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Spatial characteristics of the second-order visual pathway revealed by positional adaptation

Nature Neuroscience volume 2, pages 479–484 (1999)Cite this article

Abstract

The visual system is thought to process luminance (first-order) and contrast (second-order) information by dedicated cortical streams. To explore the spatial characteristics of the second-order pathway, we examined the effect of adaptation on spatial localization in human subjects. We show that, unlike first-order adaptation, second-order positional adaptation via cortical mechanisms transfers across orientations but not across spatial frequencies. These results support physiological evidence that these two processing streams are distinct and suggest that the cortical mechanism mediating second-order positional adaptation maintains spatial frequency information but sums signals across orientations.

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Figure 1: Demonstration of positional adaptation for first-order stimuli.
Figure 2: Demonstration of positional adaptation for second-order stimuli.
Figure 3: Orientation crossover at three different carrier spatial frequencies.
Figure 4: Spatial frequency crossover.
Figure 5: Spatial frequency bandwidths for positional adaptation.

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References

  1. Hubel, D. H. & Wiesel, T. N. Receptive fields, binocular interaction, and functional architecture in the cat's visual cortex. J. Physiol. (Lond.) 160, 106–154 ( 1962).

    Article  CAS  Google Scholar 

  2. Movshon, J. A., Thompson, I. A. & Tollhurst, D. J. Spatial summation in the receptive fields of simple cells in the cat's striate cortex. J. Physiol. (Lond.) 283, 53–77 (1978).

    Article  CAS  Google Scholar 

  3. Spitzer, H. & Hochstein, S. Simple- and complex-cell response dependences on stimulation parameters. J. Neurophysiol. 53, 1244–1265 (1985).

    Article  CAS  Google Scholar 

  4. Shapley, R. M. & Lennie, P. Spatial frequency analysis in the visual system. Annu. Rev. Neurosci. 8, 547 –583 (1985).

    Article  CAS  Google Scholar 

  5. von der Heydt, R. & Peterhans, E. Mechanisms of contour perception in monkey visual cortex. I. Lines of pattern discontinuity. J. Neurosci. 9, 1731–1748 (1989).

    Article  CAS  Google Scholar 

  6. von der Heydt, R. & Peterhans, E. & Dursteler, M. R. Periodic-pattern-selective cells in monkey visual cortex. J. Neurosci. 12, 1416–1434 (1992).

    Article  CAS  Google Scholar 

  7. Merigan, W. H., Nealey, T.A & Maunsell, J. H. Visual effects of lesions of cortical area V2 in macaques. J. Neurosci. 13, 3180– 3191 (1993).

    Article  CAS  Google Scholar 

  8. Shapley, R. M. Visual cortex: pushing the envelope. Nat. Neurosci. 1, 95–96 (1998).

    Article  CAS  Google Scholar 

  9. Li-Ming, L. & Wilson, H. R. Fourier and non-Fourier pattern discrimination. Vision Res. 36, 1907– 1918 (1996).

    Article  Google Scholar 

  10. Chubb, C. & Sperling, G. Drift-balanced random stimuli: A general basis for studying non-Fourier motion perception. J. Opt. Soc. Am. A 5, 1986–2007 (1988).

    Article  CAS  Google Scholar 

  11. Turano, K. & Pantle, A. On the mechanism that encodes the movement of contrast variations: Velocity discrimination. Vision Res. 29, 207–221 ( 1974).

    Article  Google Scholar 

  12. Derrington, A. M., Badcock, D. R. & Henning, G. B. Discriminating the direction of second-order motion at short stimulus durations. Vision Res. 33, 1785–1794 (1993).

    Article  CAS  Google Scholar 

  13. Ledgeway, T. & Smith, A. T. Evidence for separate motion-detecting mechanisms for first- and second-order motion in human vision. Vision Res. 34, 2727–2740 (1994).

    Article  CAS  Google Scholar 

  14. Vaina, L. M., Makris, N., Kennedy, D. & Cowey, A. The selective impairment of the perception of first-order motion by unilateral brain damage. Vis. Neurosci. 15, 333–348 (1998).

    Article  CAS  Google Scholar 

  15. Zhou, Y.-X. & Baker, C. L. A processing stream in mammalian visual cortex neurons for non-Fourier responses. Science 261, 98–101 (1993).

    Article  CAS  Google Scholar 

  16. Morgan, M. J. & Hotopf, W. H. Perceived diagonals in grids and lattices. Vision Res. 29, 1005– 1015 (1989).

    Article  CAS  Google Scholar 

  17. Victor, J. D. & Conte, M. M. Spatial organization of nonlinear interactions in form perception. Vision Res. 31, 1457–1488 (1991).

    Article  CAS  Google Scholar 

  18. Graham, N., Beck, J. & Sutter, A. Nonlinear processes in spatial-frequency channel models of perceived texture segregation: effects of sign and amount of contrast. Vision Res. 32, 719–743 (1992).

    Article  CAS  Google Scholar 

  19. Levi, D. M. & Waugh, S. J. Position acuity with opposite-contrast polarity features: evidence for a nonlinear collector mechanism for position acuity. Vision Res. 36, 573– 588 (1996).

    Article  CAS  Google Scholar 

  20. Olavarria, J. F., DeYoe, E. A., Knierim, J. J., Fox, J. M. & Van Essen, D. C. Neural responses to visual texture patterns in the middle temporal area of the macaque monkey. J. Neurophysiol. 68, 164–181 (1992).

