Grid cells are modulated by local head direction

Klara Gerlei,Brianna Vandrey,Matthew F Nolan,Jessica Passlack,Holly Stevens,Ioannis Papastathopoulos,Ian Hawes

doi:10.1038/s41467-020-17500-1

Klara Gerlei, Brianna Vandrey + Show 5 more

Open Access

https://doi.org/10.1038/s41467-020-17500-1

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Abstract

Grid and head direction codes represent cognitive spaces for navigation and memory. Pure grid cells generate grid codes that have been assumed to be independent of head direction, whereas conjunctive cells generate grid representations that are tuned to a single head direction. Here, we demonstrate that pure grid cells also encode head direction, but through distinct mechanisms. We show that individual firing fields of pure grid cells are tuned to multiple head directions, with the preferred sets of directions differing between fields. This local directional modulation is not predicted by previous continuous attractor or oscillatory interference models of grid firing but is accounted for by models in which pure grid cells integrate inputs from co-aligned conjunctive cells with firing rates that differ between their fields. We suggest that local directional signals from grid cells may contribute to downstream computations by decorrelating different points of view from the same location.

Highlights

Grid and head direction codes represent cognitive spaces for navigation and memory
Pure grid cells and conjunctive cells found in medial entorhinal cortex (MEC) both generate grid codes
We identified 13% of the recorded neurons (39/ 300) as having grid-like spatial firing fields using a metric based on the rotational symmetry of the autocorrelogram of their firing rate map[5]

Summary

Introduction

Grid and head direction codes represent cognitive spaces for navigation and memory. Pure grid cells generate grid codes that have been assumed to be independent of head direction, whereas conjunctive cells generate grid representations that are tuned to a single head direction. The activity of pure grid cells is thought to depend only on the position of the animal and to lack selectivity for head direction or other navigational variables[7,8] We refer to this as omnidirectional firing (Fig. 1a). Conjunctive cells have grid firing fields that manifest only when an animal moves in a particular direction[8] We refer to this as unidirectional firing (Fig. 1a). This distinction is maintained in established models for grid firing, which predict either omnidirectional firing, as suggested for pure grid cells, or selectivity for a single direction, as described for conjunctive cells[9,10,11,12,13,14,15]. The possibility that pure grid cell activity is modulated in this way by head direction has received little attention

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