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The DAPI-3 amacrine cells of the rabbit retina

  • Layne L. Wright, Colin L. Macqueen, Guy N. Elston, Heather M. Young, David V. Pow and David I. Vaney (a1)...

Abstract

In the rabbit retina, the nuclear dye, 4,6, diarnidino-2-phenylindole (DAPI), selectively labels a third type of amacrine cell, in addition to the previously characterized type a and type b cholinergic amacrine cells. In this study, these “DAPI-3” amacrine cells have been characterized with respect to their somatic distribution, dendritic morphology, and neurotransmitter content by combining intracellular injection of biotinylated tracers with wholemount immunocytochemistry. There are about 100,000 DAPI-3 amacrine cells in total, accounting for 2% of all amacrine cells in the rabbit retina, and their cell density ranges from about 130 cells/mm2 in far-peripheral retina to 770 cells/mm2 in the visual streak. The thin varicose dendrites of the DAPI-3 amacrine cells form a convoluted dendritic tree that is symmetrically bistratified in S1/S2 and S4 of the inner plexiform layer. Tracer coupling shows that the DAPI-3 amacrine cells have a fivefold dendritic-field overlap in each sublamina, with the gaps in the arborization of each cell being occupied by dendrites from neighboring cells. The DAPI-3 amacrine cells consistently show the strongest glycine immunoreactivity in the rabbit retina and they also accumulate exogenous [3H]-glycine to a high level. By contrast, the All amacrine cells, which are the best characterized glycinergic cells in the retina, are amongst the most weakly labelled of the glycine-immunopositive amacrine cells. The DAPI-3 amacrine cells costratify narrowly with the cholinergic amacrine cells and the On-Off direction-selective ganglion cells, suggesting that they may play an important role in movement detection.

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Amthor, F.R., Oyster, C.W. & Takahashi, E.S. (1983). Quantitative morphology of rabbit retinal ganglion cells. Proceedings of the Royal Society B (London), 217, 341355.
Amthor, F.R., Takahashi, E.S. & Oyster, C.W. (1984). Morphology of on-off direction-selective ganglion cells in the rabbit retina. Brain Research 298, 187190.
Bloomfield, S.A. (1992). Relationship between receptive and dendritic field size of amacrine cells in the rabbit retina. Journal of Neurophysiology 68, 711725.
Bolz, J., Thier, P., Voigt, T. & Wässle, H. (1985). Action and localization of glycine and taurine in the cat retina. Journal of Physiology 362, 395413.
Brandon, C. (1987). Cholinergic neurons in the rabbit retina: Dendritic branching and ultrastructural connectivity. Brain Research 426, 119130.
Brecha, N., Johnson, D., Peichl, L. & Wässle, H. (1988). Cholinergic amacrine cells of the rabbit retina contain glutamate decarboxylase and γ-aminobutyrate immunoreactivity. Proceedings of the National Academy of Sciences of the U.S.A. 85, 61876191.
Cajal, S.R. (1933). Die Retina der Wirbeltiere. Wiesbaden: Bergman.
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 276, 277298.
Crooks, J. & Kolb, H. (1992). Localization of GABA, glycine, glutamate and tyrosine hydroxylase in the human retina. Journal of Comparative Neurology 315, 287302.
Cunningham, J.R. & Neal, M.J. (1983). Effect of γ-aminobutyric acid agonists, glycine, taurine and neuropeptides on acetylcholine release from the rabbit retina. Journal of Physiology 336, 563577.
Cunningham, J.R., Dawson, C. & Neal, M.J. (1983). Evidence for a cholinergic feedback mechanism in the rabbit retina. Journal of Physiology 340, 455468.
Ehinger, B. & Zucker, C.L. (1996). Prominent GABA-A receptors characterize a distinctive cell type in rabbit retina, DAPI-3. Investigative Ophthalmology and Visual Science 37, S138.
Famiglietti, E.V. (1983). ‘Starburst’ amacrine cells and cholinergic neurons: Mirror-symmetric ON and OFF amacrine cells of rabbit retina. Brain Research 261, 138144.
Famiglietti, E.V. (1987). Starburst amacrine cells in cat retina are associated with bistratified, presumed directionally selective, ganglion cells. Brain Research 413, 404408.
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.
Famiglietti, E.V. (1992). 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.
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.
Famiglietti, E.V. & Tumosa, N. (1987). Immunocytochemical staining of cholinergic amacrine cells in rabbit retina. Brain Research 413, 398403.
Hampson, E.C.G.M., Vaney, D.I. & Weiler, R. (1992). Dopaminergic modulation of gap junction permeability between amacrine cells in mammalian retina. Journal of Neuroscience 12, 49114922.
Hendrickson, A.E., Koontz, M.A., Pourcho, R.G., Sarthy, P.V. & Goebel, D.J. (1988). Localization of glycine-containing neurons in the Macaca monkey retina. Journal of Comparative Neurology 273, 473487.
Hughes, A. (1985). New perspectives in retinal organization. Progress in Retinal Research 4, 243313.
