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Motor cortex excitability and connectivity in chronic stroke: a multimodal model of functional reorganization

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Abstract

Cerebral ischemia triggers a cascade of cellular processes, which induce neuroprotection, inflammation, apoptosis and regeneration. At the neural network level, lesions concomitantly induce cerebral plasticity. Yet, many stroke survivors are left with a permanent motor deficit, and only little is known about the neurobiological factors that determine functional outcome after stroke. Transcranial magnetic stimulation (TMS) and magnetic resonance imaging (MRI) are non-invasive approaches that allow insights into the functional (re-) organization of the cortical motor system. We here combined neuronavigated TMS, MRI and analyses of connectivity to investigate to which degree recovery of hand function depends on corticospinal tract (CST) damage and biomarkers of cerebral plasticity like cortical excitability and motor network effective connectivity. As expected, individual motor performance of 12 stroke patients with persistent motor deficits was found to depend upon the degree of CST damage but also motor cortex excitability and interhemispheric connectivity. In addition, the data revealed a strong correlation between reduced ipsilesional motor cortex excitability and reduced interhemispheric inhibition in severely impaired patients. Interindividual differences in ipsilesional motor cortex excitability were stronger related to the motor deficit than abnormal interhemispheric connectivity or CST damage. Multivariate linear regression analysis combining the three factors accounted for more than 80 % of the variance in functional impairment. The inter-relation of cortical excitability and reduced interhemispheric inhibition provides direct multi-modal evidence for the disinhibition theory of the contralesional hemisphere following stroke. Finally, our data reveal a key mechanism (i.e., the excitability-related reduction in interhemispheric inhibition) accounting for the rehabilitative potential of novel therapeutic approaches which aim at modulating cortical excitability in stroke patients.

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Abbreviations

AH:

Affected hand

AMT:

Active motor threshold

ARAT:

Action research arm test

CST:

Corticospinal tract

DCM:

Dynamic causal modeling

DTI:

Diffusion tensor imaging

EMG:

Electromyography

EPI:

Echo planar imaging

FDI:

First dorsal interosseus muscle

FDR:

False discovery rate

fMRI:

Functional magnetic resonance imaging

FWE:

Family-wise error

FWHM:

Full width at half maximum

GLM:

General linear model

IHI:

Interhemispheric inhibition

JTT:

Jebsen–Taylor hand function test

M1:

Primary motor cortex

MEP:

Motor evoked potential

MNI:

Montreal Neurological Institute

MP-RAGE:

Magnetization-prepared rapid acquisition gradient echo

MRI:

Magnetic resonance imaging

mRS:

Modified Rankin Scale

MSO:

Maximum stimulator output

NIHSS:

National Institutes of Health Stroke Scale

ROI:

Region of interest

rTMS:

Repetitive transcranial magnetic stimulation

SD:

Standard deviation

SMA:

Supplementary motor area

SPM:

Statistical parametric mapping

tDCS:

Transcranial direct current stimulation

TMS:

Transcranial magnetic stimulation

UH:

Unaffected hand

V1:

Primary visual cortex

vPMC:

Ventral premotor cortex

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Acknowledgments

CG is supported by the German Research Foundation (DFG GR 3285/2-1). SBE acknowledges funding by the Helmholtz Initiative on Systems-Biology “The Human Brain Model” and the NIH (R01-MH074457). GRF gratefully acknowledges additional support from the Marga and Walter Boll Stiftung.

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Authors and Affiliations

  1. Neuromodulation and Neurorehabilitation, Max Planck Institute for Neurological Research, Gleueler Str. 50, 50931, Cologne, Germany

    Lukas J. Volz, Anna-Sophia Sarfeld, Svenja Diekhoff, Anne K. Rehme, Eva-Maria Pool & Christian Grefkes

  2. Department of Neurology, University of Cologne, Cologne, Germany

    Lukas J. Volz, Anna-Sophia Sarfeld, Gereon R. Fink & Christian Grefkes

  3. Institute of Neuroscience and Medicine (INM-1, INM-3), Juelich Research Centre, Jülich, Germany

    Simon B. Eickhoff, Gereon R. Fink & Christian Grefkes

  4. Institute for Clinical Neuroscience and Medical Psychology, Heinrich-Heine University, Düsseldorf, Germany

    Simon B. Eickhoff

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  1. Lukas J. Volz
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  2. Anna-Sophia Sarfeld
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Correspondence to Christian Grefkes.

Additional information

L.J. Volz and A.-S. Sarfeld contributed equally to this work.

Electronic supplementary material

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Supplementary Figure 1: Alternative models used for Bayesian Model Selection. (TIFF 18911 kb)

Supplementary material 2 (TIFF 14766 kb)

429_2013_702_MOESM3_ESM.tif

Supplementary Figure 2: (A) Endogenous connectivity (B) and effective connectivity during movements of the unaffected hand estimated via DCM. Coupling parameters (in 1/s [Hertz]) indicate connection strength, which is coded in color. Positive values (green) refer to promotion of neural activity. Negative values (red) indicate inhibition of neural activity (P < 0.05, FDR corrected). IL, ipsilesional hemisphere; CL, contralesional hemisphere. (TIFF 9936 kb)

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Volz, L.J., Sarfeld, AS., Diekhoff, S. et al. Motor cortex excitability and connectivity in chronic stroke: a multimodal model of functional reorganization. Brain Struct Funct 220, 1093–1107 (2015). https://doi.org/10.1007/s00429-013-0702-8

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