Reference frames for spatial navigation and declarative memory: Individual differences in performance support the phylogenetic continuity hypothesis

Abstract

Recent experimental evidence has led to the idea that the neural mechanisms supporting spatial navigation have been flexibly adapted to organize concepts and memories through spatial codes. The “phylogenetic continuity hypothesis” (Buszáki & Moser, 2013) further proposes that the mechanisms supporting episodic and semantic memory would have respectively evolved from self-based (i.e. egocentric) and map-based (i.e. allocentric) spatial navigation mechanisms. Recent studies have observed traces of this phylogenetic continuity in human behavior, but the full original model has not yet been tested. Here, we evaluated the relationships between the four model components by using two sets of tasks in the spatial navigation and declarative memory domains based on complex materials and emphasizing the self vs. map-based processing (i.e. route vs. survey component for spatial navigation and episodic vs. semantic component for declarative memory). Consistent with the model predictions, the results of a multiple multivariate regression analysis revealed a specific across-domain relationship, such that route-based navigation performance specifically predicted episodic memory performance (self-based, egocentric components), while survey navigation performance specifically predicted the semantic memory one (map-based, allocentric components). The results of an additional regression analysis on the within-domain transformation process from self-based to map-based representations confirmed that route-based navigation specifically predicted survey navigation, while episodic memory specifically predicted semantic memory. Our results provide further behavioral evidence in support of the general hypothesis that the neural machinery evolved to map the physical world might have been recycled to organize memory and conceptual knowledge. Crucially, they also support the more specific hypothesis that the organizational principles involved in higher-level processing of information have inherited the fundamental distinction between different reference frames (egocentric vs. allocentric) for navigation in the physical world.