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April 18, 2017; 88 (16) Article

Distinct white matter alterations following severe stroke

Longitudinal DTI study in neglect

Roza M. Umarova, Lena Beume, Marco Reisert, Christoph P. Kaller, Stefan Klöppel, Irina Mader, Volkmar Glauche, Valerij G. Kiselev, Marco Catani, Cornelius Weiller
First published March 22, 2017, DOI: https://doi.org/10.1212/WNL.0000000000003843
Roza M. Umarova
From the Department of Neurology (R.M.U., L.B., C.P.K., V.G., C.W.), Freiburg Brain Imaging (R.M.U., L.B., C.P.K., S.K., I.M., V.G., C.W.), BrainLinks-BrainTools Cluster of Excellence (R.M.U., L.B., C.P.K., S.K., C.W.), Department of Psychiatry and Psychotherapy (R.M.U., S.K.), Medical Physics, Department of Radiology (M.R., V.G.K.), and Department of Neuroradiology (I.M.), Medical Center–University of Freiburg, Faculty of Medicine, University of Freiburg, Germany; University Hospital of Old Age Psychiatry (S.K.), University of Bern, Switzerland; and NatBrainLab (M.C.), Institute of Psychiatry, King's College London, UK.
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Lena Beume
From the Department of Neurology (R.M.U., L.B., C.P.K., V.G., C.W.), Freiburg Brain Imaging (R.M.U., L.B., C.P.K., S.K., I.M., V.G., C.W.), BrainLinks-BrainTools Cluster of Excellence (R.M.U., L.B., C.P.K., S.K., C.W.), Department of Psychiatry and Psychotherapy (R.M.U., S.K.), Medical Physics, Department of Radiology (M.R., V.G.K.), and Department of Neuroradiology (I.M.), Medical Center–University of Freiburg, Faculty of Medicine, University of Freiburg, Germany; University Hospital of Old Age Psychiatry (S.K.), University of Bern, Switzerland; and NatBrainLab (M.C.), Institute of Psychiatry, King's College London, UK.
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Marco Reisert
From the Department of Neurology (R.M.U., L.B., C.P.K., V.G., C.W.), Freiburg Brain Imaging (R.M.U., L.B., C.P.K., S.K., I.M., V.G., C.W.), BrainLinks-BrainTools Cluster of Excellence (R.M.U., L.B., C.P.K., S.K., C.W.), Department of Psychiatry and Psychotherapy (R.M.U., S.K.), Medical Physics, Department of Radiology (M.R., V.G.K.), and Department of Neuroradiology (I.M.), Medical Center–University of Freiburg, Faculty of Medicine, University of Freiburg, Germany; University Hospital of Old Age Psychiatry (S.K.), University of Bern, Switzerland; and NatBrainLab (M.C.), Institute of Psychiatry, King's College London, UK.
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Christoph P. Kaller
From the Department of Neurology (R.M.U., L.B., C.P.K., V.G., C.W.), Freiburg Brain Imaging (R.M.U., L.B., C.P.K., S.K., I.M., V.G., C.W.), BrainLinks-BrainTools Cluster of Excellence (R.M.U., L.B., C.P.K., S.K., C.W.), Department of Psychiatry and Psychotherapy (R.M.U., S.K.), Medical Physics, Department of Radiology (M.R., V.G.K.), and Department of Neuroradiology (I.M.), Medical Center–University of Freiburg, Faculty of Medicine, University of Freiburg, Germany; University Hospital of Old Age Psychiatry (S.K.), University of Bern, Switzerland; and NatBrainLab (M.C.), Institute of Psychiatry, King's College London, UK.
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Stefan Klöppel
From the Department of Neurology (R.M.U., L.B., C.P.K., V.G., C.W.), Freiburg Brain Imaging (R.M.U., L.B., C.P.K., S.K., I.M., V.G., C.W.), BrainLinks-BrainTools Cluster of Excellence (R.M.U., L.B., C.P.K., S.K., C.W.), Department of Psychiatry and Psychotherapy (R.M.U., S.K.), Medical Physics, Department of Radiology (M.R., V.G.K.), and Department of Neuroradiology (I.M.), Medical Center–University of Freiburg, Faculty of Medicine, University of Freiburg, Germany; University Hospital of Old Age Psychiatry (S.K.), University of Bern, Switzerland; and NatBrainLab (M.C.), Institute of Psychiatry, King's College London, UK.
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Irina Mader
From the Department of Neurology (R.M.U., L.B., C.P.K., V.G., C.W.), Freiburg Brain Imaging (R.M.U., L.B., C.P.K., S.K., I.M., V.G., C.W.), BrainLinks-BrainTools Cluster of Excellence (R.M.U., L.B., C.P.K., S.K., C.W.), Department of Psychiatry and Psychotherapy (R.M.U., S.K.), Medical Physics, Department of Radiology (M.R., V.G.K.), and Department of Neuroradiology (I.M.), Medical Center–University of Freiburg, Faculty of Medicine, University of Freiburg, Germany; University Hospital of Old Age Psychiatry (S.K.), University of Bern, Switzerland; and NatBrainLab (M.C.), Institute of Psychiatry, King's College London, UK.
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Volkmar Glauche
From the Department of Neurology (R.M.U., L.B., C.P.K., V.G., C.W.), Freiburg Brain Imaging (R.M.U., L.B., C.P.K., S.K., I.M., V.G., C.W.), BrainLinks-BrainTools Cluster of Excellence (R.M.U., L.B., C.P.K., S.K., C.W.), Department of Psychiatry and Psychotherapy (R.M.U., S.K.), Medical Physics, Department of Radiology (M.R., V.G.K.), and Department of Neuroradiology (I.M.), Medical Center–University of Freiburg, Faculty of Medicine, University of Freiburg, Germany; University Hospital of Old Age Psychiatry (S.K.), University of Bern, Switzerland; and NatBrainLab (M.C.), Institute of Psychiatry, King's College London, UK.
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Valerij G. Kiselev
From the Department of Neurology (R.M.U., L.B., C.P.K., V.G., C.W.), Freiburg Brain Imaging (R.M.U., L.B., C.P.K., S.K., I.M., V.G., C.W.), BrainLinks-BrainTools Cluster of Excellence (R.M.U., L.B., C.P.K., S.K., C.W.), Department of Psychiatry and Psychotherapy (R.M.U., S.K.), Medical Physics, Department of Radiology (M.R., V.G.K.), and Department of Neuroradiology (I.M.), Medical Center–University of Freiburg, Faculty of Medicine, University of Freiburg, Germany; University Hospital of Old Age Psychiatry (S.K.), University of Bern, Switzerland; and NatBrainLab (M.C.), Institute of Psychiatry, King's College London, UK.
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Marco Catani
From the Department of Neurology (R.M.U., L.B., C.P.K., V.G., C.W.), Freiburg Brain Imaging (R.M.U., L.B., C.P.K., S.K., I.M., V.G., C.W.), BrainLinks-BrainTools Cluster of Excellence (R.M.U., L.B., C.P.K., S.K., C.W.), Department of Psychiatry and Psychotherapy (R.M.U., S.K.), Medical Physics, Department of Radiology (M.R., V.G.K.), and Department of Neuroradiology (I.M.), Medical Center–University of Freiburg, Faculty of Medicine, University of Freiburg, Germany; University Hospital of Old Age Psychiatry (S.K.), University of Bern, Switzerland; and NatBrainLab (M.C.), Institute of Psychiatry, King's College London, UK.
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Cornelius Weiller
From the Department of Neurology (R.M.U., L.B., C.P.K., V.G., C.W.), Freiburg Brain Imaging (R.M.U., L.B., C.P.K., S.K., I.M., V.G., C.W.), BrainLinks-BrainTools Cluster of Excellence (R.M.U., L.B., C.P.K., S.K., C.W.), Department of Psychiatry and Psychotherapy (R.M.U., S.K.), Medical Physics, Department of Radiology (M.R., V.G.K.), and Department of Neuroradiology (I.M.), Medical Center–University of Freiburg, Faculty of Medicine, University of Freiburg, Germany; University Hospital of Old Age Psychiatry (S.K.), University of Bern, Switzerland; and NatBrainLab (M.C.), Institute of Psychiatry, King's College London, UK.
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Citation
Distinct white matter alterations following severe stroke
Longitudinal DTI study in neglect
Roza M. Umarova, Lena Beume, Marco Reisert, Christoph P. Kaller, Stefan Klöppel, Irina Mader, Volkmar Glauche, Valerij G. Kiselev, Marco Catani, Cornelius Weiller
Neurology Apr 2017, 88 (16) 1546-1555; DOI: 10.1212/WNL.0000000000003843

