Hostname: page-component-8448b6f56d-c4f8m Total loading time: 0 Render date: 2024-04-20T12:08:14.762Z Has data issue: false hasContentIssue false
  • English
  • Français

Morphology, dendritic field size, somal size, density, and coverage of M and P retinal ganglion cells of dichromatic Cebus monkeys

Published online by Cambridge University Press:  02 June 2009

Elizabeth S. Yamada ,
Luiz Carlos L. Silveira  and
V. Hugh Perry
Elizabeth S. Yamada
Affiliation:
Departmento de Fisiologia, Universidade Federal do Pará, Belém 66075–900, Pará, Brasil
Luiz Carlos L. Silveira
Affiliation:
Departmento de Fisiologia, Universidade Federal do Pará, Belém 66075–900, Pará, Brasil
V. Hugh Perry
Affiliation:
University Department of Pharmacology, University of Oxford OX1 3QT England, UK
Get access Rights & Permissions [Opens in a new window]

Abstract

Male Cebus monkeys are all dichromats, but about two thirds of the females are trichromats. M and P retinal ganglion cells were studied in the male Cebus monkey to investigate the relationship of their morphology to retinal eccentricity. Retinal ganglion cells were retrogradely labeled after optic nerve deposits of biocytin to reveal their entire dendritic tree. Cebus M and P ganglion cell morphology revealed by biocytin retrograde filling is similar to that described for macaque and human M and P ganglion cells obtained by in vitro intracellular injection of HRP and neurobiotin. We measured 264 and 441 M and P ganglion cells, respectively. M ganglion cells have larger dendritic field and cell body size than P ganglion cells at any comparable temporal or nasal eccentricity. Dendritic trees of both M and P ganglion cells are smaller in the nasal than in the temporal region at eccentricities greater than 5 mm and 2 mm for M and P ganglion cells, respectively. The depth of terminal dendrites allows identification of both inner and outer subclasses of M and P ganglion cells. The difference in dendritic tree size between inner and outer cells is small or absent. Comparison between Cebus and Macaca shows that M and P ganglion cells have similar sizes in the central retinal region. The results support the view that M and P pathways are similarly organized in diurnal dichromat and trichromat primates.

Keywords

VisionCapuchin monkeyParallel processingBiocytin, M and P retinal ganglion cells
Type
Research Articles
Information
Visual Neuroscience , Volume 13 , Issue 6 , November 1996 , pp. 1011 - 1029
Copyright
Copyright © Cambridge University Press 1996

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., Kolb, H. & Pflug, R. (1987). Identification of a subtype of cone photoreceptor, likely to be blue sensitive in the human retina. Journal of Comparative Neurology 255, 18–34.Google Scholar
Bowmaker, J.K. (1991). Visual pigments and colour vision in primates. In From Pigments to Perception, Advances in Understanding Visual Process, ed. Valsero, A. & Lee, B.B., pp. 1–9. New York: Plenum Press.Google Scholar
Boycott, B.B. & Dowling, J.E. (1969). Organization of the primate retina: Light microscopy. Philosophical Transactions of the Royal Society B (London) 255, 109–184.Google Scholar
Casagrande, V.A. (1994). A third parallel visual pathway to primate area VI. Trends in Neuroscience 17, 305–310.Google Scholar
Casagrande, V.A. & Kaas, J.H. (1994). The afferent, intrinsic, and efferent connections of primary visual cortex in primates. In Cerebral Cortex, ser. ed. Peters, A., Vol. 10: Primary Visual Cortex in Primates, ed. Peters, A. & Rockland, K.S., pp. 201–259. New York: Plenum Press.Google Scholar
Charman, W.N. (1991). Limits on visual performance set by the eye's optics and the retinal cone mosaic. In Vision and Visual Dysfunction, ser. ed. Cronly-Dillon, J.R., Vol. 5: Limits of Vision, ed. Kulikowski, J.J., Walsh, V. & Murray, I.J., pp. 81–96. Hound-mills, Basingstoke, Hampshire and London: MacMillan Press.Google Scholar
