Focusing on what matters: Modulation of the human hippocampus by relational attention.

Abstract

Hippocampal episodic memory is fundamentally relational, comprising links between events and the spatiotemporal contexts in which they occurred. Such relations are also important over shorter timescales, during online perception. For example, how do we assess the relative spatial positions of objects, their temporal order, or the relationship between their features? Here, we investigate the role of the hippocampus in online relational processing by manipulating attention to different kinds of relations. While undergoing fMRI, participants viewed two images in rapid succession on each trial and performed one of three relational tasks, judging the images' relative: spatial positions, temporal onsets, or sizes. Additionally, they sometimes judged whether one image was tilted, irrespective of the other. This served as a baseline item task with no demands on relational processing. The hippocampus showed reliable deactivation when participants attended to relational vs. item information. Attention to temporal relations was associated with the most robust deactivation. One interpretation of such deactivation is that it reflects hippocampal disengagement. If true, there should be reduced information content and noisier activity patterns for the temporal vs. other tasks. Instead, multivariate pattern analysis revealed more stable hippocampal representations in the temporal task. This increased pattern similarity was not simply a reflection of lower univariate activity. Thus, the hippocampus differentiates between relational and item processing even during online perception, and its representations of temporal relations are particularly robust. These findings suggest that the relational computations of the hippocampus extend beyond long-term memory, enabling rapid extraction of relational information in perception.