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L and M cone proportions in polymorphic New World monkeys

Published online by Cambridge University Press:  06 September 2006

GERALD H. JACOBS  and
GARY A. WILLIAMS
GERALD H. JACOBS
Affiliation:
Neuroscience Research Institute and Department of Psychology, University of California, Santa Barbara, California
GARY A. WILLIAMS
Affiliation:
Neuroscience Research Institute and Department of Psychology, University of California, Santa Barbara, California
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Abstract

Platyrrhine monkeys typically have only a single X-chromosome opsin gene. Alleles of this gene code for multiple versions of middle- to long-wavelength cone photopigments. X-chromosome inactivation provides heterozygous females with a retinal mosaic of cones containing either of two types of M and L pigment, thus establishing the photopigment basis for trichromatic color vision. This study examined the proportions of L and M cones created by this process. For that purpose, electroretinogram flicker photometry was used to obtain complete spectral sensitivity functions from 60 heterozygous female monkeys drawn from seven genera of platyrrhine monkeys. To obtain estimates of cone proportions, these functions were subsequently fit with linear combinations of L and M cone fundamentals that were derived from similar recordings made on conspecific animals having only one type of M/L pigment. Consistent with a random X-chromosome inactivation process, the average L:M cone weighting across the sample was close to unity. At the same time, there were significant individual variations in L:M cone proportions. The genesis of this variation and its implications for seeing are discussed.

Keywords

Platyrrhine monkeysCone pigmentsCone proportionsX-chromosome inactivationERG
Type
GENETICS
Information
Visual Neuroscience , Volume 23 , Issue 3-4 , May 2006 , pp. 365 - 370
Copyright
© 2006 Cambridge University Press

