Reduced Medial Frontal Positivity During the Stimulus-Response Interval Precedes Action Errors and Explains Task Deficits in Attention-Deficit Hyperactivity Disorder

Abstract

Brain mechanisms responsible for errors during cognitive tasks are poorly understood, particularly in adolescents with attention-deficit hyperactivity disorder (ADHD). Using subject-specific multimodal imaging (EEG, MRI, behavior) during flanker task performance by a sample of 94 human adolescents (mean age = 15.5 years, 50% female) with varying degrees of ADHD symptomatology, we examined the degree to which amplitudes of source-resolved event-related potentials (ERPs) from brain independent components within a critical (but often ignored) period in the action selection process, the stimulus-response interval, predicted motor response errors (across trials) and error rates (across individuals). Reduced amplitudes of Frontocentral P3 (peaking at approximately 390 milliseconds in stimulus-locked ERPs) and Pre-Movement Positivity (PMP, peaking at approximately 110 milliseconds pre-response in response-locked ERPs) in projections from posterior medial frontal cortex (pMFC) predicted erroneous responses, and reduced amplitude of PMP predicted a larger participant error rate. After regressing stimulus-from response-locked ERPs, we concluded that errors primarily depended upon response selection processes reflected in PMP amplitude. Finally, mediation analyses showed that smaller PMPs on correct response trials was associated with the higher frequency of errors committed by adolescents with more ADHD symptoms. These results bolster the importance of pMFC in action selection and support the possible value of using PMP as an intervention target to remediate performance deficits in ADHD.