Online formation of a hierarchical cognitive map for object–place association by theta phase coding

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Object-place associative memory, the storage of object and place conjunctions based on a one-time experience, is hippocampal-dependent in humans. Theta phase precession, a type of neural dynamics observed in the rat hippocampus, has recently been suggested to serve a role in instantaneous memory formation based on a one-time experience, while its functional role in associating distinct types of information (object and place information) is unclear. In this study, we hypothesize that theta phase encoding with theta phase precession contributes to the storage of object-place associations. To examine this hypothesis, we propose a neural network model of the corticohippocampal system, including central-peripheral visual pathways and theta phase coding in the hippocampus. Memory storage computer experiments demonstrate that the hippocampal network successfully stores the object-place associations of a one-time experience. Interestingly, it is also found that a random visual input sequence results in a robust formation of asymmetric connections between objects and scenes instantaneously after a single trial. Furthermore, it is found that scene-object connections and scene-scene connections form a hierarchical network representing the spatial alignment of scenes and objects in the environment. Our findings indicate that the theta phase coding, as observed in the rat hippocampus, can facilitate the online memory storage of complex environments in humans as a hierarchical cognitive map.