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Rod bipolar cells in the retina of the capuchin monkey (Cebus apella): Characterization and distribution

Published online by Cambridge University Press:  27 August 2009

SORAIA VALÉRIA O.C. LAMEIRÃO ,
DANIA E. HAMASSAKI ,
ANDERSON R. RODRIGUES ,
SILENE MARIA A. DE LIMA ,
BARBARA L. FINLAY  and
LUIZ CARLOS L. SILVEIRA
SORAIA VALÉRIA O.C. LAMEIRÃO
Affiliation:
Departamento de Fisiologia, Instituto de Ciências Biológicas, Universidade Federal do Pará, Belém, Pará, Brazil
DANIA E. HAMASSAKI
Affiliation:
Departamento de Biologia Celular e do Desenvolvimento, Instituto de Ciências Biomédicas, Universidade de São Paulo, São Paulo, São Paulo, Brazil
ANDERSON R. RODRIGUES
Affiliation:
Departamento de Fisiologia, Instituto de Ciências Biológicas, Universidade Federal do Pará, Belém, Pará, Brazil
SILENE MARIA A. DE LIMA
Affiliation:
Departamento de Fisiologia, Instituto de Ciências Biológicas, Universidade Federal do Pará, Belém, Pará, Brazil
BARBARA L. FINLAY
Affiliation:
Department of Psychology, Cornell University, Ithaca, New York, U.S.A.
LUIZ CARLOS L. SILVEIRA*
Affiliation:
Departamento de Fisiologia, Instituto de Ciências Biológicas, Universidade Federal do Pará, Belém, Pará, Brazil Núcleo de Medicina Tropical, Universidade Federal do Pará, Belém, Pará, Brazil
*
*Address correspondence and reprint requests to: Dr. Luiz Carlos de Lima Silveira, Núcleo de Medicina Tropical, Universidade Federal do Pará, Av. Generalíssimo Deodoro 92 (Umarizal), 66075-110 Belém, Pará, Brazil. E-mail: [email protected]
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Abstract

Rod bipolar cells in Cebus apella monkey retina were identified by an antibody against the alpha isoform of protein kinase C (PKCα), which has been shown to selectively identify rod bipolars in two other primates and various mammals. Vertical sections were used to confirm the identity of these cells by their characteristic morphology of dendrites and axons. Their topographic distribution was assessed in horizontal sections; counts taken along the dorsal, ventral, nasal, and temporal quadrants. The density of rod bipolar cells increased from 500 to 2900 cells/mm2 at 1 mm from the fovea to reach a peak of 10,000–12,000 cells/mm2 at 4 mm, approximately 5 deg of eccentricity, and then gradually decreased toward retinal periphery to values of 5000 cells/mm2 or less. Rod to rod bipolar density ratio remained between 10 and 20 across most of the retinal extension. The number of rod bipolar cells per retina was 6,360,000 ± 387,433 (mean ± s.d., n = 6). The anti-PKCα antibody has shown to be a good marker of rod bipolar cells of Cebus, and the cell distribution is similar to that described for other primates. In spite of the difference in the central retina, the density variation of rod bipolar cells in the Cebus and Macaca as well as the convergence from rod to rod bipolar cells are generally similar, suggesting that both retinae stabilize similar sensitivity (as measured by rod density) and convergence.

