Abstract
Traditional color vision theory posits that three types of retinal photopigments transduce light into a trivariate neural color code, thereby explaining color-matching behaviors. Thisprinciple of trichromacy is in need of reexamination in view of molecular genetics results suggesting that a substantial percentage of women possess more than three classes of retinal photopigments. At issue is the question of whether four-photopigment retinas necessarily yield trichromatic color perception. In the present paper, we review results and theory underlying the accepted photoreceptor-based model of trichromacy. A review of the psychological literature shows that gender-linked differences in color perception warrant further investigation of retinal photopigment classes and color perception relations. We use genetic analyses to examine an important position in the gene sequence, and we empirically assess and compare the color perception of individuals possessing more than three retinal photopigment genes with those possessing fewer retinal photopigment genes. Women with four-photopigment genotypes are found to perceive significantly more chromatic appearances in comparison with either male or female trichromat controls. We provide a rationale for this previously undetected finding and discuss implications for theories of color perception and gender differences in color behavior.
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Almirall, H., &Gutierrez, E. (1987). Auditory and visual reaction time in adults during long performance.Perceptual & Motor Skills,65, 543–552.
Anyan, W.R., Jr., &Quillian, W. W., II (1971). The naming of primary colors by children.Child Development,42, 1629–1632.
Asenjo, A. B., Rim, J., &Oprian, D. D. (1994). Molecular determinants of human red /green color discrimination.Neuron,12, 1131–1138.
Blough, P. M., &Slavin, L. K. (1987). Reaction time assessments of gender differences in visual-spatial performance.Perception & Psychophysics,41, 276–281.
Boker, S. (1997). A measurement of the adaptation of color vision to the spectral environment.Psychological Science,8, 130–143.
Boring, E. G. (1942).Sensation and perception in the history of experimental psychology. New York: Appleton-Century-Crofts.
Boynton, R. M., Schafer, W. & Neun, M. E. (1964). Hue-wavelength relation measured by color-naming method for three retinal locations.Science,146, 666–668.
Brabyn, L. B., &McGuinness, D. (1979). Gender differences in response to spatial frequency and stimulus orientation.Perception & Psychophysics,26, 319–324.
Brindley, G. S. (1960).Physiology of the retina and the visual pathway. London: Edward Arnold.
Buckalew, L. W., &Buckalew, N. M. (1989). Note on color preference and color vision test performance.Perception & Motor Skills,69, 1039–1042.
Campbell, F. W. (1986). In search of the spectrum’s elusive yellow.Ophthalmic Physiological Optics,6, 129–133.
Cohn, S. A., Emmerich, D. S., &Carlson, E. A. (1989). Differences in the responses of heterozygous carriers of color blindness and normal controls to briefly presented stimuli.Vision Research,29, 255–262.
Crone, R. A. (1959). Spectral sensitivity in color-defective subjects and heterozygous carriers.American Journal of Ophthalmology,48, 231–238.
Dartnall, H. J. A., Bowmaker, J. K., &Mollon, J. D. (1983). Human visual pigments: Microspectrophotometric results from the eyes of seven persons.Proceedings of the Royal Society of London: Series B,220, 115–13.
Deeb, S. S., &Motulsky, A. G. (1996). Molecular genetics of human color vision.Behavioral Genetics,26, 195–206.
DeMarco, P., Pokorny, J., &Smith, V. C. (1992). Full spectrum cone sensitivity functions for X-chromosome-linked anomalous trichromats.Journal of the Optical Society of America A,9, 1465–1476.
DeVries, H. L. (1948). The luminosity curve of the eye as determined by the measurements with the flickerphotometer.Physica,XIV, 367–380.
Dimmick, F. L., &Hubbard, M. R. (1939). The spectral location of psychologically unique yellow, green and blue.American Journal of Psychology,52, 242–251.
Feig, K., &Ropers, H. (1978). On the incidence of unilateral and bilateral colour blindness in heterozygous females.Journal of Human Genetics,41, 313–323.
Furbee, L. N., Maynard, K., Smith, J., Benfer, B. A., Jr.,Quick, S., &Ross, L. (1997). The emergence of color cognition from color perception.Journal of Linguistic Anthropology,6, 223–240.
Hardin, C. L., &Maffi, L. (Eds.) (1997).Color categories in thought and language. Cambridge: Cambridge University Press.
