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Distinct algorithms for combining landmarks and path integration in medial entorhinal, visual and retrosplenial cortex

During navigation, animals estimate their position using path integration and landmarks, engaging many brain areas. Whether these areas follow specialized or universal cue integration principles remains unknown. Here, we combined electrophysiology with virtual reality to quantify cue integration across thousands of neurons in three areas that support navigation: primary visual (V1), retrosplenial (RSC) and medial entorhinal cortex (MEC). Path integration influenced position estimates in MEC more than in V1 and RSC. V1 coded position retrospectively, likely reflecting delays in sensory processing, whereas MEC coded position prospectively, and RSC was intermediate between the two. In combining path integration with landmarks, MEC showed signatures of Kalman filtering, and we report a distance-tuned neural population that could implement such filtering through attractor dynamics. Our results show that during navigation, MEC serves as a specialized cortical hub for reconciling path integration and landmarks to estimate position and suggest an algorithm for calculating these estimates.