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Hierarchy of cortical responses underlying binocular rivalry

Abstract

During binocular rivalry, physical stimulation is dissociated from conscious visual awareness. Human brain imaging reveals a tight linkage between the neural events in human primary visual cortex (V1) and the dynamics of perceptual waves during transitions in dominance during binocular rivalry. Here, we report results from experiments in which observers' attention was diverted from the rival stimuli, implying that: competition between two rival stimuli involves neural circuits in V1, and attention is crucial for the consequences of this neural competition to advance to higher visual areas and promote perceptual waves.

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Figure 1: Rival stimuli, percepts and corresponding regions of primary visual cortex (V1).
Figure 2: Temporal sequences of fMRI responses, averaged across trials for one observer in each experimental condition and each visual area.
Figure 3: fMRI response latency differences averaged across observers.
Figure 4: Traveling waves of cortical activity, averaged across four observers, in each visual area.
Figure 5: Control experiments.

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References

  1. 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  Google Scholar 

  2. 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  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  5. Gail, A., Brinksmeyer, H.J. & Eckhorn, R. Perception-related modulations of local field potential power and coherence in primary visual cortex of awake monkey during binocular rivalry. Cereb. Cortex 14, 300–313 (2004).

    Article  Google Scholar 

  6. Haynes, J.D. & Rees, G. Predicting the stream of consciousness from activity in human visual cortex. Curr. Biol. 15, 1301–1307 (2005).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  8. Rees, G., Kreiman, G. & Koch, C. Neural correlates of consciousness in humans. Nat. Rev. Neurosci. 3, 261–270 (2002).

    Article  CAS  Google Scholar 

  9. Tong, F. Primary visual cortex and visual awareness. Nat. Rev. Neurosci. 4, 219–229 (2003).

    Article  CAS  Google Scholar 

  10. Wilson, H.R., Blake, R. & Lee, S.H. Dynamics of travelling waves in visual perception. Nature 412, 907–910 (2001).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  13. Heeger, D.J., Huk, A.C., Geisler, W.S. & Albrecht, D.G. Spikes versus BOLD: what does neuroimaging tell us about neuronal activity? Nat. Neurosci. 3, 631–633 (2000).

    Article  CAS  Google Scholar 

  14. Boynton, G.M., Engel, S.A., Glover, G.H. & Heeger, D.J. Linear systems analysis of functional magnetic resonance imaging in human V1. J. Neurosci. 16, 4207–4221 (1996).

    Article  CAS  Google Scholar 

  15. Nishida, S., Sasaki, Y., Murakami, I., Watanabe, T. & Tootell, R.B. Neuroimaging of direction-selective mechanisms for second-order motion. J. Neurophysiol. 90, 3242–3254 (2003).

    Article  Google Scholar 

  16. Reynolds, J.H. & Chelazzi, L. Attentional modulation of visual processing. Annu. Rev. Neurosci. 27, 611–647 (2004).

    Article  CAS  Google Scholar 

  17. Sasaki, Y. & Watanabe, T. The primary visual cortex fills in color. Proc. Natl. Acad. Sci. USA 101, 18251–18256 (2004).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  19. Tse, P.U., Martinez-Conde, S., Schlegel, A.A. & Macknik, S.L. Visibility, visual awareness, and visual masking of simple unattended targets are confined to areas in the occipital cortex beyond human V1/V2. Proc. Natl. Acad. Sci. USA 102, 17178–17183 (2005).

    Article  CAS  Google Scholar 

  20. Wunderlich, K., Schneider, K.A. & Kastner, S. Neural correlates of binocular rivalry in the human lateral geniculate nucleus. Nat. Neurosci. 8, 1595–1602 (2005).

    Article  CAS  Google Scholar 

  21. Haynes, J.D., Deichmann, R. & Rees, G. Eye-specific effects of binocular rivalry in the human lateral geniculate nucleus. Nature 438, 496–499 (2005).

    Article  CAS  Google Scholar 

  22. Hupe, J.M. et al. Cortical feedback improves discrimination between figure and background by V1, V2 and V3 neurons. Nature 394, 784–787 (1998).

    Article  CAS  Google Scholar 

  23. Lamme, V.A. & Roelfsema, P.R. The distinct modes of vision offered by feedforward and recurrent processing. Trends Neurosci. 23, 571–579 (2000).

    Article  CAS  Google Scholar 

  24. Hupe, J.M. et al. Feedback connections act on the early part of the responses in monkey visual cortex. J. Neurophysiol. 85, 134–145 (2001).

