Is Implicit Processing of Fearful Faces Impaired in ASD?

Background: Being able to quickly read faces and facial expressions is crucial for social interactions, and even survival. Many studies suggest that individuals with autism spectrum disorder (ASD) show deficits in emotion recognition, especially with regard to fearful faces. In addition, it has been suggested that individuals with ASD may show a reduced preference for the eye region and may focus more on the mouth region.

Objectives: The present study aims at examining the nature of face processing impairments in 23 8-to-12 year old children with ASD versus 23 matched typically developing (TD) control children. In particular, we investigated the neural sensitivity to implicitly discriminate between neutral and fearful faces, and whether this relates to behavioural indices of facial emotional processing and to atypical visual scanning patterns of the face.

Methods: We combined fast periodic visual stimulation (FPVS) with scalp electroencephalography (EEG) and eye-tracking. The general principle of FPVS EEG is that it elicits a steady-state visual evoked potential at exactly the same frequency of visual stimulation. If oddball fearful faces are periodically interleaved in a series of neutral faces, sensitivity to these socio-communicative cues can be quantified by assessing the neural response at the oddball frequency. Additional within-subject manipulations comprised the orientation of the faces (upright versus inverted) and the positioning of the fixation cross (on the eye region versus on the mouth region). Behavioural indices of face processing comprised the detection of non-periodic emotional faces in a stream of neutral faces, the assessment of the Emotion Recognition Task and the Emotion-Matching Task, and the assessment of visual scanning patterns during explicit emotion recognition tasks.

Results: Neural responses at the oddball frequency and its harmonics are present in both groups of children, and both groups show a similar face inversion effect (with reduced responses for inverted faces and a shift from higher-level lateral occipito-temporal response peaks for upright faces towards lower-level medial-occipital response peaks for inverted faces). Unexpectedly, in both groups occipito-temporal responses were increased when focusing on the mouth as compared to the eye region, regardless of the orientation of the faces. Most importantly, between-group analyses showed significantly reduced bilateral occipito-temporal and medial occipital responses in ASD compared to TD, regardless whether faces were presented upright versus inverted or whether fixation was on the eyes or on the mouth. These implicit EEG data will be complemented with explicit behavioural emotion processing data and with face scanning patterns obtained via eye tracking.

Conclusions: Analyses show clear peaks at the oddball frequency and its harmonics in both the ASD and control group, meaning that children with ASD are capable to implicitly discriminate facial expressions. Reduced responses for inverted faces indicate the presence of the inversion effect in ASD and TDs. However, generally reduced neural oddball responses in the presence of equal baseline responses indicate that children with ASD have a lower sensitivity to fearful faces, compared to controls. This suggests a quantitative difference in emotion processing abilities.