Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-23T06:48:38.288Z Has data issue: false hasContentIssue false
  • English
  • Français

Horizontal cell morphology in nocturnal and diurnal primates: A comparison between owl-monkey (Aotus) and capuchin monkey (Cebus)

Published online by Cambridge University Press:  06 October 2005

SETSUKO N. DOS SANTOS ,
JOSÉ WESLEY L. DOS REIS ,
MANOEL DA SILVA FILHO ,
JAN KREMERS  and
LUIZ CARLOS L. SILVEIRA
SETSUKO N. DOS SANTOS
Affiliation:
Departamento de Fisiologia, Universidade Federal do Pará, Belém, Pará Brasil
JOSÉ WESLEY L. DOS REIS
Affiliation:
Departamento de Fisiologia, Universidade Federal do Pará, Belém, Pará Brasil
MANOEL DA SILVA FILHO
Affiliation:
Departamento de Fisiologia, Universidade Federal do Pará, Belém, Pará Brasil
JAN KREMERS
Affiliation:
Department of Experimental Ophthalmology, University of Tübingen, Germany
LUIZ CARLOS L. SILVEIRA
Affiliation:
Departamento de Fisiologia, Universidade Federal do Pará, Belém, Pará Brasil
Get access Rights & Permissions [Opens in a new window]

Abstract

Horizontal cell morphology was studied in the retina of the nocturnal owl-monkey, Aotus, and compared with that of its diurnal, close relative, the capuchin monkey, Cebus. Cells were initially labeled with DiI and the staining was later photoconverted in a stable precipitated using DAB as chromogen. The sizes of cell bodies, dendritic fields, and axon terminals, number of dendritic clusters, intercluster spacing, and intercone spacing were measured at increasing eccentricities. Two distinct morphological classes of horizontal cells were identified, which resembled those of H1 and H3 cells described in diurnal monkeys. A few examples of a third class, possibly corresponding to the H2 cells of diurnal monkeys, were labeled. Both H1 and H3 cells increased in size and had increasing numbers of dendritic clusters with eccentricity. H3 cells were larger and had a larger number of dendritic clusters than H1 cells. Owl-monkey H1 cells had larger dendritic fields than capuchin monkey H1 cells at all quadrants in the central and midperipheral retinal regions, but the difference disappeared in the far periphery. Owl-monkey and capuchin monkey H1 cells had about the same number of dendritic clusters across eccentricity. As owl-monkey H1 cells were larger than capuchin monkey H1 cells, the equal number of clusters in these two primates was due to the fact that they were more spaced in the owl-monkey cells. H1 intercluster distance closely matched intercone spacing for both the owl-monkey and capuchin monkey retinas. On the other hand, H3 intercluster distance was larger than intercone spacing in the retina of both primates. Owl-monkey H1 axon terminals had 2–3 times more knobs than capuchin monkey H1 axon terminals in spite of having about the same size and, consequently, knob density was 2–3 times higher for owl-monkey than capuchin monkey H1 axon terminals across all eccentricities. The differences observed between owl-monkey and capuchin monkey horizontal cells, regarding the morphology of their dendritic trees and axon terminals, may be related to the differences found in the cone-to-rod ratio in the retina of these two primates. They seem to represent retinal specializations to the nocturnal and diurnal life styles of the owl-monkey and capuchin monkey, respectively.

Keywords

Horizontal cellsRetinal circuitryPrimate visionAotusCebusCarbocyanine dye
Type
Research Article
Information
Visual Neuroscience , Volume 22 , Issue 4 , July 2005 , pp. 405 - 415
Copyright
2005 Cambridge University Press

