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Neural architecture of the “transient” ON directionally selective (class IIb1) ganglion cells in rabbit retina, partly co-stratified with starburst amacrine cells

Published online by Cambridge University Press:  31 May 2016

EDWARD V. FAMIGLIETTI*
Affiliation:
Department of Molecular Pharmacology, Physiology, and Biotechnology, Brown University, and Division of Ophthalmology, Rhode Island Hospital Providence, RI 02903
*
*Address correspondence to: E. V. Famiglietti, M.D., Ph.D., P. O. Box 252, Narragansett, RI 02882. E-mail: [email protected]

Abstract

Recent physiological studies coupled with intracellular staining have subdivided ON directionally selective (DS) ganglion cells of rabbit retina into two types. One exhibits more “transient” and more “brisk” responses (ON DS-t), and the other has more “sustained’ and more “sluggish” responses (ON DS-s), although both represent the same three preferred directions and show preference for low stimulus velocity, as reported in previous studies of ON DS ganglion cells in rabbit retina. ON DS-s cells have the morphology of ganglion cells previously shown to project to the medial terminal nucleus (MTN) of the accessory optic system, and the MTN-projecting, class IVus1 cells have been well-characterized previously in terms of their dendritic morphology, branching pattern, and stratification. ON DS-t ganglion cells have a distinctly different morphology and exhibit heterotypic coupling to amacrine cells, including axon-bearing amacrine cells, with accompanying synchronous firing, while ON DS-s cells are not coupled. The present study shows that ON DS-t cells are morphologically identical to the previously well-characterized, “orphan” class IIb1 ganglion cell, previously regarded as a member of the “brisk-concentric” category of ganglion cells. Its branching pattern, quantitatively analyzed, is similar to that of the morphological counterparts of X and Y cells, and very different from that of the ON DS-s ganglion cell. Close analysis of the dendritic stratification of class IIb1 ganglion cells together with fiducial cells indicates that they differ from that of the ON DS-s cells. In agreement with one of the three previous studies, class IIb1/ON DS-t cells, unlike class IVus1/ON DS-s ganglion cells, in the main do not co-stratify with starburst amacrine cells. As the present study shows, however, portions of their dendrites do deviate from the main substratum, coming within range of starburst boutons. Parsimony favors DS input from starburst amacrine cells both to ON DS-s and to ON DS-t ganglion cells, given the similarity of their DS responses, but further studies will be required to substantiate the origin of the DS responses of ON DS-t cells. Previously reported OFF DS responses in ON DS-t cells, unmasked by pharmacological agents, and mediated by gap junctions with amacrine cells, suggests an unusual trans-sublaminar organization of directional selectivity in the inner plexiform layer, connecting sublamina a and sublamina b.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2016 

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References

Ackert, J.M., Farajian, R., Volgyi, B. & Bloomfield, S.A. (2009). GABA blockade unmasks an OFF response in ON direction selective ganglion cells in the mammalian retina. Journal of Physiology 587, 44814495.CrossRefGoogle Scholar
Ackert, J.M., Wu, S.H., Lee, J.C., Abrams, J., Hu, E.H., Perlman, I. & Bloomfield, S.A. (2006). Light-induced changes in spike synchronization between coupled ON direction selective ganglion cells in the mammalian retina. Journal of Neuroscience 26, 42064215.CrossRefGoogle ScholarPubMed
