Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-15T13:21:46.890Z Has data issue: false hasContentIssue false
  • English
  • Français

The topography of cone photoreceptors in the retina of a diurnal rodent, the agouti (Dasyprocta aguti)

Published online by Cambridge University Press:  01 March 2009

FERNANDO ALLAN de FARIAS ROCHA ,
PETER K. AHNELT ,
LEO PEICHL ,
CÉZAR A. SAITO ,
LUIZ CARLOS L. SILVEIRA  and
SILENE MARIA A. DE LIMA
FERNANDO ALLAN de FARIAS ROCHA*
Affiliation:
Departamento de Fisiologia, Instituto de Ciências Biológicas, Universidade Federal do Pará, Belém, Pará, Brazil
PETER K. AHNELT
Affiliation:
Institut für Physiologie, Medizinische Universität Wien, Wien, Austria
LEO PEICHL
Affiliation:
Max-Planck-Institut für Hirnforschung, Deutschordenstr. 46, D-60528, Frankfurt a. M., Germany
CÉZAR A. SAITO
Affiliation:
Departamento de Fisiologia, Instituto de Ciências Biológicas, Universidade Federal do Pará, Belém, Pará, Brazil
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
SILENE MARIA A. DE LIMA
Affiliation:
Departamento de Fisiologia, Instituto de Ciências Biológicas, Universidade Federal do Pará, Belém, Pará, Brazil
*
*Address correspondence and reprint requests to: Dr. Fernando Allan de Farias Rocha, Departamento de Fisiologia, Instituto de Ciências Biológicas, Universidade Federal do Pará, 66075-900 Belém, Pará, Brazil. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The presence, density distribution, and mosaic regularity of cone types were studied in the retina of the diurnal agouti, Dasyprocta aguti. Longwave-sensitive (L-) and shortwave-sensitive (S-) cones were detected by antibodies against the respective cone opsins. L- and S-cones were found to represent around 90 and 10% of the cone population, respectively. There was no evidence for L- and S-opsin coexpression in agouti cones. L-cone densities were highest, up to 14,000/mm2, along a horizontal visual streak located about 2–3 mm dorsal to the optic nerve, and the L-cone distribution showed a dorsoventral asymmetry with higher densities in ventral (about 10,000/mm2) than in dorsal (about 4000/mm2) retinal regions. This L-cone topography parallels the agouti’s ganglion cell topography. S-cones had a peak density of 1500–2000/mm2 in the central retinal region but did not form a visual streak. Their distribution also showed a dorsoventral asymmetry with densities around 600/mm2 in dorsal and around 1000/mm2 in ventral retinal regions. The patterning of cone arrays was assessed by the density recovery profile analysis. At all eccentricities evaluated, the S-cone mosaic less efficiently packed than the L-cone mosaic. Rod densities ranged from 47,000/mm2 in peripheral to 64,000/mm2 in central retina, and rod:cone ratios were 4:1–9:1. The comparatively low rod density and high cone proportion appear well adapted to the diurnal lifestyle of the agouti.

Keywords

Cone opsinCone mosaicVisual streakHystricomorph rodentsImmunocytochemistry
Type
Research Articles
Information
Visual Neuroscience , Volume 26 , Issue 2 , March 2009 , pp. 167 - 175
Copyright
Copyright © Cambridge University Press 2009

