Navigation Patterns and Scent Marking: Underappreciated Contributors to Hippocampal and Entorhinal Spatial Representations?

Abstract

According to the currently prevailing theory, hippocampal formation constructs and maintains cognitive spatial maps. Most of the experimental evidence for this theory comes from the studies on navigation in laboratory rats and mice, typically male animals. While these animals exhibit a rich repertoire of behaviors associated with navigation, including locomotion, head movements, whisking, sniffing, raring and scent marking, the contribution of these behavioral patterns to the hippocampal spatially-selective activity has not been sufficiently studied. Instead, many publications have considered animal position in space as the major variable that affects the firing of hippocampal place cells and entorhinal grid cells. Here we argue that future work should focus on a more detailed examination of different behaviors exhibited during navigation to better understand the mechanism of spatial tuning in hippocampal neurons. As an inquiry in this direction, we have analyzed data from two datasets, shared online, containing recordings from rats navigating in square and round arenas. Our analyses revealed patchy navigation patterns, evident from the spatial maps of animal position, velocity and acceleration. Moreover, grid cells available in the datasets exhibited similar periodicity as the navigation parameters. These findings indicate that activity of grid cells could affect navigation parameters and/or vice versa. Additionally, we speculate that scent marks left by navigating animals could contribute to neuronal responses while rats and mice sniff their environment; the act of sniffing could modulate neuronal discharges even in virtual visual environments. Accordingly, we propose that future experiments should contain additional controls for navigation patterns, whisking, sniffing and maps composed of scent marks.

Keywords: chicken or egg dilemma; grid cells; head direction cells; hippocampal formation; navigation behavior; place cells; scent marking.

Figure 1

Navigation trajectories during open-field foraging in a square arena. Columns of panels (left, middle, right) correspond to different recording sessions for the same rat. (A–C) Trajectories from a rat foraging for Froot Loops in a square arena. (D–F) Occupancy map constructed from the trajectories. (G–I) Vector fields for navigation velocity plotted together with color-coded maps of vector-field divergence. (J–L) Autocorrelation for velocity divergence. Data was taken from the shared dataset: http://dx.doi.org/10.6080/K0Z60KZ9. Experimental sessions: hc2. Original study: Mizuseki et al. (2009a,b).

Figure 2

Navigation trajectories and grid-cell patterns during open-field foraging in a round arena. Panels (A–L) correspond to one rat, panels (M–R) to a different rat. (A,M) Trajectories from rats foraging for chocolate crumbs in a round arena. (B) Vector field for navigation velocity plotted together with a color-coded map of the field curl. (C) Vector field for acceleration, and its curl. (D,N) Occupancy maps for the trajectories shown in (A,M), respectively. (E) Vector field for acceleration and its divergence. (G,P) Maps representing activity of grid cells. (H) Crosscorrelation between cell activity and velocity curl. (I) Crosscorrelation between cell activity and acceleration curl. (K) Crosscorrelation between cell activity and velocity divergence. (L,R) Crosscorrelation between cell activity and acceleration divergence. Data was taken from the shared dataset: https://www.ntnu.edu/kavli/research/grid-cell-data. Original study: Hafting et al. (2005).