Keywords

Rod bipolar cellsCapuchin monkeyPrimatesPKCαImmunocytochemistry
Type
Research Articles
Information
Visual Neuroscience , Volume 26 , Issue 4 , July 2009 , pp. 389 - 396
Copyright
Copyright © Cambridge University Press 2009

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References

Andrade-da-Costa, B.L.S. & Hokoç, J.N. (2000). Photoreceptor topography of the retina in the New World monkey Cebus apella. Vision Research 40, 2395–2409.CrossRefGoogle ScholarPubMed
Barnstable, C.J., Akagawa, K., Hofstein, R. & Horn, J.P. (1983). Monoclonal antibodies that label discrete cell types in mammalian nervous system. Quantitative Biology 48, 863–876.CrossRefGoogle ScholarPubMed
Bloomfield, S.A. & Dacheux, R.F. (2001). Rod vision: Pathways and processing in the mammalian retina. Progress in Retinal and Eye Research 20, 351–384.CrossRefGoogle ScholarPubMed
Boycott, B.B. & Dowling, J.E. (1969). Organization of the primate retina: Light microscopy. Philosophical Transactions of the Royal Society of London. Series B 255, 109–184.Google Scholar
Brosnan, S.F. & de Waal, F.B.M. (2003). Monkeys reject unequal pay. Nature 425, 297–299.CrossRefGoogle ScholarPubMed
Caminos, E.A., Velasco, M.J., Aijón, J. & Lara, J.M. (1999). Protein kinase c-like immunoreactive cells in embryo and chicken retinae. Developmental Brain Research 118, 227–230.CrossRefGoogle Scholar
Chan, T.L., Martin, P.R., Clunas, N. & Grünert, U. (2001). Bipolar cell diversity in the primate retina: Morphologic and immunocytochemical analysis of a New World monkey, the marmoset Callithrix jacchus. The Journal of Comparative Neurology 437, 219–239.CrossRefGoogle ScholarPubMed
Curcio, C.A., Sloan, K.R., Kalina, R.E. & Hendrickson, A.E. (1990). Human photoreceptor topography. The Journal of Comparative Neurology 292, 497–523.CrossRefGoogle ScholarPubMed
Daw, N.W., Jensen, J.R. & Brunken, W.J. (1990). Rod pathways in mammalian retina. Trends in Neurosciences 13, 110–115.CrossRefGoogle Scholar
Diogo, A.C.M., Soares, J.G.M., Koulakov, A., Albright, T.D. & Gattass, R. (2003). Electrophysiological imaging of functional architecture in the cortical middle temporal visual area of Cebus apella monkey. The Journal of Neuroscience 23, 3881–3898.CrossRefGoogle ScholarPubMed
Dkhissi-Benyahya, O., Szel, A., Degrip, W.J. & Cooper, H.M. (2001). Short and mid-wavelength cone distribution in a nocturnal strepsirrhine primate (Microcebus murinus). The Journal of Comparative Neurology 438, 490–504.CrossRefGoogle Scholar
Dos Reis, J.L., Carvalho, W.A., Saito, C.A. & Silveira, L.C.L. (2002). Morphology of horizontal cells in the retina of the capuchin monkey, Cebus apella: How many classes are found in dichromatic primates? The Journal of Comparative Neurology 443, 105–123.CrossRefGoogle ScholarPubMed
Finlay, B.L., Franco, E.C.S., Yamada, E.S., Crowley, J.C., Parsons, M.E., Muniz, J.A.P.C. & Silveira, L.C.L. (2008). Number and topography of cones, rods and optic nerve axons in New and Old World primates. Visual Neuroscience 25, 289–299.CrossRefGoogle ScholarPubMed
Finlay, B.L., Silveira, L.C.L. & Reichenbach, A. (2005). Comparative aspects of visual system development. In The Structure, Function and Evolution of the Primate Visual System, ed. Kremers, J., pp. 37–72. Chichester, UK: John Wiley & Sons.CrossRefGoogle Scholar
