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

Brain Stimulation

Volumn 1, Issue 4, 2008, Pages 363-369

  Reis, Janine ^a   Robertson, Edwin M ^b   Krakauer, John W ^c   Rothwell, John ^d   Marshall, Lisa ^e   Gerloff, Christian ^f   Wassermann, Eric M ^a   Pascual Leone, Alvaro ^b   Hummel, Friedhelm ^f   Celnik, Pablo A ^g   Classen, Joseph ^h   Floel, Agnes ⁱ   Ziemann, Ulf ^j   Paulus, Walter ^k   Siebner, Hartwig R ^l   Born, Jan ^e   Cohen, Leonardo G ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c Och Spine at New York Presbyterian Hospitals   (United States)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

^e UNIVERSITY OF LÜBECK   (Germany)

^f UNIVERSITY OF HAMBURG   (Germany)

^g JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^h UNIVERSITY OF WÜRZBURG   (Germany)

ⁱ UNIVERSITY OF MÜNSTER   (Germany)

^j GOETHE UNIVERSITY   (Germany)

^k UNIVERSITY OF GÖTTINGEN   (Germany)

^l UNIVERSITY OF KIEL   (Germany)

more..

Author keywords

learning; motor; stroke; transcranial direct current stimulation; transcranial magnetic stimulation

Indexed keywords

ADAPTATION; ASSOCIATIVE MEMORY; BRAIN DEPTH STIMULATION; HUMAN; LONG TERM MEMORY; MEMORY CONSOLIDATION; MENTAL DISEASE; MOTOR CORTEX; MOTOR PERFORMANCE; NEUROLOGIC DISEASE; NEUROMUSCULAR FACILITATION; PRIORITY JOURNAL; REVIEW; STATE DEPENDENT LEARNING; TRANSCRANIAL DIRECT CURRENT STIMULATION; TRANSCRANIAL MAGNETIC STIMULATION; VOLUNTEER; LEARNING; MEMORY; MOTOR ACTIVITY; PHYSIOLOGY; PROCEDURES; PSYCHOMOTOR PERFORMANCE; TRANSCUTANEOUS NERVE STIMULATION;

HUMANS; LEARNING; MEMORY; MOTOR ACTIVITY; PSYCHOMOTOR PERFORMANCE; TRANSCRANIAL MAGNETIC STIMULATION; TRANSCUTANEOUS ELECTRIC NERVE STIMULATION;

EID: 56349151800     PISSN: 1935861X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brs.2008.08.001     Document Type: Review

References (85)

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