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

REFERENCES

Ahnelt, P. & Kolb, H. (1994a). Horizontal cells and cone photoreceptors in primate retina: A Golgi-light microscopy study of spectral connectivity. Journal of Comparative Neurology 343, 387–405.Google Scholar
Ahnelt, P. & 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
Boycott, B.B. & Kolb, H. (1973). The horizontal cells of the rhesus monkey. Journal of Comparative Neurology 148, 115–140.Google Scholar
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, 345–379.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 Callithrix jacchus: A comparison with macaque monkey. Visual Neuroscience 14, 125–140.Google 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. Journal of Comparative Neurology 437, 219–239.Google Scholar
Dacey, D.M. & Lee, B.B. (1994). The “blue-on” opponent pathway in primate retina originates from a distinct bistratified ganglion cell type. Nature (London) 367, 731–735.Google Scholar
Dacey, D.M., Lee, B.B., Stafford, D.K., Pokorny, J., & Smith, V.C. (1996). Horizontal cells of the primate retina: Cone specificity without spectral opponency. Science (New York) 271, 656–659.Google Scholar
Da Silva Filho, M., Santos, R.N., Santos, D.V.V., Dos Santos, S.N., & Silveira, L.C.L. (2003). Fotoconversão: Um método simples para revelar a morfologia celular. XVIII FESBE Annual Meeting Abstracts CD-ROM, 16729.html, Program. No 01.05.035.
De Lima, S.M.A., Silveira, L.C.L., & Perry, V.H. (1996). Distribution of M retinal ganglion cells in diurnal and nocturnal New-World monkeys. Journal of Comparative Neurology 368, 538–552.Google Scholar
Dos Reis, J.W.L., De Carvalho, W.A., Saito, C.A., & Silveira, L.C.L. (2002). The 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., Dos Reis, J.W.L., Kremers, J., & Silveira, L.C.L. (2000). Morphology and size of owl monkey horizontal cells. ARVO Annual Meeting Abstracts. Investigative Ophthalmology and Visual Science 41, S944.Google Scholar
Fernández, E., Bolea, J.A., Ortega, G., & Louis, E. (1999). Are neurons multifractals? Journal of Neuroscience Methods 89, 151–157.Google Scholar
Finlay, B.L., Silveira, L.C.L., & Reichenbach, A. (2005). Comparative aspects of visual system development. In Structure, Function, and Evolution of the Primate Visual System, ed. Kremers, J., pp. 37–72, Chichester, England: John Wiley & Sons.
Franco, E.C.S. (2002). Análise Comparativa da Distribuição e Número Total de Fotorreceptores em Seis Espécies de Primatas do Novo Mundo: Correlação com a Hipótese do Escalonamento Neuronal. M.Sc. Thesis. Belém: Universidade Federal do Pará.
Ghosh, K.K., Goodchild, A.K., Sefton, A.E., & Martin, P.R. (1996). The morphology of retinal ganglion cells in the New World marmoset monkey Callithrix jacchus. Journal of Comparative Neurology 366, 76–92.Google Scholar
Ghosh, K.K., Martin, P.R., & Grünert, U. (1997). Morphological analysis of the blue cone pathway in the retina of a New World monkey, the marmoset Callithrix jacchus. Journal of Comparative Neurology 379, 211–225.Google Scholar
Goodchild, A.K., Ghosh, K.K., & Martin, P.R. (1996a). A comparison of photoreceptor spatial density and ganglion cell morphology in the retina of human, macaque monkey, cat, and the marmoset Callithrix jacchus. Journal of Comparative Neurology 366, 55–75.Google Scholar
Goodchild, A.K., Chan, T.L., & Grünert, U. (1996b). Horizontal cell connections with short-wavelength-sensitive cones in macaque monkey retina. Visual Neuroscience 13, 833–845.Google Scholar
Jacobs, G.H. & Neitz, J. (1987). Polymorphism of the middle wavelength cone in two species of South American monkey: Cebus apella and Callicebus molloch. Vision Research 27, 1263–1268.Google Scholar
Jacobs, G.H. & Deegan, II, J.F. (2001). Photopigments and colour vision in New World monkeys from the family Atelidae. Proceedings of the Royal Society B (London) 268, 695–702.Google Scholar
Jacobs, G.H. & Deegan, II, J.F. (2003). Cone pigment variations in four genera of New World monkeys. Vision Research 43, 227–236.Google Scholar
Jacobs, G.H., Neitz, J., & Crognale, M. (1987). Color vision polymorphism and its photopigment basis in a callitrichid monkey (Saguinus fuscicolis). Vision Research 27, 2089–2100.Google Scholar
Jacobs, G.H., Neitz, J., & Neitz, M. (1993a). Genetic basis of polymorphism in the color vision of platyrrhine monkeys. Vision Research 33, 269–274.Google Scholar
Jacobs, G.H., Deegan, II, J.F., Neitz, J., Crognale, M.A., & Neitz, M. (1993b). Photopigments and colour vision in the nocturnal monkey, Aotus. Vision Research 33, 1773–1783.Google Scholar
Jacobs, G.H., Neitz, M., Deegan, II, J.F., & Neitz, J.A. (1996a). Trichromatic colour vision in New World monkeys. Nature (London) 382, 156–158.Google Scholar
Jacobs, G.H., Neitz, M., & Neitz, J. (1996b). Mutations in S-cone pigment genes and the absence of colour vision in two species of nocturnal primate. Proceedings of the Royal Society B (London) 263, 705–710.Google Scholar
Jelinek, H.F. & Fernández, E. (1998). Neurons and fractals: How reliable and useful are calculations of fractal dimensions? Journal of Neuroscience Methods 81, 9–18.Google Scholar