He, J. C., &Shevell, S. K. (1995). Variation in color matching and discrimination among deuteranomalous trichromats: Theoretical implications of small differences in photopigments.Vision Research,35, 2579–2588.
Hecht, S., &Shlaer, S. (1936). The color vision of dichromats.Journal of General Physiology,20, 57–93.
Hsia, Y. &Graham, C. H. (1957). Spectral luminosity curves for protanopic, deuteranopic and normal subjects.Proceedings of the National Academy of Science,43, 1011–1019.
Jacobs, G. H. (1998). Photopigments and seeing—Lessons from natural experiments.Investigative Ophthalmology & Visual Science,39, 2205–2216.
Jameson, D., &Hurvich, L. M. (1956). Theoretical analysis of anomalous trichromatic color vision.Journal of the Optical Society of America,46, 1075–1089.
Jordan, G., &Mollon, J. D. (1993). A study of women heterozygous for color deficiencies.Vision Research,33, 1495–1508.
Judd, D. B. (1945). Standard response functions for protanopic and deuteranopic vision.Journal of the Optical Society of America,35, 199–221.
Kraft, T. W., Neitz, J., &Neitz, M. (1998). Spectra of human cones.Vision Research,38, 3663–3670.
Krill, A. E., &Beutler, E. (1964). The red-light absolute threshold in heterozygote protan carriers.Investigative Ophthalmology,3, 107–118.
Krill, A. E., &Beutler, E. (1965). Red light thresholds in heterozygote carriers of protanopia: Genetic implications.Science,149, 186–188.
Lakoff, R. T. (1975).Language and woman’s place. San Francisco: Harper & Row.
Lyon, M. F. (1961). Gene action in the X chromosome of the mouse(Mus musculus L.).Nature,190, 372–373.
MacLeod, D. I. A. (1985). Receptoral constraints on colour appearance. In D. Ottoson & S. Zeki (Eds.),Central and peripheral mechanisms of colour vision (pp. 103–116). London: Macmillian.
MacLeod, D. I. A., & von der Twer, T. (2000).The pleistochrome: Optimal opponent codes for natural colors. Manuscript submitted for publication.
Maloney, L. T. (1992). Color constancy and color perception: The linear models framework. In D. E. Meyer & S. Kornblum (Eds.),Attention and performance XIV: Synergies in experimental psychology, artificial intelligence, and cognitive neuroscience (pp. 59–78). Cambridge, MA: MIT Press.
Mausfeld, R. (1998). Color perception: From Grassman codes to a dual code for object and illumination colors. In W. G. K. Backhaus, R. Kliegl, & J. S. Werner (Eds.),Color vision: Perspectives from different disciplines (pp. 219–250). New York: Walter de Gruyter.
Mausfeld, R., &Niederée, R. (1993). Inquiries into relational concepts of colour based on an incremental principle of colour coding for minimal relational stimuli.Perception,22, 427–462.
McGuinness, D. (1976). Away from a unisex psychology: Individual differences in visual sensory and perceptual processes.Perception,5, 279–294.
McGuinness, D., &Lewis, I. (1976). Sex differences in visual persistence: Experiments on the Ganzfeld and afterimages.Perception,5, 295–301.
Menzel, R. (1985). Colour pathways and colour vision in the honeybee. In D. Ottoson & S. Zeki (Eds.),Central and peripheral mechanisms of colour vision (Proceedings of an International Symposium at the Wenner-Gren Center, Vol. 43, pp. 211–233). London: Macmillan.
Merbs, S. L., &Nathans, J. (1992a). Absorption spectra of human cone pigments.Nature,356, 433–435.
Merbs, S. L., &Nathans, J. (1992b). Absorption spectra of hybrid pigments responsible for anomalous color vision.Science,258, 464–466.
Merbs, S. L., &Nathans, J. (1993). Role of hydroxyl-bearing amino acids in differentially tuning the absorption spectra of the human red and green cone pigments.Photochemical Photobiology,58, 706–710.
Miller, S. A., Dykes, D. D., &Polesky, H. F. (1998). A simple salting out procedure for extracting DNA from human nucleated cells.Nucleic Acids Research,16, 1215.
