Spatial cell firing during virtual navigation of open arenas by head-restrained mice

Guifen Chen,John Andrew King,Yi Lu,Francesca Cacucci,Neil Burgess

doi:10.7554/elife.34789

Abstract

We present a mouse virtual reality (VR) system which restrains head-movements to horizontal rotations, compatible with multi-photon imaging. This system allows expression of the spatial navigation and neuronal firing patterns characteristic of real open arenas (R). Comparing VR to R: place and grid, but not head-direction, cell firing had broader spatial tuning; place, but not grid, cell firing was more directional; theta frequency increased less with running speed, whereas increases in firing rates with running speed and place and grid cells' theta phase precession were similar. These results suggest that the omni-directional place cell firing in R may require local-cues unavailable in VR, and that the scale of grid and place cell firing patterns, and theta frequency, reflect translational motion inferred from both virtual (visual and proprioceptive) and real (vestibular translation and extra-maze) cues. By contrast, firing rates and theta phase precession appear to reflect visual and proprioceptive cues alone.

Highlights

Virtual reality (VR) offers a powerful tool for investigating spatial cognition, allowing experimental control and environmental manipulations that are impossible in the real world
We show that the system allows expression of the characteristic 2-d firing patterns of place cells, head-direction cells and grid cells in electrophysiological recordings, making their underlying mechanisms accessible to investigation by manipulations of the virtual reality (VR)
We have demonstrated the ability of a novel mouse virtual reality (VR) system to allow expression of spatial learning and memory in open environments, following related work in rats (Aronov and Tank, 2014; Holscher et al, 2005; Cushman et al, 2013)

Summary

Introduction

Virtual reality (VR) offers a powerful tool for investigating spatial cognition, allowing experimental control and environmental manipulations that are impossible in the real world. The modulation of firing of place cells or grid cells along a single dimension, such as distance travelled along a specific trajectory or path, can be observed as virtual environments are explored by head-fixed mice (Chen et al, 2013; Dombeck et al, 2010; Harvey et al, 2009; Domnisoru et al, 2013; Schmidt-Hieber and Hausser, 2013; Heys et al, 2014; Low et al, 2014; Cohen et al, 2017) or body-fixed rats (Ravassard et al, 2013; Acharya et al, 2016; Aghajan et al, 2015). The two-dimensional firing patterns of place, grid and head-direction cells in real-world open arenas are not seen in these systems, in which the animal cannot physically rotate through 360 ̊

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