How heterogeneous place cell responding arises from homogeneous grids—A contextual gating hypothesis

Abstract

How entorhinal grids generate hippocampal place fields remains unknown. The simplest hypothesis-that grids of different scales are added together-cannot explain a number of place field phenomena, such as (1) Summed grids form a repeating, dispersed activation pattern whereas place fields are focal and nonrepeating; (2) Grid cells are active in all environments but place cells only in some, and (3) Partial environmental changes cause either heterogeneous ("partial") remapping in place cells whereas they result in all-or-nothing "realignment" remapping in grid cells. We propose that this dissociation between grid cell and place cell behavior arises in the entorhinal-dentate projection. By our view, the grid-cell/place-cell projection is modulated by context, both organizationally and activationally. Organizationally, we propose that when the animal first enters a new environment, the relatively homogeneous input from the grid cells becomes spatially clustered by Hebbian processes in the dendritic tree so that inputs active in the same context and having overlapping fields come to terminate on the same sub-branches of the tree. Activationally, when the animal re-enters the now-familiar environment, active contextual inputs select (by virtue of their clustered terminations) which parts of the dendritic tree, and therefore which grid cells, drive the granule cell. Assuming this pattern of projections, our model successfully produces focal hippocampal place fields that remap appropriately to contextual changes.