Entorhinal-hippocampal interactions lead to globally coherent representations of space

The firing maps of grid cells in the entorhinal cortex are thought to provide an efficient metric system capable of supporting spatial inference in all environments. However, whether spatial representations of grid cells are determined by local environment cues or are organized into globally coherent patterns remains undetermined. We propose a navigation model containing a path integration system in the entorhinal cortex and a cognitive map system in the hippocampus. In the path integration system, grid cell network and head direction (HD) cell network integrate movement and visual information, and form attractor states to represent the positions and head directions of the animal. In the cognitive map system, a topological map is constructed capturing the attractor states of the path integration system as nodes and the transitions between attractor states as links. On loop closure, when the animal revisits a familiar place, the topological map is calibrated to minimize odometry errors. The change of the topological map is mapped back to the path integration system, to correct the states of the grid cells and the HD cells. The proposed model was tested on iRat, a rat-like miniature robot, in a realistic maze. Experimental results showed that, after familiarization of the environment, both grid cells and HD cells develop globally coherent firing maps by map calibration and activity correction. These results demonstrate that the hippocampus and the entorhinal cortex work together to form globally coherent metric representations of the environment. The underlying mechanisms of the hippocampal-entorhinal circuit in capturing the structure of the environment from sequences of experience are critical for understanding episodic memory.