Miyahara, E., Pokorny, J., Smith, V. C., Baron, R., &Baron, E. (1998). Color vision in two observers with highly biased LWS/MWS cone ratios.Vision Research,38, 601–612.
Mollon, J. D. (1992). Worlds of difference.Nature,356, 378–379.
Mollon, J. D. (1995). Seeing colour. In T. Lamb & J. Bourriau (Eds.),Colour, art & science (pp. 127–150). Cambridge: Cambridge University Press.
Nagy, A. L., MacLeod, D. I. A., Heyneman, N. E., &Eiser, A. (1981). Four cone pigments in women heterozygous for color deficiency.Journal of the Optical Society of America,71, 719–722.
Nathans, J. (1997). The genes for color vision. In A. Byrne & D. R. Hilbert (Eds.),Readings on Color, Vol. 2: The science of color (pp. 249–258). Cambridge, MA: MIT Press.
Nathans, J., Piantanida, T. P., Eddy, R. L., Shows, T. B., &Hogness, D. S. (1986). Molecular genetics of inherited variation in human color vision.Science,232, 203–210.
Nathans, J., Thomas, D., &Hogness, D. S. (1986). Molecular genetics of human color vision: The genes encoding blue, green, and red pigments.Science,232, 193–202.
Neitz, J., &Jacobs, G. H. (1986). Polymorphism of the long-wavelength cone in normal human color vision.Nature,323, 623–625.
Neitz, J., &Neitz, M. (1994). Colour vision defects. In A. S. Wright & B. Jay (Eds.),Molecular genetics of inherited eye disorders (pp. 217–257). Chur: Harwood.
Neitz, J., Neitz, M., &Jacobs, G. H. (1993). More than three different cone pigments among people with normal color vision.Vision Research,33, 117–122.
Neitz, M., Kraft, T. W., &Neitz, J. (1998). Expression of L-cone pigment gene subtypes in females.Vision Research,38, 3221–3225.
Neitz, M., &Neitz, J. (1998). Molecular genetics and the biological basis of color vision. In W. G. K. Backhaus, R. Kliegl, & J. S. Werner (Eds.),Color Vision: Perspectives from different disciplines (pp. 101–119). New York: Walter de Gruyter.
Neitz, M., Neitz, J., &Jacobs, G. H. (1995). Genetic basis of photopigment variations in human dichromats.Vision Research,35, 2095–2130.
Nerger, J. L. (1988).The relative numbers of long-wavelength-sensitive to middle-wavelength-sensitive cones in the human fovea and parafovea. Unpublished doctoral dissertation, University of California at San Diego, La Jolla.
Nowaczyk, R. H. (1982). Sex-related differences in the color lexicon.Language & Speech,25, 257–265.
Piantanida, T. P. (1976). Polymorphism of human color vision.American Journal of Optometry & Physiological Optics,53, 647–657.
Pickford, R. W. (1959). Some heterozygous manifestations of colourblindness.British Journal of Physiological Optics,16, 83–95.
Pokorny, J., &Smith, V. C. (1977). Evaluation of a single pigment shift model of anomalous trichromacy.Journal of the Optical Society of America,67, 1196–1209.
Pokorny, J., &Smith, V. C. (1982). New observations concerning redgreen colour defects.Colour Research & Application,7, 159–164.
Poynter, D. (1988). Variability in brightness matching of colored lights.Human Factors,30, 143–151.
Purdy, D. (1931). Spectral hue as a function of intensity.American Journal of Psychology,43, 541–559.
Regan, B. C., Reffin, J. P., &Mollon, J. D. (1994). Luminance noise and the rapid determination of discrimination ellipses in colour deficiency.Vision Research,34, 1279–1299.
Rich, E. (1977). Sex-related difference in color vocabulary.Language & Speech,20, 404–409.
Roorda, A., &Williams, D. R. (1999). The arrangement of the three cone classes in the living human eye.Nature,397, 520–522.
Saito, M. (1994). A cross-cultural study on color preference in three Asian cities: Comparison between Tokyo, Taipei and Tianjin.Japanese Psychological Research,36, 219–232.
Saito, M. (1996). A comparative study of color preferences in Japan, China and Indonesia with emphasis on the preference for white.Perceptual & Motor Skills,83, 115–128.
Saito, M. (1999). Blue and seven phenomena among Japanese students.Perceptual & Motor Skills,89, 532–536.
