Neural features of sustained emotional information processing in autism spectrum disorder

Abstract

Emotion dysregulation is common in autism spectrum disorder; a better understanding of the underlying neural mechanisms could inform treatment development. The tendency toward repetitive cognition in autism spectrum disorder may also increase susceptibility to perseverate on distressing stimuli, which may then increase emotion dysregulation. Therefore, this study investigated the mechanisms of sustained processing of negative information in brain activity using functional magnetic resonance imaging. We used an event-related task that alternated between emotional processing of personally relevant negative words, neutral words, and a non-emotional task. A priori criteria were developed to define heightened and sustained emotional processing, and feature conjunction analysis was conducted to identify all regions satisfying these criteria. Participants included 25 adolescents with autism spectrum disorder and 23 IQ-, age-, and gender-matched typically developing controls. Regions satisfying all a priori criteria included areas in the salience network and the prefrontal dorsolateral cortex, which are areas implicated in emotion regulation outside of autism spectrum disorder. Collectively, activity in the identified regions accounted for a significant amount of variance in emotion dysregulation in the autism spectrum disorder group. Overall, these results may provide a potential neural mechanism to explain emotion dysregulation in autism spectrum disorder, which is a significant risk factor for poor mental health. Lay abstract Many individuals with autism spectrum disorder struggle with emotions that are intense and interfering, which is referred to as emotion dysregulation. Prior research has established that individuals with autism may be more likely than individuals who are not autistic to have repetitive thoughts. It is possible that persistent thoughts about negative or distressing stimuli may contribute to emotion dysregulation in autism spectrum disorder. This study aimed to identify areas of the brain with evidence of persistent processing of negative information via functional magnetic resonance neuroimaging. We used a task that alternated between emotional processing of personally relevant negative words, neutral words, and a non-emotional task. Criteria were developed to define heightened and persistent emotional processing, and analyses were conducted to identify all brain regions satisfying these criteria. Participants included 25 adolescents with autism spectrum disorder and 23 typically developing adolescents who were similar to the autism spectrum disorder group in IQ, age, and gender ratios. Brain regions identified as having greater and continued processing following negative stimuli in the autism spectrum disorder group as compared with the typically developing group included the salience network and the prefrontal dorsolateral cortex. These areas have been previously implicated in emotion dysregulation outside of autism spectrum disorder. Collectively, brain activity in the identified regions was associated with parent-reported emotion dysregulation in the autism spectrum disorder group. These results help to identify a potential process in the brain associated with emotion dysregulation in autism spectrum disorder. This information may be useful for the development of treatments to decrease emotion dysregulation in autism spectrum disorder.