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:

Fragmentation of grid cell maps in a multicompartment environment

Abstract

To determine whether entorhinal spatial representations are continuous or fragmented, we recorded neural activity in grid cells while rats ran through a stack of interconnected, zig-zagged compartments of equal shape and orientation (a hairpin maze). The distribution of spatial firing fields was markedly similar across all compartments in which running occurred in the same direction, implying that the grid representation was fragmented into repeating submaps. Activity at neighboring positions was least correlated at the transitions between different arms, indicating that the map split regularly at the turning points. We saw similar discontinuities among place cells in the hippocampus. No fragmentation was observed when the rats followed similar trajectories in the absence of internal walls, implying that stereotypic behavior alone cannot explain the compartmentalization. These results indicate that spatial environments are represented in entorhinal cortex and hippocampus as a mosaic of discrete submaps that correspond to the geometric structure of the space.

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

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

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

Figure 1: Grid fields repeat across arms with similar running directions.
Figure 2: Population analysis for a single-cell ensemble.
Figure 3: Population analysis for all trials and all rats.
Figure 4: Representations were reset near the turning points.
Figure 5: Shortcut experiments suggest a path-integration mechanism.
Figure 6: Firing pattern of hippocampal place cells in the hairpin maze.
Figure 7: Preserved two-dimensional grid representations in a virtual hairpin maze.

Similar content being viewed by others

References

  1. O'Keefe, J. & Dostrovsky, J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 34, 171–175 (1971).

    Article  CAS  Google Scholar 

  2. O'Keefe, J. & Nadel, L. The Hippocampus as a Cognitive Map (Oxford University Press, New York, 1978).

    Google Scholar 

  3. Muller, R.U., Kubie, J.L. & Ranck, J.B. Jr. Spatial firing patterns of hippocampal complex-spike cells in a fixed environment. J. Neurosci. 7, 1935–1950 (1987).

    Article  CAS  Google Scholar 

  4. Wilson, M.A. & McNaughton, B.L. Dynamics of the hippocampal ensemble code for space. Science 261, 1055–1058 (1993).

    Article  CAS  Google Scholar 

  5. Kjelstrup, K.B. et al. Finite scale of spatial representation in the hippocampus. Science 321, 140–143 (2008).

    Article  CAS  Google Scholar 

  6. Leutgeb, S., Leutgeb, J.K., Treves, A., Moser, M.B. & Moser, E.I. Distinct ensemble codes in hippocampal areas CA3 and CA1. Science 305, 1295–1298 (2004).

    Article  CAS  Google Scholar 

  7. Bostock, E., Muller, R.U. & Kubie, J.L. Experience-dependent modifications of hippocampal place cell firing. Hippocampus 1, 193–205 (1991).

    Article  CAS  Google Scholar 

  8. Colgin, L.L., Moser, E.I. & Moser, M.B. Understanding memory through hippocampal remapping. Trends Neurosci. 31, 469–477 (2008).

    Article  CAS  Google Scholar 

  9. Muller, R.U. & Kubie, J.L. The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells. J. Neurosci. 7, 1951–1968 (1987).

    Article  CAS  Google Scholar 

  10. Wood, E.R., Dudchenko, P.A. & Eichenbaum, H. The global record of memory in hippocampal neuronal activity. Nature 397, 613–616 (1999).

    Article  CAS  Google Scholar 

  11. Pastalkova, E., Itskov, V., Amarasingham, A. & Buzsaki, G. Internally generated cell assembly sequences in the rat hippocampus. Science 321, 1322–1327 (2008).

    Article  CAS  Google Scholar 

  12. Hampson, R.E., Heyser, C.J. & Deadwyler, S.A. Hippocampal cell firing correlates of delayed-match-to-sample performance in the rat. Behav. Neurosci. 107, 715–739 (1993).

    Article  CAS  Google Scholar 

  13. Wood, E.R., Dudchenko, P.A., Robitsek, R.J. & Eichenbaum, H. Hippocampal neurons encode information about different types of memory episodes occurring in the same location. Neuron 27, 623–633 (2000).

    Article  CAS  Google Scholar 

  14. Frank, L.M., Brown, E.N. & Wilson, M. Trajectory encoding in the hippocampus and entorhinal cortex. Neuron 27, 169–178 (2000).

