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Research ArticleFunctional
Open Access

Functional Homotopic Changes in Multiple Sclerosis with Resting-State Functional MR Imaging

Y. Zhou, M. Milham, X.-N. Zuo, C. Kelly, H. Jaggi, J. Herbert, R.I. Grossman and Y. Ge
American Journal of Neuroradiology June 2013, 34 (6) 1180-1187; DOI: https://doi.org/10.3174/ajnr.A3386
Y. Zhou
aFrom the Radiology/Center for Biomedical Imaging (Y.Z., H.J., J.H., R.I.G., Y.G.)
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M. Milham
bNew York University Child Study Center (M.M., X.-N.Z., C.K.), New York University School of Medicine, New York, New York
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X.-N. Zuo
bNew York University Child Study Center (M.M., X.-N.Z., C.K.), New York University School of Medicine, New York, New York
cLaboratory for Functional Connectome and Development (X.-N.Z.), Key Laboratory of Behavioral Science, Magnetic Resonance Imaging Research Center, Institute of Psychology, Chinese Academy of Sciences, Beijing, China.
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C. Kelly
bNew York University Child Study Center (M.M., X.-N.Z., C.K.), New York University School of Medicine, New York, New York
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H. Jaggi
aFrom the Radiology/Center for Biomedical Imaging (Y.Z., H.J., J.H., R.I.G., Y.G.)
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J. Herbert
aFrom the Radiology/Center for Biomedical Imaging (Y.Z., H.J., J.H., R.I.G., Y.G.)
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R.I. Grossman
aFrom the Radiology/Center for Biomedical Imaging (Y.Z., H.J., J.H., R.I.G., Y.G.)
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Y. Ge
aFrom the Radiology/Center for Biomedical Imaging (Y.Z., H.J., J.H., R.I.G., Y.G.)
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  • Fig 1.
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    Fig 1.

    Whole-brain voxelwise homotopic RSFC pattern by use of multiple linear regression models in control (A) and MS (B) groups. Homotopic RSFC was computed within 1 hemisphere (left side) for each pair of homotopic voxels and corrected by the Gaussian random field theory (minimum Z > 2.3; cluster level, P < .05, corrected). The final statistical maps are visualized as 6 hemispheric surfaces (cortical regions) with 6-mm full width at half maximum and multiple axial images (subcortical regions). Compared with control participants, patients demonstrated decreased VMHC in several cortical regions (long arrows) including the frontal, temporal, and occipital lobes and increased VMHC mainly in the subcortical regions (short arrows).

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    Fig 2.

    Comparison results of whole-brain voxelwise VMHC maps between patients with MS and healthy control participants (NC) showed regions with significantly decreased (blue) and increased VMHC (red and yellow) in patients compared with control participants corrected with Gaussian random field theory (minimum Z > 2.3; cluster level; P < .05, corrected).

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    Fig 3.

    Comparison results of global (A) and regional (B) VMHC differences between patients with MS and healthy control participants. There was significantly reduced global VMHC in patients compared with control participants (P = .04) (A). Regional analysis showed significantly higher interhemispheric correlation in the primary cortical regions (ie, visual, somatosensory, motor, and auditory cortices) compared with unimodal and heteromodal regions (B) in both groups. Significantly lower VMHC was found only in the primary cortex in patients compared with control participants (P < .05). Error bars denote standard error in each group.

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    Fig 4.

    Structural differences measured with midsagittal CC area (A) and the FA of the entire CC (B) between patients with MS and control participants showed a significantly reduced midsagittal CC area (P = .026) and FA (P = .0018) in patients compared with control participants. The boxes have lines at the lower quartile (horizontal blue lines), median (horizontal red lines), and upper quartile values. The whiskers are lines extending from each end of the boxes to show the extent of the rest of the data. The “notch” marks the 95% confidence interval for the medians, which can be used to differentiate 2 groups. Namely 2 medians will differ significantly with P < .05 if the 2 notch intervals do not overlap.

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    Fig 5.

