Spatially Periodic Computation in the Entorhinal-Hippocampal Circuit During Navigation

Abstract

To enable navigation in both physical and mental spaces, the human brain employs a cognitive map constructed from the global metrics of the entorhinal cortex and the local representations of the hippocampus. However, how these two regions coordinate to enable navigation remains poorly understood. 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 in the hippocampal activity that tracked navigation directions from object variants to the central prototype. This hippocampal periodicity was phase-locked with the well-documented 6-fold periodicity of the entorhinal cortex, suggesting hierarchical interaction between these regions. Consistent with this neural pattern, a corresponding 3-fold periodicity was observed in behavioral performance, which was synchronized with hippocampal activity. Finally, an EC-HPC PhaseSync model reproduced this phenomenon, in which the 6-fold activity periodicity of entorhinal grid cells across directions projects vectorial representations to the hippocampus, and the collection of these vectors exhibits 3-fold periodicity to represent conceptual directions. Together, these findings reveal a periodic mechanism through which entorhinal grid codes structure hippocampal vector representations.