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.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
O'Keefe, J. & Nadel, L. The Hippocampus as a Cognitive Map(Oxford University Press, Oxford, (1978).
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).
Aguirre, G. K. & D'Esposito, M. Environmental knowledge is subserved by separable dorsal/ventral neural areas. J. Neurosci. 17, 2512–2518 (1997).
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).
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).
Rolls, E. T., Robertson, R. G. & Georges-Francois, P. Spatial view cells in the primate hippocampus. Eur. J. Neurosci. 9, 1789–1794 (1997).
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).
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).
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).
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).
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).
Hermer, L. & Spelke, E. S. Ageometric process for spatial reorientation in young children. Nature 370, 57–59 (1994).
Hermer, L. & Spelke, E. Modularity and development: the case of spatial reorientation. Cognition 61, 195–232 (1996).
Cheng, K. Apurely geometric module in the rat's spatial representation. Cognition 23, 149–178 (1986).
Margules, J. & Gallistel, C. R. Heading in the rat: determination by environmental shape. Anim. Learn. Behav. 16, 404–410 (1988).
Gallistel, C. R. The Organization of Learning(MIT Press, Cambridge, MA, (1990).
Biegler, R. & Morris, R. G. M. Landmark stability is a prerequisite for spatial but not discrimination learning. Nature 361, 631–633 (1993).
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).
Fodor, J. A. The Modularity of Mind(MIT Press, Cambridge, MA, (1983).
Habib, M. & Sirigu, A. Pure topographical disorientation: a definition and anatomical basis. Cortex 23, 73–85 (1987).
Landis, T., Cummings, J. L., Benson, D. F. & Palmer, E. P. Loss of topographic familiarity: an environmental agnosia. Arch. Neurol. 43, 132–136 (1986).
Maguire, E. A., Burke, T., Philips, J. & Staunton, H. Topographical disorientation following unilateral temporal lobe lesions in humans. Neuropsychologia 34, 994–1001 (1996).
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).
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).
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.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Epstein, R., Kanwisher, N. A cortical representation of the local visual environment. Nature 392, 598–601 (1998). https://doi.org/10.1038/33402
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/33402
This article is cited by
-
A retinotopic code structures the interaction between perception and memory systems
Nature Neuroscience (2024)
-
Longitudinal development of category representations in ventral temporal cortex predicts word and face recognition
Nature Communications (2023)
-
Human brain responses are modulated when exposed to optimized natural images or synthetically generated images
Communications Biology (2023)
-
Multiple visual objects are represented differently in the human brain and convolutional neural networks
Scientific Reports (2023)
-
Entorhinal grid-like codes and time-locked network dynamics track others navigating through space
Nature Communications (2023)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.