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Independent variation of retinal S and M cone photoreceptor topographies: A survey of four families of mammals

Published online by Cambridge University Press:  06 September 2006

PETER KURT AHNELT
Affiliation:
Department of Physiology, Medical University of Vienna, Vienna, Austria
CHRISTIAN SCHUBERT
Affiliation:
Department of Physiology, Medical University of Vienna, Vienna, Austria
ANNA KÜBBER-HEISS
Affiliation:
Department of Veterinary Pathology, Veterinary University Vienna, Vienna, Austria
ALEXANDRA SCHIVIZ
Affiliation:
Department of Physiology, Medical University of Vienna, Vienna, Austria
ELISABETH ANGER
Affiliation:
Department of Physiology, Medical University of Vienna, Vienna, Austria

Abstract

In mammals, cone photoreceptor subtypes are thought to establish topographies that reflect the species-relevant properties of the visual environment. Middle- to long-wavelength-sensitive (M) cones are the dominant population and in most species they form an area centralis at the visual axis. Short-wavelength-sensitive (S) cone topographies do not always match this pattern. We here correlate the interrelationship of S and M cone topographies in representatives of several mammalian orders with different visual ecology, including man, cheetah, cat, Eurasian lynx, African lion, wild hog, roe deer, and red deer. Retinas were labeled with opsin antisera and S and M cone distributions as well as S/M cone ratios were mapped. We find that species inhabiting open environments show M cone horizontal streaks (cheetah, pig, deer). Species living in structured habitats (tiger, lynx, red deer) have increased S cone densities along the retinal margin. In species with active vision (cheetah, bear, tiger, man), S cone distributions are more likely to follow the centripetal M cone gradients. Small species show a ventral bias of peak S cone density which either matches the peak of M cone density in a temporal area centralis (diurnal sciurid rodents, tree shrews) or not (cat, manul, roe deer).

Thus, in addition to habitat structure, physical size and specific lifestyle patterns (e.g. food acquisition) appear to underlie the independent variations of M and S cone topographies.

