Hostname: page-component-8448b6f56d-42gr6 Total loading time: 0 Render date: 2024-04-23T21:57:59.978Z Has data issue: false hasContentIssue false
  • English
  • Français

Photopigment optical density of the human foveola and a paradoxical senescent increase outside the fovea

Published online by Cambridge University Press:  25 February 2005

AGNES B. RENNER ,
HOLGER KNAU ,
MAUREEN NEITZ ,
JAY NEITZ  and
JOHN S. WERNER
AGNES B. RENNER
Affiliation:
Department of Ophthalmology and Section of Neurobiology, Physiology and Behavior, University of California, Davis, Sacramento
HOLGER KNAU
Affiliation:
Department of Ophthalmology and Section of Neurobiology, Physiology and Behavior, University of California, Davis, Sacramento
MAUREEN NEITZ
Affiliation:
Department of Ophthalmology and Department of Cell Biology, Neurobiology, and Anatomy, Medical College of Wisconsin, Milwaukee
JAY NEITZ
Affiliation:
Department of Ophthalmology and Department of Cell Biology, Neurobiology, and Anatomy, Medical College of Wisconsin, Milwaukee
JOHN S. WERNER
Affiliation:
Department of Ophthalmology and Section of Neurobiology, Physiology and Behavior, University of California, Davis, Sacramento
Get access Rights & Permissions [Opens in a new window]

Abstract

Photopigment optical density (OD) of middle-(M) and long-(L) wavelength-sensitive cones was determined to evaluate the hypothesis that reductions in the amount of photopigment are responsible for age-dependent sensitivity losses of the human cone pathways. Flicker thresholds were measured at the peak and tail of the photoreceptor's absorption spectrum as a function of the intensity of a bleaching background. Photopigment OD was measured at 0 (fovea), 2, 4, and 8 deg in the temporal retina by use of a 0.3-deg-diameter test spot. Seventy-two genetically characterized dichromats were studied so that the L- and M-cones could be analyzed separately. Subjects included 28 protanopes with M- but no L-cones and 44 deuteranopes with L- but no M-cones (all male, age range 12–29 and 55–83 years). Previous methods have not provided estimates of photopigment OD for separate cone classes in the foveola. In this study, it was found that foveolar cones are remarkably efficient, absorbing 78% of the available photons (OD = 0.65). Photopigment OD decreased exponentially with retinal eccentricity independently of age and cone type. Paradoxically, the OD of perifoveal cones increased significantly with age. Over the 70-year age range of our participants, the perifoveal M- and L-cones showed a 14% increase in capacity to absorb photons despite a 30% decrease in visual sensitivity over the same period.

Keywords

ConesPhotopigment optical densityAgingDichromacyColor blindness
Type
Research Article
Information
Visual Neuroscience , Volume 21 , Issue 6 , November 2004 , pp. 827 - 834
Copyright
© 2004 Cambridge University Press

