Concurrent TMS to the primary motor cortex augments slow motor learning
Open accessAbstract
Transcranial magnetic stimulation (TMS) has shown promise as a treatment tool, with one FDA approved use. While TMS alone is able to up- (or down-) regulate a targeted neural system, we argue that TMS applied as an adjuvant is more effective for repetitive physical, behavioral and cognitive therapies, that is, therapies which are designed to alter the network properties of neural systems through Hebbian learning. We tested this hypothesis in the context of a slow motor learning paradigm. Healthy right-handed individuals were assigned to receive 5 Hz TMS (TMS group) or sham TMS (sham group) to the right primary motor cortex (M1) as they performed daily motor practice of a digit sequence task with their non-dominant hand for 4 weeks. Resting cerebral blood flow (CBF) was measured by H2(15)O PET at baseline and after 4 weeks of practice. Sequence performance was measured daily as the number of correct sequences performed, and modeled using a hyperbolic function. Sequence performance increased significantly at 4 weeks relative to baseline in both groups. The TMS group had a significant additional improvement in performance, specifically, in the rate of skill acquisition. In both groups, an improvement in sequence timing and transfer of skills to non-trained motor domains was also found. Compared to the sham group, the TMS group demonstrated increases in resting CBF specifically in regions known to mediate skill learning namely, the M1, cingulate cortex, putamen, hippocampus, and cerebellum. These results indicate that TMS applied concomitantly augments behavioral effects of motor practice, with corresponding neural plasticity in motor sequence learning network. These findings are the first demonstration of the behavioral and neural enhancing effects of TMS on slow motor practice and have direct application in neurorehabilitation where TMS could be applied in conjunction with physical therapy.
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TMS applied during various learning tasks increases performance, possibly by stimulating local hebbian learning.
“Applied during various learning tasks (e.g., motor learning; Narayana et al., 2014 and number processing; Cohen Kadosh, Soskic, Iuculano, Kanai, & Walsh, 2010), TMS increases performance, possibly by stimulating local hebbian learning (i.e. enhancing the connections between cells active together).”
From From early markers to neuro-developmental mechanisms of autism (2014) · cites this paper as Narayana et al., 2014
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The assessment and analysis of handedness: The Edinburgh inventory
Oldfield, R. C. (1971) · Neuropsychologia · doi:10.1016/0028-3932(71)90067-4 · Cited by 35,900 · see citing works
Advances in functional and structural MR image analysis and implementation as FSL
Smith, S. M., Jenkinson, M., Woolrich, M. W., Beckmann, C. F., Behrens, T. E. J., Johansen-Berg, H., Bannister, P. R., De Luca, M., Drobnjak, I., Flitney, D. E., et al. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2004.07.051 · Cited by 13,630 · see citing works
Co-Planar Stereotaxic Atlas of the Human Brain
Talairach, J., & Tournoux, P. (1988) · Medical Entomology and Zoology · Cited by 11,798 · see citing works
Co-planar stereotaxic atlas of the human brain
Laitinen, L. (1989) · Clinical Neurology and Neurosurgery · doi:10.1016/0303-8467(89)90128-5 · Cited by 7,565 · see citing works
Rossi, S., Hallett, M., Rossini, P. M., & Pascual-Leone, A. (2009) · Clinical Neurophysiology · doi:10.1016/j.clinph.2009.08.016 · Cited by 5,367 · see citing works
NON-INVASIVE MAGNETIC STIMULATION OF HUMAN MOTOR CORTEX
Barker, A. T., Jalinous, R., & Freeston, I. L. (1985) · The Lancet · doi:10.1016/s0140-6736(85)92413-4 · Cited by 4,466 · see citing works
Rossini, P. M., Barker, A. T., Berardelli, A., Caramia, M. D., Caruso, G., Cracco, R. Q., Dimitrijević, M. R., Hallett, M., Katayama, Y., Lücking, C. H., et al. (1994) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(94)90029-9 · Cited by 3,030 · 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 1× · see citing works
“Higher frequencies of TMS generally have shown facilitationwhile rates less than 1 Hz have demonstrated inhibition at least in the motor system (Chen et al., 1997; Ridding and Rothwell, 2007).”
