Change-resistance distinguishes the representational geometries of human spatial memory and mouse CA1 in deformed environments

Abstract

Prior work has highlighted qualitative similarities between the neural instantiations of cognitive maps in rodents and memory-guided navigation in humans, suggesting a conservation of representational structure across species. Yet evidence of cross-species differences in neural coding continues to mount. Our ability to reconcile these similarities and differences has been inherently limited by the qualitative nature of our cross-species comparisons. To overcome this limitation, here we combine recent technical and theoretical advances to characterize the representational geometry of human spatial memory during a diverse set of environmental deformations and compare this geometry to that of mouse CA1. Across three untethered immersive virtual reality experiments (n > 100 participants per experiment), we find that deformations induce compounding local distortions in human spatial memory. These distortions yield a representational geometry which closely resembles a change-resistant version of that of mouse hippocampal CA1 during analogous deformations. The geometries of mouse CA1 subpopulations with higher firing rates, spatial tuning stability, and spatial tuning specificity all better resembled that of human spatial memory. The precision, but not accuracy, of human spatial memory also modulated cross-species resemblance. The local impact of deformations scaled up when humans navigated a larger environment, preserving representational geometry and cross-species resemblance. Neither geometry nor cross-species resemblance depended on the human visual advantage during retrieval. Together, these results establish a common cross-species resemblance in the representational geometry of mouse CA1 and human spatial memory during environmental deformations, with a notable difference in the resistance to change between these assays.