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:

Visual cortex maps are optimized for uniform coverage

Nature Neuroscience volume 3, pages 822–826 (2000)Cite this article

Abstract

Cat visual cortex contains a topographic map of visual space, plus superimposed, spatially periodic maps of ocular dominance, spatial frequency and orientation. It is hypothesized that the layout of these maps is determined by two constraints: continuity or smooth mapping of stimulus properties across the cortical surface, and coverage uniformity or uniform representation of combinations of map features over visual space. Here we use a quantitative measure of coverage uniformity (c′) to test the hypothesis that cortical maps are optimized for coverage. When we perturbed the spatial relationships between ocular dominance, spatial frequency and orientation maps obtained in single regions of cortex, we found that cortical maps are at a local minimum for c′. This suggests that coverage optimization is an important organizing principle governing cortical map development.

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: Experimental data from three of the cats on which calculations were based.
Figure 2: Effects of various reflections and rotations of one or more maps, relative to each other, on coverage uniformity.
Figure 3: Effect of displacing one of the maps sideways relative to the other two by a fixed amount (offsets are multiples of one pixel, 0.036 mm).

Similar content being viewed by others

References

  1. Hubel, D. H. & Wiesel, T. N. Receptive fields, binocular interaction, and functional architecture of cat striate cortex. J. Physiol. (Lond.) 160, 106–154 ( 1962).

    Article  CAS  Google Scholar 

  2. Hubel, D. H. & Wiesel, T. N. Receptive fields and functional architecture of monkey striate cortex. J. Physiol. (Lond.) 195, 215–243 (1968).

    Article  CAS  Google Scholar 

  3. Hubel, D. H. & Wiesel, T. N. Sequence regularity and geometry of orientation columns in the monkey striate cortex. J. Comp. Neurol. 158, 267–294 ( 1974).

    Article  CAS  Google Scholar 

  4. Hubel, D. H. & Wiesel, T. N. Functional architecture of macaque monkey visual cortex. Proc. R. Soc. Lond. B 198, 1–59 (1977).

    Article  CAS  Google Scholar 

  5. Swindale, N. V., Matsubara, J. A. & Cynader, M. S. Surface organization of orientation and direction selectivity in cat area 18. J. Neurosci. 7, 1414–1427 (1987).

    Article  CAS  Google Scholar 

  6. Shmuel, A. & Grinvald, A. Functional organization for direction of motion and its relationship to orientation maps in area 18. J. Neurosci. 16, 6945–6964 (1996).

    Article  CAS  Google Scholar 

  7. Weliky, M., Bosking, W. H. & Fitzpatrick, D. A systematic map of direction preference in primary visual cortex. Nature 379, 725– 728 (1996).

    Article  CAS  Google Scholar 

  8. Tootell, R. B. H., Silverman, M. S., Hamilton, S. L., De Valois, R. L. & Switkes, E. Functional anatomy of macaque striate cortex. III. Color. J. Neurosci. 8, 1569–1593 (1988).

    Article  CAS  Google Scholar 

  9. Thompson, I. D. & Tolhurst, D. J. The representation of spatial frequency in cat visual cortex: a 14C-2-deoxyglucose study. J. Physiol. (Lond.) 300, 58– 59 (1981).

    Google Scholar 

  10. Tootell, R. B. H., Silverman, M. S. & De Valois, R. L. Spatial frequency columns in primary visual cortex . Science 214, 813–815 (1981).

    Article  CAS  Google Scholar 

  11. Shoham, D., Hübener, M., Schulze, S., Grinvald, A. & Bonhoeffer, T. Spatio-temporal frequency domains and their relation to cytochrome oxidase staining in cat visual cortex. Nature 385, 529–533 ( 1997).

    Article  CAS  Google Scholar 

  12. DeAngelis, G. C., Ghose, G. M., Ohzawa, I. & Freeman, R. D. Functional micro-organization of primary visual cortex: receptive field analysis of nearby neurons. J. Neurosci. 19, 4046– 4064 (1999).

    Article  CAS  Google Scholar 

  13. Hübener, M., Shoham, D., Grinvald, A. & Bonhoeffer, T. Spatial relationships among three columnar systems in cat area 17. J. Neurosci. 17, 9270–9284 (1997).

