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Horizontal cells in the retina of a diurnal rodent, the agouti (Dasyprocta aguti)

Published online by Cambridge University Press:  03 February 2006

S.M.A. DE LIMA ,
P.K. AHNELT ,
T.O. CARVALHO ,
J.S. SILVEIRA ,
F.A.F. ROCHA ,
C.A. SAITO  and
L.C.L. SILVEIRA
S.M.A. DE LIMA
Affiliation:
Departamento de Fisiologia, Centro de Ciências Biológicas, Universidade Federal do Pará, Belém, Pará, Brazil
P.K. AHNELT
Affiliation:
Institut für Physiologie, Medizinische Universität Wien, Wien, Austria
T.O. CARVALHO
Affiliation:
Departamento de Fisiologia, Centro de Ciências Biológicas, Universidade Federal do Pará, Belém, Pará, Brazil
J.S. SILVEIRA
Affiliation:
Departamento de Fisiologia, Centro de Ciências Biológicas, Universidade Federal do Pará, Belém, Pará, Brazil
F.A.F. ROCHA
Affiliation:
Departamento de Fisiologia, Centro de Ciências Biológicas, Universidade Federal do Pará, Belém, Pará, Brazil
C.A. SAITO
Affiliation:
Departamento de Fisiologia, Centro de Ciências Biológicas, Universidade Federal do Pará, Belém, Pará, Brazil
L.C.L. SILVEIRA
Affiliation:
Departamento de Fisiologia, Centro de Ciências Biológicas, Universidade Federal do Pará, Belém, Pará, Brazil
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Abstract

The morphology and distribution of normally placed and displaced A horizontal cells were studied in the retina of a diurnal hystricomorph rodent, the agouti Dasyprocta aguti. Cells were labeled with anti-calbindin immunocytochemistry. Dendritic-field size reaches a minimum in the visual streak, of about 9000 μm2, and increases toward the retinal periphery both in the dorsal and ventral regions. There is a dorsoventral asymmetry, with dorsal cells being larger than ventral cells at equal distances from the streak. The peak value for cell density of 281 ± 28 cells/mm2 occurs in the center of the visual streak, decreasing toward the dorsal and ventral retinal periphery, paralleling the increase in dendritic-field size. Along the visual streak, the decline in cell density is less pronounced, remaining between 100–200 cells/mm2 in the temporal and nasal periphery. Displaced horizontal cells are rare and occur in the retinal periphery. They tend to be smaller than normally placed horizontal cells in the ventral region, whilst no systematic difference was observed between the two cell groups in the dorsal region. Mosaic regularity was studied using nearest-neighbor analysis and the Ripley function. When mosaic regularity was determined removing the displaced horizontal cells, there was a slight increase in the conformity ratio, but the bivariate Ripley function indicated some repulsive dependence between the two mosaics. Both results were near the level of significance. A similar analysis performed in the capybara retina, a closely related hystricomorph rodent bearing a higher density of displaced horizontal cells than found in the agouti, suggested spatial independence between the two mosaics, normally placed versus displaced horizontal cells.

Keywords

Displaced horizontal cellsRetinal circuitryHystricomorph rodentsCalbindin
Type
Research Article
Information
Visual Neuroscience , Volume 22 , Issue 6 , November 2005 , pp. 707 - 720
Copyright
© 2005 Cambridge University Press

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References

REFERENCES

Ahnelt, P.K. & Kolb, H. (1994a). Horizontal cells and cone photoreceptors in primate retina: A Golgi-light microscopic study of spectral connectivity. Journal of Comparative Neurology 343, 387–405.Google Scholar
Ahnelt, P.K. & Kolb, H. (1994b). Horizontal cells and cone photoreceptors in primate retina: A Golgi-electron microscopic study of spectral connectivity. Journal of Comparative Neurology 343, 406–427.Google Scholar
Arrese, C., Dunlop, S.A., Harman, A.M., Braekevelt, C.R., Ross, W.M., Shand, J., & Beazley, L.D. (1999). Retinal structure and visual acuity in a polyprotodont marsupial, the fat-tailed dunnart (Sminthopsis crassicaudata). Brain Behavior and Evolution 53, 111–126.Google Scholar
