Non-invasive brain stimulation (NIBS) and motor recovery after stroke;Neuromodulation corticale non invasive (NIBS) et récupération motrice post-AVC

Annals of Physical and Rehabilitation Medicine

Volumn 57, Issue 8, 2014, Pages 530-542

  Simonetta Moreau, M ^a,b  

^a CHU PURPAN   (France)

^b UNIVERSITÉ PAUL SABATIER   (France)

Author keywords

Brain plasticity; Motor recovery; PAS; RTMS; Stroke; TBS; TDCS

Indexed keywords

BRAIN DEPTH STIMULATION; CEREBROVASCULAR ACCIDENT; ELECTRIC CURRENT; ELECTRODE; ELECTROPHYSIOLOGY; HUMAN; MOTOR CORTEX; MOTOR PERFORMANCE; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY; NERVE STIMULATION; NON INVASIVE BRAIN STIMULATION; PAIRED ASSOCIATIVE STIMULATION; SCALP; SHORT SURVEY; THETA BURST STIMULATION; TRANSCRANIAL DIRECT CURRENT STIMULATION; TRANSCRANIAL MAGNETIC STIMULATION; ADULT; BRAIN; CONVALESCENCE; NEUROREHABILITATION; PATHOPHYSIOLOGY; PROCEDURES; STROKE;

ADULT; BRAIN; HUMANS; MOTOR CORTEX; NEUROLOGICAL REHABILITATION; NEURONAL PLASTICITY; RECOVERY OF FUNCTION; STROKE; TRANSCRANIAL DIRECT CURRENT STIMULATION; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 84911913252     PISSN: 18770657     EISSN: 18770665     Source Type: Journal    
DOI: 10.1016/j.rehab.2014.08.003     Document Type: Short Survey

References (86)

