Reactivation of single-episode pain patterns in the hippocampus and decision making

Abstract

Aversive and rewarding experiences can exert a strong influence on subsequent behavior. While decisions are often supported by the value of single past episodes, most research has focused on the role of well-learned value associations. Recent studies have begun to investigate the influence of reward-associated episodes, but it is unclear if these results generalize to negative experiences such as pain. To investigate whether and how the value of previous aversive experiences modulates behavior and brain activity, in our experiments female and male human 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, at test, participants exhibited significant pain value memory. 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 significant reactivation of pain-related patterns of activity in the hippocampus, such that activity significantly discriminated high versus low pain episodes. Further, stronger reactivation in the anterior hippocampus was related to improved pain value memory performance. Our results demonstrate that single incidental aversive experiences can build memories that affect decision making and that this influence may be supported by the hippocampus. Significance StatementAversive and rewarding experiences can exert a strong influence on our subsequent behavior. While decisions are often supported by single past negative or positive episodes, most research has focused on the role of well-learned value associations. In experiments using aversive heat pain in conjunction with incidental objects, we found that participants choices were biased by the level of pain associated with the objects. Further, when participants saw the objects again, pain-related neural patterns in the hippocampus were re-expressed and this was related to pain value memory performance. These results suggest a mechanism by which even single negative experiences can guide our later decisions.