Concurrent TMS to the primary motor cortex augments slow motor learning

NeuroImage

Volumn 85, Issue , 2014, Pages 971-984

  Narayana, Shalini ^a,b,c   Zhang, Wei ^c   Rogers, William ^c   Strickland, Casey ^d   Franklin, Crystal ^c   Lancaster, Jack L ^c   Fox, Peter T ^c,e  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^b LE BONHEUR CHILDREN S HOSPITAL   (United States)

^c UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^d FLORIDA STATE UNIVERSITY   (United States)

^e VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Digit sequence practice; Hebbian learning; Hyperbolic function; Motor learning; Motor learning network; Motor system; Primary motor cortex; Skill transfer; TMS

Indexed keywords

ACCURACY; ADULT; BEHAVIOR CHANGE; BRAIN BLOOD FLOW; BRAIN FUNCTION; BRAIN REGION; CEREBELLUM; CINGULATE GYRUS; CLINICAL EFFECTIVENESS; CONTROLLED STUDY; FEMALE; FLOW RATE; HEARING IMPAIRMENT; HIPPOCAMPUS; HUMAN; HUMAN EXPERIMENT; IMAGE ANALYSIS; LEARNING; MALE; MOTOR LEARNING; MOTOR PERFORMANCE; NEUROIMAGING; OUTCOME ASSESSMENT; POSITRON EMISSION TOMOGRAPHY; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; PUTAMEN; REVIEW; SENSITIVITY ANALYSIS; STIMULUS RESPONSE; TASK PERFORMANCE; TOOTH DISEASE; TRANSCRANIAL MAGNETIC STIMULATION;

DIGIT SEQUENCE PRACTICE; HEBBIAN LEARNING; HYPERBOLIC FUNCTION; MOTOR LEARNING; MOTOR LEARNING NETWORK; MOTOR SYSTEM; PRIMARY MOTOR CORTEX; SKILL TRANSFER; TMS;

ADULT; BRAIN; FEMALE; HUMANS; LEARNING; MALE; MOTOR CORTEX; MOTOR SKILLS; NEURONAL PLASTICITY; POSITRON-EMISSION TOMOGRAPHY; TASK PERFORMANCE AND ANALYSIS; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 84889686807     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2013.07.024     Document Type: Review

References (88)

