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Research ArticleNew Research, Disorders of the Nervous System

Carriage of Supernumerary Sex Chromosomes Decreases the Volume and Alters the Shape of Limbic Structures

Ajay Nadig, Paul K. Reardon, Jakob Seidlitz, Cassidy L. McDermott, Jonathan D. Blumenthal, Liv S. Clasen, Francois Lalonde, Jason P. Lerch, M. Mallar Chakravarty and Armin Raznahan
eNeuro 19 October 2018, 5 (5) ENEURO.0265-18.2018; DOI: https://doi.org/10.1523/ENEURO.0265-18.2018
Ajay Nadig
1Developmental Neurogenomics Unit, Human Genetics Branch, National Institute of Mental Health, Bethesda, Maryland 20892
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Paul K. Reardon
1Developmental Neurogenomics Unit, Human Genetics Branch, National Institute of Mental Health, Bethesda, Maryland 20892
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Jakob Seidlitz
1Developmental Neurogenomics Unit, Human Genetics Branch, National Institute of Mental Health, Bethesda, Maryland 20892
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Cassidy L. McDermott
1Developmental Neurogenomics Unit, Human Genetics Branch, National Institute of Mental Health, Bethesda, Maryland 20892
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Jonathan D. Blumenthal
1Developmental Neurogenomics Unit, Human Genetics Branch, National Institute of Mental Health, Bethesda, Maryland 20892
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Liv S. Clasen
1Developmental Neurogenomics Unit, Human Genetics Branch, National Institute of Mental Health, Bethesda, Maryland 20892
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Francois Lalonde
1Developmental Neurogenomics Unit, Human Genetics Branch, National Institute of Mental Health, Bethesda, Maryland 20892
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Jason P. Lerch
2 Department of Medical Biophysics, University of Toronto, Toronto, Ontario M5T 1R8, Canada
3Neurosciences and Mental Health, the Hospital for Sick Children, Toronto, Ontario M5T 3H7, Canada
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M. Mallar Chakravarty
4Cerebral Imaging Centre, Douglas Mental Health University Institute, McGill University, Montreal, Quebec H3A OG4, Canada
5Department of Psychiatry, McGill University, Montreal, Quebec H3A OG4, Canada
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Armin Raznahan
1Developmental Neurogenomics Unit, Human Genetics Branch, National Institute of Mental Health, Bethesda, Maryland 20892
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    Figure 1.

    Bulk volume analysis of amygdala and hippocampus. (A) Total brain volume (tbv), amygdala, and hippocampus volume across karyotype groups, relative to typically developing males (XY). (B) Scaling of amygdala and hippocampus volume in the allometric sample (amygdala β1 = 0.89; hippocampus β1 = 0.76). (C) Comparisons of regional volume across sex and sex chromosome complement. FDR-corrected log(p) values are shown. Presence of color indicates statistical significance, and color identity/sign indicates direction of effect: for contrast A-B, blue and negative values indicate smaller volume in A versus B, red and positive value indicate larger volume in A versus B.

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    Figure 2.

    Surface-based analysis of amygdala and hippocampus shape. (A) Map of vertex-wise surface area scaling coefficients from log-log linear model with total bilateral region surface area. (B) Binarized surface maps showing areas of significant surface area contraction (blue) or expansion (red) for each patient contrast. (C) Spatial correlation of uncorrected t-statistic maps demonstrating convergence of SCA effects. AMY: Amygdala, HC: Hippocampus.

Tables

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    Table 1.

    Participant characteristics

    Participant characteristics
    GroupXXXYXXXXXYXYYXXYYXXXXYAllometric
    sample
    n877928562519579 (34 F)
    Age, y
    Mean (SD)12.7 (5.1)12.7 (4.6)12.3 (5.7)12.7 (4.9)12.2 (4.9)14.0 (5.5)12.9 (4.8)13.0 (0.6)
    Range5.4–25.15.2–25.55.0–24.85.2–26.05.7–23.05.0–23.07.7–17.212.0–14.0
    FSIQ
    Mean (SD)*113.9 (12.3)116.6 (13.3)94.1 (14.2)97.6 (17.1)91.0 (14.6)86.9 (12.9)55.7 (7.23)116.3 (12.4)
    SES
    Mean (SD)*47.3 (17.1)48.0 (21.3)40.9 (15.9)56.0 (20.7)58.1 (22.4)45.5 (22.6)68.8 (22.4)34.1 (19.7)
    • FSIQ, Full scale IQ; SES, socioeconomic status.

    • ↵* p < 0.01 for omnibus test of significant variation across groups in core sample.

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    Table 2.

    Descriptive statistics for bulk volume analysis

    Descriptive Statistics by Karyotype GroupOmnibus test for group differences
    Karyotype (n)XX (87)XY (79)XXX (28)XXY (56)XYY (25)XXYY (19)XXXXY (5)F statistic−log(p)
    Total brain volume, cm320.9319.67
        Mean1261139211791287141812911131
        SEM9.7413.822.817.824.929.736.1
    Amygdala, cm323.7822.15
        Mean2.322.542.052.262.432.191.86
        SEM0.020.030.040.030.060.050.06
    Hippocampus, cm39.648.95
        Mean4.304.573.984.324.684.333.82
        SEM0.040.050.070.070.120.120.13
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Carriage of Supernumerary Sex Chromosomes Decreases the Volume and Alters the Shape of Limbic Structures
Ajay Nadig, Paul K. Reardon, Jakob Seidlitz, Cassidy L. McDermott, Jonathan D. Blumenthal, Liv S. Clasen, Francois Lalonde, Jason P. Lerch, M. Mallar Chakravarty, Armin Raznahan
eNeuro 19 October 2018, 5 (5) ENEURO.0265-18.2018; DOI: 10.1523/ENEURO.0265-18.2018

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Carriage of Supernumerary Sex Chromosomes Decreases the Volume and Alters the Shape of Limbic Structures
Ajay Nadig, Paul K. Reardon, Jakob Seidlitz, Cassidy L. McDermott, Jonathan D. Blumenthal, Liv S. Clasen, Francois Lalonde, Jason P. Lerch, M. Mallar Chakravarty, Armin Raznahan
eNeuro 19 October 2018, 5 (5) ENEURO.0265-18.2018; DOI: 10.1523/ENEURO.0265-18.2018
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Keywords

  • amygdala
  • CNV
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  • sex chromosome aneuploidy

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