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Brain Advance Access originally published online on December 19, 2005
Brain 2006 129(3):791-808; doi:10.1093/brain/awh713
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© The Author (2005). Published by Oxford University Press on behalf of the Guarantors of Brain. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org

Multimodal imaging of brain reorganization in motor areas of the contralesional hemisphere of well recovered patients after capsular stroke

Christian Gerloff1,2, Khalaf Bushara2, Alexandra Sailer1, Eric M. Wassermann4, Robert Chen2, Takahiro Matsuoka2, Daniel Waldvogel2, George F. Wittenberg3, Kenji Ishii2, Leonardo G. Cohen3 and Mark Hallett2

1 Cortical Physiology Research Group, Department of Neurology, Eberhard–Karls University Medical School, Tuebingen, Germany; Sections of 2 Human Motor Control and 3 Human Cortical Physiology, Medical Neurology Branch and 4 Brain Stimulation Unit, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD, USA

Correspondence to: Christian Gerloff, MD, Department of General Neurology, Hertie Institute for Clinical Brain Research, University of Tuebingen, Hoppe-Seyler Street 3, 72076 Tuebingen, Germany E-mail: christian.gerloff{at}uni-tuebingen.de or Mark Hallett, MD, NINDS, National Institutes of Health, 10 Center Drive, MSC-1428, Bethesda, Maryland 20892, USA, E-mail: hallettm{at}ninds.nih.gov

Clinical recovery after stroke can be significant and has been attributed to plastic reorganization and recruitment of novel areas previously not engaged in a given task. As equivocal results have been reported in studies using single imaging or electrophysiological methods, here we applied an integrative multimodal approach to a group of well-recovered chronic stroke patients (n = 11; aged 50–81 years) with left capsular lesions. Focal activation during recovered hand movements was assessed with EEG spectral analysis and H215O-PET with EMG monitoring, cortico–cortical connectivity with EEG coherence analysis (cortico–cortical coherence) and corticospinal connectivity with transcranial magnetic stimulation (TMS). As seen from comparisons with age-matched controls, our patients showed enhanced recruitment of the lateral premotor cortex of the lesioned hemisphere [Brodmann area (BA) 6], lateral premotor and to a lesser extent primary sensorimotor and parietal cortex of the contralesional hemisphere (CON-H; BA 4 and superior parietal lobule) and left cerebellum (patients versus controls, Z > 3.09). EEG coherence analysis showed that after stroke cortico–cortical connections were reduced in the stroke hemisphere but relatively increased in the CON-H (ANOVA, contrast analysis, P < 0.05), suggesting a shift of functional connectivity towards the CON-H. Nevertheless, fast conducting corticospinal transmission originated exclusively from the lesioned hemisphere. No direct ipsilateral motor evoked potentials (MEPs) could be elicited with TMS over the contralesional primary motor cortex (iM1) in stroke patients. We conclude that (i) effective recovery is based on enhanced utilization of ipsi- and contralesional resources, (ii) basic corticospinal commands arise from the lesioned hemisphere without recruitment of (‘latent’) uncrossed corticospinal tract fibres and (iii) increased contralesional activity probably facilitates control of recovered motor function by operating at a higher-order processing level, similar to but not identical with the extended network concerned with complex movements in healthy subjects.

Key Words: Plasticity; stroke; recovery; motor control; motor cortex

Abbreviations: APB = abductor pollicis brevis muscle; BA = Brodmann area; COG = center of gravity; CON-H = contralesional hemisphere; DAM-H = damaged (stroke) hemisphere; EOI = electrode of interest; EDC = extensor digitorum communis; ERD = event-related desynchronization; FWHM = full width at half maximum; iM1 = ipsilateral (= contralesional) primary motor cortex; M1 = primary motor cortex; MEP = motor evoked potential; MRC = Medical Research Council; MT = motor threshold; NAP = number of active positions (from which TMS responses are elicited); OP = optimal point for eliciting a defined muscle response with TMS; POI = (electrode) pairs of interest; PT = pyramidal tract; rCBF = regional cerebral blood flow; ROI = region of interest; SMA = supplementary motor area; SPL = superior parietal lobule; SPM = statistical parametric map; tDCS = transcranial direct current stimulation; tanh–1 = inverse hyperbolic tangent; TMS = transcranial magnetic stimulation; TRCoh = task-related coherence; TrlogPow = task-related log-transformed power; TRPow = task-related power; TRtanh–1Coh = task-related inverse hyperbolic tangent-transformed coherence

Received July 31, 2005. Revised September 29, 2005. Accepted November 7, 2005.


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