepts of the synapses
Eccles, J. C. (1990) · Journal of Neuroscience · doi:10.1523/jneurosci.10-12-03769.1990 · Cited by 41 · see citing works
Methodology and application of TMS mapping.
Thickbroom, G. W., Byrnes, M. L., & Mastaglia, F. L. (1999) · PubMed · Cited by 41 · see citing works
Self-citationHamada, 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 · see citing works
Benwell, N. M., Mastaglia, F. L., & Thickbroom, G. W. (2006) · Experimental Brain Research · doi:10.1007/s00221-006-0579-3 · Cited by 33 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Modulation of brain plasticity in stroke: a novel model for neurorehabilitation
Pino, G. D., Pellegrino, G., Assenza, G., Capone, F., Ferreri, F., Formica, D., Ranieri, F., Tombini, M., Ziemann, U., Rothwell, J. C., et al. (2014) · Nature Reviews Neurology · doi:10.1038/nrneurol.2014.162 · Cited by 984 · see citing works
Ridding, M. C., & Ziemann, U. (2010) · The Journal of Physiology · doi:10.1113/jphysiol.2010.190314 · Cited by 787 · see citing works
Physiology of repetitive transcranial magnetic stimulation of the human brain
Hoogendam, J. M., Ramakers, G. M. J., & Di Lazzaro, V. (2010) · Brain Stimulation · doi:10.1016/j.brs.2009.10.005 · Cited by 669 · see citing works
Enhancement of human cognitive performance using transcranial magnetic stimulation (TMS)
Luber, B., & Lisanby, S. H. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2013.06.007 · Cited by 508 · see citing works
Peterchev, A. V., Wagner, T. A., Miranda, P. C., Nitsche, M. A., Paulus, W., Lisanby, S. H., Pascual‐Leone, Á., & Bikson, M. (2011) · Brain stimulation · doi:10.1016/j.brs.2011.10.001 · Cited by 433 · see citing works
Using non-invasive brain stimulation to augment motor training-induced plasticity
Bolognini, N., Pascual‐Leone, Á., & Fregni, F. (2009) · Journal of NeuroEngineering and Rehabilitation · doi:10.1186/1743-0003-6-8 · Cited by 413 · see citing works
Pell, G. S., Roth, Y., & Zangen, A. (2010) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2010.10.003 · Cited by 410 · see citing works
Consensus paper: Combining transcranial stimulation with neuroimaging
Siebner, H. R., Bergmann, T. O., Bestmann, S., Massimini, M., Johansen‐Berg, H., Mochizuki, H., Bohning, D. E., Boorman, E. D., Groppa, S., Miniussi, C., et al. (2009) · Brain stimulation · doi:10.1016/j.brs.2008.11.002 · Cited by 356 · see citing works
Random Noise Stimulation Improves Neuroplasticity in Perceptual Learning
Fertonani, A., Pirulli, C., & Miniussi, C. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.2002-11.2011 · Cited by 341 · see citing works
Siebner, H. R., Hartwigsen, G., Kassuba, T., & Rothwell, J. C. (2009) · Cortex · doi:10.1016/j.cortex.2009.02.007 · Cited by 345 · see citing works
Efficacy and Time Course of Theta Burst Stimulation in Healthy Humans
Wischnewski, M., & Schutter, D. J. L. G. (2015) · Brain stimulation · doi:10.1016/j.brs.2015.03.004 · Cited by 329 · see citing works
Bolognini, N., Vallar, G., Casati, C., Latif, L. A., El-Nazer, R., Williams, J., Banco, E., Macea, D. D., Tesio, L., Chessa, C., et al. (2011) · Neurorehabilitation and Neural Repair · doi:10.1177/1545968311411056 · Cited by 318 · 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
Gersner, R., Kravetz, E., Feil, J., Pell, G., & Zangen, A. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.6751-10.2011 · Cited by 313 · see citing works
Ekhtiari, H., Tavakoli, H., Addolorato, G., Baeken, C., Bonci, A., Campanella, S., Castelo-Branco, L. E. C., Challet‐Bouju, G., Clark, V. P., Claus, E. D., et al. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.06.007 · Cited by 305 · see citing works
Vlachos, A., Müller‐Dahlhaus, F., Rosskopp, J., Lenz, M., Ziemann, U., & Deller, T. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.0409-12.2012 · Cited by 252 · see citing works
THETA-BURST STIMULATION: A NEW FORM OF TMS TREATMENT FOR DEPRESSION?