Clark, W.E. Le Gros (1941). The laminar organization and cell content of the lateral geniculate body in the monkey. Journal of Anatomy (London) 75, 419–433.Google Scholar
Croner, L.J. & Kaplan, E. (1995). Receptive fields of P and M ganglion cells across the primate retina. Vision Research 35, 7–24.CrossRefGoogle Scholar
Dacey, D.M. (1993 a). Morphology of a small-field bistratified ganglion cell type in the macaque and human retina. Visual Neuroscience 10, 1081–1098.Google Scholar
Dacey, D.M. (1993 b). The mosaic of midget ganglion cells in the human retina. Journal of Neuroscience 13, 5334–5355.Google Scholar
Dacey, D.M. & Brace, S. (1992). A coupled network for parasol but not for midget ganglion cells in the primate retina. Visual Neuroscience 9, 279–290.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 367, 731–735.Google Scholar
Dacey, D.M. & Petersen, M.R. (1992). Dendritic field size and morphology of midget and parasol ganglion cells of the human retina. Proceedings of the National Academy of Sciences of the U. S. A. 89, 9666–9670.Google Scholar
De Monasterio, P.M., McCrane, E.P., Newlander, J.K. & Schein, S.J. (1985). Density profile of blue-sensitive cones along the horizontal meridian of macaque retina. Investigative Ophthalmology and Visual Science 26, 289–302.Google Scholar
Do Nascimento, R.S.V., Picanço-Diniz, C.W., Silveira, L.C.L. & Arruda, A.P. (1994). Colunas de dominância ocular no Cebus apella reveladas pela histoquímica de NADPH-diaforase. Resumas da IX Reunião Anual da FESSE, p. 49.Google Scholar
Do Nascimento, R.S.V., Picanç-Diniz, C.W. & Silveira, L.C.L. (1996). Complete reconstructions and quantitative analyses of ocular dominance columns of VI of Cebus monkey revealed by NADPH-diaphorase histochemistry. Investigative Ophthalmology and Visual Science (Suppl.) 37, S479.Google Scholar
Do Nascimento, R.S.V. (1995). Estudo das colunas de dominancia ocular do Cebus apella pela histoquímica de NADPH-diaforase. M. Se. Thesis, Belém: Universidade Federal do Pará & Museu Paraense Emílio Goeldi.Google Scholar
Fiorani, M. Jr., Gatass, R., Rosa, M.G.P. & Sousa, A.P.B. (1989). Visual area MT in the Cebus monkey: Location, visuotopic organization, and variability. Journal of Comparative Neurology 287, 98–118.Google Scholar
Gattass, R., Sousa, A.P.B. & Rosa, M.G.P. (1987). Visual topography of VI in the Cebus monkey. Journal of Comparative Neurology 259, 529–548.Google Scholar
Ghosh, K.K., Goodchild, A.K., Sefton, A.E. & Martin, P. (1996). The morphology of retinal ganglion cells in the New World marmoset monkey Callithrixjacchus. Journal of Comparative Neurology 366, 76–92.Google Scholar
Goodchild, A.K., Ghosh, K.K. & Martin, P. (1996). 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
Hendry, S.H.C. & Yoshioka, T. (1994). A neurochemically distinct third channel in the macaque dorsal lateral geniculate nucleus. Science 264, 575–577.CrossRefGoogle ScholarPubMed
Hess, D.T. & Edwards, M.A. (1987). Anatomical demonstration of ocular segregation in the retinogeniculocortical pathway of the New World capuchin monkey (Cebus apella). Journal of Comparative Neurology 264, 409–420.Google Scholar
Hunt, D.M., Williams, A.J., Bowmaker, J.K. & Mollon, J.D. (1993). Structure and evolution of the polymorphic photopigment gene of the marmoset. Vision Research 33, 147–154.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. & Neitz, J. (1987 a). Polymorphism of the middle wavelength cone in two species of South American monkey: Cebus apella and Callicebus moloch. Vision Research 27, 1263–1268.Google Scholar