Fiorani, M. Jr, Gattass, R., Rosa, M. & Sousa, A.P.B. (1989). Visual area MT in the Cebus monkey: Location visuotopic organization and variability. The Journal of Comparative Neurology 259, 529–548.Google Scholar
Franco, E.C.S., Finlay, B.L., Silveira, L.C.L., Yamada, E.S. & Crowley, J.C. (2000). Conservation of absolute foveal area in a New World monkeys: A constraint on eye size and conformation. Brain, Behavior and Evolution 56, 276–286.CrossRefGoogle Scholar
Gattass, R., Souza, A.P.B. & Rosa, M.G.P. (1987). Visual topography of V1 in the Cebus monkey. The Journal of Comparative Neurology 259, 529–548.CrossRefGoogle ScholarPubMed
Greferath, U., Grünert, U. & Wässle, H. (1990). Rod bipolar cells in the mammalian retina show protein kinase c-like immunoreactivity. The Journal of Comparative Neurology 301, 433–442.CrossRefGoogle ScholarPubMed
Grünert, U. & Martin, P.R. (1991). Rod bipolar cells in the macaque monkey retina: Immunoreactivity and connectivity. The Journal of Neuroscience 11, 2742–2758.CrossRefGoogle ScholarPubMed
Grünert, U., Martin, P.R. & Wässle, H. (1994). Immunocytochemical analysis of bipolar cells in the macaque monkey retina. The Journal of Comparative Neurology 348, 607–627.CrossRefGoogle ScholarPubMed
Hendrickson, A., Djajadi, H.R., Nakamura, L., Possin, D.E. & Sajuthi, D. (2000). Nocturnal tarsier retina has both short and long/medium-wavelength cones in an unusual topography. The Journal of Comparative Neurology 424, 718–730.3.0.CO;2-Z>CrossRefGoogle Scholar
Jacobs, G.H. (1998). Photopigments and seeing—Lessons from natural experiments. Investigative Ophthalmology and Visual Science 39, 2205–2216.Google ScholarPubMed
Jansen, A.K., Lima, B. & Gattass, R. (2004). GABA inactivation of visual area MT modifies direction selectivity of V2 neurons in Cebus monkeys. Clinical and Experimental Pharmacology & Physiology 31, 1580–1590.Google Scholar
Kolb, H. & Zhang, L. (1997). Immunostaining with antibodies against protein kinase c isoforms in the fovea of the monkey retina. Microscopy Research and Technique 36, 57–75.3.0.CO;2-W>CrossRefGoogle ScholarPubMed
Kolb, H., Zhang, L. & Dekorver, L. (1993). Differential staining of neurons in the human retina with antibodies to protein kinase c isozymes. Visual Neuroscience 10, 341–351.CrossRefGoogle ScholarPubMed
Koulen, P., Brandstatter, J.H., Kroger, S., Enz, R., Bormann, J. & Wässle, H. (1997). Immunocytochemical localization of the GABA (C) receptor rho subunits in the cat, goldfish and chick retina. The Journal of Comparative Neurology 380, 520–532.3.0.CO;2-3>CrossRefGoogle Scholar
Krebs, W. & Krebs, I.P. (1989). Quantitative morphology of the central fovea in the primate retina. American Journal of Anatomy 184, 225–236.CrossRefGoogle ScholarPubMed
Lee, B.B., Silveira, L.C.L., Yamada, E.S., Hunt, D.M., Kremers, J., Martin, P.R., Troy, J.B. & da Silva Filho, M. (2000). Visual responses of ganglion cells of a New World primate, the capuchin monkey, Cebus apella. The Journal of Physiology 528, 573–590.CrossRefGoogle ScholarPubMed
Lima, B., Fiorani, M. Jr & Gattass, R. (2004). Changes of ongoing activity in Cebus monkey perirhinal cortex correlates with behavioral performance. Brazilian Journal of Medical and Biological Research 38, 59–63.CrossRefGoogle Scholar
Lima, S.M., Silveira, L.C.L. & Perry, V.H. (1996). The distribution of M ganglion cells in diurnal and nocturnal New World monkeys. The Journal of Comparative Neurology 368, 538–552.3.0.CO;2-5>CrossRefGoogle ScholarPubMed
