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:

Reorganization of human cortical maps caused by inherited photoreceptor abnormalities

Nature Neuroscience volume 5, pages 364–370 (2002)Cite this article

Abstract

We describe a compelling demonstration of large-scale developmental reorganization in the human visual pathways. The developmental reorganization was observed in rod monochromats, a rare group of congenitally colorblind individuals who virtually lack cone photoreceptor function. Normal controls had a cortical region, spanning several square centimeters, that responded to signals initiated in the all-cone foveola but was inactive under rod viewing conditions; in rod monochromats this cortical region responded powerfully to rod-initiated signals. The measurements trace a causal pathway that begins with a genetic anomaly that directly influences sensory cells and ultimately results in a substantial central reorganization.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

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

Figure 1: Visual field eccentricity plots in three experimental conditions.
Figure 2: Responses in foveolar and parafoveal regions in three experimental conditions.
Figure 3: Visual field eccentricity plots in V1 for two normal trichromats (H.B., A.B.).
Figure 4: Visual field eccentricity plots in V1 for three rod monochromats (S.H., D.G., K.N.).
Figure 5: Theoretical analysis and simulation of the visual field eccentricity plot.
Figure 6: Visual field eccentricity measurement methods.
Figure 7: Visual field eccentricity plots are independent of correlation threshold.

Similar content being viewed by others

References

  1. Østerberg, G. A. Topography of the layer of rods and cones in the human retina. Acta Ophthamol. 6, 1–103 (1935).

    Google Scholar 

  2. Polyak, S. L. The Retina (Univ. of Chicago Press, Chicago, IL, 1941).

    Google Scholar 

  3. Ahnelt, P. K., Kolb, H. & Pflug, R. Identification of a subtype of cone photoreceptor, likely to be blue sensitive, in the human retina. J. Comp. Neurol. 255, 18–34 (1987).

    Article  CAS  Google Scholar 

  4. Curcio, C. A., Sloan, K. R., Kalina, R. E. & Hendrickson, A. E. Human photoreceptor topography. J. Comp. Neurol. 292, 497–523 (1990).

    Article  CAS  Google Scholar 

  5. Horton, J. C. & Hoyt, W. F. The representation of the visual field in human striate cortex. A revision of the classic Holmes map. Arch. Ophthalmol. 109, 816–824 (1991).

    Article  CAS  Google Scholar 

  6. Hadjikhani, N. & Tootell, R. B. Projection of rods and cones within human visual cortex. Hum. Brain Mapp. 9, 55–63 (2000).

    Article  CAS  Google Scholar 

  7. Kohl, S. et al. Total color-blindness is caused by mutations in the gene encoding the α-subunit of the cone photoreceptor cGMP-gated cation channel. Nat. Genet. 19, 257–259 (1998).

    Article  CAS  Google Scholar 

  8. Kohl, S. et al. Mutations in the CNGB3 gene encoding the β-subunit of the cone photoreceptor cGMP-gated channel are responsible for achromatopsia (ACHM3) linked to chromosome 8q21. Hum. Mol. Genet. 9, 2107–2116 (2000).

    Article  CAS  Google Scholar 

  9. Sharpe, L. T., Stockman, A., Jagle, H. & Nathans, J. in Color Vision: From Genes to Perception (eds Gegenfurtner, K. & Sharpe, L. T.) 3–52 (Cambridge Univ. Press, Cambridge, 1999).

    Google Scholar 

  10. Glickstein, M. & Heath, G. G. Receptors in the monochromat eye. Vision Res. 15, 633–636 (1975).

    Article  CAS  Google Scholar 

  11. Sharpe, L. T. & Nordby, K. in Night Vision: Basic, Clinical and Applied Aspects (eds Hess, R. F., Sharpe, L.T. & Nordby, K.) 335–389 (Cambridge Univ. Press, Cambridge, 1990).

    Google Scholar 

  12. Weliky, M. & Katz, L. C. Correlational structure of spontaneous neuronal activity in the developing lateral geniculate nucleus in vivo. Science 285, 599–604 (1999).

    Article  CAS  Google Scholar 

  13. White, L. E., Coppola, D. M. & Fitzpatrick, D. The contribution of sensory experience to the maturation of orientation selectivity in ferret visual cortex. Nature 411, 1049–1052 (2001).

    Article  CAS  Google Scholar 

  14. Gilbert, C. D. & Wiesel, T. N. Receptive field dynamics in adult primary visual cortex. Nature 365, 150–152 (1992).

    Article  Google Scholar 

  15. Kaas, J. H. Plasticity of sensory and motor maps in adult mammals. Annu. Rev. Neurosci. 14, 137–167 (1991).

    Article  CAS  Google Scholar 

  16. Heinen, S. J. & Skavenski, A. A. Recovery of visual responses in foveal V1 neurons following bilateral foveal lesions in adult monkey. Exp. Brain Res. 83, 670–674 (1991).

    Article  CAS  Google Scholar 

  17. Crair, M. C., Gillespie, D. C. & Stryker, M. P. The role of visual experience in the development of columns in cat visual cortex. Science 279, 566–570 (1998).

    Article  CAS  Google Scholar 

  18. Engel, S. A., Glover, G. H. & Wandell, B. A. Retinotopic organization in human visual cortex and the spatial precision of functional MRI. Cereb. Cortex 7, 181–192 (1997).