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, 7296.CrossRefGoogle ScholarPubMed
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, 97121.CrossRefGoogle ScholarPubMed
Anderson, J.R., Jones, B.W., Watt, C.B., Shaw, M.V., Yang, J.H., Demill, D., Lauritzen, J.S., Lin, Y., Rapp, K.D., Mastronarde, D., Koshevoy, P., Grimm, B., Tasdizen, T., Whitaker, R. & Marc, R.E. (2011). Exploring the retinal connectome. Molecular Vision 17, 355379.Google ScholarPubMed
Ariel, M. & Daw, N.W. (1982a). Effects of cholinergic drugs on receptive field properties of rabbit retinal ganglion cells. Journal of Physiology 324, 135160.CrossRefGoogle ScholarPubMed
Ariel, M. & Daw, N.W. (1982b). Pharmacological analysis of directionally sensitive rabbit retinal ganglion cells. Journal of Physiology 324, 161185.CrossRefGoogle ScholarPubMed
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 173, 377407.CrossRefGoogle ScholarPubMed
Barlow, H.B. & Levick, W.R. (1965). The mechanism of directionally selective units in rabbit's retina. Journal of Physiology 178, 477504.CrossRefGoogle ScholarPubMed
Bloomfield, S.A. & Xin, D. (1997). A comparison of receptive-field and tracer-coupling size of amacrine and ganglion cells in the rabbit retina. Visual Neuroscience 14, 11531165.CrossRefGoogle ScholarPubMed
Bloomfield, S.A., Xin, D. & Osborne, T. (1997). Light-induced modulation of coupling between AII amacrine cells in the rabbit retina. Visual Neuroscience 14, 565576.CrossRefGoogle ScholarPubMed
Brandon, C. (1987). Cholinergic neurons in the rabbit retina: Dendritic branching and ultrastructural connectivity. Brain Research 426, 119130.CrossRefGoogle ScholarPubMed
Brandon, C. & Criswell, M.H. (1995). Displaced starburst amacrine cells of the rabbit retina contain the 67 kDa isoform, but not the 65 kDa isoform, of glutamate decarboxylase. Visual Neuroscience 12, 10531061.CrossRefGoogle Scholar
Brecha, N., Johnson, D., Peichl, L. & Wässle, H. (1988). Cholinergic amacrine cells of the rabbit retina contain glutamate decarboxylase and gamma-aminobutyrate immunoreactivity. Proceedings of the National Academy of Sciences of the United States of America 85, 61876191.CrossRefGoogle ScholarPubMed
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, 163174.CrossRefGoogle Scholar
Caldwell, J.H. & Daw, N.W. (1978). New properties of rabbit retinal ganglion cells. Journal of Physiology 276, 257276.CrossRefGoogle ScholarPubMed
Cleland, B.G. & Levick, W.R. (1974). Properties of rarely encountered types of ganglion cells in the cat’s retina and an overall classification. Journal of Physiology 240, 457492.CrossRefGoogle Scholar
Cleveland, W.S. (1979). Robust locally weighted regression and smoothing scatterplots. Journal of the American Statistical Association 70, 548554.Google Scholar
Dacheux, R.F., Chimento, M.F. & Amthor, F.R. (2003). Synaptic input to the ON–OFF directionally selective ganglion cell in the rabbit retina. Journal of Comparative Neurology 456, 267278.CrossRefGoogle Scholar
Dhande, O.S., Estevez, M.E., Quattrochi, L.E., El-Danaf, R.N., Nguyen, P.L., Berson, D.M. & Huberman, A.D. (2013). Genetic dissection of retinal inputs to brainstem nuclei controlling image stabilization. Journal of Neuroscience 33, 1779717813.CrossRefGoogle ScholarPubMed
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, 1117.CrossRefGoogle ScholarPubMed
Dowling, J.E. & Werblin, F.S. (1969). Organization of retina of the mudpuppy, Necturus maculosus. I. Synaptic structure. Journal of Neurophysiology 32, 315338.CrossRefGoogle ScholarPubMed
Efron, B. & Tibshirani, R. (1991). Statistical data analysis in the computer age. Science 253, 390395.CrossRefGoogle ScholarPubMed