Chung, S. W., Hoy, K. E., & Fitzgerald, P. B. (2014) · Depression and Anxiety · doi:10.1002/da.22335 · Cited by 253 · see citing works
Can noninvasive brain stimulation enhance cognition in neuropsychiatric disorders?
Demirtas-Tatlidede, A., Vahabzadeh-Hagh, A. M., & Pascual-Leone, A. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.06.020 · Cited by 236 · see citing works
The Dynamic Duo: Combining noninvasive brain stimulation with cognitive interventions
Sathappan, A. V., Luber, B. M., & Lisanby, S. H. (2018) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2018.10.006 · Cited by 225 · see citing works
Bentwich, J., Dobronevsky, E., Aichenbaum, S., Shorer, R., Peretz, R., Khaigrekht, M., Gandelman‐Marton, R., & Rabey, J. M. (2011) · Journal of Neural Transmission · doi:10.1007/s00702-010-0578-1 · Cited by 224 · see citing works
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 · see citing works
Theta-Burst Transcranial Magnetic Stimulation Alters Cortical Inhibition
Benali, A., Trippe, J., Weiler, E., Mix, A., Petrasch‐Parwez, E., Girzalsky, W., Eysel, U. T., Erdmann, R., & Funke, K. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.1379-10.2011 · Cited by 215 · see citing works
Neuromodulation of chronic headaches: position statement from the European Headache Federation
Martelletti, P., Jensen, R., Antal, A., Arcioni, R., Brighina, F., de Tommaso, M., Franzini, A., Fontaine, D., Heiland, M., Jürgens, T. P., et al. (2013) · The Journal of Headache and Pain · doi:10.1186/1129-2377-14-86 · Cited by 210 · see citing works
Veniero, D., Vossen, A. Y., Groß, J., & Thut, G. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00477 · Cited by 202 · see citing works
Wagner, T., Rushmore, J., Eden, U. T., & Valero‐Cabré, A. (2008) · Cortex · doi:10.1016/j.cortex.2008.10.002 · Cited by 189 · see citing works
Mechanisms and applications of theta-burst rTMS on the human motor cortex
Cárdenas-Morales, L., Nowak, D. A., Kammer, T., Wolf, R. C., & Schönfeldt-Lecuona, C. (2010) · Brain Topography · doi:10.1007/s10548-009-0084-7 · Cited by 209 · see citing works
Modulation of cortical inhibition by rTMS – findings obtained from animal models
Funke, K., & Benali, A. (2011) · The Journal of Physiology · doi:10.1113/jphysiol.2011.206573 · Cited by 173 · see citing works
Hanlon, C. A., Dowdle, L. T., Austelle, C. W., DeVries, W., Mithoefer, O., Badran, B. W., & George, M. S. (2015) · Brain Research · doi:10.1016/j.brainres.2015.02.053 · Cited by 166 · see citing works
Lee, J., Choi, B. H., Oh, E., Sohn, E. H., & Lee, A. Y. (2016) · Journal of Clinical Neurology · doi:10.3988/jcn.2016.12.1.57 · Cited by 166 · see citing works
Marra, H., Myczkowski, M. L., Memória, C. M., Arnaut, D., Ribeiro, P. L., Mansur, C. G., Alberto, R. L., Bellini, B. B., da Silva, A. A. F., Tortella, G., et al. (2015) · Behavioural Neurology · doi:10.1155/2015/287843 · Cited by 161 · see citing works
Repetitive Transcranial Magnetic Stimulation of the Brain
Tang, A. D., Thickbroom, G. W., & Rodger, J. (2015) · The Neuroscientist · doi:10.1177/1073858415618897 · Cited by 157 · see citing works
Self-citationModulation of human corticospinal excitability by paired associative stimulation
Carson, R. G., & Kennedy, N. C. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00823 · Cited by 156 · see citing works
Transcranial Magnetic and Direct Current Stimulation in Children
Hameed, M. Q., Dhamne, S. C., Gersner, R., Kaye, H. L., Oberman, L. M., Pascual‐Leone, Á., & Rotenberg, A. (2017) · Current Neurology and Neuroscience Reports · doi:10.1007/s11910-017-0719-0 · Cited by 149 · see citing works