    Mean FA of the entire CC and global VMHC in all participants (A) showed significant positive correlation (r = 0.3; P = .03). Mean FA of CC segment 5 (occipital projections) and mean VMHC in the occipital regions showed significant positive correlation (r = 0.43; P = .037) in patients with MS (B). There was a significant negative correlation between the Expanded Disability Status Scale score and the mean FA of CC (r = −0.61; P = .013) in the patients (C). The mean FA of CC also significantly correlates with the lesion load (r = −0.92; P < .0001) (D).

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    Fig 6.

    Interhemispheric and intrahemispheric structural and functional connectivity of cortical motor regions. A, On the basis of whole-brain fiber tractography from FA images, a sphere with a radius of 4.5 mm was placed in the posterior motor triangle area as a seed to select both transcallosal (interhemispheric fibers indicated in red) and nontranscallosal CST (intrahemispheric fibers indicated in blue) motor fibers to define the connecting terminal cortices for VMHC evaluation. B, A representative example of different VMHC values in 2 separate terminal regions showed higher VMHC (0.68) in motor regions connected with transcallosal fibers compared with premotor regions (0.29) projected by nontranscallosal CST fibers. C, Group comparison of transcallosal VMHC and nontranscallosal VMHCs showed much higher value in transcallosal regions. There was significantly reduced VMHC in transcallosal motor regions in patients compared with control participants (P = .03) but not in nontranscallosal CST regions (P = .09).

Tables

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    Table 1:

    Brain regions showing decreased VMHC in patients with MS vs control participants

    Brain RegionBAX,Y,Z, MNI (mm)Cluster SizeMaximal Z Score
    Visual (calcarine)17−10, −94, −29053.83
    Primary somatosensory1−50, −16, 462863.8
    Lateral occipital19−34, −74, −41633.58
    Middle temporal22−66, −46, 81294.07
    Frontal pole11−36, 64, −61263.52
    Superior temporal48−54, −4, −2933.88
    Inferior occipital18−24, −70, −16653.41
    Middle occipital37−38, −42, −28643.06
    Fusiform37−22, −54, −14593.35
    Cuneus19−12, −82, 34573.68
    • Note:—Only the right side is listed because of symmetric computation between the hemispheres, P-values were obtained with cluster-level multiple comparison correction (corrected P < .05; cluster size >20); BA indicates Brodmann area; MNI, Montreal Neurological Institute.

    • View popup
    Table 2:

    Brain regions showing increased VMHC in patients with MS vs control participants

    Brain RegionBAX,Y,Z, MNI (mm)Cluster SizeMaximal Z Score
    Orbital frontal/insular48−26, −12, −141603.45
    Thalamus−−2, −24, 12403.16
    Cerebellum−−10, −82, −26403.44
    Pallidum−−10, 4, −4233.19
    Inferior temporal20−48, −34, −20223.71
    • Note:—Only the right side is listed because of symmetric computation between the hemispheres. P-values were obtained with cluster-level multiple comparison correction (corrected, P < .05; cluster size >20); BA indicates Brodmann area; MNI, Montreal Neurological Institute.

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American Journal of Neuroradiology: 34 (6)
American Journal of Neuroradiology
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1 Jun 2013
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Cite this article
Y. Zhou, M. Milham, X.-N. Zuo, C. Kelly, H. Jaggi, J. Herbert, R.I. Grossman, Y. Ge
Functional Homotopic Changes in Multiple Sclerosis with Resting-State Functional MR Imaging
American Journal of Neuroradiology Jun 2013, 34 (6) 1180-1187; DOI: 10.3174/ajnr.A3386

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Functional Homotopic Changes in Multiple Sclerosis with Resting-State Functional MR Imaging
Y. Zhou, M. Milham, X.-N. Zuo, C. Kelly, H. Jaggi, J. Herbert, R.I. Grossman, Y. Ge
American Journal of Neuroradiology Jun 2013, 34 (6) 1180-1187; DOI: 10.3174/ajnr.A3386
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