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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.

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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.

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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.

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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.

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Correspondence to Edvard I Moser.

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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

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