Neural and behavioral correlates of the reward positivity

The ability to utilize reward information to adaptively guide behavior to meet current and future goals is essential to successfully navigate through daily life. Through carefully controlled behavioral studies, it has been shown that mesocorticolimbic reward circuit activation can represent reward expectations related to future outcomes, errors in those expectations, motivation, and signals related to goal-driven behaviors. Over the last two decades, there has been an increased interest in the functional role of the anterior midcingulate cortex (MCC) in these reward-related processes. In humans, the reward processing function of MCC has been largely investigated using a component of the event-related brain potential (ERP) called the reward positivity (Rew-P). The Rew-P reflects the receipt of reward prediction error (RPE) signals carried by the midbrain dopamine system to MCC, where they are utilized to learn the value of rewards for the purpose of selecting and motivating the execution of goal-directed behavior. Despite the evidence in favor of this proposal, it has been challenged due to mixed findings about the neural source of the Rew-P and whether it reflects a reinforcement learning process. Thus, it’s still remains unclear whether the Rew-P reflects RPE-related activity in the MCC in the context of trial-to-trial behavioral adaptation and goal-directed behavior. This dissertation aims to clarify these uncertainties through multiple methodological approaches: simultaneous EEG-fMRI recordings combined with univariate regression analysis and neural decoding techniques, and novel mobile EEG combined with AR to enhance the ecological validity of the Rew-P and its behavioral correlates.In Study 1, EEG decoding demonstrated peak classification accuracy (56%) at 275ms post-feedback at electrode FCz, aligning with the conventional Rew-P latency (240–340ms). Similarly, fMRI decoding yielded the second highest classification accuracy (54%) within the right MCC (area 32pr). EEG-fMRI regression analyses further confirmed trial-level associations between EEG-derived Rew-P amplitudes and MCC BOLD activity, embedded within a distributed reward network including dorsolateral prefrontal cortex, orbitofrontal cortex, parahippocampal gyrus, and striatal structures. In line with previous work, these results identify the MCC, particularly subregion area 32pr, as the primary neural generator of the Rew-P. In Study 2a, using combined mobile EEG and AR revealed that the Rew-P remains detectable under naturalistic and physically interactive task conditions. In Study 2b, we replicated the finding but also show the Rew-P to be sensitive to RPE-related activity (e.g., sensitive to valence and magnitude of reward) and behavioral analyses highlighted significant correlations between Rew-P amplitude and trial-to-trial reward learning strategies, underscoring its role in adaptive behavior. This thesis significance not only resides in its novel methods to identify the neural generator of the Rew-P, but a closer examination of the role of the MCC reward function and its behavioral correlates in a naturalistic setting constitute a major advance in the understanding of MCC reward function and treatment of MCC dysregulation in clinical disorders.