Hostname: page-component-78c5997874-fbnjt Total loading time: 0 Render date: 2024-11-19T10:33:30.621Z Has data issue: false hasContentIssue false
  • English
  • Français

Wide-field ganglion cells in macaque retinas

Published online by Cambridge University Press:  06 October 2005

ELIZABETH S. YAMADA ,
ANDREA S. BORDT  and
DAVID W. MARSHAK
ELIZABETH S. YAMADA
Affiliation:
Department of Neurobiology and Anatomy, University of Texas Medical School, Houston Departamento de Fisiologia, Universidade Federal do Pará, Belém, Brasil
ANDREA S. BORDT
Affiliation:
Department of Neurobiology and Anatomy, University of Texas Medical School, Houston
DAVID W. MARSHAK
Affiliation:
Department of Neurobiology and Anatomy, University of Texas Medical School, Houston
Get access Rights & Permissions [Opens in a new window]

Abstract

To describe the wide-field ganglion cells, they were injected intracellularly with Neurobiotin using an in vitro preparation of macaque retina and labeled with streptavidin-Cy3. The retinas were then labeled with antibodies to choline acetyltransferase and other markers to indicate the depth of the dendrites within the inner plexiform layer (IPL) and analyzed by confocal microscopy. There were eight different subtypes of narrowly unistratified cells that ramified in each of the 5 strata, S1–5, including narrow thorny, large sparse, large moderate, large dense, large radiate, narrow wavy, large very sparse, and fine very sparse. There were four types of broadly stratified cells with dendritic trees extending from S4 to S2. One type resembled the parvocellular giant cell and another the broad thorny type described previously in primates. Another broadly stratified cell was called multi-tufted based on its distinctive dendritic branching pattern. The fourth type had been described previously, but not named; we called it broad wavy. There was a bistratified type with its major arbor in S5, the same level as the blue cone bipolar cell; it resembled the large, bistratified cell with blue ON-yellow OFF responses described recently. Two wide-field ganglion cell types were classified as diffuse because they had dendrites throughout the IPL. One had many small branches and was named thorny diffuse. The second was named smooth diffuse because it had straighter dendrites that lacked these processes. Dendrites of the large moderate and multi-tufted cells cofasciculated with ON-starburst cell dendrites and were, therefore, candidates to be ON- and ON–OFF direction-selective ganglion cells, respectively. We concluded that there are at least 15 morphoplogical types of wide-field ganglion cells in macaque retinas.

Keywords

AcetylcholinePlexiformStratificationConfocal
Type
Research Article
Information
Visual Neuroscience , Volume 22 , Issue 4 , July 2005 , pp. 383 - 393
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

