Aged; Electrodes; Female; Gray Matter/pathology/physiopathology; Humans; Magnetic Resonance Imaging; Male; Middle Aged; Motor Cortex/pathology/physiopathology; Stroke/pathology/physiopathology/therapy; Stroke Rehabilitation; Transcranial Direct Current Stimulation
Abstract :
[en] Anodal transcranial direct current stimulation (tDCS) can boost the effects of motor training and facilitate plasticity in the healthy human brain. Motor rehabilitation depends on learning and plasticity, and motor learning can occur after stroke. We tested whether brain stimulation using anodal tDCS added to motor training could improve rehabilitation outcomes in patients after stroke. We performed a randomized, controlled trial in 24 patients at least 6 months after a first unilateral stroke not directly involving the primary motor cortex. Patients received either anodal tDCS (n= 11) or sham treatment (n= 13) paired with daily motor training for 9 days. We observed improvements that persisted for at least 3 months post-intervention after anodal tDCS compared to sham treatment on the Action Research Arm Test (ARAT) and Wolf Motor Function Test (WMFT) but not on the Upper Extremity Fugl-Meyer (UEFM) score. Functional magnetic resonance imaging (MRI) showed increased activity during movement of the affected hand in the ipsilesional motor and premotor cortex in the anodal tDCS group compared to the sham treatment group. Structural MRI revealed intervention-related increases in gray matter volume in cortical areas, including ipsilesional motor and premotor cortex after anodal tDCS but not sham treatment. The addition of ipsilesional anodal tDCS to a 9-day motor training program improved long-term clinical outcomes relative to sham treatment in patients after stroke.
Disciplines :
Human health sciences: Multidisciplinary, general & others
Author, co-author :
Allman, Claire
Amadi, Ugwechi
Winkler, Anderson ; Université de Liège - ULiège > Form. doc. sc. bioméd. & pharma.
Wilkins, Leigh
Filippini, Nicola
Kischka, Udo
Stagg, Charlotte J.
Johansen-Berg, Heidi
Language :
English
Title :
Ipsilesional anodal tDCS enhances the functional benefits of rehabilitation in patients after stroke.
Publication date :
2016
Journal title :
Science Translational Medicine
ISSN :
1946-6234
eISSN :
1946-6242
Publisher :
American Association for the Advancement of Science, United States
Volume :
8
Issue :
330
Pages :
330re1
Peer reviewed :
Peer Reviewed verified by ORBi
Commentary :
Copyright (c) 2016, American Association for the Advancement of Science.
A. Sunderland, D. J. Tinson, E. L. Bradley, D. Fletcher, R. Langton Hewer, D. T. Wade, Enhanced physical therapy improves recovery of arm function after stroke. A randomised controlled trial. J. Neurol. Neurosurg. Psychiatry 55, 530-535 (1992).
G. Kwakkel, R. C. Wagenaar, J. W. R. Twisk, G. J. Lankhorst, J. C. Koetsier, Intensity of leg and arm training after primary middle-cerebral-Artery stroke: A randomised trial. Lancet 354, 191-196 (1999).
C. J. Stagg, H. Johansen-Berg, in Stroke Rehabilitation: Insights from Neuroscience and Imaging, L. M. Carey, Ed. (Oxford Univ. Press, Oxford, 2012).
J. W. Krakauer, Motor learning: Its relevance to stroke recovery and neurorehabilitation. Curr. Opin. Neurol. 19, 84-90 (2006).
P. M. Matthews, H. Johansen-Berg, H. Reddy, Non-invasive mapping of brain functions and brain recovery: Applying lessons from cognitive neuroscience to neurorehabilitation. Restor. Neurol. Neurosci. 22, 245-260 (2004).
M. A. Nitsche, W. Paulus, Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J. Physiol. 527, 633-639 (2000).
C. J. Stagg, J. G. Best, M. C. Stephenson, J. O'Shea, M. Wylezinska, Z. T. Kincses, P. G. Morris, P. M. Matthews, H. Johansen-Berg, Polarity-sensitive modulation of cortical neurotransmitters by transcranial stimulation, J. Neurosci. 29, 5202-5206 (2009).
C. J. Stagg, G. Jayaram, D. Pastor, Z. T. Kincses, P. M. Matthews, H. Johansen-Berg, Polarity and timing-dependent effects of transcranial direct current stimulation in explicit motor learning. Neuropsychologia 49, 800-804 (2011).
M. A. Nitsche, A. Schauenburg, N. Lang, D. Liebetanz, C. Exner, W. Paulus, F. Tergau, Facilitation of implicit motor learning by weak transcranial direct current stimulation of the primary motor cortex in the human. J. Cogn. Neurosci. 15, 619-626 (2003).
P. S. Boggio, A. Nunes, S. P. Rigonatti, M. A. Nitsche, A. Pascual-Leone, F. Fregni, Repeated sessions of noninvasive brain DC stimulation is associated with motor function improvement in stroke patients. Restor. Neurol. Neurosci. 25, 123-129 (2007).
