Abstract

Direct imaging of the retina by adaptive optics allows assessment of the relative number of long-wavelength-sensitive (L) and middle-wavelength-sensitive (M) cones in living human eyes. We examine the functional consequences of variation in the relative numbers of L and M cones (L/M cone ratio) for two observers whose ratios were measured by direct imaging. The L/M cone ratio for the two observers varied considerably, taking on values of 1.15 and 3.79. Two sets of functional data were collected: spectral sensitivity measured with the flicker electroretinogram (ERG) and the wavelength of unique yellow. A genetic analysis was used to determine L and M cone spectra appropriate for each observer. Rayleigh matches confirmed the use of these spectra. We determined the relative strength of L and M cone contributions to ERG spectral sensitivity by fitting the data with a weighted sum of L and M cone spectra. The relative strengths so determined (1.06 and 3.38) were close to the cone ratios established by direct imaging. Thus variation in L/M cone ratio is preserved at the sites tapped by the flicker ERG. The wavelength of unique yellow varied only slightly between the two observers (576.8 and 574.7 nm). This small variation indicates that neural factors play an important role in stabilizing unique yellow against variation in the L/M cone ratio.

© 2000 Optical Society of America

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  59. M. L. Bieber, J. M. Kraft, J. S. Werner, “Effects of known variations in photopigments on L/M cone ratios estimated from luminous efficiency functions,” Vision Res. 38, 1961–1966 (1998).
    [CrossRef] [PubMed]
  60. D. A. Baylor, B. J. Nunn, J. L. Schnapf, “Spectral sensitivity of cones of the monkey Macaca fascicularis,” J. Physiol. (London) 390, 145–160 (1987).
  61. V. Smith, J. Pokorny, “Spectral sensitivity of the foveal cone photopigments between 400 and 500 nm,” Vision Res. 15, 161–171 (1975).
    [CrossRef] [PubMed]
  62. P. DeMarco, J. Pokorny, V. C. Smith, “Full-spectrum cone sensitivity functions for X-chromosome-linked anomalous trichromats,” J. Opt. Soc. Am. A 9, 1465–1476 (1992).
    [CrossRef] [PubMed]
  63. Y. Chang, S. A. Burns, M. R. Krietz, “Red–green flicker photometry and nonlinearities in the flicker electroretinogram,” J. Opt. Soc. Am. A 10, 1413–1422 (1993).
    [CrossRef] [PubMed]
  64. G. R. Cole, T. Hine, W. McIlhagga, “Detection mechanisms in L-, M-, and S-cone contrast space,” J. Opt. Soc. Am. A 10, 38–51 (1993).
    [CrossRef] [PubMed]

2000 (1)

1999 (6)

J. J. Kremers, T. Usui, H. P. Scholl, L. T. Sharpe, “Cone signal contributions to electrograms in dichromats and trichromats,” Invest. Ophthalmol. Visual Sci. 40, 920–930 (1999).

D. H. Brainard, J. Calderone, A. K. Nugent, G. H. Jacobs, “Flicker ERG responses to stimuli parametrically modulated in color space,” Invest. Ophthalmol. Visual Sci. 40, 2840–2847 (1999).

J. Verweij, L. C. Diller, D. R. Williams, D. M. Dacey, “The relative strength of L and M cone inputs to H1 horizontal cells in primate retina,” Invest. Ophthalmol. Visual Sci. Suppl. 40, S240 (1999).

L. C. Diller, J. Verweij, D. R. Williams, D. M. Dacey, “L and M cone inputs to peripheral parasol and midget ganglion cells in primate retina,” Invest. Ophthalmol. Visual Sci. Suppl. 40, S817 (1999).

K. Bumsted, A. Hendrickson, “Distribution and development of short-wavelength cones differ between Macaca monkey and human fovea,” J. Comp. Neurol. 403, 502–516 (1999).
[CrossRef] [PubMed]

A. Roorda, D. R. Williams, “The arrangement of the three cone classes in the living human eye,” Nature 397, 520–522 (1999).
[CrossRef] [PubMed]

1998 (7)

S. A. Hagstrom, J. Neitz, M. Neitz, “Variations in cone populations for red–green color vision examined by analysis of mRNA,” NeuroReport 9, 1963–1967 (1998).
[CrossRef] [PubMed]

