A fundamental property of many associative memory networks is the ability to decorrelate overlapping input patterns before information is stored1,2,3,4,5. In the hippocampus, this neuronal pattern separation is expressed as the tendency of ensembles of place cells6 to undergo extensive ‘remapping’ in response to changes in the sensory or motivational inputs to the hippocampus7,8,9,10,11,12,13. Remapping is expressed under some conditions as a change of firing rates in the presence of a stable place code (‘rate remapping’)14, and under other conditions as a complete reorganization of the hippocampal place code in which both place and rate of firing take statistically independent values (‘global remapping’)14. Here we show that the nature of hippocampal remapping can be predicted by ensemble dynamics in place-selective grid cells in the medial entorhinal cortex15,16, one synapse upstream of the hippocampus. Whereas rate remapping is associated with stable grid fields, global remapping is always accompanied by a coordinate shift in the firing vertices of the grid cells. Grid fields of co-localized medial entorhinal cortex cells move and rotate in concert during this realignment. In contrast to the multiple environment-specific representations coded by place cells in the hippocampus, local ensembles of grid cells thus maintain a constant spatial phase structure, allowing position to be represented and updated by the same translation mechanism in all environments encountered by the animal.
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We thank S. Leutgeb, T. Solstad, B. L. McNaughton and M. P. Witter for discussion, R. Skjerpeng for programming, and I. Hammer, K. Haugen, K. Jenssen and H. Waade for technical assistance. This work was supported by a Centre of Excellence grant from the Norwegian Research Council.
Author Contributions M.F., T.H., M.-B.M. and E.I.M. planned experiments and analyses. M.F., T.H. and M.-B.M. performed the experiments and analysed the data. A.T. gave advice on analyses, and E.I.M. wrote the paper. All authors discussed the results and contributed to the manuscript.
Reprints and permissions information is available at www.nature.com/reprints. The authors declare no competing financial interests.
This file contains Supplementary Figures 1-12 with Legends, Supplementary Methods, Supplementary Tables 1-3, Supplementary Discussion and Supplementary Notes with additional references. Supplementary Figures 1-3 show representative recording locations in MEC and CA3, examples of global remapping and rate remapping in CA3 (rate maps for the complete cell sample in one animal and for all cells that were active in both environments in all animals), and crosscorrelation matrices for the entire set of grid-cell ensembles. Supplementary Figures 4-12 show additional crosscorrelations for individual cells and cell ensembles, simultaneous recordings from MEC and CA3, experiments addressing contiguity of grid realignment in MEC and global remapping in CA3, analyses of ensemble coactivity and rate distribution across grid vertices, and two models for global remapping in hippocampus during grid realignment in MEC. Supplementary Tables 1-3 show numbers of cells and experiments for individual rats, averaged firing properties of MEC and CA3 cells, and behavioural data. (PDF 9054 kb)
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Fyhn, M., Hafting, T., Treves, A. et al. Hippocampal remapping and grid realignment in entorhinal cortex. Nature 446, 190–194 (2007). https://doi.org/10.1038/nature05601
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