    Article  Google Scholar 

  14. Bartfeld, E. & Grinvald, A. Relationships between orientation-preference pinwheels, cytochrome oxidase blobs, and ocular dominance columns in primate striate cortex. Proc. Natl. Acad. Sci. USA 89, 11905–11909 (1992).

    Article  CAS  Google Scholar 

  15. Obermayer, K. & Blasdel, G. G. Geometry of orientation and ocular dominance columns in monkey striate cortex. J. Neurosci. 13, 4114–4129 (1993).

    Article  CAS  Google Scholar 

  16. Swindale, N. V. Coverage and the design of striate cortex. Biol. Cybern. 65, 415–424 (1991).

    Article  CAS  Google Scholar 

  17. Albus, K. A quantitative study of the projection area of the central and paracentral visual field in area 17 of the cat. I. The precision of the topography. Exp. Brain Res. 24, 159–179 (1975).

    Article  CAS  Google Scholar 

  18. Hetherington, P. A. & Swindale, N. V. Receptive field and orientation scatter studied by tetrode recording in cat area 17 . Visual Neurosci. 16, 637– 652 (1999).

    Article  CAS  Google Scholar 

  19. Das, A. & Gilbert, C. D. Distortions of visuotopic map match orientation singularities in primary visual cortex. Nature 387, 594–598 ( 1997).

    Article  CAS  Google Scholar 

  20. Obermayer, K., Ritter, H. & Schulten, K. A principle for the formation of the spatial structure of cortical feature maps. Proc. Natl. Acad. Sci. USA 87, 8345–8349 (1990).

    Article  CAS  Google Scholar 

  21. Obermayer, K., Blasdel, G. G. & Schulten, K. Statistical-mechanical analysis of self-organization and pattern formation during the development of visual maps. Phys. Rev. A 45, 7568–7589 ( 1992).

    Article  CAS  Google Scholar 

  22. Swindale, N. V. The development of topography in the visual cortex: a review of models. Network 7, 161–247 ( 1996).

    Article  CAS  Google Scholar 

  23. Swindale, N. V. How many maps are there in visual cortex? Cereb. Cortex (in press).

  24. Durbin, R. & Willshaw, D. J. An analogue approach to the travelling salesman problem using an elastic net method. Nature 326, 698–691 ( 1987).

    Article  Google Scholar 

  25. Durbin, R. & Mitchison, G. A dimension reduction framework for understanding cortical maps. Nature 343, 644–647 (1990).

    Article  CAS  Google Scholar 

  26. Kohonen, T. Self-organized formation of topologically correct feature maps. Biol. Cybern. 43, 59–69 (1982).

    Article  Google Scholar 

  27. Swindale, N. V. Elastic nets, travelling salesmen and cortical maps. Curr. Biol. 2, 429–431 ( 1992).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from the National Science and Engineering Research Council of Canada and the Medical Research Council of Canada to N.V.S. Additional support came from the Max-Planck-Gesellschaft and the EC Biotech Program (M.H. and T.B.) and from the Wolfson Foundation and German-Israeli Research Foundation to A.G.

Author information

Authors and Affiliations

  1. Dept. of Ophthalmology, University of British Columbia ,, 2550 Willow St., Vancouver, V5Z 3N9, B.C., Canada

    Nicholas V. Swindale

  2. Department of Neurobiology,, The Weizmann Institute of Science, Rehovot, 76100, Israel

    Doron Shoham & Amiram Grinvald

  3. Max-Planck-Institut für Neurobiologie, Am-Klopferspitz 18A,, Martinsried, D-82152, Germany

    Tobias Bonhoeffer & Mark Hübener

Authors
  1. Nicholas V. Swindale
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Doron Shoham
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Amiram Grinvald
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tobias Bonhoeffer
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mark Hübener
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nicholas V. Swindale.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Swindale, N., Shoham, D., Grinvald, A. et al. Visual cortex maps are optimized for uniform coverage. Nat Neurosci 3, 822–826 (2000). https://doi.org/10.1038/77731

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/77731

This article is cited by

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