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Membrane potential dynamics of grid cells

A Corrigendum to this article was published on 27 November 2013

Abstract

During navigation, grid cells increase their spike rates in firing fields arranged on a markedly regular triangular lattice, whereas their spike timing is often modulated by theta oscillations. Oscillatory interference models of grid cells predict theta amplitude modulations of membrane potential during firing field traversals, whereas competing attractor network models predict slow depolarizing ramps. Here, using in vivo whole-cell recordings, we tested these models by directly measuring grid cell intracellular potentials in mice running along linear tracks in virtual reality. Grid cells had large and reproducible ramps of membrane potential depolarization that were the characteristic signature tightly correlated with firing fields. Grid cells also demonstrated intracellular theta oscillations that influenced their spike timing. However, the properties of theta amplitude modulations were not consistent with the view that they determine firing field locations. Our results support cellular and network mechanisms in which grid fields are produced by slow ramps, as in attractor models, whereas theta oscillations control spike timing.

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Figure 1: Schematics of membrane potential predicted by different model families.
Figure 2: Tetrode recordings from grid cells in two-dimensional arenas and virtual linear tracks.
Figure 3: Whole-cell recordings from grid cells.
Figure 4: Grid cells exhibit slow intracellular ramps of depolarization and theta oscillations with variable amplitudes.
Figure 5: Ramps contain more information about position.
Figure 6: Ramps, not oscillations, are the primary drive of field formation.

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Acknowledgements

We thank C. Harvey, R. Low, A. Miri, S. Lewallen, J. Rickgauer, D. Little, D. Barson, D. Aronov, W. Bialek, I. Fiete and G. Buzsaki for helpful discussions. This work was supported by NINDS grant 5RC1NS068148-02 and 1R37NS081242-01, NIMH grant 5R01MH083686-04, NIH Postdoctoral Fellowship grant F32NS070514-01A1 (A.A.K.), and an NSF Graduate Research Fellowship (C.D.).

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Contributions

C.D. performed whole-cell recording experiments and histological identification. A.A.K. performed tetrode experiments; A.A.K. and D.W.T. designed the system for measuring grid cell activity in virtual reality; C.D. analysed the data with strategy and methods contributions from A.A.K. and D.W.T.; C.D. and D.W.T. wrote the paper.

Corresponding author

Correspondence to David W. Tank.

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The authors declare no competing financial interests.

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Supplementary Figures 1

This file contains Supplementary Figures 1–9. This file was corrected on 27 November 2013. (PDF 22051 kb)

Supplementary Figures 2

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Domnisoru, C., Kinkhabwala, A. & Tank, D. Membrane potential dynamics of grid cells. Nature 495, 199–204 (2013). https://doi.org/10.1038/nature11973

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