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Neuronal responses to edges defined by luminance vs. temporal texture in macaque area V1

Published online by Cambridge University Press:  02 June 2009

Avi Chaudhuri
Affiliation:
Department of Psychology, McGill University, 1205 Dr. Penfield Avenue, Montreal, QC H3A 1B1 Canada.
Thomas D. Albright
Affiliation:
Department of Psychology, McGill University, 1205 Dr. Penfield Avenue, Montreal, QC H3A 1B1 Canada.

Abstract

We examined the responsivity, orientation selectivity, and direction selectivity of a sample of neurons in cortical area V1 of the macaque using visual stimuli consisting of drifting oriented contours defined by each of two very different figural cues: luminance contrast and temporal texture. Comparisons of orientation and direction tuning elicited by the different cues were made in order to test the hypothesis that the neuronal representations of these parameters are form-cue invariant. The majority of the sampled cells responded to both stimulus types, although responses to temporal texture stimuli were generally weaker than those elicited by luminance-defined stimuli. Of those units exhibiting orientation selectivity when tested with the luminance-defined stimuli, more than half were also selective for the orientation of the temporal texture stimuli. There was close correspondence between the preferred orientations and tuning bandwidths revealed with the two stimulus types. Of those units exhibiting directional selectivity when tested with the luminance-defined stimuli, about two-thirds were also selective for the direction of the temporal texture stimuli. There was close correspondence between the preferred directions revealed with the two stimulus types, although bidirectional responses were somewhat more common when temporal texture stimuli were used. These results indicate that many V1 neurons encode orientation and direction of motion of retinal image features in a manner that is largely independent of whether the feature is defined by luminance or temporal texture contrast. These neurons may contribute to perceptual phenomena in which figural cue identity is disregarded.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1997

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References

Adelson, E.A. & Movshon, J.A. (1982). Phenomenal coherence of moving visual patterns. Nature 300, 523525.CrossRefGoogle ScholarPubMed
Albright, T.D. (1984). Direction and orientation selectivity of neurons in visual area MT of the macaque. Journal of Neurophysiology 52, 11061130.CrossRefGoogle ScholarPubMed
Albright, T.D. (1987). Isoluminant motion processing in macaque visual area MT. Society for Neuroscience Abstracts 13, 1626.Google Scholar
Albright, T.D. (1992). Form-cue invariant motion processing in primate visual cortex. Science 255, 11411143.CrossRefGoogle ScholarPubMed
Albright, T.D. (1993). Cortical processing of visual motion. In Visual Motion and Its Use in the Stabilization of Gaze, ed. Wallman, J. & Miles, F.A., pp. 177201. Amsterdam: Elsevier.Google Scholar
Albright, T.D. & Chaudhuri, A. (1989). Orientation selective responses to motion contrast boundaries in macaque VI. Society for Neuroscience Abstracts 15, 323.Google Scholar
Anstis, S.M. (1980). The perception of apparent movement. Philosophical Transactions of the Royal Society B (London) 290, 153168.Google ScholarPubMed
Batschelet, E. (1965). Statistical Methods for the Analysis of Problems in Animal Orientation and Certain Biological Rhythms. American Institute of Biological Sciences, Washington, D.C.Google Scholar
