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.

References

  1. 1

    O'Keefe, J. & Dostrovsky, J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 34, 171–175 (1971)

  2. 2

    Muller, R. U., Kubie, J. L. & Ranck, J. B. Spatial firing patterns of hippocampal complex-spike cells in a fixed environment. J. Neurosci. 7, 1935–1950 (1987)

  3. 3

    O'Keefe, J. & Conway, D. H. Hippocampal place units in the freely moving rat: why they fire where they fire. Exp. Brain Res. 31, 573–590 (1978)

  4. 4

    Muller, R. U. & Kubie, J. L. The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells. J. Neurosci. 7, 1951–1968 (1987)

  5. 5

    Wilson, M. A. & McNaughton, B. L. Dynamics of the hippocampal ensemble code for space. Science 261, 1055–1058 (1993)

  6. 6

    Aguirre, G. K., Detre, J. A., Alsop, D. C. & D'Esposito, M. The parahippocampus subserves topographical learning in man. Cereb. Cortex 6, 823–829 (1998)

  7. 7

    Aguirre, G. K., Zarahn, E. & D'Esposito, M. An area within human ventral cortex sensitive to “building” stimuli: evidence and implications. Neuron 21, 373–383 (1996)

  8. 8

    Maguire, E. et al. Knowing where and getting there: a human navigation network. Science 280, 921–924 (1998)

  9. 9

    Epstein, R. & Kanwisher, N. A cortical representation of the local visual environment. Nature 392, 598–601 (1998)

  10. 10

    Epstein, R., Graham, K. & Downing, P. E. Viewpoint specific scene representations in human parahippocampal cortex. Neuron 37, 865–876 (2003)

  11. 11

    Kreiman, G., Koch, C. & Fried, I. Category-specific visual responses of single neurons in the human medial temporal lobe. Nature Neurosci. 3, 946–953 (2000)

  12. 12

    Cameron, K. A., Yashar, S., Wilson, C. L. & Fried, I. Human hippocampal neurons predict how well word pairs will be remembered. Neuron 30, 289–298 (2001)

  13. 13

    Ojemann, G., Schoenfield-McNeill, J. & Corina, D. Anatomic subdivisions in human temporal cortical neuronal activity related to recent verbal memory. Nature Neurosci. 5, 64–71 (2002)

  14. 14

    Georges-Francois, P., Rolls, E. T. & Robertson, R. G. Spatial view cells in the primate hippocampus: allocentric view not head direction or eye position or place. Cereb. Cortex 9, 197–212 (1999)

  15. 15

    Robertson, R. G., Rolls, E. T. & Georges-Francios, P. Head-direction cells in the primate presubiculum. Hippocampus 9, 206–219 (1999)

  16. 16

    Matsumura, N., Nishijo, H., Tamura, R., Eifuku, S. & Ono, T. Spatial- and task-dependent neuronal responses during real and virtual translocation in the monkey hippocampal formation. J. Neurosci. 19, 2381–2393 (1999)

  17. 17

    Markus, E. J. et al. Interactions between location and task affect the spatial and directional firing of hippocampal neurons. J. Neurosci. 15, 7079–7094 (1995)

  18. 18

    Burgess, N., Maguire, E. & O'Keefe, J. The human hippocampus and spatial and episodic memory. Neuron 35, 625–641 (2002)

  19. 19

    Quirk, G. J., Muller, R. U., Kubie, J. L. & Ranck, J. B. The positional firing properties of medial entorhinal neurons: description and comparison with hippocampal place cells. J. Neurosci. 12, 1945–1963 (1992)

  20. 20

    Frank, L. M., Brown, E. N. & Wilson, M. A. Trajectory encoding in the hippocampus and entorhinal cortex. Neuron 27, 169–178 (2000)

  21. 21

    Tolman, E. C. Cognitive maps in rats and men. Psych. Rev. 55, 189–208 (1948)

  22. 22

    O'Keefe, J. & Nadel, L. The Hippocampus as a Cognitive Map (Oxford Univ. Press, Oxford, 1978)

  23. 23

    Caplan, J. B. et al. Human theta oscillations related to sensorimotor integration and spatial learning. J. Neurosci. 23, 4726–4736 (2003)

  24. 24

    Fried, I. et al. Cerebral microdialysis combined with single-neuron and electroencephalographic recording in neurosurgical patients. Technical note. J. Neurosurg. 91, 697–705 (1999)

  25. 25

    Fried, I., MacDonald, K. & Wilson, C. L. Single neuron activity in human hippocampus and amygdala during recognition of faces and objects. Neuron 18, 753–765 (1997)

  26. 26

    Witter, M. in The Parahippocampal Region: Organization and Role in Cognitive Functions (eds Witter, M. & Wouterlood, F.) 3–19 (Oxford Univ. Press, Oxford, 2002)

  27. 27

    Skaggs, W. E., McNaughton, B. L., Gothard, K. M. & Markus, E. J. in Advances in Neural Information Processing Systems (eds Hanson, S. J., Cowan, J. D. & Giles, C. L.) 1030–1037 (Morgan-Kaufman, San Mateo, California, 1993)

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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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The authors declare that they have no competing financial interests.

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