Ikeda, H. & Sheardown, M.J. (1983). Transmitters mediating inhibition of ganglion cells in the cat retina: Iontophoretic studies in vivo. Neuroscience 8, 837853.
Kittila, C.A. & Massey, S.C. (1995). Effect of ON pathway blockade on directional selectivity in the rabbit retina. Journal of Neurophysiology 73, 703712.
Kolb, H. & Famiglietti, E.V. (1974). Rod and cone pathways in the inner plexiform layer of cat retina. Science 186, 4749.
Kolb, H., Nelson, R. & Mariani, A. (1981). Amacrine cells, bipolar cells and ganglion cells of the cat retina: A Golgi study. Vision Research 21, 10811114.
Kolb, H., Linberg, K.A. & Fisher, S.K. (1992). Neurons of the human retina: A Golgi study. Journal of Comparative Neurology 318, 147187.
Koontz, M.A., Hendrickson, L.E., Brace, S.T. & Hendrickson, A.E. (1993). Immunocytochemical localization of GABA and glycine in amacrine and displaced amacrine cells of macaque monkey retina. Vision Research 18, 26172628.
Kosaka, T., Tauchi, M. & Dahl, J.L. (1988). Cholinergic neurons contain GABA-like and/or glutamic acid decarboxylase-like immunoreactivities in various brain regions of the rat. Experimental Brain Research 70, 605617.
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, 173216.
Maranto, A.R. (1982). Neuronal mapping: a photooxidation reaction makes Lucifer yellow useful for electron microscopy. Science 217, 953955.
Marc, R.E. (1989). The role of glycine in the mammalian retina. Progress in Retinal Research 8, 67107.
Marc, R.E. & Liu, W.-L.S. (1985). (3H)glycine-accumulating neurons of the human retina. Journal of Comparative Neurology 232, 241260.
Marc, R.E., Liu, W.-L.S., Kalloniatis, M., Raiguel, S.F. & Van Haesendonck, E. (1990). Patterns of glutamate immunoreactivity in the goldfish retina. Journal of Neuroscience 10, 40064034.
Marc, R.E., Murry, R.F., Fisher, S.K., Lewis, G.P. & Linberg, K.A. (1995 a). The cellular amino acid signatures of the cat retina: Transitions from normal to pathological states following retinal detachment. Investigative Ophthalmology and Visual Science 36, S383.
Marc, R.E., Murry, R.F. & Basinger, S.F. (1995 b). Pattern recognition of amino acid signatures in retinal neurons. Journal of Neuroscience 15, 51065129.
Mariani, A.P. (1990). Amacrine cells of the rhesus monkey retina. Journal of Comparative Neurology 301, 382400.
Mariani, A.P. & Hersh, L.B. (1988). Synaptic organization of cholinergic amacrine cells in the rhesus monkey retina. Journal of Comparative Neurology 267, 269280.
Masland, R.H. & Tauchi, M. (1986). The cholinergic amacrine cell. Trends in Neurosciences 9, 218223.
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 B (London) 223, 79100.
Massey, S.C. (1990). Cell types using glutamate as a neurotransmitter in the vertebrate retina. Progress in Retinal Research 9, 399425.
Massey, S.C., Redburn, D.A. & Crawford, M.L.J. (1983). The effects of 2-amino-4-phosphonobutyric acid (APB) on the ERG and ganglion cell discharge of rabbit retina. Vision Research 23, 16071613.
Millar, T.J. & Morgan, I.G. (1987). Cholinergic amacrine cells in the rabbit retina synapse onto other cholinergic amacrine cells. Neuroscience Letters 74, 281285.
Mills, S.L. & Massey, S.C. (1991). Labeling and distribution of AII amacrine cells in the rabbit retina. Journal of Comparative Neurology 304, 491501.
Müller, F., Wässle, H. & Voigt, T. (1988). Pharmacological modulation of the rod pathway in the cat retina. Journal of Neurophysiology 59, 16571672.
Neal, M.J. & Cunningham, J.R. (1995). Baclofen enhancement of acetylcholine release from amacrine cells in the rabbit retina by reduction of glycinergic inhibition. Journal of Physiology 482, 363372.
Neal, M.J., Cunningham, J.R., James, T.A., Joseph, M. & Collins, J.F. (1981). The effect of 2-amino-4-phosphonobutyrate (APB) on acetylcholine release from the rabbit retina: Evidence for ON-channel input to cholinergic amacrine cells. Neuroscience Letters 26, 301305.
Neal, M.J., Cunningham, J.R., Hutson, P. & Semark, J.E. (1992). Calcium dependent release of acetylcholine and γ-aminobutyric acid from the rabbit retina. Neurochemistry International 20, 4353.
O'Malley, D.M. & Masland, R.H. (1989). Co-release of acetylcholine and γ-aminobutyric acid by a retinal neuron. Proceedings of the National Academy of Sciences of the U.S.A. 86, 34143418.
O'Malley, D.M., Sandell, J.H. & Masland, R.H. (1992). Co-release of acetylcholine and GABA by the starburst amacrine cells. Journal of Neuroscience 12, 13941408.
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.