Beck, J. (1966). Perceptual grouping produced by changes in orientation and shape. Science 154, 538540.CrossRefGoogle ScholarPubMed
Bergen, J.R. & Julesz, B. (1983). Parallel versus serial processing in rapid pattern discrimination. Nature 303, 696698.CrossRefGoogle ScholarPubMed
Cavanagh, P. (1987). Reconstructing the third dimension: Interactions between color, texture, motion, binocular disparity, and shape. Computer Vision, Graphics, and Image Processing 37, 171195.CrossRefGoogle Scholar
Cavanagh, P., Arguin, M. & von Grunau, M. (1989). Interattribute apparent motion. Vision Research 29, 11971204.CrossRefGoogle ScholarPubMed
Cavanagh, P. & Leclerc, Y.G. (1989). Shape from shadows. Journal of Experimental Psychology 15, 327.Google ScholarPubMed
Cavanagh, P. & Mather, G. (1989). Motion: The long and short of it. Spatial Vision 4, 103129.Google Scholar
Chao, L.L. (1974). Statistics. Methods and Analyses. London: McGraw-Hill.Google Scholar
Charles, E.R. & Logothetis, N.K. (1989). The responses of middle temporal (MT) neurons to isoluminant stimuli. Investigative Ophthalmology and Visual Science (Suppl.) 30, 427.Google 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 ScholarPubMed
Derrington, A.M. & Lennie, P. (1984). Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. Journal of Physiology (London) 335, 219240.CrossRefGoogle Scholar
DeValois, R.L., Yund, E.W. & Hepler, N. (1982). The orientation and direction selectivity of cells in the macaque visual cortex. Vision Research 22, 531544.CrossRefGoogle Scholar
Dobkins, K.R. & Albright, T.D. (1994). What happens if it changes color when it moves?: The nature of chromatic input to macaque visual area MT. Journal of Neuroscience 14, 48544870.CrossRefGoogle ScholarPubMed
Dow, B.M. (1974). Functional classes of cells and their laminar distribution in monkey visual cortex. Journal of Neurophysiology 37, 927946.CrossRefGoogle ScholarPubMed
Gegenfurtner, K.R., Kiper, D.C., Beusmans, J.M., Carandini, M., Zaidi, Q. & Movshon, J.A. (1994). Chromatic properties of neurons in macaque MT. Visual Neuroscience 11, 455466.CrossRefGoogle ScholarPubMed
Gouras, P. (1974). Opponent-colour cells in different layers of foveal striate cortex. Journal of Physiology (London) 238, 583602.CrossRefGoogle ScholarPubMed
Gouras, P. & Kruger, J. (1979). Responses of cells in foveal visual cortex of the monkey to pure color contrast. Journal of Neurophysiology 42, 850860.CrossRefGoogle ScholarPubMed
Gregory, R.L. (1977). Vision with equiluminant colour contrast: 1. A projection technique and observations. Perception 6, 113119.CrossRefGoogle Scholar
Grosof, D.H., Shapley, R.M. & Hawken, M.J. (1993). Macaque V1 neurons can signal ‘illusory’ contours. Nature 365, 550552.CrossRefGoogle ScholarPubMed
Hawken, M.J., Parker, A.J. & Lund, J.S. (1988). Laminar organization and contrast sensitivity of direction-selective cells in the striate cortex of the old world monkey. Journal of Neuroscience 8, 35413548.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1968). Receptive fields and functional architecture of monkey striate cortex. Journal of Physiology (London) 195, 215243.CrossRefGoogle ScholarPubMed
Judge, S.J., Richmond, B.J. & Chu, F.C. (1980). Implantation of magnetic search coil for measurement of eye position: An improved method. Vision Research 20, 535538.CrossRefGoogle Scholar
Julesz, B. (1971). Foundations of Cyclopean Perception. Chicago, Illinois: University of Chicago Press.Google Scholar
Julesz, B. (1981). Textons, the elements of texture perception, and their interaction. Nature 290, 9597.CrossRefGoogle Scholar