Jacobs, G.H. & Neitz, J. (1987 b). Inheritance of color vision in a New World monkey (Saimiri sciureus). Proceedings of the National Academy of Sciences of the U.S.A. 84, 2545–2549.CrossRefGoogle Scholar
Jacobs, G.H., Neitz, J. & Crognale, M. (1987). Color vision polymorphism and its photopigment basis in a callitrichid monkey (Saguinus fuscicollis). Vision Research 27, 2089–2100.Google Scholar
Kaplan, E. & Shapley, R.M. (1986). The primate retina contains two types of ganglion cells, with high and low contrast sensitivity. Proceedings of the National Academy of Sciences of the U. S. A. 83, 2755–2757.Google Scholar
Kolb, H. & Dekorver, L. (1991). Midget ganglion cells of parafovea of the human retina: a study by electron microscopy and serialsection reconstruction. Journal of Comparative Neurology 303, 617–636.Google Scholar
Kolb, H. & Lipetz, L.E. (1991). The anatomical basis for colour vision in the vertebrate retina. In Vision and Visual Dysfunction, ser. ed. Cronly-Dillon, J.R., Vol. 6: The Perception of Colour, ed. Gouras P. pp. 128–145. Houndmills, Basingstoke, Hampshire and London: MacMillan Press.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
Kremers, J., Lee, B.B. & Kaiser, P.K. (1992). Sensitivity of macaque retinal ganglion cells and human observers to combined luminance and chromatic temporal modulation. Journal of the Optical Society of America A 9, 1477–1485.Google Scholar
Kremers, J., Lee, B.B., Pokorny, J. & SMITH V.C. (1993). Responses of macaque ganglion cells and human observers to compound periodic waveforms. Vision Research 33, 1997–2011.Google Scholar
Laughlin, S.B. (1983). Matching coding to scenes to enhance efficiency. In Physical and Biological Processing of Images, ed. Braddick, O.J. & Sleigh, A.C., pp. 42–52. Berlin: Springer.Google Scholar
Lee, B.B., Pokorny, J., Smith, V.C., Martin, P.R. & Valberg, A. (1990). Luminance and chromatic modulation sensitivity of macaque ganglion cells and human observers. Journal of the Optical Society of America A 7, 2223–2236.Google Scholar
Lee, B.B., Pokorny, J., Smith, V.C. & Kremers, J. (1994). Responses to pulses and sinusoids in macaque ganglion cells. Vision Research 34, 3081–3096.CrossRefGoogle ScholarPubMed
Lee, B.B., Silveira, L.C.L., Yamada, E.S., Silva-Filho, M. & Hunt, D.M. (1995). Estudo eletrofisiológico das respostas visuais das células ganglionares retinianas M e P do Cebus apella. Resumas da X Reunião Anual da FESBE, p. 9.Google Scholar
Leventhal, A.C., Rodieck, R.W. & Dreher, B. (1981). Retinal ganglion cell classes in the Old World monkey: Morphology and central projections. Science 213, 1139–1142.Google Scholar
Lima, S.M.A. (1993). Distribuição das Células Ganglionares M em Retinas de Primatas Diurnos e Notarnos. M. Se. Thesis, Belém: Universidade Federai do Pará & Museu Paraense Emílio Goeldi.Google Scholar
Lima, S.M.A., Siveira, L.C.L. & Perry, V.H. (1993). The M-ganglion cell density gradient in New World monkeys. Brazilian Journal of Medical and Biological Research 26, 961–964.Google Scholar
Lima, S.M.A., Silveira, L.C.L. & Perry, V.H. (1996). The distribution of M retinal ganglion cells in diurnal and nocturnal New World monkeys. Journal of Comparative Neurology 368, 538–552.Google Scholar
Livingstone, M. & Hubel, D.H. (1987). Psychophysical evidence for separate channels for the perception of form, color, movement, and depth. Journal of Neuroscience 7, 3416–3468.Google Scholar
Merigan, W.H. (1991). P and M pathway spacialization in the macaque. In From Pigments to Perception, Advances in Understanding Visual Process, ed. Valbero, A. & Lee, B.B., pp. 117–125. New York: Plenum Press.Google Scholar
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. Proceeding of the Royal Society B (London) 222, 373–399.Google Scholar
