Abstract

Grid cells in entorhinal and parahippocampal cortices contribute to a network, centered on the hippocampal place cell system, that constructs a representation of spatial context for use in navigation and memory. In doing so, they use metric cues such as the distance and direction of nearby boundaries to position and orient their firing field arrays (grids). The present study investigated whether they also use purely nonmetric “context” information such as color and odor of the environment. We found that, indeed, purely nonmetric cues—sufficiently salient to cause changes in place cell firing patterns—can regulate grid positioning; they do so independently of orientation, and thus interact with linear but not directional spatial inputs. Grid cells responded homogeneously to context changes. We suggest that the grid and place cell networks receive context information directly and also from each other; the information is used by place cells to compute the final decision of the spatial system about which context the animal is in, and by grid cells to help inform the system about where the animal is within it.

Highlights

  • The entorhinal–hippocampal network forms the core of a spatial memory system that supports cognitive processes such as navigation and episodic memory

  • We suggest that the grid and place cell networks receive context information directly and from each other; the information is used by place cells to compute the final decision of the spatial system about which context the animal is in, and by grid cells to help inform the system about where the animal is within it

  • This study aimed to determine whether grid cells, an important part of the brain network that computes spatial location, respond only to metric spatial information or could respond to purely nonmetric “contextual” cues manipulated via changes in the color and/or odor of the environment

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Summary

Introduction

The entorhinal–hippocampal network forms the core of a spatial memory system that supports cognitive processes such as navigation and episodic memory. While hippocampal place cells exhibit focal, sparse, and irregular activity patches (firing fields) on an open-field arena, entorhinal grid cells show spatially regular firing field arrays (Hafting et al 2005). A previous study of grid cells found that, while metric environmental change induced translation and sometimes rotation of grids, nonmetric change (to box color) caused no shift of grids (Fyhn et al 2007), suggesting insensitivity to nonmetric inputs Those contextual changes did not induce “global remapping” (Leutgeb and Leutgeb 2007) of hippocampal place cells, and so may not have been salient enough to trigger responding by the grid cell system.

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