BackgroundFunctional MRI evidence for adult motor cortex plasticity during motor skill learning
Kami, A., Meyer, G., Jezzard, P., Adams, M. M., Turner, R., & Ungerleider, L. G. (1995) · Nature · doi:10.1038/377155a0 · Cited by 1,883 · see citing works
Pascual‐Leone, Á., Nguyet, D., Cohen, L. G., Brasil-Neto, J. P., Cammarota, Á., & Hallett, M. (1995) · Journal of Neurophysiology · doi:10.1152/jn.1995.74.3.1037 · Cited by 1,410 · see citing works
Reis, J., Schambra, H. M., Cohen, L. G., Buch, E. R., Fritsch, B., Zarahn, E., Celnik, P. A., & Krakauer, J. W. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0805413106 · Cited by 1,401 · see citing works
Karni, A., Meyer, G., Rey-Hipolito, C., Jezzard, P., Adams, M. M., Turner, R., & Ungerleider, L. G. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.3.861 · Cited by 1,387 · see citing works
Reorganization and plasticity in the adult brain during learning of motor skills
Doyon, J., & Benali, H. (2005) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2005.03.004 · Cited by 1,028 · see citing works
Contributions of the basal ganglia and functionally related brain structures to motor learning
Doyon, J., Bellec, P., Amsel, R., Penhune, V., Monchi, O., Carrier, J., Lehéricy, S., & Benali, H. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.11.012 · Cited by 783 · see citing works
Study and Modulation of Human Cortical Excitability With Transcranial Magnetic Stimulation
Pascual‐Leone, Á., Tormos, J. M., Keenan, J. P., Tarazona, F., Cañete, C., & Catalá, M. D. (1998) · Journal of Clinical Neurophysiology · doi:10.1097/00004691-199807000-00005 · Cited by 779 · see citing works
Transcranial magnetic stimulation: new insights into representational cortical plasticity
Siebner, H. R., & Rothwell, J. C. (2003) · Experimental Brain Research · doi:10.1007/s00221-002-1234-2 · Cited by 753 · see citing works
Strengthening of horizontal cortical connections following skill learning
Rioult-Pedotti, M. S., Friedman, D. J., Hess, G., & Donoghue, J. P. (1998) · Nature Neuroscience · doi:10.1038/678 · Cited by 703 · see citing works
Is there a future for therapeutic use of transcranial magnetic stimulation?
Ridding, M. C., & Rothwell, J. C. (2007) · Nature Reviews Neuroscience · doi:10.1038/nrn2169 · Cited by 687 · see citing works
Imaging brain plasticity during motor skill learning
Ungerleider, L. (2002) · Neurobiology of Learning and Memory · doi:10.1006/nlme.2002.4091 · Cited by 641 · see citing works
Mechanisms of use-dependent plasticity in the human motor cortex
Bütefisch, C. M., Davis, B. C., Wise, S. P., Sawaki, L. A., Kopylev, L., Claßen, J., & Cohen, L. G. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.7.3661 · Cited by 613 · see citing works
An fMRI Study of the Role of the Medial Temporal Lobe in Implicit and Explicit Sequence Learning
Schendan, H. E., Searl, M. M., Melrose, R. J., & Stern, C. E. (2003) · Neuron · doi:10.1016/s0896-6273(03)00123-5 · Cited by 610 · see citing works
Kleim, J. A., Hogg, T. M., VandenBerg, P. M., Cooper, N. R., Hines, R. M., & Remple, M. S. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.3440-03.2004 · Cited by 595 · see citing works
Ziemann, U., Ilic, T. V., Pauli, C., Meintzschel, F., & Ruge, D. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.5016-03.2004 · Cited by 587 · see citing works
Slotema, C. W., Blom, J. D., Hoek, H. W., & Sommer, I. E. C. (2010) · The Journal of Clinical Psychiatry · doi:10.4088/jcp.08m04872gre · Cited by 584 · see citing works
Boggio, P. S., Nunes, A., Rigonatti, S. P., Nitsche, M. A., Pascual‐Leone, Á., & Fregni, F. (2007) · Restorative Neurology and Neuroscience · doi:10.3233/rnn-2007-00375 · Cited by 523 · see citing works
Fox, P. T., & Raichle, M. E. (1984) · Journal of Neurophysiology · doi:10.1152/jn.1984.51.5.1109 · Cited by 500 · see citing works
Self-citationFox, P. T., Mintun, M. A., Reiman, E. M., & Raichle, M. E. (1988) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.1988.111 · Cited by 498 · see citing works
Self-citationTherapeutic trial of repetitive transcranial magnetic stimulation after acute ischemic stroke
Khedr, E. M., Ahmed, M. A., Fathy, N., & Rothwell, J. C. (2005) · Neurology · doi:10.1212/01.wnl.0000173067.84247.36 · Cited by 486 · see citing works
Both the Hippocampus and Striatum Are Involved in Consolidation of Motor Sequence Memory
Albouy, G., Sterpenich, V., Balteau, E., Vandewalle, G., Desseilles, M., Dang-Vu, T., Darsaud, A., Ruby, P., Luppi, P.-H., Degueldre, C., et al. (2008) · Neuron · doi:10.1016/j.neuron.2008.02.008 · Cited by 463 · see citing works
Kim, Y., You, S. H., Ko, M.-H., Park, J., Lee, K. H., Jang, S. H., Yoo, W., & Hallett, M. (2006) · Stroke · doi:10.1161/01.str.0000221233.55497.51 · Cited by 453 · see citing works
Imaging Brain Plasticity: Conceptual and Methodological Issues— A Theoretical Review
Poldrack, R. A. (2000) · NeuroImage · doi:10.1006/nimg.2000.0596 · Cited by 409 · see citing works
Time scales in motor learning and development.
