Adverse Childhood Experience Is Associated With Disrupted White Matter Integrity in Autism Spectrum Disorder: A Diffusion Tensor Imaging Study.

Hiroaki Yoshikawa,Rio Ishida,Ryota Hashimoto,Manabu Makinodan,Kimihiko Kichikawa,Toshifumi Kishimoto,Naoko Kishimoto,Soichiro Kitamura,Fumihiko Yasuno,Masato Takahashi,Yuka Yasuda,Toshiteru Miyasaka,Kiwamu Matsuoka

doi:10.3389/fpsyt.2021.823260

Abstract

Individuals with autism spectrum disorder (ASD) have an increased risk of adverse childhood experiences (ACEs) than typically developed (TD) children. Since multiple lines of studies have suggested that ACEs are related to myelination in the frontal lobe, an exposure to ACEs can be associated with white matter microstructural disruption in the frontal lobe, which may be implicated in subsequential psychological deficits after the adulthood. In this study, we investigated the relationship between ACEs and microstructural integrity on frontal lobe-related white matter tracts using diffusion tensor imaging in 63 individuals with ASD and 38 TD participants. Using a tractography-based analysis, we delineated the uncinate fasciculus (UF), dorsal cingulum (Ci), and anterior thalamic radiation (ATR), which are involved in the neural pathology of ASD, and estimated each diffusion parameter. Compared to the TD participants, individuals with ASD displayed significantly lower fractional anisotropy (FA) and higher radial diffusivity (RD) in the left ATR. Then, ASD individuals exposed to severe ACEs displayed higher RD than those exposed to mild ACEs and TD participants in the left ATR. Moreover, the severity of ACEs, particularly neglect, correlated with lower FA and higher RD in the left UF and ATR in individuals with ASD, which was not observed in TD participants. These results suggest that an exposure to ACEs is associated with abnormality in the frontal lobe-related white matter in ASD.

Highlights

Autism spectrum disorder (ASD) is a major neurodevelopmental disorder characterized by impaired social communication and restricted repetitive behaviors [1]
There were no significant differences in the age, intelligence quotient (IQ), years of education, sex, handedness, and Autism-Spectrum Quotient Japanese version (AQ-J) and ADOS-2 scores between those with autism spectrum disorder (ASD) with high and low Child Abuse and Trauma Scale (CATS) scores (Supplementary Table 1)
adverse childhood experiences (ACEs) severity was correlated with white matter microstructural alterations in the left uncinate fasciculus (UF) and anterior thalamic radiation (ATR), of which neglect and demonstrated a significant correlation with the left UF and ATR, in addition emotional abuse indicated a significant correlation with the left ATR

Summary

Introduction

Autism spectrum disorder (ASD) is a major neurodevelopmental disorder characterized by impaired social communication and restricted repetitive behaviors [1]. These characteristics often make it difficult to establish appropriate interpersonal relationships in daily and social life. Children with developmental disabilities, including ASD, are likely to experience maltreatment, bullying, and maladaptation in the local community and social life [9]. These adverse childhood experiences (ACEs) reportedly cause poor selfesteem and motivation, resulting in subsequent psychiatric comorbidities, such as depression, anxiety, and substance abuse in adults with ASD [10]

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