    Article  CAS  Google Scholar 

  21. Shapley, R. M. in Higher-Order Processing in the Visual System. Ciba Foundation Symposia 71–87 (Wiley, New York, 1994).

    Google Scholar 

  22. Mareschal, I. & Baker, C. L. A cortical locus for the processing of contrast-defined contours. Nat. Neurosci. 1, 150–154 (1998).

    Article  CAS  Google Scholar 

  23. Pantle, A. & Sekuler, R. Size detecting mechanisms in human vision. Science 162, 1146– 1148 (1968).

    Article  CAS  Google Scholar 

  24. Blakemore, C. & Campbell, F. W. On the existence of neurons in the human visual system selectively sensitive to the orientation and size of retinal images. J. Physiol. (Lond.) 203, 237–260 (1969).

    Article  CAS  Google Scholar 

  25. Gibson, J. J. & Radner, M. Adaptation, aftereffect, and contrast in the perception of tilted lines. I. Quantitative studies. J. Exp. Psychol. 20, 453–467 (1937).

    Article  Google Scholar 

  26. Moulden, B., Renshaw, J. & Mather, G. Two channels for flicker in the human visual system. Perception 13, 387–400 (1984).

    Article  CAS  Google Scholar 

  27. McCollough, C. Color adaptation of edge detectors in the human visual system. Science 149, 1113–1114 ( 1965).

    Article  Google Scholar 

  28. Pantle, A. Motion aftereffect magnitude as a measure of spatiotemporal response properties of direction-selective analysers. Vision Res. 14, 1229–1236 (1974).

    Article  CAS  Google Scholar 

  29. Whitaker, D., McGraw, P. V. & Levi, D. M. The influence of adaptation on perceived visual location. Vision Res. 37, 2207–2216 (1997).

    Article  CAS  Google Scholar 

  30. Sutherland, N. S. Figural after-effects and apparent size. J. Exp. Psychol. 13, 222–228 (1961).

    Article  Google Scholar 

  31. Mareschal, I. & Baker, C. L. Temporal and spatial response to second-order stimuli in cat area 18. J. Neurophysiol. 80, 2811–2823 (1998).

    Article  CAS  Google Scholar 

  32. Burton, G. J. Evidence for non-linear response process in the visual system from measurements on the thresholds of spatial beat frequencies. Vision Res. 13, 1211–1255 (1973).

    Article  CAS  Google Scholar 

  33. Henning, G. B., Hertz, G. B. & Broadbent, D. E. Some experiments bearing on the hypothesis that the visual system analyses patterns in independent bands of spatial frequency. Vision Res. 15, 887–897 (1975).

    Article  CAS  Google Scholar 

  34. Nachmias, J. N. & Rogowitz, B. E. Masking by spatially modulated gratings. Vision Res. 23, 1621–1629 (1983).

    Article  CAS  Google Scholar 

  35. Derrington, A. M. & Badcock, D. R. Detecting spatial beats: non-linearity or contrast increment detection? Vision Res. 27, 343–348 ( 1986).

    Article  Google Scholar 

  36. Klein, S. A. & Levi, D. M. Hyperacuity thresholds of 1 sec: Theoretical predictions and empirical validation. J. Opt. Soc. Am. A 2, 1170–1190 ( 1985).

    Article  CAS  Google Scholar 

  37. Wilson, H. R. Responses of spatial mechanisms can explain hyperacuity. Vision Res. 26, 453–469 ( 1986).

    Article  CAS  Google Scholar 

  38. Georgeson, M. A. Human vision combines oriented filters to compute edges. Proc. R. Soc. Lond. B 249, 235–245 (1992).

    Article  CAS  Google Scholar 

  39. Thomas, J. P. & Olzak, L. A. Uncertainty experiments support the roles of second-order mechanisms in spatial frequency and orientation discriminations. J. Opt. Soc. Am. A 13, 689–696 (1996).

    Article  CAS  Google Scholar 

  40. Nothdurft, H. C. in Structural and Functional Organization of the Neocortex (eds. Albowitz, B., Albus, K., Kuhnt, U., Nothdurft, H. C. & Wahle, P.) 375–384 (Springer, Berlin, 1994).

    Google Scholar 

  41. Sagi, D. in Early Vision and Beyond (eds. Papathomas, T. V., Chubb, C., Gorea, A. & Kowler, E.) 69–78 (MIT Press, Cambridge, Massachusetts, 1995).

    Google Scholar 

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Acknowledgements

P.V.M. is supported by a Vision Research Training Fellowship from the Wellcome Trust. D.M.L. is supported by grant RO1EY01728 from the National Eye Institute, NIH, Bethesda, Maryland.

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Authors and Affiliations

  1. Department of Optometry, University of Bradford, Richmond Road, Bradford, BD7 1DP, UK

    Paul V. McGraw & David Whitaker

  2. College of Optometry, University of Houston, Calhoun Boulevard, Houston, 77204-6052, Texas, USA

    Dennis M. Levi

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  1. Paul V. McGraw
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  2. Dennis M. Levi
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  3. David Whitaker
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Correspondence to Paul V. McGraw.

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McGraw, P., Levi, D. & Whitaker, D. Spatial characteristics of the second-order visual pathway revealed by positional adaptation. Nat Neurosci 2, 479–484 (1999). https://doi.org/10.1038/8150

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