Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

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

Nature Neuroscience volume 14, pages 1182–1188 (2011)Cite this article

Subjects

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.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

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.

Similar content being viewed by others

References

  1. Burgess, N. Spatial cognition and the brain. Ann. NY Acad. Sci. 1124, 77–97 (2008).

    Article  Google Scholar 

  2. 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).

    Article  CAS  Google Scholar 

  3. 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).

    Article  CAS  Google Scholar 

  4. Boccara, C.N. et al. Grid cells in pre- and parasubiculum. Nat. Neurosci. 13, 987–994 (2010).

    Article  CAS  Google Scholar 

  5. Barry, C., Hayman, R., Burgess, N. & Jeffery, K.J. Experience-dependent rescaling of entorhinal grids. Nat. Neurosci. 10, 682–684 (2007).

    Article  CAS  Google Scholar 

  6. O'Keefe, J. & Nadel, L. The Hippocampus as a Cognitive Map (Clarendon Press, 1978).

  7. 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).

  8. 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).

    Article  CAS  Google Scholar 

  9. 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).

    Google Scholar 

  10. Jeffery, K.J. Integration of the sensory inputs to place cells: what, where, why, and how? Hippocampus 17, 775–785 (2007).

    Article  Google Scholar 

  11. Knierim, J.J. & McNaughton, B.L. Hippocampal place-cell firing during movement in three-dimensional space. J. Neurophysiol. 85, 105–116 (2001).

    Article  CAS  Google Scholar 

  12. 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).

    Article  CAS  Google Scholar 

  13. 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).

    Article  Google Scholar 

  14. Derdikman, D. et al. Fragmentation of grid cell maps in a multicompartment environment. Nat. Neurosci. 12, 1325–1332 (2009).

    Article  CAS  Google Scholar 

  15. Nitz, D.A. Path shape impacts the extent of CA1 pattern recurrence both within and across environments. J. Neurophysiol. 105, 1815–1824 (2011).

    Article  Google Scholar 

  16. 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).

    Article  CAS  Google Scholar 

  17. 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).

    Article  CAS  Google Scholar 

  18. 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).

    Article  Google Scholar 

  19. Fuhs, M.C. & Touretzky, D.S. A spin glass model of path integration in rat medial entorhinal cortex. J. Neurosci. 26, 4266–4276 (2006).

    Article  CAS  Google Scholar 

  20. Tafforin, C. & Campan, R. Ethological experiments on human orientation behavior within a three-dimensional space—in microgravity. Adv. Space Res. 14, 415–418 (1994).

    Article  CAS  Google Scholar 

  21. 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).

    Article  CAS  Google Scholar 

  22. Sargolini, F. et al. Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science 312, 758–762 (2006).

    Article  CAS  Google Scholar 

Download references

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

Author notes

  1. Robin Hayman, Madeleine A Verriotis and Aleksandar Jovalekic: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Cognitive, Division of Psychology and Language Sciences, Institute of Behavioural Neuroscience, Perceptual and Brain Sciences, University College London, London, UK

    Robin Hayman, Madeleine A Verriotis, Aleksandar Jovalekic & Kathryn J Jeffery

  2. Center for Neural Science, New York University, New York, New York, USA

    André A Fenton

  3. Department of Physiology and Pharmacology, State University of New York, Brooklyn, New York, USA

    André A Fenton

  4. Axona Ltd, Herts, UK

    Aleksandar Jovalekic

Authors
  1. Robin Hayman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Madeleine A Verriotis
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Aleksandar Jovalekic
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. André A Fenton
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kathryn J Jeffery
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

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.

Corresponding author

Correspondence to Kathryn J Jeffery.

Ethics declarations

Competing interests

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

Supplementary information

Supplementary Text and Figures

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

Rights and permissions

Reprints and permissions

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn.2892

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing