Overlap among spatial memories triggers repulsion of hippocampal representations

Abstract

Across the domains of spatial navigation and episodic memory, the hippocampus is thought to play a critical role in disambiguating (pattern separating) representations of overlapping events. However, the mechanisms underlying hippocampal pattern separation are not fully understood. Here, using a naturalistic route-learning paradigm and spatiotemporal pattern analysis of human fMRI data, we found that hippocampal representations of overlapping routes gradually diverged with learning to the point that they became less similar than representations of non-overlapping events. This representational reversal of the objective route similarity (a) was selective to the hippocampus, (b) only occurred for the specific route segments that were shared across routes, and (c) was predicted by the degree to which individual hippocampal voxels were initially shared across route representations. These findings indicate that event overlap triggers a repulsion of hippocampal representations--a finding that provides critical mechanistic insight into how and why hippocampal representations become separated.