Cortical dissociation of spatial reference frames during place navigation

Abstract

Animals rely on both sensory perception and memory when navigating relative to learned allocentric locations. Incoming sensory stimuli, which arrive from an egocentric perspective, must be integrated into an allocentric reference frame to allow neural computations that direct an animal toward a learned goal. This egocentric-allocentric spatial transformation has been proposed to involve projections from the rodent postrhinal cortex (POR), which receives strong visual input, to the medial entorhinal cortex (MEC), which contains allocentric spatial cell types such as grid and border cells. A major step toward understanding this transformation is to identify how POR and MEC spatial representations differ during place navigation, which is currently unknown. To answer this question, we recorded single neurons from POR and MEC as rats engaged in a navigation task that required them to repeatedly visit a learned uncued allocentric location in an open field arena to receive a randomly scattered food reward. While neurons in both regions displayed strong tuning to the spatial structure of the environment, neither showed bias toward the goal location despite strongly biased behavior. Critically, when local visual landmarks were manipulated to place the visual scene in conflict with the learned location, POR neurons adjusted their tuning preferences to follow the visual landmarks, while MEC neurons remained in register with the true global reference frame. These findings reveal a strong dissociation between POR and MEC spatial reference frames during place navigation and raise questions regarding the mechanisms underlying integration of POR egocentric signals into the MEC allocentric spatial map.