Task-anchored grid cell firing is selectively associated with successful path integration-dependent behaviour

Abstract

Grid firing fields have been proposed as a neural substrate for spatial localisation in general or for path integration in particular. While there are theoretical arguments to support each possibility, it has been challenging to directly test whether and when grid cells contribute to behaviours. Here, we investigate firing of grid and non-grid cells in the medial entorhinal cortex during a location memory task. We find that grid firing can either be anchored to the task environment, or can encode distance travelled independently of the task reference frame. Anchoring varied between and within sessions, while spatial firing of non-grid cells was either coherent with the grid population, or was stably anchored to the task environment. We took advantage of the variability in task-anchoring to evaluate whether and when encoding of location by grid cells might contribute to behaviour. We find that when reward location is indicated by a visual cue performance is similar regardless of whether grid cells are task-anchored or not, arguing against a role for grid representations when location cues are available. By contrast, in the absence of the visual cue, performance was enhanced when grid cells were anchored to the task environment. Our results suggest that anchoring of grid cells to task reference frames selectively enhances performance when path integration is required.