Euler, T., Detwiler, P.B. & Denk, W. (2002). Directionally selective calcium signals in dendrites of starburst amacrine cells. Nature 418, 845852.CrossRefGoogle ScholarPubMed
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, 15591563.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. (1983). ‘Starburst’ amacrine cells and cholinergic neurons: Mirror-symmetric on and off amacrine cells of rabbit retina. Brain Research 261, 138144.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. (1985). Starburst amacrine cells: Morphological constancy and systematic variation in the anisotropic field of rabbit retinal neurons. Journal of Neuroscience 5, 562577.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. (1987). Starburst amacrine cells in cat retina are associated with bistratified, presumed directionally selective, ganglion cells. Brain Research 413, 404408.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. (1990). Three categories of very wide-field amacrine cells in rabbit retina: Polyaxonal, HLPalpha, and HLPbeta amacrine cells. Investigative Ophthalmology and Visual Science 31, 37.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, 4070.CrossRefGoogle ScholarPubMed
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, 295321.CrossRefGoogle 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, 322335.CrossRefGoogle Scholar
Famiglietti, E.V. (1992c). Polyaxonal amacrine cells of rabbit retina: Morphology and stratification of Pa1 cells. Journal of Comparative Neurology 316, 391405.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. (1992d). Polyaxonal amacrine cells of rabbit retina: Size and distribution of Pa1 cells. Journal of Comparative Neurology 316, 406421.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. (1992e). Polyaxonal amacrine cells of rabbit retina: Pa2, Pa3, and Pa4 cells. Light and electron microscopic studies with a functional interpretation. Journal of Comparative Neurology 316, 422446.CrossRefGoogle ScholarPubMed
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, 145162.CrossRefGoogle ScholarPubMed
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, 323346.CrossRefGoogle 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, 347358.CrossRefGoogle Scholar
Famiglietti, E.V. (2005a). 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 485, 357391.CrossRefGoogle Scholar
Famiglietti, E.V. (2005b). “Small-tufted” ganglion cells and two visual systems for the detection of object motion in rabbit retina. Visual Neuroscience 22, 509534.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. (2008). Wide-field cone bipolar cells and the blue-ON pathway to color-coded ganglion cells in rabbit retina. Visual Neuroscience 25, 5366.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. (2009). Bistratified ganglion cells of rabbit retina: Neural architecture for contrast-independent visual responses. Visual Neuroscience 26, 195213.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. & Kolb, H. (1975). A bistratified amacrine cell and synaptic circuitry in the inner plexiform layer of the retina. Brain Research 84, 293300.CrossRefGoogle Scholar
Famiglietti, E.V. & Kolb, H. (1976). Structural basis for ON- and OFF-center responses in retinal ganglion cells. Science 194, 193195.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. & Sharpe, S.J. (1994). Development of ChAT and GAD immunoreactivity in relation to starburst amacrine cells of rabbit retina. Society for Neuroscience Abstracts 20, 729.Google Scholar
