Skip to main content
Log in

The place cell activity in three-dimensional space generated by multiple grid cell inputs

  • Original Paper
  • Published:
Nonlinear Dynamics Aims and scope Submit manuscript

Abstract

How the brain encodes spatial information is an important topic. Experimental and theoretical progresses achieved in this area mainly focused on the neuronal response in the lower-dimensional space such as a linear track or a horizontal flat arena. How the real three-dimensional (3-D) space is represented in the brain is unknown. Grid cells in the medial entorhinal cortex and the place cells in the hippocampus are the principal spatial neurons, and the grid cells provide important inputs to the place cells. In order to simulate the place cell activity in higher dimension, we proposed a rotating-integration model to generate the place field on non-horizontal surfaces for crawling animal in 3-D space. By referring to the gravity signal as an anchor, preferred directions of the grid cell will be rotated with the animal’s body plane during navigating on the surfaces. Then, multiple grid cell patterns with distributed orientations and wavelengths are integrated to form the firing field(s) of a place cell. The results can not only account for the known experimental recordings but also predict a segment planar encoding property of place cell on novel complex surfaces. It suggests that the spatial cognition for crawling animal is achieved by a mosaic of lower-dimensional codes rather than the full volumetric perception. This work can help us understand how the spatial information provided by the external physical world is represented and processed by the neuronal systems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data Availability

The current work has no associated data.

References

  1. Tolman, E.C.: Cognitive maps in rats and men. Psychol. Rev. 55(4), 189–208 (1948). https://doi.org/10.1037/h0061626

    Article  Google Scholar 

  2. O’Keefe, J., Dostrovsky, J.: The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 34(1), 171–5 (1971). https://doi.org/10.1016/0006-8993(71)90358-1

    Article  Google Scholar 

  3. Park, E., Dvorak, D., Fenton, A.: Ensemble place codes in hippocampus: CA1, CA3, and dentate gyrus place cells have multiple place fields in large environments. PLoS ONE 6(7), e22349 (2011). https://doi.org/10.1371/journal.pone.0022349

    Article  Google Scholar 

  4. Wilson, M.A., McNaughton, B.L.: Dynamics of the hippocampal ensemble code for space. Science 5124(261), 1055–8 (1993). https://doi.org/10.1126/science.8351520

    Article  Google Scholar 

  5. Yates, D.: Place cells as route planners. Nat. Rev. Neurosci. 14(6), 380–381 (2013). https://doi.org/10.1038/nrn3514

    Article  Google Scholar 

  6. Wang, Y., Wang, R., Zhu, Y.: Optimal path-finding through mental exploration based on neural energy field gradients. Cognit. Neurodyn. 11(1), 99–111 (2017). https://doi.org/10.1007/s11571-016-9412-2

    Article  Google Scholar 

  7. Zeng, T., Si, B.: A brain-inspired compact cognitive mapping system. Cognit. Neurodyn. 15, 91–101 (2021). https://doi.org/10.1007/s11571-020-09621-6

    Article  Google Scholar 

  8. Fyhn, M., Molden, S., Moser, E.I., Moser, M.B.: Spatial representation in the entorhinal cortex. Science 305(5688), 1258–1264 (2004)

    Article  Google Scholar 

  9. Hafting, T., Fyhn, M., Molden, S., Moser, M.B., Moser, E.I.: Microstructure of a spatial map in the entorhinal cortex. Nature 436(7052), 801–806 (2005)

    Article  Google Scholar 

  10. Sargolini, F., Fyhn, M., Hafting, T., et al.: Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science 312(5774), 758–62 (2006). https://doi.org/10.1126/science.1125572

    Article  Google Scholar 

  11. Solstad, T., Moser, E.I., Einevoll, G.T.: From grid cells to place cells: a mathematical model. Hippocampus 16, 1026–31 (2006). https://doi.org/10.1002/hipo.20244

