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.
Subscribe to Journal
Get full journal access for 1 year
only $18.75 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Burgess, N. Spatial cognition and the brain. Ann. NY Acad. Sci. 1124, 77–97 (2008).
Moser, E.I., Kropff, E. & Moser, M.B. Place cells, grid cells, and the brain's spatial representation system. Annu. Rev. Neurosci. 31, 69–89 (2008).
Hafting, T., Fyhn, M., Molden, S., Moser, M.B. & Moser, E.I. Microstructure of a spatial map in the entorhinal cortex. Nature 436, 801–806 (2005).
Boccara, C.N. et al. Grid cells in pre- and parasubiculum. Nat. Neurosci. 13, 987–994 (2010).
Barry, C., Hayman, R., Burgess, N. & Jeffery, K.J. Experience-dependent rescaling of entorhinal grids. Nat. Neurosci. 10, 682–684 (2007).
O'Keefe, J. & Nadel, L. The Hippocampus as a Cognitive Map (Clarendon Press, 1978).
Jeffery, K. Navigating in a 3D world. in Animal Thinking: Contemporary Issues in Comparative Cognition (eds. Menzel, R. & Fischer, J.) (MIT Press, in the press).
Hartley, T., Burgess, N., Lever, C., Cacucci, F. & O'Keefe, J. Modeling place fields in terms of the cortical inputs to the hippocampus. Hippocampus 10, 369–379 (2000).
Skaggs, W.E., McNaughton, B.L., Gothard, K.M. & Markus, E.J. An information-theoretic approach to deciphering the hippocampal code. Adv. Neural Inf. Process. Syst. 5, 1031–1037 (1993).
Jeffery, K.J. Integration of the sensory inputs to place cells: what, where, why, and how? Hippocampus 17, 775–785 (2007).
Knierim, J.J. & McNaughton, B.L. Hippocampal place-cell firing during movement in three-dimensional space. J. Neurophysiol. 85, 105–116 (2001).
Knierim, J.J., McNaughton, B.L. & Poe, G.R. Three-dimensional spatial selectivity of hippocampal neurons during space flight. Nat. Neurosci. 3, 209–210 (2000).
Jeffery, K.J., Anand, R.L. & Anderson, M.I. A role for terrain slope in orienting hippocampal place fields. Exp. Brain Res. 169, 218–225 (2006).
Derdikman, D. et al. Fragmentation of grid cell maps in a multicompartment environment. Nat. Neurosci. 12, 1325–1332 (2009).
Nitz, D.A. Path shape impacts the extent of CA1 pattern recurrence both within and across environments. J. Neurophysiol. 105, 1815–1824 (2011).
Stackman, R.W., Tullman, M.L. & Taube, J.S. Maintenance of rat head direction cell firing during locomotion in the vertical plane. J. Neurophysiol. 83, 393–405 (2000).
McNaughton, B.L., Battaglia, F.P., Jensen, O., Moser, E.I. & Moser, M.B. Path integration and the neural basis of the 'cognitive map'. Nat. Rev. Neurosci. 7, 663–678 (2006).
O'Keefe, J. & Burgess, N. Dual phase and rate coding in hippocampal place cells: theoretical significance and relationship to entorhinal grid cells. Hippocampus 15, 853–866 (2005).
Fuhs, M.C. & Touretzky, D.S. A spin glass model of path integration in rat medial entorhinal cortex. J. Neurosci. 26, 4266–4276 (2006).
Tafforin, C. & Campan, R. Ethological experiments on human orientation behavior within a three-dimensional space—in microgravity. Adv. Space Res. 14, 415–418 (1994).
Leutgeb, J.K., Leutgeb, S., Moser, M.B. & Moser, E.I. Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science 315, 961–966 (2007).
Sargolini, F. et al. Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science 312, 758–762 (2006).
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.
K.J.J. is a non-shareholding co-director of Axona Ltd., which is owned by a family member.
About this article
Cite this article
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
Animal Cognition (2020)
Journal of Comparative Physiology A (2020)
Can we study 3D grid codes non-invasively in the human brain? Methodological considerations and fMRI findings
Trends in Cognitive Sciences (2019)
Journal of Neurophysiology (2019)