    Article  CAS  Google Scholar 

  15. Markus, E.J. et al. Interactions between location and task affect the spatial and directional firing of hippocampal neurons. J. Neurosci. 15, 7079–7094 (1995).

    Article  CAS  Google Scholar 

  16. Young, B.J., Fox, G.D. & Eichenbaum, H. Correlates of hippocampal complex-spike cell activity in rats performing a nonspatial radial maze task. J. Neurosci. 14, 6553–6563 (1994).

    Article  CAS  Google Scholar 

  17. Touretzky, D.S. & Redish, A.D. Theory of rodent navigation based on interacting representations of space. Hippocampus 6, 247–270 (1996).

    Article  CAS  Google Scholar 

  18. Eichenbaum, H., Dudchenko, P., Wood, E., Shapiro, M. & Tanila, H. The hippocampus, memory and place cells: is it spatial memory or a memory space? Neuron 23, 209–226 (1999).

    Article  CAS  Google Scholar 

  19. Sharp, P.E. Subicular cells generate similar spatial firing patterns in two geometrically and visually distinctive environments: Comparison with hippocampal place cells. Behav. Brain Res. 85, 71–92 (1997).

    Article  CAS  Google Scholar 

  20. Taube, J.S. The head direction signal: origins and sensory-motor integration. Annu. Rev. Neurosci. 30, 181–207 (2007).

    Article  CAS  Google Scholar 

  21. Taube, J.S., Muller, R.U. & Ranck, J.B. Jr. Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J. Neurosci. 10, 420–435 (1990).

    Article  CAS  Google Scholar 

  22. Ranck, J.B. Head direction cells in the deep cell layer of dorsal presubiculum in freely moving rats. in Electrical Activity of the Archicortex (eds G. Buzsaki & C.H. Vanderwolf) 217–220 (Akademiai Kiado, Budapest, 1985).

    Google Scholar 

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

    Article  CAS  Google Scholar 

  24. Fyhn, M., Molden, S., Witter, M.P., Moser, E.I. & Moser, M.B. Spatial representation in the entorhinal cortex. Science 305, 1258–1264 (2004).

    Article  CAS  Google Scholar 

  25. 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 

  26. Taube, J.S., Muller, R.U. & Ranck, J.B. Head-direction cells recorded from the postsubiculum in freely moving rats. 2. Effects of environmental manipulations. J. Neurosci. 10, 436–447 (1990).

    Article  CAS  Google Scholar 

  27. Johnson, A., Seeland, K. & Redish, A.D. Reconstruction of the postsubiculum head direction signal from neural ensembles. Hippocampus 15, 86–96 (2005).

    Article  Google Scholar 

  28. Hargreaves, E.L., Yoganarasimha, D. & Knierim, J.J. Cohesiveness of spatial and directional representations recorded from neural ensembles in the anterior thalamus, parasubiculum, medial entorhinal cortex and hippocampus. Hippocampus 17, 826–841 (2007).

    Article  Google Scholar 

  29. Yoganarasimha, D., Yu, X. & Knierim, J.J. Head direction cell representations maintain internal coherence during conflicting proximal and distal cue rotations: comparison with hippocampal place cells. J. Neurosci. 26, 622–631 (2006).

    Article  CAS  Google Scholar 

  30. Fyhn, M., Hafting, T., Treves, A., Moser, M.B. & Moser, E.I. Hippocampal remapping and grid realignment in entorhinal cortex. Nature 446, 190–194 (2007).

    Article  CAS  Google Scholar 

  31. Moser, E.I. & Moser, M.B. A metric for space. Hippocampus 18, 1142–1156 (2008).

    Article  Google Scholar 

  32. Redish, A.D., McNaughton, B.L. & Barnes, C.A. Place cell firing shows an inertia-like process. Neurocomputing 32, 235–241 (2000).

    Article  Google Scholar 

  33. 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 

  34. McNaughton, B.L., Barnes, C.A. & O'Keefe, J. The contributions of position, direction, and velocity to single unit activity in the hippocampus of freely moving rats. Exp. Brain Res. 52, 41–49 (1983).

    Article  CAS  Google Scholar 

  35. Hafting, T., Fyhn, M., Bonnevie, T., Moser, M.B. & Moser, E.I. Hippocampus-independent phase precession in entorhinal grid cells. Nature 453, 1248–1252 (2008).

    Article  CAS  Google Scholar 

  36. Hasselmo, M.E. Grid cell mechanisms and function: contributions of entorhinal persistent spiking and phase resetting. Hippocampus 18, 1213–1229 (2008).