Newell, K. M., Liu, Y.-T., & Mayer‐Kress, G. (2001) · Psychological Review · doi:10.1037/0033-295x.108.1.57 · Cited by 407 · see citing works
Korman, M., Raz, N., Flash, T., & Karni, A. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2035019100 · Cited by 378 · see citing works
Parallel contributions of cerebellar, striatal and M1 mechanisms to motor sequence learning
Penhune, V. B., & Steele, C. J. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.09.044 · Cited by 373 · see citing works
Motor sequence learning with the nondominant left hand
Grafton, S. T., Hazeltine, E., & Ivry, R. B. (2002) · Experimental Brain Research · doi:10.1007/s00221-002-1181-y · Cited by 366 · see citing works
Dopaminergic Projections from Midbrain to Primary Motor Cortex Mediate Motor Skill Learning
Hosp, J. A., Pekanovic, A., Rioult-Pedotti, M. S., & Luft, A. R. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.5411-10.2011 · Cited by 354 · see citing works
Fox, P. T., & Mintun, M. A. (1989) · PubMed · Cited by 336 · see citing works
Self-citationPeinemann, A., Reimer, B., Löer, C., Quartarone, A., Münchau, A. M., Conrad, B., & Siebner, H. R. (2004) · Clinical Neurophysiology · doi:10.1016/j.clinph.2004.02.005 · Cited by 317 · see citing works
Learning as accumulation: A reexamination of the learning curve.
Mazur, J., & Hastie, R. (1978) · Psychological Bulletin · doi:10.1037/0033-2909.85.6.1256 · Cited by 295 · see citing works
Brain correlates of stuttering and syllable production: A PET performance-correlation analysis
Fox, P. T. (2000) · Brain · doi:10.1093/brain/123.10.1985 · Cited by 264 · see citing works
Self-citationA modality‐independent approach to spatial normalization of tomographic images of the human brain
Lancaster, J. L., Glass, T. G., Lankipalli, B. R., Downs, H., Mayberg, H. S., & Fox, P. T. (1995) · Human Brain Mapping · doi:10.1002/hbm.460030305 · Cited by 256 · see citing works
Self-citationMintun, M. A., Fox, P. T., & Raichle, M. E. (1989) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.1989.13 · Cited by 240 · see citing works
Self-citationGrafton, S. T., Woods, R. P., Mazziotta, J. C., & Phelps, M. E. (1991) · Journal of Neurophysiology · doi:10.1152/jn.1991.66.3.735 · Cited by 240 · see citing works
DeCoteau, W. E., Thorn, C. A., Gibson, D. J., Courtemanche, R., Mitra, P. P., Kubota, Y., & Graybiel, A. M. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0700818104 · Cited by 239 · see citing works
Kleim, J. A., Hines, R. M., VandenBerg, P. M., MacDonald, E., Mulrooney, R., & Pocock, D. (2003) · Neurological Research · doi:10.1179/016164103771953862 · Cited by 238 · see citing works
Adkins, D. L., & Jones, T. A. (2003) · Neurological Research · doi:10.1179/016164103771953853 · Cited by 235 · see citing works
Column‐based model of electric field excitation of cerebral cortex
Fox, P. T., Narayana, S., Tandon, N., Sandoval, H., Fox, S. P., Kochunov, P. V., & Lancaster, J. L. (2004) · Human Brain Mapping · doi:10.1002/hbm.20006 · Cited by 231 · see citing works
Self-citationLasting cortical activation after repetitive TMS of the motor cortex
Siebner, H. R., Peller, M., Willoch, F., Minoshima, S., Boecker, H., Auer, C., Drzezga, A. E., Conrad, B., & Bartenstein, P. (2000) · Neurology · doi:10.1212/wnl.54.4.956 · Cited by 225 · see citing works
