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Number and topography of cones, rods and optic nerve axons in New and Old World primates

Published online by Cambridge University Press:  03 July 2008

BARBARA L. FINLAY ,
EDNA CRISTINA S. FRANCO ,
ELIZABETH S. YAMADA ,
JUSTIN C. CROWLEY ,
MICHAEL PARSONS ,
JOSÉ AUGUSTO P.C. MUNIZ  and
LUIZ CARLOS L. SILVEIRA
BARBARA L. FINLAY*
Affiliation:
Departments of Psychology and Neurobiology and Behavior, Cornell University, Ithaca, New York
EDNA CRISTINA S. FRANCO
Affiliation:
Universidade Federal do Pará, Centro de Ciências Biológicas, Departamento de Fisiologia, Belém, Pará, Brasil
ELIZABETH S. YAMADA
Affiliation:
Universidade Federal do Pará, Centro de Ciências Biológicas, Departamento de Fisiologia, Belém, Pará, Brasil
JUSTIN C. CROWLEY
Affiliation:
Departments of Psychology and Neurobiology and Behavior, Cornell University, Ithaca, New York
MICHAEL PARSONS
Affiliation:
Departments of Psychology and Neurobiology and Behavior, Cornell University, Ithaca, New York
JOSÉ AUGUSTO P.C. MUNIZ
Affiliation:
Centro Nacional de Primatas, Ananindeua, Pará, Brasil
LUIZ CARLOS L. SILVEIRA
Affiliation:
Universidade Federal do Pará, Núcleo de Medicina Tropical, Belém, Pará, Brasil
*
Address correspondence and reprint requests to: Barbara L. Finlay, Department of Psychology, Uris Hall, Cornell University, Ithaca, NY 14853. E-mail: [email protected]
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Abstract

To better understand the evolution of spatial and color vision, the number and spatial distributions of cones, rods, and optic nerve axon numbers were assessed in seven New World primates (Cebus apella, Saimiri ustius, Saguinus midas niger, Alouatta caraya, Aotus azarae, Calllithrix jacchus, and Callicebus moloch). The spatial distribution and number of rods and cones was determined from counts of retinal whole mounts. Optic axon number was determined from optic nerve sections by electron microscopy. These data were amassed with existing data on retinal cell number and distribution in Old World primates, and the scaling of relative densities and numbers with respect to retinal area, eye and brain sizes, and foveal specializations were evaluated. Regular scaling of all cell types was observed, with the exceptionally large, rod-enriched retina of the nocturnal owl monkey Aotus azarae, and the unusually high cone density of the fovea of the trichromatic howler monkey Alouatta caraya presenting interesting variations on this basic plan. Over all species, the lawful scaling of rods, cones, and retinal ganglion cell number is hypothesized to result from a conserved sequence of cell generation that defends retinal acuity and sensitivity over a large range of eye sizes.

Keywords

RetinaNew and Old World primateConeRodOptic nerveRetinal ganglion cellAllometryFovea
Type
Research Article
Information
Visual Neuroscience , Volume 25 , Issue 3 , May 2008 , pp. 289 - 299
Copyright
Copyright © Cambridge University Press 2008