P. D. Gowdy, C. M. Cicerone, “The spatial arrangement of the L and M cones in the central fovea of the living human eye,” Vision Res. 38, 2575–2589 (1998).
[CrossRef]

E. Miyahara, J. Pokorny, V. C. Smith, R. Baron, “Color vision in two observers with highly biased LWS/MWS cone ratios,” Vision Res. 38, 601–612 (1998).
[CrossRef] [PubMed]

T. Usui, J. Kremers, L. T. Sharpe, E. Zrenner, “Flicker cone ERG in dichromats and trichromats,” Vision Res. 38, 3391–3396 (1998).
[CrossRef]

T. W. Kraft, J. Neitz, M. Neitz, “Spectra of human L cones,” Vision Res. 38, 3663–3670 (1998).
[CrossRef]

L. T. Sharpe, A. Stockman, H. Jagle, H. Knau, G. Klausen, A. Reitner, J. Nathans, “Red, green, and red–green hybrid pigments in the human retina: correlations between deduced protein sequences and psychophysically measured spectral sensitivities,” J. Neurosci. 18, 10053–10069 (1998).
[PubMed]

M. L. Bieber, J. M. Kraft, J. S. Werner, “Effects of known variations in photopigments on L/M cone ratios estimated from luminous efficiency functions,” Vision Res. 38, 1961–1966 (1998).
[CrossRef] [PubMed]

1997 (3)

M. Kalloniatis, M. J. Pianta, “L and M cone input into spectral sensitivity functions: a reanalysis,” Vision Res. 37, 799–811 (1997).
[CrossRef] [PubMed]

G. H. Jacobs, J. F. Deegan, “Spectral sensitivity of macaque monkeys measured with ERG flicker photometry,” Visual Neurosci. 14, 921–928 (1997).
[CrossRef]

J. Liang, D. R. Williams, D. Miller, “Supernormal vision and high-resolution retinal imaging through adaptive optics,” J. Opt. Soc. Am. A 14, 2884–2892 (1997).
[CrossRef]

1996 (2)

T. T. J. M. Berenschot, J. van de Kraats, D. van Norren, “Foveal cone mosaic and visual pigment density in dichromats,” J. Physiol. (London) 492, 307–314 (1996).

G. H. Jacobs, J. Neitz, K. Krogh, “Electroretinogram flicker photometry and its applications,” J. Opt. Soc. Am. A 13, 641–648 (1996).
[CrossRef]

1995 (1)

M. Neitz, J. Neitz, A. Grishok, “Polymorphism in the number of genes encoding long-wavelength-sensitive cone pigments among males with normal color vision,” Vision Res. 35, 2395–2407 (1995).
[CrossRef] [PubMed]

1994 (1)

A. B. Asenjo, J. Rim, D. D. Oprian, “Molecular determinants of human red/green colour discrimination,” Neuron 12, 1131–1138 (1994).
[CrossRef] [PubMed]

1993 (4)

S. L. Merbs, J. Nathans, “Role of hydroxyl-bearing amino acids in differentially tuning the absorption spectra of the human red and green cone pigments,” Photochem. Photobiol. 58, 706–710 (1993).
[CrossRef] [PubMed]

Y. Chang, S. A. Burns, M. R. Krietz, “Red–green flicker photometry and nonlinearities in the flicker electroretinogram,” J. Opt. Soc. Am. A 10, 1413–1422 (1993).
[CrossRef] [PubMed]

G. R. Cole, T. Hine, W. McIlhagga, “Detection mechanisms in L-, M-, and S-cone contrast space,” J. Opt. Soc. Am. A 10, 38–51 (1993).
[CrossRef] [PubMed]

C. M. Diaz-Araya, J. M. Provis, F. A. Billson, “NADPH-diaphorase histochemistry reveals cone distributions in adult human retinae,” Aust. NZ J. Ophthalmol. 21, 171–179 (1993).

