Asymmetric representation of aversive prediction errors in Pavlovian threat conditioning

Survival in biological environments requires learning associations between predictive sensory cues and threaten-ing outcomes. Such aversive learning may be implemented through reinforcement learning algorithms that are driven by the signed difference between expected and encountered outcomes, termed prediction errors (PEs). While PE-based learning is well established for reward learning, the role of putative PE signals in aversive learn-ing is less clear. Here, we used functional magnetic resonance imaging in humans (21 healthy men and women) to investigate the neural representation of PEs during maintenance of learned aversive associations. Four visual cues, each with a different probability (0, 33, 66, 100%) of being followed by an aversive outcome (electric shock), were repeatedly presented to participants. We found that neural activity at omission (US-) but not oc-currence of the aversive outcome (US +) encoded PEs in the medial prefrontal cortex. More expected omission of aversive outcome was associated with lower neural activity. No neural signals fulfilled axiomatic criteria, which specify necessary and sufficient components of PE signals, for signed PE representation in a whole-brain search or in a-priori regions of interest. Our results might suggest that, different from reward learning, aversive learning does not involve signed PE signals that are represented within the same brain region for all conditions.

Automated summary

Survival in biological environments requires learning associations between predictive sensory cues and threatening outcomes, which may be implemented through reinforcement learning algorithms driven by prediction errors (PEs). This study investigated the neural representation of PEs during maintenance of learned aversive associations using fMRI, revealing that PEs were encoded in the medial prefrontal cortex during the omission of aversive outcomes.