Differences in neural activity when processing emotional arousal and valence in autism spectrum disorders

Abstract

Individuals with autism spectrum disorders (ASD) often have difficulty recognizing and interpreting facial expressions of emotion, which may impair their ability to navigate and communicate successfully in their social, interpersonal environments. Characterizing specific differences between individuals with ASD and their typically developing (TD) counterparts in the neural activity subserving their experience of emotional faces may provide distinct targets for ASD interventions. Thus we used functional magnetic resonance imaging (fMRI) and a parametric experimental design to identify brain regions in which neural activity correlated with ratings of arousal and valence for a broad range of emotional faces. Participants (51 ASD, 84 TD) were group-matched by age, sex, IQ, race, and socioeconomic status. Using task-related change in blood-oxygen-level-dependent (BOLD) fMRI signal as a measure, and covarying for age, sex, FSIQ, and ADOS scores, we detected significant differences across diagnostic groups in the neural activity subserving the dimension of arousal but not valence. BOLD-signal in TD participants correlated inversely with ratings of arousal in regions associated primarily with attentional functions, whereas BOLD-signal in ASD participants correlated positively with arousal ratings in regions commonly associated with impulse control and default-mode activity. Only minor differences were detected between groups in the BOLD signal correlates of valence ratings. Our findings provide unique insight into the emotional experiences of individuals with ASD. Although behavioral responses to face-stimuli were comparable across diagnostic groups, the corresponding neural activity for our ASD and TD groups differed dramatically. The near absence of group differences for valence correlates and the presence of strong group differences for arousal correlates suggest that individuals with ASD are not atypical in all aspects of emotion-processing. Studying these similarities and differences may help us to understand the origins of divergent interpersonal emotional experience in persons with ASD. Hum Brain Mapp 37:443-461, 2016. © 2015 Wiley Periodicals, Inc.

Keywords: arousal; autism spectrum disorders; fMRI; facial emotion; valence.

Figure 1

Emotion paradigm.

Figure 2

Emotion‐specific group comparisons of behavioral findings.

Figure 3

Arousal correlates (A) Regions of significant correlations of BOLD‐signal with ratings of arousal for TD participants. (Positive correlations are coded in red to yellow, and inverse correlations are coded in green to blue.). (B) Scatterplots of correlations for BOLD‐signal with ratings of arousal for TD participants (green) or participants with ASD (purple). (C) Regions of significant correlations of BOLD‐signal with ratings of arousal for participants with ASD. (D) The regions where the correlation of arousal ratings with BOLD‐signal for participants with ASD differs significantly from the correlation of arousal ratings with BOLD‐signal for TD participants. (ASD > TD coded in red to yellow, TD >ASD coded in blue to green). (E) Scatterplots of correlations for BOLD‐signal with ratings of arousal for TD participants (green) and participants with ASD (purple) in regions where the correlation of arousal ratings with BOLD for participants with ASD differs significantly from the correlation of arousal ratings with BOLD for TD participants.

Figure 4

Linear and quadratic correlations of arousal with BOLD‐signal in ASD (A) Regions of significant linear correlations of BOLD‐signal with ratings of arousal for participants with ASD. (Positive correlations are coded in red to yellow, and inverse correlations are coded in green to blue.). (B) Scatterplots of linear correlations for BOLD‐signal with ratings of arousal for participants with ASD (orange). (C) Regions of significant linear correlations of BOLD‐signal with ratings of arousal combined with regions of significant quadratic correlations of arousal ratings for participants with ASD. Positive linear correlations with arousal are shown alone (orange), quadratic correlations with arousal alone (fuschia), and linear+quadratic correlations with arousal (red). (D) Scatterplots of correlations between BOLD‐signal change and ratings of linear+quadratic correlations with arousal for participants with ASD (red) in regions where BOLD correlated positively for both linear and quadratic correlations with arousal ratings.

Figure 5

Valence correlates (A) Regions of significant correlations of BOLD‐signal with ratings of valence for TD participants. (Positive correlations are coded in red to yellow, and inverse correlations are coded in green to blue.). (B) Scatterplots of correlations for BOLD‐signal with ratings of valence for TD participants (green) or participants with ASD (purple). (C) Regions of significant correlations of BOLD‐signal with ratings of valence for participants with ASD. (D) The regions where the correlation of valence ratings with BOLD for participants with ASD differs significantly from the correlation of valence ratings with BOLD for TD participants. (ASD > TD coded in red to yellow, TD >ASD coded in blue to green). (E) Scatterplots of correlations for BOLD‐signal with ratings of valence for TD participants (green) and participants with ASD (purple) in regions where the correlation of valence ratings with BOLD for participants with ASD differs significantly from the correlation of valence ratings with BOLD for TD participants.