Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-05T14:11:22.320Z Has data issue: false hasContentIssue false
  • English
  • Français

Origins of uncrossed retinofugal projections in normal and hypopigmented mice

Published online by Cambridge University Press:  02 June 2009

Grant W. Balkema  and
Ursula C. Dräger
Grant W. Balkema
Affiliation:
Department of Neurobiology, Harvard Medical School, Boston
Ursula C. Dräger
Affiliation:
Department of Neurobiology, Harvard Medical School, Boston
Get access Rights & Permissions [Opens in a new window]

Abstract

In albinos, the retinofugal projections to the ipsilateral side of the brain are reduced (e.g., see Guillery, 1969; LaVail et al., 1978; Lund, 1965). Although all ganglion cell types are affected, in mice the displaced ganglion cell population is the main target of the albino mutation (Dräger & Olsen, 1980). Here we tested whether this preferential effect on displaced ganglion cells is a general consequence of the melanin reduction or a pleiotropic effect unique to the albino locus, retrogradely tracing tracing retinal ganglion cells in normal C57BL/6J mice and in several non-allelic hypopigmentation mutants on the same background: albino (C57BL/6J-c2J), beige (C57BL/6J-bg), pale ear (C57BL/6J-ep), ruby-eye/haze (C57BL/6J-ru-2hz), and pearl (C57BL/6J-pe). All mutants have lower overall cell counts in the ipsilateral projection, but the displaced population is disproportionately affected: the albinos contain 42% of the normal number of displaced ganglion cells, and the other mutants have an average 57% of normal counts.

The reduction in uncrossed retinofugal projections in albinos affects the inputs to the lateral geniculate nucleus and the superior colliculus, but not to the suprachiasmatic nucleus (Dräger, 1974). To address the question in which way the susceptible uncrossed projections differ from the nonsusceptible one, we compared ganglion cells backfilled from the suprachiasmatic nucleus to ganglion cells backfilled from the optic tract at geniculate level. Whereas the uncrossed optic tract projection originates from the binocular region in the ventro-temporal retina and contains a high fraction of large and displaced ganglion cells (Dräger & Olsen, 1980), both the crossed and uncrossed inputs to the suprachiasmatic nucleus originate from the entire retina with a relative preference for the lower nasal region that corresponds to part of the monocular visual field; all ganglion cells projecting to the suprachiasmatic nucleus are of medium size, and they are located in the ganglion cell layer.

These observations allow the following conclusions: (1) All genetic mutants which cause a reduction in ocular melanin, regardless of the molecular or cell-biological mechanism underlying the pigment reduction, result in decreased uncrossed projections; this confirms previous reports (LaVail et al., 1978, Sanderson et al., 1974). (2) The decrease affects only projections involved in binocular vision. (3) In mice, the ganglion cells displaced to the inner nuclear layer, and hence located closer to the retinal pigment epithelium, are disproportionately affected by the melanin reductions. These observations may provide cues to the spatio-temporal mechanism of the melanin action in the embryonic visual system.

Keywords

Suprachiasmatic nucleusMelaninAlbinismDisplaced ganglion cellsCalcium
Type
Research Articles
Information
Visual Neuroscience , Volume 4 , Issue 6 , June 1990 , pp. 595 - 604
Copyright
Copyright © Cambridge University Press 1990

