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Bistratified ganglion cells of rabbit retina: Neural architecture for contrast-independent visual responses

Published online by Cambridge University Press:  01 March 2009

EDWARD V. FAMIGLIETTI
EDWARD V. FAMIGLIETTI*
Affiliation:
Department of Surgery (Ophthalmology), Brown University School of Medicine, Providence, Rhode Island
*
*Address correspondence and reprint requests to: Edward V. Famiglietti, 235 Angell Street, Providence, RI 02903. E-mail: edward_famiglietti@brown.edu
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Abstract

Bistratified (BS) ganglion cells have long been recognized in vertebrate retina. Thirty years ago, it became clear that bistratification allows the integration of ON and OFF retinal pathways to produce contrast-independent responses in ganglion cells. Best studied is the type 1 bistratified (BS1) ganglion cell of rabbit retina, the physiologically well-characterized ON-OFF directionally selective (DS) ganglion cell, which is co-stratified with the two types of starburst amacrine (SA) cells in sublaminae a and b of the inner plexiform layer (IPL). DS responses have recently been documented in the latter. In this report, BS1 cells are further studied and are used as “fiducials” to characterize a second type of BS ganglion cell. An example of a possible third type is shown to be distinct from examples of BS1 and BS2 cells. All three have two distinct, narrowly stratified arborizations, one in sublamina a and one in sublamina b. All have similar dimensions, except for their dendritic trees, differing also in branching pattern. BS1 cells have compact, regular, highly branched trees; BS2 cells have significantly larger, more sparsely branched, irregular, radiate trees; the proposed BS3 type is intermediate in field size, and its branching pattern is different from the first two. BS2 and BS3 cells are co-stratified, branching nearer to the margins of the IPL, out of range of SA cells. In a previous report by others, illustrating the morphology of intracellularly stained ganglion cells, one example each of both “orientation-selective” ganglion cells and “uniformity detectors” resembles the BS2 cell. A rationale is presented for correlating BS2 cells with uniformity detectors.

Keywords

Directional selectivityOrientation selectivityUniformity detectorON and OFF pathways
Type
Research Articles
Information
Visual Neuroscience , Volume 26 , Issue 2 , March 2009 , pp. 195 - 213
Copyright
Copyright © Cambridge University Press 2009

