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February 05, 2019; 92 (6) Article

Selective atrophy of the connected deepest cortical layers following small subcortical infarct

Eyal Lotan, Ido Tavor, Daniel Barazany, Shani Ben-Amitay, Chen Hoffmann, Galia Tsarfaty, Yaniv Assaf, David Tanne
First published January 11, 2019, DOI: https://doi.org/10.1212/WNL.0000000000006884
Eyal Lotan
From the Department of Diagnostic Imaging (E.L., I.T., C.H., G.T.) and Stroke Center (D.T.), Department of Neurology and Sagol Neuroscience Center, Sheba Medical Center, Tel Hashomer, Ramat Gan; and Sackler Faculty of Medicine (E.L., I.T., C.H., G.T., D.T.), Sagol School of Neuroscience (I.T., Y.A.), Strauss Center for Computational Neuroimaging (D.B.), and Department of Neurobiology (S.B.-A., Y.A.), George S. Wise Faculty of Life Sciences, Tel Aviv University, Israel.
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Ido Tavor
From the Department of Diagnostic Imaging (E.L., I.T., C.H., G.T.) and Stroke Center (D.T.), Department of Neurology and Sagol Neuroscience Center, Sheba Medical Center, Tel Hashomer, Ramat Gan; and Sackler Faculty of Medicine (E.L., I.T., C.H., G.T., D.T.), Sagol School of Neuroscience (I.T., Y.A.), Strauss Center for Computational Neuroimaging (D.B.), and Department of Neurobiology (S.B.-A., Y.A.), George S. Wise Faculty of Life Sciences, Tel Aviv University, Israel.
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Daniel Barazany
From the Department of Diagnostic Imaging (E.L., I.T., C.H., G.T.) and Stroke Center (D.T.), Department of Neurology and Sagol Neuroscience Center, Sheba Medical Center, Tel Hashomer, Ramat Gan; and Sackler Faculty of Medicine (E.L., I.T., C.H., G.T., D.T.), Sagol School of Neuroscience (I.T., Y.A.), Strauss Center for Computational Neuroimaging (D.B.), and Department of Neurobiology (S.B.-A., Y.A.), George S. Wise Faculty of Life Sciences, Tel Aviv University, Israel.
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Shani Ben-Amitay
From the Department of Diagnostic Imaging (E.L., I.T., C.H., G.T.) and Stroke Center (D.T.), Department of Neurology and Sagol Neuroscience Center, Sheba Medical Center, Tel Hashomer, Ramat Gan; and Sackler Faculty of Medicine (E.L., I.T., C.H., G.T., D.T.), Sagol School of Neuroscience (I.T., Y.A.), Strauss Center for Computational Neuroimaging (D.B.), and Department of Neurobiology (S.B.-A., Y.A.), George S. Wise Faculty of Life Sciences, Tel Aviv University, Israel.
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Chen Hoffmann
From the Department of Diagnostic Imaging (E.L., I.T., C.H., G.T.) and Stroke Center (D.T.), Department of Neurology and Sagol Neuroscience Center, Sheba Medical Center, Tel Hashomer, Ramat Gan; and Sackler Faculty of Medicine (E.L., I.T., C.H., G.T., D.T.), Sagol School of Neuroscience (I.T., Y.A.), Strauss Center for Computational Neuroimaging (D.B.), and Department of Neurobiology (S.B.-A., Y.A.), George S. Wise Faculty of Life Sciences, Tel Aviv University, Israel.
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Galia Tsarfaty
From the Department of Diagnostic Imaging (E.L., I.T., C.H., G.T.) and Stroke Center (D.T.), Department of Neurology and Sagol Neuroscience Center, Sheba Medical Center, Tel Hashomer, Ramat Gan; and Sackler Faculty of Medicine (E.L., I.T., C.H., G.T., D.T.), Sagol School of Neuroscience (I.T., Y.A.), Strauss Center for Computational Neuroimaging (D.B.), and Department of Neurobiology (S.B.-A., Y.A.), George S. Wise Faculty of Life Sciences, Tel Aviv University, Israel.
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Yaniv Assaf
From the Department of Diagnostic Imaging (E.L., I.T., C.H., G.T.) and Stroke Center (D.T.), Department of Neurology and Sagol Neuroscience Center, Sheba Medical Center, Tel Hashomer, Ramat Gan; and Sackler Faculty of Medicine (E.L., I.T., C.H., G.T., D.T.), Sagol School of Neuroscience (I.T., Y.A.), Strauss Center for Computational Neuroimaging (D.B.), and Department of Neurobiology (S.B.-A., Y.A.), George S. Wise Faculty of Life Sciences, Tel Aviv University, Israel.
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David Tanne
From the Department of Diagnostic Imaging (E.L., I.T., C.H., G.T.) and Stroke Center (D.T.), Department of Neurology and Sagol Neuroscience Center, Sheba Medical Center, Tel Hashomer, Ramat Gan; and Sackler Faculty of Medicine (E.L., I.T., C.H., G.T., D.T.), Sagol School of Neuroscience (I.T., Y.A.), Strauss Center for Computational Neuroimaging (D.B.), and Department of Neurobiology (S.B.-A., Y.A.), George S. Wise Faculty of Life Sciences, Tel Aviv University, Israel.
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Selective atrophy of the connected deepest cortical layers following small subcortical infarct
Eyal Lotan, Ido Tavor, Daniel Barazany, Shani Ben-Amitay, Chen Hoffmann, Galia Tsarfaty, Yaniv Assaf, David Tanne
Neurology Feb 2019, 92 (6) e567-e575; DOI: 10.1212/WNL.0000000000006884