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

Ahnelt, P.K. (1985). Characterization of the color related receptor mosaic in the ground squirrel retina. Vision Research 25, 1557–1567.Google Scholar
Ahnelt, P.K., Fernandez, E., Martinez, O., Bolea, J.A. & Kubber-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 17, 580–588.CrossRefGoogle ScholarPubMed
Ahnelt, P.K., Hokoç, J.N. & Rohlich, P. (1995). Photoreceptors in a primitive mammal, the South American opossum, Didelphis marsupialis aurita: Characterization with anti-opsin immunolabeling. Visual Neuroscience 12, 793–804.Google Scholar
Ahnelt, P.K. & Kolb, H. (2000). The mammalian photoreceptor mosaic-adaptive design. Progress in Retinal and Eye Research 19, 711–777.Google Scholar
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, 513–523.Google Scholar
Bowmaker, J.K. & Hunt, D.M. (2006). Evolution of vertebrate visual pigments. Current Biology 16, R484–R489.CrossRefGoogle ScholarPubMed
Calderone, J.B. & Jacobs, G.H. (1995). Regional variations in the relative sensitivity to UV light in the mouse retina. Visual Neuroscience 12, 463–468.CrossRefGoogle ScholarPubMed
Carleton, M.D. & Musser, G.G. (2005). Order Rodentia. In Mammal Species of the World–A Taxonomic and Geographic Reference, ed. Wilson, D.E. & Reeder, D.M., pp. 745–752. Baltimore, MD: Johns Hopkins University Press.Google Scholar
Carvalho, L.S., Cowing, J.A., Wilkie, S.E., Bowmaker, J.K. & Hunt, D.M. (2006). Shortwave visual sensitivity in tree and flying squirrels reflects changes in lifestyle. Current Biology 16, R81–R83.CrossRefGoogle ScholarPubMed
Chávez, A.E., Bozinovic, F., Peichl, L. & Palacios, A.G. (2003). Retinal spectral sensitivity, fur coloration and urine reflectance in the genus Octodon (Rodentia): Implications for visual ecology. Investigative Ophthalmology & Visual Science 44, 2290–2296.Google Scholar
Cornish, E.E., Hendrickson, A.E. & Provis, J.M. (2004). Distribution of short-wavelength-sensitive cones in human fetal and postnatal retina: Early development of spatial order and density profiles. Vision Research 44, 2019–2026.CrossRefGoogle ScholarPubMed
Costa, E.T., do Nascimento, J.L.M., Picanço-Diniz, C.W., da Silva Filho, M. & Quaresma, J.A.S. (1996). Histochemical characterization of NADPH-diaforase activity in area 17 of diurnal and nocturnal primates and rodents. Brazilian Journal of Medical and Biological Research 29, 1355–1362.Google Scholar
de Lima, S.M.A., Ahnelt, P.K., Carvalho, T.O., Silveira, J.S., Rocha, F.A.F., Saito, C.A. & Silveira, L.C.L. (2005). Horizontal cells in the retina of a diurnal rodent, the agouti (Dasyprocta agouti). Visual Neuroscience 22, 707–720.Google Scholar
de Lima, S.M.A., Rocha, F.A.F., Hokoc, J.N. & Ahnelt, P.K. (2001). Identification and distribution of cones types in a diurnal rodents, the Agouti. Investigative Ophthalmology & Visual Science 42(Suppl.), S631.Google Scholar
Deegan, J.F. II & Jacobs, G.H., (1993). On the identity of the cone types of the rat retina. Experimental Eye Research 56, 375–377.CrossRefGoogle ScholarPubMed
Elston, G.N., Elston, A., Aurelio-Freire, M., Leal, W.G., Dias, I.A., Pereira, A. Jr, Silveira, L.C.L., & Picanço-Diniz, C.W. (2006). Specialization of pyramidal cell structure in the visual areas V1, V2 and V3 of the South American rodent, Dasyprocta primnolopha. Brain Research 1106, 99–110.CrossRefGoogle ScholarPubMed
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, 1151–1175.CrossRefGoogle ScholarPubMed
Glösmann, M. & Ahnelt, P.K. (1998). Coexpression of M- and S-opsin extends over the entire inferior mouse retina. Investigative Ophthalmology & Visual Science 39, S1059.Google Scholar
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, 139–146.Google Scholar
Gomes, F.L., Yamada, E.S. & Silveira, L.C.L. (1998). Morphology, size, and distribution of the alpha retinal ganglion cells of the agouti, Dasyprocta aguti. Investigative Ophthalmology & Visual Science 39, S563.Google Scholar
Grzimek, B. (1968). Grzimek’s Animal Life Encyclopedia. New York: Van Nostrand Reinhold.Google Scholar
Haverkamp, S., Wässle, H., Duebel, J., Kuner, T., Augustine, G.J., Feng, G. & Euler, T. (2005). The primordial, blue-cone system of the mouse retina. Journal of Neuroscience 25, 5438–5445.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
