Reduced Regional Gray Matter Volume in the Frontal Lobe May be the Neural Basis Underlying Atypical Sensory Processing in Autism Spectrum Disorder

Background: Atypical sensory processing, such as sensory hypersensitivity and hypoesthesia, exists in individuals with autism spectrum disorder (ASD), and affects social functioning. Although many studies have shown that sensory processing is an important feature for understanding ASD, the neural substrates underlying abnormal sensory processing in ASD individuals remain unknown. Current studies in typically developing subjects (TD) have suggested that atypical sensory processing is associated with reduced gray matter volume in the precentral gyrus; however, no studies have reported on reduced gray matter volume in the precentral gyrus in ASD individuals. Therefore, we hypothesize that a different neural basis contributes to atypical sensory processing in ASD.

Objectives: The present study aimed to investigate the structural abnormality that may be involved in atypical sensory processing in ASD.

Methods: We acquired structural MRI data using a 3T scanner and assessed individual differences in sensory processing using the Adolescent/Adult Sensory Profile questionnaire in adults with ASD (n = 11) without intellectual disabilities and psychotropic medications, and in sex, handedness-, and intelligence- matched TD subjects (n = 14). We used MRI Cloud to analyze structural MRI, which is a cloud-based tool for calculating the regional brain volume with a multi-atlas template. We used intracranial volume as a covariate in comparisons of regional gray matter volume and correlational analyses.

Results: ASD adults had significantly higher scores for low registrations (t = 4.969, p <0.001), sensory sensitivity (t = 4.554, p < 0.001), and sensory avoidance (t = 6.288, p < 0.001) than did TD subjects. The regional gray matter volume was lower in the ASD than in the TD adults in several brain regions, including the right middle frontal gyrus (F = 6.564, p = 0.018). Correlational analyses, revealed a negative relationship between gray matter volumes in the right middle frontal gyrus and hypersensitivity (r = –0.504, p = 0.012), thus indicating that reduced right middle frontal gyrus may be the neural basis underlying atypical sensory processing in ASD. Additionally, reduced gray matter volume in the right middle frontal gyrus was also associated with a more severe autism symptom measured using the Social Responsiveness Scale-2. (r = –0.427, p = 0.020), thus suggesting that reduced gray matter volume in the right middle frontal gyrus may be a common feature of atypical sensory processing and other ASD symptoms.

Conclusions: Current studies reveal that the right middle frontal gyrus is involved in reorienting attention from an exogenous stimulus. Our results suggest that reduced gray matter volume in MFG represents the neural underpinnings of sensory processing in ASD. Therefore, we propose that defective function in attention control may also be closely associated with hypersensitivity in ASD individuals. Additionally, reduced gray matter volume in the right frontal gyrus is a common neural basis underlying atypical sensory processing and other ASD symptoms such as social impairment and repetitive restricted behavior.