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:

Optimal transsaccadic integration explains distorted spatial perception

Nature volume 422, pages 76–80 (2003)Cite this article

Abstract

We scan our surroundings with quick eye movements called saccades, and from the resulting sequence of images we build a unified percept by a process known as transsaccadic integration. This integration is often said to be flawed, because around the time of saccades, our perception is distorted1,2,3,4,5,6 and we show saccadic suppression of displacement (SSD): we fail to notice if objects change location during the eye movement7,8. Here we show that transsaccadic integration works by optimal inference. We simulated a visuomotor system with realistic saccades, retinal acuity, motion detectors and eye-position sense, and programmed it to make optimal use of these imperfect data when interpreting scenes. This optimized model showed human-like SSD and distortions of spatial perception. It made new predictions, including tight correlations between perception and motor action (for example, more SSD in people with less-precise eye control) and a graded contraction of perceived jumps; we verified these predictions experimentally. Our results suggest that the brain constructs its evolving picture of the world by optimally integrating each new piece of sensory or motor information.

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: Predicted and actual saccadic suppression of displacement (SSD).
Figure 2: Perception and motor control.
Figure 3: Contraction of perceived jumps.

Similar content being viewed by others

References

  1. Matin, L. & Pearce, D. G. Visual perception of direction for stimuli flashed during voluntary saccadic eye movements. Science 148, 1485–1488 (1965)

    Article  ADS  CAS  Google Scholar 

  2. Honda, H. Saccade-contingent displacement of the apparent position of visual stimuli flashed on a dimly illuminated structured background. Vision Res. 33, 709–716 (1993)

    Article  CAS  Google Scholar 

  3. Ross, J., Morrone, M. C. & Burr, D. C. Compression of space before saccades. Nature 386, 598–601 (1997)

    Article  ADS  CAS  Google Scholar 

  4. Morrone, M. C., Ross, R. & Burr, D. C. Apparent position of visual targets during real and simulated saccadic eye movements. J. Neurosci. 17, 7941–7953 (1997)

    Article  CAS  Google Scholar 

  5. Cai, R. H., Pouget, A., Schlag-Rey, M. & Schlag, J. Perceived geometrical relationships affected by eye-movement signals. Nature 386, 601–604 (1997)

    Article  ADS  CAS  Google Scholar 

  6. Lappe, M., Awater, H. & Krekelberg, B. Postsaccadic visual references generate presaccadic compression of space. Nature 403, 892–895 (2000)

    Article  ADS  CAS  Google Scholar 

  7. Mack, A. An investigation of the relationship between eye and retinal image movement in the perception of movement. Percept. Psychophys. 8, 291–298 (1970)

    Article  Google Scholar 

  8. Bridgeman, B., Hendry, D. & Stark, L. Failure to detect displacement of the visual world during saccadic eye movements. Vision Res. 15, 719–722 (1975)

    Article  CAS  Google Scholar 

  9. Westheimer, G. Spatial vision. Annu. Rev. Psychol. 35, 201–226 (1984)

    Article  CAS  Google Scholar 

  10. Carpenter, R. H. S. in Vision and Visual Dysfunctions (ed. Carpenter, R. H. S.) 1–10 (Macmillan, Boca Raton, 1991)

    Google Scholar 

  11. Choudhury, B. P. & Crossey, A. D. Slow-movement sensitivity in the human field of vision. Physiol. Behav. 26, 125–128 (1981)

    Article  CAS  Google Scholar 

  12. Tynan, P. D. & Sekuler, R. Motion processing in peripheral vision: Reaction time and perceived velocity. Vision Res. 22, 61–68 (1982)

    Article  CAS  Google Scholar 

  13. Burr, D. C., Holt, J., Johnstone, J. R. & Ross, J. Selective depression of motion sensitivity during saccades. J. Physiol. (Lond.) 333, 1–15 (1982)

    Article  CAS  Google Scholar 

  14. Burr, D. C., Morrone, M. C. & Ross, J. Selective suppression of the magnocellular visual pathway during saccadic eye movements. Nature 371, 511–513 (1994)