Neitz, M., Neitz, J. & Jacobs, G.H. (1991). Spectral tuning of pigments underlying red-green color vision. Science 252, 971–974.Google Scholar
Peichl, L. & Wässle, H. (1979). Size, scatter and coverage of ganglion cell receptive field centres in the cat retina. Journal of Physiology (London) 291, 117–141.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, 1125–1137.Google Scholar
Perry, V.H., Oehler, R. & Cowey, A. (1984). Retinal ganglion cells that project to the dorsal lateral geniculate nucleus in the macaque monkey. Neuroscience 12, 1101–1123.Google Scholar
Picanço-Diniz, C.W., Silveira, L.C.L., Yamada, E.S. & Martin, K.A.C. (1992). Biocytin as retrograde tracer in mammal visual system. Brazilian Journal of Medical and Biological Research 25, 57–62.Google Scholar
Polyak, S.L. (1941). The Vertebrate Retina. Chicago, Illinois: University of Chicago Press.Google Scholar
Purpura, K., Kaplan, E. & Shapley, R.M. (1988). Background light and contrast gain of primate P and M retinal ganglion cells. Proceedings of the National Academy of Sciences of the U. S. A. 85, 4534–4537.Google Scholar
Purpura, K., Kaplan, E., Tranchina, D. & Shapley, R.M. (1990). Light adaptation in the primate retina: Analysis of changes in gain and dynamics of monkey retinal ganglion cells. Visual Neuroscience 4, 75–93.CrossRefGoogle ScholarPubMed
Robinson, S.R. (1991). Development of the mammalian retina. In Vision and Visual Dysfunction, ser. ed. Cronly-Dillon, J.R., Vol. 3: Neuroanatomy of the Visual Pathways and their Development, ed. Dreher, B. & Robinson, S.R., pp. 69–128. Houndmills, Basing-stoke, Hampshire and London: MacMillan Press.Google Scholar
Rodieck, R.W. (1991). Which cells code for color? In From Pigments to Perception, Advances in Understanding Visual Processes, ed. Valberg, A. & Lee, B.B., pp. 83–93. New York: Plenum Press.CrossRefGoogle Scholar
Rodieck, R.W., Binmoeller, K.F. & Dineen, J. (1985). Parasol and midget ganglion cells of the human retina. Journal of Comparative Neurology 233, 115–132.Google Scholar
Rodieck, R.W., Brening, R.K. & Watanabe, M. (1993). The origin of parallel visual pathways. In Contrast Sensitivity, Proceedings of the Retina Research Foundation Symposia, Volumes, ed. Shapley, R. & Lam, D.M.K., pp. 117–144. Cambridge, Massachusetts: The MIT Press.Google Scholar
Rosa, M.G.P., Gatass, R., Fiorani, M. Jr., & Soares, J.G.M. (1992). Laminar, columnar, and topographic aspects of ocular dominance in the primary visual cortex of Cebus monkeys. Experimental Brain Research 88, 249–264.Google Scholar
Rosa, M.G.P., Sousa, A.P.B. & Gatass, R. (1988). Representation of the visual field in the second visual area in the Cebus monkey. Journal of Comparative Neurology 275, 326–345.CrossRefGoogle ScholarPubMed
Rowe, M.H. (1991). Functional organization of the retina. In Vision and Visual Dysfunction, ser. ed. Cronly-Dillon, J.R., Vol. 3: Neuroanatomy of the Visual Pathways and Their Development, ed. Dreher, B. & Robinson, S.R., pp. 1–68. England: MacMillan Press.Google Scholar
Schaeffel, F. & Howland, H.C. (1988). Mathematical model of emmetropization in the chicken. Journal of the Optical Society of America A 5, 2080–2086.Google Scholar
Schiller, P.H., Logothetis, N.K. & Charles, E.R. (1990 a). Role of the color-opponent and broad-band channels in vision. Visual Neuroscience 5, 321–346.Google Scholar
Schiller, P.H., Logothetis, N.K. & Charles, E.R. (1990 b). Functions of the colour-opponent and broad-band channels of the visual system. Nature (London) 343, 68–70.Google Scholar
Shapley, R. & Perry, V.H. (1986). Cat and monkey ganglion cells and their visual functions roles. Trends in Neuroscience 9, 229–235.Google Scholar