Luo, X., Ghosh, K.K., Martin, P.R. & Grünert, U. (1999). Analysis of two types of cone bipolar cells in the retina of a New Word monkey, the marmoset, Callithrix jaccus. Visual Neuroscience 16, 707–719.CrossRefGoogle Scholar
Moura, A.C.A. & Lee, P.C. (2004). Capuchin stone tool use in caatinga dry forest. Science 306, 1909.CrossRefGoogle ScholarPubMed
Negishi, K., Kato, S. & Teranishi, T. (1988). Dopamine cells and rod bipolar cells contain protein kinase C-like immunoreactivity in some vertebrates retinas. Neuroscience Letters 94, 247–252.CrossRefGoogle ScholarPubMed
Nishizuka, Y. (1984). The role of protein kinase C in cell surface signal transduction and tumour promotion. Nature 308, 693–698.CrossRefGoogle ScholarPubMed
Ogden, T. (1975). The receptor mosaic of Aotus trivirgatus: Distribution of rods and cones. The Journal of Comparative Neurology 163, 193–202.CrossRefGoogle ScholarPubMed
Onoda, N. (1988). A monoclonal antibody specific for subpopulation of retinal bipolar cells in vertebrates. Neuroscience Research 8, 113–125.Google ScholarPubMed
Onoda, N. & Fujita, S.C. (1987). A monoclonal antibody specific for subpopulation of retinal bipolar cells in the frog and other vertebrates. Brain Research 416, 359–363.CrossRefGoogle ScholarPubMed
Osborne, N.N., Broyden, N.J., Barnett, N.L. & Morris, N.J. (1991). Protein kinase c (α and β) immunoreactivity in rabbit and rat retina: Effect of phorbol esters and transmitter agonists on immunoreactivity and translocation of the enzyme from cytosolic to membrane compartments. Journal of Neurochemistry 57, 594–604.CrossRefGoogle ScholarPubMed
Packer, O., Hendrickson, A.E. & Curcio, C.A. (1989). Photoreceptor topography of the retina in the adult pigtail macaque (Macaca nemestrina). The Journal of Comparative Neurology 288, 165–183.CrossRefGoogle ScholarPubMed
Perry, V.H. & Cowey, A. (1985). The ganglion cell and cone distributions in the monkey’s retina: Implication for the central magnification factors. Vision Research 25, 1795–1810.CrossRefGoogle ScholarPubMed
Pinzón-Duarte, G.K., Kohler, K., Arango-Gonzalez, B. & Guenther, E. (2000). Cell differentiation, synaptogenesis and influence of the retinal pigment epithelium in a rat neonatal organotypic retinal culture. Vision Research 40, 3455–3465.CrossRefGoogle Scholar
Polyak, S.L. (1941). The Retina. Chicago, IL: University of Chicago Press.Google Scholar
Rolls, E.T. & Cowey, A. (1970). Topography of the retina and striate cortex and its relationship to visual acuity in rhesus monkeys and squirrel monkeys. Experimental Brain Research 10, 298–310.CrossRefGoogle ScholarPubMed
Rosa, M.G.P. & Gattass, R. (1988). Representation of the visual field in the second visual area in the Cebus monkey. The Journal of Comparative Neurology 275, 326–345.CrossRefGoogle ScholarPubMed
Silveira, L.C.L. (2004). Comparative study of the primate retina. In The Primate Visual System, ed. Kaas, J.H. & Collins, C.E., pp. 29–51. Boca Raton, FL: CRC Press.Google Scholar
Silveira, L.C.L. & Perry, V.H. (1991). The topography of magnocellular projecting ganglion cells (M-ganglion cells) in the primate retina. Neuroscience 40, 217–237.CrossRefGoogle ScholarPubMed
