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Articles, Neurobiology of Disease

Callosal Function in Pediatric Traumatic Brain Injury Linked to Disrupted White Matter Integrity

Emily L. Dennis, Monica U. Ellis, Sarah D. Marion, Yan Jin, Lisa Moran, Alexander Olsen, Claudia Kernan, Talin Babikian, Richard Mink, Christopher Babbitt, Jeffrey Johnson, Christopher C. Giza, Paul M. Thompson and Robert F. Asarnow
Journal of Neuroscience 15 July 2015, 35 (28) 10202-10211; DOI: https://doi.org/10.1523/JNEUROSCI.1595-15.2015
Emily L. Dennis
1Imaging Genetics Center, Mary and Mark Stevens Institute for Neuroimaging and Informatics, Keck School of Medicine, University of Southern California, Marina del Rey, California 90292,
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Monica U. Ellis
2Department of Psychiatry and Biobehavioral Sciences, Semel Institute for Neuroscience and Human Behavior, UCLA, Los Angeles, California 90024,
3Fuller Theological Seminary School of Psychology, Pasadena, California 91101,
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Sarah D. Marion
3Fuller Theological Seminary School of Psychology, Pasadena, California 91101,
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Yan Jin
1Imaging Genetics Center, Mary and Mark Stevens Institute for Neuroimaging and Informatics, Keck School of Medicine, University of Southern California, Marina del Rey, California 90292,
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Lisa Moran
2Department of Psychiatry and Biobehavioral Sciences, Semel Institute for Neuroscience and Human Behavior, UCLA, Los Angeles, California 90024,
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Alexander Olsen
2Department of Psychiatry and Biobehavioral Sciences, Semel Institute for Neuroscience and Human Behavior, UCLA, Los Angeles, California 90024,
4Department of Psychology, Norwegian University of Science and Technology, NO-7491 Trondheim, Norway,
5Department of Physical Medicine and Rehabilitation, St. Olavs Hospital, Trondheim University Hospital, NO-7030 Trondheim, Norway,
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Claudia Kernan
2Department of Psychiatry and Biobehavioral Sciences, Semel Institute for Neuroscience and Human Behavior, UCLA, Los Angeles, California 90024,
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Talin Babikian
2Department of Psychiatry and Biobehavioral Sciences, Semel Institute for Neuroscience and Human Behavior, UCLA, Los Angeles, California 90024,
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Richard Mink
6Harbor-UCLA Medical Center and Los Angeles BioMedical Research Institute, Department of Pediatrics, Torrance, California 90502,
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Christopher Babbitt
7Miller Children's Hospital, Long Beach, California 90806,
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Jeffrey Johnson
8LAC+USC Medical Center, Department of Pediatrics, Los Angeles, California 90033,
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Christopher C. Giza
9UCLA Brain Injury Research Center, Department of Neurosurgery and Division of Pediatric Neurology, Mattel Children's Hospital, Los Angeles, California 90095,
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Paul M. Thompson
1Imaging Genetics Center, Mary and Mark Stevens Institute for Neuroimaging and Informatics, Keck School of Medicine, University of Southern California, Marina del Rey, California 90292,
10Departments of Neurology, Pediatrics, Psychiatry, Radiology, Engineering, and Ophthalmology, University of Southern California, Los Angeles, California 90033, and
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Robert F. Asarnow
2Department of Psychiatry and Biobehavioral Sciences, Semel Institute for Neuroscience and Human Behavior, UCLA, Los Angeles, California 90024,
11Department of Psychology, UCLA, Los Angeles, California 90024
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  • Figure 1.
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    Figure 1.

    Differences between IHTT-slow and control groups in FA. Whole-tract differences in FA between IHTT-slow and control. The p values are shown corresponding to the color bar, and results were FDR corrected across all points on all tracts tested (q < 0.05; critical p threshold = 0.0038). For simplicity, only tracts with at least 5% of the tract showing significant differences are displayed. IFO, Inferior fronto-occipital fasciculus; ILF, inferior longitudinal fasciculus.

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    Figure 2.

    Differences between IHTT-slow and control groups in MD. Whole-tract differences in MD between IHTT-slow and control groups. The p values are shown corresponding to the color bar, and results were FDR corrected across all points on all tracts tested (q < 0.05; critical p threshold = 0.0036). For simplicity, only tracts with at least 5% of the tract showing significant differences are displayed.

  • Figure 3.
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    Figure 3.

    Differences between IHTT-normal and control groups. Whole-tract differences in FA between IHTT-normal and control groups across all tracts tested. The p values are shown corresponding to the color bar, and results were FDR corrected across all points on all tracts tested (q < 0.05; critical p threshold = 6.5 × 10−4). All tracts showing significant differences are shown. CST, Corticospinal tract; IFO, inferior fronto-occipital fasciculus.

  • Figure 4.
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    Figure 4.

    Element-wise associations with cognitive performance. Significant associations between element-wise FA and our performance index, covarying for age, sex, and scanner. Results were FDR corrected across all points on all tracts tested (q < 0.05; critical p threshold = 4.42 × 10−4), with CC-frontal as the only tract showing significant effects.

  • Figure 5.
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    Figure 5.

    Joint effects of FA and IHTT on cognitive performance. Significant results from the partial F test comparing a reduced model (age, sex, and IHTT group) with a full model (age, sex, IHTT-group, and element-wise FA) with cognitive performance as the response variable. For simplicity, only tracts with at least 5% of the tract significant are shown. The F statistic is shown along the tract corresponding to the color bar. PRCG, Precentral gyrus; ATR, anterior thalamic radiation; ILF, inferior longitudinal fasciculus; IFOF, inferior fronto-occipital fasciculus; CST, corticospinal tract.

