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Mosaic properties of midget and parasol ganglion cells in the marmoset retina

Published online by Cambridge University Press:  06 October 2005

BRETT A. SZMAJDA ,
ULRIKE GRÜNERT  and
PAUL R. MARTIN
BRETT A. SZMAJDA
Affiliation:
National Vision Research Institute of Australia, Carlton, Australia Department of Optometry and Vision Sciences, The University of Melbourne, Australia
ULRIKE GRÜNERT
Affiliation:
National Vision Research Institute of Australia, Carlton, Australia Department of Optometry and Vision Sciences, The University of Melbourne, Australia
PAUL R. MARTIN
Affiliation:
National Vision Research Institute of Australia, Carlton, Australia Department of Optometry and Vision Sciences, The University of Melbourne, Australia
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Abstract

We measured mosaic properties of midget and parasol ganglion cells in the retina of a New World monkey, the common marmoset Callithrix jacchus. We addressed the functional specialization of these populations for color and spatial vision, by comparing the mosaic of ganglion cells in dichromatic (“red–green color blind”) and trichromatic marmosets. Ganglion cells were labelled by photolytic amplification of retrograde marker (“photofilling”) following injections into the lateral geniculate nucleus, or by intracellular injection in an in vitro retinal preparation. The dendritic-field size, shape, and overlap of neighboring cells were measured. We show that in marmosets, both midget and parasol cells exhibit a radial bias, so that the long axis of the dendritic field points towards the fovea. The radial bias is similar for parasol cells and midget cells, despite the fact that midget cell dendritic fields are more elongated than are those of parasol cells. The dendritic fields of midget ganglion cells from the same (ON or OFF) response-type array show very little overlap, consistent with the low coverage of the midget mosaic in humans. No large differences in radial bias, or overlap, were seen on comparing retinae from dichromatic and trichromatic animals. These data suggest that radial bias in ganglion cell populations is a consistent feature of the primate retina. Furthermore, they suggest that the mosaic properties of the midget cell population are associated with high spatial resolution rather than being specifically associated with trichromatic color vision.

Keywords

Callithrix jacchusNew World primateColor visionCoverageDendritic-field orientation
Type
Research Article
Information
Visual Neuroscience , Volume 22 , Issue 4 , July 2005 , pp. 395 - 404
Copyright
2005 Cambridge University Press