Hicks, D. & Molday, R.S. (1986). Differential immunogold-dextran labeling of bovine and frog rod and cone cells using monoclonal antibodies against bovine rhodopsin. Experimental Eye Research 42, 55–71.CrossRefGoogle ScholarPubMed
Jacobs, G.H. (1993). The distribution and nature of colour vision among the mammals. Biological Reviews 68, 413–471.Google Scholar
Jacobs, G.H., Calderone, J.B., Fenwick, J.A., Krogh, K. & Williams, G.A. (2003). Visual adaptations in a diurnal rodent, Octodon degus. Journal of Comparative Physiology A 189, 347–361.Google Scholar
Jacobs, G.H. & Deegan, J.F. (1994). Spectral sensitivity, photopigments, and color vision in the guinea pig (Cavia porcellus). Behavioral Neuroscience 108, 993–1004.Google Scholar
Jacobs, G.H., Fenwick, J.A. & Williams, G.A. (2001). Cone-based vision of rats for ultraviolet and visible lights. Journal of Experimental Biology 204, 2439–2446.CrossRefGoogle ScholarPubMed
Jacobs, G.H., Neitz, J. & Deegan, J.F. (1991). Retinal receptors in rodents maximally sensitive to ultraviolet light. Nature 353, 655–656.Google Scholar
Jacobs, G.H., Williams, G.A. & Fenwick, J.A. (2004). Influence of cone pigment coexpression on spectral sensitivity and color vision in the mouse. Vision Research 44, 1615–1622.Google Scholar
Jacobs, G.H. & Yolton, R.L. (1969). Dichromacy in the ground squirrel. Nature 223, 414–415.CrossRefGoogle ScholarPubMed
Jacobs, G.H. & Yolton, R.L. (1971). Visual sensitivity and color vision in ground squirrels. Vision Research 11, 511–537.Google Scholar
Jeon, C.J., Strettoi, E. & Masland, R.H. (1998). The major cell populations of the mouse retina. Journal of Neuroscience 18, 8936–8946.CrossRefGoogle ScholarPubMed
Kouyama, N. & Marshak, D.W. (1997). The topographical relationship between two neuronal mosaics in the short wavelength-sensitive system of the primate retina. Visual Neuroscience 14, 159–167.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, 685–691.CrossRefGoogle ScholarPubMed
Long, K.O. & Fisher, S.K. (1983). The distributions of photoreceptors and ganglion cells in the California ground squirrel, Spermophilus beecheyi. Journal of Comparative Neurology 221, 329–340.CrossRefGoogle ScholarPubMed
Lukáts, A., Dkhissi-Benyahya, O., Szepessy, Z., Rohlich, P., Vigh, B., Bennett, N.C., Cooper, H.M. & Szél, A. (2002). Visual pigment coexpression in all cones of two rodents, the Siberian hamster, and the pouched mouse. Investigative Ophthalmology & Visual Science 43, 2468–2473.Google Scholar
Lukáts, A., Szabo, A., Rohlich, P., Vigh, B. & Szél, A. (2005). Photopigment coexpression in mammals: Comparative and developmental aspects. Histology and Histopathology 20, 551–574.Google Scholar
Lyubarsky, A.L., Falsini, B., Pennesi, M.E., Valentini, P. & Pugh, E.N. Jr. (1999). UV- and midwave-sensitive cone-driven retinal responses of the mouse: A possible phenotype for coexpression of cone photopigments. Journal of Neuroscience 19, 442–455.CrossRefGoogle 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, 1–14.Google Scholar
Martin, P.R., Grünert, U., Chan, T.L. & Bumsted, K. (2000). Spatial order in short-wavelength-sensitive cone photoreceptors: A comparative study of the primate retina. Journal of the Optical Society of America A 17, 557–567.Google Scholar
Müller, B. & Peichl, L. (1989). Topography of cones and rods in the tree shrew retina. Journal of Comparative Neurology 282, 581–594.Google Scholar
Oswaldo-Cruz, E., Picanço-Diniz, C.W. & Silveira, L.C.L. (1985). Physiological optics of some Amazon rodents with contrasting life style. Journal of Physiology 367, 18P.Google Scholar
Parry, J.W.L. & Bowmaker, J.K. (2002). Visual pigment coexpression in guinea pig cones: A microspectrophotometric study. Investigative Ophthalmology & Visual Science 43, 1662–1665.Google Scholar
Peichl, L. (2005). Diversity of mammalian photoreceptor properties: Adaptations to habitat and lifestyle? Anatomical Record Part A 287A, 1001–1012.Google Scholar
Peichl, L., Chavez, A.E., Ocampo, A., Mena, W., Bozinovic, F. & Palacios, A.G. (2005). Eye and vision in the subterranean rodent cururo (Spalacopus cyanus, Octodontidae). Journal of Comparative Neurology 486, 197–208.Google Scholar
Peichl, L. & González-Soriano, J. (1994). Morphological types of horizontal cell in rodent retinae: A comparison of rat, mouse, gerbil, and guinea pig. Visual Neuroscience 11, 501–517.CrossRefGoogle ScholarPubMed
