Spatially Periodic Computation in the Entorhinal-Hippocampal Circuit During Navigation

Abstract To achieve the computational goal of navigating in both physical and mental spaces, the human brain employs a cognitive map constructed by the global metrics of the entorhinal cortex and the local locations of the hippocampus. However, the mechanism by which these two areas interact to support navigation remains unclear. Here, we designed an object-matching task where human participants unknowingly manipulated object variants arranged in a ring-like structure around a central prototype. Functional MRI revealed a 3- fold spatial periodicity of hippocampal activity, which tracked the navigation trajectories from the original object variants to the central prototype in the object space. Importantly, this spatial periodicity of the hippocampus was phase-locked with the well-documented 6-fold periodicity of the entorhinal cortex, suggesting a periodic mechanism connecting these two areas. In addition, the 3-fold periodicity was replicated in human behavior, which varied with a function of spatial directions and phase-locked with hippocampal activity. Finally, we proposed an EC-HPC PhaseSync model, illustrating a framework of the hippocampal-entorhinal network, in which the 6-fold spatial periodicity of entorhinal grid cell populations embeds vector fields that are represented in the hippocampus for conceptual navigation.