Visual boundary cues, alone, can anchor place and grid cells in virtual reality

The hippocampal formation contains neurons responsive to an animals current location and orientation, which together provide the organism with a neural map of space1-3. Spatially tuned neurons rely on external landmark cues and internally generated movement information to estimate position4,5. An important class of landmark cue are the boundaries delimiting an environment, which can define place cell field position6,7 and stabilise grid cell firing8. However, the precise nature of the sensory information used by the hippocampus to detect boundaries remains unknown. Here we use 2-dimensional virtual reality (VR)9 to show that purely visual cues from the surrounding walls are both sufficient and necessary to stabilise place and grid cell responses. Unstable grid cells retain internally coherent, hexagonally arranged firing fields, but these fields drift with respect to the virtual environment over periods >5 sec. Optic flow from a virtual floor does not slow drift dynamics, emphasising the importance of boundary-related visual information. Surprisingly, place fields are more stable close to boundaries even when these are invisible. Invisible boundary locations can only be inferred from the relative movements of the animal and a reward beacon, specifically, from the mismatch between observed beacon movement and that predicted from motor output. This shows that boundary information can be detected through sensorimotor feedback. We find that subsets of place cells show allocentric directional tuning towards the beacon, with strength of tuning correlating with place field stability when boundaries are removed.