Adolescents with ASD Show Atypical Electrophysiological (EEG) Responses to a Novel Theory of Mind Reasoning Task: An ERP Study

Background: Theory of Mind (ToM) reasoning involves making attributions about others’ mental states and is critical for understanding and predicting others’ behavior in social situations. Impairments in social communication, including deficits in ToM, are a core feature of autism spectrum disorders (ASD). Previous research using electroencephalography (EEG) has examined event-related potentials (ERPs) elicited during ToM reasoning tasks in TD youth (Liu, et al., 2004, 2009b; Meinhardt, et al. 2011; Sabbagh & Taylor, 2000), suggesting that correct ToM reasoning is associated with two distinct ERP components. The Late Positive Complex (LPC) is thought to index more automatic processing of conditional salience or expectancy, while the Late Slow Wave (LSW) is related to mental state attributions. However, prior research has not examined ERP correlates of ToM reasoning in adolescents with ASD, hindering understanding of the neurocognitive elements and time-course of ToM in ASD.

Objectives: Investigate whether LPC and LSW ERP amplitudes differ in TD relative to ASD adolescents in a novel ToM task.

Methods: 33 Adolescent participants (22 male; M=13.0 years, SD=1.8) included 19 TD and 14 ASD with ADOS-2 confirmed diagnosis and IQ > 70. During EEG acquisition, participants viewed illustrated, narrated ToM vignettes and were asked to make mental state inferences about the characters’ behavior (McKown et al., 2015). Individual response options were presented sequentially after the conclusion of the vignette, allowing target ERPs to be time-locked to the presentation of correct and incorrect response options. ERPs were measured at parietal electrode sites and extracted as mean area amplitudes within discrete post-stimulus time windows (LPC 300-600ms; LSW 600-1200ms). An independent groups t-test was used to assess group differences in behavioral response accuracy. LPC and LSW ERP data were analyzed in two separate 2 (ASD, TD) by 2 (correct, incorrect) repeated measures ANOVAs (RM-ANOVAs).

Results: The ASD group made significantly more errors than the TD group on the ToM task (t(39)=2.185, p=.035). RM-ANOVA revealed significant main effects at the LPC (F(1,31)=14.86, p=.009) and the LSW (F(1,31)=4.167), p=0.05), such that correct responses were larger than incorrect responses (Figure 1). Diagnosis x Response Accuracy interactions were marginally significant for the LPC (F(1,31)=3.71, p=.063) and significant for the LSW (F(1,31)=4.36, p=.045) (Figure 2). During both epochs, the TD group evinced a greater neural response to correct relative to incorrect responses compared to the ASD group.

Conclusions: Results indicate that youth with ASD demonstrate neural and behavioral deficits in complex ToM reasoning. Individuals with ASD demonstrated marginally attenuated differentiation between correct-vs-incorrect ToM vignettes at the LPC, and attenuated differentiation at the LSW. The LPC has been associated with more attentional aspects of ToM reasoning, whereas the LSW has been associated with more elaborative processing of mental states (Meinhardt et al. 2011. This could suggest that early differences in the LPC might be contributing to later observed differences in the LSW. To probe this effect, future studies should examine the relative contribution of individual ERP components to complex ToM in order to best pinpoint the processing stage at which ToM deficits first occur.