1992 (3)

J. D. Mollon, J. K. Bowmaker, “The spatial arrangement of cones in the primate fovea,” Nature 360, 677–679 (1992).
[CrossRef] [PubMed]

S. C. Merbs, J. Nathans, “Absorption spectra of human cone photopigments,” Nature 356, 433–435 (1992).
[CrossRef] [PubMed]

P. DeMarco, J. Pokorny, V. C. Smith, “Full-spectrum cone sensitivity functions for X-chromosome-linked anomalous trichromats,” J. Opt. Soc. Am. A 9, 1465–1476 (1992).
[CrossRef] [PubMed]

1991 (3)

M. Neitz, J. Neitz, G. H. Jacobs, “Spectral tuning of pigments underlying red–green color vision,” Science 252, 971–973 (1991).
[CrossRef] [PubMed]

C. A. Curcio, K. Allen, K. Sloan, C. Lerea, I. Klock, A. Milam, “Distribution and morphology of human cone photoreceptors stained with anti-blue opsin,” J. Comp. Neurol. 312, 610–624 (1991).
[CrossRef] [PubMed]

M. F. Wesner, J. Pokorny, S. K. Shevell, V. C. Smith, “Foveal cone detection statistics in color-normals and dichromats,” Vision Res. 31, 1021–1037 (1991).
[CrossRef] [PubMed]

1990 (3)

P. K. Ahnelt, C. Keri, R. Pflug, “Identification of pedicles of putative blue-sensitive cones in human retina,” J. Comp. Neurol. 293, 39–53 (1990).
[CrossRef] [PubMed]

K. C. Wikler, P. Rakic, “Distribution of photoreceptor subtypes in the retina of diurnal and nocturnal primates,” J. Neurosci. 10, 3390–3401 (1990).
[PubMed]

J. Neitz, G. H. Jacobs, “Polymorphism in normal human color vision and its mechanism,” Vision Res. 30, 621–636 (1990).
[CrossRef] [PubMed]

1989 (2)

C. M. Cicerone, J. L. Nerger, “The relative numbers of long-wavelength-sensitive to middle-wavelength-sensitive cones in the human fovea centralis,” Vision Res. 26, 115–128 (1989).
[CrossRef]

R. L. P. Vimal, J. Pokorny, V. C. Smith, S. K. Shevell, “Foveal cone thresholds,” Vision Res. 29, 61–78 (1989).
[CrossRef] [PubMed]

1987 (4)

C. M. Cicerone, “Constraints placed on color vision models by the relative numbers of different cone classes in human fovea centralis,” Farbe 34, 59–66 (1987).

J. Pokorny, V. C. Smith, “L/M cone ratios and the null point of the perceptual red/green opponent system,” Farbe 34, 53–57 (1987).

P. K. Ahnelt, H. Kolb, R. Pflug, “Identification of a subtype of cone photoreceptor, likely to be blue sensitive, in the human retina,” J. Comp. Neurol. 255, 18–34 (1987).
[CrossRef] [PubMed]

D. A. Baylor, B. J. Nunn, J. L. Schnapf, “Spectral sensitivity of cones of the monkey Macaca fascicularis,” J. Physiol. (London) 390, 145–160 (1987).

1986 (1)

E. F. MacNichol, “A unifying presentation of photopigment spectra,” Vision Res. 26, 1543–1556 (1986).
[CrossRef] [PubMed]

1985 (1)

F. M. de Monasterio, E. P. McCrane, J. K. Newlander, S. J. Schein, “Density profile of blue-sensitive cones along the horizontal meridian of macaque retina,” Invest. Ophthalmol. Visual Sci. 26, 289–302 (1985).

1983 (1)

D. R. Williams, R. J. Collier, “Consequences of spatial sampling by a human photoreceptor mosaic,” Science 221, 385–387 (1983).
[CrossRef] [PubMed]

1981 (3)

D. Williams, D. I. A. MacLeod, M. Hayhoe, “Foveal tritanopia,” Vision Res. 21, 1341–1356 (1981).
[CrossRef] [PubMed]

D. Williams, D. I. A. MacLeod, M. Hayhoe, “Punctate sensitivity of the blue sensitive mechanism,” Vision Res. 21, 1357–1375 (1981).
[CrossRef]

S. M. Dawis, “Polynomial expressions of pigment nomograms,” Vision Res. 21, 1427–1430 (1981).
[CrossRef] [PubMed]

1979 (1)

W. W. Dawson, G. L. Trick, C. Litzkow, “An improved electrode for electroretinography,” Invest. Ophthalmol. Visual Sci. 19, 988–991 (1979).

