Reactivation of pain-related patterns in the hippocampus from single past episodes relates to successful memory-based decision making

Aversive and rewarding previous experiences can exert a strong influence on our subsequent behavior. During decision making, sampling from these previous episodes may support our choices, but relatively little is known about how the value of single experiences is represented. Further, while recent research has investigated reward-associated episodes, it is unclear if these results generalize to negative experiences such as pain. To investigate whether value-related regions or the hippocampus represent the value of previous aversive experiences, in our experiments participants experienced episodes of high or low pain in conjunction with incidental, trial-unique neutral pictures. In an incentive-compatible surprise test phase, we found that participants avoided pain-paired objects. In a separate fMRI experiment, participants exhibited significant source memory for value. Neurally, when participants were re-exposed to pain-paired objects, we found no evidence for reactivation of pain-related patterns in pain-responsive regions such as the anterior insula. Critically, however, we found that patterns of activity in the hippocampus significantly discriminated episodic pain associations. Further, stronger reactivation in the anterior hippocampus was related to improved value memory performance. Our results demonstrate that single incidental aversive experiences can build reliable memories that affect decision making and that this influence may be supported by the hippocampus.