Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Selective neural representation of objects relevant for navigation

Nature Neuroscience volume 7, pages 673–677 (2004)Cite this article

Abstract

As people find their way through their environment, objects at navigationally relevant locations can serve as crucial landmarks. The parahippocampal gyrus has previously been shown to be involved in object and scene recognition. In the present study, we investigated the neural representation of navigationally relevant locations. Healthy human adults viewed a route through a virtual museum with objects placed at intersections (decision points) or at simple turns (non-decision points). Event-related functional magnetic resonance imaging (fMRI) data were acquired during subsequent recognition of the objects in isolation. Neural activity in the parahippocampal gyrus reflected the navigational relevance of an object's location in the museum. Parahippocampal responses were selectively increased for objects that occurred at decision points, independent of attentional demands. This increase occurred for forgotten as well as remembered objects, showing implicit retrieval of navigational information. The automatic storage of relevant object location in the parahippocampal gyrus provides a part of the neural mechanism underlying successful navigation.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Virtual museum and recognition task.
Figure 2: Toys compared to non-toys.
Figure 3: Decision-point versus non-decision-point objects.
Figure 4: Remembered and forgotten objects.

Similar content being viewed by others

References

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

    Article  CAS  PubMed  Google Scholar 

  2. Burgess, N., Jeffery, K.J. & O'Keefe, J. (eds.) The Hippocampal and Parietal Foundations of Spatial Cognition (Oxford Univ. Press, Oxford, 1999).

    Google Scholar 

  3. 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).

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  5. Maguire, E.A., Frith, C.D., Burgess, N., Donnett, J.G. & O'Keefe, J. Knowing where things are: parahippocampal involvement in encoding object locations in virtual large-scale space. J. Cogn. Neurosci. 10, 61–76 (1998).

    Article  CAS  PubMed  Google Scholar 

  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 (1996).

    Article  CAS  PubMed  Google Scholar 

  7. Ekstrom, A.D. et al. Cellular networks underlying human spatial navigation. Nature 425, 184–187 (2003).

    Article  CAS  PubMed  Google Scholar 

  8. Maguire, E.A. et al. Navigation-related structural change in the hippocampi of taxi drivers. Proc. Natl. Acad. Sci. USA, 97, 4398–4403 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  10. Wood, E., Dudchenko, P.A., Robitsek, R.J. & Eichenbaum, H. Hippocampal neurons encode information about different types of memory episodes occurring in the same location. Neuron 27, 623–633 (2000).

    Article  CAS  PubMed  Google Scholar 

  11. Grön, G., Wunderlich, A.P., Spitzer, M., Tomaczak, R. & Riepe, M.W. Brain activation during human navigation: gender-different neural network as substrate of performance. Nat. Neurosci. 3, 404–408 (2000).

    Article  PubMed  Google Scholar 

  12. Dragoi, G., Harris, K.D. & Buzsáki, G. Place representation within hippocampal networks is modified by long-term potentiation. Neuron 39, 843–853 (2003).

    Article  CAS  PubMed  Google Scholar 

  13. Duezel, E. et al. Human hippocampal and parahippocampal activity during visual associative recognition memory for spatial and nonspatial stimulus configurations. J. Neurosci. 23, 9439–9444 (2003).

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  15. Bar, M. & Aminoff, E. Cortical analysis of visual context. Neuron 38, 347–358 (2003).

    Article  CAS  PubMed  Google Scholar 

  16. Golledge, R.G. (ed.) Wayfinding Behavior (Johns Hopkins Univ. Press, Baltimore, 1999).

    Google Scholar 

  17. Blades, M. & Medlicott, L. Developmental differences in the ability to give route directions from a map. J. Environ. Psychol. 12, 175–185 (1992).

    Article  Google Scholar 

  18. Johnsrude, I.S., Owen, A.M., Crane, J., Milner, B. & Evans, A.C. A cognitive activation study of memory for spatial relationships. Neuropsychologia 37, 829–841 (1999).

    Article  CAS  PubMed  Google Scholar 

  19. Daniel, M.-P. & Denis, M. Spatial descriptions as navigational aids: a cognitive analysis of route directions. Kognitionswissenschaft 7, 45–52 (1998).

    Article  Google Scholar 

  20. Ungerleider, L.G. & Mishkin, M. Two cortical visual systems. in Analysis of Visual Behavior (eds. Ingle, D.J., Goodale, M.A. & Mansfield, R.J.W.) 549–586 (MIT Press, Cambridge, Massachusetts, 1982).

