BRAIN STIMULATION: Basic, Translational, and Clinical Research in Neuromodulation
Volume 1, Issue 4 , Pages 363-369 , October 2008

Consensus: Can transcranial direct current stimulation and transcranial magnetic stimulation enhance motor learning and memory formation?

  • Janine Reis, MD

      Affiliations

    • Human Cortical Physiology Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland
    • ,
  • Edwin M. Robertson, MD, D. Phil

      Affiliations

    • Berenson-Allen Center for Noninvasive Brain Stimulation, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts
    • ,
  • John W. Krakauer, MD

      Affiliations

    • Motor Performance Laboratory, Dept. of Neurology, Columbia University, New York, New York
    • ,
  • John Rothwell, PhD

      Affiliations

    • Institute of Neurology, Queen Square, London, United Kingdom
    • ,
  • Lisa Marshall, PhD

      Affiliations

    • Department of Neurology and Clinical Neuroendocrinology, University of Lübeck, Lübeck, Germany
    • ,
  • Christian Gerloff, MD

      Affiliations

    • Department of Neurology, University of Hamburg, Hamburg, Germany
    • ,
  • Eric M. Wassermann, MD

      Affiliations

    • Brain Stimulation Unit, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland
    • ,
  • Alvaro Pascual-Leone, MD, PhD

      Affiliations

    • Berenson-Allen Center for Noninvasive Brain Stimulation, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts
    • ,
  • Friedhelm Hummel, MD

      Affiliations

    • Department of Neurology, University of Hamburg, Hamburg, Germany
    • ,
  • Pablo A. Celnik, MD

      Affiliations

    • Department of Physical Medicine and Rehabilitation, Johns Hopkins University, Baltimore, Maryland
    • ,
  • Joseph Classen, MD

      Affiliations

    • Human Cortical Physiology and Motor Control Laboratory, Department of Neurology, University of Würzburg, Würzburg, Germany
    • ,
  • Agnes Floel, MD

      Affiliations

    • Department of Neurology, University of Münster and IZKF Münster, Münster, Germany
    • ,
  • Ulf Ziemann, MD

      Affiliations

    • Department of Neurology, Goethe-University of Frankfurt, Frankfurt, Germany
    • ,
  • Walter Paulus, MD

      Affiliations

    • Department of Clinical Neurophysiology, University of Goettingen, Goettingen, Germany
    • ,
  • Hartwig R. Siebner, MD, PhD

      Affiliations

    • Brain mapping laboratory, Department of Neurology, Christian-Albrechts University, Kiel, Germany
    • ,
  • Jan Born, PhD

      Affiliations

    • Department of Neurology and Clinical Neuroendocrinology, University of Lübeck, Lübeck, Germany
    • ,
  • Leonardo G. Cohen, MD

      Affiliations

    • Human Cortical Physiology Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland
    • Corresponding Author InformationCorrespondence: Leonardo G. Cohen, Human Cortical Physiology Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health 10 Center Drive, Bethesda, MD 20892-1430.

Received 5 June 2008 ,Revised 29 July 2008 ,Accepted 2 August 2008.

