Skip to main content Accessibility help
×
Home

Photoreceptors in a primitive mammal, the South American opossum, Didelphis marsupialis aurita: Characterization with anti-opsin immunolabeling

  • Peter K. Ahnelt (a1), Jan Nora Hokoç (a2) and Pal Röhlich (a3)

Abstract

The retinas of placental mammals appear to lack the large number and morphological diversity of cone subtypes found in diurnal reptiles. We have now studied the photoreceptor layer of a South American marsupial (Didelphis marsupialis aurita) by peanut agglutinin labeling of the cone sheath and by labeling of cone outer segments with monoclonal anti-visual pigment antibodies that have been proven to consistently label middle-to-long wavelength (COS-1) and short-wavelength (OS-2) cone subpopulations in placental mammals. Besides a dominant rod population (max. = 400,000/mm2) four subtypes of cones (max. = 3000/mm2) were identified. The outer segments of three cone subtypes were labeled by COS-1: a double cone with a principal cone containing a colorless oil droplet, a single cone with oil droplet, and another single cone. A second group of single cones lacking oil droplets was labeled by OS-2 antibody. The topography of these cone subtypes showed striking anisotropies. The COS-1 labeled single cones without oil droplets were found all over the retina and constituted the dominant population in the area centralis located in the temporal quadrant of the upper, tapetal hemisphere. The population of OS-2 labeled cones was also ubiquitous although slightly higher in the upper hemisphere (200/mm2). The COS-1 labeled cones bearing an oil droplet, including the principal member of double cones, were concentrated (800/mm2) in the inferior, non-tapetal half of the retina. The two spectral types of single cones resemble those of dichromatic photopic systems in most placental mammals. The additional set of COS-1 labeled cones is a distinct marsupial feature. The presence of oil droplets in this cone subpopulation, its absence in the area centralis, and the correlation with the non-tapetal inferior hemisphere suggest a functional specialization, possibly for mesopic conditions. Thus, sauropsid features have been retained but probably with a modified function.