Silveira, L.C.L., Lee, B.B., Yamada, E.S., Kremers, J. & Hunt, D.M. (1998). Post-receptoral mechanisms of colour vision in New World primates. Vision Research 38, 3329–3337.CrossRefGoogle ScholarPubMed
Silveira, L.C.L., Lee, B.B., Yamada, E.S., Kremers, J., Hunt, D.M., Martin, P.R. & Gomes, F.L. (1999). Ganglion cells of a short wavelength sensitive cone pathway in New World monkeys: Morphology and physiology. Visual Neuroscience 16, 333–343.CrossRefGoogle Scholar
Silveira, L.C.L., Picanço-Diniz, C.W., Sampaio, L.F.S. & Oswaldo-Cruz, E. (1989). Retinal ganglion cell distribution in the Cebus monkey: A comparison with the cortical magnification factors. Vision Research 29, 1471–1483.CrossRefGoogle ScholarPubMed
Silveira, L.C.L., Yamada, E.S., Franco, E.C.S. & Finlay, B.L. (2001). The specialisation of the owl monkey retina for night vision. Color Research & Application 26, S118–S122.3.0.CO;2-9>CrossRefGoogle Scholar
Silveira, L.C.L., Yamada, E.S., Perry, V.H. & Picanço-Diniz, C.W. (1994). M and P retinal ganglion cells of the diurnal and nocturnal New World monkeys. NeuroReport 5, 2077–2081.CrossRefGoogle ScholarPubMed
Tan, Y. & Li, W.H. (1999). Trichromatic vision in prosimians. Nature 402, 36.CrossRefGoogle ScholarPubMed
Troilo, D., Howland, H.C. & Judge, S.J. (1993). Visual optics and retinal cone topography in the common marmoset (Callithrix jacchus). Vision Research 33, 1301–1310.CrossRefGoogle ScholarPubMed
Wikler, K.C. & Rakic, P. (1990). Distribution of photoreceptor subtypes in the retina of diurnal and nocturnal primate. The Journal of Neuroscience 10, 3390–3401.CrossRefGoogle Scholar
Wikler, K.C., Williams, R.W. & Rakic, P. (1990). Photoreceptor mosaic: Number and distribution of rods and cones in the rhesus monkey retina. The Journal of Comparative Neurology 297, 499–508.CrossRefGoogle ScholarPubMed
Wilder, H.D., Grünert, U., Lee, B.B. & Martin, P.R. (1996). Topography of ganglion cells and photoreceptors in the retina of a New World monkey: The marmoset Callithrix jacchus. Visual Neuroscience 13, 335–352.CrossRefGoogle ScholarPubMed
Wood, J.G., Hart, C.E., Mazzei, G.J., Girard, P.R. & Kuo, J.F. (1988). Distribution of protein kinase c immunoreactivity in rat retina. Histochemical Journal 20, 63–68.CrossRefGoogle ScholarPubMed
Wood, J.P.M., McCord, R.J. & Osborne, N.N. (1997). Retinal protein kinase c. Neurochemical International 30, 119–136.CrossRefGoogle ScholarPubMed
Yamada, E.S., Silveira, L.C.L., Gomes, F.L. & Lee, B.B. (1996 a). The retinal ganglion cell classes of New World primates. Revista Brasileira de Biologia 56(Suppl. 1), 381–396.Google ScholarPubMed
Yamada, E.S., Silveira, L.C.L. & Perry, V.H. (1996 b). Morphology, dendritic field size, somal size, density and coverage of M and P retinal ganglion cells of dichromatic Cebus monkey. Visual Neuroscience 13, 1011–1029.CrossRefGoogle Scholar
Yamada, E.S., Silveira, L.C.L., Perry, V.H. & Franco, E.C.S. (2001). Morphology and dendritic field size of M and P retinal ganglion cells of the owl monkey. Vision Research 41, 119–131.CrossRefGoogle Scholar
Young, H.M. & Vaney, D.I. (1991). The retinae of prototherian mammals possess neuronal types that are characteristic of non-mammalian retinae. Visual Neuroscience 5, 61–66.CrossRefGoogle Scholar
Zhang, D. & Yeh, H.H. (1991). Protein kinase c-like immunoreactivity in rod bipolar cells of the rat retina: A developmental study. Visual Neuroscience 6, 429–437.CrossRefGoogle ScholarPubMed