Hippocampus guides adaptive learning during dynamic social interactions

Abstract

How do we evaluate whether someone will make a good friend or collaborative peer? A hallmark of human cognition is the ability to make adaptive decisions based on information garnered from limited prior experiences. Using an interactive social task measuring adaptive choice (deciding who to re-engage or avoid) in male and female participants, we find the hippocampus supports value-based social choices following single shot learning. These adaptive choices elicited a suppression signal in the hippocampus, revealing sensitivity for the subjective perception of a person and how well they treat you during choice. The extent to which the hippocampus was suppressed was associated with flexibly interacting with prior generous individuals and avoiding selfish individuals. Further, we found that hippocampal signals during decision-making were related to subsequent memory for a person and the offer they made before. Consistent with the hippocampus leveraging previously executed choices to solidify a reliable neural signature for future adaptive behavior, we also observed a later hippocampal enhancement. These findings highlight the hippocampus playing a multifaceted role in socially adaptive learning.

SIGNIFICANCE STATEMENT

Adaptively navigating social interactions requires an integration of prior experiences with information gleaned from the current environment. While most research has focused on striatal-based feedback learning, open questions remain regarding the role of hippocampal-based episodic memory systems. Here, we show that during social decisions based on prior experience, hippocampal suppression signals were sensitive to adaptive choice, while hippocampal enhancements was related to subsequent memory for the original social interaction. These findings highlight the hippocampus playing a multifaceted role in socially adaptive learning.