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:

Continuous flash suppression reduces negative afterimages

Abstract

Illusions that produce perceptual suppression despite constant retinal input are used to manipulate visual consciousness. Here we report on a powerful variant of existing techniques, continuous flash suppression. Distinct images flashed successively at 10 Hz into one eye reliably suppress an image presented to the other eye. The duration of perceptual suppression is at least ten times greater than that produced by binocular rivalry. Using this tool we show that the strength of the negative afterimage of an adaptor was reduced by half when it was perceptually suppressed by input from the other eye. The more completely the adaptor was suppressed, the more strongly the afterimage intensity was reduced. Paradoxically, trial-to-trial visibility of the adaptor did not correlate with the degree of reduction. Our results imply that formation of afterimages involves neuronal structures that access input from both eyes but that do not correspond directly to the neuronal correlates of perceptual awareness.

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: Continuous flash suppression.
Figure 2: CFS suppresses a Gabor patch and reduces its afterimage.
Figure 3: Mondrian flashes themselves do not reduce the afterimage of the Gabor.
Figure 4: Relationship between afterimage reduction and the reliability of suppression.
Figure 5: Visibility and afterimage reduction.

Similar content being viewed by others

References

  1. Koch, C. The Quest for Consciousness: A Neurobiological Approach (Roberts, Greenwood Village, Colorado, 2004).

    Google Scholar 

  2. Blake, R. & Fox, R. Adaptation to invisible gratings and the site of binocular rivalry suppression. Nature 249, 488–490 (1974).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  4. Rajimehr, R. Unconscious orientation processing. Neuron 41, 663–673 (2004).

    Article  CAS  PubMed  Google Scholar 

  5. Hofstoetter, C., Koch, C. & Kiper, D.C. Motion-induced blindness does not affect the formation of negative afterimages. Conscious. Cogn. 13, 691–708 (2004).

    Article  PubMed  Google Scholar 

  6. Macknik, S.L. & Martinez-Conde, S. Dichoptic visual masking reveals that early binocular neurons exhibit weak interocular suppression: implications for binocular vision and visual awareness. J. Cogn. Neurosci. 16, 1049–1059 (2004).

    Article  PubMed  Google Scholar 

  7. Rees, G., Russell, C., Frith, C.D. & Driver, J. Inattentional blindness versus inattentional amnesia for fixated but ignored words. Science 286, 2504–2507 (1999).

    Article  CAS  PubMed  Google Scholar 

  8. Bonneh, Y.S., Cooperman, A. & Sagi, D. Motion-induced blindness in normal observers. Nature 411, 798–801 (2001).

    Article  CAS  PubMed  Google Scholar 

  9. Logothetis, N.K. & Schall, J.D. Neuronal correlates of subjective visual perception. Science 245, 761–763 (1989).

    Article  CAS  PubMed  Google Scholar 

  10. Leopold, D.A. & Logothetis, N.K. Activity changes in early visual cortex reflect monkeys' percepts during binocular rivalry. Nature 379, 549–553 (1996).

    Article  CAS  PubMed  Google Scholar 

  11. Sheinberg, D.L. & Logothetis, N.K. The role of temporal cortical areas in perceptual organization. Proc. Natl. Acad. Sci. USA 94, 3408–3413 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Lumer, E.D., Friston, K.J. & Rees, G. Neural correlates of perceptual rivalry in the human brain. Science 280, 1930–1934 (1998).

    Article  CAS  PubMed  Google Scholar 

  13. Tong, F., Nakayama, K., Vaughan, J.T. & Kanwisher, N. Binocular rivalry and visual awareness in human extrastriate cortex. Neuron 21, 753–759 (1998).

    Article  CAS  PubMed  Google Scholar 

  14. Polonsky, A., Blake, R., Braun, J. & Heeger, D.J. Neuronal activity in human primary visual cortex correlates with perception during binocular rivalry. Nat. Neurosci. 3, 1153–1159 (2000).

    Article  CAS  PubMed  Google Scholar 

  15. Pasley, B.N., Mayes, L.C. & Schultz, R.T. Subcortical discrimination of unperceived objects during binocular rivalry. Neuron 42, 163–172 (2004).

    Article  CAS  PubMed  Google Scholar 

  16. Williams, M.A., Morris, A.P., McGlone, F., Abbott, D.F. & Mattingley, J.B. Amygdala responses to fearful and happy facial expressions under conditions of binocular suppression. J. Neurosci. 24, 2898–2904 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Wolfe, J.M. Reversing ocular dominance and suppression in a single flash. Vision Res. 24, 471–478 (1984).

    Article  CAS  PubMed  Google Scholar 

  18. Kreiman, G., Fried, I. & Koch, C. Single-neuron correlates of subjective vision in the human medial temporal lobe. Proc. Natl. Acad. Sci. USA 99, 8378–8383 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Wilke, M., Logothetis, N.K. & Leopold, D.A. Generalized flash suppression of salient visual targets. Neuron 39, 1043–1052 (2003).

    Article  CAS  PubMed  Google Scholar 

  20. Lack, L.C. Selective Attention and the Control of Binocular Rivalry 117–169 (Mouton, The Hague, The Netherlands, 1978).

  21. Wiesenfelder, H. & Blake, R. The neural site of binocular rivalry relative to the analysis of motion in the human visual system. J. Neurosci. 10, 3880–3888 (1990).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Blake, R. Psychoanatomical strategies for studying human visual perception. in Early Vision and Beyond (eds. Papathomas, T.V., Chubb, C., Gorea, A., & Kowler, E.) 17–25 (M.I.T. Press, Cambridge, Massachusetts, 1995).

    Google Scholar 

  23. Moradi, F., Koch, C. & Shimojo, S. Face adaptation depends on seeing the face. Neuron 45, 169–175 (2005).

    Article  CAS  PubMed  Google Scholar 

  24. Blake, R. & Logothetis, N.K. Visual competition. Nat. Rev. Neurosci. 3, 13–21 (2002).

    Article  CAS  PubMed  Google Scholar 

  25. Alpern, M. & Barr, L. Durations of the after-images of brief light flashes and the theory of the Broca and Sulzer phenomenon. J. Opt. Soc. Am. 52, 219–221 (1962).

    Article  CAS  PubMed  Google Scholar 

  26. Brindley, G.S. Two new properties of foveal after-images and a photochemical hypothesis to explain them. J. Physiol. (Lond.) 164, 168–179 (1962).

    Article  CAS  Google Scholar 

  27. Loomis, J.M. The photopigment bleaching hypothesis of complementary after-images: a psychophysical test. Vision Res. 12, 1587–1594 (1972).

    Article  CAS  PubMed  Google Scholar 

  28. Loomis, J.M. Complementary afterimages and the unequal adapting effects of steady and flickering light. J. Opt. Soc. Am. 68, 411–416 (1978).

    Article  CAS  PubMed  Google Scholar 

  29. Virsu, V. & Laurinen, P. Long-lasting afterimages caused by neural adaptation. Vision Res. 17, 853–860 (1977).

    Article  CAS  PubMed  Google Scholar 

  30. Sakitt, B. Psychophysical correlates of photoreceptor activity. Vision Res. 16, 129–140 (1976).

    Article  CAS  PubMed  Google Scholar 

  31. Wilson, H.R. A neural model of foveal light adaptation and afterimage formation. Vis. Neurosci. 14, 403–423 (1997).

    Article  CAS  PubMed  Google Scholar 

  32. Kelly, D.H. & Martinez-Uriegas, E. Measurements of chromatic and achromatic afterimages. J. Opt. Soc. Am. A 10, 29–37 (1993).

