Living off the grid: Spatial representations show systematic non-Euclidean distortions regardless of their age and how measured

Abstract

Spatial memory is invaluable for most mobile organisms, yet nature of the underlying representations that we employ for spatial memory has been fiercely contested. On the one hand, the presence of place cells in the hippocampus and grid cells in the medial entorhinal cortex appear to support the argument spatial representations may follow Euclidean axioms, termed "the cognitive map hypothesis." On the other hand, decades of behavioral research in humans reveals that spatial memory often shows characteristic distortions, leading to the alternative, cognitive graph hypothesis, to account for this aspect of spatial memory. Importantly, the majority of laboratory studies tend to occur within novel environments in which participants often have only limited exposure and no personal relevance. We were interested in studying large-scale memory across multiple time scales: from a virtual environment (e.g., learned over several minutes) to a college campus (e.g., months to a few years) to a hometown environment (e.g., many years). Across several tasks, we found that participants exhibited systematic distortions in their memory for all of these environments. Likewise, we found significant correlations between performance on several spatial memory tasks (both between participants and within-participant analyses of patterns of errors), thus suggesting that these tasks tap into partially overlapping cognitive representations and supporting their construct validity. Altogether, our findings provide clear evidence for cognitive graph hypothesis and support the construct validity of several spatial memory tasks within large-scale, real-world environments that are learned over the course of several months to years. Public Significance StatementSpatial memory is key for our ability to live independent lives (e.g., patients with Alzheimers disease lose independence, partially due to disorientation in familiar environments). Typical laboratory-based measures of spatial memory use novel environments that may differ in complexity vs. real-world environments (e.g., size, layout, number of landmarks, duration of exploration, personal relevance). We leveraged breakthroughs in technology to study spatial memory across several tasks and temporal scales, from a novel environment navigated over the course of several minutes to a university campus (e.g., months to years) to hometowns (e.g., years to decades). We observed consistent evidence for systematic distortions in spatial memory, which supports the hypothesis that spatial memory is supported by a cognitive graph, thus posing an important challenge to the extremely influential Euclidean, "cognitive map" hypothesis that was awarded a Nobel Prize in 2014.