Increased Gray Matter Volume and Resting-State Functional Connectivity in Somatosensory Cortex and their Relationship with Autistic Symptoms in Young Boys with Autism Spectrum Disorder

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Abstract

Autism spectrum disorder (ASD) has been widely recognized as a complex neurodevelopmental disorder. A large number of neuroimaging studies suggest abnormalities in brain structure and function of patients with ASD, but there is still no consistent conclusion. We sought to investigate both of the structural and functional brain changes in 3–7-year-old children with ASD compared with typically developing controls (TDs), and to assess whether these alterations are associated with autistic behavioral symptoms. Firstly, we applied an optimized method of voxel-based morphometry (VBM) analysis on structural magnetic resonance imaging (sMRI) data to assess the differences of gray matter volume (GMV) between 31 autistic boys aged 3–7 and 31 age- and handness-matched male TDs. Secondly, we used clusters with between-group differences as seed regions to generate intrinsic functional connectivity maps based on resting-state functional connectivity magnetic resonance imaging (rs-fcMRI) in order to evaluate the functional impairments induced by structural alterations. Brain-behavior correlations were assessed among GMV, functional connectivity and symptom severity in children with ASD. VBM analyses revealed increased GMV in left superior temporal gyrus (STG) and left postcentral gyrus (PCG) in ASD children, comparing with TDs. Using left PCG as a seed region, ASD children displayed significantly higher positive connectivity with right angular gyrus (AG) and greater negative connectivity with right superior parietal gyrus (SPG) and right superior occipital gyrus (SOG), which were associated with the severity of symptoms in social interaction, communication and self-care ability. We suggest that stronger functional connectivity between left PCG and right AG, SPG, and SOG detected in young boys with ASD may serve as important indicators of disease severity. Our study provided preliminary functional evidence that may underlie impaired higher-order multisensory integration in ASD children.

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Most cited references 37

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Unusual brain growth patterns in early life in patients with autistic disorder: an MRI study.

E Courchesne, C. Karns, H Davis … (2001)

To quantify developmental abnormalities in cerebral and cerebellar volume in autism. The authors studied 60 autistic and 52 normal boys (age, 2 to 16 years) using MRI. Thirty autistic boys were diagnosed and scanned when 5 years or older. The other 30 were scanned when 2 through 4 years of age and then diagnosed with autism at least 2.5 years later, at an age when the diagnosis of autism is more reliable. Neonatal head circumferences from clinical records were available for 14 of 15 autistic 2- to 5-year-olds and, on average, were normal (35.1 +/- 1.3 cm versus clinical norms: 34.6 +/- 1.6 cm), indicative of normal overall brain volume at birth; one measure was above the 95th percentile. By ages 2 to 4 years, 90% of autistic boys had a brain volume larger than normal average, and 37% met criteria for developmental macrencephaly. Autistic 2- to 3-year-olds had more cerebral (18%) and cerebellar (39%) white matter, and more cerebral cortical gray matter (12%) than normal, whereas older autistic children and adolescents did not have such enlarged gray and white matter volumes. In the cerebellum, autistic boys had less gray matter, smaller ratio of gray to white matter, and smaller vermis lobules VI-VII than normal controls. Abnormal regulation of brain growth in autism results in early overgrowth followed by abnormally slowed growth. Hyperplasia was present in cerebral gray matter and cerebral and cerebellar white matter in early life in patients with autism.

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Brain growth across the life span in autism: age-specific changes in anatomical pathology.

Eric Courchesne, Kathleen Campbell, Stephanie Solso (2011)

Autism is marked by overgrowth of the brain at the earliest ages but not at older ages when decreases in structural volumes and neuron numbers are observed instead. This has led to the theory of age-specific anatomic abnormalities in autism. Here we report age-related changes in brain size in autistic and typical subjects from 12 months to 50 years of age based on analyses of 586 longitudinal and cross-sectional MRI scans. This dataset is several times larger than the largest autism study to date. Results demonstrate early brain overgrowth during infancy and the toddler years in autistic boys and girls, followed by an accelerated rate of decline in size and perhaps degeneration from adolescence to late middle age in this disorder. We theorize that underlying these age-specific changes in anatomic abnormalities in autism, there may also be age-specific changes in gene expression, molecular, synaptic, cellular, and circuit abnormalities. A peak age for detecting and studying the earliest fundamental biological underpinnings of autism is prenatal life and the first three postnatal years. Studies of the older autistic brain may not address original causes but are essential to discovering how best to help the older aging autistic person. Lastly, the theory of age-specific anatomic abnormalities in autism has broad implications for a wide range of work on the disorder including the design, validation, and interpretation of animal model, lymphocyte gene expression, brain gene expression, and genotype/CNV-anatomic phenotype studies. Copyright © 2010 Elsevier B.V. All rights reserved.

