Efficient and flexible representation of higher-dimensional cognitive variables with grid cells

Abstract

© 2020 Klukas et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. We shed light on the potential of entorhinal grid cells to efficiently encode variables of dimension greater than two, while remaining faithful to empirical data on their low-dimensional structure. Our model constructs representations of high-dimensional inputs through a combination of low-dimensional random projections and “classical” low-dimensional hexagonal grid cell responses. Without reconfiguration of the recurrent circuit, the same system can flexibly encode multiple variables of different dimensions while maximizing the coding range (per dimension) by automatically trading-off dimension with an exponentially large coding range. It achieves high efficiency and flexibility by combining two powerful concepts, modularity and mixed selectivity, in what we call “mixed modular coding”. In contrast to previously proposed schemes, the model does not require the formation of higher-dimensional grid responses, a cell-inefficient and rigid mechanism. The firing fields observed in flying bats or climbing rats can be generated by neurons that combine activity from multiple grid modules, each representing higher-dimensional spaces according to our model. The idea expands our understanding of grid cells, suggesting that they could implement a general circuit that generates on-demand coding and memory states for variables in high-dimensional vector spaces.