    Article  Google Scholar 

  12. Barry, C., Hayman, R., Burgess, N., Jeffery, K.: Experience-dependent rescaling of entorhinal grids. Nat. Neurosci. 10(6), 682–684 (2007)

    Article  Google Scholar 

  13. Hayman, R., Verriotis, M.A., Jovalekic, A., Fenton, A.A., Jeffery, K.J.: Anisotropic encoding of three-dimensional space by place cells and grid cells. Nat. Neurosci. 14(9), 1182–8 (2011). https://doi.org/10.1038/nn.2892

    Article  Google Scholar 

  14. Rowland, D.C., Moser, M.B.: A three-dimensional neural compass. Nature 517(7533), 156–7 (2015). https://doi.org/10.1038/nature14076

    Article  Google Scholar 

  15. Yartsev, M.M., Ulanovsky, N.: Representation of three-dimensional space in the hippocampus of flying bats. Science 340(6130), 367–372 (2013). https://doi.org/10.1126/science.1235338

    Article  Google Scholar 

  16. Wang, Y., Xu, X., Wang, R.: The place cell activity is information-efficient constrained by energy. Neural Netw. 116, 110–118 (2019). https://doi.org/10.1016/j.neunet.2019.04.001

    Article  Google Scholar 

  17. Wang, Y., Wang, R., Xu, X.: Neural energy supply-consumption properties based on Hodgkin-Huxley model. Neural Plast. 2017, 1–11 (2017)

    Google Scholar 

  18. Wang, Y., Xu, X., Zhu, Y., Wang, R.: Neural energy mechanism and neurodynamics of memory transformation. Nonlinear Dyn. 97(1), 697–714 (2019)

    Article  Google Scholar 

  19. Chen, X., Yang, T.: A neural network model of basal ganglia’s decision-making circuitry. Cognit. Neurodyn. 15, 17–26 (2021). https://doi.org/10.1007/s11571-020-09609-2

    Article  Google Scholar 

  20. Tozzi, A., Ahmad, M.Z., Peters, J.F.: Neural computing in four spatial dimensions. Cognit. Neurodyn. 15, 349–357 (2021). https://doi.org/10.1007/s11571-020-09598-2

    Article  Google Scholar 

  21. Riley, S.N., Davies, J.: A spiking neural network model of spatial and visual mental imagery. Cognit. Neurodyn. 14(2), 239–251 (2020). https://doi.org/10.1007/s11571-019-09566-5

  22. Šterk, M., Dolenšek, J., Bombek, L.K., Markovič, R., et al.: Assessing the origin and velocity of Ca2+ waves in three-dimensional tissue: insights from a mathematical model and confocal imaging in mouse pancreas tissue slices. Commun. Nonlinear Sci. Numer. Simul. 93, 105495 (2021). https://doi.org/10.1016/j.cnsns.2020.105495

    Article  MATH  Google Scholar 

  23. Gosak, M., Markovič, R., Dolenšek, J., et al.: Network science of biological systems at different scales: a review. Phys. Life Rev. 24, 118–135 (2018). https://doi.org/10.1016/j.plrev.2017.11.003

  24. Cash, S., Yuste, R.: Linear summation of excitatory inputs by CA1 pyramidal neurons. Neuron 22(2), 383–394 (1999). https://doi.org/10.1016/S0896-6273(00)81098-3

    Article  Google Scholar 

  25. Gasparini, S., Jeffrey, C.M.: State-dependent dendritic computation in hippocampal CA1 pyramidal neurons. J. Neurosci. 26(7), 2088–2100 (2006). https://doi.org/10.1523/JNEUROSCI.4428-05.2006

    Article  Google Scholar 

  26. Laurens, J., Kim, B., Dickman, J.D., Angelaki, D.E.: Gravity orientation tuning in macaque anterior thalamus. Nat. Neurosci. 19(12), 1566–1568 (2016). https://doi.org/10.1038/nn.4423

