Learning an efficient place cell map from grid cells using non-negative sparse coding

Abstract

Cells in the entorhinal cortex (EC) contain rich spatial information and projects strongly to the hippocampus where a cognitive map is supposedly created. These cells range from cells with structured spatial selectivity, such as grid cells in the medial entorhinal cortex (MEC) that are selective to an array of spatial locations that form a hexagonal grid, to weakly spatial cells, such as non-grid cells in the MEC and lateral entorhinal cortex (LEC) that contain spatial information but have no structured spatial selectivity. However, in a small environment, place cells in the hippocampus are generally selective to a single location of the environment, while granule cells in the dentate gyrus of the hippocampus have multiple discrete firing locations but lack spatial periodicity. Given the anatomical connection from the EC to the hippocampus, how the hippocampus retrieves information from upstream EC remains unclear. Here, we propose a unified learning model that can describe the spatial tuning properties of both hippocampal place cells and dentate gyrus granule cells based on non-negative sparse coding from EC input. Sparse coding plays an important role in many cortical areas and is proposed here to have a key role in the hippocampus. Our results show that the hexagonal patterns of MEC grid cells with various orientations, grid spacings and phases are necessary for the model to learn different place cells that efficiently tile the entire spatial environment. However, if there is a lack of diversity in any grid parameters or a lack of hippocampal cells in the network, this will lead to the emergence of hippocampal cells that have multiple firing locations. More surprisingly, the model can also learn hippocampal place cells even when weakly spatial cells, instead of grid cells, are used as the input to the hippocampus. This work suggests that sparse coding may be one of the underlying organising principles for the navigational system of the brain. Significance StatementThe brain can perform extremely complex spatial navigation tasks, but how it does this remains unclear. Here we show that the principle of sparse coding can be used to learn the hippocampal place map in a way that efficiently tiles the entire spatial environment using EC inputs, namely either grid cells or weakly spatial cells. This demonstrates that the hippocampus can retrieve spatial information from the entorhinal cortex using an efficient representation and that sparse coding may be one of the underlying principles of the navigational system of the brain.