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 · see citing works
Retinotopic organization of early visual spatial attention effects as revealed by PET and ERPs
Woldorff, M. G., Fox, P. T., Matzke, M., Lancaster, J. L., Veeraswamy, S., Zamarripa, F., Seabolt, M., Glass, T. G., Gao, J., Martin, C. C., et al. (1997) · Human Brain Mapping · doi:10.1002/(sici)1097-0193(1997)5:4 · Cited by 195 · see citing works
Self-citationHomeostatic and Nonhomeostatic Modulation of Learning in Human Motor Cortex
Jung, P., & Ziemann, U. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.0222-09.2009 · Cited by 191 · see citing works
Long-term effects of rTMS on motor recovery in patients after subacute stroke
Kim, Y., Chang, W., Bang, O. Y., Kim, S. T., Park, Y. H., & Lee, P. (2010) · Journal of Rehabilitation Medicine · doi:10.2340/16501977-0590 · Cited by 182 · see citing works
Repetitive Transcranial Magnetic Stimulation as an Adjunct to Constraint-Induced Therapy
Malcolm, M. P., Triggs, W. J., Light, K. E., Rothi, L. J. G., Wu, S. S. X., Reid, K., & Nadeau, S. E. (2007) · American Journal of Physical Medicine & Rehabilitation · doi:10.1097/phm.0b013e31813e0de0 · Cited by 173 · see citing works
Quartarone, A., Bagnato, S., Rizzo, V., Morgante, F., Santangelo, A., Battaglia, F., Messina, C., Siebner, H., & Girlanda, P. (2005) · Experimental Brain Research · doi:10.1007/s00221-004-2052-5 · Cited by 171 · see citing works
Motor cortex activation is related to force of squeezing
Cramer, S. C., Weisskoff, R. M., Schaechter, J. D., Nelles, G., Foley, M., Finklestein, S. P., & Rosen, B. R. (2002) · Human Brain Mapping · doi:10.1002/hbm.10040 · Cited by 168 · see citing works
Non-invasive magnetic stimulation of the human motor cortex
Baker, A. (1985) · The Lancet · Cited by 161 · see citing works
Dual-tDCS Enhances Online Motor Skill Learning and Long-Term Retention in Chronic Stroke Patients
Lefebvre, S., Laloux, P., Peeters, A. P., Desfontaines, P., Jamart, J., & Vandermeeren, Y. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2012.00343 · Cited by 151 · see citing works
Changes occur in resting state network of motor system during 4weeks of motor skill learning
Ma, L., Narayana, S., Robin, D. A., Fox, P. T., & Xiong, J. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.06.014 · Cited by 147 · see citing works
Self-citationThe power of spectral density analysis for mapping endogenous BOLD signal fluctuations
Duff, E. P., Johnston, L. A., Xiong, J., Fox, P. T., Mareels, I., & Egan, G. F. (2008) · Human Brain Mapping · doi:10.1002/hbm.20601 · Cited by 144 · see citing works
Self-citationMa, L., Wang, B., Narayana, S., Hazeltine, E., Chen, X., Robin, D. A., Fox, P. T., & Xiong, J. (2010) · Brain Research · doi:10.1016/j.brainres.2009.12.073 · Cited by 141 · see citing works
Self-citationNeuroanatomical Correlates of Motor Acquisition and Motor Transfer
Seidler, R. D., & Noll, D. C. (2008) · Journal of Neurophysiology · doi:10.1152/jn.01187.2007 · Cited by 133 · see citing works
Encoding of Motor Skill in the Corticomuscular System of Musicians
Gentner, R., Gorges, S., Weise, D., Kampe, K. A., Buttmann, M., & Claßen, J. (2010) · Current Biology · doi:10.1016/j.cub.2010.09.045 · Cited by 117 · see citing works
Polanía, R. H., Paulus, W., & Nitsche, M. A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0030971 · Cited by 105 · see citing works
Siebner, H. R., Takano, B., Peinemann, A., Schwaiger, M., Conrad, B., & Drzezga, A. E. (2001) · NeuroImage · doi:10.1006/nimg.2001.0889 · Cited by 103 · see citing works
Kim, Y., Park, J., Ko, M.-H., Jang, S. H., & Lee, P. K. W. (2004) · Neuroscience Letters · doi:10.1016/j.neulet.2004.05.113 · Cited by 102 · see citing works
Xiong, J., Ma, L., Wang, B., Narayana, S., Duff, E. P., Egan, G. F., & Fox, P. T. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.11.016 · Cited by 95 · see citing works
Self-citationCortical Plasticity During Three-Week Motor Skill Learning
Hluštı́k, P., Solodkin, A., Noll, D. C., & Small, S. L. (2004) · Journal of Clinical Neurophysiology · doi:10.1097/00004691-200405000-00006 · Cited by 91 · see citing works
Ragert, P., Dinse, H. R., Pleger, B., Wilimzig, C., Frombach, E., Schwenkreis, P., & Tegenthoff, M. (2003) · Neuroscience Letters · doi:10.1016/s0304-3940(03)00745-6 · Cited by 81 · see citing works
Evaluation of an image‐guided, robotically positioned transcranial magnetic stimulation system
Lancaster, J. L., Narayana, S., Wenzel, D., Luckemeyer, J., Roby, J. W., & Fox, P. T. (2004) · Human Brain Mapping · doi:10.1002/hbm.20041 · Cited by 77 · see citing works
Self-citationrTMS with motor training modulates cortico-basal ganglia-thalamocortical circuits in stroke patients
Chang, W. H., Kim, Y., Yoo, W., Goo, K.-H., Park, C.-H., Kim, S. T., & Pascual‐Leone, Á. (2012) · Restorative Neurology and Neuroscience · doi:10.3233/rnn-2012-110162 · Cited by 72 · see citing works
High frequency rTMS modulation of the sensorimotor networks: Behavioral changes and fMRI correlates
Yoo, W., You, S. H., Ko, M.-H., Kim, S. T., Park, C.-H., Park, J., Ohn, S. H., Hallett, M., & Kim, Y. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.10.035 · Cited by 72 · see citing works
Boyd, L. A., & Linsdell, M. A. (2009) · BMC Neuroscience · doi:10.1186/1471-2202-10-72 · Cited by 71 · see citing works
Intensity modulation of TMS‐induced cortical excitation: Primary motor cortex
Fox, P. T., Narayana, S., Tandon, N., Fox, S. P., Sandoval, H., Kochunov, P., Capaday, C., & Lancaster, J. L. (2005) · Human Brain Mapping · doi:10.1002/hbm.20192 · Cited by 70 · see citing works
Self-citationMotor Skill Learning, Retention, and Control Deficits in Parkinson's Disease
Maurer, L. K., Reuter, I., & Müller, H. (2011) · PLoS ONE · doi:10.1371/journal.pone.0021669 · Cited by 47 · see citing works
Orban, P., Peigneux, P., Lungu, O., Debas, K., Barakat, M., Bellec, P., Benali, H., Maquet, P., & Doyon, J. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.01.040 · Cited by 45 · see citing works
Geerdink, Y. A., Aarts, P. B. M., & Geurts, A. C. H. (2013) · Research in Developmental Disabilities · doi:10.1016/j.ridd.2012.11.011 · Cited by 45 · see citing works
Agostino, R., Iezzi, E., Dinapoli, L., Gilio, F., Conte, A., Mari, F., & Berardelli, A. (2007) · Experimental Brain Research · doi:10.1007/s00221-006-0838-3 · Cited by 42 · see citing works
Complex spatio-temporal dynamics of fMRI BOLD: A study of motor learning
Duff, E. P., Xiong, J., Wang, B., Cunnington, R., Fox, P. T., & Egan, G. F. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2006.09.006 · Cited by 41 · see citing works
Self-citationApplications of transcranial magnetic stimulation in studies on motor learning.
