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The relationship between ambient lighting conditions, absolute dark-adapted thresholds, and rhodopsin in black and hypopigmented mice

Published online by Cambridge University Press:  25 February 2005

GERARD H. DALY ,
JESSICA M. DILEONARDO ,
NATALIE R. BALKEMA  and
GRANT W. BALKEMA
GERARD H. DALY
Affiliation:
Biology Department, Boston College, Chestnut Hill
JESSICA M. DILEONARDO
Affiliation:
Biology Department, Boston College, Chestnut Hill
NATALIE R. BALKEMA
Affiliation:
Biology Department, Boston College, Chestnut Hill
GRANT W. BALKEMA
Affiliation:
Biology Department, Boston College, Chestnut Hill
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Abstract

Significant variation in absolute dark-adapted thresholds is observed both within and between strains of mice with differing ocular pigmentation levels. Differences in threshold within a single strain are related to the Williams' photostasis effect, that is, photoreceptor rhodopsin levels are dependent upon ambient lighting conditions. To examine threshold differences among strains, we equalized rhodopsin levels by maintaining albino mice (c2J/c2J) at 2 × 10−4 cd/m2 (dim light) and black mice at 2 × 102 cd/m2 (bright light). This resulted in ocular rhodopsin levels for albino mice (albino—dim) of 494 ± 11 pmoles/eye and rhodopsin levels for black mice (black—bright) of 506 ± 25 pmoles/eye. For comparison, rhodopsin levels in black mice maintained in dim light are 586 ± 46 pmoles/eye and 217 ± 46 pmoles/eye in albino mice maintained in bright light. We found similar dark-adapted thresholds (6.38 log cd/m2vs. 6.47 log cd/m2)) in albino and black mice with equivalent rhodopsin determined with a water maze test. This suggests that dark-adapted thresholds are directly related to rhodopsin levels regardless of the level of ocular melanin. The number of photoreceptors, photoreceptor layer thickness, and outer segment length did not differ significantly between albino (dark) and black mice (bright). These results demonstrate that the visual sensitivity defect found in hypopigmented animals is secondary to abnormal rhodopsin regulation and that hypopigmented animals have either an improper input to the photostasis mechanism or that the photostasis mechanism is defective.

Keywords

HypopigmentationAlbinoVisual thresholdsRetinal degeneration
Type
Research Article
Information
Visual Neuroscience , Volume 21 , Issue 6 , November 2004 , pp. 925 - 934
Copyright
© 2004 Cambridge University Press

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Footnotes

This paper is dedicated to the loving memory of Grant W. Balkema, a true friend and mentor.

