Place cells are spatially modulated neurons found in the hippocampus that underlie spatial memory and navigation: how these neurons represent 3D space is crucial for a full understanding of spatial cognition. We wirelessly recorded place cells in rats as they explored a cubic lattice climbing frame which could be aligned or tilted with respect to gravity. Place cells represented the entire volume of the mazes: their activity tended to be aligned with the maze axes, and when it was more difficult for the animals to move vertically the cells represented space less accurately and less stably. These results demonstrate that even surface-dwelling animals represent 3D space and suggests there is a fundamental relationship between environment structure, gravity, movement and spatial memory.

We investigated how entorhinal grid cells encode volumetric space. On a horizontal surface, grid cells usually produce multiple, spatially focal, approximately circular firing fields that are evenly sized and spaced to form a regular, close-packed, hexagonal array. This spatial regularity has been suggested to underlie navigational computations. In three dimensions, theoretically the equivalent firing pattern would be a regular, hexagonal close packing of evenly sized spherical fields. In the present study, we report that, in rats foraging in a cubic lattice, grid cells maintained normal temporal firing characteristics and produced spatially stable firing fields. However, although most grid fields were ellipsoid, they were sparser, larger, more variably sized and irregularly arranged, even when only fields abutting the lower surface (equivalent to the floor) were considered. Thus, grid self-organization is shaped by the environment’s structure and/or movement affordances, and grids may not need to be regular to support spatial computations.

Summary Flexible navigation relies on a cognitive map of space, thought to be implemented by hippocampal place cells: neurons that exhibit location-specific firing. In connected environments, optimal navigation requires keeping track of one’s location and of the available connections between subspaces. We examined whether the dorsal CA1 place cells of rats encode environmental connectivity in four geometrically identical boxes arranged in a square. Rats moved between boxes by pushing saloon-type doors that could be locked in one or both directions. Although rats demonstrated knowledge of environmental connectivity, their place cells did not respond to connectivity changes, nor did they represent doorways differently from other locations. Place cells coded location in a global reference frame, with a different map for each box and minimal repetitive fields despite the repetitive geometry. These results suggest that CA1 place cells provide a spatial map that does not explicitly include connectivity.

We investigated how access to the vertical dimension influences the natural exploratory and foraging behaviour of rats. Using high-accuracy three-dimensional tracking of position in two- and three-dimensional environments, we sought to determine (i) how rats navigated through the environments with respect to gravity, (ii) where rats chose to form their home bases in volumetric space, and (iii) how they navigated to and from these home bases. To evaluate how horizontal biases may affect these behaviours, we compared a 3D maze where animals preferred to move horizontally to a different 3D configuration where all axes were equally energetically costly to traverse. Additionally, we compared home base formation in two-dimensional arenas with and without walls to the three-dimensional climbing mazes. We report that many behaviours exhibited by rats in horizontal spaces naturally extend to fully volumetric ones, such as home base formation and foraging excursions. We also provide further evidence for the strong differentiation of the horizontal and vertical axes: rats showed a horizontal movement bias, they formed home bases mainly in the bottom layers of both mazes and they generally solved the vertical component of return trajectories before and faster than the horizontal component. We explain the bias towards horizontal movements in terms of energy conservation, while the locations of home bases are explained from an information gathering view as a method for correcting self-localisation.

13Place cells are spatially modulated neurons found in the hippocampus that underlie 14 spatial memory and navigation: how these neurons represent 3D space is crucial for a full 15 understanding of spatial cognition. We wirelessly recorded place cells in rats as they 16 explored a cubic lattice climbing frame which could be aligned or tilted with respect to 17 gravity. Place cells represented the entire volume of the mazes: their activity tended to be 18 aligned with the maze axes, and when it was more difficult for the animals to move vertically 19 the cells represented space less accurately and less stably. These results demonstrate that 20 even surface-dwelling animals represent 3D space and suggests there is a fundamental 21 relationship between environment structure, gravity, movement and spatial memory. 22 firing of spatial neurons differed between the floor and the wall, the horizontal and vertical 41 components of firing on the wall did not appreciably differ. Taking these findings together, it 42 seems that the differences in spatial encoding previously seen in the vertical dimension may 43 be due to the different constraints on movement, or the locomotor 'affordances' in the 44 different dimensions 8 . Meanwhile, a study of flying bats found that place fields did not 45 deviate statistically from spherical 9 , suggesting a spatial map of equal resolution in all 46 dimensions (isotropic). 47

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