Baimbridge, K.G., Celio, M.R., & Rogers, J.H. (1992). Calcium-binding proteins in the nervous system. Trends Neuroscience 15, 303–308.Google Scholar
Batini, C., Guegan, M., Palestini, M., & Thomasset, M. (1991). The immunocytochemical distribution of calbindin-D28k and parvalbumin in identified neurons of the pulvinar-lateralis posterior complex of the cat. Neuroscience Letters 130, 203–207.Google Scholar
Besag, J. (1977). Contribution to the discussion of Dr. Ripley's paper. Journal of Royal Statistical Society B 39, 193–195.Google Scholar
Bloomfield, S.A. & Miller, R.F. (1982). A physiological and morphological study of the horizontal cell types of the rabbit retina. Journal Comparative Neurology 208, 288–303.Google Scholar
Boycott, B.B., Peichl, L., & Wässle, H. (1978). Morphological types of horizontal cell in the retina of the domestic cat. Proceedings of the Royal Society B (London) 229, 345–379.Google Scholar
Cajal, S.R. (1893). Lá rétine des vertebrés. La Cellule 9, 17–257.Google Scholar
Cajal, S.R. (1919). Lá desorientacíon inicial de las neuronas retinianas de axon curto. Trabajos del Laboratório de Investigaciones Biológicas 17, 65–86.Google Scholar
Celio, M.R. (1990). Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35, 375–475.Google Scholar
Celio, M.R. & Heizmann, C.W. (1981). Calcium-binding protein parvalbumin as a neuronal marker. Nature 293, 300–302.Google Scholar
Chan, T.L., Goodchild, A.K., & Martin, P.R. (1997). The morphology and distribution of horizontal cells in the retina of a New World monkey, the marmoset Callthrix Jacchus: A comparison with macaque monkey. Journal of Comparative Neurology 393, 196–209.Google Scholar
Chiquet, C., Dkhissi-Benyahya, O., Chounlamountry, N., Szél, A., Degrip, W.J., & Cooper, H.M. (2002). Characterization of calbindin-positive cones in primates. Neuroscience 115, 1323–1333.Google Scholar
Cook, J.E. (1996). Spatial properties of retinal mosaics: An empirical evaluation of some existing measures. Visual Neuroscience 13, 15–30.Google Scholar
Cuenca, N., Deng, P., Linberg, K.A., Lewis, G.P., Fisher, S.K., & Kolb, H. (2002). The neurons of the ground squirrel retina as revealed by immunostains for calcium binding proteins and neurotransmitters. Journal of Neurocytology 31, 649–666.Google Scholar
Dacey, D.M., Lee, B.B., Stafford, D.K., Pokorny, J., & Smith, V.C. (1996). Horizontal cell of the primate retina: Cone specificity without spectral opponency. Science (New York) 271, 656–659.Google Scholar
Dacheux, R.M. & Raviola, E. (1982). Horizontal cells in the retina of the rabbit. Journal of Neuroscience 2, 1486–1493.Google Scholar
de Lima, S.M.A., Dos Santos, S.N., Carvalho, J.I.L.M., & Silveira, L.C.L. (2003). Calbindin immunocytochemistry labels the retina of diurnal and nocturnal New World anthropoids differently. Structure, Function and Evolution of the Primate Visual System—PRIMAVISION (Tübingen), Abstracts, 56.Google Scholar
Diggle, P.J. (1983). Statistical Analysis of Spatial Point Pattern. New York: Academic Press.
Diggle, P.J. (1986). Displaced amacrine cells in the retina of a rabbit: Analysis of a bivariate spatial point pattern. Journal of Neuroscience Methods 18, 115–125.Google Scholar
Do Nascimento, J.L.M., Do Nascimento, R.S.V., Damasceno, B.A., & Silveira, L.C.L. (1991). The neurons of the retinal ganglion cell layer of the guinea pig: Quantitative analysis of their distribution and size. Brazilian Journal of Medical and Biological Research 24, 199–214.Google Scholar
Dos Reis, J.W.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 horizontal cell classes are found in dichromatic primates. Journal of Comparative Neurology 443, 105–123.Google Scholar
Dos Santos, S.N. (2002). Análise Quantitativa da Morfologia das Células Horizontais de um Primata Noturno, o Macaco-da-noite (Aotus sp.). Ph.D. Thesis. Belém: Universidade Federal do Pará.
