Hostname: page-component-76fb5796d-x4r87 Total loading time: 0 Render date: 2024-04-25T07:54:42.829Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  02 June 2009

Peter K. Ahnelt ,
Jan Nora Hokoç  and
Pal Röhlich
Peter K. Ahnelt
Affiliation:
Department of General and Comparative Physiology, University of Vienna, Vienna, Austria
Jan Nora Hokoç
Affiliation:
Instituto de Biofisica, Centro de Ciencias da Saude, Univ. Fed. do Rio de Janeiro, Brasil
Pal Röhlich
Affiliation:
Laboratory I of Electron Microscopy and Department of Anatomy II, Semmelweis University of Medicine, H-1450 Budapest, Hungary
Get access Rights & Permissions [Opens in a new window]

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.

Keywords

VisionRetinaConesPhotopigmentsOpsinMarsupialOpossum
Type
Research Articles
Information
Visual Neuroscience , Volume 12 , Issue 5 , September 1995 , pp. 793 - 804
Copyright
Copyright © Cambridge University Press 1995

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

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, 406–427.CrossRefGoogle ScholarPubMed
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, 489–499.CrossRefGoogle ScholarPubMed
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, 546–557.Google Scholar
Bowmaker, J.K. (1977). The visual pigments, oil droplets and spectral sensitivity of the pigeon. Vision Research 17, 1129–1138.CrossRefGoogle ScholarPubMed
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, 1093–1104.CrossRefGoogle ScholarPubMed
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, 74–81.Google ScholarPubMed
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, 1–15.CrossRefGoogle ScholarPubMed
Friedman, H. (1967). Colour vision in the Virginia opossum. Nature 213, 835–936.CrossRefGoogle Scholar
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, 19–27.CrossRefGoogle ScholarPubMed
Govardovskii, V.I. & Zueva, L.V. (1987). Photoreceptors and visual pigments in sturgeons. Journal of Evolutionary Biochemistry and Physiology 23, 685–686.Google Scholar
Hoffmann, C.K. (1876–1877). Zur Anatomie der Retina. II. Über den Bau der Retina bei den Beutelthieren. Niederländisches Archiv für Zoologie 3, 195–198.Google Scholar
Hokoç, J.N. & Oswaldo-Cruz, E. (1978). Quantitative analysis of the opossum's optic nerve: an electron microscopic study. Journal of Comparative Neurology 182, 773–778.CrossRefGoogle Scholar
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, 385–396.CrossRefGoogle ScholarPubMed
Hokoç, J.N. & Moraes, A.M.M. (1992). Beta-like ganglion cells in the opossum retina: A Golgi study. Journal of Neurocytology 21, 614–622.CrossRefGoogle ScholarPubMed
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, 293–303.Google ScholarPubMed
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.Google Scholar
Jacobs, G.H. (1993). The distribution and nature of colour vision among the mammals. Biological Review 68, 413–471.CrossRefGoogle ScholarPubMed
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, 1157–1166.CrossRefGoogle ScholarPubMed
Kolb, H. (1994). The architecture of functional neural circuits in the vertebrate retina. Investigative Ophthalmology and Visual Science 35, 2385–2404.Google ScholarPubMed
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, 1207–1221.CrossRefGoogle ScholarPubMed
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. 128–145. London: Mac-millan Press.Google Scholar
Marshall, L.G., Case, J.A. & Woodburne, M.O. (1990). Phylogenetic relationships of the families of marsupials. Current Mammalogy 2, 433–505.Google Scholar
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, 465–467.Google Scholar
O'Day, K.J. (1938). The visual cells of the platypus (Ornithorhynchus). British Journal of Ophthalmology 22, 321–328.CrossRefGoogle Scholar
Ohtsuka, T. (1985). Relation of spectral types to oil droplet in cones of turtle retina. Science 229, 874–877.CrossRefGoogle ScholarPubMed
Ohtsuka, T. & Kawamata, K. (1990). Telodendrial contact of HRP-filled photoreceptors in the turtle retina: Pathways of photoreceptor coupling. Journal of Comparative Neurology 292, 599–613.CrossRefGoogle ScholarPubMed
Oswaldo-Cruz, E., Hokoç, J.N. & Sousa, A.P.B. (1979). A schematic eye for the opossum. Vision Research 19, 263–278.CrossRefGoogle ScholarPubMed
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, 465–480.CrossRefGoogle ScholarPubMed
Röhlich, P. & Szél, A. (1993). Binding sites of photoreceptor-specific antibodies COS-1, OS-2 and AO. Current Eye Research 12, 935–944.CrossRefGoogle ScholarPubMed
Silveira, L.C.L., Picanço-Diniz, C.W. & Oswaldo-Cruz, E. (1982). Contrast sensitivity function and visual acuity of the opossum. Vision Research 22, 1371–1377.sCrossRefGoogle ScholarPubMed
Szél, A., Takacs, L., Monostori, E., Diamantstein, T, Vich-Teichmann, I. & Röhlich, P. (1986a). Monoclonal antibody recognizing cone visual pigment. Experimental Eye Research 43, 871–883.CrossRefGoogle ScholarPubMed
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, 895–904.CrossRefGoogle ScholarPubMed
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, 593–602.CrossRefGoogle ScholarPubMed
Szél, A. & Röhlich, P. (1992). Two cone types of rat retina detected by anti-visual pigment antibodies. Experimental Eye Research 55, 47–52.CrossRefGoogle ScholarPubMed
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, 327–342.CrossRefGoogle ScholarPubMed
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. 275–293. New York, London: Plenum Press.CrossRefGoogle Scholar
Tovee, M.J. (1994). The molecular genetics and evolution of primate colour vision. Trends in Neurosciences 17, 30–35.CrossRefGoogle ScholarPubMed
Walls, G.H. (1939). Notes on the retinae of two opossum genera. Journal of Morphology 64, 67–87.CrossRefGoogle Scholar
Wikler, K.C. & Rakic, P. (1990). Distribution of photoreceptor sub-types in the retina of diurnal and nocturnal primates. Journal of Neuroscience 10, 3390–3401.CrossRefGoogle Scholar
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, 61–66.CrossRefGoogle ScholarPubMed
Young, H.M. & Pettigrew, J.D. (1991). Cone photoreceptors lacking oil droplets in the retina of the echidna, Tachyglossus aculeatus (Monotremata). Visual Neuroscience 6, 409–420.CrossRefGoogle ScholarPubMed