One-shot entorhinal maps enable flexible navigation in novel environments

Abstract

Animals face the substantial challenge of navigating novel environments to find food, shelter, or mates. In mammals, hexagonal grid cells in the medial entorhinal cortex create a map-like population representation of the external environment 1-7. However, it remains unclear how the grid map can adapt to novel environmental features on a rapid, behaviorally relevant time scale. By recording over fifteen thousand grid cells in mice navigating virtual environments, we found grid cell activity was weakly anchored to landmark inputs through a fixed circuit relationship. A computational model based on this fixed circuit assumption accurately predicted grid spatial patterns in environments with novel landmark rearrangements. Finally, a medial entorhinal cortex-dependent task revealed that while grid cell firing patterns remain anchored to landmarks, behavior can adapt to changes in landmark location via a downstream region implementing behavioral time scale synaptic plasticity 8. This fixed but weak anchoring of grid cells to landmarks endows the grid map with powerful computational properties. The fixed nature allows the generation of rapid stable maps for novel environments after a single exposure. The weak nature allows these rapidly formed maps to incur only small distortions between distances traveled in real versus neural space. Overall, such rapid low distortion mapping can then mediate accurate navigational behavior in rapidly changing environments through downstream plasticity.