Eglen, S.J., Raven, M.A., Tamrazian, E., & Reese, B.E. (2003). Dopaminergic amacrine cells in the inner nuclear layer and ganglion cell layer comprise a single functional retinal mosaic. Journal of Comparative Neurology 466, 343–355.Google Scholar
Fisher, S.K. & Boycott, B.B. (1974). Synaptic connections made by horizontal cells within outer plexiform layer of retina of cat and rabbit. Proceedings of the Royal Society B (London) 186, 317–331.Google Scholar
Gallego, A. (1971). Horizontal and amacrine cells in the mammals retina. Vision Research (Suppl.) 3, 33–50.Google Scholar
Glösmann, M., Reitsamer, H., Ahnelt, P., & Pflug, R. (1997). Horizontal cells of the golden hamster retina with a note on proximal axon-like projections. Abstracts of the ARVO Annual Meeting. Investigative Ophthalmology and Visual Science 38, S618.Google Scholar
Goodchild, A.K., Chan, T.L., & Grünert, U. (1996). Horizontal cell connections with short wavelength-sensitive cones in macaque monkey retina. Visual Neuroscience 13, 833–845.Google Scholar
Graur, D., Hide, W.A., & Li, W.H. (1991). Is the guinea-pig a rodent? Nature 351, 649–652.Google Scholar
Grzimek, B. (1968). Animal Life Encyclopedia. New York: Van Nostrand Reinhold.
Günhan, E., Van Der List, D., & Chalupa, L.M. (2003). Ectopic photoreceptor and bipolar cells in the developing and mature retina. Journal of Neuroscience 23, 1383–1389.Google Scholar
Hamano, K., Kiyama, H., Emson, P.C., Manabe, R., Nakauchi, M., & Tohyama, M. (1990). Localization of two calcium binding proteins, calbindin (28kD) and parvalbumin (12 kD), in the vertebrate retina. Journal of Comparative Neurology 302, 417–424.Google Scholar
Harman, A.M. (1994). Horizontal cells in the retina of the bush-tailed possum. Experimental Brain Research 98, 168–171.Google Scholar
Harman, A.M. & Ferguson, J. (1994). Morphology and birth dates of horizontal cells in the retina of a marsupial. Journal of Comparative Neurology 340, 392–404.Google Scholar
Haverkamp, S., Haeseleer, F., & Hendrickson, A. (2003). A comparison of immunocytochemical markers to identify bipolar cell types in human and monkey retina. Visual Neuroscience 20, 589–600.Google Scholar
Hebel, R. (1976). Distribution of retinal ganglion cells in five mammalian species (pig, sheep, ox, horse, dog). Anatomy and Embryology 150, 45–51.Google Scholar
Hemmi, J.M. & Grünert, U. (1999). Distribution of photoreceptor types in the retina of a marsupial, the tammar wallaby (Macropus eugenii). Visual Neuroscience 16, 291–302.Google Scholar
Jande, S.S., Maler, L., & Lawson, D.E.M. (1981). Immunohistochemical mapping of vitamin D-dependent calcium binding protein in the brain. Nature (London) 294, 765–767.Google Scholar
Johnson, P.T., Williams, R.R., Cusato, K., & Reese, B.E. (1999). Rods and cones project to the inner plexiform layer during development. Journal of Comparative Neurology 414, 1–12.Google Scholar
Kolb, H. (1974). The connections between horizontal cells and photoreceptors in the retina of the cat: Electron microscopy of Golgi preparations. Journal of Comparative Neurology 155, 1–14.Google Scholar
Kolb, H., Fernandez, E., Schouten, J., Ahnelt, P., Linberg, K.A., & Fisher, S.K. (1994). Are there three types of horizontal cells in the human retina? Journal of Comparative Neurology 343, 370–386.Google Scholar
Kolb, H., Linberg, K., & Fisher, S.K. (1992). Neurons of the human retina: A Golgi study. Journal of Comparative Neurology 318, 147–187.Google Scholar
Kolb, H. & Normann, R.A. (1982). A-type horizontal cells of the superior edge of the linear visual streak of the rabbit retina have oriented, elongated dendritic trees. Vision Research 22, 905–916.Google Scholar
Linberg, K.A., Suemune, S., & Fisher, S.K. (1996). The retinal neurons of the California ground squirrel, Spermophilus beecheyi: A Golgi study. Journal of Comparative Neurology 365, 173–216.Google Scholar
Mariani, A.P. (1985). Multiaxonal horizontal cells in the retina of the tree shrew, Tupaia glis. Journal of Comparative Neurology 233, 553–563.Google Scholar
Massey, S.C. & Mills, S.L. (1996). A calbindin immunoreactive cone bipolar cell type in the rabbit retina. Journal of Comparative Neurology 366, 15–33.Google Scholar
