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:

Undercounting features and missing features: evidence for a high-level deficit in strabismic amblyopia

Nature Neuroscience volume 3, pages 496–501 (2000)Cite this article

Abstract

Abnormal visual development in strabismic amblyopia drastically affects visual perception and properties of neurons in primary visual cortex (V1). To test the notion that amblyopia also has consequences for higher visual areas, we asked humans with amblyopia to count briefly presented features. Using the amblyopic eye, strabismic amblyopes counted inaccurately, markedly underestimating the number of features. This inaccuracy was not due to low-level considerations (blur, visibility, crowding, undersampling or topographical jitter), as they also underestimated the number of features missing from a uniform grid. Rather, counting deficits in strabismic amblyopes reflected a higher-level limitation in the number of features the amblyopic visual system can individuate.

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: Examples of stimuli.
Figure 2: Experiment 1: counting patches.
Figure 3: Number reported versus number of features for experiment 1.
Figure 4: Experiment 2: counting ‘missing features’.
Figure 5: Experiment 2: counting ‘vertical features’.
Figure 6: Effect of cueing on attention.

Similar content being viewed by others

References

  1. Weisel, T. N. Postnatal development of the visual cortex and the influence of environment. Nature 299, 583–591 (1982).

    Article  Google Scholar 

  2. Smith, E. L., III et al. Residual binocular interactions in the striate cortex of monkeys reared with abnormal binocular vision. J. Neurophysiol. 78, 1353–1362 (1997).

    Article  Google Scholar 

  3. Kiorpes, L., Kiper, D. C., O'Keefe, L. P., Cavanaugh, J. R. & Movshon, J.A. Neuronal correlates of amblyopia in the visual cortex of macaque monkeys with experimental strabismus and anisometropia. J. Neurosci. 18, 6411–6424 (1998).

    Article  CAS  Google Scholar 

  4. Hess, R.F. Developmental sensory impairment: amblyopia or tarachopia. Hum. Neurobiol. 1, 17–29 (1982).

    CAS  PubMed  Google Scholar 

  5. Levi, D.M. in Vision and Visual Dysfunction. Vol. 10B (ed. Cronly-Dillon, J.) 212–238 (Macmillan, New York, 1991).

    Google Scholar 

  6. Levi, D. M. & Klein, S. A. Vernier acuity, crowding and amblyopia. Vision Res. 25, 979–991 (1985).

    Article  CAS  Google Scholar 

  7. Levi, D. M. & Klein, S.A. Sampling in spatial vision. Nature 320, 360–362 (1986).

    Article  CAS  Google Scholar 

  8. Wang, H., Levi, D. M. & Klein, S.A. Spatial uncertainty and sampling efficiency in amblyopic position acuity. Vision Res. 38, 1239–1251 (1998).

    Article  CAS  Google Scholar 

  9. Levi, D. M., Klein, S. A. & Sharma, V. Position jitter and undersampling in pattern perception. Vision Res. 39, 445–465 (1999).

    Article  CAS  Google Scholar 

  10. Pylyshyn, Z. et al. Multiple parallel access in visual attention. Can. J. Exp. Psychol. 48, 260–283 (1994).

    Article  CAS  Google Scholar 

  11. Trick, L. M. & Pylyshyn, Z.W. Why are small and large numbers enumerated differently? A limited-capacity preattentive stage in vision. Psychol. Rev. 101, 80–102 (1994).

    Article  CAS  Google Scholar 

  12. Jevons, W.S. The power of numerical discrimination. Nature 3, 281–282 (1871).

  13. Atkinson, J., Campbell, F. W. & Francis, M.R. The magic number 4 ± 0: A new look at visual numerosity judgments. Perception 5, 327–334 (1976)

    Article  CAS  Google Scholar 

  14. Levi, D. M. & Harwerth, R.S. Spatiotemporal interactions in anisometropic and strabismic amblyopia. Invest. Ophthalmol. Vis. Sci. 16, 90–95 (1977).

    CAS  PubMed  Google Scholar 

  15. Hess, R. F. & Howell, E.R. The threshold contrast sensitivity function in strabismic amblyopia: Evidence for a two-type classification. Vision Res. 17, 1049–1055 (1977).

    Article  CAS  Google Scholar 

  16. Bradley, A. & Freeman, R.D. Contrast sensitivity in anisometropic amblyopia. Invest. Ophthalmol. Vis. Sci. 21, 467–476 (1981).