Famiglietti, E.V. & Sundquist, S.J. (2010). Development of excitatory and inhibitory neurotransmitters in transitory cholinergic neurons, starburst amacrine cells, and GABAergic amacrine cells of rabbit retina, with implications for previsual and visual development of retinal ganglion cells. Visual Neuroscience 27, 1942.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. & Tumosa, N. (1986). The organization of cholinergic neurons in rabbit retina. In Retinal Signal Systems, Degenerations and Transplants, ed. Agardh, E. & Ehinger, B., pp. 3746. Amsterdam: Elsevier.Google Scholar
Famiglietti, E.V. & Tumosa, N. (1987). Immunocytochemical staining of cholinergic amacrine cells in rabbit retina. Brain Research 413, 398403.CrossRefGoogle ScholarPubMed
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, 129139.CrossRefGoogle ScholarPubMed
Gauvain, G. & Murphy, G.J. (2015). Projection-specific characteristics of retinal input to the brain. Journal of Neuroscience 35, 65756583.CrossRefGoogle ScholarPubMed
Grzywacz, N.M., Tootle, J.S. & Amthor, F.R. (1997). Is the input to a GABAergic or cholinergic synapse the sole asymmetry in rabbit’s retinal directional selectivity? Visual Neuroscience 14, 3954.CrossRefGoogle ScholarPubMed
He, S., Jin, Z.F. & Masland, R.H. (1999). The nondiscriminating zone of directionally selective retinal ganglion cells: Comparison with dendritic structure and implications for mechanism. Journal of Neuroscience 19, 80498056.CrossRefGoogle ScholarPubMed
He, S. & Masland, R.H. (1998). ON direction-selective ganglion cells in the rabbit retina: Dendritic morphology and pattern of fasciculation. Visual Neuroscience 15, 369375.CrossRefGoogle ScholarPubMed
Hoshi, H., Tian, L.M., Massey, S.C. & Mills, S.L. (2011). Two distinct types of ON directionally selective ganglion cells in the rabbit retina. Journal of Comparative Neurology 519, 25092521.CrossRefGoogle Scholar
Huberman, A.D., Wei, W., Elstrott, J., Stafford, B.K., Feller, M.B. & Barres, B.A. (2009). Genetic identification of an On–Off direction-selective retinal ganglion cell subtype reveals a layer-specific subcortical map of posterior motion. Neuron 62, 327334.CrossRefGoogle ScholarPubMed
Jensen, R.J. (1991). Intracellular recording of light responses from visually identified ganglion cells in the rabbit retina. Journal of Neuroscience Methods 40, 101112.CrossRefGoogle ScholarPubMed
Johnson, C.D. & Epstein, M.L. (1986). Monoclonal antibodies and polyvalent antiserum to chicken choline acetyltransferase. Journal of Neurochemistry 46, 968976.CrossRefGoogle ScholarPubMed
Kanjhan, R. & Sivyer, B. (2010). Two types of ON direction-selective ganglion cells in rabbit retina. Neuroscience Letters 483, 105109.CrossRefGoogle Scholar
Kanjhan, R. & Vaney, D.I. (2008). Semi-loose seal neurobiotin electroporation for combined structural and functional analysis of neurons. Pflugers Archiv. European Journal of Physiology 457, 561568.CrossRefGoogle ScholarPubMed
Kay, J.N., De la Huerta, I., Kim, I.J., Zhang, Y., Yamagata, M., Chu, M.W., Meister, M. & Sanes, J.R. (2011). Retinal ganglion cells with distinct directional preferences differ in molecular identity, structure, and central projections. Journal of Neuroscience 31, 77537762.CrossRefGoogle ScholarPubMed
Kim, I.J., Zhang, Y., Yamagata, M., Meister, M. & Sanes, J.R. (2008). Molecular identification of a retinal cell type that responds to upward motion. Nature 452, 478482.CrossRefGoogle ScholarPubMed
Lee, S., Chen, L., Chen, M., Ye, M., Seal, R.P. & Zhou, Z.J. (2014). An unconventional glutamatergic circuit in the retina formed by vGluT3 amacrine cells. Neuron 84, 708715.CrossRefGoogle ScholarPubMed
Lee, S., Kim, K. & Zhou, Z.J. (2010). Role of ACh-GABA cotransmission in detecting image motion and motion direction. Neuron 68, 11591172.CrossRefGoogle ScholarPubMed
