Stimulation targeting higher motor areas in stroke rehabilitation: A proof-of-concept, randomized, double-blinded placebo-controlled study of effectiveness and underlying mechanisms

Restorative Neurology and Neuroscience

Volumn 33, Issue 6, 2015, Pages 911-926

  Cunningham, David A ^a,b   Varnerin, Nicole ^a   Machado, Andre ^a   Bonnett, Corin ^a   Janini, Daniel ^a   Roelle, Sarah ^a   Potter Baker, Kelsey ^a   Sankarasubramanian, Vishwanath ^a   Wang, Xiaofeng ^a   Yue, Guang ^c   Plow, Ela B ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b KENT STATE UNIVERSITY   (United States)

^c KESSLER FOUNDATION   (United States)

Author keywords

constraint induced movement therapy; motor recovery; premotor cortex; Stroke rehabilitation; transcranial direct current stimulation; transcranial magnetic stimulation

Indexed keywords

ADULT; AGED; ARTICLE; BRAIN ANALYSIS; BRAIN DAMAGE; BRAIN HEMORRHAGE; BRAIN ISCHEMIA; BRAIN MAPPING; CAREGIVER SUPPORT; CHRONIC DISEASE; CLINICAL ARTICLE; CLINICAL EFFECTIVENESS; CONSTRAINT INDUCED THERAPY; CONTROLLED STUDY; DAILY LIFE ACTIVITY; DISEASE SEVERITY; DOUBLE BLIND PROCEDURE; EXCITABILITY; FATIGUE; FEMALE; FUNCTIONAL STATUS ASSESSMENT; HEMISPHERE; HUMAN; IMAGING SOFTWARE; MALE; MIDDLE AGED; MOTOR ACTIVITY; MOTOR DYSFUNCTION ASSESSMENT; MOTOR PERFORMANCE; MULTICHANNEL RECORDER; NERVE STIMULATOR; NEUROPHYSIOLOGY; PREMOTOR CORTEX; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; SCORING SYSTEM; SUPPLEMENTARY MOTOR AREA; TRANSCRANIAL DIRECT CURRENT STIMULATION; TRANSCRANIAL MAGNETIC STIMULATOR; TREATMENT DURATION; TREATMENT RESPONSE; CONVALESCENCE; HEMISPHERIC DOMINANCE; MOTOR CORTEX; MUSCULOSKELETAL MANIPULATION; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PILOT STUDY; PROCEDURES; PROGNOSIS; STROKE; STROKE REHABILITATION; TRANSCRANIAL MAGNETIC STIMULATION; TREATMENT OUTCOME;

AGED; DOUBLE-BLIND METHOD; FEMALE; FUNCTIONAL LATERALITY; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; MOTOR CORTEX; MOTOR SKILLS; MUSCULOSKELETAL MANIPULATIONS; PILOT PROJECTS; PROGNOSIS; RECOVERY OF FUNCTION; STROKE; STROKE REHABILITATION; TRANSCRANIAL DIRECT CURRENT STIMULATION; TRANSCRANIAL MAGNETIC STIMULATION; TREATMENT OUTCOME;

EID: 84947602403     PISSN: 09226028     EISSN: 18783627     Source Type: Journal    
DOI: 10.3233/RNN-150574     Document Type: Article

References (90)

