Longitudinal Cortical Development During Adolescence and Young Adulthood in Autism Spectrum Disorder: Increased Cortical Thinning but Comparable Surface Area Changes

doi:10.1016/j.jaac.2015.03.007

Journal of the American Academy of Child & Adolescent Psychiatry

Volume 54, Issue 6, June 2015, Pages 464-469

https://doi.org/10.1016/j.jaac.2015.03.007 Get rights and content

Objective

Prior reports suggest that autism spectrum disorder (ASD) is associated with atypically excessive early brain growth. Recent cross-sectional studies suggest that later cortical development during adolescence/adulthood might also be aberrant, although longitudinal designs are required to evaluate atypical growth trajectories. The present study sought to examine longitudinal changes in cortical thickness and surface area among adolescents and young adults with ASD.

Method

Two high-resolution anatomic magnetic resonance imaging scans approximately 2 years apart were acquired from 17 adolescents with ASD and 18 typically developing (TD) adolescents, matched on age (range = 14–24 years), IQ, sex ratio, and handedness (70 scans total). The FreeSurfer image analysis suite was used to quantify longitudinal changes in cortical thickness and surface area.

Results

Accelerated cortical thinning for the ASD group as compared to the TD group was found in 2 areas in the left hemisphere, the posterior portion of ventral temporal cortex and superior parietal cortex (cluster corrected p < .01). For ventral temporal cortex, cortical thinning was associated with everyday executive function impairments, and thinner cortex at time 2 was correlated with ASD social symptoms. Differences in surface area changes were not detected.

Conclusion

The present longitudinal study extends prior cross-sectional research by demonstrating increased cortical thinning (in portions of temporal and parietal cortex) but comparable surface area growth rates in participants with ASD compared to TD controls during adolescence and into young adulthood. These findings provide further evidence for atypical cortical development beyond the early years in ASD, marked by increased cortical thinning in late adolescence/young adulthood.

Section snippets

Study Participants

A total of 17 adolescents and young adults with higher-functioning ASD and 18 TD adolescents and young adults matched on age, IQ, sex ratio, handedness, and time between scans (Table 1) underwent MRI scanning. Each participant provided 2 scans each, for a total of 70 structural MRI brain images (note that all of the participants described here were part of a much larger sample from which cross-sectional results based on a single MRI scan per individual have been previously reported12, 15). All

Results

There was accelerated cortical thinning for the group with ASD as compared to the TD group, with 2 areas in the left hemisphere, the posterior region of the ventral occipitotemporal cortex (ASD: mean = −0.20 mm/y, SD = 0.18; TD: mean = −0.02 mm/y, SD = 0.08) and superior parietal cortex (ASD: mean = −0.14 mm/y, SD = 0.10; TD: mean = −0.01 mm/y, SD = 0.06) surviving cluster correction (p < .01; Figure 1 and Table 2 [results are not meaningfully altered when a corrected threshold of p < .05 is

Discussion

The present longitudinal study complements and extends prior cross-sectional research by demonstrating extended cortical thinning in ASD during adolescence and into young adulthood. Specifically, in portions of the temporal and parietal lobes, thinning of the cortex appears to have slowed in TD individuals, whereas this process continues to occur in these regions in individuals with ASD during this developmental window. In contrast, SA, another component of cortical volume, appears to exhibit

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During later childhood and adolescence, there seems to be, on average, a slowing of brain growth and increased cortical thinning, with an inconsistent trajectory versus TD individuals, such that no case-control differences in whole brain volume are usually found in adults (Hernandez et al., 2015; Zielinski et al., 2014). However, some atypicalities affecting specific regions remain dynamic well into adulthood, and several cross-sectional and longitudinal studies have reported greater age-dependent reductions in brain volumes and cortical thinning affecting temporal and parietal areas during adolescence and early adulthood in ASD relative to TD individuals (Lange et al., 2015; Wallace et al., 2010; Wallace et al., 2015; Zielinski et al., 2014). On the contrary, findings for surface area suggest comparable growth rates in both populations, or even a smaller decline in these brain regions in ASD during this period (Mensen et al., 2017; Wallace et al., 2015).
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: This article is discussed in an editorial by Dr. Kelly N. Botteron on page 442.

: This work was supported by the Intramural Research Program at NIMH, National Institutes of Health (NIH) under grant number 1-ZIA-MH002920-05. Ethics approval for this study was granted by the NIH Combined Neuroscience Institutional Review Board under protocol number 10-M-0027.

: The authors wish to express their gratitude to the individuals and families who volunteered their time to contribute to this research.

: Disclosure: Dr. Kenworthy has received financial compensation as an author of the Behavior Rating Inventory of Executive Function, which is used in this study. Drs. Wallace, Giedd, Martin, Mr. Eisenberg, Ms. Robustelli, and Mr. Dankner report no biomedical financial interests or potential conflicts of interest.

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New researchLongitudinal Cortical Development During Adolescence and Young Adulthood in Autism Spectrum Disorder: Increased Cortical Thinning but Comparable Surface Area Changes

Objective

Method

Results

Conclusion

Section snippets

Study Participants

Results

Discussion

Neuron

Psychiatry Res

Biol Psychiatry

NeuroImage

NeuroImage

NeuroImage

NeuroImage

NeuroImage

NeuroImage

NeuroImage

J Am Acad Child Adolesc Psychiatry

Diagnostic and Statistical Manual of Mental Disorders

Compared to what? Early brain overgrowth in autism and the perils of population norms

Biol Psychiatry

Increased gray-matter volume in medication-naïve high-functioning children with autism spectrum disorder

Psychol Med

Distinct genetic influences on cortical surface area and cortical thickness

Cereb Cortex

How does your cortex grow?

J Neurosci

Early brain overgrowth in autism associated with an increase in cortical surface area before age 2 years

Arch Gen Psychiatry

Longitudinal changes in cortical thickness in autism and typical development

Brain

Measures of cortical grey matter structure and development in children with autism spectrum disorder

J Autism Dev Disord

Age-related temporal and parietal cortical thinning in autism spectrum disorders

Brain

New research
Longitudinal Cortical Development During Adolescence and Young Adulthood in Autism Spectrum Disorder: Increased Cortical Thinning but Comparable Surface Area Changes