Miller, J.J. & Baimbridge, K.G. (1983). Biochemical and immunohistochemical correlates of kindling-induced epilepsy: Role of calcium binding protein. Brain Research 278, 322–326.Google Scholar
Mills, S.L. & Massey, S.C. (1994). Distribution and coverage of A- and B-type horizontal cells stained with neurobiotin in the rabbit retina. Visual Neuroscience 11, 549–560.Google Scholar
Müller, B. & Peichl, L. (1993). Horizontal cell in the cone-dominated tree shrew retina: Morphology, photoreceptor contacts, and topographical distribution. Journal of Neuroscience 13, 3628–3646.Google Scholar
Pasteels, B., Miki, N., Hatakenaka, S., & Pochet, R. (1987). Immunohistochemical cross reactivity and electrophoretic comigration between calbindin D-27 kDa and visinin. Brain Research 412, 107–113.Google Scholar
Pasteels, B., Rogers, J., Blachier, F., & Pochet, R. (1990). Calbindin and calretinin localization in retina from different species. Visual Neuroscience 5, 1–16.Google Scholar
Peichl, L. & González-Soriano, J. (1994). Morphological types of horizontal cells in rodent retinae: A comparison of rat, mouse, gerbil and guinea pig. Visual Neuroscience 11, 501–517.Google Scholar
Peichl, L., Sandmann, D., & Boycott, B.B. (1998). Comparative anatomy and function of mammalian horizontal cells. In Development and Organization of the Retina: From Molecules to Function, ed. Chalupa, L.M. & Finlay, B.L., pp. 147–172. New York: Plenum Press.
Perry, V.H. & Cowey, A. (1985). The ganglion cell and cone distributions in the monkey's retina: Implications for central magnification factors. Vision Research 25, 1795–1810.Google Scholar
Picanço-Diniz, C.W., Oliveira, H.L.S., Silveira, L.C.L., & Oswaldo-Cruz, E. (1989). The visual cortex of the agouti (Dasyprocta aguti): Architectonic subdivisions. Brazilian Journal of Medical and Biological Research 22, 121–138.Google Scholar
Picanço-Diniz, C.W., Silveira, L.C.L., De Carvalho, M.S.P., & Oswaldo-Cruz, E. (1991). Contralateral visual field representation in area 17 of the cerebral cortex of the agouti: A comparison between cortical magnification factor and retinal ganglion cell distribution. Neuroscience 44, 325–333.Google Scholar
Picanço-Diniz, C.W., Silveira, L.C.L., & Oswaldo-Cruz, E. (1992). A comparative survey of magnification factors and retinal ganglion cell topography of lateral-eyed mammals. In The Visual System from Genesis to Maturity, ed. Lent, R., pp. 188–197. Boston, Massachusetts: Birkhauser.
Pochet, R., Pasteels, B., Seto-Ohshima, A., Bastinelli, E., Kitajima, S., & Van Eldik, L.J. (1991). Calmodulin and calbindin localization in the retina from six vertebrate species. Journal of Comparative Neurology 314, 750–762.Google Scholar
Polyak, S.L. (1941). The Retina. Chicago, Illinois: University of Chicago Press.
Prada, F.A., Armengol, J., & Génis-Gálvez, J.M. (1984). Displaced horizontal cells in the chick retina. Journal of Morphology 182, 221–225.Google Scholar
Rabié, A., Thomasset, M., Parkes, C.O., & Clavel, M.C. (1985). Immunocytochemistry detection of 28000-MW calcium-binding protein in horizontal cells of the rat retina. Cell and Tissue Research 240, 493–496.Google Scholar
Ripley, B.D. (1976). The second-order analysis of stationary point processes. Journal of Applied Probability 13, 255–266.Google Scholar
Röhrenbeck, J., Wässle, H., & Heizmann, C.W. (1987). Immunocytochemical labeling of horizontal cells in mammalian retina using antibodies against calcium binding proteins. Neuroscience Letters 77, 255–260.Google Scholar
Röhrenbeck, J., Wässle, H., & Boycott, B.B. (1989). Horizontal cells in the monkey retina: Immunocytochemical staining with antibodies against calcium binding proteins. European Journal of Neuroscience 1, 407–420.Google Scholar
Saito, C.A., Yamada, E.S., De Lima, S.M.A., & Silveira, L.C.L. (2005). Células horizontais classe a da capivara: Relação espacial entre os mosaicos de células tópicas e deslocadas avaliada com procedimentos de estatística espacial. Resumos da XIX Reunião Anual da Federação de Sociedades de Biologia Experimental, Águas de Lindóia (submitted).
