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.

  • Letter
  • Published:

Responses of primary visual cortical neurons to binocular disparity without depth perception

Abstract

The identification of brain regions that are associated with the conscious perception of visual stimuli is a major goal in neuroscience1. Here we present a test of whether the signals on neurons in cortical area V1 correspond directly to our conscious perception of binocular stereoscopic depth. Depth perception requires that image features on one retina are first matched with appropriate features on the other retina. The mechanisms that perform this matching can be examined by using random-dot stereograms2, in which the left and right eyes view randomly positioned but binocularly correlated dots. We exploit the fact that anticorrelated random-dot stereograms (in which dots in one eye are matched geometrically to dots of the opposite contrast in the other eye) do not give rise to the perception of depth3 because the matching process does not find a consistent solution. Anticorrelated random-dot stereograms contain binocular features that could excite neurons that have not solved the correspondence problem. We demonstrate that disparity-selective neurons in V1 signal the disparity of anticorrelated random-dot stereograms, indicating that they do not unambiguously signal stereoscopic depth. Hence single V1 neurons cannot account for the conscious perception of stereopsis, although combining the outputs of many V1 neurons could solve the matching problem. The accompanying paper4 suggests an additional function for disparity signals from V1: they may be important for the rapid involuntary control of vergence eye movements (eye movements that bring the images on the two foveae into register).

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

Access options

Buy this article

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

Figure 1: Example stereograms.
Figure 2: Responses of a model complex cell to RDS.
Figure 3: Responses of two complex neurons to disparity in correlated (filled symbols) and anticorrelated (open symbols) dynamic RDS.
Figure 4: Summary of effect of stimulus anticorrelation on the disparity selectivity of 72 cells.

Similar content being viewed by others

References

  1. Crick, F. & Koch, C. Are we aware of neural activity in primary visual cortex? Nature 375, 121–123 (1995).

    Article  ADS  CAS  Google Scholar 

  2. Julesz, B. Foundations of Cyclopean Perception(University of Chicago Press, (1971).

    Google Scholar 

  3. Cogan, A. I., Lomakin, A. J. & Rossi, A. Depth in anticorrelated stereograms. Vision Res. 33, 1959–1975 (1993).

    Article  CAS  Google Scholar 

  4. Masson, G. S., Busettini, C. & Miles, F. A. Vergence eye movements in response to binocular disparity without depth perception. Nature 389, 283–286 (1997).

    Article  ADS  CAS  Google Scholar 

  5. Marr, D. & Poggio, T. Acomputatonal theory of human stereo vision. Proc. R. Soc. Lond. B 204, 301–328 (1979).

    Article  ADS  CAS  Google Scholar 

  6. Grimson, W. E. L. Acomputer implementation of a theory of human stereo vision. Phil. Trans. R. Soc. Lond. B 292, 217–253 (1981).

    Article  ADS  CAS  Google Scholar 

  7. Barlow, H. B., Blakemore, C. & Pettigrew, J. D. The neural mechanisms of binocular depth discrimination. J. Physiol. (Lond.) 193, 327–342 (1967).

    Article  CAS  Google Scholar 

  8. Nikara, T., Bishop, P. O. & Pettigrew, J. D. Analysis of retinal correspondence by studying receptive fields of binocular single units in cat striate cortex. Exp. Brain Res. 6, 353–372 (1968).

    Article  CAS  Google Scholar 

  9. Poggio, G., Motter, B. C., Squatrito, S. & Trotter, Y. Responses of neurons in visual cortex (V1 and V2) of the alert macaque to dynamic random dot stereograms. Vision Res. 25, 397–405 (1985).

    Article  CAS  Google Scholar 

  10. Ohzawa, I., DeAngelis, G. C. & Freeman, R. D. Stereoscopic depth discrimination in the visual cortex: Neurons ideally suited as disparity detectors. Science 249, 1037–1041 (1990).

    Article  ADS  CAS  Google Scholar 

  11. Qian, N. Computing stereo disparity and motion with known binocular properties. Neural Computat. 6, 390–404 (1994).

    Article  Google Scholar 

  12. Poggio, G. F., Gonzalez, F. & Krause, F. Stereoscopic mechanisms in monkey visual cortex: binocular correlation and disparity selectivity. J. Neurosci. 8, 4531–4550 (1988).

    Article  CAS  Google Scholar 

  13. Poggio, G. & Poggio, T. The analysis of stereopsis. Annu. Rev. Neurosci. 7, 379–412 (1984).

    Article  CAS  Google Scholar 

  14. Poggio, G. F. & Fisher, B. Binocular interactions and depth sensitivity in striate and prestriate cortex of behaving rhesus monkey. J. Neurophysiol. 40, 1392–1405 (1977).

    Article  CAS  Google Scholar 

  15. Poggio, G. Mechanisms of stereopsis in monkey visual cortex. Cerebr. Cort. 3, 193–204 (1995).

    Article  Google Scholar 

  16. Judge, S. J., Richmond, B. J. & Chu, F. C. Implantation of magnetic search coils for measurement of eye position: an improved method. Vision Res. 30, 535–538 (1980).

    Article  Google Scholar 

  17. Skottun, B. C. et al. Classifying simple and complex cells on the basis of response modulation. Vision Res. 31, 1079–1086 (1991).

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the Wellcome Trust and the Royal Society.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to B. G. Cumming.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cumming, B., Parker, A. Responses of primary visual cortical neurons to binocular disparity without depth perception. Nature 389, 280–283 (1997). https://doi.org/10.1038/38487

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/38487

This article is cited by

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.

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