Neural Correlates of Face and Eye Gaze Processing Differentiate Children with Autism Spectrum Disorder (ASD) and/or Attention Deficit Hyperactivity Disorder (ADHD)

Background: There is considerable clinical and genetic overlap between autism spectrum disorders (ASD) and attention deficit hyperactivity disorder (ADHD). In particular both disorders demonstrate social impairments (Uekermann et al. 2010; Rommelse et al. 2011). In typical development, neurophysiological brain responses differentiate upright and inverted faces, and direct and averted gaze (Farroni et al. 2002; Taylor, Batty & Itier, 2004), and recent work has demonstrated that the gaze effect is only found for upright faces in the right hemisphere (Mercure et al. in prep). While absence or reductions in these effects are consistently found in ASD (McPartland et al. 2004; Senju et al. 2005), the impact of ADHD or co-occurring ADHD in ASD on these effects is unknown. By measuring neurophysiological responses to face stimuli, it is possible to directly capture abnormalities in fast-occurring responses to faces.

Objectives: (1) To investigate the specificity of face processing abnormalities to ASD and (2) to elucidate the neural basis of the common comorbidity between these two disorders.

Methods: Event-related potentials were recorded during presentation of face stimuli in 20 males with ASD, 18 males with ADHD, 28 males with ASD+ADHD and 26 typically developing (TD) males between 8 and 13 years of age. Peak amplitudes of the P1, the N170 and a peak-to-peak difference score between the two components, were entered into separate repeated measures ANOVAs with factors Orientation (Upright, Inverted), Gaze (Direct, Averted) and Montage (Left, Medial, Right, Anterior Midline). Due to developmental changes, the effect of age was analysed both as a covariate and an independent variable (8-10 years vs. 11-13 years).

Results: Across all groups, an interaction between orientation and gaze emerged indicating a gaze effect in upright faces (increased amplitude for averted gaze) and not inverted faces. Children with ASD demonstrated reduced and bilateral neurophysiological responses across all face stimuli compared to typical controls and children with ADHD, who exhibited greater amplitude over the right hemisphere. Children with comorbid ASD+ADHD showed intermediate abnormalities that were not significantly different to neither ASD-only nor ADHD-only participants. Age effects differed between participant groups: all clinical groups demonstrated a more pronounced developmental change in the face inversion effect (reduced amplitude for inverted faces in younger subjects compared to enhanced amplitude for inverted faces in older subjects).

Conclusions: Topographical and amplitude atypicalities in neurophysiological responses to faces are specific to ASD compared to ADHD. Children with ASD+ADHD present as a hybrid of both disorders with deficits equivalent to the addition of each disorder individually. Age has a substantial effect on neurophysiological responses to faces in all clinical groups, suggestive of altered developmental processes. Such findings emphasize the utility of electrophysiological measurement in characterizing this common comorbidity, by highlighting shared and distinct abnormalities to target in genetic research and intervention studies.