    Article  Google Scholar 

  27. Wang, Y., Xu, X., Pan, X., Wang, R.: Grid cell activity and path integration on 2-D manifolds in 3-D space. Nonlinear Dyn. 104, 1767–1780 (2021). https://doi.org/10.1007/s11071-021-06337-y

    Article  Google Scholar 

  28. Burgess, N., O’Keefe, J.: Models of place and grid cell firing and theta rhythmicity. Current Opinion Neurobiol. 21(5), 734–44 (2011). https://doi.org/10.1016/j.conb.2011.07.002

    Article  Google Scholar 

  29. Casali, G., Bush, D., Jeffery, K.: Altered neural odometry in the vertical dimension. Proceedings of the National Academy of Sciences of the United States of America 116(10), 4631–4636 (2019). https://doi.org/10.1073/pnas.1811867116

  30. Goldstein, H., Poole, C., Safko, J.: Classical Mechanics, 2nd edn. Addison-Wesley, USA (1980)

    MATH  Google Scholar 

  31. Hayman, R., Casali, G., Wilson, J.J., Jeffery, K.: Grid cells on steeply sloping terrain: evidence for planar rather than volumetric encoding. Front. Psychol. 6, 925 (2015). https://doi.org/10.3389/fpsyg.2015.00925

  32. Yartsev, M.M., Witter, M.P., Ulanovsky, N.: Grid cells without theta oscillations in the entorhinal cortex of bats. Nature 479(7371), 103–7 (2011). https://doi.org/10.1038/nature10583

    Article  Google Scholar 

  33. Porter, B.S., Schmidt, R., Bilkey, D.K.: Hippocampal place cell encoding of sloping terrain. Hippocampus 28(11), 767–782 (2018). https://doi.org/10.1002/hipo.22966

    Article  Google Scholar 

  34. Wang, Y., Xu, X., Wang, R.: An energy model of place cell network in three dimensional space. Front. Neurosci. 12, 264 (2018). https://doi.org/10.3389/fnins.2018.00264

    Article  Google Scholar 

  35. Laurens, J., Meng, H., Angelaki, D.E.: Neural representation of orientation relative to gravity in the macaque cerebellum. Neuron 80(6), 1508–1518 (2013). https://doi.org/10.1016/j.neuron.2013.09.029

    Article  Google Scholar 

  36. Ravishankar Rao, A.: An oscillatory neural network model that demonstrates the benefits of multisensory learning. Cognit. Neurodyn. 12, 481–99 (2018). https://doi.org/10.1007/s11571-018-9489-x

    Article  Google Scholar 

  37. Wang, Y., Xu, X., Wang, R.: Energy features in spontaneous up and down oscillations. Cognit. Neurodyn. 15, 65–75 (2021). https://doi.org/10.1007/s11571-020-09597-3

    Article  Google Scholar 

  38. Wang, Y., Xu, X., Wang, R.: Modeling the grid cell activity on non-horizontal surfaces based on oscillatory interference modulated by gravity. Neural Netw. 141, 199–210 (2021)

    Article  Google Scholar 

Download references

Acknowledgements

We thank the editor and anonymous reviewers for their valuable feedback and insightful advice. We thank the National Natural Science Foundation of China and Natural Science Foundation of Shanghai for supporting this research.

Funding

This work is supported by the National Natural Science Foundation of China (Nos.12172132, 11802095, 11702096, 12072113) and the Natural Science Foundation of Shanghai (No.19zr1473100).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yihong Wang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Code availability

The code generated for the current study is available from the corresponding author on reasonable request.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file 1 (pdf 157 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xu, X., Wang, Y. & Wang, R. The place cell activity in three-dimensional space generated by multiple grid cell inputs. Nonlinear Dyn 108, 1719–1731 (2022). https://doi.org/10.1007/s11071-022-07247-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11071-022-07247-3

Navigation