Frontal theta links prediction errors to behavioral adaptation in reinforcement learning

Investigations into action monitoring have consistently detailed a frontocentral voltage deflection in the event-related potential (ERP) following the presentation of negatively valenced feedback, sometimes termed the feedback-related negativity (FRN). The FRN has been proposed to reflect a neural response to prediction errors during reinforcement learning, yet the single-trial relationship between neural activity and the quanta of expectation violation remains untested. Although ERP methods are not well suited to single-trial analyses, the FRN has been associated with theta band oscillatory perturbations in the medial prefrontal cortex. Mediofrontal theta oscillations have been previously associated with expectation violation and behavioral adaptation and are well suited to single-trial analysis. Here, we recorded EEG activity during a probabilistic reinforcement learning task and fit the performance data to an abstract computational model (Q-learning) for calculation of single-trial reward prediction errors. Single-trial theta oscillatory activities following feedback were investigated within the context of expectation (prediction error) and adaptation (subsequent reaction time change). Results indicate that interactive medial and lateral frontal theta activities reflect the degree of negative and positive reward prediction error in the service of behavioral adaptation. These different brain areas use prediction error calculations for different behavioral adaptations, with medial frontal theta reflecting the utilization of prediction errors for reaction time slowing (specifically following errors), but lateral frontal theta reflecting prediction errors leading to working memory-related reaction time speeding for the correct choice.