The place-cell representation of volumetric space in rats

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

A boundary vector cell model of place field repetition

Hippocampal place cells are thought to form the neural substrate of a global cognitive map. However, in multicompartment mazes, these cells exhibit locally repeating representations, undermining the global cognitive map view of place cells. This phenomenon appears to be related to the repetitive layout of these mazes, but still no hypothesis adequately explains it. Here, we use a boundary vector cell (BVC) model of place cell firing to model the activity of place cells in numerous multicompartment environments. The activity of modeled place cells bears a striking resemblance to experimental data, replicating virtually every major experimental result. Our results support the BVC model and indicate that locally repeating place cell firing could result purely from local geometry

Volumetric spatial behaviour in rats reveals the anisotropic organisation of navigation

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

Insensitivity of place cells to the value of spatial goals in a two-choice flexible navigation task

Hippocampal place cells show position-specific activity, thought to reflect a self-localization signal. Several reports also point to some form of goal encoding by place cells. We investigated this by asking whether they also encode the value of spatial goals, which is a crucial information for optimizing goal-directed navigation. We used a continuous place navigation task in which male rats navigate to one of two (freely chosen) unmarked locations and wait, triggering the release of reward which is then located and consumed elsewhere. This allows sampling of place fields, and dissociates spatial goal from reward consumption. The two goals varied in the amount of reward provided, allowing assessment of whether the rats factored goal value into their navigational choice, and of possible neural correlates of this value. Rats successfully learned the task, indicating goal localization, and they preferred higher-value goals, indicating processing of goal value. Replicating previous findings, there was goal-related activity in the out-of-field firing of CA1 place cells, with a ramping-up of firing rate during the waiting period, but no general over-representation of goals by place fields, an observation that we extended to CA3 place cells. Importantly, place cells were not modulated by goal value. This suggests that dorsal hippocampal place cells encode space independently of its associated value, despite the effect of that value on spatial behavior. Our findings are consistent with a model of place cells in which they provide a spontaneously constructed value-free spatial representation, rather than encoding other navigationally relevant, but non-spatial, information

Hippocampal place cells encode global location but not connectivity in a complex space

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

Humans Construct Survey Estimates on the Fly from a Compartmentalised Representation of the Navigated Environment

Despite its relevance for navigation surprisingly little is known about how goal direction bearings to distant locations are computed. Behavioural and neuroscientific models proposing the path integration of previously navigated routes are supported indirectly by neural data, but behavioral evidence is lacking. We show that humans integrate navigated routes post-hoc and incrementally while conducting goal direction estimates. Participants learned a multi-corridor layout by walking through a virtual environment. Throughout learning, participants repeatedly performed pairwise pointing from the start location, end location, and each turn location between segments. Pointing latency increased with the number of corridors to the target and decreased with pointing experience rather than environmental familiarity. Bimodal pointing distributions indicate that participants made systematic errors, for example, mixing up turns or forgetting segments. Modeling these error sources suggests that pointing did not rely on one unified, but rather multiple representations of the experimental environment. We conclude that participants performed incremental on-the-fly calculations of goal direction estimates within compartmentalised representations, which was quicker for nearby goals and became faster with repeated pointing. Within navigated environments humans do not compute difference vectors from coordinates of a globally consistent integrated “map in the head”