Silveira, L.C.L., Lee, B.B., Yamada, E.S., Kremers, J. & Hunt, D.M. (1996). Retinal ganglion cell responses in a dichromatic primate, Cebus apella. Investigative Ophthalmology and Visual Science (Suppl.) 37, S1056.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.Google Scholar
Silveira, L.C.L., PicançO-Uiniz, 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., Yamada, E.S., Perry, V.H. & PicançO-Uiniz, C.W. (1994 a). M and P retinal ganglion cells of diurnal and nocturnal New World monkeys. Investigative Ophthalmology and Visual Science (Suppl.) 35, 2126.Google Scholar
Silveira, L.C.L., Yamada, E.S., Perry, V.H. & Picanço-Diniz, C.W. (1994 b). M and P retinal ganglion cells of diurnal and nocturnal New World monkeys. NeuroReport 5, 2077–2081.Google Scholar
Silveira, L.C.L., Yamada, E.S. & Perry, V.H. (1995). Small-field bistratified retinal ganglion cells of the Cebus monkey. Fourth IBRO World Congress of Neuroscience Abstracts (Kyoto, Japan), p. 279.Google Scholar
Sousa, A.P.B., Piñon, M.C.G.P., Gatass, R. & Rosa, M.G.P. (1991). Topographic organization of cortical input to striate cortex in the Cebus monkey: A fluorescent tracer study. Journal of Comparative Neurology 308, 665–682.Google Scholar
Tovée, M.J. (1993). Colour vision in New World monkeys and the singlelocus X-chromosome theory. Brain, Behaviour, and Evolution 42, 116–127.Google Scholar
Tovée, M.J. (1994). The molecular genetics and evolution of primate colour vision. Trends in Neurosciences 17, 30–37.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.Google Scholar
Wässle, H., Boycott, B.B. & Röhrenbeck, J. (1989). Horizontal cells in the monkey retina: Cone connections and dendrite network. European Journal of Neuroscience 1, 421–435.Google Scholar
Wässle, H. & Boycott, B.B. (1991). Functional architecture of the mammalian retina. Physiological Reviews 71, 447–480.Google Scholar
Wässle, H., Grünert, U., Martin, P.R. & Boycott, B.B. (1994). Color coding in the primate retina: Predictions and constrains from anatomy. In Structural and Functional Organization of the Neocortex, ed. Albowitz, B., Albus, K., Kuhnt, U., Nothdurft, H.-Ch. & Wahle, P., pp. 94–104. Berlin: Springer-Verlag.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
Watanabe, M. & Rodieck, R.W. (1989). Parasol and midget ganglion cells. Journal of Comparative Neurology 289, 434–454.Google Scholar
Williams, A.J., Hunt, D.M., Bowmaker, J.K. & Molon, J.D. (1992). The polymorphic photopigments of the marmoset: Spectral tuning and genetic basis. EMBO Journal 11, 2039–2045.Google Scholar
Yamada, E.S. (1995). Organizaçño Morfofuncionaldo Sistema Visual de Primatas Platirrinos: Ançlise Quantitativa da Morfologia, Densidade e Cobertura Dendrítica das Células Canglionares Retinianas M e P de Cebuse Aotus. D. Se. Thesis, Belém: Universidade Federai do Pará & Museu Paraense Emílio Goeldi.Google Scholar
Yamada, E.S., Silveira, L.C.L. & Perry, V.H. (1995 a). M and P retinal ganglion cells of the Cebus monkey. Investigative Ophthalmology and Visual Science (Suppl.) 36, 931.Google Scholar
Yamada, E.S., Silveira, L.C.L., Lee, B.B., & Gomes, F.L. (1995 b) Espécimes dicromatas de Callithrix jacchus possuem células ganglionares M e P. Resumas da X Reunião Anual da FESBE, p. 11.Google Scholar
Yamada, E.S., Silveira, L.C.L. & Perry, V.H. (1996). The morphology and photoreceptor convergence of Aotus M and P retinal ganglion cells. Investigative Ophthalmology and Visual Science (Suppl.) 37, S631.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
Young, F.A. & Leary, G.A. (1991). Refractive error in relation to the development of the eye. In Vision and Visual Dysfunction, ser. ed. Cronly-Dillon, J.R., Vol. 1: Visual Optics and Visual Instrumentation, ed. Charman W.N., pp. 1–68. Houndmills, Basingstoke, Hampshire and London: MacMillan Press.Google Scholar