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Neural mechanisms mediating responses to abutting gratings: Luminance edges vs. illusory contours

Published online by Cambridge University Press:  24 April 2006

YUNING SONG
Affiliation:
McGill Vision Research Unit, Department of Ophthalmology, McGill University, Montréal, Québec, Canada
CURTIS L. BAKER
Affiliation:
McGill Vision Research Unit, Department of Ophthalmology, McGill University, Montréal, Québec, Canada

Abstract

The discontinuities of phase-shifted abutting line gratings give rise to perception of an “illusory contour” (IC) along the line terminations. Neuronal responses to such ICs have been interpreted as evidence for a specialized visual mechanism, since such responses cannot be predicted from conventional linear receptive fields. However, when the spatial scale of the component gratings (carriers) is large compared to the neuron's luminance passband, these IC responses might be evoked simply by the luminance edges at the line terminations. Thus by presenting abutting gratings at a series of carrier spatial scales to cat A18 neurons, we were able to distinguish genuine nonlinear responses from those due to luminance edges. Around half of the neurons (both simple and complex types) showed a bimodal response pattern to abutting gratings: one peak at a low carrier spatial frequency range that overlapped with the luminance passband, and a second distinct peak at much higher frequencies beyond the neuron's grating resolution. For those bimodally responding neurons, the low-frequency responses were sensitive to carrier phase, but the high-frequency responses were phase-invariant. Thus the responses at low carrier spatial frequencies could be understood via a linear model, while the higher frequency responses represented genuine nonlinear IC processing. IC responsive neurons also demonstrated somewhat lower spatial preference to the periodic contours (envelopes) compared to gratings, but the optimal orientation and motion direction for both were quite similar. The nonlinear responses to ICs could be explained by the same energy mechanism underlying responses to second-order stimuli such as contrast-modulated gratings. Similar neuronal preferences for ICs and for gratings may contribute to the form-cue invariant perception of moving contours.