D. G. Nair, V. Renga, R. Lindenberg, L. Zhu, G. Schlaug, Optimizing recovery potential through simultaneous occupational therapy and non-invasive brain-stimulation using tDCS. Restor. Neurol. Neurosci. 29, 411-420 (2011).
R. Lindenberg, V. Renga, L. L. Zhu, D. Nair, G. Schlaug, Bihemispheric brain stimulation facilitates motor recovery in chronic stroke patients. Neurology 75, 2176-2184 (2010).
A. Bastani, S. Jaberzadeh, Does anodal transcranial direct current stimulation enhance excitability of the motor cortex and motor function in healthy individuals and subjects with stroke: A systematic review and meta-Analysis. Clin. Neurophysiol. 123, 644-657 (2012).
A. J. Butler, M. Shuster, E. O'Hara, K. Hurley, D. Middlebrooks, K. Guilkey, A meta-Analysis of the efficacy of anodal transcranial direct current stimulation for upper limb motor recovery in stroke survivors. J. Hand Ther. 26, 162-171 (2013).
J. E. Harris, J. J. Eng, W. C. Miller, A. S. Dawson, A self-Administered Graded Repetitive Arm Supplementary Program (GRASP) improves arm function during inpatient stroke rehabilitation: A multi-site randomized controlled trial. Stroke 40, 2123-2128 (2009).
A. R. Fugl-Meyer, L. Jääskö, I. Leyman, S. Olsson, S. Steglind, The post-stroke hemiplegic patient. 1. A method for evaluation of physical performance. Scand. J. Rehab. Med. 7, 13-31 (1975).
R. C. Lyle, A performance test for assessment of upper limb function in physical rehabilitation treatment and research. Int. J. Rehabil. Res. 4, 483-492 (1981).
S. L. Wolf, P. A. Catlin, M. Ellis, A. L. Archer, B. Morgan, A. Piacentino, Assessing Wolf motor function test as outcome measure for research in patients after stroke. Stroke 32, 1635-1639 (2001).
F. C. Hummel, L. G. Cohen, Non-invasive brain stimulation: A new strategy to improve neurorehabilitation after stroke? Lancet Neurol. 5, 708-712 (2006).
J. Reis, H. M. Schambra, L. G. Cohen, E. R. Buch, B. Fritsch, E. Zarahn, P. A. Celnik, J. W. Krakauer, Noninvasive cortical stimulation enhances motor skill acquisition over multiple days through an effect on consolidation, Proc. Natl. Acad. Sci. U.S.A. 106, 1590-1595 (2009).
D.-Y. Kim, J.-Y. Lim, E. K. Kang, D. S. You, M.-K. Oh, B.-M. Oh, N.-J. Paik, Effect of transcranial direct current stimulation on motor recovery in patients with subacute stroke. Am. J. Phys. Med. Rehabil. 89, 879-886 (2010).
H. Johansen-Berg, M. F. S. Rushworth, M. D. Bogdanovic, U. Kischka, S. Wimalaratna, P. M. Matthews, The role of ipsilateral premotor cortex in hand movement after stroke. Proc. Natl. Acad. Sci. U.S.A. 99, 14518-14523 (2002).
M. Lotze, J. Markert, P. Sauseng, J. Hoppe, C. Plewnia, C. Gerloff, The role of multiple contralesional motor areas for complex hand movements after internal capsular lesion. J. Neurosci. 26, 6096-6102 (2006).
Y.-w. Hsieh, C.-y. Wu, K.-c. Lin, Y.-f. Chang, C.-l. Chen, J.-s. Liu, Responsiveness and validity of three outcome measures of motor function after stroke rehabilitation. Stroke 40, 1386-1391 (2009).
J.-H. Lin, M.-J. Hsu, C.-F. Sheu, T.-S. Wu, R.-T. Lin, C.-H. Chen, C.-L. Hsieh, Psychometric comparisons of 4 measures for assessing upper-extremity function in people with stroke. Phys. Ther. 89, 840-850 (2009).
A. Pollock, S. E. Farmer, M. C. Brady, P. Langhorne, G. E. Mead, J. Mehrholz, F. van Wijck, Interventions for improving upper limb function after stroke. Cochrane Database Syst. Rev. 11, CD010820 (2014).
S. R. Zeiler, J. W. Krakauer, The interaction between training and plasticity in the poststroke brain. Curr. Opin. Neurol. 26, 609-616 (2013).
T. Kitago, J. Goldsmith, M. Harran, L. Kane, J. Berard, S. Huang, S. L. Ryan, P. Mazzoni, J. W. Krakauer, V. S. Huang, Robotic therapy for chronic stroke: General recovery of impairment or improved task-specific skill? J. Neurophysiol. 114, 1885-1894 (2015).