Lee, S. & Zhou, Z.J. (2006). The synaptic mechanism of direction selectivity in distal processes of starburst amacrine cells. Neuron 51, 787799.CrossRefGoogle ScholarPubMed
Levick, W. (1967). Receptive fields and trigger features of ganglion cells in the visual streak of the rabbit’s retina. Journal of Physiology 188, 285307.CrossRefGoogle Scholar
Levick, W.R., Oyster, C.W. & Takahashi, E. (1969). Rabbit lateral geniculate nucleus: Sharpener of directional information. Science 165, 712714.CrossRefGoogle ScholarPubMed
MacNeil, M.A. & Gaul, P.A. (2008). Biocytin wide-field bipolar cells in rabbit retina selectively contact blue cones. Journal of Comparative Neurology 506, 615.CrossRefGoogle ScholarPubMed
Mangel, S.C. & Dowling, J.E. (1985). Responsiveness and receptive field size of carp horizontal cells are reduced by prolonged darkness and dopamine. Science 229, 11071109.CrossRefGoogle ScholarPubMed
Marc, R.E. & Liu, W. (2000). Fundamental GABAergic amacrine cell circuitries in the retina: Nested feedback, concatenated inhibition, and axosomatic synapses. Journal of Comparative Neurology 425, 560582.3.0.CO;2-D>CrossRefGoogle ScholarPubMed
Marshak, D.W. & Mills, S.L. (2014). Short-wavelength cone-opponent retinal ganglion cells in mammals. Visual Neuroscience 31, 165175.CrossRefGoogle ScholarPubMed
Masland, R.H. & Ames, A. 3rd (1976). Responses to acetylcholine of ganglion cells in an isolated mammalian retina. Journal of Neurophysiology 39, 12201235.CrossRefGoogle Scholar
Masland, R.H. & Mills, J.W. (1979). Autoradiographic identification of acetylcholine in the rabbit retina. Journal of Cell Biology 83, 159178.CrossRefGoogle ScholarPubMed
Mills, S.L., Tian, L.M., Hoshi, H., Whitaker, C.M. & Massey, S.C. (2014). Three distinct blue-green color pathways in a mammalian retina. Journal of Neuroscience 34, 17601768.CrossRefGoogle Scholar
O’Malley, D.M. & Masland, R.H. (1989). Co-release of acetylcholine and gamma-aminobutyric acid by a retinal neuron. Proceedings of the National Academy of Sciences of the United States of America 86, 34143418.CrossRefGoogle ScholarPubMed
Oyster, C.W. (1968). The analysis of image motion by the rabbit retina. Journal of Physiology 199, 613635.CrossRefGoogle ScholarPubMed
Oyster, C.W., Amthor, F.R. & Takahashi, E.S. (1993). Dendritic architecture of ON–OFF direction-selective ganglion cells in the rabbit retina. Vision Research 33, 579608.CrossRefGoogle ScholarPubMed
Peichl, L., Ott, H. & Boycott, B.B. (1987). Alpha ganglion cells in mammalian retinae. Proceedings of the Royal Society of London. Series B: Biological Sciences 231, 169197.Google ScholarPubMed
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, 657674.CrossRefGoogle Scholar
Rivlin-Etzion, M., Zhou, K., Wei, W., Elstrott, J., Nguyen, P.L., Barres, B.A., Huberman, A.D. & Feller, M.B. (2011). Transgenic mice reveal unexpected diversity of ON–OFF direction-selective retinal ganglion cell subtypes and brain structures involved in motion processing. Journal of Neuroscience 31, 87608769.CrossRefGoogle ScholarPubMed
Rodieck, R.W. & Brening, R.K. (1983). Retinal ganglion cells: Properties, types, genera, pathways and trans-species comparisons. Brain, Behavior and Evolution 23, 121164.CrossRefGoogle ScholarPubMed
Roska, B. & Werblin, F. (2001). Vertical interactions across ten parallel, stacked representations in the mammalian retina. Nature 410, 583587.CrossRefGoogle ScholarPubMed
Rowe, M.H. & Stone, J. (1977). Naming of neurones. Classification and naming of cat retinal ganglion cells. Brain, Behavior and Evolution 14, 185216.CrossRefGoogle ScholarPubMed