References 

  1. Jahanshahi M, Rothwell J. Transcranial magnetic stimulation studies of cognition: an emerging field. Exp Brain Res. 2000;131:1–9
  2. Butefisch CM, Khurana V, Kopylev L, Cohen LG. Enhancing encoding of a motor memory in the primary motor cortex by cortical stimulation. J Neurophysiol. 2004;91:2110–2116
  3. Duque J, Mazzocchio R, Stefan K, et al. Memory formation in the motor cortex ipsilateral to a training hand. Cereb Cortex. 2008;18:1395–1406
  4. Hummel F, Celnik P, Giraux P, et al. Effects of non-invasive cortical stimulation on skilled motor function in chronic stroke. Brain. 2005;128(Pt 3):490–499
  5. Pascual-Leone A, Valls-Sole J, Wassermann EM, Hallett M. Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex. Brain. 1994;117(Pt 4):847–858
  6. Wassermann EM. Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the Safety of Repetitive Transcranial Magnetic Stimulation, June 5-7, 1996. Electroencephalogr Clin Neurophysiol. 1998;108:1–16
  7. Flöel A, Rösser N, Michka O, et al. Noninvasive brain stimulation improves language learning. J Cogn Neurosci. 2008;20:1415–1422
  8. Robertson E, Press D, Pascual-Leone A. Off-line learning and the primary motor cortex. J Neurosci. 2005;25:6372–6378
  9. Marshall L, Helgadóttir H, Mölle M, Born J. Boosting slow oscillations during sleep potentiates memory. Nature. 2006;444:610–613
  10. Chen R, Classen J, Gerloff C, et al. Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology. 1997;48:1398–1403
  11. Nitsche MA, Liebetanz D, Tergau F, Paulus W. [Modulation of cortical excitability by transcranial direct current stimulation]. [German] Nervenarzt. 2002;73:332–335
  12. Bestmann S, Baudewig J, Siebner HR, et al. Subthreshold high-frequency TMS of human primary motor cortex modulates interconnected frontal motor areas as detected by interleaved fMRI-TMS. Neuroimage. 2003;20:1685–1696
  13. Muellbacher W, Ziemann U, Wissel J, et al. Early consolidation in human primary motor cortex. Nature. 2002;415:640–644
  14. Miniussi C, Cappa SF, Cohen L, et al. Efficacy of repetitive transcranial magnetic stimulation/transcranial direct current stimulation in cognitive neurorehabilitation. Brain Stimulation. 2008;1:326–336
  15. Cohen LG, Celnik P, Pascual-Leone A, et al. Functional relevance of cross-modal plasticity in blind humans. Nature. 1997;389:180–183
  16. Siebner HR, Rothwell J. Transcranial magnetic stimulation: new insights into representational cortical plasticity. Exp Brain Res. 2003;148:1–16
  17. Squire LR. Memory systems of the brain: a brief history and current perspective. Neurobiol Learn Mem. 2004;82:171–177
  18. Dudai Y. The neurobiology of consolidations, or, how stable is the engram?. Annu Rev Psychol. 2004;55:51–86
  19. Karni A, Meyer G, Rey-Hipolito C, et al. The acquisition of skilled motor performance: fast and slow experience-driven changes in primary motor cortex. Proc Natl Acad Sci U S A. 1998;95:861–868
  20. Walker MP, Brakefield T, Morgan A, et al. Practice with sleep makes perfect: sleep-dependent motor skill learning. Neuron. 2002;35:205–211
  21. Shadmehr R, Krakauer J. A computational neuroanatomy for motor control. Exp Brain Res. 2008;185:359–381
  22. Izawa J, Rane T, Donchin O, Shadmehr R. Motor adaptation as a process of reoptimization. J Neurosci. 2008;28:2883–2891
  23. Fernández-Ruiz J, Díaz R. Prism adaptation and aftereffect: specifying the properties of a procedural memory system. Learn Mem. 1999;6:47–53
  24. Baraduc P, Lang N, Rothwell JC, Wolpert DM. Consolidation of dynamic motor learning is not disrupted by rTMS of primary motor cortex. Curr Biol. 2004;14:252–256
  25. Kitazawa S, Kimura T, Uka T. Prism adaptation of reaching movements: specificity for the velocity of reaching. J Neurosci. 1997;17:1481–1492
  26. Hund-Georgiadis M, von Cramon DY. Motor-learning-related changes in piano players and non-musicians revealed by functional magnetic-resonance signals. Exp Brain Res. 1999;125:417–425
  27. Memmert D. Long-term effects of type of practice on the learning and transfer of a complex motor skill. Percept Mot Skills. 2006;103:912–916
  28. Karni A, Sagi D. The time course of learning a visual skill. Nature. 1993;365:250–252
  29. StickgoldSleep-dependent memory consolidation R. Nature. 2005;437:1272–1278
  30. Walker M, Brakefield T, Seidman J, et al. Sleep and the time course of motor skill learning. Learn Mem. 2003;10:275–284
  31. Gais S, Albouy G, Boly M, et al. Sleep transforms the cerebral trace of declarative memories. Proc Natl Acad Sci U S A. 2007;104:18778–18783