1. Adkins-Muir D.L., Jones T.A. Cortical electrical stimulation combined with rehabilitative training: enhanced functional recovery and dendritic plasticity following focal cortical ischemia in rats. Neurol. Res. 2003, 25(8):780-788.
2. Agostino R., Iezzi E., Dinapoli L., Gilio F., Conte A., Mari F., Berardelli A. Effects of 5Hz subthreshold magnetic stimulation of primary motor cortex on fast finger movements in normal subjects. Exp. Brain Res. 2007, 180(1):105-111.
3. Albouy G., Sterpenich V., Balteau E., Vandewalle G., Desseilles M., ng-Vu T., et al. Both the hippocampus and striatum are involved in consolidation of motor sequence memory. Neuron 2008, 58:261-272.
4. Barker A.T., Jalinous R., Freeston I.L. Non-invasive magnetic stimulation of the human motor cortex. Lancet 1985, 1:1106-1107.
5. Boggio P.S., Nunes A., Rigonatti S.P., Nitsche M.A., Pascual-Leone A., Fregni F. Repeated sessions of noninvasive brain DC stimulation is associated with motor function improvement in stroke patients. Restor. Neurol. Neurosci. 2007, 25(2):123-129.
6. Boutin A., Badets A., Salesse R.N., Fries U., Panzer S., Blandin Y. Practice makes transfer of motor skills imperfect. Psychol. Res. 2012, 76(5):611-625.
7. Boutin A., Panzer S., Salesse R.N., Blandin Y. Testing promotes effector transfer. Acta Psychol. (Amst.) 2012, 141(3):400-407.
8. Boyd L.A., Linsdell M.A. Excitatory repetitive transcranial magnetic stimulation to left dorsal premotor cortex enhances motor consolidation of new skills. BMC Neurosci. 2009, 10:72.
9. Bütefisch C.M., Davis B.C., Wise S.P., Sawaki L., Kopylev L., Classen J., Cohen L.G. Mechanisms of use-dependent plasticity in the human motor cortex. Proc. Natl. Acad. Sci. U. S. A. 2000, 97(7):3661-3665.
10. Bütefisch C.M., Khurana V., Kopylev L., Cohen L.G. Enhancing encoding of a motor memory in the primary motor cortex by cortical stimulation. J. Neurophysiol. 2004, 91(5):2110-2116.
11. Chang W.H., Kim Y.H., Bang O.Y., Kim S.T., Park Y.H., Lee P.K. Long-term effects of rTMS on motor recovery in patients after subacute stroke. J. Rehabil. Med. 2010, 42(8):758-764.
12. Chang W.H., Kim Y.H., Yoo W.K., Goo K.H., Park C.H., Kim S.T., Pascual-Leone A. rTMS with motor training modulates cortico-basal ganglia-thalamocortical circuits in stroke patients. Restor. Neurol. Neurosci. 2012, 30(3):179-189.
13. Chen R., Classen J., Gerloff C., Celnik P., Wassermann E.M., Hallett M., et al. Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology 1997, 48(5):1398-1403.
14. Cramer S.C., Weisskoff R.M., Schaechter J.D., Nelles G., Foley M., Finklestein S.P., et al. Motor cortex activation is related to force of squeezing. Hum. Brain Mapp. 2002, 16(4):197-205.
15. DeCoteau W.E., Thorn C., Gibson D.J., Courtemanche R., Mitra P., Kubota Y., et al. Learning-related coordination of striatal and hippocampal theta rhythms during acquisition of a procedural maze task. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:5644-5649.
16. Doyon J., Benali H. Reorganization and plasticity in the adult brain during learning of motor skills. Curr. Opin. Neurobiol. 2005, 15(2):161-167.
17. Doyon J., Bellec P., Amsel R., Penhune V., Monchi O., Carrier J., et al. Contributions of the basal ganglia and functionally related brain structures to motor learning. Behav. Brain Res. 2009, 199(1):61-75.
18. Duff E., Xiong J., Wang B., Cunnington R., Fox P., Egan G. Complex spatio-temporal dynamics of fMRI BOLD: a study of motor learning. NeuroImage 2007, 34(1):156-168.
19. Duff E.P., Johnston L.A., Xiong J., Fox P.T., Mareels I., Egan G.F. The power of spectral density analysis for mapping endogenous BOLD signal fluctuations. Hum. Brain Mapp. 2008, 29(7):778-790.
20. 15O tissue activity. J. Nucl. Med. 1989, 30:141-149.
21. Fox P.T., Raichle M.E. Stimulus rate dependence of regional cerebral blood flow in human striatal cortex, demonstrated by positron emission tomography. J. Neurophysiol. 1984, 51(5):1109-1120.
22. Fox P.T., Mintun M.A., Reiman E.M., Raichle M.E. Enhanced detection of focal brain responses using intersubject averaging and change-distribution analysis of subtracted PET images. J. Cereb. Blood Flow Metab. 1988, 8:642-653.
23. Fox P.T., Ingham R.J., Ingham J.C., Zamarripa F., Xiong J.H., Lancaster J.L. Brain correlates of stuttering and syllable production. a PET performance-correlation analysis. Brain 2000, 123(Pt 10):1985-2004.