References

REFERENCES

Abercrombie, M. (1946). Estimation of nuclear population from microtome sections. Anatomical Record 94, 239–247.Google Scholar
Balkema, G.W. (1979). A study of visual abnormalities in mutant mice: A retinal sensitivity defect in the mutant mouse pearl. Doctoral Thesis, Purdue University.
Balkema, G.W. (1988). Elevated dark-adopted thresholds in albino rodents. Investigative Ophthalmology and Visual Science 29, 544–549.Google Scholar
Balkema, G.W., Jr. & Pinto, L.H. (1982). Electrophysiology of retinal ganglion cells in the mouse: A study of a normally pigmented mouse and a congenic hypopigmentation mutant, pearl. Journal of Neurophysiology 48, 968–980.Google Scholar
Balkema, G.W. & Drager, U.C. (1991). Impaired visual thresholds in hypopigmented animals. Visual Neuroscience 6, 577–585.Google Scholar
Balkema, G.W. & MacDonald, S. (1998). Increased absolute light sensitivity in himalayan mice with cold-induced ocular pigmentation. Visual Neuroscience 15, 841–849.Google Scholar
Balkema, G.W., Jr., Pinto, L.H., Dräger, U.C., & Vanable, J.W., Jr. (1981). Characterization of abnormalities in the visual system of the mutant mouse pearl. Journal of Neuroscience 1, 1320–1329.Google Scholar
Balkema, G.W., Cusick, K., & Nguyen, T.H. (2001). Diurnal variation in synaptic ribbon length and visual threshold. Visual Neuroscience 18, 789–797.Google Scholar
Behn, D., Doke, A., Racine, J., Casanova, C., Chemtob, S., & Lachapelle, P. (2003). Dark adaptation is faster in pigmented than albino rats. Documenta Ophthalmologica 106, 153–159.Google Scholar
Chan, S.O., Baker, G.E., & Guillery, R.W. (1993). Differential action of the albino mutation on two components of the rat's uncrossed retinofugal pathway. Journal of Comparative Neurology 336, 362–377.Google Scholar
Creel, D. (1980). Inappropriate use of albino animals as models in research. Pharmacology and Biochemistry Behavior 12, 969–967.Google Scholar
Cronin, C.A., Ryan, A.B., Talley, E.M., & Scrable, H. (2003). Tyrosinase expression during neuroblast divisions affects later pathfinding by retinal ganglion cells. Journal of Neuroscience 23, 11692–11697.Google Scholar
Danciger, M., Matthes, M.T., Yasamura, D., Akhmedov, N.B., Rickabaugh, T., Gentleman, S., Redmond, T.M., La Vail, M.M., & Farber, D.B. (2000). A QTL on distal chromosome 3 that influences the severity of light-induced damage to mouse photoreceptors. Mammalian Genome 11, 422–427.Google Scholar
Danciger, M., Lyon, J., Worrill, D., Hoffman, S., Lem, J., Reme, C.E., Wenzel, A., & Grimm, C. (2004). New retinal light damage QTL in mice with the light-sensitive RPE65 LEU variant. Mammalian Genome 15, 277–283.Google Scholar
Donatien, P. & Jeffery, G. (2002). Correlation between rod photoreceptor numbers and levels of ocular pigmentation. Investigative Ophthalmology and Visual Science 43, 1198–1203.Google Scholar
Dräger, U.C. (1985). Calcium binding in pigmented and albino eyes. Proceedings of the National Academy of Science of the U.S.A. 82, 6716–6720.Google Scholar
Dräger, U.C. & Balkema, G.W. (1987). Does melanin do more than protect from light? Neuroscience Research Suppl. 6, S75–86.Google Scholar
Fain, G.L., Matthews, H.R., Cornwall, M.C., & Koutalos, Y. (2001). Adaptation in vertebrate photoreceptors. Physiological Review 81, 117–151.Google Scholar
Fox, D.A., Poblenz, A.T., & He, L. (1999). Calcium overload triggers rod photoreceptor apoptotic cell death in chemical-induced and inherited retinal degenerations. Annals of the New York Academy of Science 893, 282–285.Google Scholar
Fox, D.A., Poblenz, A.T., He, L., Harris, J.B., & Medrano, C.J. (2003). Pharmacological strategies to block rod photoreceptor apoptosis caused by calcium overload: A mechanistic target-site approach to neuroprotection. European Journal of Ophthalmology 13 (Suppl. 3), S44–56.Google Scholar
