A Memory Model of Rodent Spatial Navigation: Place Cells are Memories Arranged in a Grid and Grid Cells are Non-spatial

A theory and neurocomputational model are presented that explain grid cell responses as the byproduct of equally dissimilar hippocampal memories. On this account, place and grid cells are best understood as the natural consequence of memory encoding and retrieval. In the proposed memory model, place cells represent memories that are conjunctions of both spatial and non-spatial attributes, and grid cells primarily represent the non-spatial attributes (e.g., sounds, surface texture, etc.) found throughout the two-dimensional recording enclosure. Place cells support memories of the locations where non-spatial attributes can be found (e.g., positions with a particular sound), which are arranged in a hexagonal lattice owing to memory encoding and consolidation processes (pattern separation) as applied to situations in which the non-spatial attributes are found at all locations of a two-dimensional surface. Grid cells exhibit their spatial firing pattern owing to feedback from hippocampal place cells (i.e., a hexagonal pattern of remembered locations for the non-spatial attribute represented by a grid cell). The model explains: 1) grid fields that appear to be centered outside the box; 2) the toroidal nature of grid field representations; 3) grid field alignment with the enclosure borders; 4) modules in which grid cells have the same orientation and spacing but different phases; 5) head direction conjunctive grid cells that become simple head direction cells in the absence of hippocampal feedback; 6) the instant existence of grid fields in a novel environment; 7) the slower learning of place cells; 8) the manner in which head direction sensitivity of place cells changes near borders and in narrow passages; 9) the kinds of changes that underlie remapping of place cells; and 10) grid-like responses for two-dimensional coordinate systems other than navigation.