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References

REFERENCES

Blessing, E.M., Solomon, S.G., Hashemi-Nezhad, M., Morris, B.J., & Martin, P.R. (2004). Chromatic and spatial properties of parvocellular cells in the lateral geniculate nucleus of the marmoset (Callithrix jacchus). Journal of Physiology 557, 229–245.Google Scholar
Dacey, D.M. (1993a). 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. (1993b). 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 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., Peterson, B.B., Robinson, F.R., & Gamlin, P.D. (2003). Fireworks in the primate retina: In vitro photodynamics reveals diverse LGN-projecting ganglion cell types. Neuron 37, 15–27.Google Scholar
Diller, L., Packer, O.S., Verweij, J., McMahon, M.J., Williams, D.R., & Dacey, D.M. (2004). L and M cone contributions to the midget and parasol ganglion cell receptive fields of macaque monkey retina. Journal of Neuroscience 24, 1079–1088.Google Scholar
Eysel, U.T., Peichl, L., & Wässle, H. (1985). Dendritic plasticity in the early postnatal feline retina: Quantitative characteristics and sensitive period. Journal of Comparative Neurology 242, 134–145.Google Scholar
Ghosh, K.K., Goodchild, A.K., Sefton, A.E., & Martin, P.R. (1996). Morphology of retinal ganglion cells in a New World monkey, the marmoset Callithrix jacchus. Journal of Comparative Neurology 366, 76–92.Google Scholar
Grünert, U., Greferath, U., Boycott, B.B., & Wässle, H. (1993). Parasol (P alpha) ganglion-cells of the primate fovea: Immunocytochemical staining with antibodies against GABA-A receptors. Vision Research 33, 1–14.Google Scholar
Harlow, E. & Lane, D. (1988). Antibodies: A laboratory manual. New York: Cold Spring Harbor Laboratory.
Jacobs, G.H. (1983). Differences in spectral response properties of LGN cells in male and female squirrel monkeys. Vision Research 23, 461–468.Google Scholar
Jan, Y.N. & Jan, L.Y. (2003). The control of dendrite development. Neuron 40, 229–242.Google Scholar
Kremers, J. & Weiss, S. (1997). Receptive field dimensions of lateral geniculate cells in the common marmoset (Callithrix jacchus). Vision Research 37, 2171–2181.Google Scholar
Lee, B.B., Creutzfeldt, O.D., & Elepfandt, A. (1979). The responses of magno- and parvocellular cells of the monkey's lateral geniculate body to moving stimuli. Experimental Brain Research 35, 547–557.Google Scholar
Lennie, P., Haake, P.W., & Williams, D.R. (1991). The design of chromatically opponent receptive fields. In Computational Models of Visual Processing, ed. Landy, M.S. & Movshon, J.A., pp. 71–82. Cambridge, Massachusetts: MIT Press.
Leventhal, A.G. (1983). Relationship between preferred orientation and receptive field position of neurons in cat striate cortex. Journal of Comparative Neurology 220, 476–483.Google Scholar
Leventhal, A.G., Ault, S.J., Vitek, D.J., & Shou, T. (1989). Extrinsic determinants of retinal ganglion cell development in primates. Journal of Comparative Neurology 286, 170–189.Google Scholar
Leventhal, A.G., 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
Leventhal, A.G. & Schall, J.D. (1983). Structural basis of orientation sensitivity of cat retinal ganglion cells. Journal of Comparative Neurology 220, 465–475.Google Scholar
Levick, W.R. & Thibos, L.N. (1982). Analysis of orientation bias in cat retina. Journal of Physiology 329, 243–261.Google Scholar
Lin, B., Wang, S.W., & Masland, R.H. (2004). Retinal ganglion cell type, size, and spacing can be specified independent of homotypic dendritic contacts. Neuron 43, 475–485.Google Scholar
Lohmann, C. & Wong, R.O. (2001). Cell-type specific dendritic contacts between retinal ganglion cells during development. Journal of Neurobiology 48, 150–162.Google Scholar
Martin, P.R., Lee, B.B., White, A.J., Solomon, S.G., & Rüttiger, L. (2001). Chromatic sensitivity of ganglion cells in the peripheral primate retina. Nature 410, 933–936.Google Scholar
McIlwain, J.T. (1986). Point images in the visual system: New interest in an old idea. Trends in Neurosciences 9, 354–358.Google Scholar
Montague, P.R. & Friedlander, M.J. (1989). Expression of an intrinsic growth strategy by mammalian retinal neurons. Proceedings of the National Academy of Sciences of the U.S.A. 86, 7223–7227.Google Scholar
Passaglia, C.L., Troy, J.B., Rüttiger, L., & Lee, B.B. (2002). Orientation sensitivity of ganglion cells in primate retina. Vision Research 42, 683–694.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 Research 25, 1795–1810.Google Scholar
Perry, V.H. & Linden, R. (1982). Evidence for dendritic competition in the developing retina. Nature 297, 683–685.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
Polyak, S.L. (1941). The Retina. Chicago, IL: University of Chicago Press.
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
Schall, J.D. & Leventhal, A.G. (1987). Relationships between ganglion cell dendritic structure and retinal topography in the cat. Journal of Comparative Neurology 257, 149–159.Google Scholar
Schall, J.D., Perry, V.H., & Leventhal, A.G. (1986a). Retinal ganglion cell dendritic fields in old-world monkeys are oriented radially. Brain Research 368, 18–23.Google Scholar
Schall, J.D., Vitek, D.J., & Leventhal, A.G. (1986b). Retinal constraints on orientation specificity in cat visual cortex. Journal of Neuroscience 6, 823–836.Google Scholar
Shou, T., Leventhal, A.G., Thompson, K.G., & Zhou, Y. (1995). Direction biases of X and Y type retinal ganglion cells in the cat. Journal of Neurophysiology 73, 1414–1421.Google Scholar
Shou, T.D. & Leventhal, A.G. (1989). Organized arrangement of orientation-sensitive relay cells in the cat's dorsal lateral geniculate nucleus. Journal of Neuroscience 9, 4287–4302.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., 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
Smith, E.L., Chino, Y.M., Ridder, W.H., Kitagawa, K., & Langston, A. (1990). Orientation bias of neurons in the lateral geniculate nucleus of macaque monkeys. Visual Neuroscience 5, 525–545.Google Scholar
Solomon, S.G., Lee, B.B., White, A.J., Ruttiger, L., & Martin, P.R. (2005). Chromatic organization of ganglion cell receptive fields in the peripheral retina. Journal of Neuroscience 25, 4527–4539.Google Scholar
Solomon, S.G., White, A.J., & Martin, P.R. (2002). Extraclassical receptive field properties of parvocellular, magnocellular, and koniocellular cells in the primate lateral geniculate nucleus. Journal of Neuroscience 22, 338–349.Google Scholar
Vaney, D.I. (1992). Photochromic intensification of diaminobenzidine reaction product in the presence of tetrazolium salts: Applications for intracellular labelling and immunohistochemistry. Journal of Neuroscience Methods 44, 217–223.Google Scholar
Vidyasagar, T.R. & Urbas, J.V. (1982). Orientation sensitivity of cat LGN neurones with and without inputs from visual cortical areas 17 and 18. Experimental Brain Research 46, 157–169.Google Scholar
Wässle, H. & Boycott, B.B. (1991). Functional architecture of the mammalian retina. Physiological Reviews 71, 447–480.Google Scholar
Wässle, H., Boycott, B.B., & Illing, R.B. (1981a). Morphology and mosaic of on- and off-beta cells in the cat retina and some functional considerations. Proceedings of the Royal Society B (London) 212, 177–195.Google Scholar
Wässle, H., Peichl, L., & Boycott, B.B. (1981b). Dendritic territories of cat retinal ganglion cells. Nature 292, 344–345.Google Scholar
Wässle, H., Peichl, L., & Boycott, B.B. (1981c). Morphology and topography of on- and off-alpha cells in the cat retina. Proceedings of the Royal Society B (London) 212, 157–175.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 of the primate retina. Journal of Comparative Neurology 289, 434–454.Google Scholar
White, A.J., Solomon, S.G., & Martin, P.R. (2001). Spatial properties of koniocellular cells in the lateral geniculate nucleus of the marmoset Callithrix jacchus. Journal of Physiology 533, 519–535.Google Scholar
White, A.J., Wilder, H.D., Goodchild, A.K., Sefton, A.J., & Martin, P.R. (1998). Segregation of receptive field properties in the lateral geniculate nucleus of a New-World monkey, the marmoset Callithrix jacchus. Journal of Neurophysiology 80, 2063–2076.Google Scholar
Wong, R.O. & Ghosh, A. (2002). Activity-dependent regulation of dendritic growth and patterning. Nature Reviews Neuroscience. 3, 803–812.Google Scholar
Xu, X., Ichida, J., Shostak, Y., Bonds, A.B., & Casagrande, V.A. (2002). Are primate lateral geniculate nucleus (LGN) cells really sensitive to orientation or direction? Visual Neuroscience 19, 97–108.Google Scholar
Yamada, E.S., Silveira, L.C., & Perry, V.H. (1996). 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