Amthor, F.R., Takahashi, E.S., & Oyster, C.W. (1989). Morphologies of rabbit retinal ganglion cells with complex receptive fields. Journal of Comparative Neurology 280, 97–121.Google Scholar
Berson, D.M., Pu, M., & Famiglietti, E.V. (1998). The zeta cell: A new ganglion cell type in cat retina. Journal of Comparative Neurology 399, 269–288.Google Scholar
Boycott, B.B. & Wässle, H. (1974). The morphological types of ganglion cells of the domestic cat's retina. Journal of Physiology 240, 397–419.Google Scholar
Cleland, B.G., Levick, W.R., & Wässle, H. (1975). Physiological identification of a morphological class of cat retinal ganglion cells. Journal of Physiology 248, 151–171.Google Scholar
Dacey, D.M. (1989). Monoamine-accumulating ganglion cell type of the cat's retina. Journal of Comparative Neurology 288, 59–80.Google Scholar
Dacey, D.M. (1994). Physiology, morphology and spatial densities of identified ganglion cell types in primate retina. Ciba Foundation Symposium 184, 12–28; discussion 28–34, 63–70.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
de Monasterio, F.M. (1978). Properties of ganglion cells with atypical receptive-field organization in retina of macaques. Journal of Neurophysiology 41, 1435–1449.Google Scholar
Dong, W., Sun, W., Zhang, Y., Chen, X., & He, S. (2004). Dendritic relationship between starburst amacrine cells and direction selective ganglion cells in the rabbit retina. Journal of Physiology 556.1, 11–17.Google Scholar
Enroth-Cugell, C. & Robson, J.G. (1966). The contrast sensitivity of retinal ganglion cells of the cat. Journal of Physiology 187, 517–552.Google Scholar
Famiglietti, E.V. (1992a). New metrics for analysis of dendritic branching patterns demonstrating similarities and differences in ON and ON–OFF directionally selective retinal ganglion cells. Journal of Comparative Neurology 324, 295–321.Google Scholar
Famiglietti, E.V. (1992b). Dendritic co-stratification of ON and ON–OFF directionally selective ganglion cells with starburst amacrine cells in rabbit retina. Journal of Comparative Neurology 324, 322–335.Google Scholar
Famiglietti, E.V. (2004). Class I and class II ganglion cells of rabbit retina: A structural basis for X and Y (brisk) cells. Journal of Comparative Neurology 478, 323–346.Google Scholar
He, S. & Masland, R.H. (1998). ON direction-selective ganglion cells in the rabbit retina: Dendritic morphology and pattern of fasciculation. Visual Neuroscience 15, 369–375.Google Scholar
Isayama, T., Berson, D.M., & Pu, M. (2000). Theta ganglion cell type of cat retina. Journal of Comparative Neurology 417, 32–48.Google Scholar
Jacoby, R.A., Wiechmann, A.F., Amara, S.G., Leighton, B.H., & Marshak, D.W. (2000). Diffuse bipolar cells provide input to OFF parasol ganglion cells in the macaque retina. Journal of Comparative Neurology 416, 6–18.Google Scholar
Kaplan, E. & Shapley, R.M. (1982). X and Y cells in the lateral geniculate nucleus of macaque monkeys. Journal of Physiology 330, 125–143.Google Scholar
Kolb, H., Linberg, K.A., & Fisher, S.K. (1992). Neurons of the human retina: A Golgi study. Journal of Comparative Neurology 318, 147–187.Google Scholar
Linberg, K.A., Suemune, S., & Fisher, S.K. (1996). Retinal neurons of the California ground squirrel, Spermophilus beecheyi: A Golgi study. Journal of Comparative Neurology 365, 173–216.Google Scholar
Marshak, D.W. (2001). Synaptic inputs to dopaminergic neurons in mammalian retinas. Progress in Brain Research 131, 83–91.Google Scholar
O'Brien, B.J., Isayama, T., Richardson, R., & Berson, D.M. (2002). Intrinsic physiological properties of cat retinal ganglion cells. Journal of Physiology 538, 787–802.Google Scholar
Peterson, B.B. & Dacey, D.M. (1999). Morphology of wide-field, monostratified ganglion cells of the human retina. Visual Neuroscience 16, 107–120.Google Scholar
Peterson, B.B. & Dacey, D.M. (2000). Morphology of wide-field bistratified and diffuse human retinal ganglion cells. Visual Neuroscience 17, 567–578.Google Scholar
Peterson, B.B., Liao, H.-W., Dacey, D.M., Yau, K.-W., Gamlin, P.D., Robinson, F.R., & Marshak D.W. (2003). Functional architecture of the photoreceptive ganglion cell in primate retina: Morphology, mosaic organization and central targets of melanopsin immunostained cells. Investigative Ophthalmology and Visual Science 44, program no 5182, 2003.Google Scholar
Polyak, S.L. (1941). The Retina. Chicago, Illinois: University of Chicago Press.
Pu, M.L. & Amthor, F.R. (1990). Dendritic morphologies of retinal ganglion cells projecting to the nucleus of the optic tract in the rabbit. Journal of Comparative Neurology 302, 657–674.Google Scholar
Pu, M., Berson, D.M., & Pan, T. (1994). Structure and function of retinal ganglion cells innervating the cat's geniculate wing: An in vitro study. Journal of Neuroscience 14, 4338–4358.Google Scholar
Rockhill, R.L., Daly, F.J., MacNeil, M.A., Brown, S.P., & Masland, R.H. (2002). The diversity of ganglion cells in a mammalian retina. Journal of Neuroscience 22, 3831–3843.Google Scholar
Rodieck, R.W. (1988). The primate retina. In Comparative Primate Biology, ed. Steklis, H.D., pp. 203–278. New York: Alan R. Liss, Inc.
Rodieck, R.W. & Brening, R.K. (1983). Retinal ganglion cells: Properties, types, genera, pathways and trans-species comparisons. Brain, Behavior, and Evolution 23, 121–164.Google Scholar
Rodieck, R.W. & Marshak, D.W. (1992). Spatial density and distribution of choline acetyltransferase immunoreactive cells in human, macaque and baboon retinas. Journal of Comparative Neurology 321, 46–64.Google Scholar
Rodieck, R.W. & Watanabe, M. (1993). Survey of the morphology of macaque retinal ganglion cells that project to the pretectum, superior colliculus, and parvicellular laminae of the lateral geniculate nucleus. Journal of Comparative Neurology 338, 289–303.Google Scholar
Roska, B. & Werblin, F. (2001). Vertical interactions across ten parallel, stacked representations in the mammalian retina. Nature 410, 583–587.Google Scholar
Schiller, P.H. & Malpeli, J.G. (1977). Properties and tectal projections of monkey retinal ganglion cells. Journal of Neurophysiology 40, 428–445.Google Scholar
Sun, W., Li, N., & He, S. (2002). Large-scale morphological survey of mouse retinal ganglion cells. Journal of Comparative Neurology 451, 115–126.Google Scholar
Wässle, H., Voigt, T., & Patel, B. (1987). Morphological and immunocytochemical identification of indoleamine-accumulating neurons in the cat retina. Journal of Neuroscience 7, 1574–1585.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