    Article  ADS  CAS  Google Scholar 

  15. Shiori, S. & Cavanagh, P. Saccadic suppression of low-level motion. Vision Res. 29, 915–928 (1989)

    Article  Google Scholar 

  16. Ilg, U. & Hoffmann, K.-P. Motion perception during saccades. Vision Res. 33, 211–220 (1993)

    Article  CAS  Google Scholar 

  17. Steinbach, M. J. Proprioceptive knowledge of eye position. Vision Res. 27, 1737–1744 (1986)

    Article  Google Scholar 

  18. von Helmholtz, H. Handbuch der physiologischen Optik (Leopold Voss, Hamburg and Leipzig, 1910)

    MATH  Google Scholar 

  19. von Holst, E. & Mittelstaedt, H. Das Reafferenzprinzip (Wechselwirkung zwischen Zentralnervensystem und Peripherie). Naturwissenschaften 37, 464–476 (1950)

    Article  ADS  Google Scholar 

  20. Sperry, R. W. Neural basis of the spontaneous optokinetic response produced by visual inversion. J. Comp. Physiol. Psychol. 43, 482–489 (1950)

    Article  CAS  Google Scholar 

  21. Dassonville, P., Schlag, J. & Schlag-Rey, M. Oculomotor localization relies on a dampened representation of saccadic eye movement displacement in human and nonhuman primates. Vis. Neurosci. 9, 261–269 (1992)

    Article  CAS  Google Scholar 

  22. Honda, H. Interaction of extraretinal eye position signals in a double-step saccade task: Psychophysical estimation. Exp. Brain Res. 113, 327–336 (1997)

    Article  CAS  Google Scholar 

  23. Li, W. & Matin, L. The influence of saccade length on the saccadic suppression of displacement detection. Percept. Psychophys. 48, 453–458 (1990)

    Article  CAS  Google Scholar 

  24. Li, W. & Matin, L. Saccadic suppression of displacement: Separate influences of saccade size and of target retinal eccentricity. Vision Res. 37, 1779–1797 (1997)

    Article  CAS  Google Scholar 

  25. Gysen, V., De Graef, P. & Verfaillie, K. Detection of intrasaccadic displacements and depth rotations of moving objects. Vision Res. 42, 379–391 (2002)

    Article  Google Scholar 

  26. Deubel, H., Schneider, W. X. & Bridgeman, B. Postsaccadic target blanking prevents saccadic suppression of image displacement. Vision Res. 36, 985–996 (1996)

    Article  CAS  Google Scholar 

  27. Bridgeman, B., Van der Heijden, A. H. C. & Velichovsky, B. M. A theory of visual stability across saccadic eye movements. Behav. Brain Sci. 17, 247–292 (1994)

    Article  Google Scholar 

  28. MacKay, D. M. in Handbook of Sensory Physiology Vol. VII/3 (ed. Jung, R.) 307–332 (Springer, Berlin, 1973)

    Google Scholar 

  29. Van Opstal, A. J. & Van Gisbergen, J. A. M. Scatter in the metrics of saccades and properties of the collicular motor map. Vision Res. 29, 1183–1196 (1989)

    Article  CAS  Google Scholar 

  30. Kontsevich, L. L. & Tyler, C. W. Bayesian adaptive estimation of psychometric slope and threshold. Vision Res. 39, 2729–2737 (1999)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank S. Sun for invaluable programming, H. Wang for help with experiments, and I. Frenkel, P. Hallett, C. Hawkins, D. Henriques, E. Klier, J. C. Martinez Trujillo, P. Medendorp and K. Schreiber for comments on the manuscript. This study was supported by the Canadian Institutes for Health Research. J.D.C. is supported by the Canadian Research Chair Program.

Author information

Authors and Affiliations

  1. Departments of Physiology and Medicine, University of Toronto, 1 King's College Circle, M5S 1A8, Toronto, Canada

    Matthias Niemeier & Douglas B. Tweed

  2. Canadian Institutes of Health Research, Group for Action and Perception,

    Matthias Niemeier, J. Douglas Crawford & Douglas B. Tweed

  3. Centre for Vision Research, York University, 4700 Keele Street, M3J 1P3, Toronto, Canada

    Matthias Niemeier, J. Douglas Crawford & Douglas B. Tweed

Authors
  1. Matthias Niemeier
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. Douglas Crawford
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Douglas B. Tweed
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Douglas B. Tweed.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Cite this article

Niemeier, M., Crawford, J. & Tweed, D. Optimal transsaccadic integration explains distorted spatial perception. Nature 422, 76–80 (2003). https://doi.org/10.1038/nature01439

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature01439

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

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