Rizzo, V., Siebner, H. R., Morgante, F., Mastroeni, C., Girlanda, P., & Quartarone, A. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhn144 · Cited by 145 · see citing works
Noninvasive Stimulation of the Human Brain: Activation of Multiple Cortical Circuits
Lazzaro, V. D., Rothwell, J. C., & Capogna, M. (2017) · The Neuroscientist · doi:10.1177/1073858417717660 · Cited by 136 · see citing works
The effects of motor cortex rTMS on corticospinal descending activity
Lazzaro, V. D., Profice, P., Pilato, F., Dileone, M., Oliviero, A., & Ziemann, U. (2010) · Clinical Neurophysiology · doi:10.1016/j.clinph.2009.11.007 · Cited by 137 · see citing works
Enhancing verbal episodic memory in older and young subjects after non-invasive brain stimulation
Manenti, R., Brambilla, M., Petesi, M., Ferrari, C., & Cotelli, M. (2013) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2013.00049 · Cited by 135 · see citing works
Makowiecki, K., Harvey, A. R., Sherrard, R. M., & Rodger, J. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0723-14.2014 · Cited by 130 · see citing works
Grehl, S., Viola, H. M., Fuller-Carter, P. I., Carter, K. W., Dunlop, S. A., Hool, L. C., Sherrard, R. M., & Rodger, J. (2014) · Brain stimulation · doi:10.1016/j.brs.2014.09.012 · Cited by 129 · see citing works
Reithler, J., Peters, J. C., & Sack, A. T. (2011) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2011.04.004 · Cited by 124 · see citing works
Changes in Plasticity Across the Lifespan
Oberman, L. M., & Pascual‐Leone, Á. (2013) · Progress in brain research · doi:10.1016/b978-0-444-63327-9.00016-3 · Cited by 125 · see citing works
Noninvasive brain stimulation to modulate neuroplasticity in traumatic brain injury
Villamar, M. F., Santos Portilla, A., Fregni, F., & Zafonte, R. (2012) · Neuromodulation: Technology at the Neural Interface · doi:10.1111/j.1525-1403.2012.00474.x · Cited by 119 · see citing works
Bijsterbosch, J. D., Barker, A. T., Lee, K.-H., & Woodruff, P. W. R. (2012) · Medical & Biological Engineering & Computing · doi:10.1007/s11517-012-0922-8 · Cited by 115 · see citing works
Rodger, J., Mo, C., Wilks, T., Dunlop, S. A., & Sherrard, R. M. (2012) · The FASEB Journal · doi:10.1096/fj.11-194878 · Cited by 109 · see citing works
Consensus: New methodologies for brain stimulation
Huang, Y., Sommer, M., Thickbroom, G. W., Hamada, M., Pascual-Leonne, A., Paulus, W., Claßen, J., Peterchev, A. V., Zangen, A., & Ugawa, Y. (2008) · Brain stimulation · doi:10.1016/j.brs.2008.09.007 · Cited by 112 · see citing works
Self-citationOberman, L. M., Enticott, P. G., Casanova, M. F., Rotenberg, A., Pascual‐Leone, Á., McCracken, J. T., & the TMS in ASD Consensus Group (2015) · Autism Research · doi:10.1002/aur.1567 · Cited by 110 · see citing works
Spiegel, D. P., Byblow, W. D., Hess, R. F., & Thompson, B. S. (2013) · Neurorehabilitation and neural repair · doi:10.1177/1545968313491006 · Cited by 108 · see citing works
New modalities of brain stimulation for stroke rehabilitation
Edwardson, M. A., Lucas, T. H., Carey, J. R., & Fetz, E. E. (2012) · Experimental Brain Research · doi:10.1007/s00221-012-3315-1 · Cited by 109 · see citing works
Luber, B. M., Davis, S. W., Bernhardt, E. R., Neacsiu, A. D., Kwapil, L., Lisanby, S. H., & Strauman, T. J. (2017) · NeuroImage · doi:10.1016/j.neuroimage.2016.12.083 · Cited by 109 · see citing works
Network Connectivity and Individual Responses to Brain Stimulation in the Human Motor System
Cárdenas‐Morales, L., Volz, L. J., Michely, J., Rehme, A. K., Pool, E., Nettekoven, C., Eickhoff, S. B., Fink, G. R., & Grefkes, C. (2013) · Cerebral Cortex · doi:10.1093/cercor/bht023 · Cited by 108 · see citing works
