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“Small-tufted” ganglion cells and two visual systems for the detection of object motion in rabbit retina

Published online by Cambridge University Press:  06 October 2005

E.V. FAMIGLIETTI
E.V. FAMIGLIETTI
Affiliation:
Department of Surgery (Ophthalmology), Brown University, Providence
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Abstract

Small-tufted (ST) ganglion cells of rabbit retina are divided into eight types based upon morphology, branching pattern, level of dendritic stratification, and quantitative dimensional analysis. Only one of these types has been previously characterized in Golgi preparations, and four may be discerned in the work of others. Given their small dendritic-field size, and assuming uniform mosaics of each across the retina, ST cells comprise about 45% of all rabbit ganglion cells, and are therefore of major functional significance. Four ST cells occur as two paramorphic (a/b) pairs, and thus belong to class III, as previously defined. Four branch in sublaminae a and b of the inner plexiform layer (IPL) and therefore belong to class IV. ST cells have small cell bodies 10–15 μm in diameter, small axons 0.7–1.3 μm in diameter, and small dendritic-field diameters, 40–110 μm in mid-visual streak. The dendrites of ST cells are highly branched, and bear spines and appendages of varying length, but vary from type to type. Class III.2 cells and class III.3 cells are partly bistratified. Class IV small-tufted cells differ characteristically in multiple features of dendritic branching and stratification. Class III small-tufted cells apparently have concentric (ON-center and OFF-center) receptive fields and may have “sluggish-transient” (class III.2) and “sluggish-sustained” (class III.3) physiology. Class IV cells include the “local-edge-detector” (LED) (class IVst1), and are all expected to give ON–OFF responses to small, centered, slowly moving visual stimuli. Based upon systematic variation in dendritic-field size across the retina, ST cells may be divided into two groups. In this “universal prey” species, they may belong to two systems of motion detection, typified by ON–OFF directionally selective and LED ganglion cells, respectively, specialized for detection of rapid motion at the horizon for land-based predators, and slow motion for airborne predators.

Keywords

Local-edge-detectorSluggish concentric cellDendritic spinesVisual acuitymovement detection
Type
Research Article
Information
Visual Neuroscience , Volume 22 , Issue 4 , July 2005 , pp. 509 - 534
Copyright
2005 Cambridge University Press