  32. Marshall L, Born J. The contribution of sleep to hippocampus-dependent memory consolidation. Trends Cogn Sci. 2007;11:442–450
  33. Fischer S, Hallschmid M, Elsner AL, Born J. Sleep forms memory for finger skills. Proc Natl Acad Sci U S A. 2002;99:11987–11991
  34. Robertson EM, Pascual-Leone A, Press DZ. Awareness modifies the skill-learning benefits of sleep. Curr Biol. 2004;14:208–212
  35. Brown RM, Robertson EM. Off-line processing: reciprocal interactions between declarative and procedural memories. J Neurosci. 2007;27:10468–10475
  36. Krakauer JW, Ghez C, Ghilardi MF. Adaptation to visuomotor transformations: consolidation, interference, and forgetting. J Neurosci. 2005;25:473–478
  37. Huber R, Ghilardi MF, Massimini M, Tononi G. Local sleep and learning. Nature. 2004;430:78–81
  38. Robertson EM, Pascual-Leone A, Miall RC. Current concepts in procedural consolidation. Nat Rev Neurosci. 2004;5:576–582
  39. Goedert KM, Willingham DB. Patterns of interference in sequence learning and prism adaptation inconsistent with the consolidation hypothesis. Learn Mem. 2002;9:279–292
  40. Brashers-Krug T, Shadmehr R, Bizzi E. Consolidation in human motor memory. Nature. 1996;382:252–255
  41. Shadmehr R, Brashers-Krug T. Functional stages in the formation of human long-term motor memory. J Neurosci. 1997;17:409–419
  42. Korman M, Doyon J, Doljansky J, et al. Daytime sleep condenses the time course of motor memory consolidation. Nat Neurosci. 2007;10:1206–1213
  43. Walker MP, Brakefield T, Hobson JA, Stickgold R. Dissociable stages of human memory consolidation and reconsolidation. Nature. 2003;425:616–620
  44. Wright DL, Black CB, Immink MA, et al. Long-term motor programming improvements occur via concatenation of movement sequences during random but not during blocked practice. J Mot Behav. 2004;36:39–50
  45. Immink MA, Wright DL. Motor programming during practice conditions high and low in contextual interference. J Exp Psychol Hum Percept Perform. 2001;27:423–437
  46. Ungerleider LG, Doyon J, Karni A. Imaging brain plasticity during motor skill learning. Neurobiol Learn Mem. 2002;78:553–564
  47. Nezafat R, Shadmehr R, Holcomb HH. Long-term adaptation to dynamics of reaching movements: a PET study. Exp Brain Res. 2001;140:66–76
  48. Grafton ST, Hazeltine E, Ivry RB. Abstract and effector-specific representations of motor sequences identified with PET. J Neurosci. 1998;18:9420–9428
  49. Honda M, Deiber MP, Ibanez V, et al. Dynamic cortical involvement in implicit and explicit motor sequence learning: a PET study. Brain. 1998;121:2159–2173
  50. Classen J, Liepert J, Wise SP, et al. Rapid plasticity of human cortical movement representation induced by practice. J Neurophysiol. 1998;79:1117–1123
  51. Tong C, Flanagan JR. Task-specific internal models for kinematic transformations. J Neurophysiol. 2003;90:578–585
  52. Hadipour-Niktarash A, Lee CK, Desmond JE, Shadmehr R. Impairment of retention but not acquisition of a visuomotor skill through time-dependent disruption of primary motor cortex. J Neurosci. 2007;27:13413–13419
  53. Richardson AG, Overduin SA, Valero-Cabré A, et al. Disruption of primary motor cortex before learning impairs memory of movement dynamics. J Neurosci. 2006;26:12466–12470
  54. Pascual-Leone A, Grafman J, Hallett M. Modulation of cortical motor output maps during development of implicit and explicit knowledge. Science. 1994;263:1287–1289
  55. Robertson EM, Press DZ, Pascual-Leone A. Off-line learning and the primary motor cortex. J Neurosci. 2005;25:6372–6378
  56. Nissen M, Bullemer P. Attentional requirements of learning: evidence from performance measures. Cognit Psychol. 1987;19:1–32
  57. Plautz EJ, Milliken GW, Nudo RJ. Effects of repetitive motor training on movement representations in adult squirrel monkeys: role of use versus learning. Neurobiol Learn Mem. 2000;74:27–55
  58. Nudo RJ, Milliken GW, Jenkins WM, Merzenich MM. Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys. J.Neurosci. 1996;16:785–807
  59. Duque J, Murase N, Celnik P, et al. Intermanual Differences in movement-related interhemispheric inhibition. J Cogn Neurosci. 2007;19:204–213
  60. Reis J, Swayne OB, Vandermeeren Y, et al. Contribution of transcranial magnetic stimulation to the understanding of cortical mechanisms involved in motor control. J Physiol. 2008;586:325–351
  61. Ward NS, Cohen LG. Mechanisms underlying recovery of motor function after stroke. Arch. Neurol. 2004;61:1844–1848