Volz, L. J., Benali, A., Mix, A., Neubacher, U., & Funke, K. (2013) · Brain stimulation · doi:10.1016/j.brs.2013.01.008 · Cited by 105 · see citing works
Bashir, S., Mizrahi, I., Weaver, K., Fregni, F., & Pascual‐Leone, Á. (2010) · PM&R · doi:10.1016/j.pmrj.2010.10.015 · Cited by 109 · see citing works
Time-course of "off-line" prefrontal rTMS effects - a PET study
Eisenegger, C., Treyer, V., Fehr, E., & Knoch, D. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.04.172 · Cited by 109 · see citing works
Hermiller, M. S., Chen, Y. F., Parrish, T. B., & Voss, J. L. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.0486-20.2020 · Cited by 103 · see citing works
Byblow, W. D., Stinear, C. M., Smith, M., Bjerre, L., Flaskager, B. K., & McCambridge, A. B. (2012) · PLoS ONE · doi:10.1371/journal.pone.0033882 · Cited by 97 · see citing works
Carmel, J. B., & Martin, J. H. (2014) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2014.00051 · Cited by 96 · see citing works
Cortical excitability and neurology: insights into the pathophysiology.
Badawy, R. A. B., Loetscher, T., Macdonell, R. A. L., & Brodtmann, A. G. (2012) · Europe PMC (PubMed Central) · Cited by 96 · see citing works
Hanlon, C. A., Dowdle, L. T., & Henderson, J. (2018) · Pharmacological Reviews · doi:10.1124/pr.116.013649 · Cited by 94 · see citing works
Transcranial magnetic stimulation in cognitive rehabilitation
Miniussi, C., & Rossini, P. M. (2011) · Neuropsychological Rehabilitation · doi:10.1080/09602011.2011.562689 · Cited by 94 · see citing works
Non-invasive brain stimulation of the aging brain: State of the art and future perspectives
Tatti, E., Rossi, S., Innocenti, I., Rossi, A., & Santarnecchi, E. (2016) · Ageing Research Reviews · doi:10.1016/j.arr.2016.05.006 · Cited by 94 · see citing works
Korchounov, A., & Ziemann, U. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.75 · Cited by 98 · see citing works
Personalized Transcranial Magnetic Stimulation in Psychiatry
Cocchi, L., & Zalesky, A. (2018) · Biological Psychiatry Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2018.01.008 · Cited by 89 · see citing works
Motor Cortical Plasticity in Parkinson’s Disease
Udupa, K., & Chen, R. E. (2013) · Frontiers in Neurology · doi:10.3389/fneur.2013.00128 · Cited by 87 · see citing works
Cash, R. F. H., Ziemann, U., Murray, K., & Thickbroom, G. W. (2009) · Journal of Neurophysiology · doi:10.1152/jn.00782.2009 · Cited by 85 · see citing works
Self-citationSchilberg, L., Schuhmann, T., & Sack, A. T. (2017) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_01100 · Cited by 82 · see citing works
Hermiller, M. S., VanHaerents, S. A., Raij, T., & Voss, J. L. (2018) · Hippocampus · doi:10.1002/hipo.23054 · Cited by 81 · see citing works
Noh, N. A., Fuggetta, G., Manganotti, P., & Fiaschi, A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0035080 · Cited by 79 · see citing works
Mix, A., Benali, A., Eysel, U. T., & Funke, K. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07425.x · Cited by 78 · see citing works
Non-pharmacological intervention for memory decline
Cotelli, M., Manenti, R., Zanetti, O., & Miniussi, C. (2012) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2012.00046 · Cited by 76 · see citing works
Sheffer, C. E., Bickel, W. K., Brandon, T. H., Franck, C. T., Deen, D., Panissidi, L., Abdali, S. A., Pittman, J. C., Lunden, S. E., Prashad, N., et al. (2017) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2017.09.037 · Cited by 70 · see citing works
Transcranial stimulation and cognition