1. Donoghue J.P. Plasticity of adult sensorimotor representations. Curr Opin Neurobiol 1995, 5:749-754.
2. Merzenich M.M., Nelson R.J., Stryker M.P., Cynader M.S., Schoppmann A., Zook J.M. Somatosensory cortical map changes following digit amputation in adult monkeys. J Comp Neurol 1984, 224:591-605.
3. Rossini P.M., Altamura C., Ferreri F., Melgari J.M., Tecchio F., Tombini M., et al. Neuroimaging experimental studies on brain plasticity in recovery from stroke. Eura Medicophys 2007, 43:241-254.
4. Cramer S.C., Nelles G., Benson R.R., Kaplan J.D., Parker R.A., Kwong K.K., et al. A functional MRI study of subjects recovered from hemiparetic stroke. Stroke 1997, 28:2518-2527.
5. Chollet F., DiPiero V., Wise R.J., Brooks D.J., Dolan R.J., Frackowiak R.S. The functional anatomy of motor recovery after stroke in humans: a study with positron emission tomography. Ann Neurol 1991, 29:63-71.
6. Weiller C., Chollet F., Friston K.J., Wise R.J., Frackowiak R.S. Functional reorganization of the brain in recovery from striatocapsular infarction in man. Ann Neurol 1992, 31:463-472.
7. Loubinoux I., Carel C., Pariente J., Dechaumont S., Albucher J.F., Marque P., et al. Correlation between cerebral reorganization and motor recovery after subcortical infarcts. Neuroimage 2003, 20:2166-2180.
8. Tombari D., Loubinoux I., Pariente J., Gerdelat A., Albucher J.F., Tardy J., et al. A longitudinal fMRI study: in recovering and then in clinically stable sub-cortical stroke patients. Neuroimage 2004, 23:827-839.
9. Ward N.S., Cohen L.G. Mechanisms underlying recovery of motor function after stroke. Arch Neurol 2004, 61:1844-1848.
10. Calautti C., Baron J.C. Functional neuroimaging studies of motor recovery after stroke in adults: a review. Stroke 2003, 34:1553-1566.
11. Ward N.S., Brown M.M., Thompson A.J., Frackowiak R.S. Neural correlates of motor recovery after stroke: a longitudinal fMRI study. Brain 2003, 126:2476-2496.
12. Rossini P.M., Tecchio F., Pizzella V., Lupoi D., Cassetta E., Pasqualetti P. Interhemispheric differences of sensory hand areas after monohemispheric stroke: MEG/MRI integrative study. Neuroimage 2001, 14:474-485.
13. Rossini P.M., Tecchio F., Pizzella V., Lupoi D., Cassetta E., Pasqualetti P., et al. On the reorganization of sensory hand areas after mono-hemispheric lesion: a functional (MEG)/anatomical (MRI) integrative study. Brain Res 1998, 26:153-166.
14. Calautti C., Leroy F., Guincestre J.Y., Baron J.C. Displacement of primary sensorimotor cortex activation after subcortical stroke: a longitudinal PET study with clinical correlation. Neuroimage 2003, 19:1650-1654.
15. Calautti C., Naccarato M., Jones P.S., Sharma N., Day D.D., Carpenter A.T., et al. The relationship between motor deficit and hemisphere activation balance after stroke: a 3T fMRI study. Neuroimage 2007, 34:322-331.
16. Werhahn K.J., Conforto A.B., Kadom N., Hallett M., Cohen L.G. Contribution of the ipsilateral motor cortex to recovery after chronic stroke. Ann Neurol 2003, 54:464-472.
17. Johansen-Berg H., Rushworth M.F., Bogdanovic M.D., Kischka U., Wimalaratna S., Matthews P.M. The role of ipsilateral premotor cortex in hand movement after stroke. Proc Natl Acad Sci U S A 2002, 29:14518-14523.
18. Gerloff C., Bushara K., Sailer A., Wassermann E.M., Chen R., Matsuoka T., et al. Multimodal imaging of brain reorganization in motor areas of the contralesional hemisphere of well recovered patients after capsular stroke. Brain 2006, 129:791-808.
19. Lotze M., Markert J., Sauseng P., Hoppe J., Plewnia C., Gerloff C. The role of multiple contralesional motor areas for complex hand movements after internal capsular lesion. J Neurosci 2006, 31:6096-6102.
20. Cicinelli P., Traversa R., Rossini P.M. Post-stroke reorganization of brain motor output to the hand: a 2-4 month follow-up with focal magnetic transcranial stimulation. Electroencephalogr Clin Neurophysiol 1997, 105:438-450.
21. Traversa R., Cicinelli P., Pasqualetti P., Filippi M., Rossini P.M. Follow-up of interhemispheric differences of motor evoked potentials from the "affected" and "unaffected" hemispheres in human stroke. Brain Res 1998, 24803:1-8.