24. Fox P.T., Narayana S., Tandon N., Sandoval H., Fox S.P., Kochunov P., et al. Column-based model of electric field excitation of cerebral cortex. Hum. Brain Mapp. 2004, 22(1):1-14.
25. Fox P.T., Narayana S., Tandon N., Fox S.P., Sandoval H., Kochunov P., et al. Intensity modulation of TMS induced cortical excitation: primary motor cortex. Hum. Brain Mapp. 2006, 27(6):478-487.
26. Geerdink Y., Aarts P., Geurts A.C. Motor learning curve and long-term effectiveness of modified constraint-induced movement therapy in children with unilateral cerebral palsy: a randomized controlled trial. Res. Dev. Disabil. 2013, 34(3):923-931.
27. Gentner R., Gorges S., Weise D., Aufm Kampe K., Buttmann M., Classen J. Encoding of motor skill in the corticomuscular system of musicians. Curr. Biol. 2010, 20(20):1869-1874.
28. Grafton S.T., Woods R.P., Mazziotta J.C., Phelps M.E. Somatotopic mapping of the primary motor cortex in humans: activation studies with cerebral blood flow and positron emission tomography. J. Neurophysiol. 1992, 66(3):735-743.
29. Grafton S.T., Hazeltine E., Ivry R.B. Motor sequence learning with the nondominant left hand. A PET functional imaging study. Exp. Brain Res. 2002, 146(3):369-378.
30. Hebb D.O. Physiological learning theory. J. Abnorm. Child Psychol. 1976, 4(4):309-314.
31. Hlustík P., Solodkin A., Noll D.C., Small S.L. Cortical plasticity during three-week motor skill learning. J. Clin. Neurophysiol. 2004, 21(3):180-191.
32. Hosp J.A., Pekanovic A., Rioult-Pedotti M.S., Luft A.R. Dopaminergic projections from midbrain to primary motor cortex mediate motor skill learning. J. Neurosci. 2011, 31(7):2481-2487. (16).
33. Jung P., Ziemann U. Homeostatic and nonhomeostatic modulation of learning in human motor cortex. J. Neurosci. 2009, 29(17):5597-5604.
34. Karni A., Meyer G., Jezzard P., Adams M.M., Turner R., Ungerleider L.G. Functional MRI evidence for adult motor cortex plasticity during motor skill learning. Nature 1995, 377(6545):155-158.
35. Karni A., Meyer G., Rey-Hipolito C., Jezzard P., Adams M.M., Turner R., et al. The acquisition of skilled motor performance: fast and slow experience-driven changes in primary motor cortex. PNAS 1998, 95:250-252.
36. Khedr E.M., Ahmed M.A., Fathy N., Rothwell J.C. Therapeutic trial of repetitive transcranial magnetic stimulation after acute ischemic stroke. Neurology 2005, 65(3):466-468.
37. Kim Y.H., Park J.W., Ko M.H., Jang S.H., Lee P.K. Facilitative effect of high frequency subthreshold repetitive transcranial magnetic stimulation on complex sequential motor learning in humans. Neurosci. Lett. 2004, 367(2):181-185.
38. Kim Y.H., You S.H., Ko M.H., Park J.W., Lee K.H., Jang S.H., Yoo W.K., Hallett M. Repetitive transcranial magnetic stimulation-induced corticomotor excitability and associated motor skill acquisition in chronic stroke. Stroke 2006, 37(6):1471-1476.
39. Kleim J.A., Jones T.A. Principles of experience-dependent neural plasticity: implications for rehabilitation after brain damage. J. Speech Lang. Hear. Res. 2008, 51(1):S225-S239.
40. Kleim J.A., Bruneau R., VandenBerg P., MacDonald E., Mulrooney R., Pocock D. Motor cortex stimulation enhances motor recovery and reduces peri-infarct dysfunction following ischemic insult. Neurol. Res. 2003, 25(8):789-793.
41. Kleim J.A., Hogg T.M., VandenBerg P.M., Cooper N.R., Bruneau R., Remple M. Cortical synaptogenesis and motor map reorganization occur during late, but not early, phase of motor skill learning. J. Neurosci. 2004, 24(3):628-633.
42. Korman M., Raz N., Flash T., Karni A. Multiple shifts in the representation of a motor sequence during the acquisition of skilled performance. Proc. Natl. Acad. Sci. U. S. A. 2003, 100(21):12492-12497.
43. Lancaster J.L., Glass T.G., Lankipalli B.R., Downs H., Mayberg H.S., Fox P.T. A modality-independent approach to spatial normalization of tomographic images of the human brain. Hum. Brain Mapp. 1995, 3:209-223.
44. Lancaster J.L., Rainey L.H., Summerlin J.L., Freitas C.S., Fox P.T., Evans A.C., et al. Automated labeling of the human brain: a preliminary report on the development and evaluation of a forward-transform method. Hum. Brain Mapp. 1997, 5:238-242.
