Sequential development of task representation from hippocampus to prefrontal cortex supports goal-directed spatial navigation

Successful goal-directed navigation requires the coordination between the hippocampus and medial prefrontal cortex. However, it is not fully confirmed that the medial prefrontal cortex learns its spatial code from the hippocampus. To test this, we examined spatial representations of the intermediate hippocampus and medial prefrontal cortex while rats learned a spatial navigation task. Rats performed a goal-directed spatial navigation task in 2D VR to find an unmarked goal zone, and we discovered robust directional tuning of single neurons in both regions. Neural manifold analysis further confirmed population-level directional tuning in both regions, with manifolds having ring-like geometry. We found that this ring-like structure evolved after learning, in a way that the hippocampal-prefrontal manifolds converged to a shared geometry. Furthermore, this evolution of ring-like structure was preceded by the hippocampus at the trial level. It was further verified that the evolution of the ring-like structure is linked to phase locking to the hippocampal theta rhythm, particularly in the prefrontal manifolds. Our findings provide compelling evidence that spatial representations of the hippocampal-prefrontal network become aligned after learning, and also highlight the information flow from the hippocampus to the medial prefrontal cortex during this geometry synchronization.