    Article  CAS  Google Scholar 

  25. Haynes, J.D., Tregellas, J. & Rees, G. Attentional integration between anatomically distinct stimulus representations in early visual cortex. Proc. Natl. Acad. Sci. USA 102, 14925–14930 (2005).

    Article  CAS  Google Scholar 

  26. Gross, J. et al. Modulation of long-range neural synchrony reflects temporal limitations of visual attention in humans. Proc. Natl. Acad. Sci. USA 101, 13050–13055 (2004).

    Article  CAS  Google Scholar 

  27. Dehaene, S., Changeux, J.P., Naccache, L., Sackur, J. & Sergent, C. Conscious, preconscious and subliminal processing: a testable taxonomy. Trends Cogn. Sci. 10, 204–211 (2006).

    Article  Google Scholar 

  28. Wilson, H.R. Computational evidence for a rivalry hierarchy in vision. Proc. Natl. Acad. Sci. USA 100, 14499–14503 (2003).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  30. Nguyen, V.A., Freeman, A.W. & Wenderoth, P. The depth and selectivity of suppression in binocular rivalry. Percept. Psychophys. 63, 348–360 (2001).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  32. Lee, S.H. & Blake, R. Rival ideas about binocular rivalry. Vision Res. 39, 1447–1454 (1999).

    Article  CAS  Google Scholar 

  33. 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  CAS  Google Scholar 

  34. Leopold, D.A. & Logothetis, N.K. Multistable phenomena: changing views in perception. Trends Cogn. Sci. 3, 254–264 (1999).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  36. Malach, R., Amir, Y., Harel, M. & Grinvald, A. Relationship between intrinsic connections and functional architecture revealed by optical imaging and in vivo targeted biocytin injections in primate striate cortex. Proc. Natl. Acad. Sci. USA 90, 10469–10473 (1993).

    Article  CAS  Google Scholar 

  37. Gilbert, C.D., Das, A., Ito, M., Kapadia, M. & Westheimer, G. Spatial integration and cortical dynamics. Proc. Natl. Acad. Sci. USA 93, 615–622 (1996).

    Article  CAS  Google Scholar 

  38. Angelucci, A. et al. Circuits for local and global signal integration in primary visual cortex. J. Neurosci. 22, 8633–8646 (2002).

    Article  CAS  Google Scholar 

  39. Stettler, D.D., Das, A., Bennett, J. & Gilbert, C.D. Lateral connectivity and contextual interactions in macaque primary visual cortex. Neuron 36, 739–750 (2002).

    Article  CAS  Google Scholar 

  40. VanRullen, R. & Koch, C. Is perception discrete or continuous? Trends Cogn. Sci. 7, 207–213 (2003).

    Article  Google Scholar 

  41. Glover, G.H. Simple analytic spiral K-space algorithm. Magn. Reson. Med. 42, 412–415 (1999).

    Article  CAS  Google Scholar 

  42. Nestares, O. & Heeger, D.J. Robust multiresolution alignment of MRI brain volumes. Magn. Reson. Med. 43, 705–715 (2000).

    Article  CAS  Google Scholar 

  43. Sperling, G. & Melchner, M.J. The attention operating characteristic: examples from visual search. Science 202, 315–318 (1978).

    Article  CAS  Google Scholar 

  44. Engel, S.A. et al. fMRI of human visual cortex. Nature 369, 525 (1994).

    Article  CAS  Google Scholar 

  45. Sereno, M.I. et al. Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. Science 268, 889–893 (1995).

    Article  CAS  Google Scholar 

  46. Efron, B. Bootstrap confidence intervals for a class of parametric problems. Biometrika 72, 45–58 (1985).

    Article  Google Scholar 

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Acknowledgements

We thank N. Logothetis, C. Koch, R. Marois, M. Landy, F. Tong, M. Carrasco, T. Movshon and the late F. Crick for comments on earlier drafts of the manuscript. This work was supported by grants from the US National Institutes of Health to D.J.H. (R01-EY12741 and R01-EY16752) and to R.B. (R03-EY14437 and R01-EY13356), and a grant from the Brain Research Center of 21st Century Frontier Research Program funded by the Ministry of Science and Technology, the Republic of Korea, to S.H.L. (M103KV010018-07K2201-01810). Some of these data were acquired while D.J.H. and S.H.L. were at Stanford University and while R.B. was a visiting scholar at New York University.

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Correspondence to Sang-Hun Lee.

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Lee, SH., Blake, R. & Heeger, D. Hierarchy of cortical responses underlying binocular rivalry. Nat Neurosci 10, 1048–1054 (2007). https://doi.org/10.1038/nn1939

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