Pupillary Response to Faces in Children with Autism

Background: Among the most prominent features of the social communication impairment in autism is the tendency to avoid direct eye contact with others. From a young age, children with autism look at faces less than typically developing children and tend to avoid eye contact, even with their primary caregiver. However, there is controversy over the reason for this reduced eye contact. Do they avoid eye contact because they experience the eyes of others to be aversive? Or, are they not motivated to look at eyes because they find the eyes uninteresting? Objectives: To investigate the underlying causes for this reduced eye contact and abnormal facial fixation behavior, we monitored gaze fixation and pupillary diameter as a measure of autonomic response in children with autism and age-matched typically developing children while they looked at human emotional faces. Methods: A group of high-functioning individuals with autism (n=20) was compared to a group of typically developing children (n=18) as they viewed faces displaying either happy, fearful, angry or neutral emotions. Subjects viewed faces in two conditions. In the “gaze-direct” condition, the eyes were gazing directly at the subject, while in the “gaze-averted” condition, the eyes were averted from the subject. Eye fixation crosses appeared before each face to cue gaze to the eye region. Using an infrared eye-tracking device, pupillary diameter and fixation patterns for each type of stimuli were compared within and between the two groups. Results: Overall, children with autism and typically developing children showed similar fixation behavior and pupillary responses; however, they showed marked difference in their pupillary response sensitivity to gaze direction for happy faces. Typically developing children showed increased pupillary diameter to happy faces with direct gaze compared to those with averted gaze (p<0.05), whereas children with autism did not show such sensitivity to gaze direction for happy faces (p>0.05). Of potential concern is whether or not these pupillary response differences could be secondary to differences in fixation behavior; however, for happy faces, fixation duration did not correlate with modulation of the pupillary response by the gaze direction across both groups for any of the regions (R2 all below 0.073, p>0.1). Thus, there was no systematic relationship between fixation behavior and the pupillary gaze effects. Conclusions: We interpret the increased pupillary diameter to happy faces with direct gaze in typically developing children to reflect the intrinsic reward value of a smiling face looking directly at an individual. The lack of this effect in children with autism is consistent with the hypothesis that throughout development, children with autism are less motivated to look at the eyes and face because of impaired processing of social reward. We hypothesize that the failure to attach a reward value to social stimuli in the individuals with autism early in the development may result in weaker motivation to look at faces. In turn, this may hinder the development of neuronal circuits specialized for processing faces, and more broadly lead to a cascade of negative consequences for social development.