Copyright

References

Hide All
Ahnelt, P.K. & Kolb, H. (1994). Horizontal cells and cone photoreceptors in human retina: A Golgi–electron microscope study of spectral connectivity. Journal of Comparative Neurology 343, 406427.
Allodi, S., Cavaicante, L.A., Hokoç, J.N. & Bernardes, R.F. (1992). Genesis of neurons of the retinal ganglion cell layer in the opossum. Anatomy and Embryology 185, 489499.
Blanks, J.C. & Johnson, L.V. (1984). Specific binding of peanut lectin to a class of retinal photoreceptor cells. Investigative Ophthalmology and Visual Science 5, 546557.
Bowmaker, J.K. (1977). The visual pigments, oil droplets and spectral sensitivity of the pigeon. Vision Research 17, 11291138.
Braekevelt, C.R. (1973). Fine structure and photoreceptors of the retinal pigment epithelium and photoreceptor cells of an Australian marsupial Setonix brachyurus. Canadian Journal of Zoology 51, 10931104.
Cserháti, P., Szél, A. & Röhlich, P. (1989). Four cone types characterized by anti-visual pigment antibodies in the pigeon retina. Investigative Ophthalmology and Visual Science 30, 7481.
Fernández, E., Cuenca, N. & De Juan, J. (1993). A compiled BASIC program for analysis of spatial point patterns, application to retinal studies. Journal of Neuroscience Methods 50, 115.
Friedman, H. (1967). Colour vision in the Virginia opossum. Nature 213, 835936.
Govardovskii, V.I., Röhlich, P., Szél, A. & Khokhlova, T.V. (1992). Cones in the retina of the Mongolian gerbil, Meriones unguiculatus: An immunocytochemical and electrophysiological study. Vision Research 32, 1927.
Govardovskii, V.I. & Zueva, L.V. (1987). Photoreceptors and visual pigments in sturgeons. Journal of Evolutionary Biochemistry and Physiology 23, 685686.
Hoffmann, C.K. (1876–1877). Zur Anatomie der Retina. II. Über den Bau der Retina bei den Beutelthieren. Niederländisches Archiv für Zoologie 3, 195198.
Hokoç, J.N. & Oswaldo-Cruz, E. (1978). Quantitative analysis of the opossum's optic nerve: an electron microscopic study. Journal of Comparative Neurology 182, 773778.
Hokoç, J.N. & Oswaldo-Cruz, E. (1979). A regional specialization in the opossum's retina: Quantitative analysis of the ganglion cell layer. Journal of Comparative Neurology 183, 385396.
Hokoç, J.N. & Moraes, A.M.M. (1992). Beta-like ganglion cells in the opossum retina: A Golgi study. Journal of Neurocytology 21, 614622.
Hokoç, J.N., Gawryszewski, L.G., Volchan, E. & Rocha-Miranda, C.E. (1992). The retinal distribution of ganglion cells with crossed and uncrossed projections and the visual field representation of the opossum. Anais da Academia Brasileira de Ciencias 64, 293303.
Hokoç, J.N., de Oliveira, M.M.M. & Ahnelt, P. (1993). Three types of horizontal cells in a primitive mammal, the opossum (Didelphis marsupialis aurita): A Golgi-LM study. Investigative Ophthalmology and Visual Science (Suppl.) 34, 1152.
Jacobs, G.H. (1993). The distribution and nature of colour vision among the mammals. Biological Review 68, 413471.
Kawata, A., Oishi, T., Fukada, Y., Shichida, Y. & Yoshtzawa, T. (1992). Photoreceptor cell types in the retina of various vertebrate species: Immunocytochemistry with antibodies against rhodopsin and iodopsin. Photochemistry and Pholobiology 56, 11571166.
Kolb, H. (1994). The architecture of functional neural circuits in the vertebrate retina. Investigative Ophthalmology and Visual Science 35, 23852404.
Kolb, H. & Wang, H.H. (1985). The distribution of photoreceptors, dopaminergic amacrine cells and ganglion cells in the retina of the North American Opossum (Didelphis virginiana). Vision Research 25, 12071221.
Kolb, H. & Lipetz, L.E. (1991). The anatomical basis for colour vision in the vertebrate retina. In Vision and Visual Dysfunction, VI. The Perception of Colour, ed. Gouras, P., pp. 128145. London: Mac-millan Press.
Marshall, L.G., Case, J.A. & Woodburne, M.O. (1990). Phylogenetic relationships of the families of marsupials. Current Mammalogy 2, 433505.
O'Day, K. (1935). A preliminary note on the presence of double cones and oil droplets in the retina of marsupials. Journal of Anatomy 70, 465467.
O'Day, K.J. (1938). The visual cells of the platypus (Ornithorhynchus). British Journal of Ophthalmology 22, 321328.
Ohtsuka, T. (1985). Relation of spectral types to oil droplet in cones of turtle retina. Science 229, 874877.
Ohtsuka, T. & Kawamata, K. (1990). Telodendrial contact of HRP-filled photoreceptors in the turtle retina: Pathways of photoreceptor coupling. Journal of Comparative Neurology 292, 599613.
Oswaldo-Cruz, E., Hokoç, J.N. & Sousa, A.P.B. (1979). A schematic eye for the opossum. Vision Research 19, 263278.
Rapaport, D.H., Wilson, P.D. & Rowe, M.H. (1981). The distribution of ganglion cells in the retina of the North American opossum (Didelphis virginiana). Journal of Comparative Neurology 199, 465480.
Röhlich, P. & Szél, A. (1993). Binding sites of photoreceptor-specific antibodies COS-1, OS-2 and AO. Current Eye Research 12, 935944.
Silveira, L.C.L., Picanço-Diniz, C.W. & Oswaldo-Cruz, E. (1982). Contrast sensitivity function and visual acuity of the opossum. Vision Research 22, 13711377.s
Szél, A., Takacs, L., Monostori, E., Diamantstein, T, Vich-Teichmann, I. & Röhlich, P. (1986a). Monoclonal antibody recognizing cone visual pigment. Experimental Eye Research 43, 871883.
Szél, A., Röhlich, P. & Govardovskii, V. (1986b). Immunocytochemical discrimination of visual pigments in the retinal photoreceptors of the nocturnal gecko, Teratoscincus scincus. Experimental Eye Research 43, 895904.
Szél, A., Diamantstein, T & Röhlich, P. (1988). Identification of the blue sensitive cones in the mammalian retina by anti-visual pigment antibody. Journal of Comparative Neurology 273, 593602.
Szél, A. & Röhlich, P. (1992). Two cone types of rat retina detected by anti-visual pigment antibodies. Experimental Eye Research 55, 4752.
Szél, A., Röhlich, P., Caffe, A.R., Juliusson, B., Aouirre, G. & van Veen, T. (1992). Unique topographic separation of two spectral classes of cones in the mouse retina. Journal of Comparative Neurology 325, 327342.
Szél, A. & Röhlich, P. (1989). Colour vision and immunologically identifiable photoreceptor subtypes. In Neurobiology of Sensory Systems, ed. Sing, R.N. & Strausfeld, N.J., pp. 275293. New York, London: Plenum Press.
Tovee, M.J. (1994). The molecular genetics and evolution of primate colour vision. Trends in Neurosciences 17, 3035.
Walls, G.H. (1939). Notes on the retinae of two opossum genera. Journal of Morphology 64, 6787.
Wikler, K.C. & Rakic, P. (1990). Distribution of photoreceptor sub-types in the retina of diurnal and nocturnal primates. Journal of Neuroscience 10, 33903401.
Young, H.M. & Vaney, D.I. (1990). The retinae of Prototherian mammals possess neuronal types that are characteristic of non-mammalian retinae. Visual Neuroscience 5, 6166.
Young, H.M. & Pettigrew, J.D. (1991). Cone photoreceptors lacking oil droplets in the retina of the echidna, Tachyglossus aculeatus (Monotremata). Visual Neuroscience 6, 409420.

Keywords

Related content

Powered by UNSILO

Photoreceptors in a primitive mammal, the South American opossum, Didelphis marsupialis aurita: Characterization with anti-opsin immunolabeling

  • Peter K. Ahnelt (a1), Jan Nora Hokoç (a2) and Pal Röhlich (a3)

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed.