Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-17T11:22:56.229Z Has data issue: false hasContentIssue false

Rod bipolar cells in the cone-dominated retina of the tree shrew Tupaia belangeri

Published online by Cambridge University Press:  02 June 2009

Brigitte Müller
Affiliation:
Max-Planck Institut für Hirnforschung, Frankfurt/M., Germany
Leo Peichl
Affiliation:
Max-Planck Institut für Hirnforschung, Frankfurt/M., Germany

Abstract

The tree shrew has a cone-dominated retina with a rod proportion of 5%, in contrast to the common mammalian pattern of rod-dominated retinae. As a first step to elucidate the rod pathway in the tree shrew retina, we have demonstrated the presence of rod bipolar cells and studied their morphology and distribution by light and electron microscopy.

Rod bipolar cells were labeled with an antiserum against the protein kinase C (PKC), a phosphorylating enzyme. Intense PKC immunoreactivity was found in perikarya, axons, and dendrites of rod bipolar cells. The cell bodies are located in the sclerad part of the inner nuclear layer, the dendrites ascend to the outer plexiform layer where they are postsynaptic to rod spherules, and an axon descends towards the inner plexiform layer (IPL). The axons branch, and terminate in the vitread third of the IPL where mammalian rod bipolar cells are known to terminate. Two amacrine cell processes are always seen as the postsynaptic elements (dyads). Dendritic and axonal arbors of rod bipolar cells are rather large, up to 100 μm in diameter. The topographical distribution of the rod bipolar cells was analyzed quantitatively in tangential sections.Their density ranges from 300 cells/mm2 in peripheral retina to 900 cells/mm2 more centrally. The distribution is rather flat with no local extremes. Consistent with the low rod proportion in tree shrew, the rod bipolar cell density is low compared to the rod-dominated cat retina for example (36,000-47,000 rod bipolar cells/mm2). Rod-to-rod bipolar cell ratios in the tree shrew retina range from smaller than 1 to about 7, and thus are also lower than in cat.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1991

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

Boycott, B.B. & Dowling, J.E. (1969). Organization of the primate retina: light microscopy. Philosophical Transactions of the Royal Society B (London) 255, 109184.Google Scholar
Boycott, B.B. & Kolb, H. (1973). The connections between bipolar cells and photoreceptor cells in the retina of the domestic cat. Journal of Comparative Neurology 148, 91114.CrossRefGoogle ScholarPubMed
Boycott, B.B., Hopkins, J.M. & Sperling, H.G. (1987). Cone connections of the horizontal cells of the rhesus monkey's retina. Proceedings of the Royal Society B (London) 229, 345379.Google ScholarPubMed
Cajal, S.R. (1893). La rétine des vertébrés. Cellule 9, 119257.Google Scholar
Dacheux, R.F. & Raviola, E. (1986). The rod pathway in the rabbit retina: a depolarizing bipolar and amacrine cell. Journal of Neuroscience 6, 331345.CrossRefGoogle ScholarPubMed
Daw, N.W., Jensen, R.J. & Brunken, W.J. (1990). Rod pathways in mammalian retinae. Trends in Neuroscience 13, 110115.CrossRefGoogle ScholarPubMed
Dietrich, C.E. (1969). Die Feinstruktur der Photorezeptoren des Spitzhörnchens (Tupaia glis). Anatomischer Anzeiger 125, 305312.Google Scholar
Famiglietti, E.V. & Kolb, H. (1975). A bistratified amacrine cell and synaptic circuitry in the inner plexiform layer of the retina. Brain Research 84, 293300.CrossRefGoogle Scholar
Foelix, R.F., Kretz, R. & Rager, G. (1987). Structure and postnatal development of photoreceptors and their synapses in the retina of the tree shrew (Tupaia belangeri). Cell and Tissue Research 247,287297.Google Scholar
Freed, M.A., Smith, R.G. & Sterling, P. (1987). Rod bipolar array in the cat retina: pattern of input from rods and GABA-accumulating amacrine cells. Journal of Comparative Neurology 266, 445455.Google Scholar
Greferath, U., Grünert, U. & Wässle, H. (1990). Rod bipolar cells in the mammalian retina show protein kinase C-like immunoreactivity. Journal of Comparative Neurology 301, 433442.Google Scholar
Grünert, U. & Martin, P.R. (1990). Rod bipolar cells in the macaque monkey retina: light and electron microscopy. Investigative Ophthalmology and Visual Science (Suppl.) 31, 536.Google Scholar
Hsu, S.M., Raine, L. & Fanger, H. (1981). Use of avidin-biotin peroxidase complex (ABC) in immunoperoxidase techniques. Journal of Histochemistry and Cytochemistry 29, 577580.Google Scholar
Kolb, H. (1970). Organization of the outer plexiform layer of the primate retina: Electron microscopy of Golgi-impregnated cells. Philosophical Transactions of the Royal Society B (London) 258, 261283.Google Scholar
Kolb, H. (1977). The organization of the outer plexiform layer in the retina of the cat: electron-microscopic observations. Journal of Neurocytology 6, 131153.CrossRefGoogle ScholarPubMed
Kolb, H. (1979). The inner plexiform layer in the retina of the cat: electron-microscopic observations. Journal of Neurocytology 8, 295329.CrossRefGoogle ScholarPubMed
Kolb, H. & Famiglietti, E.V. (1974). Rod and cone pathways in the inner plexiform layer of the cat retina. Science 186, 4749.Google Scholar
Kolb, H. & Famiglietti, E.V. (1976). Rod and cone pathways in the retina of the cat. Investigative Ophthalmology and Visual Science 15, 935946.Google Scholar
Kolb, H. & Nelson, R. (1983). Rod pathways in the retina of the cat. Vision Research 23, 301312.CrossRefGoogle ScholarPubMed
Kühne, J-H. (1983). Rod receptors in the retina of Tupaia belangeri. Anatomical Embryology (Berlin) 167, 95102.CrossRefGoogle ScholarPubMed
Linberg, K.A. & Fisher, S.K. (1988). Ultrastructural evidence that horizontal cell axon terminals are presynaptic in the human retina. Journal of Comparative Neurology 268, 281297.CrossRefGoogle ScholarPubMed
Mariani, A.P. (1985). Multiaxonal horizontal cells in the retina of the tree shrew (Tupaia glis). Journal of Comparative Neurology 233, 553563.CrossRefGoogle ScholarPubMed
McGuire, B.A., Stevens, J.K. & Sterling, P. (1984). Microcircuitry of bipolar cells in the cat retina. Journal of Neuroscience 4, 29202938.CrossRefGoogle ScholarPubMed
Missotten, L. (1965). The Ultrastructure of the Human Retina. Brüssel: Arscia Uitgaven.Google Scholar
Müller, B. (1989). Demonstration of neurons in the presumed rod pathway of the tree shrew retina. European Journal of Neuroscience (Suppl.) 2, 80.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
Müller, B. & Peichl, L. (1991). Morphology and distribution of catecholaminergic amacrine cells in the cone-dominated tree shrew retina. Journal of Comparative Neurology (in press).Google Scholar
Negishi, K., Kato, S. & Teranishi, T. (1988). Dopamine cells and rod bipolar cells contain protein kinase C-like immunoreactivity in some vertebrate retinas. Neuroscience Letters 94, 247252.CrossRefGoogle ScholarPubMed
Nishizuka, Y. (1986). Studies and perspectives of protein kinase C. Science 233, 305312.Google Scholar
Petry, H.M. & Hárosi, F.I. (1990). Visual pigments of the tree shrew (Tupaia belangeri) and greater galago (Galago crassicaudatus): a microspectrometric investigation. Vision Research 30, 839851.Google Scholar
Petry, H.M., Wooton, B.R., Kelly, J.P. & Agarwala, S. (1987). Effects of adaptation on tree shrew ERG spectral sensitivity. Neuroscience Abstracts 13, 1301.Google Scholar
Samorajski, T., Ordy, J.M. & Keefe, J.R. (1966). Structural organization of the retina in the tree shrew (Tupaia glis). Journal of Cell Biology 28, 489504.Google Scholar
Schäfer, D. (1969). Untersuchungen zur Sehphysiology des Spitzhörnschens (Tupaia glis). Zeitschrift der Vergleichenden Physiologie 63, 204226.Google Scholar
Steinberg, R.H., Reid, R.H. & Lacy, P.L. (1973). The distribution of rods and cones in the retina of the cat (Felis domesticus). Journal of Comparative Neurology 148, 229248.CrossRefGoogle ScholarPubMed
Sterling, P. (1983). Microcircuitry of the cat retina. Annual Reviews of Neuroscience 6, 149185.CrossRefGoogle ScholarPubMed
Sterling, P., Freed, M.A. & Smith, R.G. (1988). Architecture of rod and cone circuits to the ON-beta ganglion cell. Journal of Neuroscience 8, 623642.CrossRefGoogle Scholar
Stettoi, E., Dacheux, R.F. & Raviola, E. (1990). Synaptic connections of rod bipolar cells in the inner plexiform layer of the rabbit retina. Journal of Comparative Neurology 295, 449466.Google Scholar
van, Doncen P.A.M., ter, Laak H.J., Thijssen, J.M. & Vendrik, A.J.H. (1976). Functional classification of cells in the optic tract of a tree shrew. Experimental Brain Research 24, 441446.Google Scholar
Voigt, T. & Wässle, H. (1987). Dopaminergic innervation of AII amacrine cells in mammalian retina. Journal of Neuroscience 7, 41154128.Google Scholar
Young, H.M. & Vaney, D.I. (1990). The retina of prototherian mammals possess neuronal types that are characteristic of nonmammalian retinae. Visual Neuroscience 5, 6166.Google Scholar