Neural and visual processing of social gaze cueing in typical and ASD adults

Atypical eye gaze in joint attention is a clinical characteristic of autism spectrum disorder (ASD). Despite this documented symptom, neural processing of joint attention tasks in real-life social interactions is not understood. To address this knowledge gap, functional-near infrared spectroscopy (fNIRS) and eye-tracking data were acquired simultaneously as ASD and typically developed (TD) individuals engaged in a gaze-directed joint attention task with a live human and robot partner. We test the hypothesis that face processing deficits in ASD are greater for interactive faces than for simulated (robot) faces. Consistent with prior findings, neural responses during human gaze cueing modulated by face visual dwell time resulted in increased activity of ventral frontal regions in ASD and dorsal parietal systems in TD participants. Hypoactivity of the right dorsal parietal area during live human gaze cueing was correlated with autism spectrum symptom severity: Brief Observations of Symptoms of Autism (BOSA) scores (r = -0.86). Contrarily, neural activity in response to robot gaze cueing modulated by visual acquisition factors activated dorsal parietal systems in ASD, and this neural activity was not related to autism symptom severity (r = 0.06). These results are consistent with the hypothesis that altered encoding of incoming facial information to the dorsal parietal cortex is specific to live human faces in ASD. These findings open new directions for understanding joint attention difficulties in ASD by providing a connection between superior parietal lobule activity and live interaction with human faces. Lay SummaryLittle is known about why it is so difficult for autistic individuals to make eye contact with other people. We find that in a live face-to-face viewing task with a robot, the brains of autistic participants were similar to typical participants but not when the partner was a live human. Findings suggest that difficulties in real-life social situations for autistic individuals may be specific to difficulties with live social interaction rather than general face gaze.