Miniussi, C., & Ruzzoli, M. (2013) · Handbook of clinical neurology · doi:10.1016/b978-0-444-53497-2.00056-5 · Cited by 73 · see citing works
Coppola, G., Pasqua, V. D., Pierelli, F., & Schoenen, J. E. (2012) · Cephalalgia · doi:10.1177/0333102412446313 · Cited by 72 · see citing works
Transcranial magnetic stimulation in Gilles de la Tourette syndrome
Orth, M. (2009) · Journal of Psychosomatic Research · doi:10.1016/j.jpsychores.2009.07.014 · Cited by 72 · see citing works
Chen, R. E., & Udupa, K. (2009) · Motor Control · doi:10.1123/mcj.13.4.442 · Cited by 71 · see citing works
Noninvasive brain stimulation in neurorehabilitation
Sandrini, M., & Cohen, L. (2013) · Handbook of Clinical Neurology · doi:10.1016/b978-0-444-53497-2.00040-1 · Cited by 66 · see citing works
Associative Motor Cortex Plasticity: Direct Evidence in Humans
Lazzaro, V. D., Dileone, M., Pilato, F., Profice, P., Oliviero, A., Mazzone, P., Insola, A., Capone, F., Ranieri, F., & Tonali, P. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhn255 · Cited by 70 · see citing works
Luber, B. M., Steffener, J., Tucker, A. M., Habeck, C. G., Peterchev, A. V., Deng, Z., Basner, R. C., Stern, Y., & Lisanby, S. H. (2013) · SLEEP · doi:10.5665/sleep.2712 · Cited by 68 · see citing works
Li, Y., Yan, X., Liu, J., Li, L., Hu, X., Sun, H., & Tian, J. (2014) · Neurochemistry International · doi:10.1016/j.neuint.2014.06.004 · Cited by 67 · see citing works
Zareen, N., Shinozaki, M., Ryan, D., Alexander, H., Amer, A., Truong, D. Q., Khadka, N., Sarkar, A. D., Naeem, S., Bikson, M., et al. (2017) · Experimental Neurology · doi:10.1016/j.expneurol.2017.08.004 · Cited by 68 · see citing works
Torres, J., Drebing, D. E., & Hamilton, R. H. (2013) · Restorative Neurology and Neuroscience · doi:10.3233/rnn-130314 · Cited by 64 · see citing works
Eggers, C., Fink, G. R., & Nowak, D. A. (2010) · Journal of Neurology · doi:10.1007/s00415-010-5597-1 · Cited by 66 · see citing works
Cárdenas‐Morales, L., Grön, G., & Kammer, T. (2010) · Human Brain Mapping · doi:10.1002/hbm.21160 · Cited by 63 · see citing works
Labedi, A., Benali, A., Mix, A., Neubacher, U., & Funke, K. (2014) · Brain stimulation · doi:10.1016/j.brs.2014.02.010 · Cited by 62 · see citing works
A primer on priming the human motor cortex
Siebner, H. R. (2010) · Clinical Neurophysiology · doi:10.1016/j.clinph.2009.12.009 · Cited by 63 · see citing works
Cristofanilli, M., Harris, V., Zigelbaum, A., Goossens, A. M., Lu, A. Z., Rosenthal, H. E., & Sadiq, S. A. (2011) · Stem Cells and Development · doi:10.1089/scd.2010.0547 · Cited by 63 · see citing works
Noninvasive Neuromodulation in Poststroke Gait Disorders
Chieffo, R., Comı, G., & Leocani, L. (2015) · Neurorehabilitation and neural repair · doi:10.1177/1545968315586464 · Cited by 61 · see citing works
Time-course of changes in neuronal activity markers following iTBS-TMS of the rat neocortex
Hoppenrath, K., & Funke, K. (2013) · Neuroscience Letters · doi:10.1016/j.neulet.2013.01.003 · Cited by 60 · see citing works
Inducing Homeostatic-Like Plasticity in Human Motor Cortex Through Converging Corticocortical Inputs
Pötter‐Nerger, M., Fischer, S., Mastroeni, C., Groppa, S., Deuschl, G., Volkmann, J., Quartarone, A., Münchau, A. M., & Siebner, H. R. (2009) · Journal of Neurophysiology · doi:10.1152/jn.91046.2008 · Cited by 61 · see citing works
Oberman, L. M., Pascual‐Leone, Á., & Rotenberg, A. (2014) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2014.00627 · Cited by 65 · see citing works
Moretti, J., & Rodger, J. (2022) · Current Research in Neurobiology · doi:10.1016/j.crneur.2022.100033 · Cited by 60 · see citing works
