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Research ArticleNew Research, Development

Differential Rates of Perinatal Maturation of Human Primary and Nonprimary Auditory Cortex

Brian B. Monson, Zach Eaton-Rosen, Kush Kapur, Einat Liebenthal, Abraham Brownell, Christopher D. Smyser, Cynthia E. Rogers, Terrie E. Inder, Simon K. Warfield and Jeffrey J. Neil
eNeuro 15 January 2018, 5 (1) ENEURO.0380-17.2017; DOI: https://doi.org/10.1523/ENEURO.0380-17.2017
Brian B. Monson
1Department of Pediatric Newborn Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115
2Department of Radiology, Boston Children’s Hospital, Harvard Medical School, Boston, MA 02115
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Zach Eaton-Rosen
3Translational Imaging Group, University College London, London, WC1E 7JE United Kingdom
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Kush Kapur
4Department of Neurology, Boston Children’s Hospital, Harvard Medical School, Boston, MA 02115
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Einat Liebenthal
5Department of Psychiatry, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115
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  • ORCID record for Einat Liebenthal
Abraham Brownell
1Department of Pediatric Newborn Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115
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Christopher D. Smyser
6Department of Neurology, Washington University School of Medicine, St. Louis, MO 63130
7Department of Pediatrics, Washington University School of Medicine, St. Louis, MO 63130
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Cynthia E. Rogers
7Department of Pediatrics, Washington University School of Medicine, St. Louis, MO 63130
8Department of Psychiatry, Washington University School of Medicine, St. Louis, MO 63130
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Terrie E. Inder
1Department of Pediatric Newborn Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115
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Simon K. Warfield
2Department of Radiology, Boston Children’s Hospital, Harvard Medical School, Boston, MA 02115
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Jeffrey J. Neil
4Department of Neurology, Boston Children’s Hospital, Harvard Medical School, Boston, MA 02115
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Figures

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  • Figure 1.
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    Figure 1.

    Development of the left hemisphere temporal plane from 28 to 40 weeks PMA. HG (demarcated with white dashed lines) is forming by 28 weeks PMA and has an adult-like appearance by 40 weeks PMA. pAC and nAC are located in medial and lateral HG, respectively.

  • Figure 2.
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    Figure 2.

    Flowchart detailing retention and follow-up of the very preterm cohort. TEA, term-equivalent age.

  • Figure 3.
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    Figure 3.

    Changes in GM diffusion parameters with increasing age along the length of HG from medial (primary) to lateral (nonprimary). Changes are shown for (A) FA, (B) MD, (C) AD, and (D) RD. Curves are separated by age group (in weeks), indicated by color. Shading indicates ±1 SE. FT, full-term controls.

  • Figure 4.
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    Figure 4.

    Changes in GM diffusion parameters as a function of PMA for primary (blue) and nonprimary (green) auditory cortex in HG. Changes are shown for (A) FA, (B) MD, (C) AD, and (D) RD. Curves represent results from linear mixed-effects models. Values for full-term controls are denoted by crosses (×).

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    Figure 5.

    Changes in WM diffusion parameters with increasing age along the length of HG from medial (primary) to lateral (nonprimary). Changes are shown for (A) FA, (B) MD, (C) AD, and (D) RD. Curves are separated by age group (in weeks), indicated by color. Shading indicates ±1 SE. FT, full-term controls.

  • Figure 6.
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    Figure 6.

    Changes in WM diffusion parameters as a function of PMA for primary (blue) and nonprimary (green) auditory cortex in HG. Changes are shown for (A) FA, (B) MD, (C) AD, and (D) RD. Curves represent results from linear mixed-effects models. Values for full-term controls are denoted by crosses (×).

Tables

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    Table 1.

    Sample characteristics for children followed up at two years old, separated by room type

    Open bay (n = 22)Private room (n = 24)p value
    Mean (SD)
    Birth GA (weeks)26.3 (1.7)27 (2.1)0.20
    Birthweight (grams)883 (242)983 (250)0.17
    Length of stay (days)92 (18)91 (25)0.81
    PMA at scan (weeks)37.8 (1.2)38.3 (1.5)0.16
    Maternal age (years)29.1 (8.5)29.8 (7.3)0.79
    Social risk score (out of 5)1.45 (1.34)1.30 (1.26)0.70
    n (%)
    Male10 (45)10 (42)0.80
    SGA1 (5)1 (4)0.95
    Infection4 (18)2 (9)0.38
    BPD12 (55)15 (68)0.35
    • GA, gestational age; SGA, small for gestational age; BPD, bronchopulmonary dysplasia.