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References

REFERENCES

Andrade da Costa, B.L.S. & Hokoç, J.L. (2000). Photoreceptor topography of the retina in the New World monkey Cebus apella. Vision Research 40, 2395–2409.Google Scholar
Cepko, C.L., Austin, C.P., Yang, X.J. & Alexiades, M. (1996). Cell fate determination in the vertebrate retina. Proceedings of the National Academy of Sciences USA 93, 589–595.Google Scholar
Clancy, B., Darlington, R.B. & Finlay, B.L. (1999). The course of human events: Predicting the timing of primate neural development. Developmental Science 3, 57–66.Google Scholar
Cull, G.B., Cioffi, G.A., Dong, J., Homer, L. & Wang, L. (2003). Estimating normal optic nerve axon numbers in non-human primate eyes. Journal of Glaucoma 12, 301–306.Google Scholar
Curcio, C.A., Packer, O. & Kalina, R.E. (1987). A whole mount method for sequential analysis of photoreceptor and ganglion cell topography in a single retina. Vision Research 27, 9–15.CrossRefGoogle Scholar
Curcio, C.A., Sloan, K.R., Kalina, R.E. & Hendrickson, A.E. (1990). Human photoreceptor topography. Journal of Comparative Neurology 292, 497–523.CrossRefGoogle ScholarPubMed
Finlay, B.L. & Brodsky, P.B. (2006). Cortical evolution as the expression of a program for disproportionate growth and the proliferation of areas. In Evolution of Nervous Systems, Mammals, vol. 3. ed. Kaas, J.H. & Krubitzer, L.A., pp. 73–96. Oxford: Academic Press.Google Scholar
Finlay, B.L. & Darlington, R.B. (1995). Linked regularities in the development and evolution of mammalian brains. Science 268, 1578–1584.CrossRefGoogle ScholarPubMed
Finlay, B.L., Dyer, M.A., da Silva Filho, M., Muniz, J.A.P.C. & Silveira, L.C.L. (2007). Developmental programs coordinating size and niche variations in the primate eye and retina. In Abstracts Book of the 19th Symposium of the International Colour Vision Society (ICVS), ed. Silveira, L.C.L., Ventura, D.F. & Lee, B.B., pp. 67–68. Belém, Brazil: EDUFPA.Google Scholar
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. New York: John Wiley & Sons.Google Scholar
Fischer, Q.S. & Kirby, M.A. (1991). Number and distribution of retinal ganglion cells in anubis baboons (Papio anubis). Brain, Behavior and Evolution 37, 189–204.CrossRefGoogle ScholarPubMed
Fleagle, J.G. (1988). Primate Evolution and Adaptation. New York: Academic Press.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 new world monkeys—A constraint on eye size and conformation. Brain Behavior and Evolution 56, 276–286.CrossRefGoogle ScholarPubMed
Franco, E.C.S., Yamada, E.S., Silveira, L.C.L. & Finlay, B.L. (2007). Distribution and total number of the photoreceptors in callitrichin primates: Callithrix jacchus jacchus and Saguinus midas niger. In Abstracts Book of the 19th Symposium of the International Colour Vision Society (ICVS), ed. Silveira, L.C.L., Ventura, D.F. & Lee, B.B., pp. 177–178. Belém, Brazil: EDUFPA.Google Scholar
Gerhart, J. & Kirschner, M. (1997). Cells, Embryos and Evolution. Malden, MA: Blackwell Science.Google Scholar
Heesy, C.P. & Ross, C.F. (2001). Evolution of activity patterns and chromatic vision in primates: morphometrics, genetics and cladistics. Journal of Human Evolution 40, 111–149.Google Scholar
Hendrickson, A.E. (1994). Primate foveal development: A microcosm of current questions in neurobiology. Investigative Ophthalmology and Visual Science 35, 3129–3133.Google ScholarPubMed
Herbin, M., Boire, D. & Ptito, M. (1997). Size and distribution of retinal ganglion cells in the St. Kitts green monkey (Cercopithecus aethiops sabeus). Journal of Comparative Neurology 383, 459–472.3.0.CO;2-1>CrossRefGoogle ScholarPubMed
Hoke, K.L. & Fernald, R.D. (1997). Rod photoreceptor neurogenesis. Progress in Retinal and Eye Research 16, 31–49.CrossRefGoogle Scholar
Jacobs, G.H. (1998). Photopigments and seeing—Lessons from natural experiments—The Proctor Lecture. Investigative Ophthalmology and Visual Science 39, 2205–2216.Google Scholar
Jacobs, G.H., Neitz, M. & Neitz, J. (1996). Mutations in S-cone pigment genes and absence of color vision in two species of nocturnal primate. Proceedings of the Royal Society of London B 263, 705–710.Google Scholar
Johns, P.R. (1979). Growth and neurogenesis in adult goldfish retina. In Developmental Neurobiology of Vision, vol. 27, ed. Freeman, R.D., pp. 345–357. New York: Plenum.CrossRefGoogle Scholar
Jonas, J.B., Schmidt, A.M., Mullerbergh, J.A., Schlotzerschrehardt, U.M. & Nauman, G.O.H. (1992). Human optic nerve fiber count and optic disc size. Investigative Ophthalmology and Visual Science 33, 2012–2018.Google ScholarPubMed