45. Lancaster J.L., Narayana S., Wenzel D., Luckemeyer J., Roby J., Fox P.T. Evaluation of an image-guided robotically-positioned transcranial magnetic stimulation system. Hum. Brain Mapp. 2004, 22(4):329-340.
46. Lefebvre S., Laloux P., Peeters A., Desfontaines P., Jamart J., Vandermeeren Y. Dual-tDCS enhances online motor skill learning and long-term retention in chronic stroke patients. Front. Hum. Neurosci. 2012, 6:343.
47. Ma L., Wang B., Narayana S., Hazeltine E., Chen X., Robin D.A., et al. Changes in regional activity are accompanied with changes in inter-regional connectivity during 4weeks motor learning. Brain Res. 2010, 1318C:64-76.
48. Ma L., Narayana S., Robin D.A., Fox P.T., Xiong J. Changes occur in resting state network of motor system during 4weeks of motor skill learning. NeuroImage 2011, 58(1):226-233.
49. Malcolm M.P., Triggs W.J., Light K.E., Gonzalez Rothi L.J., Wu S., Reid K., et al. Repetitive transcranial magnetic stimulation as an adjunct to constraint induced therapy: an exploratory randomized controlled trial. Am. J. Phys. Med. Rehabil. 2007, 86(9):707-715.
50. Mazur J.E., Hastie R. Learning as accumulation: a reexamination of the learning curve. Psychol. Bull. 1978, 85(6):1256-1274.
51. Mintun M.A., Fox P.T., Raichle M.E. A highly accurate method of localizing regions of neuronal activation in the human brain with positron emission tomography. J. Cereb. Blood Flow Metab. 1989, 9(1):96-103.
52. Newell K.M., Liu Y.T., Mayer-Kress G. Time scales in motor learning and development. Psychol. Rev. 2001, 108(1):57-82.
53. Oldfield R.C. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1971, 9(1):97-113.
54. Orban P., Peigneux P., Lungu O., Debas K., Barakat M., Bellec P., et al. Functional neuroanatomy associated with the expression of distinct movement kinematics in motor sequence learning. Neuroscience 2011, 179:94-103.
55. Pascual-Leone A., Nguyet D., Cohen L.G., Brasil-Neto J.P., Cammarota A., Hallett M. Modulation of muscle responses evoked by transcranial magnetic stimulation during the acquisition of new fine motor skills. J. Neurophysiol. 1995, 74(3):1037-1045.
56. Pascual-Leone A., Tormos J.M., Keenan J., Tarazona F., Cañete C., Catalá M.D. Study and modulation of human cortical excitability with transcranial magnetic stimulation. J. Clin. Neurophysiol. 1998, 15(4):333-343.
57. Pascual-Leone A., Tarazona F., Catalá M.D. Applications of transcranial magnetic stimulation in studies on motor learning. Electroencephalogr. Clin. Neurophysiol. Suppl. 1999, 51:157-161.
58. Peinemann A., Reimer B., Löer C., Quartarone A., Münchau A., Conrad B., Siebner H.R. Long-lasting increase in corticospinal excitability after 1800 pulses of subthreshold 5Hz repetitive TMS to the primary motor cortex. Clin. Neurophysiol. 2004, 115(7):1519-1526.
59. Pendt L.K., Reuter I., Müller H. Motor skill learning, retention, and control deficits in Parkinson's disease. PLoS One 2011, 6(7):e21669.
60. Penhune V.B., Steele C.J. Parallel contributions of cerebellar, striatal and M1 mechanisms to motor sequence learning. Behav. Brain Res. 2012, 226(2):579-591.
61. Platz T., Roschka S., Christel M.I., Duecker F., Rothwell J.C., Sack A. Early stages of motor skill learning and the specific relevance of the cortical motor system - a combined behavioural training and theta burst TMS study. Restor. Neurol. Neurosci. 2012, 30(3):199-211.
62. Platz T., Roschka S., Doppl K., Roth C., Lotze M., Sack A.T., et al. Prolonged motor skill learning - a combined behavioural training and theta burst TMS study. Restor. Neurol. Neurosci. 2012, 30(3):213-224.
63. Polanía R., Paulus W., Nitsche M.A. Reorganizing the intrinsic functional architecture of the human primary motor cortex during rest with non-invasive cortical stimulation. PLoS One 2012, 7(1):e30971.
64. Poldrack R.A. Imaging brain plasticity: conceptual and methodological issues - a theoretical review. NeuroImage 2000, 12(1):1-13.
65. Quartarone A., Bagnato S., Rizzo V., Morgante F., Sant'angelo A., Battaglia F., et al. Distinct changes in cortical and spinal excitability following high-frequency repetitive TMS to the human motor cortex. Exp. Brain Res. 2005, 161(1):114-124.
66. Rábago C.A., Lancaster J.L., Narayana S., Zhang W., Fox P.T. Automated-parameterization of the motor evoked potential and cortical silent period induced by transcranial magnetic stimulation. Clin. Neurophysiol. 2009, 120(8):1577-1587.