1. Avanzino L, Bassolino M, Pozzo T, Bove M, 2011 Use-dependent hemispheric balance. J Neurosci 31 9 3423 3428
2. Avanzino L, Teo JT, Rothwell JC, 2007 Intracortical circuits modulate transcallosal inhibition in humans. J Physiol 583 Pt 1 99 114
3. Biernaskie J, Szymanska A, Windle V, Corbett D, 2005 Bi-hemispheric contribution to functional motor recovery of the affected forelimb following focal ischemic brain injury in rats. Eur J Neurosci 21 4 989 999
4. Bolognini N, Pascual-Leone A, Fregni F, 2009 Using non-invasive brain stimulation to augment motor training-induced plasticity. J Neuroeng Rehabil 6 8
5. Bolognini N, Vallar G, Casati C, Latif LA, El-Nazer R, Williams J, 2011 Neurophysiological and behavioral effects of tDCS combined with constraint-induced movement therapy in poststroke patients. Neurorehabil Neural Repair 25 9 819 829
6. Boros K, Poreisz C, Munchau A, Paulus W, Nitsche MA, 2008 Premotor transcranial direct current stimulation (tDCS) affects primary motor excitability in humans. Eur J Neurosci 27 5 1292 1300
7. Bradnam LV, Stinear CM, Barber PA, Byblow WD, 2012 Contralesional hemisphere control of the proximal paretic upper limb following stroke. Cereb Cortex 22 11 2662 2671
8. Bradnam LV, Stinear CM, Byblow WD, 2013 Ipsilateral motor pathways after stroke: Implications for non-invasive brain stimulation. Front Hum Neurosci 7 184
9. Broeks JG, Lankhorst GJ, Rumping K, Prevo AJ, 1999 The long-term outcome of arm function after stroke: Results of a follow-up study. Disabil Rehabil 21 8 357 364
10. Burke Quinlan E, Dodakian L, See J, McKenzie A, Le V, Wojnowicz M, 2015 Neural function, injury, and stroke subtype predict treatment gains after stroke. Ann Neurol 77 1 132 145
11. Carey JR, Evans CD, Anderson DC, Plow [nee(Bhatt)] E, Nagpal A, Kimberley TJ, 2008 Safety of 6-Hz primed low-frequency rTMS in stroke. Neurorehabil Neural Repair 22 2 185 192
12. Carey JR, Kimberley TJ, Lewis SM, Auerbach EJ, Dorsey L, Rundquist P, 2002 Analysis of fMRI and finger tracking training in subjects with chronic stroke. Brain 125 Pt 4 773 788
13. Chen R, Yung D, Li JY, 2003 Organization of ipsilateral excitatory and inhibitory pathways in the human motor cortex. J Neurophysiol 89 3 1256 1264
14. Cramer SC, Nelles G, Benson RR, Kaplan JD, Parker RA, Kwong KK, 1997 A functional MRI study of subjects recovered from hemiparetic stroke. Stroke 28 12 2518 2527
15. Cunningham DA, Machado A, Janini D, Varnerin N, Bonnett C, Yue G, 2014 The Assessment of Inter-Hemispheric Imbalance using Imaging and Non-Invasive Brain Stimulation in Patients with Chronic Stroke. Arch Phys Med Rehabil 96 4 Suppl S94 S103
16. Dancause N, Nudo RJ, 2011 Shaping plasticity to enhance recovery after injury. Prog Brain Res 192 273 295
17. Di Lazzaro V, Dileone M, Capone F, Pellegrino G, Ranieri F, Musumeci G, 2014 Immediate and late modulation of interhemipheric imbalance with bilateral transcranial direct current stimulation in acute stroke. Brain Stimul 7 6 841 848
18. Di Lazzaro V, Ranieri F, Profice P, Pilato F, Mazzone P, Capone F, 2013 Transcranial direct current stimulation effects on the excitability of corticospinal axons of the human cerebral cortex. Brain Stimul 6 4 641 643
19. Di Pino G, Pellegrino G, Assenza G, Capone F, Ferreri F, Formica D, 2014 Modulation of brain plasticity in stroke: A novel model for neurorehabilitation. Nat Rev Neurol