Julesz, B. & Payne, R.A. (1968). Differences between monocular and binocular stroboscopic movement perception. Vision Research 8, 433444.CrossRefGoogle ScholarPubMed
Knierim, J.J. & Van Essen, D.C. (1992). Neuronal responses to static texture patterns in area V1 of the alert macaque monkey. Journal of Neuroscience 67, 961980.Google ScholarPubMed
Koffka, K. (1935). Principles of Gestalt Psychology. New York: Harcourt, Brace.Google Scholar
Krauskopf, J. (1967). Heterochromatic stabilized images: A classroom demonstration. American Journal of Psychology 80, 632637.Google ScholarPubMed
Lelkens, A.M.M. & Koenderink, J.J. (1984). Illusory motion in visual displays. Vision Research 24, 10831090.CrossRefGoogle ScholarPubMed
Lennie, P., Krauskopf, J. & Sclar, G. (1990). Chromatic mechanisms in striate cortex of macaque. Journal of Neuroscience 10, 649669.CrossRefGoogle ScholarPubMed
Livingstone, M.S. & Hubel, D.H. (1984). Anatomy and physiology of a color system in primate primary visual cortex. Journal of Neuroscience 4, 309356.CrossRefGoogle Scholar
Livingstone, M.S. & Hubel, D.H. (1987). Psychophysical evidence for separate channels for the perception of form, color, movement, and depth. Journal of Neuroscience 7, 34163468.CrossRefGoogle ScholarPubMed
Logothetis, N.K. & Charles, E.R. (1990). V4 responses to gratings defined by random dot motion. Investigative Ophthalmology and Visual Science (Suppl.), 31, 90.Google Scholar
Lund, J.S., Lund, R.D., Hendrickson, A.E., Bunt, A.H. & Fuchs, A.F. (1975). The origin of efferent pathways from the primary visual cortex, area 17, of the macaque monkey as shown by retrograde transport of horseradish peroxidase. Journal of Comparative Neurology 164, 287305.CrossRefGoogle ScholarPubMed
Marr, D. (1982). Vision. San Francisco, California: Freeman.Google Scholar
Michael, C.R. (1978). Color vision mechanisms in monkey striate cortex: Dual-opponent cells with concentric receptive fields. Journal of Neurophysiology 41, 572588.CrossRefGoogle ScholarPubMed
Morrone, M.C. & Burr, D.C. (1988). Feature detection in human vision: A phase-dependent energy model. Proceedings of the Royal Society B (London) 235, 221245.Google Scholar
Olavarria, J., DeYoe, E.A., Knierim, J., Fox, J.M. & Van Essen, D.C. (1992). Neural responses to visual texture patterns in middle temporal area of the macaque monkey. Journal of Neurophysiology 68, 164184.CrossRefGoogle ScholarPubMed
Orban, G.A., Kennedy, H. & Bullier, J. (1986). Velocity sensitivity and direction selectivity of neurons in areas V1 and V2 of the monkey: Influence of eccentricity. Journal of Neurophysiology 56, 462480.CrossRefGoogle ScholarPubMed
Parker, A. & Hawken, M. (1988). Two-dimensional spatial structure of receptive fields in monkey striate cortex. Journal of the Optical Society of America A 5, 598605.CrossRefGoogle ScholarPubMed
Petersik, J.T., Hicks, K.I. & Pantle, A.J. (1978). Apparent movement of successively generated subjective Figures. Perception 7, 371383.CrossRefGoogle ScholarPubMed
Poggio, G.F. & Fischer, B. (1977). Binocular interaction and depth sensitivity in striate and prestriate cortex of behaving rhesus monkey. Journal of Neurophysiology 40, 13921405.CrossRefGoogle ScholarPubMed
Poggio, G.F., Gonzalez, F. & Krause, F. (1988). Stereoscopic mechanisms in monkey visual cortex: Binocular correlation and disparity selectivity. Journal of Neuroscience 8, 45314550.CrossRefGoogle ScholarPubMed
Ramachandran, V.S., Rao, V.M. & Vidyasagar, T.R. (1973 a). Apparent motion with subjective contours. Vision Research 26, 19691975.CrossRefGoogle Scholar
Ramachandran, V.S., Rao, V.M. & Vidyasagar, T.R. (1973 b). The role of contours in stereopsis. Nature 242, 412414.CrossRefGoogle Scholar
Regan, D. (1989). Orientation discrimination for objects defined by relative motion and objects defined by luminance contrast. Vision Research 29, 13891400.CrossRefGoogle ScholarPubMed
Regan, D. (1990). Spatial vision for objects defined by colour contrast, binocular disparity and motion parallax. In Spatial Vision, ed. Regan, D.London: Macmillan.Google Scholar
Regan, D. & Beverley, K.I. (1984). Figure-ground segregation by motion contrast and by luminance contrast. Journal of the Optical Society of America A 1, 433442.CrossRefGoogle ScholarPubMed
Regan, D. & Hamstra, S. (1991). Shape discrimination for motion-defined and contrast-defined form: Squareness is special. Perception 20, 315316.CrossRefGoogle ScholarPubMed
Robinson, D.A. (1963). A method of measuring eye movement using a scleral search coil in a magnetic field. IEEE Transactions in Biomedical Engineering 10, 137145.Google ScholarPubMed
Saito, H., Tanaka, K., Isono, H., Yasuda, M. & Mikami, A. (1989). Directionally selective response of cells in the middle temporal area (MT) of the macaque monkey to the movement of equiluminous opponent color stimuli. Experimental Brain Research 75, 114.CrossRefGoogle Scholar
Schiller, P.H., Finlay, B.L. & Volman, S.F. (1976 a). Quantitative studies of single-cell properties in monkey striate cortex. I. Spatio-temporal organization of receptive fields. Journal of Neurophysiology 39, 12881319.CrossRefGoogle Scholar
Schiller, P.H., Finlay, B.L. & Volman, S.F. (1976 b). Quantitative studies of single-cell properties in monkey striate cortex. II. Orientation specificity and ocular dominance. Journal of Neurophysiology 39, 13201333.CrossRefGoogle ScholarPubMed
Sclar, G., Maunsell, J.H.R. & Lennie, P. (1990). Coding of image contrast in central visual pathways of the macaque monkey. Vision Research 30, 110.CrossRefGoogle ScholarPubMed
Shimojo, S., Nakayama, K. & Silverman, G.H. (1987). Width discrimination of motion-defined and luminance-defined edges. Investigative Ophthalmology and Visual Science (Suppl.) 28, 138.Google Scholar
Sperling, G. (1976). Movement perception in computer-driven visual displays. Behavior Research Methods and Instrumentation 8, 144151.CrossRefGoogle Scholar
Stoner, G.R. & Albright, T.D. (1992 a). Motion coherency rules are form-cue invariant. Vision Research 32, 465475.CrossRefGoogle ScholarPubMed
Stoner, G.R. & Albright, T.D. (1992 b). Image segmentation cues in motion processing: Implications for modularity in vision. Journal of Cognitive Neuroscience 5, 129149.CrossRefGoogle Scholar
Ts'o, D.Y. & Gilbert, C.D. (1988). The organization of chromatic and spatial interactions in the primate striate cortex. Journal of Neuroscience 8, 17121727.CrossRefGoogle ScholarPubMed
Vautin, R.G. & Dow, B.M. (1985). Color cell groups in foveal striate cortex of the behaving macaque. Journal of Neurophysiology 54, 273292.CrossRefGoogle ScholarPubMed
Victor, J.D. & Conte, M.M. (1990). Motion mechanisms have only limited access to form information. Vision Research 30, 289301.CrossRefGoogle ScholarPubMed
Vogels, R. & Orban, G.A. (1991). Quantitative study of striate single unit responses in monkeys performing an orientation discrimination task. Experimental Brain Research 84, 111.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Watson, A.B., Nielsen, K.R.K., Poirson, A., Fitzhugh, A., Bilson, A. Nguyen, & Ahumada, A.J. (1986). Use of a raster framebuffer in vision research. Behaviour Research Methods and Instrumentation 18, 587594.CrossRefGoogle Scholar
Wilson, H.G. & Bergen, J.R. (1979). A four mechanism model for threshold spatial vision. Vision Research 19U, 1932.CrossRefGoogle ScholarPubMed