Unravelling the origin of reward positivity: a human intracranial event-related brain potential study

Reward positivity (RewP) is an event-related brain potential component that emerges ∼250-350 ms after receiving reward-related feedback stimuli and is believed to be important for reinforcement learning and reward processing. Although numerous localization studies have indicated that the anterior cingulate cortex (ACC) is the neural generator of this component, other studies have identified sources outside of the ACC, fuelling a debate about its origin. Because the results of EEG and magnetoencephalography source-localization studies are severely limited by the inverse problem, we addressed this question by leveraging the high spatial and temporal resolution of intracranial EEG. We predicted that we would identify a neural generator of rthe RewP in the caudal ACC. We recorded intracranial EEG in 19 patients with refractory epilepsy who underwent invasive video-EEG monitoring at Ghent University Hospital, Belgium. Participants engaged in the virtual T-maze task, a trial-and-error task known to elicit a canonical RewP, while scalp and intracranial EEG were recorded simultaneously. The RewP was identified using a difference wave approach for both scalp and intracranial EEG. The data were aggregated across participants to create a virtual 'meta-participant' that contained all the recorded intracranial event-related brain potentials with respect to their intracranial contact locations. We used both hypothesis-driven (focused on ACC) and exploratory (whole-brain analysis) approaches to segment the brain into regions of interest. For each region of interest, we evaluated the degree to which the time course of the absolute current density (ACD) activity mirrored the time course of the RewP, and we confirmed the statistical significance of the results using permutation analysis. The grand average waveform of the scalp data revealed a RewP at 309 ms after reward feedback with a frontocentral scalp distribution, consistent with the identification of this component as the RewP. The meta-participant contained intracranial event-related brain potentials recorded from 582 intracranial contacts in total. The ACD activity of the aggregated intracranial event-related brain potentials was most similar to the RewP in the left caudal ACC, left dorsolateral prefrontal cortex, left frontomedial cortex and left white matter, with the highest score attributed to caudal ACC, as predicted. To our knowledge, this is the first study to use intracranial EEG aggregated across multiple human epilepsy patients and current source density analysis to identify the neural generator(s) of the RewP. These results provide direct evidence that the ACC is a neural generator of the RewP.