Externalizing Behaviors in Autism Spectrum Disorder Modulate Neural Responses during a Novel Interactive Social Paradigm

Background:

Aberrant development of attention is indicated in both autism spectrum disorder (ASD) and disorders associated with externalizing behavior (e.g., conduct disorder). Attention modulates electrophysiological (EEG) neural responses elicited by visual social stimuli, and atypical patterns of these neural responses are seen in individuals with both ASD and maladaptive behavior. However, there have been few investigations into the potential influence of externalizing behaviors on neural responses to social information in ASD.

Objectives:

To examine whether externalizing behavior modulates event-related potentials (ERPs) to social information in individuals with ASD compared to typically developing (TD) controls.

Methods:

Preliminary EEG and eye tracking data were collected from children with ASD (n=49, mean age=14.17 years, mean IQ=107.41) and age/IQ matched TD controls (n=44, mean age=13.39 years, mean IQ=108.52); data collection is ongoing. Participants viewed an experimental paradigm in which onscreen faces responded contingently to participant gaze (monitored with eye tracking) with direct or averted gaze. The amplitudes and latencies of the N170, a face sensitive ERP, and the P100, an ERP associated with early sensory processing, were extracted from selected electrodes over the occipitotemporal scalp of the right and left hemispheres (RH; LH), segmented to the gaze shift. Externalizing symptomatology was measured using parent-report on the Child Behavior Checklist (CBCL). Group differences were examined using t-tests. Effects of diagnosis and gaze on ERPs were examined with two-way ANOVAs. Linear regression analyses were used to test whether externalizing behaviors significantly predicted neural responses.

Results:

Participants with ASD exhibited significantly greater parent-reported externalizing behavior than TD participants, as determined by the CBCL’s Externalizing T-Scores [t(88)=4.30, p<0.001]. Analysis of N170 peak amplitude revealed that there was a significant main effect of gaze [LH, F(1,158)=4.48, p=0.04] such that the N170 was enhanced to direct gaze compared to averted gaze. There was no main effect of diagnosis and no interaction between diagnosis and gaze (ps>0.05). In ASD but not TD, externalizing behaviors predicted N170 latency to averted gaze [LH, (b=1.36, p=0.04), (R²=0.10, F(1,43)=4.53, p=0.04)]. The analysis of P100 peak amplitude and latency indicated no main effects of diagnosis or gaze and no interaction between diagnosis and gaze (ps>0.05). Similar to the N170, externalizing behaviors predicted in ASD but not TD P100 latency to averted gaze [RH, (b=0.81, p=0.02), (R²=0.13, F(1,43)=6.22, p= 0.02)], and P100 amplitude to direct gaze [RH, (b=-0.07, p=0.01), (R²=0.11, F(1,39)=4.96, p=0.03)].

Conclusions:

Results of this novel interactive gaze paradigm indicate enhancement of the face-sensitive N170 to direct gaze across diagnostic groups, suggesting similar response to mutual gaze at initial stages of face perception. Externalizing behaviors were associated with gaze perception in children with ASD but not TD. In children with ASD, more severe externalizing behaviors were associated with slowed visual and facial processing in an avoidance-oriented social context and with more impaired visual processing in an approach-oriented one. These findings suggest that externalizing behavior may be useful in guiding strategies to stratify a heterogeneous ASD population to advance the objective of individualized, targeted therapies.