Development of superficial white matter and its structural interplay with cortical gray matter in children and adolescents

Authors

  • Minjie Wu,

    Corresponding author
    1. Pediatric Brain Research and Intervention Center, Institute for Juvenile Research and Colbeth Clinic, Department of Psychiatry, University of Illinois at Chicago, Illinois
    2. Department of Psychiatry, University of Illinois at Chicago, Illinois
    • Correspondence to: Minjie Wu, Ph.D., Pediatric Brain Research and Intervention Center, 1747 West Roosevelt Road (M/C 747), Department of Psychiatry, University of Illinois at Chicago, IL 60608. E-mail: mwu@psych.uic.edu

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  • Lisa H. Lu,

    1. Pediatric Brain Research and Intervention Center, Institute for Juvenile Research and Colbeth Clinic, Department of Psychiatry, University of Illinois at Chicago, Illinois
    2. Department of Psychology, Roosevelt University, Illinois
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  • Allison Lowes,

    1. Pediatric Brain Research and Intervention Center, Institute for Juvenile Research and Colbeth Clinic, Department of Psychiatry, University of Illinois at Chicago, Illinois
    2. Department of Psychiatry, University of Illinois at Chicago, Illinois
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  • Shaolin Yang,

    1. Department of Psychiatry, University of Illinois at Chicago, Illinois
    2. Departments of Radiology and Bioengineering, University of Illinois at Chicago, Illinois
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  • Alessandra M. Passarotti,

    1. Pediatric Brain Research and Intervention Center, Institute for Juvenile Research and Colbeth Clinic, Department of Psychiatry, University of Illinois at Chicago, Illinois
    2. Department of Psychiatry, University of Illinois at Chicago, Illinois
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  • Xiaohong J. Zhou,

    1. Departments of Radiology and Bioengineering, University of Illinois at Chicago, Illinois
    2. Department of Neurosurgery, University of Illinois at Chicago, Illinois
    3. Center for Magnetic Resonance Research, University of Illinois at Chicago, Illinois
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  • Mani N. Pavuluri

    1. Pediatric Brain Research and Intervention Center, Institute for Juvenile Research and Colbeth Clinic, Department of Psychiatry, University of Illinois at Chicago, Illinois
    2. Department of Psychiatry, University of Illinois at Chicago, Illinois
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Abstract

Healthy human brain undergoes significant changes during development. The developmental trajectory of superficial white matter (SWM) is less understood relative to cortical gray matter (GM) and deep white matter. In this study, a multimodal imaging strategy was applied to vertexwise map SWM microstructure and cortical thickness to characterize their developmental pattern and elucidate SWM-GM associations in children and adolescents. Microscopic changes in SWM were evaluated with water diffusion parameters including fractional anisotropy (FA), mean diffusivity (MD), axial diffusivity (AD), and radial diffusivity (RD) in 133 healthy subjects aged 10–18 years. Results demonstrated distinct maturational patterns in SWM and GM. SWM showed increasing FA and decreasing MD and RD underneath bilateral motor sensory cortices and superior temporal auditory cortex, suggesting increasing myelination. A second developmental pattern in SWM was increasing FA and AD in bilateral orbitofrontal regions and insula, suggesting improved axonal coherence. These SWM patterns diverge from the more widespread GM maturation, suggesting that cortical thickness changes in adolescence are not explained by the encroachment of SWM myelin into the GM-WM boundary. Interestingly, age-independent intrinsic association between SWM and cortical GM seems to follow functional organization of polymodal and unimodal brain regions. Unimodal sensory areas showed positive correlation between GM thickness and FA whereas polymodal regions showed negative correlation. Axonal coherence and differences in interstitial neuron composition between unimodal and polymodal regions may account for these SWM-GM association patterns. Intrinsic SWM-GM relationships unveiled by neuroimaging in vivo can be useful for examining psychiatric disorders with known WM/GM disturbances. Hum Brain Mapp 35:2806–2816, 2014. © 2013 Wiley Periodicals, Inc.

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