Type
Research Article
Copyright
2006 Cambridge University Press

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References

REFERENCES

Albright, T.D. (1992). Form-cue invariant motion processing in primate visual cortex. Science 225, 11411143.CrossRefGoogle Scholar
Arsenault, S.A., Wilkinson, F., & Kingdom, F.A.A. (1999). Modulation frequency and orientation tuning of second-order texture mechanisms. Journal of the Optical Society of America A 16, 427435.CrossRefGoogle Scholar
Baker, C.L. (1999). Central neural mechanisms for detecting second-order motion. Current Opinion in Neurobiology 9, 461466.CrossRefGoogle Scholar
Bergen, J.R. & Landy, M.S. (1991). Computational modelling of visual texture segregation. In Computational Models of Visual Processing, ed. Landy, M.S. & Movshon, J.A., pp. 253271. Cambridge, Massachusetts: MIT Press.
Brainard, D.H. (1997). The Psychophysics Toolbox. Spatial Vision 10, 433436.CrossRefGoogle Scholar
Chubb, C. & Sperling, G. (1988). Drift-balanced random stimuli: A general basis for studying non-Fourier motion perception. Journal of the Optical Society of America A 5, 19862007.CrossRefGoogle Scholar
Ferster, D. & Jagadeesh, B. (1991). Nonlinearity of spatial summation in simple cells of areas 17 and 18 of cat visual cortex. Journal of Neurophysiology 66, 16671679.Google Scholar
Graham, N., Beck, J., & Sutter, A. (1992). Nonlinear processes in spatial-frequency channel models of perceived segregation: Effects of sign and amount of contrast. Vision Research 32, 719743.CrossRefGoogle Scholar
Graham, N. & Sutter, A. (1998). Spatial summation in simple (Fourier) and complex (no-Fourier) texture channels. Vision Research 38, 231257.CrossRefGoogle Scholar
Grosof, D.H., Shapley, R.M., Hawken, M.J. (1993). Macaque V1 neurons can signal “illusory” contours. Nature 365, 550552.CrossRefGoogle Scholar
Grossberg, S. & Mingolla, E. (1985). Neural dynamics of form perception: Boundary completion, illusory figures, and neon color spreading. Psychological Review 92, 173211.CrossRefGoogle Scholar
Horridge, G.A., Zhang, S.W., & O'Carroll, D. (1992). Insect perception of illusory contours. Philosophical Transactions of the Royal Society B (London) 337, 5964.CrossRefGoogle Scholar
Hubel, D.H. & Wiesel, T.N. (1962). Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. Journal of Physiology 160, 106154.CrossRefGoogle Scholar
Jones, J.P. & Palmer, L.A. (1987). The two-dimensional spatial structure of simple receptive fields in cat striate cortex. Journal of Neurophysiology 58, 11871211.Google Scholar
Kennedy, J.M. (1978). Illusory contours and the ends of lines. Perception 7, 605607.CrossRefGoogle Scholar
Kingdom, F.A.A., Keeble, D., & Moulden, B. (1995). Sensitivity to orientation modulation in micropattern-based textures. Vision Research 35, 7991.CrossRefGoogle Scholar
Kingdom, F.A.A., Prins, N., & Hayes, A. (2003). Mechanism independence for texture-modulation detection is consistent with a filter-rectify-filter mechanism. Visual Neuroscience 20, 6576.CrossRefGoogle Scholar
Landy, M.S. & Bergen, J.R. (1991). Texture segregation and orientation gradient. Vision Research 31, 679691.CrossRefGoogle Scholar
Leventhal, A.G., Wang, Y., Schmolesky, M.T., & Zhou, Y. (1998). Neural correlates of boundary perception. Visual Neuroscience 15, 11071118.CrossRefGoogle Scholar
Malik, J. & Perona, P. (1990). Preattentive texture discrimination with early vision mechanisms. Journal of the Optical Society of America A 7, 923932.CrossRefGoogle Scholar
Mareschal, I. & Baker, C.L., Jr. (1998). A cortical locus for the processing of contrast-defined contours. Nature Neuroscience 1, 150154.CrossRefGoogle Scholar
Mareschal, I. & Baker, C.L., Jr. (1999). Cortical processing of second-order motion. Visual Neuroscience 16, 527540.CrossRefGoogle Scholar
Marida, K.V. (1972). Statistics of Directional Data. New York: Academic Press.
Movshon, J.A., Thompson, I.D., & Tolhurst, D.J. (1978). Spatial and temporal contrast sensitivity of neurones in areas 17 and 18 of the cat's visual cortex. Journal of Physiology 283, 101120.CrossRefGoogle Scholar
Nieder, A. (2002). Seeing more than meets the eye: Processing of illusory contours in animals. Journal of Comparative Physiology 188, 249260.CrossRefGoogle Scholar
Nieder, A. & Wagner, H. (1999). Perception and neuronal coding of subjective contours in the owl. Nature Neuroscience 2, 660663.CrossRefGoogle Scholar
Pei, X., Vidyasagar, T.R., Volgushev, M., & Creutzfeldt, O.D. (1994). Receptive field analysis and orientation selectivity of postsynaptic potentials of simple cells in cat visual cortex. Journal of Neuroscience 14, 71307140.Google Scholar
Peirce, J.W. & Lennie, P. (2002) ‘Illusory contour’ responses in early visual cortex explained by linear mechanisms. Program no. 456.4. 2002 Abstract Viewer/Itinerary Planner. Washington, DC: Society for Neuroscience. Online.
Pelli, D.G. (1997). The VideoToolbox software for visual psychophysics: Transforming numbers into movies. Spatial Vision 10, 437442.CrossRefGoogle Scholar