20. Dum RP, Strick PL, 1991 The origin of corticospinal projections from the premotor areas in the frontal lobe. J Neurosci 11 3 667 689
21. Fregni F, Pascual-Leone A, 2007 Technology insight: Noninvasive brain stimulation in neurology-perspectives on the therapeutic potential of rTMS and tDCS. Nat Clin Pract Neurol 3 7 383 393
22. Fridman EA, Hanakawa T, Chung M, Hummel F, Leiguarda RC, Cohen LG, 2004 Reorganization of the human ipsilesional premotor cortex after stroke. Brain 127 Pt 4 747 758
23. Gacs G, Fox AJ, Barnett HJ, Vinuela F, 1983 Occurrence and mechanisms of occlusion of the anterior cerebral artery. Stroke 14 6 952 959
24. Gandiga PC, Hummel FC, Cohen LG, 2006 Transcranial DC stimulation (tDCS): A tool for double-blind sham-controlled clinical studies in brain stimulation. Clin Neurophysiol 117 4 845 850
25. Halko MA, Datta A, Plow EB, Scaturro J, Bikson M, Merabet LB, 2011 Neuroplastic changes following rehabilitative training correlate with regional electrical field induced with tDCS. Neuroimage 57 3 885 891
26. Harris-Love ML, Morton SM, Perez MA, Cohen LG, 2011 Mechanisms of short-term training-induced reaching improvement in severely hemiparetic stroke patients: A TMS study. Neurorehabil Neural Repair 25 5 398 411
27. Harris JE, Eng JJ, Miller WC, Dawson AS, 2010 The role of caregiver involvement in upper-limb treatment in individuals with subacute stroke. Phys Ther 90 9 1302 1310
28. Harvey RL, Winstein CJ, Everest TrialG, 2009 Design for the everest randomized trial of cortical stimulation and rehabilitation for arm function following stroke. Neurorehabil Neural Repair 23 1 32 44
29. Hesse S, Waldner A, Mehrholz J, Tomelleri C, Pohl M, Werner C, 2011 Combined transcranial direct current stimulation and robot-Assisted arm training in subacute stroke patients: An exploratory, randomized multicenter trial. Neurorehabil Neural Repair 25 9 838 846
30. Hummel FC, Cohen LG, 2006a Non-invasive brain stimulation. Lancet Neurol 5 8 708 712
31. Hummel FC, Cohen LG, 2006b Non-invasive brain stimulation: A new strategy to improve neurorehabilitation after stroke? Lancet Neurol 5 8 708 712
32. Johansen-Berg H, Dawes H, Guy C, Smith SM, Wade DT, Matthews PM, 2002 Correlation between motor improvements and altered fMRI activity after rehabilitative therapy. Brain 125 Pt 12 2731 2742
33. Johansen-Berg H, Rushworth MF, Bogdanovic MD, Kischka U, Wimalaratna S, Matthews PM, 2002 The role of ipsilateral premotor cortex in hand movement after stroke. Proc Natl Acad Sci U S A 99 22 14518 14523
34. Kalenine S, Buxbaum LJ, Coslett HB, 2010 Critical brain regions for action recognition: Lesion symptom mapping in left hemisphere stroke. Brain 133 11 3269 3280
35. Kang SY, Kim JS, 2008 Anterior cerebral artery infarction: Stroke mechanism and clinical-imaging study in 100 patients. Neurology 70 24 Pt 2 2386 2393
36. Kim DY, Lim JY, Kang EK, You DS, Oh MK, Oh BM, 2010 Effect of transcranial direct current stimulation on motor recovery in patients with subacute stroke. Am J Phys Med Rehabil 89 11 879 886
37. Kitago T, Liang J, Huang VS, Hayes S, Simon P, Tenteromano L, 2013 Improvement after constraint-induced movement therapy: Recovery of normal motor control or task-specific compensation? Neurorehabil Neural Repair 27 2 99 109
38. Levy R, Ruland S, Weinand M, Lowry D, Dafer R, Bakay R, 2008 Cortical stimulation for the rehabilitation of patients with hemiparetic stroke: A multicenter feasibility study of safety and efficacy. J Neurosurg 108 4 707 714