Kolb, H., Mariani, A., & Gallego, A. (1980). A second type of horizontal cell in the monkey retina. Journal of Comparative Neurology 189, 31–44.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., Fernández, E., Schouten, J., Ahnelt, P., Linberg, K.A., & Fisher, S.K. (1994). Are there three types of horizontal cell in the human retina? Journal of Comparative Neurology 343, 370–386.Google Scholar
Kremers, J., Silveira, L.C.L., Yamada, E.S., & Lee, B.B. (1999). The ecology and evolution of primate colour vision. In Color Vision: From Molecular Genetics to Perception, ed. Gegenfurtner, K.R. & Sharpe, L.T., pp. 123–142. Cambridge, England: Cambridge University Press.
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. Journal of Physiology (London) 528, 573–590.Google Scholar
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 World monkey, the marmoset, Callithrix jacchus. Visual Neuroscience 16, 709–719.Google Scholar
Mandelbrot, B. (1982). The Fractal Geometry of Nature. New York: W.H. Freeman.
Mollon, J.D., Bowmaker, J.K., & Jacobs, G.H. (1984). Variations of colour vision in a New World primate can be explained by polymorphism of retinal photopigments. Proceedings of the Royal Society B (London) 222, 373–399.Google Scholar
Ogden, T.E. (1974). The morphology of retinal neurons of the owl monkey Aotes. Journal of Comparative Neurology 153, 399–428.Google Scholar
Ogden, T.E. (1975). The receptor mosaic of Aotes trivirgatus: Distribution of rods and cones. Journal of Comparative Neurology 163, 193–202.Google Scholar
Polyak, S.L. (1941). The Retina. Chicago, Illinois: University of Chicago Press.
Rodieck, R.W. (1988). The primate retina. In Comparative Primate Biology, Volume 4: Neuroscience, ed. Steklis, H.D. & Erwin, J., pp. 203–278. New York: Alan R. Liss.
Rodieck, R.W. (1989). Letter from Professor Robert W. Rodieck to Mrs. Donna Polyak, widow of Stephen Polyak. In Seeing, ed. Rodieck, R.W., pp. 24. Seattle, Washington: University of Washington.
Saito, C.A., Da Silva Filho, M., Lee, B.B., Bowmaker, J.K., Kremers, J., & Silveira, L.C.L. (2004). Alouatta trichromatic color vision—single-unit recording from retinal ganglion cells and microspectrophotometry. ARVO Annual Meeting Abstract Search and Program Planner CD-ROM, Program No 4276.
Sandell, J.H. & Masland, R.H. (1988). Photoconversion of some fluorescent markers to a diaminobenzidine product. Journal of Histochemistry and Cytochemistry 36, 555–559.Google Scholar
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, Florida: CRC Press.
Silveira, L.C.L., Yamada, E.S., Perry, V.H., & Picanço Diniz, C.W. (1994). M and P retinal ganglion cells of diurnal and nocturnal New World monkeys. NeuroReport 5, 2077–2081.Google Scholar
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.Google Scholar
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.Google Scholar
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 and Application 26, S118–S122.Google Scholar
Silveira, L.C.L., Saito, C.A., Lee, B.B., Kremers, J., Da Silva Filho, M., Kilavik, B.E., Yamada, E.S., & Perry, V.H. (2004). Morphology and physiology of primate M and P cells. Progress in Brain Research 144, 21–46.Google Scholar
Tovée, M.J., Bowmaker, J.K., & Mollon, J.D. (1992). The relationship between cone pigments and behavioural sensitivity in a New World monkey (Callithrix jacchus jacchus). Vision Research 32, 867–878.Google Scholar
Travis, D.S., Bowmaker, J.K., & Mollon, J.D. (1988). Polymorphism of visual pigments in a callitrichid monkey. Vision Research 28, 481–490.Google Scholar
Warfel, M. (1997). Fractal macros for NIH Image software. http://www.cee.cornell.edu/mdw/research.html.
Wässle, H., Boycott, B.B., & Röhrenbeck, J. (1989). Horizontal cells in the monkey retina: Cone connections and dendritic network. European Journal of Neuroscience 1, 421–435.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
Wikler, K.C. & Rakic, P. (1990). Distribution of photoreceptor subtypes in the retina of diurnal and nocturnal primates. Journal of Neuroscience 10, 3390–3401.Google Scholar
Yamada, E.S. (1995). Organização Morfofuncional do Sistema Visual de Primatas Platirrinos: Análise Quantitativa da Morfologia, Densidade e Cobertura Dendrítica das Células Ganglionares Retinianas M e P de Cebus e Aotus. Ph.D. Thesis. Belém: Universidade Federal do Pará.
Yamada, E.S., Silveira, L.C.L., & Perry, V.H. (1996a). Morphology, dendritic field size, somal size, density and coverage of M and P retinal ganglion cells of dichromatic Cebus monkeys. Visual Neuroscience 13, 1011–1029.Google Scholar
Yamada, E.S., Silveira, L.C.L., Gomes, F.L., & Lee, B.B. (1996b). The retinal ganglion cell classes of New World primates. Revista Brasileira de Biologia 56 (Suppl. 1), 381–396.Google 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.Google Scholar
Yeh, T., Lee, B.B., Kremers, J., Cowing, J.A., Hunt, D.M., Martin, P.R., & Troy, J.B. (1995). Visual responses in the lateral geniculate nucleus of dichromatic and trichromatic marmosets (Callithrix jacchus). Journal of Neuroscience 15, 7892–7904.Google Scholar