1977 (1)

R. E. Marc, H. G. Sperling, “Chromatic organization of primate cones,” Science 196, 454–456 (1977).
[CrossRef] [PubMed]

1975 (1)

V. Smith, J. Pokorny, “Spectral sensitivity of the foveal cone photopigments between 400 and 500 nm,” Vision Res. 15, 161–171 (1975).
[CrossRef] [PubMed]

1965 (1)

J. Krauskopf, R. Srebro, “Spectral sensitivity of color mechanisms: derivation from fluctuations of color appearance near threshold,” Science 150, 1477–1479 (1965).
[CrossRef] [PubMed]

1964 (2)

1947 (1)

H. L. De Vries, “The heredity of the relative numbers of red and green receptors in the human eye,” Genetica (The Hague) 24, 199–212 (1947).

Ahnelt, P. K.

P. K. Ahnelt, C. Keri, R. Pflug, “Identification of pedicles of putative blue-sensitive cones in human retina,” J. Comp. Neurol. 293, 39–53 (1990).
[CrossRef] [PubMed]

P. K. Ahnelt, H. Kolb, R. Pflug, “Identification of a subtype of cone photoreceptor, likely to be blue sensitive, in the human retina,” J. Comp. Neurol. 255, 18–34 (1987).
[CrossRef] [PubMed]

Allen, K.

C. A. Curcio, K. Allen, K. Sloan, C. Lerea, I. Klock, A. Milam, “Distribution and morphology of human cone photoreceptors stained with anti-blue opsin,” J. Comp. Neurol. 312, 610–624 (1991).
[CrossRef] [PubMed]

Asenjo, A. B.

A. B. Asenjo, J. Rim, D. D. Oprian, “Molecular determinants of human red/green colour discrimination,” Neuron 12, 1131–1138 (1994).
[CrossRef] [PubMed]

Baker, H. D.

W. A. H. Rushton, H. D. Baker, “Red/green sensitivity in normal vision,” Vision Res. 4, 75–85 (1964).
[CrossRef] [PubMed]

Baron, R.

E. Miyahara, J. Pokorny, V. C. Smith, R. Baron, “Color vision in two observers with highly biased LWS/MWS cone ratios,” Vision Res. 38, 601–612 (1998).
[CrossRef] [PubMed]

Baylor, D. A.

D. A. Baylor, B. J. Nunn, J. L. Schnapf, “Spectral sensitivity of cones of the monkey Macaca fascicularis,” J. Physiol. (London) 390, 145–160 (1987).

Berendschot, T. T. J. M.

Berenschot, T. T. J. M.

T. T. J. M. Berenschot, J. van de Kraats, D. van Norren, “Foveal cone mosaic and visual pigment density in dichromats,” J. Physiol. (London) 492, 307–314 (1996).

Bieber, M. L.

M. L. Bieber, J. M. Kraft, J. S. Werner, “Effects of known variations in photopigments on L/M cone ratios estimated from luminous efficiency functions,” Vision Res. 38, 1961–1966 (1998).
[CrossRef] [PubMed]

Billson, F. A.

C. M. Diaz-Araya, J. M. Provis, F. A. Billson, “NADPH-diaphorase histochemistry reveals cone distributions in adult human retinae,” Aust. NZ J. Ophthalmol. 21, 171–179 (1993).

Bowmaker, J. K.

J. D. Mollon, J. K. Bowmaker, “The spatial arrangement of cones in the primate fovea,” Nature 360, 677–679 (1992).
[CrossRef] [PubMed]

Brainard, D. H.

D. H. Brainard, J. Calderone, A. K. Nugent, G. H. Jacobs, “Flicker ERG responses to stimuli parametrically modulated in color space,” Invest. Ophthalmol. Visual Sci. 40, 2840–2847 (1999).

Bumsted, K.

K. Bumsted, A. Hendrickson, “Distribution and development of short-wavelength cones differ between Macaca monkey and human fovea,” J. Comp. Neurol. 403, 502–516 (1999).
[CrossRef] [PubMed]

Burns, S. A.

Calderone, J.

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G. H. Jacobs, J. Neitz, “Electrophysiological estimates of individual variation in L/M cone ratio,” in Colour Vision Deficiencies XI, B. Drum, ed. (Kluwer, Dordrecht, The Netherlands, 1993), pp. 107–112.

G. Wyszecki, W. S. Stiles, Color Science: Concepts and Methods, Quantitative Data and Formulae, 2nd ed. (Wiley, New York, 1982).