    Article  CAS  PubMed  Google Scholar 

  33. Craik, K.J.W. Origin of visual after-images. Nature 145, 512 (1940).

    Article  Google Scholar 

  34. Shimojo, S., Kamitani, Y. & Nishida, S. Afterimage of perceptually filled-in surface. Science 293, 1677–1680 (2001).

    Article  CAS  PubMed  Google Scholar 

  35. Breese, B.B. On Inhibition. Psychol. Monogr. 3, 1–65 (1899).

    Article  Google Scholar 

  36. Levelt, W.J.M. On Binocular Rivalry (Institute for Perception RVO-TNO, Soesterberg, The Netherlands, 1965).

    Google Scholar 

  37. Fox, R. & Rasche, F. Binocular rivalry and reciprocal inhibition. Percept. Psychophys. 5, 215–217 (1969).

    Article  Google Scholar 

  38. Bossink, C.J., Stalmeier, P.F. & De Weert, C.M. A test of Levelt's second proposition for binocular rivalry. Vision Res. 33, 1413–1419 (1993).

    Article  CAS  PubMed  Google Scholar 

  39. Anstis, S., Rogers, B. & Henry, J. Interactions between simultaneous contrast and coloured afterimages. Vision Res. 18, 899–911 (1978).

    Article  CAS  PubMed  Google Scholar 

  40. Hayhoe, M.M. & Williams, D.R. Disappearance of afterimages at 'impossible' locations in space. Perception 13, 455–459 (1984).

    Article  CAS  PubMed  Google Scholar 

  41. Suzuki, S. & Grabowecky, M. Attention during adaptation weakens negative afterimages. J. Exp. Psychol. Hum. Percept. Perform. 29, 793–807 (2003).

    Article  PubMed  Google Scholar 

  42. Lou, L. Effects of voluntary attention on structured afterimages. Perception 30, 1439–1448 (2001).

    Article  CAS  PubMed  Google Scholar 

  43. Weiskrantz, L. An unusual case of after-imagery following fixation of an 'imaginary' visual pattern. Q. J. Exp. Psychol. 2, 170–175 (1950).

    Article  Google Scholar 

  44. Sengpiel, F., Blakemore, C. & Harrad, R. Interocular suppression in the primary visual cortex: a possible neural basis of binocular rivalry. Vision Res. 35, 179–195 (1995).

    Article  CAS  PubMed  Google Scholar 

  45. O'Regan, J.K. & Noe, A. A sensorimotor account of vision and visual consciousness. Behav. Brain Sci. 24, 939–73 (2001).

    Article  CAS  PubMed  Google Scholar 

  46. Lamme, V.A. Why visual attention and awareness are different. Trends Cogn. Sci. 7, 12–18 (2003).

    Article  PubMed  Google Scholar 

  47. Chan, D., Crutch, S.J. & Warrington, E.K. A disorder of colour perception associated with abnormal colour after-images: a defect of the primary visual cortex. J. Neurol. Neurosurg. Psychiatry 71, 515–517 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Weiskrantz, L. Prime-sight and blindsight. Conscious. Cogn. 11, 568–581 (2002).

    Article  CAS  PubMed  Google Scholar 

  49. Schiller, P.H. & Dolan, R.P. Visual aftereffects and the consequences of visual system lesions on their perception in the rhesus monkey. Vis. Neurosci. 11, 643–665 (1994).

    Article  CAS  PubMed  Google Scholar 

  50. Brainard, D.H. The Psychophysics Toolbox. Spat. Vis. 10, 433–436 (1997).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank R. Kanai, C. Hofstoetter, D.A. Wu, F. Moradi, R. Van Rullen and S. Shimojo for discussion. This research was funded by grants from the US National Institute of Mental Health, the US National Science Foundation, the Keck Foundation and the Moore Foundation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Naotsugu Tsuchiya.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tsuchiya, N., Koch, C. Continuous flash suppression reduces negative afterimages. Nat Neurosci 8, 1096–1101 (2005). https://doi.org/10.1038/nn1500

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn1500

This article is cited by

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