Pascual‐Leone, Á., Tarazona, F., & Catalá, M. D. (1999) · PubMed · Cited by 40 · see citing works
Practice makes transfer of motor skills imperfect
Boutin, A., Badets, A., Salesse, R. N., Fries, U., Panzer, S., & Blandin, Y. (2011) · Psychological Research · doi:10.1007/s00426-011-0355-2 · Cited by 33 · see citing works
Hebb, D. O. (1976) · Research on Child and Adolescent Psychopathology · doi:10.1007/bf00922529 · Cited by 33 · see citing works
Platz, T., Roschka, S., Christel, M. I., Duecker, F., Rothwell, J. C., & Sack, A. T. (2012) · Restorative Neurology and Neuroscience · doi:10.3233/rnn-2012-110204 · Cited by 27 · see citing works
Rábago, C. A., Lancaster, J. L., Narayana, S., Zhang, W., & Fox, P. T. (2009) · Clinical Neurophysiology · doi:10.1016/j.clinph.2009.04.020 · Cited by 23 · see citing works
Self-citationSalinas, F. S., Szabó, C. Á., Zhang, W., Jones, L., Leland, M. M., Wey, H., Duong, T. Q., Fox, P. T., & Narayana, S. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.05.065 · Cited by 23 · see citing works
Self-citationSalinas, F. S., Narayana, S., Zhang, W., Fox, P. T., & Szabó, C. Á. (2013) · Brain stimulation · doi:10.1016/j.brs.2013.03.002 · Cited by 21 · see citing works
Self-citationProlonged motor skill learning – a combined behavioural training and theta burst TMS study
Platz, T., Roschka, S., Doppl, K., Roth, C., Lotze, M., Sack, A. T., & Rothwell, J. C. (2012) · Restorative Neurology and Neuroscience · doi:10.3233/rnn-2012-110205 · Cited by 16 · see citing works
Testing promotes effector transfer
Boutin, A., Panzer, S., Salesse, R. N., & Blandin, Y. (2012) · Acta Psychologica · doi:10.1016/j.actpsy.2012.09.014 · Cited by 11 · see citing works
Force sensing system for automated assessment of motor performance during fMRI
Bill Rogers, A., Zhang, W., Narayana, S., Lancaster, J. L., Robin, D. A., & Fox, P. T. (2010) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2010.04.011 · Cited by 10 · see citing works
Self-citationKleim (n.d.) · doi:10.1044/1092-4388(2008/018
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Rossi, S., Antal, A., Bestmann, S., Bikson, M., Brewer, C., Brockmöller, J., Carpenter, L. L., Cincotta, M., Chen, R., Daskalakis, J. D., et al. (2021) · Clinical Neurophysiology · doi:10.1016/j.clinph.2020.10.003 · Cited by 1,573 · see citing works
Experts bodies, experts minds: How physical and mental training shape the brain
Debarnot, U., Sperduti, M., Rienzo, F. D., & Guillot, A. (2014) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2014.00280 · Cited by 171 · see citing works
Neuroenhancement: Enhancing brain and mind in health and in disease
Clark, V. P., & Parasuraman, R. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2013.08.071 · Cited by 158 · see citing works
From early markers to neuro-developmental mechanisms of autism
Gliga, T., Jones, E. J. H., Bedford, R., Charman, T., & Johnson, M. H. (2014) · Developmental Review · doi:10.1016/j.dr.2014.05.003 · Cited by 150 · see citing works
Current issues related to motor sequence learning in humans
Doyon, J., Gabitov, E., Vahdat, S., Lungu, O., & Boutin, A. (2017) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2017.11.012 · Cited by 144 · see citing works
SeXX Matters in Multiple Sclerosis
Gilli, F., DiSano, K. D., & Pachner, A. R. (2020) · Frontiers in Neurology · doi:10.3389/fneur.2020.00616 · Cited by 77 · see citing works
Beynel, L., Davis, S. W., Crowell, C. A., Hilbig, S. A., Lim, W., Nguyên, D. T., Palmer, H., Brito, A., Peterchev, A. V., Luber, B., et al. (2019) · PLoS ONE · doi:10.1371/journal.pone.0213707 · Cited by 72 · see citing works
Tang, A. D., Bennett, W. R., Hadrill, C., Collins, J. M., Fulopova, B., Wills, K. E., Bindoff, A. D., Puri, R., Garry, M. I., Hinder, M. R., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-22385-8 · Cited by 38 · see citing works
