Translational differentiation of vertically displaced surfaces by grid cells

Navigation is commonly associated with two-dimensional (2D) representations of space. Recordings from place and grid cells in the rodent and bat brain have largely upheld this association. Recent studies have investigated how these 2D representations might extend into the three-dimensional (3D) world. One unexplored question is whether grid cells represent vertically separated horizontal surfaces as a single 3D space or distinct planar environments. To address this issue, we recorded grid cells as rats foraged in both an open-field environment and one with a transparent floor suspended directly above the open-field environment. Rats either actively locomoted up a ramp to the elevated environment, or they were passively moved between the two environments, to test how differences in path integration may affect grid cell firing. We found that grid cell firing patterns in the elevated environment were translated (but not rotated) relative to those in the floor environment and were consistent across active and passive sessions. The translation of the grid pattern on the elevated surface was consistent among co-recorded grid cells but differed between animals and between different groups of grid cells recorded from the same animal. Non-grid spatially modulated cells also rearranged their location preferences between the two surfaces. Overall, we did not observe any evidence that the two surfaces were represented with a single 3D representation but instead were treated as two distinct surfaces connected by a common orientation signal. These findings suggest that grid cell representations on visually distinct, vertically displaced horizontal surfaces are planar rather than volumetric.