Multimodal Evidence of Atypical Processing of Eye Gaze and Facial Emotion in Children With Autistic Traits

Shadi Bagherzadeh-Azbari; Gilbert Ka Bo Lau; Guang Ouyang; Changsong Zhou; Andrea Hildebrandt; Werner Sommer; Ming Lui

doi:10.3389/fnhum.2022.733852

Multimodal Evidence of Atypical Processing of Eye Gaze and Facial Emotion in Children With Autistic Traits

Front Hum Neurosci. 2022 Feb 15:16:733852. doi: 10.3389/fnhum.2022.733852. eCollection 2022.

Authors

Shadi Bagherzadeh-Azbari¹, Gilbert Ka Bo Lau², Guang Ouyang³, Changsong Zhou^{4

5}, Andrea Hildebrandt⁶, Werner Sommer^{1

4

7}, Ming Lui^{2

8}

Affiliations

¹ Department of Psychology, Humboldt-Universität zu Berlin, Berlin, Germany.
² Center for Child Development, Hong Kong Baptist University, Kowloon Tong, Hong Kong SAR, China.
³ Faculty of Education, The University of Hong Kong, Pokfulam, Hong Kong SAR, China.
⁴ Department of Physics, Centre for Nonlinear Studies, Hong Kong Baptist University, Kowloon Tong, Hong Kong SAR, China.
⁵ Beijing-Hong Kong-Singapore Joint Centre for Nonlinear and Complex Systems, Institute of Computational and Theoretical Studies, Hong Kong Baptist University, Kowloon Tong, Hong Kong SAR, China.
⁶ Department of Psychology and Research Center Neurosensory Science, Carl von Ossietzky Universität Oldenburg, Oldenburg, Germany.
⁷ Department of Psychology, Zhejiang Normal University, Jinhua, China.
⁸ Department of Education Studies, Hong Kong Baptist University, Kowloon Tong, Hong Kong SAR, China.

Abstract

According to the shared signal hypothesis (SSH) the impact of facial expressions on emotion processing partially depends on whether the gaze is directed toward or away from the observer. In autism spectrum disorder (ASD) several aspects of face processing have been found to be atypical, including attention to eye gaze and the identification of emotional expressions. However, there is little research on how gaze direction affects emotional expression processing in typically developing (TD) individuals and in those with ASD. This question is investigated here in two multimodal experiments. Experiment 1 required processing eye gaze direction while faces differed in emotional expression. Forty-seven children (aged 9-12 years) participated. Their Autism Diagnostic Observation Schedule (ADOS) scores ranged from 0 to 6 in the experiment. Event-related potentials (ERPs) were sensitive to gaze direction and emotion, but emotion processing did not depend on gaze direction. However, for angry faces the gaze direction effect on the N170 amplitude, as typically observed in TD individuals, diminished with increasing ADOS score. For neutral expressions this correlation was not significant. Experiment 2 required explicit emotion classifications in a facial emotion composite task while eye gaze was manipulated incidentally. A group of 22 children with ASD was compared to a propensity score-matched group of TD children (mean age = 13 years). The same comparison was carried out for a subgroup of nine children with ASD who were less trained in social cognition, according to clinician's report. The ASD group performed overall worse in emotion recognition than the TD group, independently of emotion or gaze direction. However, for disgust expressions, eye tracking data revealed that TD children fixated relatively longer on the eyes of the stimulus face with a direct gaze as compared with averted gaze. In children with ASD we observed no such modulation of fixation behavior as a function of gaze direction. Overall, the present findings from ERPs and eye tracking confirm the hypothesis of an impaired sensitivity to gaze direction in children with ASD or elevated autistic traits, at least for specific emotions. Therefore, we conclude that multimodal investigations of the interaction between emotional processing and stimulus gaze direction are promising to understand the characteristics of individuals differing along the autism trait dimension.

Keywords: ADOS; EPN; N170; autism spectrum disorder; emotion processing; face recognition; gaze direction.