Pupillary Responses to Emotional Faces in Individuals with Autism Spectrum Disorder and Their Unaffected Siblings

Background:  From a young age, individuals with ASD look less at faces than their typically developing peers. However, little is understood about the underlying cognitive and neurobiological mechanisms that contribute to this decreased attention. The pupillary response (i.e., change in pupil dilation) is regulated by the autonomic nervous system and is directly associated with amygdala activity. In a recent study, individuals with ASD demonstrated attenuated pupillary responses as they viewed happy faces, providing preliminary evidence of reduced autonomic arousal in response to social-emotional information. However, it is unclear whether this response is present when viewing neutral or fearful faces. Furthermore, no studies have investigated pupillary responses in first-degree relatives of individuals with ASD (e.g., unaffected siblings). Understanding the relationship between visual attention and pupillary responses to faces in individuals with ASD and their first-degree relatives is an important step toward elucidating the role of autonomic arousal during social-emotional information processing. 

Objectives:  To investigate looking patterns and pupillary responses in individuals with ASD and their siblings as they view emotional faces.

Methods:  Eleven individuals with ASD (mean age = 15.48), eight siblings of individuals with ASD (mean age = 13.01), and 10 typically-developing controls (mean age = 15.62), have participated in this study to date (with additional participant testing underway). Participants passively viewed 18 trials each of happy, calm, and fearful faces, taken from the NimStim Stimulus Set (Tottenham et al, 2009). A Tobii X60 eye tracker recorded eye movements and pupil dilation. Each trial lasted 3 seconds and was preceded by a scrambled, luminance-matched version of that trial. Looking time on the eyes, nose, mouth, and entire face were averaged by condition. Relative change in pupil dilation, normalized to each participant’s average pupil size during preceding scrambled faces, was averaged for each trial as well as for each 250ms interval of each trial. 

Results:  Groups did not differ on overall time spent looking at the eyes, nose, mouth, or entire face. Furthermore, no group differences were observed for average pupillary response for any of the conditions. However, groups showed unique patterns of pupillary responses over the course of the 3-second stimuli presentation. Controls showed a dramatic increase in pupil dilation in the first 250ms followed by a sharp decrease in subsequent intervals, whereas individuals with ASD and their unaffected siblings showed a flat pupil response across the course of the trial. For all conditions, controls had significantly larger pupillary responses in the first 250ms interval than both individuals with ASD and siblings, ps < .05. 

Conclusions:  This study shows that, relative to controls, individuals with ASD and their siblings demonstrate divergent patterns of autonomic arousal in response to faces, though broad measures (e.g., average pupillary response, average looking time) may not capture these differences. In particular, these findings suggest that individuals with ASD and their siblings do not experience a typical initial increase in autonomic arousal when viewing faces. This lack of initial arousal may underpin reduced attention to social-emotional information, thus leading to downstream deficits in social understanding.