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References

REFERENCES

Bowmaker, J.K., Jacobs, G.H., Spiegelhalter, D.J., & Mollon, J.D. (1985). Two types of trichromatic squirrel monkey share a pigment in the red-green spectral region. Vision Research 25, 1937–1946.CrossRefGoogle Scholar
Bowmaker, J.K., Mollon, J.D., & Jacobs, G.H. (1983). Microspectrophotometric measurements of Old and New world species of monkeys. In Colour Vision—Physiology and Psychophysics, eds. Mollon, J.D. & Sharpe, L.T., pp. 56–68. London: Academic Press.
Bowmaker, J.K., Parry, J.W.L., & Mollon, J.D. (2003). The arrangement of L and M cones in human and a primate retina. In Normal and Defective Colour Vision, eds. Mollon, J.D., Pokorny, J. & Knoblauch, K., pp. 39–50. Oxford: Oxford University Press.CrossRef
Brainard, D.H., Roorda, A., Yamauchi, Y., Calderone, J.B., Metha, A., Neitz, M., Neitz, J., Williams, D.R., & Jacobs, G.H. (2000). Functional consequences of the relative numbers of L and M cones. Journal of the Optical Society of America A 17, 607–614.CrossRefGoogle Scholar
Busque, L. & Gilliland, D.G. (1998). X-inactivation analysis in the 1990s: Promise and potential problems. Leukemia 12, 128–135.CrossRefGoogle Scholar
Carrel, L. & Willard, H.F. (2005). X-inactivation profile reveals extensive variability in X-linked gene expression in females. Nature 434, 400–404.CrossRefGoogle Scholar
Carroll, J., McMahon, C., Neitz, M., & Neitz, J. (2000). Flicker-photometric electroretinogram estimates of L:M cone photoreceptor ratio in men with photopigment spectra derived from genetics. Journal of the Optical Society of America A 17, 499–509.CrossRefGoogle Scholar
Carroll, J., Neitz, M., & Neitz, J. (2002). Estimates of L:M cone ratio from ERG flicker photometry and genetics. Journal of Vision 2, 531–542.Google Scholar
Cicerone, C. (1987). Constraints placed on color vision models by the relative numbers of the different cone classes in the human fovea centralis. Die Farbe 34, 59–66.Google Scholar
Cicerone, C.M. & Nerger, J.L. (1989). The relative numbers of long-wavelength-sensitive to middle-wavelength-sensitive cones in the human fovea centralis. Vision Research 29, 115–128.CrossRefGoogle Scholar
Deeb, S.S. (2005). The molecular basis of variation in human color vision. Clinical Genetics 67, 369–377.CrossRefGoogle Scholar
Deeb, S.S., Diller, L.C., Williams, D.R., & Dacey, D.M. (2000). Inter-individual and topographical variation in L:M cone ratios in monkey retinas. Journal of the Optical Society of America A 17, 538–544.CrossRefGoogle Scholar
De Vries, H.L. (1948). The heredity of the relative numbers of red and green receptors in the human eye. Genetica 24, 199–212.Google Scholar
Dobkins, K.R., Thiele, A., & Albright, T.D. (2000). Comparison of red-green equiluminance points in humans and macaques: Evidence for different L:M cone ratios between species. Journal of the Optical Society of America A 17, 545–556.CrossRefGoogle Scholar
Gowdy, P.D. & Cicerone, C.M. (1998). The spatial arrangement of L and M cones in the central fovea of the living human eye. Vision Research 38, 2575–2589.CrossRefGoogle Scholar
Gunther, K.L. & Dobkins, K.R. (2002). Individual differences in chromatic (red/green) contrast sensitivity are constrained by the relative number of L- versus M-cones in the eye. Vision Research 42, 1367–1378.CrossRefGoogle Scholar
Hagstrom, S.A., Neitz, J., & Neitz, M. (1998). Variations in cone populations for red-green color vision examined by analysis of mRNA. NeuroReport 9, 1963–1967.CrossRefGoogle Scholar
Hofer, H., Carroll, J., Neitz, J., Neitz, M., & Williams, D.R. (2005). Organization of the human trichromatic cone mosaic. Journal of Neuroscience 25, 9669–9679.CrossRefGoogle Scholar
Jacobs, G.H. (1984). Within-species variations in visual capacity among squirrel monkeys (Saimiri sciureus): Color vision. Vision Research 24, 1267–1277.CrossRefGoogle Scholar
Jacobs, G.H. (1998). A perspective on color vision in platyrrhine monkeys. Vision Research 38, 3307–3313.CrossRefGoogle Scholar
Jacobs, G.H. & Deegan II, J.F. (1997). Spectral sensitivity of macaque monkeys measured with ERG flicker photometry. Visual Neuroscience 14, 921–928.CrossRefGoogle Scholar
Jacobs, G.H. & Deegan II, J.F. (2001). Photopigments and colour vision in New World monkeys from the family Atelidae. Proceedings of the Royal Society B (London) 268, 695–702.CrossRefGoogle Scholar
Jacobs, G.H. & Deegan II, J.F. (2003). Cone pigment variations in four genera of New World monkeys. Vision Research 43, 227–236.CrossRefGoogle Scholar
Jacobs, G.H. & Neitz, J. (1987). Inheritance of color vision in a New World monkey (Saimiri sciureus). Proceedings of the National Academy of Sciences of the U.S.A. 84, 2545–2549.CrossRefGoogle Scholar
Jacobs, G.H. & Neitz, J. (1993). Electrophysiological estimates of individual variation in the L/M cone ratio. In Colour Vision Deficiencies XI, ed. Drum, B., pp. 107–112. Dordrecht, Netherlands: Kluwer.CrossRef
