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.
Frontiers in psychology
Robin M A Hayman, Giulio Casali, Jonathan J Wilson, Kate J Jeffery
Affiliations
Affiliations
- Department of Clinical and Experimental Epilepsy, Institute of Neurology, Faculty of Brain Sciences, University College London London, UK.
- Institute of Behavioural Neuroscience, Research Department of Experimental Psychology, Division of Psychology and Language Sciences, University College London London, UK.
PMID: 26236245
PMCID: PMC4502341 DOI: 10.3389/fpsyg.2015.00925
Abstract
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.
Keywords: dimensions; grid cells; navigation; place cells; spatial cognition; theoretical model
References
- Neuroscience. 2012 Jun 28;213:54-61 - PubMed
- Nat Neurosci. 2007 Jun;10(6):682-4 - PubMed
- Hippocampus. 2015 Dec;25(12 ):1489-500 - PubMed
- Front Psychol. 2015 Jul 14;6:927 - PubMed
- Hippocampus. 2008;18(12):1175-85 - PubMed
- J Comp Physiol Psychol. 1975 Jan;88(1):324-8 - PubMed
- Nature. 2015 Feb 12;518(7538):207-12 - PubMed
- Neural Comput. 2014 Nov;26(11):2379-94 - PubMed
- Nature. 2005 Aug 11;436(7052):801-6 - PubMed
- Behav Brain Sci. 2013 Oct;36(5):523-43 - PubMed
- Science. 2006 May 5;312(5774):758-62 - PubMed
- Annu Rev Neurosci. 2008;31:69-89 - PubMed
- Cereb Cortex. 2015 Nov;25(11):4619-27 - PubMed
- Elife. 2015 Apr 24;4:null - PubMed
Publication Types
Grant support