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A functional circuitry for edge-induced brightness perception

Nature Neuroscience volume 10, pages 1185–1190 (2007)Cite this article

Abstract

The identification of visual contours and surfaces is central to visual scene segmentation. One view of image construction argues that object contours are first identified and then surfaces are filled in. Although there are psychophysical and single-unit data to suggest that the filling-in view is correct, the underlying circuitry is unknown. Here we examine specific spike-timing relationships between border and surface responses in cat visual cortical areas 17 and 18. With both real and illusory (Cornsweet) brightness contrast stimuli, we found a border-to-surface shift in the relative timing of spike activity. This shift was absent when borders were absent and could be reversed with relocation of the stimulus border, indicating that the direction of information flow is highly dependent on stimulus conditions. Furthermore, this effect was seen predominantly in 17–18, and not 17–17, interactions. These results demonstrate a border-to-surface mechanism at early stages of visual processing and emphasize the importance of interareal circuitry in vision.

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Figure 1: Real and illusory brightness stimuli.
Figure 2: Examples of changes in spike timing interactions for 17–17 and 17-18 cell pairs with in-phase and antiphase relationships.
Figure 3: Example of reversal of peak position with border swap.
Figure 4: Peak center-of-mass positions are shifted in the border-to-surface direction.
Figure 5: Interactions are strengthened for 17–18 in-phase pairs.

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References

  1. Cornsweet, T.N. Visual Perception (Academic, New York, 1970).

    Google Scholar 

  2. Mumford, D., Kosslyn, S.M., Hillger, L.A. & Herrnstein, R.J. Discriminating figure from ground: the role of edge detection and region growing. Proc. Natl. Acad. Sci. USA 84, 7354–7358 (1987).

    Article  CAS  PubMed  Google Scholar 

  3. Adelson, E.H. Perceptual organization and the judgment of brightness. Science 262, 2042–2044 (1993).

    Article  CAS  PubMed  Google Scholar 

  4. Anderson, B.L. & Winawer, J. Image segmentation and lightness perception. Nature 434, 79–83 (2005).

    Article  CAS  PubMed  Google Scholar 

  5. Zucker, S.W. in The Encyclopedia of Artificial Intelligence (ed. Shapiro, S.) (John Wiley, New York, 1986).

    Google Scholar 

  6. Elder, J.H. & Zucker, S.W. Evidence for boundary-specific grouping. Vision Res. 38, 143–152 (1998).

    Article  CAS  PubMed  Google Scholar 

  7. Grossberg, S. & Hong, S. A neural model of surface perception: lightness, anchoring, and filling-in. Spat Vis. 19, 263–321 (2006).

    Article  PubMed  Google Scholar 

  8. Blakeslee, B., Pasieka, W. & McCourt, M.E. Oriented multiscale spatial filtering and contrast normalization: a parsimonious model of brightness induction in a continuum of stimuli including White, Howe and simultaneous brightness contrast. Vision Res. 45, 607–615 (2005).

    Article  PubMed  Google Scholar 

  9. Dakin, S.C. & Bex, P.J. Natural image statistics mediate brightness 'filling in'. Proc. Biol. Sci. 270, 2341–2348 (2003).

    Article  PubMed  PubMed Central  Google Scholar 

  10. Purves, D., Shimpi, A. & Lotto, R.B. An empirical explanation of the Cornsweet effect. J. Neurosci. 19, 8542–8551 (1999).

    Article  CAS  PubMed  Google Scholar 

  11. Komatsu, H., Kinoshita, M. & Murakami, I. Responses in the retinotopic representation of the blind spot in the macaque V1 to stimuli for perceptual filling-in. J. Neurosci. 20, 9310–9319 (2000).

    Article  CAS  PubMed  Google Scholar 

  12. Pessoa, L., Thompson, E. & Noë, A. Finding out about filling-in: a guide to perceptual completion for visual science and the philosophy of perception. Behav. Brain Sci. 21, 723–748 discussion 748–802 (1998).

    CAS  PubMed  Google Scholar 

  13. Komatsu, H. Surface representation by population coding. Behav. Brain Sci. 21, 761–762 (1998).

    Article  Google Scholar 

  14. Davey, M.P., Maddess, T. & Srinivasan, M.V. The spatiotemporal properties of the Craik-O'Brien-Cornsweet effect are consistent with 'filling-in'. Vision Res. 38, 2037–2046 (1998).

    Article  CAS  PubMed  Google Scholar 

  15. Paradiso, M.A. & Hahn, S. Filling-in percepts produced by luminance modulation. Vision Res. 36, 2657–2663 (1996).

    Article  CAS  PubMed  Google Scholar 

  16. Paradiso, M.A. Visual neuroscience: illuminating the dark corners. Curr. Biol. 10, R15–R18 (2000).

    Article  CAS  PubMed  Google Scholar 

  17. De Weerd, P., Gattass, R., Desimone, R. & Ungerleider, L.G. Responses of cells in monkey visual cortex during perceptual filling-in of an artificial scotoma. Nature 377, 731–734 (1995).