Schmidt, I. (1955). A sign of manifest heterozygosity in carriers of color deficiency.American Journal of Optometry,32, 404–408.
Shapiro, A. E. (1984).The optical papers of Isaac Newton: Vol. 1. The optical lectures 1670–1672 (pp. 539–554). Cambridge: Cambridge University Press.
Sharpe, L. T., Stockman, A., Jaegle, H., Knau, H., Klausen, G., Reitner, A, &Nathans, J. (1998). Red, green and red-green hybrid pigments in the human retina: Correlations between deduced protein sequences and psychophysically measured spectral sensitivities.Journal of Neuroscience,18, 10053–10069.
Sharpe, L. T., Stockman, A., Knau, H., &Jaegle, H. (1998). Macular pigment densities derived from central and peripheral spectral sensitivity differences.Vision Research,38, 3233–3239.
Sjoberg, S. A., Neitz, M., Balding, S. D., &Neitz, J. (1998). L-cone pigment genes expressed in normal colour vision.Vision Research,38, 3213–3219.
Smeulders, N., Campbell, F. W., &Andrews, P. R. (1994). The role of delineation and spatial frequency in the perception of the colors of the spectrum.Vision Research,34, 927–936.
Stockman, A., &Sharpe, L. T. (1998). Human cone spectral sensitivities: A progress report.Vision Research,38, 3193–3206.
Stoerig, P. (1998). Wavelength information processing versus color perception: Evidence from blindsight and color-blind sight. In W. G. K. Backhaus, R. Kliegl, & J. S. Werner (Eds.),Color vision: Perspectives from different disciplines (pp. 131–147). New York: Walter de Gruyter.
Swaringen, S., Layman, S., &Wilson, A. (1978). Sex differences in color naming.Perceptual & Motor Skills,47, 440–442.
Thomas, L. L., Curtis, A. J., &Bolton, R. (1978). Sex differences in elicited color lexicon size.Perceptual & Motor Skills,47, 77–78.
Thomson, L. C. (1954). Sensations aroused by monochromatic stimuli and their prediction.Optical Acta,1, 93–102.
Troscianko, T., Davidoff, J., Humphreys, G., Landis, T., Fahle, M., Greenlee, M., Brugger, P., &Phillips, W. (1996). Human colour discrimination based on a non-parvocellular pathway.Current Biology,6, 200–210.
Wilder, D. G. (1970).The photopic spectral sensitivity of color normal, protanopic and deuteronopic observers. Unpublished doctoral dissertation, University of California, Los Angeles.
Winderickx, J., Battisti, L., Hibiya, Y., Motulsky, A. G., &Deeb, S. S. (1993). Haplotype diversity in the human red and green opsin genes: Evidence for frequent sequence exchange in exon 3.Human Molecular Genetics Polymorphism,2, 1413–1421.
Winderickx, J., Lindsey, D. T., Sanocki, E., Teller, D. Y., Motulsky, A.G., &Deeb, S. S. (1992). Polymorphism in red photopigment underlies variation in color matching.Nature,356, 431–433.
Wyszecki, G., &Stiles, W. S. (1982).Color science: Concepts and methods, quantitative data and formulae (2nd ed.). New York: Wiley.
Yasuma, T., Tokuda, H., &Ichikawa, H. (1984). Abnormalities of cone photopigments in genetic carriers of protanomaly.Archives of Ophthalmology,102, 897–900.
Zegura, S. L. (1997). Genes, opsins, neurons, and color categories: Closing the gaps. In C. L. Hardin & L. Maffi (Eds.),Color categories in thought and language (pp. 283–292). Cambridge: Cambridge University Press.
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Portions of this research were presented at the 1998 European Conference on Visual Perception, the 1998 meeting of the Optical Society of America, and the 1998 meeting of the Psychonomic Society. Partial support was provided by the National Science Foundation (Grant NSF-9973903 to K.A.J.) and a UCSD Hellman Faculty Award (to K.A.J.).
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Jameson, K.A., Highnote, S.M. & Wasserman, L.M. Richer color experience in observers with multiple photopigment opsin genes. Psychonomic Bulletin & Review 8, 244–261 (2001). https://doi.org/10.3758/BF03196159
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DOI: https://doi.org/10.3758/BF03196159