Kainz, P.M., Neitz, J. & Neitz, M. (1998). Recent evolution of uniform trichromacy in a New World monkey. Vision Research 38, 3315–3320.CrossRefGoogle Scholar
LaVail, M.M., Rapaport, D.H. & Rakic, P. (1991). Cytogenesis in the monkey retina. Journal of Comparative Neurology 309, 86–114.CrossRefGoogle Scholar
Muller, H. (1952). Bau und Wachstum der Nezhaut des Guppy (Lebistes reticulatus). Zoologisches Jahrbuch. Abteilung Allg. Zool. Physiol. 63, 275–324.Google Scholar
Nagamachi, C.Y., Pieczarka, J.C., Muniz, J., Barros, R.M.S. & Mattevi, M.S. (1999). Proposed chromosomal phylogeny for the South American primates of the Callitrichidae family (Platyrrhini). American Journal of Primatology 49, 133–152.Google Scholar
Naito, J. (1996). Morphological and quantitative analysis of the fascicular pattern of monkey optic nerve. Cell and Tissue Research 283, 255–261.CrossRefGoogle ScholarPubMed
Ogden, T.E. (1975). The receptor mosaic of Aotes trivirgatus: distribution of rods and cones. Journal of Comparative Neurology 163, 193–202.CrossRefGoogle ScholarPubMed
Packer, O., Hendrickson, A.E., Curcio, C.A. (1989). Developmental redistribution of photoreceptors across the Macaca nemestrina (pigtail macaque). Journal of Comparative Neurology 288, 165–183.Google Scholar
Perry, V.H. & Cowey, A. (1985). The ganglion cell and cone distributions in the monkey's retina: Implications for central magnification factors. Vision Res. 25, 1795–1810.Google Scholar
Polley, E.H., Zimmerman, R.P. & Fortney, R.L. (1989). Neurogenesis and maturation of cell morphology in the development of the mammalian retina. In Development of the Vertebrate Retina. ed. Finlay, B.L. & Sengelaub, D.R., pp. 3–29. New York: Plenum.CrossRefGoogle Scholar
Rakic, P. (1983). Regulation of axon number in primate optic nerve by prenatal binocular competition. Nature 305, 135–137.Google Scholar
Reese, B.E. & Ho, K.-Y. (1988). Axon diameter distributions across monkey optic nerve. Neuroscience 27, 205–214.CrossRefGoogle Scholar
Robinson, S.R., Dreher, B. & McCall, M.J. (1989). Nonuniform retinal expansion during the formation of the rabbit's visual streak: Implications for the ontogeny of mammalian retinal topography. Visual Neuroscience 2, 201–219.CrossRefGoogle ScholarPubMed
Ross, C.F. (2000). Into the light: The origin of Anthropoidea. Annual Review of Anthropology 29, 147–194.CrossRefGoogle Scholar
Schneider, H., Sampaio, I., Harada, M.L., Barroso, C.M.L., Schneider, M.P.C., Czelusniak, J. & Goodman, M. (1996). Molecular phylogeny of the New World Monkeys (Platyrrhini, Primates) based on two unlinked nuclear genes: IRBP intron 1 and e-globin sequences. American Journal of Physical Anthropoogy 100, 153–179.Google Scholar
Schneider, H. (2000). The current status of the New World monkey phylogeny. Anais da Academia Brasileira de Ciências 72, 165–172.CrossRefGoogle ScholarPubMed
Silveira, L.C.L., Pincanco-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.Google Scholar
Silveira, L.C.L., Perry, V.H. & Yamada, E.S. (1993). The retinal ganglion cell distribution and the representation of the visual field in Area 17 of the owl monkey, Aotus trivirgatus. Visual Neuroscience 10, 887–897.CrossRefGoogle ScholarPubMed
Silveira, L.C.L., Yamada, E.S., Franco, E.C.S. & Finlay, B.L. (2001). The specialization of the owl monkey retina for night vision. Colour Research and Application 26, S118–S122.3.0.CO;2-9>CrossRefGoogle Scholar
Silveira, L.C.L., Zurawski, J.D., Parsons, M.P. & Finlay, B.L. (2004). Unusual retinal organization in the howler monkey. Alouatta caraya. Investigative Ophthalmology and Visual Science 45, E-Abstract 44.Google Scholar
Snow, R.L., Nelson, A., Driscoll, L.L., Hartman, K.L., Silveira, L.C.L. & Finlay, B.L. (1997). Scaling of the visual system, photoreceptors to extrastriate cortex, emphasizing primates. Society for Neuroscience Abstracts 23, 1308.Google Scholar
Stephan, H., Frahm, H. & Baron, G.. (1981). New and revised data on volumes of brain structures in insectivores and primates. Folia Primatologica 35, 1–29.Google Scholar
Stone, J. (1981). The whole mount handbook. A guide to the preparation and analysis of retinal whole mounts. Sidney: Maitland Publ PTY Ltd.Google Scholar
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 primates. The Journal of Neuroscience 10, 3390–3401.CrossRefGoogle ScholarPubMed
Wikler, K.C., Williams, R.C., Rakic, P. (1990). The photoreceptor mosaic: Number and distribution of rods and cones in the Rhesus monkey retina. Journal of Comparative Neurology 297, 499–508.Google Scholar
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