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A cortical representation of the local visual environment

Abstract

Medial temporal brain regions such as the hippocampal formation and parahippocampal cortex have been generally implicated in navigation1,2,3,4,5,6 and visual memory7,8,9. However, the specific function of each of these regions is not yet clear. Here we present evidence that a particular area within human parahippocampal cortex is involved in a critical component of navigation: perceiving the local visual environment. This region, which we name the ‘parahippocampal place area’ (PPA), responds selectively and automatically in functional magnetic resonance imaging (fMRI) to passively viewed scenes, but only weakly to single objects and not at all to faces. The critical factor for this activation appears to be the presence in the stimulus of information about the layout of local space. The response in the PPA to scenes with spatial layout but no discrete objects (empty rooms) is as strong as the response to complex meaningful scenes containing multiple objects (the same rooms furnished) and over twice as strong as the response to arrays of multiple objects without three-dimensional spatial context (the furniture from these rooms on a blank background). This response is reduced if the surfaces in the scene are rearranged so that they no longer define a coherent space. We propose that the PPA represents places by encoding the geometry of the local environment.

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Figure 1: Results of experiment 1, demonstrating that the PPA responds selectively to scenes.
Figure 2: Anatomical location of the PPA.
Figure 3: Results of experiment 2.
Figure 4: Results of experiment 3, showing the 5 different stimulus types with average per cent signal change in the PPA for each.

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References

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

    Google Scholar 

  2. Aguirre, G. K., Detre, J. A., Alsop, D. C. & D'Esposito, M. The parahippocampus subserves topographical learning in man. Cerebr. Cort. 6, 823–829 (1996).

    Article  CAS  Google Scholar 

  3. Aguirre, G. K. & D'Esposito, M. Environmental knowledge is subserved by separable dorsal/ventral neural areas. J. Neurosci. 17, 2512–2518 (1997).

    Article  CAS  Google Scholar 

  4. Maguire, E. A., Frackowiak, R. S. J. & Frith, C. D. Learning to find your way: a role for the human hippocampal region. Proc. R. Soc. Lond. B 263, 1745–1750 (1996).

    Article  ADS  CAS  Google Scholar 

  5. Maguire, E. A., Frackowiak, R. S. J. & Frith, C. D. Recalling routes around London: activation of the right hippocampus in taxi drivers. J. Neurosci. 17, 7103–7110 (1997).

    Article  CAS  Google Scholar 

  6. Rolls, E. T., Robertson, R. G. & Georges-Francois, P. Spatial view cells in the primate hippocampus. Eur. J. Neurosci. 9, 1789–1794 (1997).

    Article  CAS  Google Scholar 

  7. Stern, C. E.et al. The hippocampal formation participates in novel picture encoding: evidence from functional magnetic resonance imaging. Proc. Natl. Acad. Sci. USA 93, 8660–8665 (1996).

    Article  ADS  CAS  Google Scholar 

  8. Gabrielli, J. D. E., Brewer, J. B., Desmond, J. E. & Glover, G. H. Separate neural bases of two fundamental memory processes in the human medial temporal lobe. Science 276, 264–266 (1997).

    Article  Google Scholar 

  9. Gaffan, D. Scene-specific memory for objects: a model of episodic memory impairment in monkeys with fornix transection. J. Cogn. Neurosci. 6, 305–320 (1994).

    Article  CAS  Google Scholar 

  10. Aguirre, G. K., Zarahn, E. & D'Esposito, M. Studies of the neuro-anatomical components of topographical representation. Proc. Natl Acad. Sci. USA 95, 839–846 (1998).

    Article  ADS  CAS  Google Scholar 

  11. Ishai, A. Ungerleider, L. G., Martin, A., Maisog, J. M. & Haxby, J. V. fMRI reveals differential activation in the ventral object vision pathway during the perception of faces, houses, and chairs. NeuroImage 5, S149 (1997).

    Google Scholar 

  12. Hermer, L. & Spelke, E. S. Ageometric process for spatial reorientation in young children. Nature 370, 57–59 (1994).

    Article  ADS  CAS  Google Scholar 

  13. Hermer, L. & Spelke, E. Modularity and development: the case of spatial reorientation. Cognition 61, 195–232 (1996).

    Article  CAS  Google Scholar 

  14. Cheng, K. Apurely geometric module in the rat's spatial representation. Cognition 23, 149–178 (1986).

    Article  CAS  Google Scholar 

  15. Margules, J. & Gallistel, C. R. Heading in the rat: determination by environmental shape. Anim. Learn. Behav. 16, 404–410 (1988).

    Article  Google Scholar 

  16. Gallistel, C. R. The Organization of Learning(MIT Press, Cambridge, MA, (1990).

    Google Scholar 

  17. Biegler, R. & Morris, R. G. M. Landmark stability is a prerequisite for spatial but not discrimination learning. Nature 361, 631–633 (1993).

    Article  ADS  CAS  Google Scholar 

  18. Knierem, J. J., Kudrimoti, H. S. & McNaughton, B. L. Place cells, head direction cells, and the learning of landmark stability. J. Neurosci. 15, 1648–1659 (1995).

    Article  Google Scholar 

  19. Fodor, J. A. The Modularity of Mind(MIT Press, Cambridge, MA, (1983).

    Google Scholar 

  20. Habib, M. & Sirigu, A. Pure topographical disorientation: a definition and anatomical basis. Cortex 23, 73–85 (1987).

    Article  CAS  Google Scholar 

  21. Landis, T., Cummings, J. L., Benson, D. F. & Palmer, E. P. Loss of topographic familiarity: an environmental agnosia. Arch. Neurol. 43, 132–136 (1986).

    Article  CAS  Google Scholar 

  22. Maguire, E. A., Burke, T., Philips, J. & Staunton, H. Topographical disorientation following unilateral temporal lobe lesions in humans. Neuropsychologia 34, 994–1001 (1996).

    Article  Google Scholar 

  23. Bohbot, V.et al. Spatial memory deficits in patients with lesions to the right hippocampus and to the right parahippocampal cortex. Neuropsychologia(in the press).

  24. Kanwisher, N., McDermott, J. & Chun, M. M. The fusiform face area: a module in human extrastriate cortex specialized for face perception. J. Neurosci. 17, 4302–4311 (1997).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank D. Stanley, A. Harris and C. Ayasli for their assistance; E. Spelke, M. Potter, E. A. Murray, K. O'Craven, M. Chun and V. Bohbot for discussion; N. Kabani for anatomical advice; M.Chun for the image scrambling program; and B. Rosen and others at MGH for their support. R.E. was supported by an NIMH postdoctoral fellowship and N.K. was supported by grants from NIMH and the Human Frontiers Science Program.

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Correspondence to Russell Epstein.

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Epstein, R., Kanwisher, N. A cortical representation of the local visual environment. Nature 392, 598–601 (1998). https://doi.org/10.1038/33402

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