Grid cells on steeply sloping terrain: evidence for planar rather than volumetric encoding

Robin M. A. Hayman, Giulio Casali, Jonathan J. Wilson, Kate J. Jeffery
Frontiers in Psychology. 2015-07-15; 6:
DOI: 10.3389/fpsyg.2015.00925

1. Front Psychol. 2015 Jul 15;6:925. doi: 10.3389/fpsyg.2015.00925. eCollection
2015.

Grid cells on steeply sloping terrain: evidence for planar rather than
volumetric encoding.

Hayman RM(1), Casali G(2), Wilson JJ(2), Jeffery KJ(2).

Author information:
(1)Department of Clinical and Experimental Epilepsy, Institute of Neurology,
Faculty of Brain Sciences, University College London London, UK.
(2)Institute of Behavioural Neuroscience, Research Department of Experimental
Psychology, Division of Psychology and Language Sciences, University College
London London, UK.

Neural encoding of navigable space involves a network of structures centered on
the hippocampus, whose neurons -place cells – encode current location. Input to
the place cells includes afferents from the entorhinal cortex, which contains
grid cells. These are neurons expressing spatially localized activity patches,
or firing fields, that are evenly spaced across the floor in a hexagonal
close-packed array called a grid. It is thought that grids function to enable
the calculation of distances. The question arises as to whether this odometry
process operates in three dimensions, and so we queried whether grids permeate
three-dimensional (3D) space – that is, form a lattice – or whether they simply
follow the environment surface. If grids form a 3D lattice then this lattice
would ordinarily be aligned horizontally (to explain the usual hexagonal pattern
observed). A tilted floor would transect several layers of this putative
lattice, resulting in interruption of the hexagonal pattern. We model this
prediction with simulated grid lattices, and show that the firing of a grid cell
on a 40°-tilted surface should cover proportionally less of the surface, with
smaller field size, fewer fields, and reduced hexagonal symmetry. However,
recording of real grid cells as animals foraged on a 40°-tilted surface found
that firing of grid cells was almost indistinguishable, in pattern or rate, from
that on the horizontal surface, with if anything increased coverage and field
number, and preserved field size. It thus appears unlikely that the sloping
surface transected a lattice. However, grid cells on the slope displayed
slightly degraded firing patterns, with reduced coherence and slightly reduced
symmetry. These findings collectively suggest that the grid cell component of
the metric representation of space is not fixed in absolute 3D space but is
influenced both by the surface the animal is on and by the relationship of this
surface to the horizontal, supporting the hypothesis that the neural map of
space is « multi-planar » rather than fully volumetric.