Differential replay of reward and punishment paths predicts approach and avoidance

Abstract

Neural replay is implicated in planning, where states relevant to a task goal are rapidly reactivated in sequence. It remains unclear whether, during planning, replay relates to an actual prospective choice. Here, using magnetoencephalography (MEG), we studied replay in human participants while they planned to either approach or avoid an uncertain environment containing paths leading to reward or punishment. We find evidence for forward sequential replay during planning, with rapid state-to-state transitions from 20 to 90 ms. Replay of rewarding paths was boosted, relative to aversive paths, before a decision to avoid and attenuated before a decision to approach. A trial-by-trial bias toward replaying prospective punishing paths predicted irrational decisions to approach riskier environments, an effect more pronounced in participants with higher trait anxiety. The findings indicate a coupling of replay with planned behavior, where replay prioritizes an online representation of a worst-case scenario for approaching or avoiding.