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Abstract

Objective To explore whether in patients with chronic small subcortical infarct the cortical layers of the connected cortex are differentially affected and whether these differences correlate with clinical symptomatology.

Methods Twenty patients with a history of chronic small subcortical infarct affecting the corticospinal tracts and 15 healthy controls were included. Connected primary motor cortex was identified with tractography starting from infarct. T1-component probability maps were calculated from T1 relaxation 3T MRI, dividing the cortex into 5 laminar gaussian classes.

Results Focal cortical thinning was observed in the connected cortex and specifically only in its deepest laminar class compared to the nonaffected mirrored cortex (p < 0.001). There was loss of microstructural integrity of the affected corticospinal tract with increased mean diffusivity and decreased fractional anisotropy compared to the contralateral nonaffected tract (p ≤ 0.002). Clinical scores were correlated with microstructural damage of the corticospinal tracts and with thinning of the cortex and specifically only its deepest laminar class (p < 0.001). No differences were found in the laminar thickness pattern of the bilateral primary motor cortices or in the microstructural integrity of the bilateral corticospinal tracts in the healthy controls.

Conclusion Our results support the concept of secondary neurodegeneration of connected primary motor cortex after a small subcortical infarct affecting the corticospinal tract, with observations that the main cortical thinning occurs in the deepest cortex and that the clinical symptomatology is correlated with this cortical atrophy pattern. Our findings may contribute to a better understanding of structural reorganization and functional outcomes after stroke.

Glossary

CADASIL=
cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy;
CST=
corticospinal tract;
FA=
fractional anisotropy;
FLAIR=
fluid-attenuated inversion recovery;
IQR=
interquartile range;
MD=
mean diffusivity;
NIHSS=
NIH Stroke Scale;
NIHSSM=
motor components of the NIHSS (face, arm and leg weakness);
NIHSSM-Recovery=
difference between baseline NIHSSM and NIHSSM scores at the time of MRI scan;
ROI=
region of interest;
TP-SLF=
temporoparietal superior longitudinal fasciculi

Footnotes

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

  • ↵* These authors contributed equally to this work.

  • Received June 12, 2018.
  • Accepted in final form October 2, 2018.
  • © 2019 American Academy of Neurology
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