    Article  Google Scholar 

  37. O'Keefe, J. & Burgess, N. Geometric determinants of the place fields of hippocampal neurons. Nature 381, 425–428 (1996).

    Article  CAS  Google Scholar 

  38. 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 

  39. Cheng, K. A purely geometric module in the rat's spatial representation. Cognition 23, 149–178 (1986).

    Article  CAS  Google Scholar 

  40. McGregor, A., Hayward, A.J., Pearce, J.M. & Good, M.A. Hippocampal lesions disrupt navigation based on the shape of the environment. Behav. Neurosci. 118, 1011–1021 (2004).

    Article  CAS  Google Scholar 

  41. Jones, P.M., Pearce, J.M., Davies, V.J., Good, M.A. & McGregor, A. Impaired processing of local geometric features during navigation in a water maze following hippocampal lesions in rats. Behav. Neurosci. 121, 1258–1271 (2007).

    Article  Google Scholar 

  42. Pearce, J.M., Good, M.A., Jones, P.M. & McGregor, A. Transfer of spatial behavior between different environments: implications for theories of spatial learning and for the role of the hippocampus in spatial learning. J. Exp. Psychol. Anim. Behav. Process. 30, 135–147 (2004).

    Article  Google Scholar 

  43. Gothard, K.M., Skaggs, W.E. & McNaughton, B.L. Dynamics of mismatch correction in the hippocampal ensemble code for space: interaction between path integration and environmental cues. J. Neurosci. 16, 8027–8040 (1996).

    Article  CAS  Google Scholar 

  44. Redish, A.D., Rosenzweig, E.S., Bohanick, J.D., McNaughton, B.L. & Barnes, C.A. Dynamics of hippocampal ensemble activity realignment: time versus space. J. Neurosci. 20, 9298–9309 (2000).

    Article  CAS  Google Scholar 

  45. Biegler, R. Possible uses of path integration in animal navigation. Anim. Learn. Behav. 28, 257–277 (2000).

    Article  Google Scholar 

  46. Samsonovich, A. & McNaughton, B.L. Path integration and cognitive mapping in a continuous attractor neural network model. J. Neurosci. 17, 5900–5920 (1997).

    Article  CAS  Google Scholar 

  47. McNaughton, B.L. et al. Deciphering the hippocampal polyglot: the hippocampus as a path integration system. J. Exp. Biol. 199, 173–185 (1996).

    CAS  Google Scholar 

  48. Whishaw, I.Q. Place learning in hippocampal rats and the path integration hypothesis. Neurosci. Biobehav. Rev. 22, 209–220 (1998).

    Article  CAS  Google Scholar 

  49. Solstad, T., Boccara, C., Kropff, E., Moser, M.B. & Moser, E.I. Representation of geometric borders in the entorhinal cortex. Science 322, 1865–1868 (2008).

    Article  CAS  Google Scholar 

  50. Savelli, F., Yoganarasimha, D. & Knierim, J.J. Influence of boundary removal on the spatial representations of the medial entorhinal cortex. Hippocampus 18, 1270–1282 (2008).

    Article  Google Scholar 

Download references

Acknowledgements

We thank A.M. Amundgård, I. Hammer, K. Haugen, K. Jenssen, R. Skjerpeng and H. Waade for technical assistance and T. Bonnevie and G. Pfühl for help with animal training. We thank A.D. Redish and members of the Kavli Institute for Systems Neuroscience and the Centre for the Biology of Memory for useful discussions. This work was supported by the Kavli Foundation and a Centre of Excellence grant from the Norwegian Research Council.

Author information

Authors and Affiliations

Authors

Contributions

D.D., M.-B.M. and E.I.M. designed the study, M.F., J.R.W. and D.D. performed surgeries, D.D., J.R.W. and A.T. performed the experiments, M.F. and T.H. helped with training, D.D. analyzed the data, and D.D. and E.I.M. wrote the paper. All authors participated in planning and discussion.

Corresponding author

Correspondence to Edvard I Moser.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–7 (PDF 3168 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Derdikman, D., Whitlock, J., Tsao, A. et al. Fragmentation of grid cell maps in a multicompartment environment. Nat Neurosci 12, 1325–1332 (2009). https://doi.org/10.1038/nn.2396

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn.2396

This article is cited by

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