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:

Eye-specific effects of binocular rivalry in the human lateral geniculate nucleus

Nature volume 438, pages 496–499 (2005)Cite this article

Abstract

When dissimilar images are presented to the two eyes, they compete for perceptual dominance so that each image is visible in turn for a few seconds while the other is suppressed. Such binocular rivalry is associated with relative suppression of local, eye-based representations1,2,3,4 that can also be modulated by high-level influences such as perceptual grouping3,5,6. However, it is currently unclear how early in visual processing the suppression of eye-based signals can occur. Here we use high-resolution functional magnetic resonance imaging (fMRI) in conjunction with a new binocular rivalry stimulus to show that signals recorded from the human lateral geniculate nucleus (LGN) exhibit eye-specific suppression during rivalry. Regions of the LGN that show strong eye-preference independently show strongly reduced activity during binocular rivalry when the stimulus presented in their preferred eye is perceptually suppressed. The human LGN is thus the earliest stage of visual processing that reflects eye-specific dominance and suppression.

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: Ocular biases in the LGN.
Figure 2: Binocular rivalry stimulus.
Figure 3: Rivalry-related responses in LGN and V1.
Figure 4: Percept preference in LGN and V1.

Similar content being viewed by others

References

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

    Article  CAS  Google Scholar 

  2. Blake, R., Westendorf, D. & Overton, R. What is suppressed during binocular rivalry? Perception 9, 223–231 (1980)

    Article  CAS  Google Scholar 

  3. Lee, S. & Blake, R. A fresh look at interocular grouping during binocular rivalry. Vision Res. 44, 983–991 (2004)

    Article  Google Scholar 

  4. Lehky, S. R. An astable multivibrator model of binocular rivalry. Perception 17, 215–228 (1988)

    Article  CAS  Google Scholar 

  5. Kovacs, I., Papathomas, T. V., Yang, M. & Feher, A. When the brain changes its mind: interocular grouping during binocular rivalry. Proc. Natl Acad. Sci. USA 93, 15508–15511 (1996)

    Article  ADS  CAS  Google Scholar 

  6. Logothetis, N. K., Leopold, D. A. & Sheinberg, D. L. What is rivalling during binocular rivalry? Nature 380, 621–624 (1996)

    Article  ADS  CAS  Google Scholar 

  7. 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 

  8. Schroeder, C. E., Tenke, C. E., Arezzo, J. C. & Vaughan, H. G. Binocularity in the lateral geniculate nucleus of the alert monkey. Brain Res. 521, 303–310 (1990)

    Article  CAS  Google Scholar 

  9. Varela, F. J. & Singer, W. Neuronal dynamics in the visual corticothalamic pathway revealed through binocular rivalry. Exp. Brain Res. 66, 10–20 (1987)

    Article  CAS  Google Scholar 

  10. 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  Google Scholar 

  11. Lehky, S. R. & Maunsell, J. H. R. No binocular rivalry in the LGN of alert macaque monkeys. Vision Res. 36, 1225–1234 (1996)

    Article  CAS  Google Scholar 

  12. Haynes, J. D. & Rees, G. Predicting the orientation of invisible stimuli from activity in primary visual cortex. Nature Neurosci. 8, 686–691 (2005)

    Article  CAS  Google Scholar 

  13. Kamitani, Y. & Tong, F. Decoding the visual and subjective contents of the human brain. Nature Neurosci. 8, 679–685 (2005)

    Article  CAS  Google Scholar 

  14. Levelt, W. J. Note on the distribution of dominance times in binocular rivalry. Br. J. Psychol. 58, 143–145 (1967)

    Article  CAS  Google Scholar 

  15. Schneider, K. A., Richter, M. C. & Kastner, S. Retinotopic organization and functional subdivisions of the human lateral geniculate nucleus: a high-resolution functional magnetic resonance imaging study. J. Neurosci. 24, 8975–8985 (2004)

    Article  CAS  Google Scholar 

  16. Sclar, G., Maunsell, J. H. & Lennie, P. Coding of image contrast in central visual pathways of the macaque monkey. Vision Res. 31, 1148–1157 (1990)

    Google Scholar 

  17. Tong, F. & Engel, S. A. Interocular rivalry revealed in the human cortical blind-spot representation. Nature 411, 195–199 (2001)