A wearable repetitive transcranial magnetic stimulation device
Qi, Z., Liu, H., Jin, F., Wang, Y.-H., Lu, X.-F., Liu, L., Yang, Z.-Y., Fan, L.-Z., Song, M., Zuo, N.-M., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-58095-9 · Cited by 34 · see citing works
Qi, F., Nitsche, M. A., Ren, X.-P., Wang, D., & Wang, L. (2023) · Frontiers in Neurology · doi:10.3389/fneur.2023.1156987 · Cited by 30 · see citing works
Kishore, A., Popa, T., James, P., Yahia‐Cherif, L., Backer, F., Chacko, L. V., Govind, P., Pradeep, S., & Meunier, S. (2014) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2014.05.004 · Cited by 30 · see citing works
Using brain stimulation to disentangle neural correlates of conscious vision
de Graaf, T. A., & Sack, A. T. (2014) · Frontiers in Psychology · doi:10.3389/fpsyg.2014.01019 · Cited by 29 · see citing works
Poh, E. Z., Harvey, A. R., Makowiecki, K., & Rodger, J. (2018) · eNeuro · doi:10.1523/eneuro.0163-17.2018 · Cited by 20 · see citing works
Zhang, D., & Ma, Y. (2015) · Scientific Reports · doi:10.1038/srep14796 · Cited by 20 · see citing works
Lacroix, A., Proulx-Bégin, L., Hamel, R., Beaumont, L. D., Bernier, P., & Lepage, J. (2019) · Scientific Reports · doi:10.1038/s41598-019-46379-2 · Cited by 19 · see citing works
Fathoni, A. F. (2018) · International Seminar of Public Health and Education (ISPHE) · doi:10.2991/isphe-18.2018.49 · Cited by 18 · see citing works
Cortical circuit dynamics underlying motor skill learning: from rodents to humans
Kogan, E., Lu, J., & Zuo, Y. (2023) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2023.1292685 · Cited by 16 · see citing works
What can be found in scalp EEG spectrum beyond common frequency bands. EEG–fMRI study
Mareček, R., Lamoš, M., Mikl, M., Barton, M., Fajkus, J., Rektor, & Brázdil, M. (2016) · Journal of Neural Engineering · doi:10.1088/1741-2560/13/4/046026 · Cited by 16 · see citing works
Herszage, J., Dayan, E., Sharon, H., & Censor, N. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.00076 · Cited by 13 · see citing works
Qiang, L., Millard, K. A. O., Tetnowski, J. A., Narayana, S., & Cannito, M. P. (2021) · Journal of Voice · doi:10.1016/j.jvoice.2020.12.019 · Cited by 12 · see citing works
Self-citationLiu, J., Wang, J., Tan, G., Sheng, Y., Feng, L., Tang, T., Li, X., Xie, Q., Liu, H., & Wei, Y. (2023) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.2023.3294509 · Cited by 8 · see citing works
Bilateral intracortical inhibition during unilateral motor preparation and sequence learning
Hamel, R., Waltzing, B. M., Hinder, M. R., McAllister, C. J., Jenkinson, N., & Galea, J. M. (2024) · Brain stimulation · doi:10.1016/j.brs.2024.03.009 · Cited by 6 · see citing works
Taylor, S. F., Gu, P., Simmonite, M., Lasagna, C. A., Tso, I. F., Lee, T. G., Vesia, M., & Hernández-García, L. (2023) · Biological Psychiatry Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2023.10.005 · Cited by 5 · see citing works
Facial Nerve Axotomy Induces Changes on Hippocampal CA3-to-CA1 Long-term Synaptic Plasticity
Torrado-Arévalo, R., Troncoso, J., & Múnera, A. (2021) · Neuroscience · doi:10.1016/j.neuroscience.2021.08.023 · Cited by 5 · see citing works
Zhang, Y.-S., Li, Y.-D., Ou, C.-X., Bi, Z.-T., Xiao, J., Zhang, J., Wei, J.-X., Xu, J., & Huang, L. (2026) · Frontiers in Physiology · doi:10.3389/fphys.2026.1744260 · Cited by 4 · see citing works
Altered gray matter volume and functional connectivity of the motor network in young divers
Liu, X., Liu, L., Hou, F., Zhou, Z., Wu, Q., & Li, H. (2017) · Journal of X-Ray Science and Technology · doi:10.3233/xst-17305 · Cited by 4 · see citing works
Li, X., Xiang, Q., Cen, H., Zhai, Z., Gao, T., Lu, C., Dong, Y., Ye, Y., Zhang, C., Zhuo, K., et al. (2024) · Neuropsychiatric Disease and Treatment · doi:10.2147/ndt.s468219 · Cited by 3 · see citing works
