Rapid neural categorization of angry and fearful faces is specifically impaired in boys with autism spectrum disorder

Abstract

Background: Difficulties with facial expression processing may be associated with the characteristic social impairments in individuals with autism spectrum disorder (ASD). Emotional face processing in ASD has been investigated in an abundance of behavioral and EEG studies, yielding, however, mixed and inconsistent results. Methods: We combined fast periodic visual stimulation (FPVS) with EEG to assess the neural sensitivity to implicitly detect briefly presented facial expressions among a stream of neutral faces, in 23 boys with ASD and 23 matched typically developing (TD) boys. Neutral faces with different identities were presented at 6 Hz, periodically interleaved with an expressive face (angry, fearful, happy, sad in separate sequences) every fifth image (i.e., 1.2 Hz oddball frequency). These distinguishable frequency tags for neutral and expressive stimuli allowed direct and objective quantification of the expression-categorization responses, needing only four sequences of 60 s of recording per condition. Results: Both groups show equal neural synchronization to the general face stimulation and similar neural responses to happy and sad faces. However, the ASD group displays significantly reduced responses to angry and fearful faces, compared to TD boys. At the individual subject level, these neural responses allow to predict membership of the ASD group with an accuracy of 87%. Whereas TD participants show a significantly lower sensitivity to sad faces than to the other expressions, ASD participants show an equally low sensitivity to all the expressions. Conclusions: Our results indicate an emotion-specific processing deficit, instead of a general emotionprocessing problem: Boys with ASD are less sensitive than TD boys to rapidly and implicitly detect angry and fearful faces. The implicit, fast, and straightforward nature of FPVS-EEG opens new perspectives for clinical diagnosis.

Emotional vs. Neutral Face Exploration and Habituation: An Eye-Tracking Study of Preschoolers With Autism Spectrum Disorders

“…While some studies have observed impairments in emotion recognition and processing in children with ASD ( 18 , 20 ), to the best of our knowledge, no clear consensus has emerged from the many studies regarding differences in emotion exploration in children with ASD. However, several studies have suggested that “negative” emotions such as fear and anger may be less salient for children with ASD ( 51 – 53 ). For example, a recent eye-tracking study showed that high-functioning children with ASD perceive fear as less intense than their TD peers ( 52 ).…”

Combined frequency-tagging EEG and eye-tracking measures provide no support for the “excess mouth/diminished eye attention” hypothesis in autism

“…All data segments were re-referenced to a common average reference. While in frequency-tagging studies we typically apply blink correction (using ICA) for any participant blinking more than 2 standard deviations above the mean (e.g., [ 25 , 92 ], [ 96 ]), in the present study we did not perform any blink correction as none of the participants blinked excessively, i.e., more than two standard deviations above the mean across all participants (0.36 times per second). Note that frequency-tagging EEG yields responses with a high SNR at specific frequency bins, while blink artefacts are broadband and thus do not generally interfere with the responses at the predefined frequency [ 73 ].…”

Facial Expression Processing Across the Autism–Psychosis Spectra: A Review of Neural Findings and Associations With Adverse Childhood Events

“…This novel tool offers great advantages in terms of objectivity in the identification and quantification of selective responses of interest in the frequency domain of the EEG spectrum, as well as high sensitivity (i.e., high signal-to-noise ratio). A pioneering study by Van der Donck et al (124,125) applied a frequency-tagging EEG oddball paradigm to assess the neural sensitivity for rapid changes in emotional expressions, revealing reduced neural discrimination responses for fearful and angry faces in children with ASD and predicting clinical status with an 87% accuracy at the individual level.…”

“…To dissociate these alternatives, EEG paradigms directly contrasting neutral and emotional facial expressions are needed. A particularly promising approach for this would be the administration of a fast periodic visual stimulation oddball frequency-tagging paradigm, as has been applied in ASD (124,125). Thus far, this method has not been applied in primary psychosis, but it was recently administered in patients with velocardiofacial (22q11.2 deletion) syndrome, which is a well-known high-risk group for psychosis (147).…”

“…In the past years, an alternative EEG approach, called fast periodic visual stimulation frequency-tagging EEG, has been put forward, yielding promising findings pinpointing selective facial expression processing impairments in individuals with ASD (124,125) and primary psychosis (147). This novel approach reveals an objective, selective, reliable, and behaviorfree signature of impaired visual coding of facial expression, implicitly quantified from brain activity with high signal-to-noise ratio at the individual subject level.…”