67. Ragert P., Dinse H.R., Pleger B., Wilimzig C., Frombach E., Schwenkreis P., et al. Combination of 5Hz repetitive transcranial magnetic stimulation (rTMS) and tactile coactivation boosts tactile discrimination in humans. Neurosci. Lett. 2003, 348(2):105-108.
68. Reis J., Schambra H.M., Cohen L.G., Buch E.R., Fritsch B., Zarahn E., et al. Noninvasive cortical stimulation enhances motor skill acquisition over multiple days through an effect on consolidation. Proc. Natl. Acad. Sci. U. S. A. 2009, 106(5):1590-1595.
69. Ridding M.C., Rothwell J.C. Is there a future for therapeutic use of transcranial magnetic stimulation?. Nat. Rev. Neurosci. 2007, 8(7):559-567.
70. Rioult-Pedotti M.S., Friedman D., Hess G., Donoghue J.P. Strengthening of horizontal cortical connections following skill learning. Nat. Neurosci. 1998, 1(3):230-234.
71. Rogers W., Zhang W., Narayana S., Lancaster J.L., Robin D.A., Fox P.T. Force sensing system for automated assessment of motor performance during fMRI. J. Neurosci. Methods 2010, 190(1):92-94.
72. Rossi S., Hallett M., Rossini P.M., Pascual-Leone A., Safety of TMS Consensus Group Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin. Neurophysiol. 2009, 120(12):2008-2039.
73. Rossini P.M., Barker A.T., Berardelli A., Caramia M.D., Caruso G., Cracco R.Q., et al. Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. Electroencephalogr. Clin. Neurophysiol. 1994, 91(2):79-92.
74. Salinas F.S., Szabó C.Á., Zhang W., Jones L., Leland M.M., Wey H.Y., Duong T.Q., Fox P.T., Narayana S. Functional neuroimaging of the baboon during concurrent image-guided transcranial magnetic stimulation. NeuroImage 2011, 57(4):1393-1401.
75. Salinas F.S., Narayana S., Zhang W., Fox P.T., Szabó C.Á. Repetitive transcranial magnetic stimulation elicits rate dependent brain network responses in non human primates. Brain Stimul 2013, (Epub ahead of print). 10.1016/j.brs.2013.03.002.
76. Schendan H.E., Searl M.M., Melrose R.J., Stern C.E. An fMRI study of the role of the medial temporal lobe in implicit and explicit sequence learning. Neuron 2003, 37:1013-1025.
77. Seidler R.D., Noll D.C. Neuroanatomical correlates of motor acquisition and motor transfer. J. Neurophysiol. 2008, 99(4):1836-1845.
78. Siebner H.R., Rothwell J. Transcranial magnetic stimulation: new insights into representational cortical plasticity. Exp. Brain Res. 2003, 148(1):1-16.
79. Siebner H.R., Peller M., Willoch F., Minoshima S., Boecker H., Auer C., et al. Lasting cortical activation after repetitive TMS of the motor cortex: a glucose metabolic study. Neurology 2000, 54(4):956-963.
80. Siebner H.R., Takano B., Peinemann A., Schwaiger M., Conrad B., Drzezga A. Continuous transcranial magnetic stimulation during positron emission tomography: a suitable tool for imaging regional excitability of the human cortex. NeuroImage 2001, 14(4):883-890.
81. Slotema C.W., Blom J.D., Hoek H.W., Sommer I.E. Should we expand the toolbox of psychiatric treatment methods to include repetitive transcranial magnetic stimulation (rTMS)? A meta-analysis of the efficacy of rTMS in psychiatric disorders. J. Clin. Psychiatry 2010, 71(7):873-884.
82. Smith S.M., Jenkinson M., Woolrich M.W., Beckmann C.F., Behrens T.E., Johansen-Berg H., et al. Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage 2004, 23(Suppl. 1):S208-S219.
83. Talairach J., Tournoux P. Co-planar Stereotaxic Atlas of the Human Brain 1988, Thieme Medical Publishers, NY.
84. Ungerleider L.G., Doyon J., Karni A. Imaging brain plasticity during motor skill learning. Neurobiol. Learn. Mem. 2002, 78(3):553-564. (Nov).
85. Wassermannn 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. 1998, 108(1):1-16.
86. Xiong J., Ma L., Wang B., Narayana S., Duff E.P., Egan G.F., et al. Long-term motor training induced changes in regional cerebral blood flow in both task and resting states. NeuroImage 2009, 45(1):75-82.
87. Yoo W.K., You S.H., Ko M.H., Tae Kim S., Park C.H., Park J.W., Hoon Ohn S., Hallett M., Kim Y.H. High frequency rTMS modulation of the sensorimotor networks: behavioral changes and fMRI correlates. NeuroImage 2008, 39(4):1886-1889.
88. Ziemann U., Ilić T.V., Pauli C., Meintzschel F., Ruge D. Learning modifies subsequent induction of long-term potentiation-like and long-term depression-like plasticity in human motor cortex. J. Neurosci. 2004, 24(7):1666-1672.