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    Table 2.

    Regression coefficients showing effects of age and region on diffusion parameter changes

    Age2AgeRegionAge × region
    Coefficientp valueCoefficientp valueCoefficientp valueCoefficientp value
    GMFA0.594<0.001−13.163<0.001−20.0760.0130.9260.304
    MD——−4.6030.001−37.8630.028−3.5330.068
    AD——−12.055<0.001−94.541<0.001−1.7290.417
    RD——−1.3330.388−16.4400.379−4.4570.035
    WMFA——3.096<0.00124.853<0.001−1.4810.036
    MD−0.9760.006−10.1890.081−189.456<0.0017.9760.001
    AD−0.7810.044−11.0680.092−164.175<0.0015.6830.033
    RD−1.0600.003−9.9590.088−202.240<0.0019.130<0.001
    • Bold values indicate significant effects of region and age × region interactions. Coefficient values are multiplied by 103.

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    Table 3.

    Regression coefficients showing associations between diffusion parameter values at term-equivalent age and language ability at two years old, controlling for room type

    ReceptiveExpressive
    CoefficientCorrected p valueR2CoefficientCorrected p valueR2
    pGMFA−7.08>0.990.0410.83>0.990.09
    MD9.43>0.990.079.07>0.990.10
    AD6.26>0.990.059.91>0.990.12
    RD9.10>0.990.076.51>0.990.09
    nGMFA−10.46>0.990.06−29.390.040.23
    MD12.960.100.1610.410.680.14
    AD8.690.330.121.63>0.990.08
    RD11.740.140.1513.120.170.18
    pWMFA14.06>0.990.06−2.71>0.990.08
    MD2.97>0.990.049.63>0.990.12
    AD5.19>0.990.067.96>0.990.12
    RD0.44>0.990.037.87>0.990.11
    nWMFA−12.37>0.990.05−14.84>0.990.10
    MD0.26>0.990.033.86>0.990.09
    AD−0.30>0.990.032.27>0.990.08
    RD0.57>0.990.034.38>0.990.10
    • Bold values indicate a significant association. Coefficient values for diffusivity measures are multiplied by 103. p/nGM, primary/nonprimary GM.

    • View popup
    Table 4.

    Regression coefficients showing associations between diffusion parameter values at term-equivalent age and language ability at two years old, controlling for room type, social risk, and birth gestational age

    ReceptiveExpressive
    CoefficientCorrected p valueR2CoefficientCorrected p valueR2
    pGMFA−0.83>0.990.088.66>0.990.09
    MD9.11>0.990.129.07>0.990.11
    AD7.41>0.990.129.55>0.990.12
    RD8.08>0.990.126.85>0.990.10
    nGMFA−9.10>0.990.10−32.590.030.26
    MD12.110.220.1912.850.370.17
    AD8.050.550.162.62>0.990.09
    RD11.150.300.1816.230.070.23
    pWMFA15.74>0.990.12−3.71>0.990.08
    MD1.78>0.990.099.53>0.990.13
    AD4.39>0.990.107.80>0.990.12
    RD−0.50>0.990.087.98>0.990.11
    nWMFA−8.82>0.990.09−19.28>0.990.11
    MD−0.06>0.990.085.11>0.990.11
    AD−0.47>0.990.093.10>0.990.09
    RD0.20>0.990.085.68>0.990.12
    • Bold values indicate a significant association. Coefficient values for diffusivity measures are multiplied by 103. p/nGM, primary/nonprimary GM.

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Differential Rates of Perinatal Maturation of Human Primary and Nonprimary Auditory Cortex
Brian B. Monson, Zach Eaton-Rosen, Kush Kapur, Einat Liebenthal, Abraham Brownell, Christopher D. Smyser, Cynthia E. Rogers, Terrie E. Inder, Simon K. Warfield, Jeffrey J. Neil
eNeuro 15 January 2018, 5 (1) ENEURO.0380-17.2017; DOI: 10.1523/ENEURO.0380-17.2017

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Differential Rates of Perinatal Maturation of Human Primary and Nonprimary Auditory Cortex
Brian B. Monson, Zach Eaton-Rosen, Kush Kapur, Einat Liebenthal, Abraham Brownell, Christopher D. Smyser, Cynthia E. Rogers, Terrie E. Inder, Simon K. Warfield, Jeffrey J. Neil
eNeuro 15 January 2018, 5 (1) ENEURO.0380-17.2017; DOI: 10.1523/ENEURO.0380-17.2017
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Keywords

  • audition
  • cortical development
  • diffusion tensor imaging
  • neuroimaging
  • preterm infants

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