Anisotropic encoding of three-dimensional space by place cells and grid cells

Abstract

The subjective sense of space may result in part from the combined activity of place cells in the hippocampus and grid cells in posterior cortical regions such as the entorhinal cortex and pre- and parasubiculum. In horizontal planar environments, place cells provide focal positional information, whereas grid cells supply odometric (distance measuring) information. How these cells operate in three dimensions is unknown, even though the real world is three-dimensional. We investigated this issue in rats exploring two different kinds of apparatus: a climbing wall (the 'pegboard') and a helix. Place and grid cell firing fields had normal horizontal characteristics but were elongated vertically, with grid fields forming stripes. It seems that grid cell odometry (and by implication path integration) is impaired or absent in the vertical domain, at least when the rat itself remains horizontal. These findings suggest that the mammalian encoding of three-dimensional space is anisotropic.

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Figure 1: Place fields on the pegboard.
Figure 2: Grid fields on the pegboard.
Figure 3: Place fields on the helix.
Figure 4: Grid fields on the helix.
Figure 5: Hypotheses concerning the firing patterns observed in the present experiment.

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Acknowledgements

The work was supported by grants from the Wellcome Trust to K.J.J., the European Commission Framework 7 ('Spacebrain') to K.J.J. and Axona Ltd, and a National Science Foundation grant (no. IOS-0725001) to A.A.F. We thank E. Kelemen for help designing and M. Shkop for constructing the helical track, E. Leeper for building the pegboard arena, M. Witter for advice on histology and C. Barry and F. Cacucci for comments on the manuscript.

Author information

R.H., M.A.V. and A.J. contributed equally to the work. R.H. and M.A.V. implanted electrodes, recorded and analyzed the bulk of the data and wrote most of the Online Methods. A.J. recorded the bulk of the pegboard data and contributed analysis and the Online Methods. A.A.F. conceived the helical track, oversaw its construction and advised on data analysis and interpretation. K.J.J. conceived and gained funding for the overall research program, designed the pegboard and oversaw its construction, supervised the data collection and analysis and wrote the Introduction and Discussion.

Correspondence to Kathryn J Jeffery.

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Competing interests

K.J.J. is a non-shareholding co-director of Axona Ltd., which is owned by a family member.

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Supplementary Figures 1–13 and Supplementary Results (PDF 4791 kb)

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Hayman, R., Verriotis, M., Jovalekic, A. et al. Anisotropic encoding of three-dimensional space by place cells and grid cells. Nat Neurosci 14, 1182–1188 (2011). https://doi.org/10.1038/nn.2892

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