Does electroencephalogram phase variability account for reduced P3 brain potential in externalizing disorders?

•Trial to trial variation in P3-related delta and theta EEG phase predicts externalizing disorders (antisocial behavior, ADHD, substance dependence).•Time–frequency energy and phase-locking are better predictors of externalizing disorders together than either alone.•These novel findings suggest weakened neuromodulation during cognitive processes in externalizing individuals.

ObjectiveAmplitude deficits of the P3 event-related potential (ERP) are associated with externalizing psychopathology but little is known about the nature of underlying brain electrical activity that accounts for this amplitude reduction. We sought to understand if group differences in task-induced phase-locking in electroencephalographic (EEG) delta and theta frequencies may account for P3-externalizing associations.MethodsAdult males (N = 410) completed a visual oddball task and frontal and parietal P3-related delta- and theta-band phase-invariant evoked energy and inter-trial phase-locking measures were investigated with respect to the externalizing spectrum, including substance dependence, adult antisociality, and childhood disruptive disorders. We hypothesized that P3-related phase-locking is weaker in externalizing-diagnosed individuals and this might mediate prior findings of reduced evoked P3 energy.ResultsReductions in both evoked energy and phase-locking, in both frequency bands, at both scalp sites, were associated with greater odds of externalizing diagnoses. Generally, adding phase-locking to evoked energy came with better prediction model fit. Moreover, reduced theta-band phase-locking partially mediated the effects of within-frequency evoked energy on externalizing prediction.ConclusionsInter-trial phase-locking underlying P3 appears to be an important distinction between externalizing and control subjects.SignificanceThis cross-trial phase-variability for externalizing-diagnosed individuals might reflect deficient top-down “tuning” by neuromodulatory systems.