Jacobs, G.H., Neitz, J., & Krogh, K. (1996). Electroretinogram flicker photometry and its applications. Journal of the Optical Society of America A 13, 641–648.CrossRefGoogle Scholar
Jordan, G. & Mollon, J.D. (1993). A study of women heterozygous for colour deficiencies. Vision Research 33, 1495–1508.CrossRefGoogle Scholar
Jorgenson, A.L., Philip, J., Raskind, W.H., Matsushita, M., Christensen, B., Dreyer, V., & Motulsky, A.G. (1992). Different patterns of X inactivation in MZ twins discordant for red-green color-vision deficiency. American Journal of Human Genetics 51, 291–298.Google Scholar
Knau, H., Kremers, J., Schmidt, H.-J., Wolf, S., Wissinger, B., & Sharpe, L.T. (2002). M-cone opsin gene number does not correlate with variation in L-M cone sensitivity. Vision Research 42, 1888–1896.CrossRefGoogle Scholar
Latham, K.E. (2005). X chromosome imprinting and inactivation in preimplantation mammalian embryos. Trends in Genetics 21, 120–127.CrossRefGoogle Scholar
Lennie, P., Pokorny, J., & Smith, V.C. (1993). Luminance. Journal of the Optical Society of America A 10, 1283–1293.CrossRefGoogle Scholar
Lyon, M.F. (1961). Gene action in the X-chromosome of the mouse. Nature 190, 372–373.CrossRefGoogle Scholar
Marc, R.E. & Sperling, H.G. (1977). Chromatic organization of primate cones. Science 196, 454–456.CrossRefGoogle Scholar
McMahon, C., Neitz, J., Dacey, D.M., & Neitz, M. (2001). Reversed L:M cone ratio in baboon indicates that pigment gene order does not determine relative cone number. Investigative Ophthalmology and Visual Science 45, E-abstract 1725.
McMahon, C., Neitz, J., & Neitz, M. (2004). Evaluating the human X-chromosome pigment gene promotor sequences as predictors of L:M cone ratio variation. Journal of Vision 4, 203–208.Google Scholar
Migeon, B.R. (1998). Non-random X chromosome inactivation in mammalian cells. Cytogenetic and Genome Research 80, 142–148.CrossRefGoogle Scholar
Migeon, B.R. (2002). X chromosome inactivation: Theme and variations. Cytogenetic and Genome Research 99, 8–16.Google Scholar
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.CrossRefGoogle Scholar
Mollon, J.D., Bowmaker, J.K., & Jacobs, G.H. (1984). Variations of colour vision in a New World primate can be explained by polymorphism of retinal photopigments. Proceedings of the Royal Society B (London) 222, 373–399.CrossRefGoogle Scholar
Mollon, J.D. & Jordan, G. (1997). On the nature of unique hues. In John Dalton's Colour Vision Legacy, eds. Dickenson, C., Murray, I. & Carden, D., pp. 381–392. London: Taylor & Francis.
Otake, S. & Cicerone, C. (2000). L and M cone relative numerosity and red-green opponency from fovea to mid-periphery in the human retina. Journal of the Optical Society of America A 17, 615–627.CrossRefGoogle Scholar
Pokorny, J., Smith, V.C., & Wesner, M.F. (1991). Variability in cone populations and implications. In From Pigments to Perception, eds. Valberg, A. & Lee, B.B., pp. 23–34. New York: Plenum.CrossRef
Racchi, O., Mangerini, R., Rapezzi, D., Rolfo, M., Gaetani, G.F., & Ferrais, A.M. (1998). X chromosome inactivation patterns in normal females. Blood Cells, Molecules and Diseases 24, 439–447.CrossRefGoogle Scholar
Roorda, A., Mehta, A.B., Lennie, P., & Williams, D.A. (2001). Packing arrangement of the three cone classes in the primate retina. Vision Research 41, 1291–1306.CrossRefGoogle Scholar
Rushton, W.A.H. & Baker, H.D. (1964). Red/green sensitivity in normal vision. Vision Research 4, 75–85.CrossRefGoogle Scholar
Sato, K., Uehara, S., Hashiyada, M., Nabeshima, H., Sugawara, J.-i., Terada, Y., Yaegashi, N., & Okamura, K. (2004). Genetic significance of skewed X-chromosome inactivation on premature ovarian failure. American Journal of Medical Genetics 130A, 240–244.CrossRefGoogle Scholar
Sharp, A., Robinson, D., & Jacobs, P. (2000). Age- and tissue-specific variation in X chromosome inactivation ratios in normal women. Human Genetics 107, 343–349.CrossRefGoogle Scholar
Sharpe, L.T., Stockman, A., Jagle, 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.Google Scholar
Smallwood, P.M., Wang, Y., & Nathans, J. (2002). Role of a locus control region in the mutually exclusive expression of human red and green cone pigment genes. Proceedings of the National Academy of Sciences of the U.S.A. 99, 1008–1011.CrossRefGoogle Scholar
Wang, Y., Macke, J.P., Merbs, S.L., Zack, D.J., Klaunberg, B., Bennett, J., Gearhart, J., & Nathans, J. (1992). A locus control region adjacent to the human red and green visual pigment genes. Neuron 9, 429–440.CrossRefGoogle Scholar
Wang, Y., Smallwood, P.M., Cowan, M., Blesh, D., Lawler, A., & Nathans, J. (1999). Mutually exclusive expression of human red and green visual pigment-reporter transgenes occurs at high frequency in murine cone photoreceptors. Proceedings of the National Academy of Sciences of the U.S.A. 96, 5251–5256.CrossRefGoogle Scholar
Wesner, M.F., Pokorny, J., Smith, V.C., & Shevell, S.K. (1991). Foveal cone detection statistics in color normals and dichromats. Vision Research 31, 1021–1037.CrossRefGoogle Scholar