    Google Scholar 

  21. Hasher, L. & Zacks, R.T. Automatic and effortful processes in memory. J. Exp. Psychol. Gen. 108, 356–388 (1979).

    Article  Google Scholar 

  22. Caldwell, J.L. & Masson, M.E.J. Conscious and unconscious influences of memory for object location. Mem. Cognit. 29, 285–295 (2001).

    Article  CAS  PubMed  Google Scholar 

  23. Owen, A.M., Milner, B., Petrides, M. & Evans, A.C. A specific role for the right parahippocampal gyrus in the retrieval of object-location: a positron emission tomography study. J. Cogn. Neurosci. 8 588–602 (1996).

    Article  CAS  PubMed  Google Scholar 

  24. Saenz, M., Buracas, G.T. & Boynton, G.M. Global effects of feature-based attention in human visual cortex. Nat. Neurosci. 5, 631–632 (2002).

    Article  CAS  PubMed  Google Scholar 

  25. Yantis, S. et al. Transient neural activity in human parietal cortex during spatial attention shifts. Nat. Neurosci. 5, 995–1002 (2002).

    Article  CAS  PubMed  Google Scholar 

  26. Kanwisher, N. & Wojciulik, E. Visual attention: insights from brain imaging. Nat. Rev. Neurosci. 1, 91–100 (2000).

    Article  CAS  PubMed  Google Scholar 

  27. Vuilleumier, P., Armony, J.L., Driver, J. & Dolan, R.J. Effects of attention and emotion on face processing in the human brain: an event-related fMRI study. Neuron 30, 829–841 (2001).

    Article  CAS  PubMed  Google Scholar 

  28. Gabrieli, 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  CAS  PubMed  Google Scholar 

  29. Brewer, J.B., Zhao, Z., Desmond, J.E., Glover, G.H. & Gabrieli, J.D.E. Making memories: brain activity that predicts how well visual experience will be remembered. Science 281, 1185–1187 (1998).

    Article  CAS  PubMed  Google Scholar 

  30. Van Turennout, M., Ellmore, T. & Martin, A. Long-lasting cortical plasticity in the object naming system. Nat. Neurosci. 3, 1329–1334 (2000).

    Article  CAS  PubMed  Google Scholar 

  31. Henson, R., Shallice, T. & Dolan, R. Neuroimaging evidence for dissociable forms of repetition priming. Science 287, 1269–1272 (2000).

    Article  CAS  PubMed  Google Scholar 

  32. Maccoby, E.E. & Jacklin, C.N. The Psychology of Sex Differences (Stanford University Press, Stanford, California, 1974).

    Google Scholar 

  33. Hyde, J.S. How large are cognitive gender differences? A meta-analysis using w2 and d. Am. Psychologist 36, 892–901 (1981).

    Article  Google Scholar 

  34. Layton, C.A. Gender differences in wayfinding-strategies: relationship to spatial ability and spatial anxiety. Sex Roles 30, 765–779 (1994).

    Article  Google Scholar 

  35. Sandstrom, N.J., Kaufman, J. & Huettel, S.A. Males and females use different distal cues in a virtual environment navigation task. Cogn. Brain Res. 6, 351–360 (1998).

    Article  CAS  Google Scholar 

  36. Talairach, J. & Tournoux, P. A Co-Planar Stereotaxic Atlas of the Human Brain (Thieme Medical Publishers, New York, 1988).

    Google Scholar 

Download references

Acknowledgements

We thank G. Fernández, P. Hagoort and M. Coles for helpful discussions and their comments on the manuscript.

Author information

Authors and Affiliations

  1. Max Planck Institute for Psycholinguistics, Postbus 310, Nijmegen, 6500 AH, The Netherlands

    Gabriele Janzen

  2. F.C. Donders Centre for Cognitive Neuroimaging, Box 9101, Nijmegen, 6500 HB, The Netherlands

    Gabriele Janzen & Miranda van Turennout

Authors
  1. Gabriele Janzen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Miranda van Turennout
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gabriele Janzen.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Janzen, G., van Turennout, M. Selective neural representation of objects relevant for navigation. Nat Neurosci 7, 673–677 (2004). https://doi.org/10.1038/nn1257

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn1257

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing