Hostname: page-component-7c8c6479df-8mjnm Total loading time: 0 Render date: 2024-03-29T02:10:11.171Z Has data issue: false hasContentIssue false

Contrast coding by cells in the cat's striate cortex: Monocular vs. binocular detection

Published online by Cambridge University Press:  02 June 2009

Akiyuki Anzai
Affiliation:
Group in Vision Science, School of Optometry, University of California at Berkeley, Berkeley
Marcus A. Bearse Jr
Affiliation:
Group in Vision Science, School of Optometry, University of California at Berkeley, Berkeley
Ralph D. Freeman
Affiliation:
Group in Vision Science, School of Optometry, University of California at Berkeley, Berkeley
Daqing Cai
Affiliation:
Group in Vision Science, School of Optometry, University of California at Berkeley, Berkeley

Abstract

Many psychophysical studies of various visual tasks show that performance is generally better for binocular than for monocular observation. To investigate the physiological basis of this binocular advantage, we have recorded, under monocular and binocular stimulation, contrast response functions for single cells in the striate cortex of anesthetized and paralyzed cats. We applied receiver operating characteristic analysis to our data to obtain monocular and binocular neurometric functions for each cell. A contrast threshold and a slope were extracted from each neurometric function and were compared for monocular and binocular stimulation. We found that contrast thresholds and slopes varied from cell to cell but, in general, binocular contrast thresholds were lower, and binocular slopes were steeper, than their monocular counterparts. The binocular advantage ratio, the ratio of monocular to binocular thresholds for individual cells, was, on average, slightly higher than the typical ratios reported in human psychophysics. No single rule appeared to account for the various degrees of binocular summation seen in individual cells. We also found that the proportion of cells likely to contribute to contrast detection increased with stimulus contrast. Less contrast was required under binocular than under monocular stimulation to obtain the same proportion of cells that contribute to contrast detection. Based on these results, we suggest that behavioral contrast detection is carried out by a small proportion of cells that are relatively sensitive to near-threshold contrasts. Contrast sensitivity functions (CSFs) for the cell population, estimated from this hypothesis, agree well with behavioral data in both the shape of the CSF and the ratio of binocular to monocular sensitivities. We conclude that binocular summation in behavioral contrast detection may be attributed to the binocular superiority in contrast sensitivity of a small proportion of cells which are responsible for threshold contrast detection.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1995

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Albrecht, D.G. & Hamilton, D.B. (1982). Striate cortex of monkey and cat: Contrast response function. Journal of Neurophysiology 48, 217237.CrossRefGoogle ScholarPubMed
Albrecht, D.G. & Geisler, W.S. (1991). Motion selectivity and the contrast-response function of simple cells in the visual cortex. Visual Neuroscience 7, 531546.CrossRefGoogle ScholarPubMed
Anderson, P.A. & Movshon, J.A. (1989). Binocular combination of contrast signals. Vision Research 29, 11151132.CrossRefGoogle ScholarPubMed
Anzai, A. & Freeman, R.D. (1992). Contrast discrimination of cells in the cat's visual cortex: Monocular vs. binocular functions. Investigative Ophthalmology and Visual Science (Suppl.) 33, 1216.Google Scholar
Arditi, A.R., Anderson, P.A. & Movshon, J.A. (1981). Monocular and binocular detection of moving sinusoidal gratings. Vision Research 21, 329336.CrossRefGoogle ScholarPubMed
Bearse, M.A. & Freeman, R.D. (1993). Binocular summation in orientation discrimination depends on stimulus contrast and duration. Vision Research 34, 1929.CrossRefGoogle Scholar
Berkley, M.A. (1990). Behavioral determination of the spatial selectivity of contrast adaptation in cats: Some evidence for a common plan in the mammalian visual system. Visual Neuroscience 4, 413426.CrossRefGoogle ScholarPubMed
Bisti, S. & Maffei, L. (1974). Behavioural contrast sensitivity of the cat in various visual meridians. Journal of Physiology (London) 241, 201210.CrossRefGoogle ScholarPubMed
Blake, R. & Fox, R. (1973). The psychophysical inquiry into binocular summation. Perception and Psychophysics 14, 161185.CrossRefGoogle Scholar
Blake, R., Cool, S.J. & Crawford, M.L.J. (1974). Visual resolution in the cat. Vision Research 14, 12111217.CrossRefGoogle ScholarPubMed
Blake, R., Sloane, M. & Fox, R. (1981). Further developments in binocular summation. Perception and Psychophysics 30, 266276.CrossRefGoogle ScholarPubMed
Bradley, A., Skottun, B.C., Ohzawa, I., Sclar, G. & Freeman, R.D. (1987). Visual orientation and spatial frequency discrimination: A comparison of single neurons and behavior. Journal of Neurophysiology 57, 755772.CrossRefGoogle ScholarPubMed
Campbell, F.W. & Green, D.G. (1965). Monocular versus binocular visual acuity. Nature 208, 191192.CrossRefGoogle ScholarPubMed
Campbell, F.W. & Robson, J.G. (1968). Application of Fourier analysis to the visibility of gratings. Journal of Physiology (London) 197, 551566.CrossRefGoogle Scholar
Cohn, T.E., Green, D.G. & Tanner, W.P. (1975). Receiver operating characteristic analysis. Application to the study of quantum fluctuation effects in optic nerve of Rana pipiens. Journal of General Physiology 66, 583616.CrossRefGoogle Scholar
Crawford, M.L.J. & Cool, S.J. (1970). Binocular stimulation and response variability of striate cortex units in the cat. Vision Research 10, 11451153.CrossRefGoogle ScholarPubMed
Dean, A.F. (1981). The variability of discharge of simple cells in the cat striate cortex. Experimental Brain Research 44, 437440.CrossRefGoogle ScholarPubMed
De Valois, R.L., Albrecht, D.G. & Thorell, L.G. (1982). Spatial frequency selectivity of cells in macaque visual cortex. Vision Research 22, 545559.CrossRefGoogle ScholarPubMed
De Valois, R.L. & De Valois, K.K. (1988). Spatial Vision, pp. 114. New York: Oxford University Press.Google Scholar
Freeman, R.D. & Ohzawa, I. (1990). On the neurophysiological organization of binocular vision. Vision Research 30, 16611676.CrossRefGoogle ScholarPubMed
Green, D.M. & Swets, J.A. (1966). Signal Detection Theory and Psychophysics. New York: Wiley.Google Scholar
Heeger, D.J. (1991). Nonlinear model of neural responses in cat visual cortex. In Computational Models of Visual Processing, ed. Landy, M.S. & Movshon, J.A., pp. 119133. Cambridge, Massachusetts: M.I.T. Press.Google Scholar
Hubel, D.H. & Wiesel, T.N. (1962). Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. Journal of Physiology (London) 160, 106154.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
Jacobson, S.G. & Ikeda, H. (1979). Behavioural studies of spatial vision in cats reared with convergent squint: Is amblyopia due to arrest of development? Experimental Brain Research 34, 1126.CrossRefGoogle ScholarPubMed
Kato, H., Bishop, P.O. & Orban, G.A. (1981). Binocular interaction on monocularly discharged lateral geniculate and striate neurons in the cat. Journal of Neurophysiology 46, 932951.CrossRefGoogle ScholarPubMed
Legoe, G.E. (1984 a). Binocular contrast summation —I. Detection and discrimination. Vision Research 24, 373383.CrossRefGoogle Scholar
Legge, G.E. (1984 b). Binocular contrast summation —II. Quadratic summation. Vision Research 24, 385394.CrossRefGoogle ScholarPubMed
Levick, W.R. (1972). Another tungsten microelectrode. Medical and Biological Engineering 10, 510515.CrossRefGoogle ScholarPubMed
Li, Chao-yi & Creutzfeldt, O. (1984). The representation of contrast and other stimulus parameters by single neurons in area 17 of the cat. Pflügers Archiv 401, 304314.Google ScholarPubMed
Macy, A., Ohzawa, l. & Freeman, R.D. (1982). A quantitative study of the classification and stability of ocular dominance in the cat's visual cortex. Experimental Brain Research 48, 401408.CrossRefGoogle ScholarPubMed
Maffei, L., Fiorentini, A. & Bisti, S. (1973). Neural correlate of perceptual adaptation to gratings. Science 182, 10361038.CrossRefGoogle ScholarPubMed
Newsome, W.T., Britten, K.H., Movshon, J.A. & Shadlen, M. (1989). Single neurons and the perception of visual motion. In Neural Mechanisms of Visual Perception: The Second Retinal Research Foundation Symposium, ed. Lam, D. & Gilbert, C.D., pp. 171198. The Woodlands, Texas: Portfolio.Google Scholar
Ohzawa, I., Sclar, G. & Freeman, R.D. (1985). Contrast gain control in the cat's visual system. Journal of Neurophysiology 54, 651667.CrossRefGoogle ScholarPubMed
Ohzawa, I. & Freeman, R.D. (1986 a). The binocular organization of simple cells in the cat's visual cortex. Journal of Neurophysiology 56, 221242.CrossRefGoogle ScholarPubMed
Ohzawa, I. & Freeman, R.D. (1986 b). The binocular organization of complex cells in the cat's visual cortex. Journal of Neurophysiology 56, 243259.CrossRefGoogle ScholarPubMed
Pasternak, T. & Merigan, W.H. (1981). The luminance dependence of spatial vision in the cat. Vision Research 21, 13331339.CrossRefGoogle ScholarPubMed
Pirenne, M.H. (1943). Binocular and uniocular threshold of vision. Nature 152, 698699.CrossRefGoogle Scholar
Press, W.H., Flannery, B.P., Teukolsky, S.A. & Vetterling, W.T. (1988). Numerical Recipes in C: The Art of Scientific Computing, pp. 305309. New York: Cambridge University Press.Google Scholar
Rose, D. (1978). Monocular versus binocular contrast thresholds for movement and pattern. Perception 7, 195200.CrossRefGoogle ScholarPubMed
Sclar, G., Ohzawa, l. & Freeman, R.D. (1985). Contrast gain control in the kitten's visual system. Journal of Neurophysiology 54, 668675.CrossRefGoogle ScholarPubMed
Skottun, B.C., Bradley, A., Sclar, G., Ohzawa, I. & Freeman, R.D. (1987). The effects of contrast on visual orientation and spatial frequency discrimination: A comparison of single cells and behavior. Journal of Neurophysiology 57, 773786.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Thorell, L.G., De Valois, R.L. & Albrecht, D.G. (1984). Spatial mapping of monkey VI cells with pure color and luminance stimuli. Vision Research 24, 751769.CrossRefGoogle Scholar
Thorn, F. & Boynton, R.M. (1974). Human binocular summation at absolute threshold. Vision Research 14, 445458.CrossRefGoogle ScholarPubMed
Tolhurst, D.J., Movshon, J.A. & Thompson, I.D. (1981). The dependence of response amplitude and variance of cat visual cortical neurones on stimulus contrast. Experimental Brain Research 41, 414419.Google ScholarPubMed
Tolhurst, D.J., Movshon, J.A. & Dean, A.F. (1983). The statistical reliability of signals in single neurons in cat and monkey visual cortex. Vision Research 23, 775785.CrossRefGoogle Scholar
Tolhurst, D.J. (1989). The amount of information transmitted about contrast by neurones in the cat's visual cortex. Visual Neuroscience 2, 409413.CrossRefGoogle ScholarPubMed
Von Grünau, M. (1979). Binocular summation and the binocularity of cat visual cortex. Vision Research 19, 813816.CrossRefGoogle ScholarPubMed
Westendorf, D.H. & Fox, R. (1975). Binocular detection of vertical and horizontal line segments. Vision Research 15, 471476.CrossRefGoogle ScholarPubMed
Zohary, E. (1992). Population coding of visual stimuli by cortical neurons tuned to more than one dimension. Biological Cybernetics 66, 265272.CrossRefGoogle ScholarPubMed