39. Levy RM, Harvey RL, Kissela BM, Winstein CJ, Lutsep HL, Parrish TB, 2015 Epidural electrical stimulation for stroke rehabilitation: Results of the prospective, multicenter, randomized, single-blinded everest trial. Neurorehabil Neural Repair. (Epub ahead of Print)
40. Lindenberg R, Renga V, Zhu LL, Nair D, Schlaug G, 2010 Bihemispheric brain stimulation facilitates motor recovery in chronic stroke patients. Neurology 75 24 2176 2184
41. Lindenberg R, Zhu LL, Schlaug G, 2012 Combined central and peripheral stimulation to facilitate motor recovery after stroke: The effect of number of sessions on outcome. Neurorehabil Neural Repair 26 5 479 483
42. Liu Y, Rouiller EM, 1999 Mechanisms of recovery of dexterity following unilateral lesion of the sensorimotor cortex in adult monkeys. Exp Brain Res 128 1-2 149 159
43. Machado AG, Shoji A, Ballester G Jr, Marino R, 2003 Mapping of the rat's motor area after hemispherectomy: The hemispheres as potentially independent motor brains. Epilepsia 44 4 500 506
44. Malcolm MP, Triggs WJ, Light KE, Gonzalez Rothi LJ, Wu S, Reid K, 2007 Repetitive transcranial magnetic stimulation as an adjunct to constraint-induced therapy: An exploratory randomized controlled trial. Am J Phys Med Rehabil 86 9 707 715
45. Marconi B, Genovesio A, Giannetti S, Molinari M, Caminiti R, 2003 Callosal connections of dorso-lateral premotor cortex. Eur J Neurosci 18 4 775 788
46. Marshall RS, Perera GM, Lazar RM, Krakauer JW, Constantine RC, DeLaPaz RL, 2000 Evolution of cortical activation during recovery from corticospinal tract infarction. Stroke 31 3 656 661
47. Murase N, Duque J, Mazzocchio R, Cohen LG, 2004 Influence of interhemispheric interactions on motor function in chronic stroke. Ann Neurol 55 3 400 409
48. Nair DG, Renga V, Lindenberg R, Zhu L, Schlaug G, 2011 Optimizing recovery potential through simultaneous occupational therapy and non-invasive brain-stimulation using tDCS. Restor Neurol Neurosci 29 6 411 420
49. Netz J, Lammers T, Homberg V, 1997 Reorganization of motor output in the non-Affected hemisphere after stroke. Brain 120 Pt 9 1579 1586
50. Nitsche MA, Cohen LG, Wassermann EM, Priori A, Lang N, Antal A, 2008 Transcranial direct current stimulation: State of the art. Brain Stimul 1 3 206 223
51. Nitsche MA, Jakoubkova M, Thirugnanasambandam N, Schmalfuss L, Hullemann S, Sonka K, 2010 Contribution of the premotor cortex to consolidation of motor sequence learning in humans during slee. J Neurophysiol 104 5 2603 2614
52. Nouri S, Cramer SC, 2011 Anatomy and physiology predict response to motor cortex stimulation after stroke. Neurology 77 11 1076 1083
53. Nowak DA, Grefkes C, Ameli M, Fink GR, 2009 Interhemispheric competition after stroke: Brain stimulation to enhance recovery of function of the affected hand. Neurorehabil Neural Repair 23 7 641 656
54. O'Shea J, Johansen-Berg H, Trief D, Gobel S, Rushworth MF, 2007 Functionally specific reorganization in human premotor cortex. Neuron 54 3 479 490
55. Page SJ, Fulk GD, Boyne P, 2012 Clinically important differences for the upper-extremity Fugl-Meyer Scale in people with minimal to moderate impairment due to chronic stroke. Phys Ther 92 6 791 798
56. Page SJ, Levine P, Leonard A, Szaflarski JP, Kissela BM, 2008 Modified constraint-induced therapy in chronic stroke: Results of a single-blinded randomized controlled trial. Phys Ther 88 3 333 340