J. Pokorny, V. C. Smith, M. Wesner, “Variability in cone populations and implications,” in From Pigments to Perception: Advances in Understanding Visual Processes, A. Valberg, B. B. Lee, eds. (Plenum, New York, 1991), pp. 23–34.

P. Lennie, P. W. Haake, D. R. Williams, “The design of chromatically opponent receptive fields,” in Computational Models of Visual Processing, M. S. Landy, J. A. Movshon, eds. (MIT Press, Cambridge, Mass., 1991), pp. 71–82.

Further information can be provided by J. Neitz, who performed work in this regard during 1999 at the Medical College of Wisconsin. He can be reached at the address on the title page.

S. A. Hagstrom, “Characterization of cone pigment genes expressed in human retina and in individual cone photoreceptors,” Ph.D. dissertation (Medical College of Wisconsin, Milwaukee, Wis., 1995).

S. A. Hagstrom, J. Neitz, M. Neitz, “Ratio of M/L pigment gene expression decreases with retinal eccentricity,” in Colour Vision Deficiencies XIII, C. R. Cavonius, ed. (Kluwer Academic, Dordrecht, The Netherlands, 1997).

For observer AN, three rather than two equations were obtained at 640 nm.

R. J. W. Mansfield, “Primate cone photopigments and cone mechanisms,” in The Visual System, A. Fein, J. S. Levine, eds. (Liss, New York, 1985), pp. 89–106.

G. H. Jacobs, J. B. Calderone, “Evaluation of the genetic contribution to individual variations in the spectral sensitivity of deuteranopes,” in John Dalton’s Colour Vision Legacy, C. Dickinson, I. Murray, D. Carden, eds. (Taylor & Francis, London, 1997), pp. 47–54.

Further information can be provided by G. H. Jacobs, who performed work in this regard during the period 1990–1998 at the University of California, Santa Barbara. He can be reached at the address on the title page.

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Figures (4)

Fig. 1
Fig. 1

Pseudocolor images of the trichromatic cone mosaics of JW and AN at 1 deg eccentricity. Red, green, and blue colors represent the L, M, and S cones, respectively. Left: AN’s nasal retina; right: JW’s temporal retina. The scale bar represents 5 min of visual angle. Images reprinted from Ref. 10 with permission from its authors and with copyright permission from its publisher.

Fig. 2
Fig. 2

Codon numbers and amino acid positions are given for the 11 polymorphic positions encoded by exons 2–4. For exon 5, only the two positions involved in determining the spectral difference between L (Y277 and T285) and M (F277 and A285) pigments are shown. For each observer, sequence information is provided in two rows. The first row is for the L cones; the second row is for the M cones. At each position, for each cone type, there is either a black or a white circle. A key translating circle color to amino acid identity at each position is provided in the bottom two rows of the figure. The single-letter amino acid code is used: T, threonine; I, isoleucine; V, valine; Y, tyrosine; S, serine; M, methionine; A, alanine; F, phenylalanine.

Fig. 3
Fig. 3

ERG spectral sensitivity functions. Each panel shows data for one observer. The solid curves show the best fit to the measured spectra obtained with a weighted sum of L and M cone photopigment absorption spectra. Left (AN): fit with M cone λ-max value of 531 nm; L cone λ-max value of 563 nm; L/M cone ratio, 1.06. Right (JW): fit with M cone λ-max value of 531 nm; L cone λ-max value 559 nm; L/M cone ratio, 3.38. The maximum standard error of measurement for the measured sensitivities was 0.02 log unit, comparable in size with the plotted data points. The data shown are normalized so that each observer has a peak sensitivity of 0 log unit. Tabulated spectral sensitivity data may be obtained from the World Wide Web at http://color.psych.ucsb.edu/ERG/JOSA2000.txt.

Fig. 4
Fig. 4

Predictions for unique yellow based on model described in the text. The figure shows predicted wavelength for unique yellow as a function of L/M cone ratio. To make the predictions we used the Smith–Pokorny estimates of the cone spectral sensitivities, and we set the constant k by requiring that the prediction for an L/M cone ratio of 2 be 580 nm.

Tables (1)

Tables Icon

Table 1 Estimates of L/M Signal Ratio Derived from Flicker ERGa

Equations (2)

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S(λ)=log 10[(Nl/Nm)L(λ)+M(λ)]+c.
(Nl/Nm)L(λy)-kM(λy)=0,

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