Sandmann, D., Boycott, B.B., & Peichl, L. (1996a). Blue-cone horizontal cells in the retinae of horses and other Equidae. Journal of Neuroscience 16, 3381–3396.Google Scholar
Sandmann, D., Boycott, B.B., & Peichl, L. (1996b). The horizontal cells of artiodactyl retinae: A comparison with Cajal's descriptions. Visual Neuroscience 13, 735–746.Google Scholar
Schnitzer, J. & Rusoff, A.C. (1984). Horizontal cells of the mouse retina contain glutamic-acid decarboxylase-like immunoreactivity during early developmental stages. Journal of Neuroscience 4, 2948–2955.Google Scholar
Schreiner, D.S. & Jande, S.S. (1985a). Target-cells of vitamin-D in the vertebrate retina. Acta Anatomica 121, 153–162.Google Scholar
Schreiner, S.D. & Jande, S.S. (1985b). Immunocytochemical localization of vitamin-D-dependent calcium-binding protein (D-Ca-Bp) in the growing chick lymphoid organs. Anatomical Record 211, A171–A171.Google Scholar
Silveira, L.C.L., Picanço-Diniz, C.W., & Oswaldo-Cruz, E. (1989a). The distribution and size of ganglion cells in the retinae of large Amazon rodents. Visual Neuroscience 2, 221–235.Google Scholar
Silveira, L.C.L., Yamada, E.S., & Picanço-Diniz, C.W. (1989b). Displaced horizontal and biplexiform horizontal cells in the mammalian retina. Visual Neuroscience 3, 483–488.Google Scholar
Vaney, D.I. & Hughes, A. (1976). The rabbit optic nerve: Fibre diameter spectrum, fibre count, and comparison with a retinal ganglion cell count. Journal of Comparative Neurology 170, 241–252.Google Scholar
Versaux-Botteri, C., Pochet, R., & Nguyen-Legros, J. (1989). Immunohistochemical localization of GABA-containing neurons during postnatal development of the rat retina. Investigative Ophthalmology and Visual Science 30, 652–659.Google Scholar
Verstappen, A., Parmentier, M., Chirnoaga, M., Lawson, D.E.M., Pasteels, J.L., & Pochet, R. (1986). Vitamin D-dependent calcium binding protein immunoreactivity in human retina. Ophthalmic Research 18, 209–214.Google Scholar
Wässle, H. & Riemann, H.J. (1978). The mosaic of nerve cells in the mammalian retina. Proceedings of the Royal Society B (London) 200, 441–461.Google Scholar
Wässle, H., Peichl, L., & Boycott, B.B. (1978). Topography of horizontal cells in the retina of the domestic cat. Proceedings of the Royal Society B (London) 203, 269–291.Google Scholar
Wässle, H., Peichl, L., & Boycott, B.B. (1979). Quantification of horizontal cells in the domestic cat retina. Progress in Brain Research 51, 373–388.Google Scholar
Wässle, H., Dacey, D.M., Haun, T., Haverkamp, S., Grünert, U., & Boycott, B.B. (2000). The mosaic of horizontal cells in the macaque monkey retina: With a comment on biplexiform ganglion cells. Visual Neuroscience 17, 591–608.Google Scholar
West, R.W. (1976). Light and electron microscopy of the ground squirrel retina: Functional considerations. Journal of Comparative Neurology 168, 355–378Google Scholar
West, R.W. (1978). Bipolar and horizontal cells of the gray squirrel retina: Golgi morphology and receptor connections. Vision Research 18, 129–136.Google Scholar
West, R.W. & Dowling, J.E. (1975). Anatomical evidence for cone and rod-like receptors in gray squirrel, ground squirrel, and prairie-dog retinas. Journal of Comparative Neurology 159, 439–459.Google Scholar
Yamada, E.S. (1991). Organização do Sistema Visual de Roedores da Amazônia: Topografia das Células Horizontais Tipo A da Retina da Capivara, Hydrochoerus hidrochaeris. M.Sc. Thesis. Belém: Universidade Federal do Pará.
Yamada, E.S., Silveira, L.C.L., & Coimbra, A.J.F. (1992). Topography of A-type horizontal cells in the retina of capybara. Brazilian Journal of Medical and Biological Research 25, 619–632.Google Scholar