Learning place cells and remapping by decoding the cognitive map

Hippocampal place cells are known for their spatially selective firing and are believed to encode an animal's location while forming part of a cognitive map of space. These cells exhibit marked tuning curves and rate changes when an animal's environment is sufficiently manipulated, in a process known as remapping. Place cells are accompanied by many other spatially tuned cells, such as border cells and grid cells, but how these cells interact during navigation and remapping is unknown. In this work, we build a normative place cell model wherein a neural network is tasked with accurate position reconstruction and path integration. Motivated by the notion of a cognitive map, the network's position is estimated directly from its learned representations. To obtain a position estimate, we propose a non-trainable decoding scheme applied to network output units, inspired by the localized firing patterns of place cells. We find that output units learn place-like spatial representations, while upstream recurrent units become boundary-tuned. When the network is trained to perform the same task in multiple simulated environments, its place-like units learn to remap like biological place cells, displaying global, geometric, and rate remapping. These remapping abilities appear to be supported by rate changes in upstream units. While the model does not learn grid-like units, its place unit centers form clusters organized in a hexagonal lattice in open fields. When we decode the center locations of CA1 place fields in mice, we find preliminary evidence of a similar clustering tendency. This suggests a potential mechanism for the interaction between place cells, border cells, and grid cells. Our model provides a normative framework for learning spatial representations previously reserved for biological place cells, providing new insight into place cell field formation and remapping.