Hostname: page-component-76fb5796d-wq484 Total loading time: 0 Render date: 2024-04-26T07:27:03.463Z Has data issue: false hasContentIssue false

Topography of the long- to middle-wavelength sensitive cone ratio in the human retina assessed with a wide-field color multifocal electroretinogram

Published online by Cambridge University Press:  03 July 2008

JAMES A. KUCHENBECKER
Affiliation:
Department of Ophthalmology, and Department of Cell Biology, Neurobiology & Anatomy, Medical College of Wisconsin, Milwaukee, Wisconsin
MANISHA SAHAY
Affiliation:
Department of Ophthalmology, and Department of Cell Biology, Neurobiology & Anatomy, Medical College of Wisconsin, Milwaukee, Wisconsin
DIANE M. TAIT
Affiliation:
Department of Ophthalmology, and Department of Cell Biology, Neurobiology & Anatomy, Medical College of Wisconsin, Milwaukee, Wisconsin
MAUREEN NEITZ
Affiliation:
Department of Ophthalmology, and Department of Cell Biology, Neurobiology & Anatomy, Medical College of Wisconsin, Milwaukee, Wisconsin
JAY NEITZ*
Affiliation:
Department of Ophthalmology, and Department of Cell Biology, Neurobiology & Anatomy, Medical College of Wisconsin, Milwaukee, Wisconsin
*
Address correspondence and reprint requests to: Jay Neitz, Department of Ophthalmology, The Eye Institute, 925 North 87thStreet, Milwaukee, WI 53226-4812. E-mail: jneitz@mcw.edu

Abstract

The topographical distribution of relative sensitivity to red and green lights across the retina was assayed using a custom-made wide-field color multifocal electroretinogram apparatus. There were increases in the relative sensitivity to red compared to green light in the periphery that correlate with observed increases in the relative amount of long (L) compared to middle (M) wavelength sensitive opsin mRNA. These results provide electrophysiological evidence that there is a dramatic increase in the ratio of L to M cones in the far periphery of the human retina. The central to far peripheral homogeneity in cone proportions has implications for understanding the developmental mechanisms that determine the identity of a cone as L or M and for understanding the circuitry for color vision in the peripheral retina.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2008

