Altered neural odometry in the vertical dimension

Giulio Casali,Daniel Bush,Kate Jeffery

doi:10.1073/pnas.1811867116

Giulio Casali, Daniel Bush + Show 1 more

Open Access

https://doi.org/10.1073/pnas.1811867116

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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).

Highlights

Entorhinal grid cells integrate sensory and self-motion inputs to provide a spatial metric of a characteristic scale
We recorded 148 unique grid cells from the medial entorhinal cortex of 11 rats and 72 place cells from the HPC of three rats (SI Appendix, Fig. S1), all familiar with 3D environments, as they foraged in the open field, or over a floor and adjoining wall (Fig. 1A)
These parameters are reflected in the activity of place cells, which, in small spaces, produce mostly single foci of firing [2] called “firing fields”, and grid cells, which produce a grid-like array of firing fields spread across the environment [3,4,5]

Summary

Introduction

Entorhinal grid cells integrate sensory and self-motion inputs to provide a spatial metric of a characteristic scale. 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). On a steep (40 deg.) slope, grid cells were shown to exhibit similar firing patterns to those observed on a horizontal surface [10] Together, these studies suggest that perhaps grid cells perform odometry in the plane of locomotion (the surface the feet are on) regardless of its orientation in 3D space, and not in the direction orthogonal to that plane. Because of the importance of self-motion signals to grid cell odometry, we recorded “speed cells” [11] and local field potentials (LFPs), both of which have been implicated in speed encoding [12] and grid cell odometry [13, 14]

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