Atypical development of white matter microstructure of the corpus callosum in males with autism: a longitudinal investigation

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Abstract

Background

The corpus callosum is the largest white matter structure in the brain, and it is the most consistently reported to be atypical in diffusion tensor imaging studies of autism spectrum disorder. In individuals with typical development, the corpus callosum is known to undergo a protracted development from childhood through young adulthood. However, no study has longitudinally examined the developmental trajectory of corpus callosum in autism past early childhood.

Methods

The present study used a cohort sequential design over 9 years to examine age-related changes of the corpus callosum in 100 males with autism and 56 age-matched males with typical development from early childhood (when autism can first be reliably diagnosed) to mid-adulthood (after development of the corpus callosum has been completed) (3 to 41 years of age).

Results

The group with autism demonstrated a different developmental trajectory of white matter microstructure in the anterior corpus callosum’s (genu and body) fractional anisotropy, which suggests atypical brain maturation in these regions in autism. When analyses were broken down by age group, atypical developmental trajectories were present only in the youngest participants (10 years of age and younger). Significant main effects for group were found in terms of decreased fractional anisotropy across all three subregions of the corpus callosum (genu, body, and splenium) and increased mean diffusivity, radial diffusivity, and axial diffusivity in the posterior corpus callosum.

Conclusions

These longitudinal results suggest atypical early childhood development of the corpus callosum microstructure in autism that transitions into sustained group differences in adolescence and adulthood. This pattern of results provides longitudinal evidence consistent with a growing number of published studies and hypotheses regarding abnormal brain connectivity across the life span in autism.

Electronic supplementary material

The online version of this article (doi:10.1186/s13229-015-0001-8) contains supplementary material, which is available to authorized users.

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Most cited references 74

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Demyelination increases radial diffusivity in corpus callosum of mouse brain.

Sheng-Kwei Song, Jun Yoshino, Tuan Le … (2005)

Myelin damage, as seen in multiple sclerosis (MS) and other demyelinating diseases, impairs axonal conduction and can also be associated with axonal degeneration. Accurate assessments of these conditions may be highly beneficial in evaluating and selecting therapeutic strategies for patient management. Recently, an analytical approach examining diffusion tensor imaging (DTI) derived parameters has been proposed to assess the extent of axonal damage, demyelination, or both. The current study uses the well-characterized cuprizone model of experimental demyelination and remyelination of corpus callosum in mouse brain to evaluate the ability of DTI parameters to detect the progression of myelin degeneration and regeneration. Our results demonstrate that the extent of increased radial diffusivity reflects the severity of demyelination in corpus callosum of mouse brain affected by cuprizone treatment. Subsequently, radial diffusivity decreases with the progression of remyelination. Furthermore, radial diffusivity changes were specific to the time course of changes in myelin integrity as distinct from axonal injury, which was detected by betaAPP immunostaining and shown to be most extensive prior to demyelination. Radial diffusivity offers a specific assessment of demyelination and remyelination, as distinct from acute axonal damage.

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Microstructural maturation of the human brain from childhood to adulthood.

C. Lebel, L. Walker, A Leemans … (2008)

Brain maturation is a complex process that continues well beyond infancy, and adolescence is thought to be a key period of brain rewiring. To assess structural brain maturation from childhood to adulthood, we charted brain development in subjects aged 5 to 30 years using diffusion tensor magnetic resonance imaging, a novel brain imaging technique that is sensitive to axonal packing and myelination and is particularly adept at virtually extracting white matter connections. Age-related changes were seen in major white matter tracts, deep gray matter, and subcortical white matter, in our large (n=202), age-distributed sample. These diffusion changes followed an exponential pattern of maturation with considerable regional variation. Differences observed in developmental timing suggest a pattern of maturation in which areas with fronto-temporal connections develop more slowly than other regions. These in vivo results expand upon previous postmortem and imaging studies and provide quantitative measures indicative of the progression and magnitude of regional human brain maturation.

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Longitudinal development of human brain wiring continues from childhood into adulthood.