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References

REFERENCES

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.Google Scholar
Amthor, F.R., Takahashi, E.S., & Oyster, C.W. (1989a). Morphologies of rabbit retinal ganglion cells with concentric receptive fields. Journal of Comparative Neurology 280, 72–96.Google Scholar
Amthor, F.R., Takahashi, E.S., & Oyster, C.W. (1989b). Morphologies of rabbit retinal ganglion cells with complex receptive fields. Journal of Comparative Neurology 280, 97–121.Google Scholar
Badea, T.C. & Nathans, J. (2004). Quantitative analysis of neuronal morphologies in the mouse retina visualized by using a genetically directed reporter. Journal of Comparative Neurology 480, 331–351.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
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 (London) 240, 397–419.Google Scholar
Cajal, S.R.y. (1893). La rétine des vertébrés. La Cellule 9, 17–257.Google Scholar
Caldwell, J.H. & Daw, N.W. (1978a). New properties of rabbit retinal ganglion cells. Journal of Physiology (London) 276, 257–276.Google Scholar
Caldwell, J.H. & Daw, N.W. (1978b). Effects of picrotoxin and strychnine on rabbit retinal ganglion cells: Changes in centre surround receptive fields. Journal of Physiology (London) 276, 299–310.Google Scholar
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
Cleland, B.G. & Levick, W.R. (1974a). Brisk and sluggish concentrically organized ganglion cells in the cat's retina. Journal of Physiology (London) 240, 421–456.Google Scholar
Cleland, B.G. & Levick, W.R. (1974b). Properties of rarely encountered types of ganglion cells in the cat's retina and an overall classification. Journal of Physiology (London) 240, 457–492.Google Scholar
Cleveland, W.S. (1979). Robust locally weighted regression and smoothing scatterplots. Journal of the American Statistical Association 70, 548–554.Google Scholar
Dacey, D.M. (1985). Wide-spreading terminal axons in the inner plexiform layer of the cat's retina: Evidence for intrinsic axon collaterals of ganglion cells. Journal of Comparative Neurology 242, 247–262.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
Efron, B. & Tibshirani, R. (1991). Statistical data analysis in the computer age. Science 253, 390–395.Google Scholar
Famiglietti, E.V. (1981a). Starburst amacrines: 2 mirror-symmetrical retinal networks. Investigative Ophthalmology and Visual Science 20, S204.Google Scholar
Famiglietti, E.V. (1981b). Functional architecture of cone bipolar cells in mammalian retina. Vision Research 21, 1559–1563.Google Scholar
Famiglietti, E.V. (1983). 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). 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. (1987a). 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. (1987b). Morphological classification of ganglion cells in rabbit retina. Society 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. (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. (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. (2004a). 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. (2004b). 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). 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. & 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. (1978). The ganglion cells of rabbit retina. Society for Neuroscience Abstracts 4, 627.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
Feng, G., Mellor, R.H., Bernstein, M., Keller-Peck, C., Nguyen, Q.T., Wallace, M., Nerbonne, J.M., Lichtman, J.W., & Sanes, J.R. (2000). Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28, 41–51.Google Scholar
Fukuda, Y. & Stone, J. (1974). Retinal distribution and central projections of Y-, X-, and W-cells of the cat's retina. Journal of Neurophysiology 37, 749–772.Google Scholar
Gan, W.B., Grutzendler, J., Wong, W.T., Wong, R.O., & Lichtman, J.W. (2000). Multicolor “DiOlistic” labeling of the nervous system using lipophilic dye combinations. Neuron 27, 219–225.Google Scholar
Hughes, A. (1977). The topography of vision in mammals of contrasting life style: Comparative optics and retinal organisation. In Handbook of Sensory Physiology Vol. vii/5, ed. Crescitelli, F., pp. 613–756. Berlin: Springer-Verlag.
Huxlin, K.R. & Goodchild, A.K. (1997). Retinal ganglion cells in the albino rat: Revised morphological classification. Journal of Comparative Neurology 385, 309–323.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, Massachusetts: MIT Press and John Wiley.
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
MacNeil, M.A. & Masland, R.H. (1998). Extreme diversity among amacrine cells: Implications for function. Neuron 20, 971–982.Google Scholar
Marc, R.E. & Jones, B.W. (2002). Molecular phenotyping of retinal ganglion cells. Journal of Neuroscience 22, 413–427.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
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. & Brening, R.K. (1983). Retinal ganglion cells: Properties, types, genera, pathways and transspecies comparisons. Brain Behavior and Evolution 23, 121–164.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
Saito, H.A. (1983). Morphology of physiologically identified X-, Y-, and W-type retinal ganglion cells of the cat. Journal of Comparative Neurology 221, 279–288.Google Scholar
Stone, J. & Fukuda, Y. (1974). Properties of cat retinal ganglion cells: A comparison of W-cells with X- and Y-cells. Journal of Neurophysiology 37, 722–748.Google Scholar
Sun, W., Li, N., & He, S. (2002a). Large-scale morphological survey of mouse retinal ganglion cells. Journal of Comparative Neurology 451, 115–126.Google Scholar
Sun, W., Li, N., & He, S. (2002b). Large-scale morophological survey of rat retinal ganglion cells. Visual Neuroscience 19, 483–493.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
Watanabe, M. & Rodieck, R.W. (1989). Parasol and midget ganglion cells of the primate retina. Journal of Comparative Neurology 289, 434–454.Google Scholar
West, R.W. (1976). Light and electron microscopy of the ground squirrel retina: Functional considerations. Journal of Comparative Neurology 168, 355–377.Google Scholar
Yang, G. & Masland, R.H. (1992). Direct visualization of the dendritic and receptive fields of directionally selective retinal ganglion cells. Science 258, 1949–1952.Google Scholar