  62. Avanzino L, Teo JT, Rothwell JC. Intracortical circuits modulate transcallosal inhibition in humans. J Physiol. 2007;583:99–114
  63. Perez MA, Cohen LG. Mechanisms underlying functional changes in the primary motor cortex ipsilateral to an active hand. J Neurosci. 2008;28:5631–5640
  64. Kobayashi M, Hutchinson S, Théoret H, et al. Repetitive TMS of the motor cortex improves ipsilateral sequential simple finger movements. Neurology. 2004;62:91–98
  65. Schambra HM, Sawaki L, Cohen LG. Modulation of excitability of human motor cortex (M1) by 1 Hz transcranial magnetic stimulation of the contralateral M1. Clin Neurophysiol. 2003;114:130–133
  66. Plewnia C, Lotze M, Gerloff C. Disinhibition of the contralateral motor cortex by low-frequency rTMS. Neuroreport. 2003;14:609–612
  67. Wassermann EM, Wedegaertner FR, Ziemann U, et al. Crossed reduction of human motor cortex excitability by 1-Hz transcranial magnetic stimulation. Neurosci Lett. 1998;250:141–144
  68. Gilio F, Rizzo V, Siebner HR, Rothwell JC. Effects on the right motor hand-area excitability produced by low-frequency rTMS over human contralateral homologous cortex. J Physiol. 2003;551:563–573
  69. Daskalakis ZJ, Paradiso GO, Christensen BK, et al. Exploring the connectivity between the cerebellum and motor cortex in humans. J Physiol. 2004;557:689–700
  70. Koch G, Franca M, Mochizuki H, et al. Interactions between pairs of transcranial magnetic stimuli over the human left dorsal premotor cortex differ from those seen in primary motor cortex. J Physiol. 2007;578:551–562
  71. Di Lazzaro V, Ziemann U, Lemon RN. State of the art: Physiology of transcranial motor cortex stimulation. Brain Stimulation. 2008;1:345–362
  72. Nitsche MA, Paulus W. Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology. 2001;57:1899–1901
  73. Kim YH, Park JW, Ko MH, et al. Facilitative effect of high frequency subthreshold repetitive transcranial magnetic stimulation on complex sequential motor learning in humans. Neurosci Lett. 2004;367:181–185
  74. Vines BW, Nair DG, Schlaug G. Contralateral and ipsilateral motor effects after transcranial direct current stimulation. Neuroreport. 2006;17:671–674
  75. Antal A, Nitsche M, Kincses T, et al. Facilitation of visuo-motor learning by transcranial direct current stimulation of the motor and extrastriate visual areas in humans. Eur J Neurosci. 2004;19:2888–2892
  76. Nitsche M, Schauenburg A, Lang N, et al. Facilitation of implicit motor learning by weak transcranial direct current stimulation of the primary motor cortex in the human. J Cogn Neurosci. 2003;15:619–626
  77. Jebsen RH, Taylor N, Trieschmann RB, et al. An objective and standardized test of hand function. Arch Phys Med Rehabil. 1969;50:311–319
  78. Boggio P, Castro L, Savagim E, et al. Enhancement of non-dominant hand motor function by anodal transcranial direct current stimulation. Neurosci Lett. 2006;404:232–236
  79. Agostino R, Iezzi E, Dinapoli L, et al. Effects of 5 Hz subthreshold magnetic stimulation of primary motor cortex on fast finger movements in normal subjects. Exp Brain Res. 2007;180:105–111
  80. Carey JR, Fregni F, Pascual-Leone A. rTMS combined with motor learning training in healthy subjects. Restor Neurol Neurosci. 2006;24:191–199
  81. Siebner HR, Lang N, Rizzo V, et al. Preconditioning of low-frequency repetitive transcranial magnetic stimulation with transcranial direct current stimulation: evidence for homeostatic plasticity in the human motor cortex. J Neurosci. 2004;24:3379–3385
  82. Silvanto J, Muggleton NG, Cowey A, Walsh V. Neural activation state determines behavioral susceptibility to modified theta burst transcranial magnetic stimulation. Eur J Neurosci. 2007;26:523–528
  83. Ziemann US, Siebner HR. Modifying motor learning through gating and homeostatic metaplasticity. Brain Stimulation. 2008;1:60–66
  84. Ziemann U, Ilic TV, Jung P. Long-term potentiation (LTP)-like plasticity and learning in human motor cortex—investigations with transcranial magnetic stimulation (TMS). Suppl Clin Neurophysiol. 2006;59:19–25
  85. Gentner R, Wankerl K, Reinsberger C, et al. Depression of human corticospinal excitability induced by magnetic theta-burst stimulation: evidence of rapid polarity-reversing metaplasticity. Cereb Cortex. 2008;18:2046–2053

 Funding provided by the National Institutes of Health.

PII: S1935-861X(08)00325-2

doi: 10.1016/j.brs.2008.08.001

BRAIN STIMULATION: Basic, Translational, and Clinical Research in Neuromodulation
Volume 1, Issue 4 , Pages 363-369 , October 2008

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