J. W. Krakauer, in Oxford Textbook of Neurorehabilitation, V. Dietz, N. Ward, Eds. (Oxford Univ. Press, Oxford, 2015).
M. R. Borich, K. E. Brown, L. A. Boyd, Motor skill learning is associated with diffusion characteristics of white matter in individuals with chronic stroke. J. Neurol. Phys. Ther. 38, 151-160 (2013).
L. A. Boyd, B. M. Quaney, P. S. Pohl, C. J. Winstein, Learning implicitly: Effects of task and severity after stroke. Neurorehabil. Neural Repair 21, 444-454 (2007).
F. Buma, G. Kwakkel, N. Ramsey, Understanding upper limb recovery after stroke. Restor. Neurol. Neurosci. 31, 707-722 (2013).
M. F. Levin, J. A. Kleim, S. L. Wolf, What do motor "recovery" and "compensation" mean in patients following stroke? Neurorehabil. Neural Repair 23, 313-319 (2009).
C. M. Stinear, P. A. Barber, P. R. Smale, J. P. Coxon, M. K. Fleming, W. D. Byblow, Functional potential in chronic stroke patients depends on corticospinal tract integrity. Brain 130, 170-180 (2007).
C. J. Stagg, V. Bachtiar, J. O'Shea, C. Allman, R. A. Bosnell, U. Kischka, P. M. Matthews, H. Johansen-Berg, Cortical activation changes underlying stimulation-induced behavioural gains in chronic stroke. Brain 135, 276-284 (2012).
L. V. Gauthier, E. Taub, C. Perkins, M. Ortmann, V. W. Mark, G. Uswatte, Remodeling the brain: Plastic structural brain changes produced by different motor therapies after stroke. Stroke 39, 1520-1525 (2008).
J. Scholz, M. C. Klein, T. E. J. Behrens, H. Johansen-Berg, Training induces changes in whitematter architecture. Nat. Neurosci. 12, 1370-1371 (2009).
R. A. Bosnell, Z. T. Kincses, C. J. Stagg, V. Tomassini, U. Kischka, S. Jbabdi, M. W. Woolrich, J. Andersson, P. M. Matthews, H. Johansen-Berg, Motor practice promotes increased activity in brain regions structurally disconnected after subcortical stroke. Neurorehabil. Neural Repair 25, 607-616 (2011).
F. Pesarin, L. Salmaso, Permutation Tests for Complex Data: Theory, Applications and Software (John Wiley and Sons, Chichester, 2010).
A. M. Winkler, M. A. Webster, J. C. Brooks, I. Tracey, S. M. Smith, T. E. Nichols, Non-parametric combination and related permutation tests for neuroimaging. Hum. Brain Mapp. 10.1002/hbm.23115 (2016).
S. M. Smith, M. Jenkinson, M. W. Woolrich, C. F. Beckmann, T. E. J. Behrens, H. Johansen-Berg, P. R. Bannister, M. De Luca, I. Drobnjak, D. E. Flitney, R. K. Niazy, J. Saunders, J. Vickers, Y. Zhang, N. De Stefano, J. M. Brady, P. M. Matthews, Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23 (Suppl. 1), S208-S219 (2004).
S. S. Shapiro, M. B. Wilk, An analysis of variance test for normality (complete samples). Biometrika 591-611 (1965).
A. M. Winkler, G. R. Ridgway, M. A. Webster, S. M. Smith, T. E. Nichols, Permutation inference for the general linear model. Neuroimage 92, 381-397 (2014).
G. Douaud, S. Smith, M. Jenkinson, T. Behrens, H. Johansen-Berg, J. Vickers, S. James, N. Voets, K. Watkins, P. M. Matthews, A. James, Anatomically related grey and white matter abnormalities in adolescent-onset schizophrenia. Brain 130, 2375-2386 (2007).
M. Jenkinson, P. Bannister, M. Brady, S. Smith, Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 17, 825-841 (2002).
C. F. Beckmann, S. M. Smith, Probabilistic independent component analysis for functional magnetic resonance imaging. IEEE Trans. Med. Imaging 23, 137-152 (2004).
M. W. Woolrich, B. D. Ripley, M. Brady, S. M. Smith, Temporal autocorrelation in univariate linear modeling of FMRI data. Neuroimage 14, 1370-1386 (2001).
D. N. Greve, B. Fischl, Accurate and robust brain image alignment using boundary-based registration. Neuroimage 48, 63-72 (2009).
T. E. J. Behrens, M. W. Woolrich, M. Jenkinson, H. Johansen-Berg, R. G. Nunes, S. Clare, P. M. Matthews, J. M. Brady, S. M. Smith, Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magn. Reson. Med. 50, 1077-1088 (2003).
T. E. J. Behrens, H. Johansen Berg, S. Jbabdi, M. F. S. Rushworth, M. W. Woolrich, Probabilistic diffusion tractography with multiple fibre orientations: What can we gain? Neuroimage 34, 144-155 (2007).