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

Adams, J.C. (1977). Technical considerations on the use of horseradish peroxidase as a neuronal marker. Neuroscience 2, 141–145.CrossRefGoogle ScholarPubMed
Balkema, G.W. (1988). Elevated dark-adapted thresholds in albino rodents. Investigative Ophthalmology and Visual Science 29, 38–43.Google ScholarPubMed
Balkema, G.W., Mangini, N.J. & Pinto, L. H. (1983). Discrete visual defects in pearl mutant mice. Science 219, 1085–1087.CrossRefGoogle ScholarPubMed
Balkema, G.W., Mangini, N.J., Pinto, L.H. & Vanable, J.W. (1984). Visually evoked eye movements in mouse mutants and inbred strains. A screening report. Investigative Ophthalmology and Visual Science 25, 795–800.Google ScholarPubMed
Balkema, G.W., Pinto, L.H., Dräger, U.C. & Vanable, J.W. (1981). Characterization of abnormalities in the visual system of the mutant mouse pearl. Journal of Neuroscience 1, 1320–1329.CrossRefGoogle ScholarPubMed
Collewijn, H., Winterson, N.J. & DuBois, M.F. W. (1978). Optokinetic eye movements in albino rabbits: inversion in anterior visual field. Science 199, 1351–1353.CrossRefGoogle ScholarPubMed
Cooper, M.L. & Pettigrew, J.D. (1979). The retinothalamic pathway in Siamese cats. Journal of Comparative Neurology 187, 313–348.CrossRefGoogle ScholarPubMed
Creel, D. & Giolli, R.A. (1976). Retinogeniculate projections in albino and ocularly hypopigmented rats. Journal of Comparative Neurology 166, 445–456.CrossRefGoogle ScholarPubMed
Dogiel, A. (1895). Eim besonderer Typus von Nervenzellen in the mittleren gangliösen Schicht der Vögel-Retina. Anatomischer Anzeiger 10, 750–760.Google Scholar
Dräger, U.C. (1974). Autoradiography of tritiated proline and fucose transported transneuronally from the eye to the visual cortex in pigmented and albino mice. Brain Research 82, 284–292.CrossRefGoogle Scholar
Dräger, U.C. (1985 a). Birth dates of retinal ganglion cells giving rise to the crossed and uncrossed optic projections in the mouse. Proceedings of the Royal Society B (London) 224, 57–77.Google Scholar
Dräger, U.C. (1985 b). Calcium binding in pigmented and albino eyes. Proceedings of the National Academy of Sciences of the U.S.A. 82, 6716–6720.CrossRefGoogle ScholarPubMed
Deäger, U.C. (1986). Albinism and visual pathways. New England Journal of Medicine 314, 1636–1638.Google Scholar
Dräger, U.C. & Balkema, G.W. (1987). Does melanin do more than protect from light? Neuroscience Research (Suppl.) 6, S75–86.Google ScholarPubMed
Dräger, U.C. & Hofbauer, A. (1984). Antibodies to heavy neurofilament subunit detect a subpopulation of damaged ganglion cells in retina. Nature 309, 624–626.CrossRefGoogle ScholarPubMed
Dräger, U.C. & Olsen, J.F. (1980). Origins of crossed and uncrossed retinal projections in pigmented and albino mice. Journal of Comparative Neurology 191, 383–412.CrossRefGoogle ScholarPubMed
Dräger, U.C. & Olsen, J.F. (1981). Ganglion-cell distribution in the retina of the mouse. Investigative Ophthalmology and Visual Science 20, 285–293.Google ScholarPubMed
Frank, E., Harris, W.A. & Kennedy, M.B. (1980). Lysophosphatidyl choline fascilitates labeling of CNS projections with horseradish peroxidase. Journal of Neuroscience Methods 2, 183–189.CrossRefGoogle Scholar
Fujisawa, H., Morioka, H. & Watanabe, K. (1976). A decay of gap junctions in association with cell differentiation of neural retina in chick embryonic development. Journal of Cell Science 22, 285–296.Google ScholarPubMed
Guillery, R.W. (1969). An abnormal retinogeniculate projection in Siamese cats. Brain Research 14, 739–741.CrossRefGoogle ScholarPubMed
Guillery, R.W. (1974). Visual pathways in albinos. Scientific American 230, 44–54.CrossRefGoogle ScholarPubMed
Guillery, R.W., Hickey, T.L., Kaas, J.H., Felleman, D.L., Debruyn, E.J. & Sparks, D.L. (1984). Abnormal central visual pathways in the brain of an albino green monkey (Cercopithecus aethiops). Journal of Comparative Neurology 226, 165–183.CrossRefGoogle ScholarPubMed
Hanker, J.S., Yates, P.E., Metz, C.B. & Rustioni, A. (1977). A new specific sensitive and noncarcinogenic reagent for the demonstration of horseradish peroxidase. Histochemical Journal 9, 789–792.CrossRefGoogle ScholarPubMed
Hayes, B.P. (1976). Intercellular gap junctions in the developing retina and pigment epithelium of the chick. Anatomy and Embryology 150, 99–111.CrossRefGoogle Scholar
Hess, H.H. (1975). The high calcium content of retinal pigment epithelium. Experimental Eye Research 21, 471–479.CrossRefGoogle Scholar
