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The arrangement of the three cone classes in the living human eye

Abstract

Human colour vision depends on three classes of receptor, the short- (S), medium- (M), and long- (L) wavelength-sensitive cones. These cone classes are interleaved in a single mosaic so that, at each point in the retina, only a single class of cone samples the retinal image. As a consequence, observers with normal trichromatic colour vision are necessarily colour blind on a local spatial scale1. The limits this places on vision depend on the relative numbers and arrangement of cones. Although the topography of human S cones is known2,3, the human L- and M-cone submosaics have resisted analysis. Adaptive optics, a technique used to overcome blur in ground-based telescopes4, can also overcome blur in the eye, allowing the sharpest images ever taken of the living retina5. Here we combine adaptive optics and retinal densitometry6 to obtain what are, to our knowledge, the first images of the arrangement of S, M and L cones in the living human eye. The proportion of L to M cones is strikingly different in two male subjects, each of whom has normal colour vision. The mosaics of both subjects have large patches in which either M or L cones are missing. This arrangement reduces the eye's ability to recover colour variations of high spatial frequency in the environment but may improve the recovery of luminance variations of high spatial frequency.

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Figure 1: Images of the right eye of subject JW.
Figure 2: Scatter plots and histograms of individual cone absorptances.
Figure 3: Pseudocolour image of the trichromatic cone mosaic.

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References

  1. Williams, D. R., Sekiguchi, N., Haake, W., Brainard, D. H. & Packer, O. S. in From Pigments to Perception.(eds Valberg, A. & Lee, B. B.) 11–22 (Plenum, New York, (1991)).

    Book  Google Scholar 

  2. Williams, D. R., MacLeod, D. I. A. & Hayhoe, M. Punctate sensitivity of the blue sensitive mechanism. Vision Res. 21, 1357–1375 (1981).

    Article  CAS  Google Scholar 

  3. Curcio, C. A. et al. Distribution and morphology of human cone photoreceptors stained with anti-blue opsin. J. Comp. Neurol. 312, 610–624 (1991).

    Article  CAS  Google Scholar 

  4. Babcock, H. W. The possibility of compensating astronomical seeing. Publ. Astron. Soc. Pacif. 65, 229–236 (1953).

    Article  ADS  Google Scholar 

  5. Liang, J., Williams, D. R. & Miller, D. T. Supernormal vision and high-resolution retinal imaging through adaptive optics J. Opt. Soc. Am. A 14, 2884–2892 (1997).

    Article  ADS  CAS  Google Scholar 

  6. Campbell, F. W. & Rushton, W. A. H. Measurement of the scotopic pigment in the living human eye. J.Physiol. (Lond.) 130, 131–147 (1955).

    Article  CAS  Google Scholar 

  7. Rushton, W. A. H. & Baker, H. D. Red/green sensitivity in normal vision. Vision Res. 4, 75–85 (1964).

    Article  CAS  Google Scholar 

  8. Pokorny, J., Smith, V. C. & Wesner, M. in From Pigments to Perception(eds Valberg, A. & Lee, B. B.) 23–34 (Plenum, New York, (1991)).

    Book  Google Scholar 

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

    Article  Google Scholar 

  10. Vimal, R. L. P., Pokorny, J., Smith, V. C. & Shevell, S. K. Foveal cone thresholds. Vision Res. 29, 61–78 (1989).

    Article  CAS  Google Scholar 

  11. Jacobs, G. H. & Neitz, J. in Colour Vision Deficiencies Vol. XI(ed. Drum, B.) 107–112 (Kluwer Acedemic, Netherlands, (1993)).

    Book  Google Scholar 

  12. Jacobs, G. H. & Deegan, J. F. Spectral sensitivity of macaque monkeys measured with ERG flicker photometry. Vis. Neurosci. 14, 921–928 (1997).

    Article  CAS  Google Scholar 

  13. Bowmaker, J. K. & Dartnall, H. J. A. Visual pigments of rods and cones in a human retina. J. Physiol. (Lond.) 298, 501–511 (1980).

    Article  CAS  Google Scholar 

  14. Dartnall, H. J. A., Bowmaker, J. K. & Mollon, J. D. Human visual pigments: microspectrophotometric results from the eyes of seven persons. Proc. R. Soc. Lond. B 220, 115–130 (1983).

    Article  ADS  CAS  Google Scholar 

  15. Yamaguchi, T., Motulsky, A. G. & Deeb, S. S. Visual pigment gene structure and expression in human retinae. Hum. Mol. Genet. 6, 981–990 (1998).

    Article  Google Scholar 

  16. Hagstrom, S. A., Neitz, J. & Neitz, M. Variation in cone populations for red-green color vision examined by analysis of mRNA. NeuroReport 9, 1963–1967 (1998).

    Article  CAS  Google Scholar 

  17. Mollon, J. D. & Bowmaker, J. K. The spatial arrangement of cones in the primate fovea. Nature 360, 677–679 (1992).

    Article  ADS  CAS  Google Scholar 

  18. Packer, O. S., Williams, D. R. & Bensinger, D. G. Photoreceptor transmittance imaging of the primate photoreceptor mosaic. J. Neurosci. 16, 2251–2260 (1996).

    Article  CAS  Google Scholar 

  19. Holmgren, F. Uber den Farbensinn. Comp. Rend. Congr. Period. Intern. Sci. Med. Copenhagen 1, 80–98 (1884).

    Google Scholar 

  20. Krauskopf, J. Color appearance of small stimuli and the spatial distribution of color receptors. J. Opt. Soc. Am. 54, 1171 (1964).

    Article  Google Scholar 

  21. Brewster, D. On the undulations excited in the retina by the action of luminous points and lines. Lond. Edinb. Philos. Mag. J. Sci. 1, 169–174 (1832).

    Google Scholar 

  22. Sekiguchi, N., Williams, D. R. & Brainard, D. H. Efficiency in detection of isoluminant and isochromatic interference fringes. J. Opt. Soc. Am. A. 10, 2118–2133 (1993).

    Article  ADS  CAS  Google Scholar 

  23. Williams, D. R. in Advances in Photoreception: Proc. Symp. Frontiers Visual Sci. 135–148 (National Academy, Washington DC, (1990)).

    Google Scholar 

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

    Article  CAS  Google Scholar 

  25. Nathans, J., Thomas, D. & Hogness, D. S. Molecular genetics of human colour vision: the genes encoding blue, green and red pigments. Science 232, 193–202 (1986).

    Article  ADS  CAS  Google Scholar 

  26. Mollon, J. D. “Tho' she kneeled in that place where they grew...”: The uses and origins of primate colour vision. J. Exp. Biol. 146, 21–38 (1989).

    CAS  Google Scholar 

  27. Diggle, P. J. Statistical Analysis of Spatial Point Patterns(Academic, London, (1983)).

    MATH  Google Scholar 

Download references

Acknowledgements

We thank D. Brainard, D. Dacey, J. Jacobs, J. Liang, D. Miller and O. Packer for their assistance. We acknowledge financial support from the Fight for Sight research division of Prevent Blindness America (to A.R.) and the National Eye Institute and Research to Prevent Blindness (to D.R.W.).

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Roorda, A., Williams, D. The arrangement of the three cone classes in the living human eye. Nature 397, 520–522 (1999). https://doi.org/10.1038/17383

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