Sanes, J.R. & Masland, R.H. (2015). The types of retinal ganglion cells: Current status and implications for neuronal classification. Annual Review of Neuroscience 38, 221246.CrossRefGoogle ScholarPubMed
Schneider, C.A., Rasband, W.S. & Eliceiri, K.W. (2012). NIH image to ImageJ: 25 years of image analysis. Nat Methods 9, 671675.CrossRefGoogle ScholarPubMed
Simpson, J.I. (1984). The accessory optic system. Annual Review of Neuroscience 7, 1341.CrossRefGoogle ScholarPubMed
Simpson, J.I., Leonard, C.S. & Soodak, R.E. (1988). The accessory optic system. Analyzer of self-motion. Annals of the New York Academy of Sciences 545, 170179.CrossRefGoogle ScholarPubMed
Sivyer, B., van Wyk, M., Vaney, D.I. & Taylor, W.R. (2010). Synaptic inputs and timing underlying the velocity tuning of direction-selective ganglion cells in rabbit retina. Journal of Physiology 588, 32433253.CrossRefGoogle ScholarPubMed
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, 722748.CrossRefGoogle ScholarPubMed
Sun, W., Deng, Q., Levick, W.R. & He, S. (2006). ON direction-selective ganglion cells in the mouse retina. Journal of Physiology 576, 197202.CrossRefGoogle ScholarPubMed
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, 101119.Google ScholarPubMed
Trenholm, S., Johnson, K., Li, X., Smith, R.G. & Awatramani, G.B. (2011). Parallel mechanisms encode direction in the retina. Neuron 71, 683694.CrossRefGoogle ScholarPubMed
Tumosa, N., Stell, W.K., Johnson, C.D. & Epstein, M.L. (1986). Putative cholinergic interneurons in the optic tectum of goldfish. Brain Research 370, 365369.CrossRefGoogle ScholarPubMed
Vaney, D.I. (1990). The mosaic of amacrine cells in the mammalian retina. In Progress in Retinal Research, Vol. 9. ed. Osborne, N. & Chader, J., pp. 49100. Oxford: Pergamon Press.Google Scholar
Vaney, D.I., He, S., Taylor, W.R. & Levick, W.R. (2001). Direction-selective ganglion cells in the retina. In Motion Vision—Computational, Neural, and Ecological Constraints. ed. Zanker, J.M. & Zeil, J., pp. 1356. Springer: Berlin.Google Scholar
Vaney, D.I., Peichl, L., Wässle, H. & Illing, R. B. (1981). Almost all ganglion cells in the rabbit retina project to the superior colliculus. Brain Research 212, 447453.CrossRefGoogle Scholar
Vaney, D.I. & Young, H.M. (1988). GABA-like immunoreactivity in cholinergic amacrine cells of the rabbit retina. Brain Research 438, 369373.CrossRefGoogle ScholarPubMed
Volgyi, B., Xin, D., Amarillo, Y. & Bloomfield, S.A. (2001). Morphology and physiology of the polyaxonal amacrine cells in the rabbit retina. Journal of Comparative Neurology 440, 109125.CrossRefGoogle ScholarPubMed
Weng, S., Sun, W. & He, S. (2005). Identification of ON–OFF direction-selective ganglion cells in the mouse retina. Journal of Physiology 562, 915923.CrossRefGoogle ScholarPubMed
Werblin, F.S. (2010). Six different roles for crossover inhibition in the retina: Correcting the nonlinearities of synaptic transmission. Visual Neuroscience 27, 18.CrossRefGoogle ScholarPubMed
Wyatt, H.J. & Daw, N.W. (1976). Specific effects of neurotransmitter antagonists on ganglion cells in rabbit retina. Science 191, 204205.CrossRefGoogle ScholarPubMed
Yonehara, K., Ishikane, H., Sakuta, H., Shintani, T., Nakamura-Yonehara, K., Kamiji, N.L., Usui, S. & Noda, M. (2009). Identification of retinal ganglion cells and their projections involved in central transmission of information about upward and downward image motion. PLoS One 4, e4320.CrossRefGoogle ScholarPubMed
Yoshida, K., Watanabe, D., Ishikane, H., Tachibana, M., Pastan, I. & Nakanishi, S. (2001). A key role of starburst amacrine cells in originating retinal directional selectivity and optokinetic eye movement. Neuron 30, 771780.CrossRefGoogle ScholarPubMed