57. Pavlova E, Kuo MF, Nitsche MA, Borg J, 2014 Transcranial direct current stimulation of the premotor cortex: Effects on hand dexterity. Brain Res 1576 52 62
58. Plautz EJ, Barbay S, Frost SB, Friel KM, Dancause N, Zoubina EV, 2003 Post-infarct cortical plasticity and behavioral recovery using concurrent cortical stimulation and rehabilitative training: A feasibility study in primates. Neurol Res 25 8 801 810
59. Plow (Bhatt) E, Nagpal A, Greer KH, Grunewald TK, Steele JL, Wiemiller JW, 2007 Effect of finger tracking combined with electrical stimulation on brain reorganization and hand function in subjects with stroke. Exp Brain Res 182 4 435 447
60. Plow Bhatt E, Nagpal A, Greer KH, Grunewald TK, Steele JL, Wiemiller JW, 2007 Effect of finger tracking combined with electrical stimulation on brain reorganization and hand function in subjects with stroke. Exp Brain Res 182 4 435 447
61. Plow EB, Carey JR, Nudo RJ, Pascual-Leone A, 2009 Invasive cortical stimulation to promote recovery of function after stroke. Stroke 40 5 1926 1931
62. Plow EB, Cunningham DA, Beall E, Jones S, Wyant A, Bonnett C, 2013 Effectiveness and neural mechanisms associated with tDCS delivered to premotor cortex in stroke rehabilitation: Study protocol for a randomized controlled trial. Trials 14 331
63. Plow EB, Cunningham DA, Varnerin N, Machado A, 2014 Rethinking Stimulation of the Brain in Stroke Rehabilitation: Why Higher Motor Areas Might Be Better Alternatives for Patients with Greater Impairments. Neuroscientist 21 3 225 240
64. Plow EB, Machado A, 2014 Invasive Neurostimulation in Stroke Rehabilitation. Neurotherapeutics 11 3 572 582
65. Plow EB, Obretenova SN, Fregni F, Pascual-Leone A, Merabet LB, 2012a Comparison of Visual Field Training for Hemianopia With Active Versus Sham Transcranial Direct Cortical Stimulation. Neurorehabil Neural Repair 26 6 616 626
66. Plow EB, Obretenova SN, Fregni F, Pascual-Leone A, Merabet LB, 2012b Comparison of visual field training for hemianopia with active versus sham transcranial direct cortical stimulation. Neurorehabil Neural Repair 26 6 616 626
67. Plow EB, Obretenova SN, Halko MA, Kenkel S, Jackson ML, Pascual-Leone A, 2011 Combining visual rehabilitative training and noninvasive brain stimulation to enhance visual function in patients with hemianopia: A comparative case study. PM R 3 9 825 835
68. Plow EB, Obretenova SN, Jackson ML, Merabet LB, 2012 Temporal Profile of Functional Visual Rehabilitative Outcomes Modulated by Transcranial Direct Current Stimulation. Neuromodulation 15 4 367 373
69. Ramsey NF, Jansma JM, Jager G, Van Raalten T, Kahn RS, 2004 Neurophysiological factors in human information processing capacity. Brain 127 Pt 3 517 525
70. Rossi C, Sallustio F, Di Legge S, Stanzione P, Koch G, 2013 Transcranial direct current stimulation of the affected hemisphere does not accelerate recovery of acute stroke patients. Eur J Neurol 20 1 202 204
71. Rossi S, Hallett M, Rossini PM, Pascual-Leone A, 2009 Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol 120 12 2008 2039
72. Rouiller EM, Babalian A, Kazennikov O, Moret V, Yu XH, Wiesendanger M, 1994 Transcallosal connections of the distal forelimb representations of the primary and supplementary motor cortical areas in macaque monkeys. Exp Brain Res 102 2 227 243