22. Manganotti P., Acler M., Zanette G.P., Smania N., Fiaschi A. Motor cortical disinhibition during early and late recovery after stroke. Neurorehabil Neural Repair 2008, 22:396-403.
23. Kujirai T., Caramia M.D., Rothwell J.C., Day B.L., Thompson P.D., Ferbert A., et al. Corticocortical inhibition in human motor cortex. J Physiol 1993, 471:501-519.
24. Butefisch C.M., Wessling M., Netz J., Seitz R.J., Homberg V. Relationship between interhemispheric inhibition and motor cortex excitability in subacute stroke patients. Neurorehabil Neural Repair 2008, 22:4-21.
25. Cicinelli P., Pasqualetti P., Zaccagnini M., Traversa R., Oliveri M., Rossini P.M. Interhemispheric asymmetries of motor cortex excitability in the postacute stroke stage: a paired-pulse transcranial magnetic stimulation study. Stroke 2003, 34:2653-2658.
26. Liepert J., Storch P., Fritsch A., Weiller C. Motor cortex disinhibition in acute stroke. Clin Neurophysiol 2000, 111:671-676.
27. Manganotti P., Patuzzo S., Cortese F., Palermo A., Smania N., Fiaschi A. Motor disinhibition in affected and unaffected hemisphere in the early period of recovery after stroke. Clin Neurophysiol 2002, 113:936-943.
28. Swayne O.B., Rothwell J.C., Ward N.S., Greenwood R.J. Stages of motor output reorganization after hemispheric stroke suggested by longitudinal studies of cortical physiology. Cereb Cortex 2008, 18:1909-1922.
29. Ferbert A., Priori A., Rothwell J.C., Day B.L., Colebatch J.G., Marsden C.D. Interhemispheric inhibition of the human motor cortex. J Physiol 1992, 453:525-546.
30. Gerloff C., Cohen L.G., Floeter M.K., Chen R., Corwell B., Hallett M. Inhibitory influence of the ipsilateral motor cortex on responses to stimulation of the human cortex and pyramidal tract. J Physiol 1998, 510:249-259.
31. Daskalakis Z.J., Christensen B.K., Fitzgerald P.B., Roshan L., Chen R. The mechanisms of interhemispheric inhibition in the human motor cortex. J Physiol 2002, 543:317-326.
32. Duque J., Murase N., Celnik P., Hummel F., Harris-Love M., Mazzocchio R., et al. Intermanual differences in movement-related interhemispheric inhibition. J Cogn Neurosci 2007, 19:204-213.
33. Duque J., Hummel F., Celnik P., Murase N., Mazzocchio R., Cohen L.G. Transcallosal inhibition in chronic subcortical stroke. Neuroimage 2005, 28:940-946.
34. Murase N., Duque J., Mazzocchio R., Cohen L.G. Influence of interhemispheric interactions on motor function in chronic stroke. Ann Neurol 2004, 55:400-409.
35. Nowak D.A., Grefkes C., Ameli M., Fink G.R. Interhemispheric competition after stroke: brain stimulation to enhance recovery of function of the affected hand. Neurorehabil Neural Repair 2009, 23:641-656.
36. Pascual-Leone A., Tormos J.M., Keenan J., Tarazona F., Canete C., Catala M.D. Study and modulation of human cortical excitability with transcranial magnetic stimulation. J Clin Neurophysiol 1998, 15:333-343.
37. 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, 48:1398-1403.
38. Maeda F., Keenan J.P., Tormos J.M., Topka H., Pascual-Leone A. Modulation of corticospinal excitability by repetitive transcranial magnetic stimulation. Clin Neurophysiol 2000, 111:800-805.
39. Huang Y.Z., Edwards M.J., Rounis E., Bhatia K.P., Rothwell J.C. Theta burst stimulation of the human motor cortex. Neuron 2005, 45:201-206.
40. Buonomano D.V., Merzenich M.M. Cortical plasticity: from synapses to maps. Annu Rev Neurosci 1998, 21:149-186.
41. Baumer T., Lange R., Liepert J., Weiller C., Siebner H.R., Rothwell J.C., et al. Repeated premotor rTMS leads to cumulative plastic changes of motor cortex excitability in humans. Neuroimage 2003, 20:550-560.
42. Valero-Cabre A., Pascual-Leone A., Rushmore R.J. Cumulative sessions of repetitive transcranial magnetic stimulation (rTMS) build-up facilitation to subsequent TMS-mediated behavioural disruptions. Eur J Neurosci 2008, 27:765-774.
43. Lefaucheur J.P., Andre-Obadia N., Poulet E., Devanne H., Haffen E., Londero A., et al. [French guidelines on the use of repetitive transcranial magnetic stimulation (rTMS): safety and therapeutic indications]. Neurophysiol Clin 2011, 41:221-295.
44. 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. Electroencephalogr Clin Neurophysiol 1998, 108:1-16.
45. Nitsche M.A., Paulus W. Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J Physiol 2000, 15:633-639.
46. Nitsche M.A., Paulus W. Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology 2001, 27:1899-1901.
47. Fritsch B., Reis J., Martinowich K., Schambra H.M., Ji Y., Cohen L.G., et al. Direct current stimulation promotes BDNF-dependent synaptic plasticity: potential implications for motor learning. Neuron 2010, 66:198-204.
48. Poreisz C., Boros K., Antal A., Paulus W. Safety aspects of transcranial direct current stimulation concerning healthy subjects and patients. Brain Res Bull 2007, 72:208-214.
49. Ridding M.C., Uy J. Changes in motor cortical excitability induced by paired associative stimulation. Clin Neurophysiol 2003, 114:1437-1444.
50. Stefan K., Kunesch E., Cohen L.G., Benecke R., Classen J. Induction of plasticity in the human motor cortex by paired associative stimulation. Brain 2000, 3:572-584.
51. Ridding M.C., Taylor J.L. Mechanisms of motor-evoked potential facilitation following prolonged dual peripheral and central stimulation in humans. J Physiol 2001, 537:623-631.
52. Uy J., Ridding M.C., Hillier S., Thompson P.D., Miles T.S. Does induction of plastic change in motor cortex improve leg function after stroke?. Neurology 2003, 61:982-984.
53. Castel-Lacanal E., Marque P., Tardy J., de Boissezon X., Guiraud V., Chollet F., et al. Induction of cortical plastic changes in wrist muscles by paired associative stimulation in the recovery phase of stroke patients. Neurorehabil Neural Repair 2009, 23:366-372.
54. Takeuchi N., Chuma T., Matsuo Y., Watanabe I., Ikoma K. Repetitive transcranial magnetic stimulation of contralesional primary motor cortex improves hand function after stroke. Stroke 2005, 36:2681-2686.
55. Nowak D.A., Grefkes C., Dafotakis M., Eickhoff S., Kust J., Karbe H., et al. Effects of low-frequency repetitive transcranial magnetic stimulation of the contralesional primary motor cortex on movement kinematics and neural activity in subcortical stroke. Arch Neurol 2008, 65:741-747.
56. Conchou F., Loubinoux I., Castel-Lacanal E., Le Tinnier A., Gerdelat-Mas A., Faure-Marie N., et al. Neural substrates of low-frequency repetitive transcranial magnetic stimulation during movement in healthy subjects and acute stroke patients. A PET study. Hum Brain Mapp 2008.
57. Di Lazzaro V., Pilato F., Dileone M., Profice P., Capone F., Ranieri F., et al. Modulating cortical excitability in acute stroke: a repetitive TMS study. Clin Neurophysiol 2008, 119:715-723.
58. 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, 25:123-129.
59. Fregni F., Boggio P.S., Valle A.C., Rocha R.R., Duarte J., Ferreira M.J., et al. A sham-controlled trial of a 5-day course of repetitive transcranial magnetic stimulation of the unaffected hemisphere in stroke patients. Stroke 2006.
60. Liepert J., Zittel S., Weiller C. Improvement of dexterity by single session low-frequency repetitive transcranial magnetic stimulation over the contralesional motor cortex in acute stroke: a double-blind placebo-controlled crossover trial. Restor Neurol Neurosci 2007, 25:461-465.
61. Conforto A.B., Anjos S.M., Saposnik G., Mello E.A., Nagaya E.M., Santos W., et al. Transcranial magnetic stimulation in mild to severe hemiparesis early after stroke: a proof of principle and novel approach to improve motor function. J Neurol 2012, 259:1399-1405.
62. Kim Y.H., You S.H., Ko M.H., Park J.W., Lee K.H., Jang S.H., et al. Repetitive transcranial magnetic stimulation-induced corticomotor excitability and associated motor skill acquisition in chronic stroke. Stroke 2006, 37:1471-1476.
63. Fregni F., Boggio P.S., Valle A.C., Rocha R.R., Duarte J., Ferreira M.J., et al. A sham-controlled trial of a 5-day course of repetitive transcranial magnetic stimulation of the unaffected hemisphere in stroke patients. Stroke 2006, 37:2115-2122.
64. Hummel F.C., Voller B., Celnik P., Floel A., Giraux P., Gerloff C., et al. Effects of brain polarization on reaction times and pinch force in chronic stroke. BMC Neurosci 2006, 7:73.
65. Talelli P., Greenwood R.J., Rothwell J.C. Exploring theta burst stimulation as an intervention to improve motor recovery in chronic stroke. Clin Neurophysiol 2007, 118:333-342.
