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, 116 (10), 4631-4636

Altered Neural Odometry in the Vertical Dimension

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Altered Neural Odometry in the Vertical Dimension

Giulio Casali et al. Proc Natl Acad Sci U S A.

Erratum in

Abstract

Entorhinal grid cells integrate sensory and self-motion inputs to provide a spatial metric of a characteristic scale. One function of this metric may be to help localize the firing fields of hippocampal place cells during formation and use of the hippocampal spatial representation ("cognitive map"). Of theoretical importance is the question of how this metric, and the resulting map, is configured in 3D space. We find here that when the body plane is vertical as rats climb a wall, grid cells produce stable, almost-circular grid-cell firing fields. This contrasts with previous findings when the body was aligned horizontally during vertical exploration, suggesting a role for the body plane in orienting the plane of the grid cell map. However, in the present experiment, the fields on the wall were fewer and larger, suggesting an altered or absent odometric (distance-measuring) process. Several physiological indices of running speed in the entorhinal cortex showed reduced gain, which may explain the enlarged grid pattern. Hippocampal place fields were found to be sparser but unchanged in size/shape. Together, these observations suggest that the orientation and scale of the grid cell map, at least on a surface, are determined by an interaction between egocentric information (the body plane) and allocentric information (the gravity axis). This may be mediated by the different sensory or locomotor information available on a vertical surface and means that the resulting map has different properties on a vertical plane than a horizontal plane (i.e., is anisotropic).

Keywords: entorhinal cortex; grid cells; hippocampus; place cells; three-dimensional space.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Spatial firing patterns of grid cells on the floor vs. the wall. (A) Schematic representation of the floor-wall apparatus, with the side walls shown as transparent for clarity. (B) Examples of the firing patterns of seven grid cells from six rats on floor (Bottom Left, red) and wall (Top Left, turquoise). For each cell, the Left shows the animal’s path (black lines) with spikes (colored dots) superimposed, and the Right shows firing-rate heat maps from red (maximum) to blue (zero). Values above the heat maps show the peak firing rate (at left) and grid score (at right). (C) There was a significant drop in the number of grid cells on the wall compared with the floor, as shown in the pie chart representing percentages of grid cells (n = 148) that reached classification criteria on each of the two surfaces. (For the full classification, including the open field, see SI Appendix, Fig. S4O.) (DI) Firing parameters between surfaces: box plots (outside) and colored points (inside) connected by gray lines representing the same cells on floor (red) and wall (turquoise) (Left) and rain plots showing kernel density estimate of firing parameters across surfaces (Right). The code for raincloud plot visualization has been adapted from Allen et al. (23).
Fig. 2.
Fig. 2.
Preserved spatial metrics of place cells on the wall. (A) Examples of the firing patterns of six place cells, as shown in Fig. 1, classified as active: on the floor only (Top row), on floor and wall (Middle row), and on the wall only (Bottom row). (B) Pie chart showing the percentage of (n = 72) place cells active on each surface (color code as in Fig. 1C), illustrating a significant drop in the number of active cells on the wall compared with the floor. (CE) Comparison of firing parameters between surfaces, as shown in Fig. 1.
Fig. 3.
Fig. 3.
Altered speed coding on the wall. (AC) Effects of vertical locomotion on LFP theta (n = 48). (A and B) Means (lines) ± SEM (shaded areas) between surfaces (floor, red; wall, turquoise). (A) Power spectrum density (PSD) showing clear peaks in the theta band (7–11 Hz) of both surfaces but reduced power and frequency on the wall compared with the floor. (B) Theta frequency as a function of running speed showing clear reduction on the wall compared with the floor. (C) Fisher’s Z transformation of the speed/theta frequency relationship between surfaces (shown as in Fig. 1). (DF) Effects of vertical locomotion on speed cell firing. (D) There was a significant drop in the number of significant speed cells on the wall compared with the floor, as shown in the pie chart representing percentages of speed cells (n = 461) that reached classification criteria on each surface (color code as in Fig. 1C). Speed cells showed overall reduced firing rate (FR) across speed (E) and reduced speed score on the wall compared with the floor (Fisher’s Z transformation of the speed/firing rate relationship between surfaces) (F). (G and H) Effects of vertical locomotion on spiking rhythmicity of grid and speed cells. (G) Difference between mean spike train theta frequency and ΔF of grid cells (solid line) vs. speed cells (dashed line) between surfaces (floor, red; wall, turquoise) across speed. (H) There was a significant drop in the number of PPP grid cells on the wall compared with the floor, as shown in the chart representing percentages of rhythmic grid cells (n = 59) that reached PPP classification criteria on each surface (color code as in Fig. 1C).

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