    Article  CAS  PubMed  Google Scholar 

  18. Rossi, A.F., Rittenhouse, C.D. & Paradiso, M.A. The representation of brightness in primary visual cortex. Science 273, 1104–1107 (1996).

    Article  CAS  PubMed  Google Scholar 

  19. Lamme, V.A.F., Rodriguez-Rodriguez, V. & Spekreijse, H. Separate processing dynamics for texture elements, boundaries and surfaces in primary visual cortex of the macaque monkey. Cereb. Cortex. 9, 406–413 (1999).

    Article  CAS  PubMed  Google Scholar 

  20. Hung, C.P., Ramsden, B.M., Chen, L.M. & Roe, A.W. Building surfaces from borders in areas 17 and 18 of the cat. Vision Res. 41, 1389–1407 (2001).

    Article  CAS  PubMed  Google Scholar 

  21. Roe, A.W., Lu, H.D. & Hung, C.P. Cortical processing of a brightness illusion. Proc. Natl. Acad. Sci. USA 102, 3869–3874 (2005).

    Article  CAS  PubMed  Google Scholar 

  22. Bonhoeffer, T., Kim, D-S., Malonek, D., Shoham, D. & Grinvald, A. Optical imaging of the layout of functional domains in area 17 and across the area 17/18 border in cat visual cortex. Eur. J. Neurosci. 7, 1973–1988 (1995).

    Article  CAS  PubMed  Google Scholar 

  23. Bredfeldt, C.E. & Ringach, D.L. Dynamics of spatial frequency tuning in macaque V1. J. Neurosci. 22, 1976–1984 (2002).

    Article  CAS  PubMed  Google Scholar 

  24. Cavanaugh, J.R., Bair, W. & Movshon, J.A. Nature and interaction of signals from the receptive field center and surround in macaque v1 neurons. J. Neurophysiol. 88, 2530–2546 (2002).

    Article  PubMed  Google Scholar 

  25. DeAngelis, G.C., Freeman, R.D. & Ohzawa, I. Length and width tuning of neurons in the cat's primary visual cortex. J. Neurophysiol. 71, 347–374 (1994).

    Article  CAS  PubMed  Google Scholar 

  26. Ferster, D. & Jagadeesh, B. Nonlinearity of spatial summation in simple cells of areas 17 and 18 of cat visual cortex. J. Neurophysiol. 66, 1667–1679 (1991).

    Article  CAS  PubMed  Google Scholar 

  27. Issa, N.P., Trepel, C. & Stryker, M.P. Spatial frequency maps in cat visual cortex. J. Neurosci. 20, 8504–8514 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Shoham, D., Hubener, M., Schulze, S., Grinvald, A. & Bonhoeffer, T. Spatio-temporal frequency domains and their relation to cytochrome oxidase staining in cat visual cortex. Nature 385, 529–533 (1997).

    Article  CAS  PubMed  Google Scholar 

  29. Zhou, H., Friedman, H.S. & von der Heydt, R. Coding of border ownership in monkey visual cortex. J. Neurosci. 20, 6594–6611 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Sceniak, M.P., Ringach, D.L., Hawken, M.J. & Shapley, R. Contrast's effect on spatial summation by macaque V1 neurons. Nat. Neurosci. 2, 733–739 (1999).

    Article  CAS  PubMed  Google Scholar 

  31. Rossi, A.F., Desimone, R. & Ungerleider, L.G. Contextual modulation in primary visual cortex of macaques. J. Neurosci. 21, 1698–1709 (2001).

    Article  CAS  PubMed  Google Scholar 

  32. Reid, R.C. & Alonso, J.M. Specificity of monosynaptic connections from thalamus to visual cortex. Nature 378, 281–284 (1995).

    Article  CAS  PubMed  Google Scholar 

  33. Bullier, J. & Henry, G.H. Neural path taken by afferent streams in striate cortex of the cat. J. Neurophysiol. 42, 1264–1270 (1979).

    Article  CAS  PubMed  Google Scholar 

  34. Givre, S.J., Schroeder, C.E. & Arezzo, J.C. Contribution of extrastriate area V4 to the surface-recorded flash VEP in the awake macaque. Vision Res. 34, 415–428 (1994).

    Article  CAS  PubMed  Google Scholar 

  35. Schyns, P.G. & Oliva, A. From blobs to boundary edges: evidence for time- and spatial-scale–dependent scene recognition. Psychol. Sci. 5, 195–200 (1994).