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Reconceptualizing functional brain connectivity in autism from a developmental perspective

Lucina Q. Uddin, Kaustubh Supekar, Vinod Menon (2013)

While there is almost universal agreement amongst researchers that autism is associated with alterations in brain connectivity, the precise nature of these alterations continues to be debated. Theoretical and empirical work is beginning to reveal that autism is associated with a complex functional phenotype characterized by both hypo- and hyper-connectivity of large-scale brain systems. It is not yet understood why such conflicting patterns of brain connectivity are observed across different studies, and the factors contributing to these heterogeneous findings have not been identified. Developmental changes in functional connectivity have received inadequate attention to date. We propose that discrepancies between findings of autism related hypo-connectivity and hyper-connectivity might be reconciled by taking developmental changes into account. We review neuroimaging studies of autism, with an emphasis on functional magnetic resonance imaging studies of intrinsic functional connectivity in children, adolescents and adults. The consistent pattern emerging across several studies is that while intrinsic functional connectivity in adolescents and adults with autism is generally reduced compared with age-matched controls, functional connectivity in younger children with the disorder appears to be increased. We suggest that by placing recent empirical findings within a developmental framework, and explicitly characterizing age and pubertal stage in future work, it may be possible to resolve conflicting findings of hypo- and hyper-connectivity in the extant literature and arrive at a more comprehensive understanding of the neurobiology of autism.

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Author and article information

Contributors

Jia Wang: URI : http://loop.frontiersin.org/people/437454/overview

Kuang Fu: URI : http://loop.frontiersin.org/people/466106/overview

Lei Chen: URI : http://loop.frontiersin.org/people/434016/overview

Xujun Duan: URI : http://loop.frontiersin.org/people/466114/overview

Xiaonan Guo: URI : http://loop.frontiersin.org/people/466119/overview

Heng Chen: URI : http://loop.frontiersin.org/people/466109/overview

Qiong Wu: URI : http://loop.frontiersin.org/people/441194/overview

Lijie Wu: URI : http://loop.frontiersin.org/people/437424/overview

Huafu Chen: URI : http://loop.frontiersin.org/people/236962/overview

Journal

Journal ID (nlm-ta): Front Physiol

Journal ID (iso-abbrev): Front Physiol

Journal ID (publisher-id): Front. Physiol.

Title: Frontiers in Physiology

Publisher: Frontiers Media S.A.

ISSN (Electronic): 1664-042X

Publication date (Electronic): 15 August 2017

Publication date Collection: 2017

Volume: 8

Electronic Location Identifier: 588

Affiliations

[1] ¹Department of Children's and Adolescent Health, Public Health College of Harbin Medical University Harbin, China

[2] ²Department of MR Diagnosis, The Second Affiliated Hospital of Harbin Medical University Harbin, China

[3] ³Key Laboratory for NeuroInformation of Ministry of Education, School of Life Science and Technology and Center for Information in BioMedicine, University of Electronic Science and Technology of China Chengdu, China

Author notes

Edited by: Chunhua Bian, Nanjing University, China

Reviewed by: John G. Holden, University of Cincinnati, United States; Wei Chen, Fudan University, China

*Correspondence: Lijie Wu wulijiehyd@ 123456126.com

Huafu Chen chenhf@ 123456uestc.edu.cn

This article was submitted to Fractal Physiology, a section of the journal Frontiers in Physiology

†These authors have contributed equally to this work.

Article

DOI: 10.3389/fphys.2017.00588

PMC ID: 5559537

PubMed ID: 28861001

SO-VID: 8fd01824-3a20-4a0a-b471-d4a3bb8a0500

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

History

Date received : 11 May 2017

Date accepted : 31 July 2017

Page count

Figures: 2, Tables: 3, Equations: 0, References: 50, Pages: 10, Words: 7365

Funding

Funded by: National Natural Science Foundation of China 10.13039/501100001809

Award ID: 81302444

Award ID: 61533006

Award ID: 61673089

Funded by: Harbin Medical University 10.13039/100010722

Award ID: 2017JCZX19

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Increased Gray Matter Volume and Resting-State Functional Connectivity in Somatosensory Cortex and their Relationship with Autistic Symptoms in Young Boys with Autism Spectrum Disorder

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Most cited references 37

Unusual brain growth patterns in early life in patients with autistic disorder: an MRI study.

Brain growth across the life span in autism: age-specific changes in anatomical pathology.

Reconceptualizing functional brain connectivity in autism from a developmental perspective

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