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References

Amthor, F.R. & Oyster, C.W. (1995). Spatial organization of retinal information about the direction of image motion. Proceedings of the National Academy of Sciences of the United States of America 92, 4002–4005.CrossRefGoogle ScholarPubMed
Amthor, F.R., Oyster, C.W. & Takahashi, E.S. (1984). Morphology of on-off direction-selective ganglion cells in the rabbit retina. Brain Research 298, 187–190.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Ariel, M. & Daw, N.W. (1982). Pharmacological analysis of directionally sensitive rabbit retinal ganglion cells. Journal of Physiology (London) 324, 161–185.Google Scholar
Barlow, H.B., Hill, R.M. & Levick, W.R. (1964). Retinal ganglion cells responding selectively to direction and speed of image motion in the rabbit. Journal of Physiology (London) 173, 377–407.Google Scholar
Bloomfield, S.A. (1994). Orientation-sensitive amacrine and ganglion cells in the rabbit retina. Journal of Neurophysiology 71, 1672–1691.Google Scholar
Boycott, B.B. & Dowling, J.E. (1969). Organization of the primate retina: Light microscopy. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 255, 109–184.Google Scholar
Buhl, E.H. & Peichl, L. (1986). Morphology of rabbit retinal ganglion cells projecting to the medial terminal nucleus of the accessory optic system. Journal of Comparative Neurology 253, 163–174.CrossRefGoogle Scholar
Cajal, S.R.Y. (1893). La rétine des vertébrés. La Cellule 9, 17–257.Google Scholar
Caldwell, J.H. & Daw, N.W. (1978). New properties of rabbit retinal ganglion cells. Journal of Physiology (London) 276, 257–276.CrossRefGoogle ScholarPubMed
Caldwell, J.H., Daw, N.W. & Wyatt, H.J. (1978). Effects of picrotoxin and strychnine on rabbit retinal ganglion cells: lateral interactions for cells with more complex receptive fields. Journal of Physiology (London) 276, 277–298.Google Scholar
Cleveland, W.S. (1979). Robust locally weighted regression and smoothing scatterplots. Journal of the American Statistical Association 70, 548–554.Google Scholar
Efron, B. & Tibshirani, R. (1991). Statistical data analysis in the computer age. Science 253, 390–395.Google Scholar
Euler, T., Detwiler, P.B. & Denk, W. (2002). Directionally selective calcium signals in dendrites of starburst amacrine cells. Nature 418, 845–852.Google Scholar
Famiglietti, E.V. (1981 a). Starburst amacrines: 2 mirror-symmetrical retinal networks. Investigative Ophthalmology and Visual Science 20, S204.Google Scholar
Famiglietti, E.V. (1981 b). Functional architecture of cone bipolar cells in mammalian retina. Vision Research 21, 1559–1563.Google Scholar
Famiglietti, E.V. (1983 a). ‘Starburst’ amacrine cells and cholinergic neurons: Mirror-symmetric on and off amacrine cells of rabbit retina. Brain Research 261, 138–144.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. (1983 b). On and off pathways through amacrine cells in mammalian retina: The synaptic connections of “starburst” amacrine cells. Vision Research 23, 1265–1279.Google Scholar
Famiglietti, E.V. (1985 a). Starburst amacrine cells: Morphological constancy and systematic variation in the anisotropic field of rabbit retinal neurons. Journal of Neuroscience 5, 562–577.Google Scholar
Famiglietti, E.V. (1985 b). Synaptic organization of ON-OFF directionally selective ganglion cells in rabbit retina. Society for Neuroscience Abstracts 11, 337.Google Scholar
Famiglietti, E.V. (1987 a). Starburst amacrine cells in cat retina are associated with bistratified, presumed directionally selective, ganglion cells. Brain Research 413, 404–408.Google Scholar
Famiglietti, E.V. (1987 b). Morphological classification of ganglion cells in rabbit retina. Society for Neuroscience Abstracts 13, 380.Google Scholar
Famiglietti, E.V. (1990). A distinct type of displaced ganglion cell in a mammalian retina. Brain Research 535, 169–173.Google Scholar
Famiglietti, E.V. (1991). Synaptic organization of starburst amacrine cells in rabbit retina: Analysis of serial thin sections by electron microscopy and graphic reconstruction. Journal of Comparative Neurology 309, 40–70.Google Scholar
Famiglietti, E.V. (1992 a). 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. (1992 b). 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.CrossRefGoogle Scholar
Famiglietti, E.V. (1993). A ‘bilayer’ model of directional selectivity in rabbit retina. Investigative Ophthalmology and Visual Science 34, S985.Google Scholar
Famiglietti, E.V. (2002). A structural basis for omnidirectional connections between starburst amacrine cells and directionally selective ganglion cells in rabbit retina, with associated bipolar cells. Visual Neuroscience 19, 145–162.Google Scholar
Famiglietti, E.V. (2004 a). 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
Famiglietti, E.V. (2004 b). Class I and class II ganglion cells of rabbit retina: Quantitative analysis of dendritic branching patterns. Journal of Comparative Neurology 478, 347–358.Google Scholar
Famiglietti, E.V. (2005 a). Synaptic organization of “complex” ganglion cells in rabbit retina: Type and arrangement of inputs to directionally selective and local-edge-detector cells. Journal of Comparative Neurology 484, 357–391.Google Scholar
