fMRI evidence of reduced emotional face processing automaticity in autism spectrum disorders

Background: Recent evidence suggests that a rapid, automatic face-detection system is supported by subcortical structures including the amygdala, pulvinar, and superior colliculus. Early emerging abnormalities in these structures may be related to reduced social orienting in children with autism, and subsequently, to aberrant development of cortical circuits involved in face processing.

Objectives: To investigate functional abnormalities in the subcortical face processing system in adults with autism spectrum disorders (ASD).

Methods: Twenty-eight individuals with ASD and 25 controls group-matched on age, IQ, and behavioral performance were included in the fMRI study. The ASD group met diagnostic criteria on the ADI-R, ADOS-G, and DSM-IV. Stimuli were 78 photos of adults with a fearful facial expression and 78 perceptual masks created by scrambling the images. Supraliminal (23 ms) presentations of masked fearful faces were compared to scrambled-image-only blocks using FSL. Participants were instructed to press a button when pseudo-randomly presented fixation crosses appeared to ensure attention to the stimuli.

Results: Both the ASD and control groups showed significant activation in bilateral fusiform gyri and inferior occipital lobes. The control group exhibited additional significant clusters in the right amygdala, right pulvinar, and bilateral superior colliculi. In the direct group comparison, the controls showed significantly greater activation in the left amygdala, right fusiform gyrus, right pulvinar, bilateral superior colliculi, and right orbital frontal lobe. No brain region showed significantly greater activation in the ASD group compared to the controls.

Conclusions: Basic face identification mechanisms appear to be intact in the ASD. However, individuals with ASD failed to engage the subcortical brain regions involved in automatic emotional face processing, suggesting a core mechanism for impaired socioemotional processing in ASD. Further, reduced right fusiform activation in the ASD group may be related to a failure of subcortical circuits to appropriately modulate cortical brain regions in ASD.