Neural Correlates of Metacognition Impairment in Opioid Addiction.

ABSTRACT

BACKGROUND: Individuals with substance use disorder show impaired self-awareness of ongoing behavior. This deficit suggests problems with metacognition, which has been operationalized in the cognitive neuroscience literature as the ability to monitor and evaluate the success of one's own cognition and behavior. However, the neural mechanisms of metacognition have not been characterized in a population with drug addiction. METHODS: Community samples of participants with opioid use disorder (OUD) (n = 27) and healthy control participants (n = 29) performed a previously validated functional magnetic resonance imaging metacognition task (perceptual decision-making task along with confidence ratings of performance). Measures of recent drug use and addiction severity were also acquired. RESULTS: Individuals with OUD had lower metacognitive sensitivity (i.e., disconnection between task performance and task-related confidence) than control individuals. Trial-by-trial analyses showed that this overall group difference was driven by (suboptimally) low confidence in participants with OUD during correct trials. In functional magnetic resonance imaging analyses, the task engaged an expected network of brain regions (e.g., rostrolateral prefrontal cortex and dorsal anterior cingulate/supplementary motor area, both previously linked to metacognition); group differences emerged in a large ventral anterior cluster that included the medial and lateral orbitofrontal cortex and striatum (higher activation in OUD). Trial-by-trial functional magnetic resonance imaging analyses showed group differences in rostrolateral prefrontal cortex activation, which further correlated with metacognitive behavior across all participants. Exploratory analyses suggested that the behavioral and neural group differences were exacerbated by recent illicit opioid use and unexplained by general cognition. CONCLUSIONS: With confirmation and extension of these findings, metacognition and its associated neural circuits could become new, promising therapeutic targets in addiction.