Abstract

We tested whether mice can represent locations distributed throughout three-dimensional space, by developing a novel three-dimensional radial arm maze. The three-dimensional radial maze, or “radiolarian” maze, consists of a central spherical core from which arms project in all directions. Mice learn to retrieve food from the ends of the arms without omitting any arms or re-visiting depleted ones. We show here that mice can learn both a standard working memory task, in which all arms are initially baited, and also a reference memory version in which only a subset are ever baited. Comparison with a two-dimensional analogue of the radiolarian maze, the hexagon maze, revealed equally good working-memory performance in both mazes if all the arms were initially baited, but reduced working and reference memory in the partially baited radiolarian maze. This suggests intact three-dimensional spatial representation in mice over short timescales but impairment of the formation and/or use of long-term spatial memory of the maze. We discuss potential mechanisms for how mice solve the three-dimensional task, and reasons for the impairment relative to its two-dimensional counterpart, concluding with some speculations about how mammals may represent three-dimensional space.

Highlights

  • The ability to accurately navigate through the world is vital for the survival of mobile animals, and requires the perception and encoding of spatial cues associated with important locations such as food nesting location

  • Few laboratory studies of three-dimensional spatial encoding have been conducted to date, and so the aim of the present experiment was to determine whether mice could perform a 3D version of a widely used laboratory-based navigation task, the radial maze task [3]

  • Motivated by previous behavioural and electrophysiological findings, together with those from decades of behavioural research in two-dimensional environments using the radial arm maze, we developed a three-dimensional radial arm maze, the radiolarian maze, to test whether mice can represent locations distributed within 3D space and whether these representations can be maintained over time

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Summary

Introduction

The ability to accurately navigate through the world is vital for the survival of mobile animals, and requires the perception and encoding of spatial cues associated with important locations such as food nesting location. This work has primarily focused on spatial navigation in horizontal planar environments: recently, interest has been growing in the means by which larger and more dimensionally complex spaces might be represented and used in navigation (see Jeffery et al [2] for review). Few laboratory studies of three-dimensional spatial encoding have been conducted to date, and so the aim of the present experiment was to determine whether mice could perform a 3D version of a widely used laboratory-based navigation task, the radial maze task [3]. In the 3D version of the maze, which because of its spherical symmetry we have named the radiolarian maze, food rewards are located at the end of arms that project from

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