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

REFERENCES

Alpern, M. (1979). Lack of uniformity in colour matching. Journal of Physiology (London) 288, 85–105.Google Scholar
American Conference of Governmental Industrial Hygienists (ACGIH) (2003). TLV's, Threshold Limit Values and Biological Exposure Indices for 2003. American Conference of Governmental Industrial Hygienists, Cincinnati, OH.
Asenjo, A.B., Rim, J., & Oprian, D.D. (1994). Molecular determinants of human red/green color discrimination. Neuron 12, 1131–1138.Google Scholar
Berendschot, T.T.J.M., van de Kraats, J., & van Norren, D. (1996). Foveal cone mosaic and visual pigment density in dichromats. Journal of Physiology (London) 492, 307–314.Google Scholar
Bowmaker, J.K. & Dartnall, H.J.A. (1980). Visual pigments of rods and cones in a human retina. Journal of Physiology (London) 298, 501–511.Google Scholar
Burns, S.A. & Elsner, A.E. (1993). Color matching at high illuminances: Photopigment optical density and pupil entry. Journal of the Optical Society of America A 10, 221–230.Google Scholar
Carroll, J., Neitz, M., Hofer, H., Neitz, J., & Williams, D.R. (2004). Functional photoreceptor loss revealed with adaptive optics: An alternate cause of color blindness. Proceedings of the National Academy of Sciences of the U.S.A. 101, 22, 8461–8466.Google Scholar
Coile, D.C. & Baker, H.D. (1992). Foveal dark adaptation, photopigment regeneration, and aging. Visual Neuroscience 8, 27–39.Google Scholar
DeLint, P.J., Vos, J.J., Berendschot, T.T.J.M., & Van Norren, D. (1997). On the Stiles–Crawford effect with age. Investigative Ophthalmology and Visual Science 38, 1271–1274.Google Scholar
Eisner, A., Fleming, S.A., Klein, M.L., & Mauldin, W.M. (1987). Sensitivities in older eyes with good acuity: cross-sectional norms. Investigative Ophthalmology and Visual Science 28, 1824–1831.Google Scholar
Elsner, A.E., Berk, L., Burns, S.A., & Rosenberg, P.R. (1988). Aging and human cone photopigments. Journal of the Optical Society of America A 5, 2106–2112.Google Scholar
Elsner, A.E., Burns, S.A., & Webb, R.H. (1993). Mapping cone photopigment optical density. Journal of the Optical Society of America A 10, 52–58.Google Scholar
Elsner, A.E., Burns, S.A., Beausencourt, E., & Weiter, J.J. (1998). Foveal cone pigment distribution: small alterations associated with macular pigment distribution. Investigative Ophthalmology and Visual Science 39, 2394–2404.Google Scholar
Enoch, J.M. & Stiles, W.S. (1961). The colour change of monochromatic light with retinal angle of incidence. Optica Acta 8, 329–358.Google Scholar
Gerth, C., Garcia, S.M., Ma, L., Keltner, J.L., & Werner, J.S. (2002). Multifocal electroretinogram: Age-related changes for different luminance levels. Graefe's Archive for Clinical and Experimental Ophthalmology 240, 202–208.Google Scholar
Gorrand, J.-M. & Delori, F.C. (1999). Reflectance and curvature of the inner limiting membrane at the foveola. Journal of the Optical Society of America A 6, 1229–1237.Google Scholar
Keunen, J.E.E., van Norren, D., & van Meel, G.J. (1987). Density of foveal cone pigments at older age. Investigative Ophthalmology and Visual Science 28, 985–991.Google Scholar
Kilbride, P.E., Hutman, L.P., Fishman, M., & Read, J.S. (1986). Foveal cone pigment density difference in the aging human eye. Vision Research 26, 321–325.Google Scholar
King-Smith, P.E. (1973a). The optical density of erythrolable determined by retinal densitometry using the self-screening method. Journal of Physiology (London) 230, 535–549.Google Scholar
King-Smith, P.E. (1973b). The optical density of erythrolable determined by a new method. Journal of Physiology (London) 230, 551–560.Google Scholar
Knoblauch, K., Vital-Durand, F., & Barbur, J.L. (2001). Variation of chromatic sensitivity across the life span. Vision Research 41, 23–36.Google Scholar
Marcos, S., Tornow, R.-P., Elsner, A.E., & Navarro, R. (1997). Foveal cone spacing and cone photopigment density difference: Objective measurements in the same subjects. Vision Research 37, 1909–1915.Google Scholar