Catherine Lebel, Christian Beaulieu (2011)

Healthy human brain development is a complex process that continues during childhood and adolescence, as demonstrated by many cross-sectional and several longitudinal studies. However, whether these changes end in adolescence is not clear. We examined longitudinal white matter maturation using diffusion tensor tractography in 103 healthy subjects aged 5-32 years; each volunteer was scanned at least twice, with 221 total scans. Fractional anisotropy (FA) and mean diffusivity (MD), parameters indicative of factors including myelination and axon density, were assessed in 10 major white matter tracts. All tracts showed significant nonlinear development trajectories for FA and MD. Significant within-subject changes occurred in the vast majority of children and early adolescents, and these changes were mostly complete by late adolescence for projection and commissural tracts. However, association tracts demonstrated postadolescent within-subject maturation of both FA and MD. Diffusion parameter changes were due primarily to decreasing perpendicular diffusivity, although increasing parallel diffusivity contributed to the prolonged increases of FA in association tracts. Volume increased significantly with age for most tracts, and longitudinal measures also demonstrated postadolescent volume increases in several association tracts. As volume increases were not directly associated with either elevated FA or reduced MD between scans, the observed diffusion parameter changes likely reflect microstructural maturation of brain white matter tracts rather than just gross anatomy.

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Author and article information

Contributors

Brittany G Travers: btravers@wisc.edu

Do P M Tromp: tromp@wisc.edu

Nagesh Adluru: adluru@wisc.edu

Nicholas Lange: nicholas_lange@hms.harvard.edu

Dan Destiche: ddestiche@gmail.com

Chad Ennis: chad.m.ennis@gmail.com

Jared A Nielsen: jared.nielsen@hsc.utah.edu

Alyson L Froehlich: a.froehlich@utah.edu

Molly B D Prigge: Molly.Prigge@hsc.utah.edu

P Thomas Fletcher: fletcher@sci.utah.edu

Jeffrey S Anderson: andersonjeffs@gmail.com

Brandon A Zielinski: brandon.zielinski@hsc.utah.edu

Erin D Bigler: erin_bigler@byu.edu

Janet E Lainhart: jlainhart@wisc.edu

Andrew L Alexander: alalexander2@wisc.edu

Journal

Journal ID (nlm-ta): Mol Autism

Journal ID (iso-abbrev): Mol Autism

Title: Molecular Autism

Publisher: BioMed Central (London )

ISSN (Electronic): 2040-2392

Publication date (Electronic): 11 March 2015

Publication date PMC-release: 11 March 2015

Publication date Collection: 2015

Volume: 6

Electronic Location Identifier: 15

Affiliations

[ ]Occupational Therapy Program, Department of Kinesiology, University of Wisconsin-Madison, Madison, WI USA

[ ]Waisman Center, University of Wisconsin-Madison, 1500 Highland Avenue, Madison, WI 53705 USA

[ ]Department of Psychiatry, University of Wisconsin-Madison, Madison, WI USA

[ ]Department of Psychiatry, Harvard School of Medicine, Boston, MA USA

[ ]Neurostatistics Laboratory, McLean Hospital, Belmont, MA USA

[ ]Interdepartmental Program in Neuroscience, University of Utah, Salt Lake City, UT USA

[ ]Scientific Computing and Imaging Institute, University of Utah, Salt Lake City, UT USA

[ ]Department of Radiology, University of Utah, Salt Lake City, UT USA

[ ]Department of Pediatrics, University of Utah and Primary Children’s Medical Center, Salt Lake City, UT USA

[ ]School of Computing, University of Utah, Salt Lake City, UT USA

[ ]Department of Neurology, University of Utah, Salt Lake City, UT USA

[ ]Department of Psychology, Brigham Young University, Provo, UT USA

[ ]Neuroscience Center, Brigham Young University, Provo, UT 84602 USA

[ ]Department of Medical Physics, University of Wisconsin-Madison, Madison, WI USA

Article

Publisher ID: 1

DOI: 10.1186/s13229-015-0001-8

PMC ID: 4359536

PubMed ID: 25774283

SO-VID: c8c949f9-7b6f-47de-a8d1-dac889f3b1e4

License:

This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 11 October 2014

Date accepted : 26 January 2015

Custom metadata

ScienceOpen disciplines: Neurosciences

Keywords: diffusion tensor imaging,brain development,developmental disorders,childhood,adolescence,adulthood

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ScienceOpen disciplines: Neurosciences

Keywords: diffusion tensor imaging, brain development, developmental disorders, childhood, adolescence, adulthood

Atypical development of white matter microstructure of the corpus callosum in males with autism: a longitudinal investigation

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Hearing Loss and Restoration

Most cited references 74

Demyelination increases radial diffusivity in corpus callosum of mouse brain.

Microstructural maturation of the human brain from childhood to adulthood.

Longitudinal development of human brain wiring continues from childhood into adulthood.

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