Grant, S., Patel, N.N., Philp, A.R., Grey, C.N., Lucas, R.D., Foster, R.G., Bowmaker, J.K., & Jeffery, G. (2001). Rod photopigment deficits in albinos are specific to mammals and arise during retinal development. Visual Neuroscience 18, 245–251.Google Scholar
Green, D.G., Herreros de Tejada, P., & Glover, M.J. (1991). Are albino rats night blind? Investigative Ophthalmology and Visual Science 32, 2366–2371.Google Scholar
Green, D.G., Herreros-de-Tejada, P., & Glover, M.J. (1992). Night vision in mice. Investigative Ophthalmology and Visual Science 33, 1407.Google Scholar
Green, D.G., Herreros de Tejada, P., & Glover, M.J. (1994). Electrophysiological estimates of visual sensitivity in albino and pigmented mice. Visual Neuroscience 11, 919–925.Google Scholar
Gresh, J., Goletz, P.W., Crouch, R.K., & Rohrer, B. (2003). Structure–function analysis of rods and cones in juvenile, adult, and aged C57bl/6 and Balb/c mice. Visual Neuroscience 20, 211–220.Google Scholar
Harosi, F.I. & Malerba, F.E. (1975). Plane-polarized light in microspectrophotometry. Vision Research 15, 379–388.Google Scholar
Hayes, J.M. & Balkema, G.W. (1993a). Elevated dark-adapted thresholds in hypopigmented mice measured with a water maze screening apparatus. Behavior Genetics 23, 395–403.Google Scholar
Hayes, J.M. & Balkema, G.W. (1993b). Visual thresholds in mice: Comparison of retinal light damage and hypopigmentation. Visual Neuroscience 10, 931–938.Google Scholar
He, L., Poblenz, A.T., Medrano, C.J., & Fox, D.A. (2000). Lead and calcium produce rod photoreceptor cell apoptosis by opening the mitochondrial permeability transition pore. Journal of Biological Chemistry 275, 12175–12184.Google Scholar
Herreros de Tejada, P., Green, D.G., & Munoz Tedo, C. (1992). Visual thresholds in albino and pigmented rats. Visual Neuroscience 9, 409–414.Google Scholar
Herreros de Tejada, P., Munoz Tedo, C., & Costi, C. (1997). Behavioral estimates of absolute visual threshold in mice. Vision Research 37, 2427–2432.Google Scholar
Jeffery, G., Schutz, G., & Montoliu, L. (1994a). Correction of abnormal retinal pathways found with albinism by introduction of a functional tyrosinase gene in transgenic mice. Developmental Biology 166, 460–464.Google Scholar
Jeffery, G., Darling, K., & Whitmore, A. (1994b). Melanin and the regulation of mammalian photoreceptor topography. European Journal of Neuroscience 6, 657–667.Google Scholar
Jeffery, G., Brem, G., & Montoliu, L. (1997). Correction of retinal abnormalities found in albinism by introduction of a functional tyrosinase gene in transgenic mice and rabbits. Brain Research Developmental Brain Research 99, 95–102.Google Scholar
Koch, K.W. & Stryer, L. (1988). Highly cooperative feedback control of retinal rod guanylate cyclase by calcium ions. Nature 334, 64–66.Google Scholar
LaVail, M., Gorrin, G., Repaci, M., Thomas, L., & Ginsberg, H. (1987a). Genetic regulation of light damage to photoreceptors. Investigative Ophthalmology and Visual Science 28, 1043–1048.Google Scholar
LaVail, M.M., Gorrin, G.M., & Repaci, M.A. (1987b). Strain differences in sensitivity to light-induced photoreceptor degeneration in albino mice. Current Eye Research 6, 825–834.Google Scholar
LaVail, M.M., Gorrin, G.M., Repaci, M.A., & Yasumura, D. (1987c). Light-induced retinal degeneration in albino mice and rats: Strain and species differences. Progress in Clinical and Biological Research 247, 439–454.Google Scholar
Lavallee, C., Chalfoux, J., Moosally, A., & Balkema, G. (2003). Elevated free calcium levels in the sub-retinal space elevate the absolute dark-adapted threshold in hypopigmented mice. Journal of Neurophysiology 90, 3654–3662.Google Scholar