    Article  ADS  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  19. Lee, S. H., Blake, R. & Heeger, D. J. Traveling waves of activity in primary visual cortex during binocular rivalry. Nature Neurosci. 8, 22–23 (2005)

    Article  CAS  Google Scholar 

  20. Lee, S. H. & Blake, R. V1 activity is reduced during binocular rivalry. J. Vis. 2, 618–626 (2002)

    Article  Google Scholar 

  21. Logothetis, N. K. & Wandell, B. A. Interpreting the BOLD signal. Annu. Rev. Physiol. 66, 735–769 (2004)

    Article  CAS  Google Scholar 

  22. Andrews, T. J. Binocular rivalry and visual awareness. Trends Cogn. Sci. 5, 407–409 (2001)

    Article  Google Scholar 

  23. Wales, R. & Fox, R. Increment detection thresholds during binocular rivalry suppression. Percept. Psychophys. 8, 827–835 (1970)

    Article  Google Scholar 

  24. Watanabe, K., Paik, Y. & Blake, R. Preserved gain control for luminance contrast during binocular rivalry suppression. Vision Res. 44, 3065–3071 (2004)

    Article  Google Scholar 

  25. Sobel, K. V., Blake, R. & Raissian, T. A. Binocular rivalry suppression does impede buildup of the motion aftereffect. J. Vis. 4, Abstract 243 (2004)

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

    Article  ADS  CAS  Google Scholar 

  27. Fang, F. & He, S. Cortical responses to invisible objects in the human dorsal and ventral pathways. Nature Neurosci. advance online publication, 4 September 2005 (doi:10.1038/nn1537).

  28. Ichida, J. M. & Casagrande, V. A. Organization of the feedback pathway from striate cortex (V1) to the lateral geniculate nucleus (LGN) in the owl monkey (Aotus trivirgatus). J. Comp. Neurol. 454, 272–283 (2002)

    Article  Google Scholar 

  29. Singer, W. Control of thalamic transmission by corticofugal and ascending reticular pathways in the visual system. Physiol. Rev. 57, 386–420 (1977)

    Article  CAS  Google Scholar 

  30. Montero, V. & Zempel, J. The proportion and size of GABA-immunoreactive neurons in magnocellular and parvocellular layers of the lateral geniculate nucleus of the monkey. Exp. Brain Res. 62, 215–223 (1986)

    Article  CAS  Google Scholar 

  31. Kastner, S. et al. Functional imaging of the human lateral geniculate nucleus and pulvinar. J. Neurophysiol. 91, 438–448 (2002)

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by the Wellcome Trust. We thank J. Driver and P. Sterzer for comments, and E. Freeman for advice regarding the stimuli. Author Contributions J.-D.H. and G.R. conceived the experiment, R.D. wrote the pulse sequence and J.-D.H. carried out the experiment and data analysis. G.R., J.-D.H. and R.D. co-wrote the paper.

Author information

Authors and Affiliations

  1. Wellcome Department of Imaging Neuroscience, Institute of Neurology, University College London, 12 Queen Square, WC1N 3BG, London, UK

    John-Dylan Haynes, Ralf Deichmann & Geraint Rees

  2. Institute of Cognitive Neuroscience, University College London, Alexandra House, 17 Queen Square, WC1N 3AR, London, UK

    John-Dylan Haynes & Geraint Rees

Authors
  1. John-Dylan Haynes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ralf Deichmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Geraint Rees
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to John-Dylan Haynes.

Ethics declarations

Competing interests

Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Supplementary information

Supplementary Figure S1

Distribution of ocular biases in LGN and V1 under monocular viewing conditions. (DOC 60 kb)

Supplementary Figure S2

Event-related BOLD-fMRI signal changes time-locked to rivalry transitions for individual subjects. (DOC 113 kb)

Supplementary Figure S3

Results of control experiment with monocular stimulation. (DOC 42 kb)

Supplementary Figure S4

Correlation between percept-preference and eye-selectivity. (DOC 64 kb)

Supplementary Methods

Additional description of Methods used in this study that could not be included in the main text. (DOC 30 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Haynes, JD., Deichmann, R. & Rees, G. Eye-specific effects of binocular rivalry in the human lateral geniculate nucleus. Nature 438, 496–499 (2005). https://doi.org/10.1038/nature04169

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature04169

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