It's All In The Journey: Putative Strategies Extracted from Navigation Paths Predict Spatial Memory and Hippocampal Recruitment

Navigation in the real world may rely on a multitude of different strategies with distinct advantages and disadvantages. However, the characterization of spontaneous strategy use during wayfinding and underlying neural correlates are scarce. We explore data across three groups of participants who performed a virtual navigation task: (I) epilepsy patients undergoing invasive electrophysiological recordings of the hippocampus, and two groups who underwent fMRI scanning: (II) young adults at genetic risk for Alzheimers disease (APOE-e4 carriers) and (III) healthy controls. We establish three metrics by which to quantitatively characterize each taken path, with the aim of simultaneously reflecting the putative strategies used by humans to solve the task: 1. straightness of paths; 2. deviation towards the edge of the circular arena; and 3. overlap of individual paths leading to a specific object location, which putatively relate to reliance on allocentric (1) and egocentric reference frames (2 & 3). Extracted metrics were related to performance in the task and to hippocampal activity. We find that strategy use is variable within participant, changes across the experiment, and is adaptive in a group-dependent manner. While hippocampal BOLD activity and theta (gamma) power were generally inversely (positively) related, we found that the recruitment of the hippocampus was both group- and strategy- specific. Our results further our understanding of the heterogeneous and idiosyncratic nature of spatial navigation by revealing, how these behaviors are altered by disease and the subsequent compensatory neural dynamics, as well as the link between mesoscopic and macroscopic neural signals.