    Article  CAS  Google Scholar 

  19. Kapadia, M. K., Westheimer, G. & Gilbert, C. D. Dynamics of spatial summation in primary visual cortex of alert monkeys. Proc. Natl. Acad. Sci. USA 96, 12073–12078 (1999).

    Article  CAS  Google Scholar 

  20. Pettet, M. W. & Gilbert, C. D. Dynamic changes in receptive-field size in cat primary visual cortex. Proc. Natl. Acad. Sci. USA 89, 8366–8370 (1992).

    Article  CAS  Google Scholar 

  21. Das, A. & Gilbert, C. D. Topography of contextual modulations mediated by short-range interactions in primary visual cortex. Nature 399, 655–661 (1999).

    Article  CAS  Google Scholar 

  22. Kapadia, M., Gilbert, C. & Westheimer, G. A quantitative measure for short-term cortical plasticity in human vision. J. Neurosci. 14, 451–457 (1994).

    Article  CAS  Google Scholar 

  23. Andrews, T. J., Halpern, S. D. & Purves, D. Correlated size variations in human visual cortex, lateral geniculate nucleus, and optic tract. J. Neurosci. 17, 2859–2868 (1997).

    Article  CAS  Google Scholar 

  24. Rodieck, R. W. Visual pathways. Annu. Rev. Neurosci. 2, 193–225 (1979).

    Article  CAS  Google Scholar 

  25. Sharpe, L. T., Collewijn, H. & Nordby, K. Fixation, pursuit and optokinetic nystagmus in a complete achromat. Clin. Vis. Sci. 1, 39–49 (1986).

    Google Scholar 

  26. Sharpe, L. T. & Nordby, K. in Night Vision: Basic, Clinical and Applied Aspects (eds Hess, R. F., Sharpe, L.T. & Nordby, K.) 253–289 (Cambridge Univ. Press, Cambridge, 1990).

    Google Scholar 

  27. Haegerstrom-Portnoy, G., Schneck, M. E., Verdon, W. A. & Hewlett, S. E. Clinical vision characteristics of the congenital achromatopsias. I. Visual acuity, refractive error, and binocular status. Optom. Vis. Sci. 73, 446–456 (1996).

    Article  CAS  Google Scholar 

  28. Haegerstrom-Portnoy, G., Schneck, M. E., Verdon, W. A. & Hewlett, S.E. Clinical vision characteristics of the congenital achromatopsias. II. Color vision. Optom. Vis. Sci. 73, 457–465 (1996).

    Article  CAS  Google Scholar 

  29. Wandell, B. A. Computational imaging of human visual cortex. Annu. Rev. Neurosci. 22, 145–173 (1999).

    Article  CAS  Google Scholar 

  30. Wandell, B. A. Foundations of Vision (Sinauer Press, Sunderland, MA, 1995).

    Google Scholar 

  31. Brainard, D. H. The psychophysics toolbox. Spat. Vis. 10, 433–436 (1997).

    Article  CAS  Google Scholar 

  32. Meyer, C. H., Hsu, B. S., Nishimura, D. G. & Macovski, A. Fast spiral coronary artery imaging. Mag. Res. Med. 28, 202–213 (1992).

    Article  CAS  Google Scholar 

  33. Ogawa, S. et al. Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. Proc. Natl. Acad. Sci. USA 89, 5951–5955 (1992).

    Article  CAS  Google Scholar 

  34. Teo, P. C., Sapiro, G. & Wandell, B. A. Creating connected representations of cortical gray matter for functional MRI visualization. IEEE Trans. Med. Imaging 16, 852–863 (1997).

    Article  CAS  Google Scholar 

  35. Wandell, B. A., Chial, S. & Backus, B. Visualization and measurement of the cortical surface. J. Cogn. Neurosci. 12, 739–752 (2000).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This research was supported by fellowships and grants from the National Institutes of Health (EY30164), National Eye Institute (NEI), North Atlantic Treaty Organization, the Wellcome Trust and the McKnight Foundation. We are grateful to G. Haegerstrom-Portnoy and M. Schneck for referring and providing clinical data on D.G. and S.H. We also thank R. Dougherty, G. Haegerstrom-Portnoy, D. Heeger, S. Heinen, R. Hoffman, V. Koch, W. Newsome, W. Press, M. Schneck and A. Wade.

Author information

Authors and Affiliations

  1. Department of Psychology, Stanford University, Stanford, California, USA

    Heidi A. Baseler, Antony B. Morland & Brian A. Wandell

  2. Neuroscience Program, Stanford University, Stanford, California, USA

    Alyssa A. Brewer & Brian A. Wandell

  3. University of Tübingen, Tübingen, Germany

    Lindsay T. Sharpe & Herbert Jägle

Authors
  1. Heidi A. Baseler
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alyssa A. Brewer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lindsay T. Sharpe
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Antony B. Morland
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Herbert Jägle
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Brian A. Wandell
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Brian A. Wandell.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Baseler, H., Brewer, A., Sharpe, L. et al. Reorganization of human cortical maps caused by inherited photoreceptor abnormalities. Nat Neurosci 5, 364–370 (2002). https://doi.org/10.1038/nn817

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn817

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