Difficulty with interpersonal interactions is a unifying symptom of autism spectrum disorders. Yet, the neuroscientific study of ASD has focused almost exclusively on passive observation of social information. In this way, the interactive element of social behavior, most critical for understanding social function in ASD, has not been addressed. Event related potential (ERP) studies in typical development have examined brain response to dynamic faces, revealing a central P300 marking perception of facial movement. However, neural responses to facial movements that occur contingent to one’s own movement in the context of social interaction, such as responsive eye gaze, remain unexplored.
Objectives:
This study investigated electrophysiological brain responses to responsive eye gaze during social interaction. By applying gaze-responsive experimental paradigms recording both brain activity (EEG) and visual behavior (eye-tracking; ET), we sought to elucidate the temporal dynamics of the neural response to shared gaze in ASD.
Methods:
ERPs were recorded from high-functioning children with ASD (IQ > 80) and age, sex, and IQ-matched typical counterparts using a 128 electrode Geodesic Hydrocel Net. ET was recorded from a three camera remote eye-tracking system (SmartEye Pro v5.8) integrated with a stimulus presentation computer and EEG recording. Through co-registered and time-locked ET and EEG, the experimental paradigm was controlled by participant gaze. Trials began with presentation of a centrally presented fixation arrow, followed by a peripherally presented neutral face with mouth and eyes closed. Fixation arrows cued the participants to look either to the mouth or the eyes of the face. Contingent upon participant fixation, the face responded by either opening its eyes or opening its mouth. In this way, we examined four conditions: look to the eyes and eyes open (eyes:eyes), look to the eyes and the mouth opens (eyes:mouth), look to the mouth and the eyes open (mouth:eyes), look to the mouth and the mouth opens (mouth:mouth). ERPs were time-locked to face movement; P300 was extracted at central electrodes.
Results:
In typically developing children, P300 amplitude was enhanced in the eyes:eyes condition (1.7µV) relative to all other conditions (amplitudes range from -.54 to .28µV). Children with ASD did not display differential P300 amplitude across conditions and exhibited attenuated P300 amplitude relative to control participants only in the eyes:eyes condition (difference of 2.11µV).
Conclusions:
We demonstrate, for the first time, an electrophysiological marker of shared gaze; typically developing children display enhanced brain response to observed facial movement only in the context of reciprocated gaze. This index of shared gaze was not observed in children with ASD. Given the critical import of reciprocal eye contact in social development and its primacy in the emergence of autistic symptomatology, we foresee the application of similar gaze-contingent paradigms measuring this neural index of shared as critical for advancing efforts toward early detection of atypical social development.