Autism spectrum disorder (ASD) is characterized neurophysiologically by, among other things, functional connectivity abnormalities in the brain. Recent evidence suggests that the nature of these functional connectivity abnormalities might not be uniform throughout maturation. Comparing between adolescents and young adults (ages 14-21) with ASD and age- and IQ-matched typically developing (TD) individuals, we previously documented, using magnetoencephalography (MEG) data, that local functional connectivity in the fusiform face areas (FFA) and long-range functional connectivity between FFA and three higher order cortical areas were all reduced in ASD. Given the findings on abnormal maturation trajectories in ASD, we tested whether these results extend to preadolescent children (ages 7-13). We found that both local and long-range functional connectivity were in fact normal in this younger age group in ASD. Combining the two age groups, we found that local and long-range functional connectivity measures were positively correlated with age in TD, but negatively correlated with age in ASD. Last, we showed that local functional connectivity was the primary feature in predicting age in ASD group, but not in the TD group. Furthermore, local functional connectivity was only correlated with ASD severity in the older group. These results suggest that the direction of maturation of functional connectivity for processing of faces from childhood to young adulthood is itself abnormal in ASD, and that during the processing of faces, these trajectory abnormalities are more pronounced for local functional connectivity measures than they are for long-range functional connectivity measures.

The processing of information conveyed by faces is a critical component of social communication. While the neurophysiology of processing upright faces has been studied extensively in autism spectrum disorder (ASD), less is known about the neurophysiological abnormalities associated with processing inverted faces in ASD. We used magnetoencephalography (MEG) to study both long‐range and local functional connectivity, with the latter assessed using local cross‐frequency coupling, in response to inverted faces stimuli, in 7–18 years old individuals with ASD and age and IQ matched typically developing (TD) individuals. We found abnormally reduced coupling between the phase of the alpha rhythm and the amplitude of the gamma rhythm in the fusiform face area (FFA) in response to inverted faces, as well as reduced long‐range functional connectivity between the FFA and the inferior frontal gyrus (IFG) in response to inverted faces in the ASD group. These group differences were absent in response to upright faces. The magnitude of functional connectivity between the FFA and the IFG was significantly correlated with the severity of ASD, and FFA‐IFG long‐range functional connectivity increased with age in TD group, but not in the ASD group. Our findings suggest that both local and long‐range functional connectivity are abnormally reduced in children with ASD when processing inverted faces, and that the pattern of abnormalities associated with the processing of inverted faces differs from the pattern of upright faces in ASD, likely due to the presumed greater reliance on top‐down regulations necessary for efficient processing of inverted faces. Lay Summary We found alterations in the neurophysiological responses to inverted faces in children with ASD, that were not reflected in the evoked responses, and were not observed in the responses to upright faces. These alterations included reduced local functional connectivity in the fusiform face area (FFA), and decreased long‐range alpha‐band modulated functional connectivity between the FFA and the left IFG. The magnitude of long‐range functional connectivity between the FFA and the inferior frontal gyrus was correlated with the severity of ASD.

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