Intrinsic and circuit mechanisms of predictive coding in a grid cell network model

Grid cells in the medial entorhinal cortex (MEC) fire when an animal is located at the vertices of a hexagonal grid that extends across the environment. The population activity of grid cells serves as an allocentric representation of the current location of the animal. Recent studies have identified a class of grid cells that represent locations ahead of the animal. How do these predictive representations emerge from the wetware of the MEC? To address this question, we developed a detailed conductance-based model of the MEC network, constrained by existing data on the biophysical properties of stellate cells and the topology of the MEC network. Our model revealed two mechanisms underlying the emergence of a predictive code in the MEC. The first relied on a time scale associated with the HCN conductance. The other depended on the degree of asymmetry in the topology of the MEC network. The former mechanism was sufficient to explain predictive coding in layer II grid cells that represented locations shifted ahead of the current location. The shift was equivalent to ~5% of the diameter of a grid field. The latter mechanism was required to model predictive representations in layer III grid cells that were shifted forward by a distance of ~25% of the diameter of a grid field. A corollary of our model, that the extent of the predictive code changes monotonically along the dorsoventral axis of the MEC following observed changes in the properties of the HCN conductance, is borne out by recent experiments.