Oscillatory rhythm of reward: anticipation and processing of rewards in children with and without autism

Abstract

Background: Autism spectrum disorder (ASD) is a complex neurodevelopmental condition, and multiple theories have emerged concerning core social deficits. While the social motivation hypothesis proposes that deficits in the social reward system cause individuals with ASD to engage less in social interaction, the overly intense world hypothesis (sensory over-responsivity) proposes that individuals with ASD find stimuli to be too intense and may have hypersensitivity to social interaction, leading them to avoid these interactions.

Methods: EEG was recorded during reward anticipation and reward processing. Reward anticipation was measured using alpha asymmetry, and post-feedback theta was utilized to measure reward processing. Additionally, we calculated post-feedback alpha suppression to measure attention and salience. Participants were 6- to 8-year-olds with (N = 20) and without (N = 23) ASD.

Results: Children with ASD showed more left-dominant alpha suppression when anticipating rewards accompanied by nonsocial stimuli compared to social stimuli. During reward processing, children with ASD had less theta activity than typically developing (TD) children. Alpha activity after feedback showed the opposite pattern: children with ASD had greater alpha suppression than TD children. Significant correlations were observed between behavioral measures of autism severity and EEG activity in both the reward anticipation and reward processing time periods.

Conclusions: The findings provide evidence that children with ASD have greater approach motivation prior to nonsocial (compared to social) stimuli. Results after feedback suggest that children with ASD evidence less robust activity thought to reflect evaluation and processing of rewards (e.g., theta) compared to TD children. However, children with ASD evidence greater alpha suppression after feedback compared to TD children. We hypothesize that post-feedback alpha suppression reflects general cognitive engagement-which suggests that children with ASD may experience feedback as overly intense. Taken together, these results suggest that aspects of both the social motivation hypothesis and the overly intense world hypothesis may be occurring simultaneously.

Keywords: Alpha asymmetry; Autism spectrum disorder; Reward processing; Social stimuli; Theta.

Fig. 1

Stimulus presentation and timing. Feedback for the social condition is shown in the left column, and feedback for the nonsocial condition is shown in the right column. Feedback for “correct” answers is shown on top, and feedback for “incorrect” answers is shown below

Fig. 2

Anticipatory alpha asymmetry (left minus right) in temporal electrode locations. Note that negative values indicate more left dominant alpha supression, while positive values indicate more right dominant alpha supression. Data from typically developing children is shown in the top row, and data from children with autism is shown on the bottom row. Activity prior to nonsocial (arrow) stimuli is shown on the left, and activity prior to social (face) stimuli is shown on the right

Fig. 3

Correlation between anticipatory alpha asymmetry to nonsocial stimuli and ADOS-2 severity scores. Note that negative values for alpha asymmetry indicate more left dominent alpha supression, and higher ADOS-2 scores indicate more severe symptoms of autism

Fig. 4

a Post-feedback ERSP for typically developing (TD) children in the theta (4–6 Hz) and alpha band (8–12 Hz). Activity after social (face) stimuli is shown on the left, and activity after nonsocial (arrow) stimuli is shown on the right. Activity after “correct” feedback is shown in the top row, and activity after “incorrect” feedback is shown in the bottom row. b. Post-feedback ERSP for children with ASD children in the theta (4–6 Hz) and alpha band (8–12 Hz). Activity after social (face) stimuli is shown on the left, and activity after nonsocial (arrow) stimuli is shown on the right. Activity after “correct” feedback is shown in the top row, and activity after “incorrect” feedback is shown in the bottom row

Fig. 5

Theta (4–6 Hz) correlation between post-stimulus theta after “correct” social (face) feedback and ADOS-2 severity score. Note that higher ADOS-2 scores indicate more severe ASD