73. Schubotz RI, von Cramon DY, 2003 Functional-Anatomical concepts of human premotor cortex: Evidence from fMRI and PET studies. Neuroimage 20 Suppl 1 S120 S131
74. Seniow J, Bilik M, Lesniak M, Waldowski K, Iwanski S, Czlonkowska A, 2012 Transcranial magnetic stimulation combined with physiotherapy in rehabilitation of poststroke hemiparesis: A randomized, double-blind, placebo-controlled study. Neurorehabil Neural Repair 26 9 1072 1079
75. Siebner HR, Rothwell J, 2003 Transcranial magnetic stimulation: New insights into representational cortical plasticity. Exp Brain Res 148 1 1 16
76. Stinear CM, Barber PA, Smale PR, Coxon JP, Fleming MK, Byblow WD, 2007 Functional potential in chronic stroke patients depends on corticospinal tract integrity. Brain 130 Pt 1 170 180
77. Sung WH, Wang CP, Chou CL, Chen YC, Chang YC, Tsai PY, 2013 Efficacy of coupling inhibitory and facilitatory repetitive transcranial magnetic stimulation to enhance motor recovery in hemiplegic stroke patients. Stroke 44 5 1375 1382
78. Takeuchi N, Tada T, Chuma T, Matsuo Y, Ikoma K, 2007 Disinhibition of the premotor cortex contributes to a maladaptive change in the affected hand after stroke. Stroke 38 5 1551 1556
79. Talelli P, Wallace A, Dileone M, Hoad D, Cheeran B, Oliver R, 2012 Theta burst stimulation in the rehabilitation of the upper limb: A semirandomized, placebo-controlled trial in chronic stroke patients. Neurorehabil Neural Repair 26 8 976 987
80. Taub E, Uswatte G, Morris DM, 2003 Improved motor recovery after stroke and massive cortical reorganization following Constraint-Induced Movement therapy. Phys Med Rehabil Clin N Am 14 1 Suppl S77 S91. ix
81. van der Lee JH, Beckerman H, Knol DL, de Vet HC, Bouter LM, 2004 Clinimetric properties of the motor activity log for the assessment of arm use in hemiparetic patients. Stroke 35 6 1410 1414
82. Ward N, 2011 Assessment of cortical reorganisation for hand function after stroke. J Physiol 589 Pt 23 5625 5632
83. Ward NS, Brown MM, Thompson AJ, Frackowiak RS, 2003a Neural correlates of motor recovery after stroke: A longitudinal fMRI study. Brain 126 Pt 11 2476 2496
84. Ward NS, Brown MM, Thompson AJ, Frackowiak RS, 2003b Neural correlates of outcome after stroke: A cross-sectional fMRI study. Brain 126 Pt 6 1430 1448
85. Ward NS, Newton JM, Swayne OB, Lee L, Frackowiak RS, Thompson AJ, 2007 The relationship between brain activity and peak grip force is modulated by corticospinal system integrity after subcortical stroke. Eur J Neurosci 25 6 1865 1873
86. Woodbury ML, Velozo CA, Richards LG, Duncan PW, 2013 Rasch analysis staging methodology to classify upper extremity movement impairment after stroke. Arch Phys Med Rehabil 94 8 1527 1533
87. Zaaimi B, Edgley SA, Soteropoulos DS, Baker SN, 2012 Changes in descending motor pathway connectivity after corticospinal tract lesion in macaque monkey. Brain 135 Pt 7 2277 2289
88. Zeiler SR, Gibson EM, Hoesch RE, Li MY, Worley PF, O'Brien RJ, 2013 Medial premotor cortex shows a reduction in inhibitory markers and mediates recovery in a mouse model of focal stroke. Stroke 44 2 483 489
89. Zhu LL, Lindenberg R, Alexander MP, Schlaug G, 2010 Lesion load of the corticospinal tract predicts motor impairment in chronic stroke. Stroke 41 5 910 915
90. Zittel S, Weiller C, Liepert J, 2008 Citalopram improves dexterity in chronic stroke patients. Neurorehabil Neural Repair 22 3 311 314