Ultraslow entorhinal oscillations induce persistent reorganization of internal spatial representations through grid cell drift

Grid cells in the medial entorhinal cortex (MEC) of head-fixed mice exhibit ultraslow (< 0.01 Hz) oscillations (USO) during walking in a 1D running wheel in darkness. Unfortunately, there is no clear link between the functional role of these oscillations and the navigation strategy used by animals to calculate their current position by continuously summing self-motion cues (path integration). Given the synaptic projections from MEC to the hippocampus, we hypothesized that ultraslow oscillations have a role in shaping the internal spatial representation modulating path integration. A realistic computational model of the entorhinal-grid cells and hippocampal-place cells is proposed. The model exhibits ultraslow oscillations and is capable of sustaining path integration of a rodent-like simulated animal. Results indicate that ultraslow oscillations induced persistent changes in the grid cell dynamics, represented as a positional drift of grid fields. Such drift resulted in position estimation errors but generated new grid-place cell associations when combined with synaptic plasticity. We discuss that, ultraslow entorhinal oscillations produced long-lasting and structured reorganization of the internal spatial representation.