    CAS  PubMed  Google Scholar 

  17. Chino, Y. M., Smith, E. L. 3rd, Yoshida, K., Cheng, H. & Hamamoto, J. Binocular interactions in striate cortical neurons of cats reared with discordant visual inputs. J. Neurosci. 14, 5050–5067 (1994).

    Article  CAS  Google Scholar 

  18. Roelfsema, P. R., Konig, P., Engel, A. K., Sireteanu, R. & Singer, W. Reduced synchronization in the visual cortex of cats with strabismic amblyopia. Eur. J. Neurosci. 6, 1645–1655 (1994).

    Article  CAS  Google Scholar 

  19. Posner, M.I. Orienting of attention. Q. J. Exp. Psychol. 32, 3–26 (1980).

    Article  CAS  Google Scholar 

  20. Eriksen, C. W. & Murphy, T.D. Movement of attentional focus across the visual field: A critical look at the evidence. Percept. Psychophys. 42, 299–305 (1987).

    Article  CAS  Google Scholar 

  21. Nakayama, K. in Visual Coding and Efficiency (ed. Blakemore, C.) 411–422 (Cambridge Univ. Press, Cambridge, 1990).

    Google Scholar 

  22. Lu, Z. L. & Dosher, B. A. External noise distinguishes attention mechanisms. Vision. Res. 38, 1183–1198 (1998).

    Article  CAS  Google Scholar 

  23. Levi, D. M., Waugh, S. J. & Beard, B.L Spatial scale shifts in amblyopia. Vision Res. 34, 3315–3334 (1994).

    Article  CAS  Google Scholar 

  24. Balakrishnan, J. D. & Ashby, F.G. Subitizing: magical numbers or mere superstition? Psychol. Res. 54, 80–90 (1992).

    Article  CAS  Google Scholar 

  25. Sathian, K. et al. Neural evidence linking visual object enumeration and attention. J. Cogn. Neurosci. 11, 36–51 (1999).

    Article  CAS  Google Scholar 

  26. Treisman, A.M. Feature binding, attention and object perception. Phil. Trans. R. Soc. Lond. B Biol. Sci. 353, 1295–1206 (1998).

    Article  CAS  Google Scholar 

  27. Vuilleumier, P. & Rafal, R. "Both" means more than "two": localizing and counting in patients with visuospatial neglect. Nat. Neurosci. 2, 783–784 (1999).

    Article  CAS  Google Scholar 

  28. Hyvarinen, J., Hyvarinen, L. & Linnankoski, I. Modification of parietal association cortex and functional blindness after binocular deprivation in young monkeys. Exp. Brain Res. 42, 1–8 (1981).

    Article  CAS  Google Scholar 

  29. Imamura, K. et al. Reduced activity in the extrastriate visual cortex of individuals with strabismic amblyopia. Neurosci. Lett. 225, 173–176 (1997).

    Article  CAS  Google Scholar 

  30. Kooi, F. L., Toet, A., Tripathy, S. P. & Levi, D. M. The effect of similarity and duration on spatial interaction in peripheral vision. Spat. Vis. 8, 255–279 (1994).

    Article  CAS  Google Scholar 

  31. He, S., Cavanagh, P. & Intriligator, J. Attentional resolution and the locus of visual awareness. Nature 383, 334–337 (1996).

    Article  CAS  Google Scholar 

  32. Watson, A.B. Probability summation over time. Vision Res. 19, 515–522 (1979).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful to Ailene Kim for her help with the ‘missing patches’ experiment and Y. Chino for discussions on an early draft of this paper. This research was supported by research grants R01EY01728 and RO1 EY04776, a Core Center Grant P30EY07551, and short-term training grant T35EY07088 from the National Eye Institute, NIH.

Author information

Author notes

  1. Vineeta Sharma

    Present address: Alcon Laboratories, 6201 South Freeway, Fort Worth, Texas, 76134-2099, USA

Authors and Affiliations

  1. University of Houston, College of Optometry, 4901 Calhoun Blvd., Houston, 77204-6052, Texas, USA

    Vineeta Sharma & Dennis M. Levi

  2. University of California at Berkeley, School of Optometry, Berkeley, 94720-2020, California, USA

    Stanley A. Klein

Authors
  1. Vineeta Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dennis M. Levi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Stanley A. Klein
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dennis M. Levi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sharma, V., Levi, D. & Klein, S. Undercounting features and missing features: evidence for a high-level deficit in strabismic amblyopia. Nat Neurosci 3, 496–501 (2000). https://doi.org/10.1038/74872

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/74872

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