Taylor, S. F., Lee, T. G., Jonides, J. J., Tso, I. F., & Hernández-García, L. (2020) · Journal of Psychiatry and Brain Science · doi:10.20900/jpbs.20200011 · Cited by 3 · see citing works
Cognitive Enhancement Through Mathematical Problem-Solving
Saridakis, I., & Doukakis, S. (2021) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-78775-2_25 · Cited by 2 · see citing works
Advances in anxiety research: Neurocognitive mechanisms and clinical applications
Luo, Y., Qin, S., Zhu, Y., Li, Z., Zhang, Z., Jin, Z., & Xu, P. (2023) · Chinese Science Bulletin (Chinese Version) · doi:10.1360/tb-2023-0801 · Cited by 1 · see citing works
Yadav, G., Chauvaux, M., & Duqué, J. (2026) · European Journal of Neuroscience · doi:10.1111/ejn.70489 · Cited by 1 · see citing works
Biagioni, M. C., Gallo, E., Son, A. Y., Sharma, K., Fischer, S., Migdadi, H. A., Agarwal, S., Biller, T., Sills, R., Feigin, A., et al. (2019) · International Journal of Clinical Research & Trials · doi:10.15344/2456-8007/2019/134 · Cited by 1 · see citing works
Fulopova, B. (2015) · UTAS Research Repository · doi:10.25959/23238728
Interference in tactile discrmination performance by neuronal modulation
Jeong, G., Kim, J. S., Ryun, S., & Chung, C. K. (2019) · International Winter Conference on Brain-Computer Interface (BCI) · doi:10.1109/iww-bci.2019.8737347
Interventions for Changing Brain Function in Clinical Disorders
Yuan, M., & Zhu, Q. (2023) · Highlights in Science Engineering and Technology · doi:10.54097/hset.v30i.4958
Neurostimulation Tools and Approaches
Heaton, K. J., Ridgewell, C., Couse, J., & Neumeier, W. H. (2024) · Routledge eBooks · doi:10.4324/9781003378969-9
Luber, B. M., & Wiener, E. (2025) · Advances in neuroethics · doi:10.1007/978-3-031-92401-9_5
Gordon, M. S., Ehrhardt, S. E., Rideaux, R., Bradley, C., Dux, P. E., & Filmer, H. L. (2026) · Cortex · doi:10.1016/j.cortex.2026.05.009
Collins, K. C., Clark, A., Pomeroy, V. M., & Kennedy, N. C. (2026) · Brain Topography · doi:10.1007/s10548-026-01235-1
Metelski, N., & Gordon, A. M. (2026) · Disability and Rehabilitation · doi:10.1080/09638288.2026.2719950
- Authors
- Narayana, S., Zhang, W., Rogers, W., Strickland, C., Franklin, C., Lancaster, J. L., & Fox, P. T.
- Affiliations
- University of Tennessee Health Science Center (US)
- The University of Texas at San Antonio Health Science Center (US)
- Florida State University (US)
- Corresponding author
- Narayana, Shalini
- Venue
- NeuroImage
- Publisher
- Elsevier BV
- Published
- 2014-01
- Volume
- 85
- Pages
- 971-984
- ISSN
- 1053-8119 (ISSN-L)
- PMC
- PMC4331120
- OpenAlex
- W2147932968
- Cited by
- 41
- References
- 91
- Citations by year
- 2026: 5 · 2025: 2 · 2024: 3 · 2023: 6 · 2021: 3 · 2020: 4 · 2019: 5 · 2018: 3 · 2017: 2 · 2016: 1 · 2015: 2 · 2014: 4 · 2013: 1
- FWCI
- 1.49
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- NeuroImage (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Veterans Administration
- National Institute of Deafness and Communication Disorders (R21-DC009467-01A1)
- Topics
- Life Sciences › Neuroscience › Neurology › Transcranial Magnetic Stimulation Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
- Health Sciences › Medicine › Neurology › Neurological disorders and treatments
- Keywords
- transcranial magnetic stimulation, primary motor cortex, motor learning, motor sequence learning, neuroplasticity, resting cerebral blood flow, H215O PET, non-dominant hand, skill transfer, neurorehabilitation, Hebbian learning
- MeSH terms
- Adult, Brain, Female, Humans, Learning, Male, Motor Cortex, Motor Skills, Neuronal Plasticity, Task Performance and Analysis, Positron-Emission Tomography, Transcranial Magnetic Stimulation
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