Modulation of Emotional Face Processing By Visual Attentional Flexibility and Attention Deficit Hyperactivity Disorder (ADHD) Symptoms in ASD: Results from the ABC-CT Feasibility Study

Background: Face processing difficulties are common in ASD. In addition to social deficits, children with ASD often show impaired executive function(EF). Atypical face processing and impaired EF are also evident in ADHD, which often co-occurs in ASD. It is not known whether ADHD and visual attentional flexibility(VAF)—a type of EF that involves shifting, engaging, and disengaging visual-spatial attention—modulate ERPs to emotional faces in ASD.

Objectives: To examine whether ADHD and VAF modulate ERPs to emotional faces in ASD versus TD.

Methods: EEG and eye-tracking(ET) data were collected from children (4-11 years-old and DAS-2 IQ ≥ 50) with ASD (n=25) and TD (n=26). For EEG, participants viewed neutral and fearful faces, while EEG was recorded with a 128-channel Hydrocel Geodesic net at 1000Hz. ERPs (P100, N170) were extracted over left(LH) and right(RH) hemispheres. For ET, participants completed a gap-overlap task, while fixations were recorded via a SR Eyelink 1000+ binocular eye-tracker at 500Hz. A central stimulus(CS) was displayed, followed by a peripheral stimulus(PS). PS was displayed while CS was on screen (overlap), immediately after CS disappeared (baseline), or 200 ms after CS disappeared (gap). VAF effects were calculated from reaction time(RT) to PS: disengagement (overlap-baseline), facilitation (baseline-gap), and gap (overlap-gap). Childhood and Adolescent Symptom Inventory-5 measured ADHD inattention and hyperactivity/impulsivity symptoms. To examine effects of group and condition, ANOVAs were used for ERPs, and trial-level linear mixed effects modeling(LMM) was used for gap-overlap, controlling for IQ.

Results: In ASD, greater inattention related to slower P100 to fearful faces (LH; r=.69, p=.01), and greater hyperactivity/impulsivity related to slower N170 to fearful (LH; r=.59, p=.04) and neutral (RH; r=.56, p=.049) faces. In TD, greater inattention related to faster N170 to fearful faces (LH; r=-.46, p=.04). In ASD, greater inattention related to slower P100 to fearful versus neutral faces (LH; r=-.56, p=.048), and greater hyperactivity/impulsivity related to slower N170 to fearful versus neutral faces (LH; r=-.64, p=.02). Greater facilitation effect related to slower N170 to fearful versus neutral faces (RH; r=-.60, p=.04) in ASD, whereas greater gap effect related to faster N170 to fearful versus neutral faces (RH; r=.47, p=.02) in TD. Main effects of group were identified for gap-overlap RTs (p=.048), but not ERPs (p>.05). RTs were faster in ASD. Main effects of condition were identified for N170 and P100 amplitudes (p<.03) and gap-overlap RTs (p<.001). P300 will be extracted for future analyses.

Conclusions: Variability in EF-related ADHD symptoms and VAF modulate neural response to faces differently in ASD versus TD. Children with ASD with more ADHD symptoms showed slower neural responses to faces, whereas TD children showed the opposite. When comparing emotional faces, children with ASD with more ADHD symptoms showed slower neural responses to fearful versus neutral faces. Greater facilitation predicted slower neural response to fearful versus neutral faces in ASD, while greater gap effect in TD predicted the reverse. Therefore, brain response to faces may be modulated by orienting efficiency in ASD but by processing efficiency in TD, suggesting distinct relationships among EF and social perception in ASD versus TD.