A functional 'low road' subcortical fear processing pathway in adults with autism spectrum disorder

Abstract

Emotion processing has been reported to occur via a fast ‘low road’ pathway using coarse visual information and projecting from the superior colliculus to the amygdala via the pulvinar. Abnormal development in such an important pathway has been suggested to be related to reduced social orienting in children with autism spectrum disorders (ASD). It may also be a contributor in the aberrant development of cortical circuits involved in face processing. Our objective was to further investigate previous supporting evidence for an abnormal subcortical pathway in adults with ASD during fearful face processing by monitoring differences in spatial frequency-dependencies. Participants included 17 individuals with ASD and 20 typically developing controls. The ASD group met diagnostic criteria on the Autism Diagnostic Interview – Revised (ADI- R), Autism Diagnostic Observation Schedule (ADOS), and Diagnostic and Statistical Manual of Mental Disorders IV (DSM-IV). No facial feature preference was identified for gaze fixation for either group. The ASD group was attentive and accurate to a gender discrimination task though statistically less so than typically developing (TD) controls. Both the ASD and control groups showed significant activation in the right fusiform face area (FFA) and left occipital face area (OFA). The control group exhibited additional significant responses in the bilateral amygdala, pulvinar, and lateral geniculate nucleus (LGN), while the ASD group exhibited significant responses in the left pulvinar and left LGN. In group comparisons, the controls showed significantly greater activation in the bilateral amygdala, OFA, and right LGN. No brain region showed significantly greater activation in the ASD group compared to TD controls. Thus, basic face identification mechanisms appear to be functional in ASD with possible functional abnormalities in face categorizing mechanisms and early visual processing systems. While individuals with ASD failed to engage the amygdala and had variable activation in the pulvinar, these results do not implicate a dysfunctional 'low road' pathway. In fact, relative to neutral stimuli, the amygdala showed similar activation patterns for low-spatial frequency fearful images in both groups. This finding directs focus to other possible areas of neural abnormalities which may contribute to early-emerging deficits in social orienting and attention, the presumed antecedents to abnormalities in social cognition and face-selective cortical specialization.