Tables

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    Table 1.

    Demographic information on the participants included

    TBIControl group (N = 31)
    Slow (N = 16)Normal (N = 16)
    Age (years)13.9 (2.5)14.5 (3.2)14.9 (3.0)
    Gender
        Male111217
        Female5414
    IHTT (ms)25.3 (6.2)7.8 (5.2)9.3 (5.4)
    TSI (weeks)11.6 (4.8)12.2 (5.2)
        SAH46
        IVH23
        EDH75
        SDH65
        ICH75
        Contusion55
        DAI13
        ICP ↑14
        FX
            Dep57
            ND63
    • Data are average (SD) or n. We had acute CT scan information for 15 of 16 IHTT-slow and 15 of 16 IHTT-normal participants. SAH, Subarachnoid hemorrhage; IVH, intraventricular hemorrhage; EDH, epidural hematoma; SDH, subdural hematoma; ICH, intracerebral hemorrhage; DAI, diffuse axonal injury; ICP ↑, increased intracranial pressure; FX, fracture; Dep, depressed; ND, nondepressed.

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    Table 2.

    Descriptive statistics on the three IHTT groups

    NMeanSDMinimumMaximum
    IHTT-slow1625.316.441839
    IHTT-normal167.815.35116.5
    Control319.275.451.519
    Total6312.989.18
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    Table 3.

    Element-wise differences in WM integrity between the IHTT-slow and control groups, and between the IHTT-normal and control groups

    IHTT-slow vs control groupIHTT-normal vs control group
    FAMDFA
    Tract significance (%)Minimum pTract significance (%)Minimum pTract significance (%)Minimum p
    CC-frontal18.61.86E-083.51.06E-0551.28E-06
    CC-prcg1.21.74E-061.32.14E-05
    CC-pocg2.12.42E-048.71.69E-06
    CC-parietal2.91.94E-0612.64.09E-06
    CC-temporal141.94E-063.82.09E-06
    CC-occipital17.55.02E-07176.44E-08
    atr_l0.93.96E-04
    atr_r1.96.57E-052.25.26E-06
    cgc_l0.88.96E-05
    cgc_r0.92.28E-04
    cst_l2.83.34E-050.87.54E-05
    cst_r3.63.10E-053.21.86E-05
    ifo_l12.91.07E-0614.24.00E-070.96.17E-05
    ifo_r7.91.09E-0510.81.77E-06
    ilf_l3.88.61E-0631.92.43E-09
    ilf_r67.31E-069.65.39E-06
    slf_l2.71.05E-043.57.31E-06
    Fornix1.72.67E-04
    • For each tract investigated, the percentage of the tract that passed the FDR threshold is given (FDR threshold for IHTT-slow vs control FA = 0.0038, for MD = 0.0036, and for IHTT-normal vs control FA = 6.5 × 10−4), as well as the minimum p value for group differences on each tract. pocg, Postcentral gyrus; prcg, precentral gyrus.

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    Table 4.

    Descriptive statistics on the performance index scores of the three IHTT groups

    Performance indexNMeanSDMinimumMaximum
    IHTT-slow1691.3812.5276.88124.5
    IHTT-normal1699.8811.0475.75114.88
    Control31104.0810.7574.25128.5
    Total6399.7812.28
    • View popup
    Table 5.

    The results of our partial F test comparing a reduced model (age, sex, and IHTT group) with a full model (age, sex, IHTT group, and element-wise FA) with cognitive performance as the response variable

    Tract significance (%)Average F statistic
    CC-frontal16.06.4
    CC-parietal3.35.2
    CC-pocg4.86.3
    CC-prcg5.15.3
    CC-temporal4.75.5
    CC-occipital2.86.5
    atr_l9.77.1
    atr_r10.07.0
    cgc_l4.95.6
    cgc_r6.75.4
    cst_l2.45.3
    cst_r10.56.1
    Fornix3.05.4
    ifo_l2.95.4
    ifo_r12.86.3
    ilf_l3.25.4
    ilf_r9.16.8
    arc_l4.65.4
    • For each tract investigated, the percentage of the tract with a significant F statistic is given, along with the average F statistic along the tract (nonzero elements). Results were FDR corrected (q < 0.05).

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The Journal of Neuroscience: 35 (28)
Journal of Neuroscience
Vol. 35, Issue 28
15 Jul 2015
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Callosal Function in Pediatric Traumatic Brain Injury Linked to Disrupted White Matter Integrity
Emily L. Dennis, Monica U. Ellis, Sarah D. Marion, Yan Jin, Lisa Moran, Alexander Olsen, Claudia Kernan, Talin Babikian, Richard Mink, Christopher Babbitt, Jeffrey Johnson, Christopher C. Giza, Paul M. Thompson, Robert F. Asarnow
Journal of Neuroscience 15 July 2015, 35 (28) 10202-10211; DOI: 10.1523/JNEUROSCI.1595-15.2015

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Callosal Function in Pediatric Traumatic Brain Injury Linked to Disrupted White Matter Integrity
Emily L. Dennis, Monica U. Ellis, Sarah D. Marion, Yan Jin, Lisa Moran, Alexander Olsen, Claudia Kernan, Talin Babikian, Richard Mink, Christopher Babbitt, Jeffrey Johnson, Christopher C. Giza, Paul M. Thompson, Robert F. Asarnow
Journal of Neuroscience 15 July 2015, 35 (28) 10202-10211; DOI: 10.1523/JNEUROSCI.1595-15.2015
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Keywords

  • corpus callosum
  • DTI
  • ERP
  • interhemispheric transfer time
  • traumatic brain injury

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