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Cellular networks underlying human spatial navigation

Abstract

Place cells of the rodent hippocampus constitute one of the most striking examples of a correlation between neuronal activity and complex behaviour in mammals1,2. These cells increase their firing rates when the animal traverses specific regions of its surroundings, providing a context-dependent map of the environment3,4,5. Neuroimaging studies implicate the hippocampus and the parahippocampal region in human navigation6,7,8. However, these regions also respond selectively to visual stimuli9,10,11,12,13. It thus remains unclear whether rodent place coding has a homologue in humans or whether human navigation is driven by a different, visually based neural mechanism. We directly recorded from 317 neurons in the human medial temporal and frontal lobes while subjects explored and navigated a virtual town. Here we present evidence for a neural code of human spatial navigation based on cells that respond at specific spatial locations and cells that respond to views of landmarks. The former are present primarily in the hippocampus, and the latter in the parahippocampal region. Cells throughout the frontal and temporal lobes responded to the subjects' navigational goals and to conjunctions of place, goal and view.

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Figure 1: Taxi driver game.
Figure 2: Place-responsive cells.
Figure 3: View-responsive cells.
Figure 4: Goal-responsive cells.

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Acknowledgements

We acknowledge support from NIMH grants to Brandeis University, a NINDS grant to UCLA, and a grant from the Sloan Foundation. We also thank P. Steinmetz, C. Wilson and E. Behnke for technical assistance, and I. Wainwright for editorial assistance.

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Correspondence to Michael J. Kahana or Itzhak Fried.

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Ekstrom, A., Kahana, M., Caplan, J. et al. Cellular networks underlying human spatial navigation. Nature 425, 184–188 (2003). https://doi.org/10.1038/nature01964

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