Hofbauer, A. & Dräger, U.C. (1985). Depth segregation of retino-tectal projections in the mouse. Journal of Comparative Neurology 234, 465–474.CrossRefGoogle Scholar
Hood, J.D., Poole, J. P. & Freedman, L. (1976). Eye color and susceptibility to TTS. Journal of the Acoustical Society of America 59, 706–707.CrossRefGoogle ScholarPubMed
Insausti, R., Blakemore, C. & Cowan, W.M. (1984). Ganglion cell death during development of the ipsilateral retino-collicular projection in the golden hamster. Nature 308, 362–365.CrossRefGoogle Scholar
Keeler, C. (1970). Cuna moon-child albinism, 1950–1970. Journal of Heredity 61, 272–278.CrossRefGoogle ScholarPubMed
LaVail, J.H., Nixon, R.A. & Sidman, R.L. (1978). Genetic control of retinal ganglion cell projections. Journal of Comparative Neurology 182, 399–421.CrossRefGoogle ScholarPubMed
Lund, R.D. (1965). Uncrossed visual pathways of hooded and albino rats. Science 149, 1506–1507.CrossRefGoogle ScholarPubMed
Mangini, N.J., Vanable, J.W., Williams, M.A. & Pinto, L.H. (1985). The optokinetic nystagmus and ocular pigmentation of hypopigmented mouse mutants. Journal of Comparative Neurology 241,191–209.CrossRefGoogle ScholarPubMed
Moore, R.Y. (1978). Central neural control of circadian rhythms. In Frontiers in Neuroendocrinology, ed. Ganong, W.F. & Martini, L., pp. 185–206. New York: Raven Press.Google Scholar
Novak, E.K., Hui, S.W. & Swank, R.T. (1984). Platelet storage pool deficiency in mouse pigment mutations associated with seven distinct genetic loci. Blood 63, 536–544.CrossRefGoogle ScholarPubMed
O'Leary, D.D.M., Fawcet, J.W. & Cowan, W.M. (1986). Topographic targeting errors in the retinocollicular projection and their elimination by selective ganglion cell death. Journal of Neuroscience 12, 2692–2705.Google Scholar
Pak, M.W., Giolli, R.A., Pinto, L.H., Mangini, N.J., Gregory, K.M. & Vanable, J.W. (1987). Retinopretectal and accessory optic projections of normal mice and the OKN-defective mutant mice beige, beige-J, and pearl. Journal of Comparative Neurology 258, 435–446.CrossRefGoogle ScholarPubMed
Pickard, G.E. (1980). Morphological characteristics of retinal ganglion cells projecting to the suprachiasmatic nucleus: a horseradish peroxidase study. Brain Research 183, 458–465.CrossRefGoogle Scholar
Robison, W.G., Kuwabara, T. & Cogan, D.G. (1975). Lysosomes and melanin granules of the retinal pigment epithelium in a mouse model of the Chediak-Higashi syndrome. Investigative Ophthalmology and Visual Science 14, 312–317.Google Scholar
Royster, L.H., Royster, J.D. & Thomas, W.G. (1980). Representative hearing levels by race and sex in North Carolina Industry. Journal of the Acoustical Society of America 68, 551–566.CrossRefGoogle ScholarPubMed
Sanderson, K.J., Guillery, R.W. & Shackelford, R.M. (1974). Congenitally abnormal visual pathways in mink (Mustela vison) with reduced retinal pigment. Journal of Comparative Neurology 154, 225–248.CrossRefGoogle ScholarPubMed
Shatz, C.J. & Kliot, M. (1982). Prenatal misrouting of the retinogeniculate pathway in Siamese cats. Nature 300, 525–529.CrossRefGoogle ScholarPubMed
Silver, J. & Sapiro, J. (1981). Axonal guidance during development of the optic nerve: the role of pigmented epithelia and other extrinsic factors. Journal of Comparative Neurology 202, 521–538.CrossRefGoogle ScholarPubMed
Sperry, R.W. (1963). Chemoaffinity in the orderly growth of nerve fiber patterns and connections. Proceedings of the National Academy of Sciences of the U.S.A. 50, 703–710.CrossRefGoogle ScholarPubMed
Strongin, A.C. & Guillery, R.W. (1981). The distribution of melanin in the developing optic cup and stalk and its relation to cellular degeneration. Journal of Neuroscience 1, 1193–1204.CrossRefGoogle ScholarPubMed
Thompson, I.D. (1979). Changes in the uncrossed retinotectal projection after removal of the other eye at birth. Nature 279, 63–66.CrossRefGoogle ScholarPubMed
Tota, G. & Bocci, G. (1967). L'importanza del colore dell'iride nella valutazione della resistenza dell'udito all'affaticamento. Rivista Otoneuro-ostalmologica 42, 183–192.Google Scholar
Webster, M.J., Shatz, C.J., Kliot, M. & Silver, J. (1988). Abnormal pigmentation and unusual morphogenesis of the optic stalk may be correlated with retinal axon misguidance in embryonic Siamese cat. Journal of Comparative Neurology 269, 592–611.CrossRefGoogle Scholar
Winterson, B.J. & Collewijn, H. (1981). Inversion of direction selectivity to anterior fields in neurons of nucleus of the optic tract in rabbits with ocular albinism. Brain Research 220, 31–49.CrossRefGoogle ScholarPubMed