Type
PHYSIOLOGY/ANATOMY
Copyright
© 2006 Cambridge University Press

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References

REFERENCES

Ahnelt, P.K., Fernandez, E., Martinez, O., Bolea, J.A., & Kübber Heiss, A. (2000). Irregular S-cone mosaics in felid retinas. Spatial interaction with axonless horizontal cells, revealed by cross correlation. Journal of the Optical Society of America A: Optics, Image Science and Vision 17, 580588.Google Scholar
Ahnelt, P.K. & Kolb, H. (2000). The mammalian photoreceptor mosaic-adaptive design. Progress in Retinal and Eye Research 19, 711777.Google Scholar
Ahnelt, P.K., Kolb, H., & Pflug, R. (1987). Identification of a subtype of cone photoreceptor, likely to be blue sensitive, in the human retina. Journal of Comparative Neurology 255, 1834.Google Scholar
Ahnelt, P.K., Kübber-Heiss, A., Glösmann, M., & Schubert, C. (2002). Two peaks in cone topographies of the domestic pig and the European wild hog retina. Experimental Eye Research [Suppl. 2 (Proc. XV ICER, Geneva)] 72, 27.Google Scholar
Ahnelt, P.K., Schubert, C., Kübber Heiss, A., & Anger, E.M. (2005). Adaptive design in retinal cone topographies of the Cheetah and other Felids. In Investigative Ophthalmology and Visual Science (ARVO abstr). p. 195.
Applebury, M.L., Antoch, M.P., Baxter, L.C., Chun, L.L., Falk, J.D., Farhangfar, F., Kage, K., Krzystolik, M.G., Lyass, L.A., & Robbins, J.T. (2000). The murine cone photoreceptor: A single cone type expresses both S and M opsins with retinal spatial patterning. Neuron 27, 513523.Google Scholar
Beirne, R.O., Zlatkova, M.B., & Anderson, R.S. (2005). Changes in human short-wavelength-sensitive and achromatic resolution acuity with retinal eccentricity and meridian. Visual Neuroscience 22, 7986.Google Scholar
Calderone, J.B. & Jacobs, G.H. (1995). Regional variations in the relative sensitivity to UV light in the mouse retina. Visual Neuroscience 12, 463468.Google Scholar
Calderone, J.B. & Jacobs, G.H. (2003). Spectral properties and retinal distribution of ferret cones. Visual Neuroscience 20, 1117.Google Scholar
Calderone, J.B., Reese, B.E., & Jacobs, G.H. (2003). Topography of photoreceptors and retinal ganglion cells in the spotted hyena (Crocuta crocuta). Brain Behavior and Evolution 62, 182192.Google Scholar
Calkins, D.J. (2001). Seeing with S cones. Progress in Retinal and Eye Research 20, 255287.Google Scholar
Curcio, C.A., Allen, K.A., Sloan, K.R., Lerea, C.L., Hurley, J.B., Klock, I.B., & Milam, A.H. (1991). Distribution and morphology of human cone photoreceptors stained with anti-blue opsin. Journal of Comparative Neurology 312, 610624.Google Scholar
de Monasterio, F.M., McCrane, E.P., Newlander, J.K., & Schein, S.J. (1985). Density profile of blue-sensitive cones along the horizontal meridian of macaque retina. Investigative Ophthalmology and Visual Science 26, 289302.Google Scholar
Famiglietti, E.V. & Sharpe, S.J. (1995). Regional topography of rod and immunocytochemically characterized “blue” and “green” cone photoreceptors in rabbit retina. Visual Neuroscience 12, 11511175.Google Scholar
Glösmann, M. (2002). Differential patterning and coexpression of cone visual pigments in the mammalian retina: An analysis of cone photoreceptor topography in rodents and insectivores. Thesis, pp. 118, University of Vienna, Vienna.
Glösmann, M. & Ahnelt, P.K. (2002). A mouse-like retinal cone phenotype in the Syrian hamster: S opsin coexpressed with M opsin in a common cone photoreceptor. Brain Research 929, 139146.Google Scholar
Haverkamp, S., Wässle, H., Duebel, J., Kuner, T., Augustine, G.J., Feng, G., & Euler, T. (2005). The primordial, blue-cone color system of the mouse retina. Journal of Neuroscience 25, 54385445.Google Scholar
Hendrickson, A. & Hicks, D. (2002). Distribution and density of medium- and short-wavelength selective cones in the domestic pig retina. Experimental Eye Research 74, 435444.Google Scholar
Hughes, A. (1975). A comparison of retinal ganglion cell topography in the plains and tree kangaroo. Journal of Physiology (London) 244, 61P63P.Google Scholar
Hughes, A. (1977). The topography of vision in mammals of contrasting life style: Comparative optics and retinal organization. In The Visual System of Vertebrates, Vol. VII/5, ed. Crescitelli, F., pp. 613756. Berlin–Heidelberg–New York: Springer.
Hughes, A. (1981). One brush tailed possum can browse as much pasture as 0.06 sheep which may indicate why this “arboreal” animal has a visual streak: Some comments on the “terrain” theory. Vision Research 21, 957958.Google Scholar
Jacobs, G.H. (1993). The distribution and nature of colour vision among the mammals. Biological Reviews 68, 413471.Google Scholar
Juliusson, B., Bergstrom, A., Rohlich, P., Ehinger, B., Van Veen, T., & Szel, A. (1994). Complementary cone fields of the rabbit retina. Investigative Ophthalmology and Visual Science 35, 811818.Google Scholar
Kaskan, P.M., Franco, E.C., Yamada, E.S., Silveira, L.C., Darlington, R.B., & Finlay, B.L. (2005). Peripheral variability and central constancy in mammalian visual system evolution. Proceedings: Biological Sciences 272, 91100.Google Scholar
Kryger, Z., Galli-Resta, L., Jacobs, G.H., & Reese, B.E. (1998). The topography of rod and cone photoreceptors in the retina of the ground squirrel. Visual Neuroscience 15, 685691.Google Scholar
Linberg, K.A., Lewis, G.P., Shaaw, C., Rex, T.S., & Fisher, S.K. (2001). Distribution of S- and M-cones in normal and experimentally detached cat retina. Journal of Comparative Neurology 430, 343356.Google Scholar
Martin, P.R. & Grünert, U. (1999). Analysis of the short wavelength-sensitive (“blue”) cone mosaic in the primate retina: Comparison of New World and Old World monkeys. Journal of Comparative Neurology 406, 114.Google Scholar
Mullen, K.T. & Kingdom, F.A. (2002). Differential distributions of red–green and blue–yellow cone opponency across the visual field. Visual Neuroscience 19, 109118.Google Scholar
Müller, B. & Peichl, L. (1989). Topography of cones and rods in the tree shrew retina. Journal of Comparative Neurology 282, 581594.Google Scholar
Peichl, L. (1992). Topography of ganglion cells in the dog and wolf retina. Journal of Comparative Neurology 324, 603620.Google Scholar
Peichl, L. (2005). Diversity of mammalian photoreceptor properties: Adaptations to habitat and lifestyle? The Anatomical Record Part A: Discoveries in Molecular, Cellular, and Evolutionary Biology 287, 10011012.Google Scholar
Peichl, L., Chavez, A.E., Ocampo, A., Mena, W., Bozinovic, F., & Palacios, A.G. (2005a). Eye and vision in the subterranean rodent cururo (Spalacopus cyanus, Octodontidae). Journal of Comparative Neurology 486, 197208.Google Scholar
Peichl, L., Dubielzig, R.R., Kübber-Heiss, A., Schubert, C., & Ahnelt, P.K. (2005b). Retinal cone types in brown bears and the polar bear indicate dichromatic color vision. In Investigative Ophthalmology and Visual Science (ARVO Abstract), pp. 195, Ft. Lauderdale.
Peichl, L., Kunzle, H., & Vogel, P. (2000). Photoreceptor types and distributions in the retinae of insectivores. Visual Neuroscience 17, 937948.Google Scholar
Reitsamer, H., Pflug, R., Röhlich, P., & Ahnelt, P. (1997). Topographic differences of spectral sensitivity in rabbit retina. Small field ERG recordings and immunohistochemistry. In Proceedings Int.Soc. Color Vision Deficiencies. XIII (Pau), ed. Cavonius, C.R., pp. 151155. Dordrecht: Kluwer Academic Publishers.
Schiviz, A. (2006). Chromatische Organisation der Artiodactylen-Retina. Beziehungen zu Systematik und Visueller Ökologie. Thesis, Veterinary University of Vienna, Vienna.
Schultze, M. (1866). Zur Anatomie und Physiologie der Retina. Archiv für Mikroskopische Anatomie 2, 175286.Google Scholar
Silveira, L.C., Picanco Diniz, C.W., & Oswaldo Cruz, E. (1989). Distribution and size of ganglion cells in the retinae of large Amazon rodents. Visual Neuroscience 2, 221235.Google Scholar
Sperling, H.G. (1986). Spectral sensitivity, intense spectral light studies and the color receptor mosaic of primates. Vision Research 16, 647657.Google Scholar
Stone, J. (1983). Parallel Processing in the Visual System. New York: Plenum Press.
Szél, A., Röhlich, P., Caffe, A.R., & Van Veen, T. (1996). Distribution of cone photoreceptors in the mammalian retina. Microscopy Research and Technique 35, 445462.Google Scholar
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.Google Scholar