Scientific Understanding of Consciousness
Grid Cells in the Human Memory Network
Nature 463, 657-661 (4 February 2010)
Evidence for grid cells in a human memory network
Christian F. Doeller, Caswell Barry & Neil Burgess
UCL Institute of Cognitive Neuroscience, London WC1N 3AR, UK
UCL Institute of Neurology, London WC1N 3BG, UK
UCL Department of Cell and Developmental Biology, London WC1E 6BT, UK
UCL Institute of Behavioural Neuroscience, University College London, London WC1H 0AP, UK
Grid cells in the entorhinal cortex of freely moving rats provide a strikingly periodic representation of self-location which is indicative of very specific computational mechanisms. 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 other, 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.
Overall, these results suggest a network of regions containing coherently aligned neural representations with six-fold rotational symmetry, although the responses in remote regions were weaker than in right entorhinal cortex (for example, not reaching significance in the initial whole-brain split-half analysis), possibly reflecting a lower concentration of grid-like cells.
Our results provide the first evidence that human entorhinal cortex encodes virtual movement direction with six-fold symmetry, consistent with a coherently-oriented population of grid cells similar to those found in rat entorhinal cortex and pre- and parasubiculum. The dependence of directional modulation on running speed is consistent with the effects of speed on the firing rate and apparent spatial organization of grid cells, whereas effects of speed on other aspects of behaviour may also contribute. The relationship to spatial memory of the directional coherence of potential grids across entorhinal cortex provides a first indication that grid-like representations might usefully guide behaviour.
Because we can only measure effects of direction and speed (not location) in the fMRI signal, our findings could reflect the presence of grid cells, or movement-related responses from head direction, or ‘conjunctive’ directional grid cells, if they form coherent populations whose firing has six-fold rotational symmetry. We showed that conjunctive grid cells from rat entorhinal cortex have such an organization. Our finding of similar and aligned fMRI responses from subicular, posterior/medial parietal, lateral temporal, and medial prefrontal cortices indicate that populations with similar properties also exist elsewhere, a prediction directly testable in rodents. These results outline a circuit for navigation, consistent with suggestions that medial and lateral temporal, posterior and medial parietal and medial prefrontal areas cooperate to support spatial cognition, and implicate a specific type of underlying neural representation.
Our study illustrates the ability to infer neural representations in humans by using fMRI in conjunction with single-unit recording in behaving animals, promising a coherent understanding of behaviour at the neural and systems levels. The observed grid-like representations support spatial memory and are found in a circuit of regions which markedly overlaps the network for autobiographical memory and imagery. These types of regularly repeating representation may provide a clue to the neural basis of autobiographical memory, perhaps encoding temporal as well as spatial context for combination with parallel networks representing non-spatial information.
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