Where You Look on a Face Matters! Neural Correlates of Early Face Perception Are Modulated By Featural Fixation in Adults with and without Autism Spectrum Disorder

Background: The eyes play an important role in guiding social communication behaviours, with important cascading effects on social cognition. Recent neuroimaging research has also demonstrated a neural sensitivity to the eyes in neurotypical face perception, such that the N170 event-related potential (ERP) – the earliest neural marker of face and eye perception – demonstrates a consistently larger amplitude when visual fixation is enforced on the left or right eye within a face, compared to enforced fixation to other parts of the face (forehead, nasion, nose, or mouth). A handful of studies have evaluated the N170 ERP in adults with ASD, reporting reduced amplitudes or delayed latencies when adults with ASD perceive faces or eyes compared to neurotypical adults. However, ERP findings in ASD are inconsistent and despite the commonly observed eye avoidance behaviours in ASD, these ERP studies did not control for visual attention, making it difficult to know where participants were looking and how this may have impacted the ERP results.

Objectives: This study sought to control for visual fixation when adults with and without ASD viewed faces to clarify the neural correlates of early face perception in ASD and how this may be similar or different to neurotypical face perception.

Methods: High-functioning adults with ASD and age-, gender-, ethnicity-, and IQ-matched neurotypical adults were presented with faces in which visual fixation was enforced on the left eye, right eye, nasion, nose, or mouth during an oddball detection (to flowers) task. Eye movements and electroencephalography (EEG) recordings were synchronized offline, to ensure that only trials in which fixation was maintained on the feature of interest were included. EEG recordings were then time-locked to face-onset, and the left and right hemispheric electrodes which showed the maximal N170 response for all conditions were selected for each participant.

Results: Preliminary analyses (ASD = 13, neurotypical = 10) revealed a robust effect of featural fixation for both groups. N170 peak amplitudes were significantly larger when fixation was enforced on the left or right eye compared to all other features, and this pattern was largely consistent across groups. Moreover, fixation on the nasion or nose yielded the fastest N170 response in both groups, followed by the left and right eyes, followed in turn by the mouth. Whilst there were no significant group effects or interactions, there was a tendency for adults with ASD to elicit attenuated N170 amplitudes for the left eye, but slightly enhanced amplitudes for the mouth, relative to neurotypical adults.

Conclusions: These findings suggest that the early neural response to features within a face may be similar for adults with and without ASD when fixation is enforced. Therefore, difficulties with eye contact and social communicative behaviours in ASD may not stem from differences in the earliest stages of face perception and may instead be based in free-viewing preferences or later stages of face processing. These findings also highlight the importance of controlling for visual attention in ERP studies in order to more clearly refine neural mechanisms in ASD and neurotypical adults.