Revisiting the excitation/inhibition imbalance hypothesis of ASD through a clinical lens
Port, R. G., Oberman, L. M., & Roberts, T. P. L. (2019) · British Journal of Radiology · doi:10.1259/bjr.20180944 · Cited by 60 · see citing works
Sandrini, M., Manenti, R., Brambilla, M., Cobelli, C., Cohen, L. G., & Cotelli, M. (2015) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2015.12.010 · Cited by 61 · see citing works
Abdelrahman, A. A., Noaman, M. M., Fawzy, M., Moheb, A., Karim, A. A., & Khedr, E. M. (2021) · Scientific Reports · doi:10.1038/s41598-020-80927-5 · Cited by 59 · see citing works
LTD-like plasticity induced by paired associative stimulation: direct evidence in humans
Lazzaro, V. D., Dileone, M., Profice, P., Pilato, F., Oliviero, A., Mazzone, P., Iorio, R. D., Capone, F., Ranieri, F., Florio, L., et al. (2009) · Experimental Brain Research · doi:10.1007/s00221-009-1774-9 · Cited by 59 · see citing works
Tang, A. D., Bennett, W., Bindoff, A. D., Bolland, S. J., Collins, J. M., Langley, R. C., Garry, M. I., Summers, J. J., Hinder, M. R., Rodger, J., et al. (2021) · Brain stimulation · doi:10.1016/j.brs.2021.10.001 · Cited by 58 · see citing works
Augmenting Plasticity Induction in Human Motor Cortex by Disinhibition Stimulation
Cash, R. F. H., Murakami, T., Chen, R. E., Thickbroom, G. W., & Ziemann, U. (2014) · Cerebral Cortex · doi:10.1093/cercor/bhu176 · Cited by 58 · see citing works
Self-citationChang, D., Zhang, J., Peng, W., Shen, Z., Gao, X., Du, Y.-H., Ge, Q., Song, D., Shang, Y., & Wang, Z. (2018) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2018.00344 · Cited by 48 · see citing works
Variability of behavioural responses to transcranial magnetic stimulation: Origins and predictors
Nicolo, P., Ptak, R., & Guggisberg, A. G. (2015) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2015.01.033 · Cited by 56 · see citing works
Bickel, W., Snider, S. E., Quisenberry, A. J., Stein, J. S., & Hanlon, C. (2015) · Progress in Brain Research · doi:10.1016/bs.pbr.2015.07.009 · Cited by 55 · see citing works
Hendrikse, J. J., Kandola, A. A., Coxon, J. P., Rogasch, N. C., & Yücel, M. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.09.023 · Cited by 53 · see citing works
- Authors
- Thickbroom, G. W.
- Affiliations
- The University of Western Australia (AU)
- Corresponding author
- Thickbroom, Gary W.
- Venue
- Experimental Brain Research
- Published
- 2007-06-12
- Volume
- 180
- Issue
- 4
- Pages
- 583-593
- ISSN
- 0014-4819 (ISSN-L)
- 1432-1106
- OpenAlex
- W2064656928
- Cited by
- 326
- References
- 84
- Citations by year
- 2026: 12 · 2025: 14 · 2024: 4 · 2023: 13 · 2022: 10 · 2021: 23 · 2020: 19 · 2019: 11 · 2018: 15 · 2017: 17 · 2016: 22 · 2015: 22 · 2014: 24 · 2013: 33 · 2012: 23
- FWCI
- 1.24
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Experimental Brain Research (publishedVersion)
- PubMed (publishedVersion)
- UWA Profiles and Research Repository (UWA) (submittedVersion)
- 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
- transcranial magnetic stimulation, synaptic plasticity, repetitive TMS, theta burst stimulation, paired associative stimulation, spike-timing-dependent plasticity, activity-dependent plasticity, homeostatic regulation, non-invasive brain stimulation, inhibitory networks, sensorimotor integration
- MeSH terms
- Action Potentials, Animals, Brain, Humans, Models, Neurological, Nerve Net, Neural Inhibition, Synaptic Transmission, Neuronal Plasticity, Synapses, Transcranial Magnetic Stimulation
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review