Famiglietti, E.V. (2005 b). “Small-tufted” ganglion cells and two visual systems for the detection of object motion in rabbit retina. Visual Neuroscience 22, 509–534.Google Scholar
Famiglietti, E.V., Kaneko, A. & Tachibana, M. (1977). Neuronal architecture of on and off pathways to ganglion cells in carp retina. Science 198, 1267–1269.Google Scholar
Famiglietti, E.V. & Kolb, H. (1976). Structural basis for ON- and OFF-center responses in retinal ganglion cells. Science 194, 193–195.Google Scholar
Famiglietti, E.V. & Siegfried, E.C. (1979). Quantitative analysis of ganglion cells in rabbit retina. Investigative Ophthalmology and Visual Science 18, S84.Google Scholar
Famiglietti, E.V. & Vaughn, J.E. (1981). Golgi-impregnated amacrine cells and GABAergic retinal neurons: A comparison of dendritic, immunocytochemical and histochemical stratification in the inner plexiform layer of rat retina. Journal of Comparative Neurology 197, 129–139.Google Scholar
Hubel, D.H. & Wiesel, T.N. (1962). Receptive fields, binocular interaction and functional architecture in the cat’s visual cortex. Journal of Physiology (London) 160, 106–154.Google Scholar
Lettvin, J.Y., Maturana, H.R., Pitts, W.H. & McCulloch, W.S. (1961). Two remarks on the visual system of the frog. In Sensory Communication. Contributions to the Symposium on Principles of Sensory Communication, ed. Rosenblith, W.A., pp. 757–776. Cambridge, MA: MIT Press and John Wiley.Google Scholar
Levick, W. (1967). Receptive fields and trigger features of ganglion cells in the visual streak of the rabbit's retina. Journal of Physiology (London) 188, 285–307.Google Scholar
Masland, R.H. & Ames, A. III. (1976). Responses to acetylcholine of ganglion cells in an isolated mammalian retina. Journal of Neurophysiology 39, 1220–1235.Google Scholar
Masland, R.H. & Mills, J.W. (1979). Autoradiographic identification of acetylcholine in the rabbit retina. The Journal of Cell Biology 83, 159–178.Google Scholar
Masland, R.H., Mills, J.W. & Hayden, S.A. (1984). Acetylcholine-synthesizing amacrine cells: Identification and selective staining by using radioautography and fluorescent markers. Proceedings of the Royal Society of London. Series B, Biological Sciences 223, 79–100.Google Scholar
Miller, R.F. & Bloomfield, S.A. (1983). Electroanatomy of a unique amacrine cell in the rabbit retina. Proceedings of the National Academy Sciences of the United States of America 80, 3069–3073.Google Scholar
Nelson, R., Famiglietti, E.V. Jr & Kolb, H. (1978). Intracellular staining reveals different levels of stratification for on- and off-center ganglion cells in cat retina. Journal of Neurophysiology 41, 472–483.Google Scholar
Oyster, C.W. (1968). The analysis of image motion by the rabbit retina. Journal of Physiology (London) 199, 613–635.Google Scholar
Oyster, C.W., Takahashi, E.S., Fry, K.R. & Lam, D.M. (1987). Ganglion cell density in albino and pigmented rabbit retinas labeled with a ganglion cell-specific monoclonal antibody. Brain Research 425, 25–33.Google Scholar
Oyster, C.W., Takahashi, E.S. & Hurst, D.C. (1981). Density, soma size, and regional distribution of rabbit retinal ganglion cells. Journal of Neuroscience 1, 1331–1346.Google Scholar
Perry, V.H. & Linden, R. (1982). Evidence for dendritic competition in the developing retina. Nature 297, 683–685.Google Scholar
Polyak, S.L. (1941). The Retina. Chicago, IL: University of Chicago Press.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
Roska, B. & Werblin, F. (2001). Vertical interactions across ten parallel, stacked representations in the mammalian retina. Nature 410, 583–587.Google Scholar
Tartuferi, F. (1887). Sull'anatomia della retina. Internationale Monatsschrift für Anatomie und Physiologie 4, 421–441.Google Scholar
Tauchi, M. & Masland, R.H. (1984). The shape and arrangement of the cholinergic neurons in the rabbit retina. Proceedings of the Royal Society of London. Series B, Biological Sciences 223, 101–119.Google Scholar
Taylor, W.R. & Vaney, D.I. (2002). Diverse synaptic mechanisms generate directional selectivity in rabbit retina. Journal of Neuroscience 22, 7712–7720.Google Scholar
van Wyk, M., Taylor, W.R. & Vaney, D.I. (2006). Local edge detectors: A substrate for fine spatial vision at low temporal frequencies in rabbit retina. Journal of Neuroscience 26, 13250–13263.Google Scholar
Vaney, D.I. (1994). Territorial organization of direction-selective ganglion cells in rabbit retina. Journal of Neuroscience 14, 6301–6316.Google Scholar
Vaney, D.I., Levick, W.R. & Thibos, L.N. (1981). Rabbit retinal ganglion cells. Receptive field classification and axonal conduction properties. Experimental Brain Research 44, 27–33.Google Scholar
Weber, A.J., McCall, M.A. & Stanford, L.R. (1991). Synaptic inputs to physiologically identified retinal X-cells in the cat. Journal of Comparative Neurology 314, 350–366.Google Scholar
Yang, G. & Masland, R.H. (1994). Receptive fields and dendritic structure of directionally selective retinal ganglion cells. Journal of Neuroscience 14, 5267–5280.Google Scholar