The White Matter Microstructure of Basal Ganglia Related Atypical Sensory Processing in ASD

Background: Atypical sensory processing exists in individuals with ASD and white matter (WM) microstructure abnormalities may contribute to this. However, the underlying mechanisms have not been fully elucidated. Furthermore, it has been reported that atypical sensory processing is closely associated with other ASD symptoms, such as social impairment and repetitive restricted behavior and hence, it is assumed that these impairments share a common neural basis with atypical sensory processing. However, these assumptions remain to be clarified.

Objectives: This study aimed to investigate the relationship between WM microstructure and atypical sensory processing in ASD and the common neural basis with other ASD symptoms using diffusion tensor imaging (DTI) in an attempt to reveal the neural pathology of ASD, which contributes to atypical sensory processing.

Methods: We used DTI with a 3T scanner and the adolescent adult sensory profile (AASP) to investigate WM microstructure and abnormalities in sensory processing, respectively. We used MRI Cloud to analyze DTI data and calculated the fractional isotropy (FA) in each ROI. These data were acquired from 11 ASD patients without intellectual disabilities (FSIQ ≥ 80) and 14 sex-, handedness-, and intelligence-matched neurotypical subjects (NT).

Results: ASD individuals showed a higher score for both hypersensitivity (p < 0.01, d = 2.42) and hyposensitivity (p < 0.01, d = 1.17) on the AASP than did NT. A comparison of sensory processing for each sensory modality, revealed that ASD individuals obtained higher scores for touch hypersensitivity (p < 0.01, d = 1.66), activity hypersensitivity (p < 0.01, d = 2.39) and hyposensitivity (p < 0.01, d = 2.04), and auditory hypersensitivity (p < 0.01, d = 3.05) and hyposensitivity (p < 0.01, d = 1.48). In comparisons of FA, ASD had a significantly lower FA in the white matter of the left putamen (p = 0.03, d = 0.93) and right supramarginal gyrus (p = 0.03, d = 0.91) than did the NT. Correlational analyses demonstrated that FA in the left putamen was negatively correlated with activity hypersensitivity (r = –0.556, p < 0.01) and hyposensitivity (r = –0.538, p < 0.01), and auditory hypersensitivity (r = –0.449, p = 0.02) and hyposensitivity (r = –0.434, p = 0.03). Conversely, FA in the right supramarginal gyrus was not associated with any AASP scores (all p > 0.05). Moreover, FA in left putamen was negatively correlated with the total score on the Social Responsiveness Scale-2, indicating the decreased FA in the left putamen is associated with a more severe autism symptom (r = –0.457, p = 0.02). These results suggest that WM microstructure abnormalities in the left putamen are closely associated with ASD pathology.

Conclusions: Decreased FA in the left putamen is associated with atypical sensory processing of activity and auditory sense in ASD. Additionally, decreased FA in this area was also associated with more severe ASD symptoms. These results suggest that individuals with ASD have an abnormality in the WM microstructure in the left putamen, which is associated both with atypical sensory processing and other ASD symptoms.