Le Fur, N., Kelsall, S., & Mintz, B. (1996). Base substitution at different alternative splice donor sites of the tyrosinase gene in murine albinism. Genomics 37, 245–248.Google Scholar
Loeffler, K.U. & Mangini, N.J. (1998). Immunohistochemical localization of Na+/Ca2+ exchanger in human retina and retinal pigment epithelium. Graefes Archives in Clinical and Experimental Ophthalmology 236, 929–933.Google Scholar
Matthews, H.R., Murphy, R.L., Fain, G.L., & Lamb, T.D. (1988). Photoreceptor light adaptation is mediated by cytoplasmic calcium concentration. Nature 334, 67–69.Google Scholar
Munoz Tedo, C., Herreros de Tejada, P., & Green, D.G. (1994). Behavioral estimates of absolute threshold in rat. Visual Neuroscience 11, 1077–1082.Google Scholar
Nusinowitz, S., Nguyen, L., Radu, R., Kashani, Z., Farber, D., & Danciger, M. (2003). Electroretinographic evidence for altered phototransduction gain and slowed recovery from photobleaches in albino mice with a MET450 variant in RPE65. Experimental Eye Research 77, 627–638.Google Scholar
Pugh, E.N. & Lamb, T.D. (2000). Phototransduction in vertebrate rods and cones: Molecular mechanisms of amplification, recovery and light adaptation. In Stavenga, D.G., De Grip, W.J. & Pugh, E.N., Jr., eds., vol. 3. North-Holland: Elsevier Science. pp. 183–255.
Rachel, R.A., Dolen, G., Hayes, N.L., Lu, A., Erskine, L., Nowakowski, R.S., & Mason, C.A. (2002). Spatiotemporal features of early neuronogenesis differ in wild-type and albino mouse retina. Journal of Neuroscience 22, 4249–4263.Google Scholar
Rapp, L.M. & Williams, T.P.. (1980). The role of ocular pigmentation in protecting against retinal light damage. Vision Research 12, 1127–1131.Google Scholar
Raven, M.A. & Reese, B.E. (2002). Horizontal cell density and mosaic regularity in pigmented and albino mouse retina. Journal of Comparative Neurology 454, 168–176.Google Scholar
Schremser, J.L. & Williams, T.P. (1995a). Rod outer segment (ROS) renewal as a mechanism for adaptation to a new intensity environment. II. Rhodopsin synthesis and packing density. Experimental Eye Research 61, 25–32.Google Scholar
Schremser, J.L. & Williams, T.P. (1995b). Rod outer segment (ROS) renewal as a mechanism for adaptation to a new intensity environment. I. Rhodopsin levels and ROS length. Experimental Eye Research 61, 17–23.Google Scholar
Udea, Y. & Steinberg, R.H. (1993). Voltage-operated calcium channels in fresh and cultured rat retinal pigment epithelial cells. Investigative Ophthalmology 12, 3408–3418.Google Scholar
Webster, M.J. & Rowe, M.H. (1991). Disruption of developmental timing in the albino rat retina. Journal of Comparative Neurology 307, 460–474.Google Scholar
Williams, M.A., Pinto, L.H., & Gherson, J. (1985). The retinal pigment epithelium of wild type (C57BL/6J +/+) and pearl mutant (C57BL/6J pe/pe) mice. Investigative Ophthalmology and Visual Science 26, 657–669.Google Scholar
Williams, T.P. (1998). Light history and photostasis: What is a ‘normal’ rat retina? In Photostasis and Related Phenomena, ed. Williams, T.P. & Thistle, A.B., pp. 17–32. Plenum Press, New York.
Williams, T.P., Henrich, S., & Reiser, M. (1998a). Effect of eye closures and openings on photostasis in albino rats. Investigative Ophthalmology and Visual Science 39, 603–609.Google Scholar
Williams, T.P., Webbers, J.P., Giordano, L., & Henderson, R.P. (1998b). Distribution of photon absorption rates across the rat retina. Journal of Physiology 508 (Pt. 2), 515–522.Google Scholar
Williams, T.P., Squitieri, A., Henderson, R.P., & Webbers, J.P. (1999). Reciprocity between light intensity and rhodopsin concentration across the rat retina. Journal of Physiology 516 (Pt. 3), 869–874.Google Scholar