The aversion positivity: Mediofrontal cortical potentials reflect parametric aversive prediction errors and drive behavioral modification following negative reinforcement

Abstract

Reinforcement learning capitalizes on prediction errors (PEs), representing the deviation of received outcomes from expected outcomes. Mediofrontal event-related potentials (ERPs), in particular the feedback-related negativity (FRN)/reward positivity (RewP), are related to PE signaling, but there is disagreement as to whether the FRN/RewP encode signed or unsigned PEs. PE encoding can potentially be dissected by time-frequency analysis, as frontal theta [4–8 Hz] might represent poor outcomes, while central delta [1–3 Hz] might instead represent rewarding outcomes. However, cortical PE signaling in negative reinforcement is still poorly understood, and the role of cortical PE representations in behavioral reinforcement learning following negative reinforcement is relatively unexplored. We recorded EEG while participants completed a task with matched positive and negative reinforcement outcome modalities, with parametrically manipulated single-trial outcomes producing positive and negative PEs. We first demonstrated that PEs systematically influence future behavior in both positive and negative reinforcement conditions. In negative reinforcement conditions, mediofrontal ERPs positively signaled unsigned PEs in a time window encompassing the P2 potential, and negatively signaled signed PEs for a time window encompassing the FRN/RewP and frontal P3 (an “aversion positivity”). Central delta power increased parametrically with increasingly aversive outcomes, contributing to the “aversion positivity”. Finally, negative reinforcement ERPs correlated with RTs on the following trial, suggesting cortical PEs guide behavioral adaptations. Positive reinforcement PEs did not influence ERP or time-frequency activity, despite significant behavioral effects. These results demonstrate that mediofrontal PE signals are a mechanism underlying negative reinforcement learning, and that delta power increases for aversive outcomes might contribute to the “aversion positivity.”