Pessoa, L., Thompson, E., & Noe, A. (1998). Finding out about filling-in: A guide to perceptual completion for visual science and the philosophy of perception. Behavioral and Brain Sciences 21, 723748.CrossRefGoogle Scholar
Peterhans, E. (1997). Functional organization of Area V2 in the awake monkey. In Cerebral Cortex, ed. Rockland, K.S., Kaas, J.H. & Peters, A., pp. 335357. New York: Plenum Press.CrossRef
Prins, N. & Kingdom, F.A.A. (2003). Detection and discrimination of texture modulations defined by orientation, frequency and contrast. Journal of the Optical Society of America A 20, 401410.CrossRefGoogle Scholar
Ramsden, B.M., Hung, C.P., & Roe, A.W. (2001). Real and illusory contour processing in area V1 of the primate: A cortical balancing act. Cerebral Cortex 11, 648665.CrossRefGoogle Scholar
Redies, C., Crook, J.M., & Creutzfeldt, O.D. (1986). Neuronal responses to borders with and without luminance gradients in cat visual cortex and dorsal lateral geniculate nucleus. Experimental Brain Research 61, 469481.Google Scholar
Ringach, D.L., Hawken, M.J., & Shapley, R. (1997). Dynamics of orientation tuning in macaque primary visual cortex. Nature 387, 281284.CrossRefGoogle Scholar
Sheth, B.R., Sharma, J., Rao, S.C., & Sur, M. (1996). Orientation maps of subjective contours in visual cortex. Science 274, 21102115.CrossRefGoogle Scholar
Skottun, B.C. (1994). Illusory contours and linear filters. Experimental Brain Research 100, 360364.CrossRefGoogle Scholar
Skottun, B.C., De Valois, R.L., Grosof, D.H., Movshon, J.A., Albrecht, D.G., & Bonds, A.B. (1991). Classifying simple and complex cells on the basis of response modulation. Vision Research 31, 10791086.Google Scholar
Song, Y. & Baker, C.L. (2004a). A common mechanism underlying neuronal processing of contrast envelopes and illusory contours [Abstract]. Journal of Vision 4, 66a, http://journalofvision.org/4/8/66/, doi:10.1167/4.8.66.CrossRefGoogle Scholar
Song, Y. & Baker, C.L. (2004b). A cortical locus for form-cue invariant boundary perception. Program no. 986.1. Abstract Viewer/Itinerary Planner. Washington, DC: Society for Neuroscience. Online.
Soriano, M., Spillmann, L., & Bach, M. (1996). The abutting grating illusion. Vision Research 36, 109116.CrossRefGoogle Scholar
Spitzer, H. & Hochstein, S. (1985a). A complex cell receptive field model. Journal of Neurophysiology 53, 12811301.Google Scholar
Spitzer, H. & Hochstein, S. (1985b). Simple- and complex-cell response dependences on stimulation parameters. Journal of Neurophysiology 53, 12441265.Google Scholar
Sutter, A. & Graham, N. (1995). Investigating simple and complex mechanisms in texture segregation using speed-accuracy trade-off method. Vision Research 35, 28252843.CrossRefGoogle Scholar
von der Heydt, R. & Peterhans, E. (1989). Mechanisms of contour perception in monkey visual cortex. I. Lines of pattern discontinuity. Journal of Neuroscience 9, 17311748.Google Scholar
von der Heydt, R., Peterhans, E., & Baumgartner, G. (1984). Illusory contours and cortical neuron responses. Science 224, 12601262.CrossRefGoogle Scholar
Westheimer, G. & Li, W. (1996). Classifying illusory contours by means of orientation discrimination. Journal of Neurophysiology 75, 523537.Google Scholar
Wilson, H.R. (1999). Non-Fourier cortical processes in texture, form, and motion perception. In Cerebral Cortex: Models of Cortical Circuitry, ed. Ulinski, P.S. & Jones, E.G., pp. 445477. New York: Kluwer Academic/Plenum.CrossRef
Wilson, H.R. & Richards, W.A. (1992). Curvature and separation discrimination at texture boundaries. Journal of the Optical Society of America A 9, 16531662.CrossRefGoogle Scholar
Wilson, H.R. & Wilkinson, F. (1998). Detection of global structure in glass patterns: Implications for form vision. Vision Research 38, 29332947.CrossRefGoogle Scholar
Wilson, H.R., Wilkinson, F., & Asaad, W. (1997). Concentric orientation summation in human form vision. Vision Research 37, 23252330.CrossRefGoogle Scholar
Zhan, C. & Baker, C.L., Jr. (2004). Critical spatial frequencies for illusory contour processing in early visual cortex. Program no. 986.2. Abstract Viewer/Itinerary Planner. Washington, DC: Society for Neuroscience. Online.
Zhan, C.A. & Baker, C.L., Jr. (2006). Boundary cue invariance in cortical orientation maps. Cerebral Cortex, in press.Google Scholar
Zhou, Y.F., Jia, F., Tao, H.Y., & Shou, T.D. (2001). The responses to illusory contours of neurons in cortex areas 17 and 18 of the cats. Science in China Series C-Life Sciences 44, 136145.CrossRefGoogle Scholar
Zhou, Y.X. & Baker, C.L., Jr. (1993). A processing stream in mammalian visual cortex neurons for non-Fourier responses. Science 261, 98101.CrossRefGoogle Scholar
Zhou, Y.X. & Baker, C.L., Jr. (1996). Spatial properties of envelope-responsive cells in area 17 and 18 neurons of the cat. Journal of Neurophysiology 75, 10381050.Google Scholar