    Article  Google Scholar 

  36. Burr, D.C. Implications of the Craik-O'Brien illusion for brightness perception. Vision Res. 27, 1903–1913 (1987).

    Article  CAS  PubMed  Google Scholar 

  37. Hung, C.P., Ramsden, B.M. & Roe, A.W. Weakly modulated spike trains: significance, precision and correction for sample size. J. Neurophysiol. 87, 2542–2554 (2002).

    Article  PubMed  Google Scholar 

  38. Nowak, L.G., Munk, M.H.J., Nelson, J.I., James, A.C. & Bullier, J. Structural basis of cortical synchronization. I. Three types of interhemispheric coupling. J. Neurophysiol. 74, 2379–2400 (1995).

    Article  CAS  PubMed  Google Scholar 

  39. Alonso, J.-M. & Martinez, L.M. Functional connectivity between simple cells and complex cells in cat striate cortex. Nat. Neurosci. 1, 395–403 (1998).

    Article  CAS  PubMed  Google Scholar 

  40. Das, A. & Gilbert, C.D. Topography of contextual modulations mediated by short-range interactions in primary visual cortex. Nature 399, 655–661 (1999).

    Article  CAS  PubMed  Google Scholar 

  41. Siegel, M. & Konig, P. A functional gamma-band defined by stimulus-dependent synchronization in area 18 of awake behaving cats. J. Neurosci. 23, 4251–4260 (2003).

    Article  CAS  PubMed  Google Scholar 

  42. Singer, W. Neuronal synchrony: a versatile code for the definition of relations? Neuron 24, 49–65 111–25 (1999).

    Article  CAS  Google Scholar 

  43. Ts'o, D.Y., Gilbert, C.D. & Wiesel, T.N. Relationships between horizontal interactions and functional architecture in cat striate cortex as revealed by cross-correlation analysis. J. Neurosci. 6, 1160–1170 (1986).

    Article  CAS  PubMed  Google Scholar 

  44. Brody, C.D. Correlations without synchrony. Neural Comput. 11, 1537–1551 (1999).

    Article  CAS  PubMed  Google Scholar 

  45. Kinoshita, M. & Komatsu, H. Neural representation of the luminance and brightness of a uniform surface in the macaque primary visual cortex. J. Neurophysiol. 86, 2559–2570 (2001).

    Article  CAS  PubMed  Google Scholar 

  46. MacEvoy, S.P., Kim, W. & Paradiso, M.A. Integration of surface information in primary visual cortex. Nat. Neurosci. 1, 616–620 (1998).

    Article  CAS  PubMed  Google Scholar 

  47. Bravo, M., Blake, R. & Morrison, S. Cats see subjective contours. Vision Res. 28, 861–865 (1988).

    Article  CAS  PubMed  Google Scholar 

  48. De Weerd, P., Sprague, J.M., Raiguel, S., Vandenbussche, E. & Orban, G.A. Effects of visual cortex lesions on orientation discrimination of illusory contours in the cat. Eur. J. Neurosci. 5, 1695–1710 (1993).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We wish to thank F.L. Healy for technical assistance, Y.-T. Wu for statistical support and S.-S. Huang for helpful discussions. We also thank E.H. Adelson, G. Kreiman and H. Op de Beeck for helpful comments on an earlier version of the manuscript. The project was supported by US National Institutes of Health grants EY-11744, NEI 5T32 EY-07115, 5T32 DA-07290 and RR-15574, the Whitehall Foundation, Packard Foundation, Yale Brown-Coxe Postdoctoral Fellowship, Taiwan Ministry of Education Five Year Aim for the Top University Plan, and the Taiwan National Science Council and Ministry of Education Outstanding Scholar Fellowship 95-2819-B-010-001.

Author information

Authors and Affiliations

  1. Institute of Neuroscience and Brain Research Center, 155 Sec. 2 Li-Nong St., National Yang Ming University, Taipei, 112, Taiwan

    Chou P Hung

  2. Department of Neurobiology and Anatomy, Sensory Neuroscience Research Center, West Virginia University School of Medicine, Morgantown, 26506, West Virginia, USA

    Benjamin M Ramsden

  3. Department of Psychology, Vanderbilt University, 301 Wilson Hall, Nashville, 37203, Tennessee, USA

    Anna Wang Roe

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  1. Chou P Hung
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  2. Benjamin M Ramsden
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Contributions

C.P.H. and A.W.R. designed the experiments. C.P.H., B.M.R. and A.W.R. carried out the experiments and wrote the paper. C.P.H. analyzed the results.

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Correspondence to Anna Wang Roe.

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The authors declare no competing financial interests.

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Supplementary Figures 1-4, Tables 1-5, Methods (PDF 1331 kb)

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Hung, C., Ramsden, B. & Roe, A. A functional circuitry for edge-induced brightness perception. Nat Neurosci 10, 1185–1190 (2007). https://doi.org/10.1038/nn1948

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