Marshall, J. (1978). Aging changes in human cones. In XXIII Concilium Ophthalmologicum, Kyoto, ed. Shimzu, K. & Oosterhuis, J.A., pp. 375–378. Amsterdam: Elsevier North-Holland.
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. Photochemistry and Photobiology 58, 706–710.Google Scholar
Miller, S.S. (1972). Psychophysical estimates of visual pigment densities in red–green dichromats. Journal of Physiology (London) 223, 89–107.Google Scholar
Neitz, J., Neitz, M., He, J.C., & Shevell, S.K. (1999). Trichromatic color vision with only two spectrally distinct photopigments. Nature Neuroscience 2, 884–888.Google Scholar
Neitz, M., Neitz, J., & Jacobs, G.H. (1991). Spectral tuning of pigments underlying red–green color vision. Science 252, 971–974.Google Scholar
Neitz, M., Carroll, J., Renner, A., Knau, H., Werner, J.S., & Neitz, J. (2004). Variety of genotypes in males diagnosed as dichromatic on a conventional clinical anomaloscope. Visual Neuroscience 21, 205–216.Google Scholar
Picotte, C.J., Stromeyer, C.F., III, & Eskew, R.T., Jr. (1994). The foveal color-match-area-effect. Vision Research 34, 1605–1608.Google Scholar
Pokorny, J., Smith, V.C., & Starr, S.J. (1976). Variability of color mixture data—II. The effect of viewing field size on the unit coordinates. Vision Research 16, 1095–1098.Google Scholar
Polyak, S.L. (1941). The Retina. Chicago, Illinois: University of Chicago Press.
Rushton, W.A.H. (1963a). The density of chlorolable in the foveal cones of the protanope. Journal of Physiology (London) 168, 360–373.Google Scholar
Rushton, W.A.H. (1963b). Cone pigment kinetics in the protanope. Journal of Physiology (London) 168, 374–388.Google Scholar
Rushton, W.A.H. (1965). Cone pigment kinetics in the deuteranope. Journal of Physiology (London) 176, 38–45.Google Scholar
Rynders, M.C., Grosvenor, T., & Enoch, J.M. (1995). Stability of the Stiles–Crawford function in a unilateral amblyopic subject over a 38-year period: A case study. Optometry and Vision Science 72, 177–185.Google Scholar
Schefrin, B.E., Werner, J.S., Plach, M., & Utlaut, N. (1992). Sites of age-related sensitivity loss in a short-wave cone pathway. Journal of the Optical Society of America A 9, 355–363.Google Scholar
Schefrin, B.E., Shinomori, K., & Werner, J.S. (1995). Contributions of neural pathways to age-related losses in chromatic discrimination. Journal of the Optical Society of America A 12, 1233–1241.Google Scholar
Schremser, J.-L. & Williams, T.P. (1992). Photoreceptor plasticity in the albino rat retina following unilateral optic nerve section. Experimental Eye Research 55, 393–399.Google Scholar
Smith, V.C. & Pokorny, J. (1973). Psychophysical estimates of optical density in human cones. Vision Research 13, 1199–1202.Google Scholar
Stockman, A. & Sharpe, L.T. (2000). The spectral sensitivities of the middle-and long-wavelength-sensitive cones derived from measurements in observers of known genotype. Vision Research 40, 1711–1737.Google Scholar
Swanson, W.H. & Fish, G.E. (1996). Age-related changes in the color-match-area effect. Vision Research 36, 2079–2085.Google Scholar
Tucker, G.S. (1986). Refractile bodies in the inner segments of cones in the aging human retina. Investigative Ophthalmology and Visual Science 27, 708–715.Google Scholar
Viénot, F. (2001). Retinal distributions of the macular pigment and the cone effective optical density from colour matches of real observers. Color Research and Application 26, 264–268.Google Scholar
Walraven, P.L. & Bouman, M.A. (1960). Relation between directional sensitivity and spectral response curves in human vision. Journal of the Optical Society of America 50, 780–784.Google Scholar
Werner, J.S., Donnelly, S.K., & Kliegl, R. (1987). Aging and human macular pigment density; appended with translations from the work of Max Schultze and Ewald Hering. Vision Research 27, 257–268.Google Scholar
Werner, J.S., Bieber, M.L., & Schefrin, B.E. (2000). Senescence of foveal and parafoveal cone sensitivities and their relations to macular pigment density. Journal of the Optical Society of America A 17, 1918–1932.Google Scholar
Westheimer, G. (1966). The Maxwellian view. Vision Research 6, 669–682.Google Scholar