Peichl, L. & Moutairou, K. (1998). Absence of short-wavelength sensitive cones in the retinae of seals (Carnivora) and African giant rats (Rodentia). European Journal of Neuroscience 10, 2586–2594.Google ScholarPubMed
Peichl, L., Nĕmec, P. & Burda, H. (2004). Unusual cone and rod properties in subterranean African mole-rats (Rodentia, Bathyergidae). European Journal of Neuroscience 19, 1545–1558.Google Scholar
Picanço-Diniz, C.W., Oliveira, H.L., 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 ScholarPubMed
Picanço-Diniz, C.W., Silveira, L.C.L., de Carvalho, M.S. & Oswaldo-Cruz, E. (1991). Contralateral visual field representation in area 17 of the cerebral cortex of the agouti: A comparison between the 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, MA: Birkhauser.Google Scholar
Rodieck, R.W. (1991). The density recovery profile: A method for the analysis of points in the plane applicable to retinal studies. Visual Neuroscience 6, 95–111.CrossRefGoogle ScholarPubMed
Rohlich, P., van Veen, T. & Szél, A. (1994). Two different visual pigments in one retinal cone cell. Neuron 13, 1159–1166.CrossRefGoogle ScholarPubMed
Sandmann, D., Boycott, B.B. & Peichl, L. (1996). Blue-cone horizontal cells in the retinae of horses and other equidae. Journal of Neuroscience 16, 3381–3396.Google Scholar
Schiviz, A.N., Ruf, T., Kuebber-Heiss, A., Schubert, C. & Ahnelt, P.K. (2008). Retinal cone topography of artiodactyl mammals: Influence of body height and habitat. Journal of Comparative Neurology 507, 1336–1350.Google Scholar
Silveira, L.C.L. (1985). Organização do sistema visual de roedores da Amazônia: O´ptica oculare distribuição das células ganglionares retinianas. D.Sc. Thesis, Instituto de Biofísica, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil.Google Scholar
Silveira, L.C.L., Picanço-Diniz, C.W. & Oswaldo-Cruz, E. (1989). Distribution and size of ganglion cells in the retinae of large Amazon rodents. Visual Neuroscience 2, 221–235.CrossRefGoogle ScholarPubMed
Szél, A., Csorba, G., Caffe, A.R., Szél, G., Rohlich, P. & van Veen, T. (1994). Different patterns of retinal cone topography in two genera of rodents, Mus and Apodemus. Cell and Tissue Research 276, 143–150.Google Scholar
Szél, A., Diamantstein, T. & Rohlich, P. (1988). Identification of the blue-sensitive cones in the mammalian retina by anti-visual pigment antibody. Journal of Comparative Neurology 273, 593–602.Google Scholar
Szél, A., Lukáts, A., Fekete, T., Szepessy, Z. & Rohlich, P. (2000). Photoreceptor distribution in the retinas of subprimate mammals. Journal of the Optical Society of America A 17, 568–579.Google Scholar
Szél, A. & Rohlich, P. (1988). Four photoreceptor types in the ground squirrel retina as evidenced by immunocytochemistry. Vision Research 28, 1297–1302.CrossRefGoogle ScholarPubMed
Szél, A. & Rohlich, P. (1992). Two cone types of rat retina detected by anti-visual pigment antibodies. Experimental Eye Research 55, 47–52.Google Scholar
Szél, A., Rohlich, P., Caffe, A.R., Juliusson, B., Aguirre, 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., Rohlich, P., Caffe, A.R. & van Veen, T. (1996). Distribution of cone photoreceptors in the mammalian retina. Microscopy Research and Technique 35, 445–462.3.0.CO;2-H>CrossRefGoogle ScholarPubMed
Szél, A., von Schantz, M., Rohlich, P., Farber, D.B. & van Veen, T. (1993). Difference in PNA label intensity between short- and middle-wavelength sensitive cones in the ground squirrel retina. Investigative Ophthalmology & Visual Science 34, 3641–3645.Google Scholar
Wang, Y., Macke, J.P., Merbs, S.L., Zack, D.J., Klaunberg, B., Bennett, J., Gearhart, J. & Nathans, J. (1992). A locus control region adjacent to the human red and green visual pigment genes. Neuron 9, 429–440.CrossRefGoogle Scholar
Weibel, E.R. (1969). Stereological principles for morphometry in electron microscopic cytology. International Review of Cytology 26, 235–302.Google Scholar
Williams, G.A., Calderone, J.B. & Jacobs, G.H. (2005). Photoreceptors and photopigments in a subterranean rodent, the pocket gopher (Thomomys bottae). Journal of Comparative Physiology A 191, 125–134.Google Scholar
Yokoyama, S. (2000). Molecular evolution of vertebrate visual pigments. Progress in Retinal and Eye Research 19, 385–419.Google Scholar