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Evidence for grid cells in a human memory network

Abstract

Grid cells in the entorhinal cortex of freely moving rats provide a strikingly periodic representation of self-location1 which is indicative of very specific computational mechanisms2,3,4. However, the existence of grid cells in humans and their distribution throughout the brain are unknown. Here we show that the preferred firing directions of directionally modulated grid cells in rat entorhinal cortex are aligned with the grids, and that the spatial organization of grid-cell firing is more strongly apparent at faster than slower running speeds. Because the grids are also aligned with each other1,5, we predicted a macroscopic signal visible to functional magnetic resonance imaging (fMRI) in humans. We then looked for this signal as participants explored a virtual reality environment, mimicking the rats’ foraging task: fMRI activation and adaptation showing a speed-modulated six-fold rotational symmetry in running direction. The signal was found in a network of entorhinal/subicular, posterior and medial parietal, lateral temporal and medial prefrontal areas. The effect was strongest in right entorhinal cortex, and the coherence of the directional signal across entorhinal cortex correlated with spatial memory performance. Our study illustrates the potential power of combining single-unit electrophysiology with fMRI in systems neuroscience. Our results provide evidence for grid-cell-like representations in humans, and implicate a specific type of neural representation in a network of regions which supports spatial cognition and also autobiographical memory.

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Figure 1: The mean firing directions of directional grid cells are aligned with the grid.
Figure 2: fMRI: virtual reality arena and experimental logic.
Figure 3: Modulation of entorhinal cortical activity by running direction with six-fold rotational symmetry, and correlation with spatial memory.
Figure 4: fMRI adaptation to running direction and to runs at 60° from it.

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Acknowledgements

We acknowledge K. Jeffery and J. O’Keefe for providing help and facilities for single-unit recording; the Wellcome Trust Centre for Neuroimaging at UCL for providing help and scanning facilities; J. Krupic and R. Hayman for help with single-unit data collection; A. Jeewajee for help with analyses; J. King for help with virtual reality programming; and useful discussions with P. Dayan, K. Friston, U. Frith, C. Hall, A. Jeewajee, J. O’Keefe and M. Witter. This work was funded by the UK Medical Research Council and the European Union (SpaceBrain grant).

Author Contributions C.F.D., C.B. and N.B. jointly conceived and designed the experiments. C.F.D. performed the fMRI experiment and data analyses; C.B. performed the single-unit experiment and data analyses; N.B. gave direction on analyses; all authors discussed the analyses and results and contributed to writing the paper.

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Correspondence to Christian F. Doeller or Neil Burgess.

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Doeller, C., Barry, C. & Burgess, N. Evidence for grid cells in a human memory network. Nature 463, 657–661 (2010). https://doi.org/10.1038/nature08704

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