66. Ameli M., Grefkes C., Kemper F., Riegg F.P., Rehme A.K., Karbe H., et al. Differential effects of high-frequency repetitive transcranial magnetic stimulation over ipsilesional primary motor cortex in cortical and subcortical middle cerebral artery stroke. Ann Neurol 2009, 66:298-309.
67. Hesse S., Werner C., Schonhardt E.M., Bardeleben A., Jenrich W., Kirker S.G. Combined transcranial direct current stimulation and robot-assisted arm training in subacute stroke patients: a pilot study. Restor Neurol Neurosci 2007, 25:9-15.
68. 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, 86:707-715.
69. Talelli P., Wallace A., Dileone M., Hoad D., Cheeran B., Oliver R., et al. Theta burst stimulation in the rehabilitation of the upper limb: a semirandomized, placebo-controlled trial in chronic stroke patients. Neurorehabil Neural Repair 2012, 26:976-987.
70. Rossi C., Sallustio F., Di Legge S., Stanzione P., Koch G. Transcranial direct current stimulation of the affected hemisphere does not accelerate recovery of acute stroke patients. Eur J Neurol 2012, 20:202-204.
71. Grefkes C., Fink G.R. Disruption of motor network connectivity post-stroke and its noninvasive neuromodulation. Curr Opin Neurol 2012, 25:670-675.
72. Kandel M., Beis J.M., Le Chapelain L., Guesdon H., Paysant J. Non-invasive cerebral stimulation for the upper limb rehabilitation after stroke: a review. Ann Phys Rehabil Med 2012, 55:657-680.
73. Hsu W.Y., Cheng C.H., Liao K.K., Lee I.H., Lin Y.Y. Effects of repetitive transcranial magnetic stimulation on motor functions in patients with stroke: a meta-analysis. Stroke 2012, 43:1849-1857.
74. Emara T.H., Moustafa R.R., Elnahas N.M., Elganzoury A.M., Abdo T.A., Mohamed S.A., et al. Repetitive transcranial magnetic stimulation at 1Hz and 5Hz produces sustained improvement in motor function and disability after ischaemic stroke. Eur J Neurol 2010, 17:1203-1209.
75. Khedr E.M., Abdel-Fadeil M.R., Farghali A., Qaid M. Role of 1 and 3Hz repetitive transcranial magnetic stimulation on motor function recovery after acute ischaemic stroke. Eur J Neurol 2009, 16:1323-1330.
76. Sasaki N., Mizutani S., Kakuda W., Abo M. Comparison of the effects of high- and low-frequency repetitive transcranial magnetic stimulation on upper limb hemiparesis in the early phase of stroke. J Stroke Cerebrovasc Dis 2011, 22:413-418.
77. Kim D.Y., Lim J.Y., Kang E.K., You D.S., Oh M.K., Oh B.M., et al. Effect of transcranial direct current stimulation on motor recovery in patients with subacute stroke. Am J Phys Med Rehabil 2010, 89:879-886.
78. Lindenberg R., Zhu L.L., Schlaug G. Combined central and peripheral stimulation to facilitate motor recovery after stroke: the effect of number of sessions on outcome. Neurorehabil Neural Repair 2012, 26:479-483.
79. Bolognini N., Pascual-Leone A., Fregni F. Using non-invasive brain stimulation to augment motor training-induced plasticity. J Neuroeng Rehabil 2009, 6:8.
80. Celnik P., Paik N.J., Vandermeeren Y., Dimyan M., Cohen L.G. Effects of combined peripheral nerve stimulation and brain polarization on performance of a motor sequence task after chronic stroke. Stroke 2009, 40:1764-1771.
81. Hiscock A., Miller S., Rothwell J., Tallis R.C., Pomeroy V.M. Informing dose-finding studies of repetitive transcranial magnetic stimulation to enhance motor function: a qualitative systematic review. Neurorehabil Neural Repair 2008, 22:228-249.
82. Mahmoudi H., Borhani Haghighi A., Petramfar P., Jahanshahi S., Salehi Z., Fregni F. Transcranial direct current stimulation: electrode montage in stroke. Disabil Rehabil 2011, 33:1383-1388.
83. 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 2013, 6:343.
84. Zimerman M., Heise K.F., Hoppe J., Cohen L.G., Gerloff C., Hummel F.C. Modulation of training by single-session transcranial direct current stimulation to the intact motor cortex enhances motor skill acquisition of the paretic hand. Stroke 2012, 43:2185-2191.
85. Stinear C.M., Barber P.A., Smale P.R., Coxon J.P., Fleming M.K., Byblow W.D. Functional potential in chronic stroke patients depends on corticospinal tract integrity. Brain 2007, 130:170-180.
86. Stinear C.M., Barber P.A., Petoe M., Anwar S., Byblow W.D. The PREP algorithm predicts potential for upper limb recovery after stroke. Brain 2012, 135:2527-2535.