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

Albrecht, J., Jägle, H., Hood, D.C. & Sharpe, L.T. (2002). The multifocal electroretinogram (mfERG) and cone isolating stimuli: Variation in L- and M-cone driven signals across the retina. Journal of Vision 2, 543558.CrossRefGoogle Scholar
Bollinger, K., Sjoberg, S., Neitz, M. & Neitz, J. (2004). Topographical cone photopigment gene expression in deutan-type red-green color vision defects. Vision Research 34, 135145.CrossRefGoogle Scholar
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, ed. Mollon, J.D., Pokorny, J. & Knoblauch, K., pp. 3950. New York: Oxford University Press.CrossRefGoogle Scholar
Bumsted, K. & Hendrickson, A. (1999). Distribution and development of short-wavelength cones differ between Macaca monkey and human fovea. Journal of Comparative Neurology 403, 502516.3.0.CO;2-N>CrossRefGoogle ScholarPubMed
Bumsted, K., Jasoni, C., Szel, A. & Hendrickson, A. (1997). Spatial and temporal expression of cone opsins during monkey retinal development. Journal of Comparative Neurology 378, 117134.3.0.CO;2-7>CrossRefGoogle ScholarPubMed
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-Optics Image Science and Vision 17, 499509.CrossRefGoogle ScholarPubMed
Carroll, J., Neitz, M. & Neitz, J. (2002). Estimates of L:M cone ratio from ERG flicker photometry and genetics. Journal of Vision 2, 531542.CrossRefGoogle ScholarPubMed
Deeb, S.S., Diller, L.C., Williams, D.R. & Dacey, D.M. (2000). Interindividual and topographical variation of L:M cone ratios in monkey retinas. Journal of the Optical Society of America A 17, 538544.CrossRefGoogle ScholarPubMed
Gunther, K.L., Neitz, J. & Neitz, M. (2008). Nucleotide polymorphisms upstream of the X-chromosome opsin gene array tune L:M cone ratio. Visual Neuroscience this issue.Google 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, 19631967.CrossRefGoogle ScholarPubMed
Hagstrom, S.A., Neitz, M. & Neitz, J. (2000). Cone pigment gene expression in individual photoreceptors and the chromatic topography of the retina. Journal of the Optical Society of America A-Optics Image Science and Vision 17, 527537.CrossRefGoogle ScholarPubMed
Hofer, H., Carroll, J., Neitz, J., Neitz, M. & Williams, D.R. (2005). Organization of the human trichromatic cone mosaic. Journal of Neuroscience 25, 96699679.CrossRefGoogle ScholarPubMed
Hood, D.C., Yu, A.L., Zhang, X., Albrecht, J., Jägle, H. & Sharpe, L.T. (2002). The multifocal visual evoked potential and cone-isolating stimuli: Implications for L- to M-cone ratios and normalization. Journal of Vision 2, 178189.CrossRefGoogle ScholarPubMed
Jacobs, G.H., Neitz, J. & Krogh, K. (1996). Electroretinogram flicker photometry and its applications. Journal of the Optical Society of America 13, 641648.CrossRefGoogle ScholarPubMed
Knoblauch, J., Neitz, M. & Neitz, J. (2006). An urn model of the development of L/M cone ratios in human and macaque retina. Visual Neuroscience 23, 591596.CrossRefGoogle Scholar
Kremers, J., Stepien, M.W., Scholl, H.P. & Saito, C. (2003). Cone selective adaptation influences L- and M-cone driven signals in electroretinography and psychophysics. Journal of Vision 3, 146160.CrossRefGoogle ScholarPubMed
LaVail, M.M., Rapaport, D.H. & Rakic, P. (1991). Cytogenesis in the monkey retina. Journal of Comparative Neurology 309, 86114.CrossRefGoogle Scholar
Lindenberg, T., Horn, F.K. & Korth, M. (2003). Cyclic summation versus m-sequence technique in the multifocal ERG. Graefes Arch Clin Exp Ophthalmol 241, 505510.CrossRefGoogle ScholarPubMed
Martin, P.R., Grunert, U., Chan, T.L. & Bumsted, K. (2000). Spatial order in short-wavelength-sensitive cone photoreceptors: A comparative study of the primate retina. Journal of the Optical Society of America 17, 557579.CrossRefGoogle ScholarPubMed
McMahon, C., Carroll, J., Awua, S., Neitz, J. & Neitz, M. (2008). The L:M cone ratio in males of African descent with normal color vision. Journal of Vision 8, 19CrossRefGoogle Scholar
Murray, I.J., Parry, N.R., Kremers, J., Stepien, M. & Schild, A. (2004). Photoreceptor topography and cone-specific electroretinograms. Visual Neuroscience 21, 231235.CrossRefGoogle ScholarPubMed
Nathans, J. (1999). The evolution and physiology of human color vision: Insights from molecular genetic studies of visual pigments. Neuron 24, 299312.CrossRefGoogle ScholarPubMed
Nathans, J., Davenport, C.M., Maumenee, I.H., Lewis, R.A., Hejtmancik, J.F., Litt, M., Lovrien, E., Weleber, R., Bachynski, B., Zwas, F., Klingaman, R. & Fishman, G. (1989). Molecular genetics of blue cone monochromacy. Science 245, 831838.CrossRefGoogle ScholarPubMed
Neitz, M., Balding, S.D., McMahon, C., Sjoberg, S.A. & Neitz, J. (2006). Topography of long- and middle-wavelength sensitive cone opsin gene expression in human and Old World monkey retina. Visual Neuroscience 23, 379385.CrossRefGoogle ScholarPubMed
Ringrose, L. & Paro, R. (2004). Epigenetic regulation of cellular memory by the Polycomb and Trithorax group proteins. Annual Review Genetics 38, 413443.CrossRefGoogle ScholarPubMed
Roorda, A., Metha, A., Lennie, P. & Williams, D.R. (2001). Packing arrangement of the three cone classes in primate retina. Vision Research 41, 12911306.CrossRefGoogle ScholarPubMed
Roorda, A. & Williams, D.R. (1999). The arrangement of the three cone classes in the living human eye. Nature 397, 520522.CrossRefGoogle ScholarPubMed
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 USA 99, 10081011.CrossRefGoogle ScholarPubMed
Swanson, W.H., Ueno, T., Smith, V.C. & Pokorny, J. (1987). Temporal modulation sensitivity and pulse-detection thresholds for chromatic and luminance perturbations. Journal of the Optical Society of America 4, 13.Google ScholarPubMed
Valeton, J.M. (1983). Photoreceptor light adaptation models: An evaluation. Vision Research 23, 15491554.CrossRefGoogle ScholarPubMed
Valeton, J.M. & van Norren, D. (1983). Light adaptation of primate cones: An analysis based on extracellular data. Vision Research 23, 15391547.CrossRefGoogle ScholarPubMed
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, 429440.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 USA 96, 52515256.CrossRefGoogle ScholarPubMed
Xiao, M. & Hendrickson, A. (2000). Spatial and temporal expression of short, long/medium or both opsins in human fetal cones. Journal of Comparative Neurology 425, 545559.3.0.CO;2-3>CrossRefGoogle ScholarPubMed