Ultraslow entorhinal oscillations shape spatial memory through grid cell drifting

ABSTRACT Context 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. It was proposed that these oscillations may have a connection with navigational behavior. Problem There is no clear link between the functional role of these oscillations and path integration, a fundamental navigation strategy used by animals to calculate their current position and orientation by continuously summing self-motion cues. Hypothesis Given the synaptic projections from MEC to the hippocampus, we hypothesized that ultraslow oscillations have a role in linking spatiotemporal memories acquired during navigation. Methodology A realistic computational model of entorhinal-grid with ultraslow oscillations and hippocampal-place cells is proposed using synaptic plasticity between cell types, sustaining path integration of a rodent-like simulated animal. Results 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. >Discussions Ultraslow entorhinal oscillations were found to shape spatial memory through grid cell drifting, which could serve as a mechanism for flexibly accessing different spatial memories during navigation. HIGHLIGHTS Path integration dynamics hide ultraslow oscillations despite coexistence. Ultraslow oscillations significantly degrade position estimation in path integration. Grid and place fields drift after the effect of ultraslow oscillations. New spatial memories were created as a result of the ultraslow oscillation drift. Ultraslow oscillations enable dynamic access of different spatial memories