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Abstract

Objective: To distinguish white matter remodeling directly induced by stroke lesion from that evoked by remote network dysfunction, using spatial neglect as a model.

Methods: We examined 24 visual neglect/extinction patients and 17 control patients combining comprehensive analyses of diffusion tensor metrics and global fiber tracking with neuropsychological testing in the acute (6.3 ± 0.5 days poststroke) and chronic (134 ± 7 days poststroke) stroke phases.

Results: Compared to stroke controls, patients with spatial neglect/extinction displayed longitudinal white matter alterations with 2 defining signatures: (1) perilesional degenerative changes characterized by congruently reduced fractional anisotropy and increased radial diffusivity (RD), axial diffusivity, and mean diffusivity, all suggestive of direct axonal damage by lesion and therefore nonspecific for impaired attention network and (2) transneuronal changes characterized by an increased RD in contralesional frontoparietal and bilateral occipital connections, suggestive of primary periaxonal involvement; these changes were distinctly related to the degree of unrecovered neglect symptoms in chronic stroke, hence emerging as network-specific alterations.

Conclusions: The present data show how stroke entails global alterations of lesion-spared network architecture over time. Sufficiently large lesions of widely interconnected association cortex induce distinct, large-scale structural reorganization in domain-specific network connections. Besides their relevance to unrecovered domain-specific symptoms, these effects might also explain mechanisms of domain-general deficits in stroke patients, pointing to potential targets for therapeutic intervention.

GLOSSARY

AD=
axial diffusivity;
DARTEL=
diffeomorphic anatomical registration using exponentiated lie algebra;
DTI=
diffusion tensor imaging;
DWI=
diffusion-weighted imaging;
FA=
fractional anisotropy;
FWE=
family-wise error correction;
HARDI=
high angular resolution diffusion imaging;
MD=
mean diffusivity;
MNI=
Montreal Neurological Institute;
NIHSS=
NIH Stroke Scale;
PCA=
principal component analysis;
RD=
radial diffusivity;
VBM=
voxel-based morphometry

Footnotes

  • Go to Neurology.org for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • Supplemental data at Neurology.org

  • Received September 1, 2016.
  • Accepted in final form January 23, 2017.
  • © 2017 American Academy of Neurology
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