Pourcho, R.G. (1980). Uptake of [3H]glycine and [3H]GABA by amacrine cells in the cat retina. Brain Research 198, 333346.
Pourcho, R.G. & Goebel, D.J. (1985). A combined Golgi and autoradiographic study of (3H)glycine-accumulating amacrine cells in the cat retina. Journal of Comparative Neurology 233, 473480.
Pourcho, R.G. & Goebel, D.J. (1987). Visualization of endogenous glycine in cat retina: An immunocytochemical study with Fab fragments. Journal of Neuroscience 7, 11891197.
Pourcho, R.G. & Goebel, D.J. (1990). Autoradiographic and immunocytochemical studies of glycine-containing neurons in the retina. In Glycine Neurotransmission, ed. Ottersen, O.P. & Storm-Mathisen, J., pp. 355389. New York: John Wiley & Sons.
Pourcho, R.G. & Osman, K. (1986). Acetylcholinesterase localization in cat retina: A comparison with choline acetyltransferase. Experimental Eye Research 43, 585594.
Pow, D.V. & Crook, D.K. (1994). Rapid postmortem changes in the cellular localisation of amino acid transmitters in the retina as assessed by immunocytochemistry. Brain Research 653, 199209.
Pow, D.V., Wright, L.L. & Vaney, D.I. (1995). The immunocytochemical detection of amino-acid neurotransmitters in paraformaldehyde-fixed tissues. Journal of Neuroscience Methods 56, 115123.
Rodieck, R.W. & Brening, R.K. (1983). Retinal ganglion cells: Properties, types, genera, pathways and trans-species comparisons. Brain, Behavior, and Evolution 23, 121164.
Sassoè-Pognetto, M., Wässle, H. & Grünert, U. (1994). Glycinergic synapses in the rod pathway of the rat retina: Cone bipolar cells express the α1 subunit of the glycine receptor. Journal of Neuroscience 14, 51315146.
Scharfman, H.E., Kunkel, D.D. & Schwartzkroin, P.A. (1989). Intracellular dyes mask immunoreactivity of hippocampal interneurons. Neuroscience Letters 96, 2328.
Sterling, P., Freed, M.A. & Smith, R.G. (1988). Architecture of rod and cone circuits to the on-beta ganglion cell. Journal of Neuroscience 8, 623642.
Tauchi, M. & Masland, R.H. (1984). The shape and arrangement of the cholinergic neurons in the rabbit retina. Proceedings of the Royal Society B (London) 223, 101119.
Tauchi, M. & Masland, R.H. (1985). Local order among the dendrites of an amacrine cell population. Journal of Neuroscience 5, 24942501.
Taylor, W.R. & Wässle, H. (1995). Receptive field properties of starburst cholinergic amacrine cells in the rabbit retina. European Journal of Neuroscience 7, 23083221.
Vaney, D.I. (1984). ‘Coronate’ amacrine cells in the rabbit retina have the ‘starburst’ dendritic morphology. Proceedings of the Royal Society B (London) 220, 501508.
Vaney, D.I. (1985). The morphology and topographic distribution of AII amacrine cells in the cat retina. Proceedings of the Royal Society B (London) 224, 475488.
Vaney, D.I. (1990). The mosaic of amacrine cells in the mammalian retina. Progress in Retinal Research 9, 49100.
Vaney, D.I. (1991). Many diverse types of retinal neurons show tracer coupling when injected with biocytin or Neurobiotin. Neuroscience Letters 125, 187190.
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, 217223.
Vaney, D.I. (1994 a). Patterns of neuronal coupling in the retina. Progress in Retinal and Eye Research 13, 301355.
Vaney, D.I. (1994 b). Territorial organization of direction-selective ganglion cells in rabbit retina. Journal of Neuroscience 14, 63016316.
Vaney, D.I. & Hughes, A.A. (1990). Is there more than meets the eye? In Vision: Coding and Efficiency, ed. Blakemore, C., pp. 7483. Cambridge: Cambridge University Press.
Vaney, D.I. & Young, H.M. (1988 a). GABA-like immunoreactivity in cholinergic amacrine cells of the rabbit retina. Brain Research 438, 369373.
Vaney, D.I. & Young, H.M. (1988 b). GABA-like immunoreactivity in NADPH-diaphorase amacrine cells of the rabbit retina. Brain Research 474, 380385.
Vaney, D.I., Peichl, L. & Boycott, B.B. (1981). Matching populations of amacrine cells in the inner nuclear and ganglion cell layers of the rabbit retina. Journal of Comparative Neurology 199, 373391.
Vaney, D.I., Collin, S.P. & Young, H.M. (1989). Dendritic relationships between cholinergic amacrine cells and direction-selective retinal ganglion cells. In Neurobiology of the Inner Retina, NATO ASI Series, Vol. H31, ed. Weiler, R. & Osborne, N.N., pp. 157168. Berlin: Springer Verlag.
Vaney, D.I., Gynther, I.C. & Young, H.M. (1991 a). Rod-signal interneurons in the rabbit retina: 2. AII amacrine cells. Journal of Comparative Neurology 310, 154169.
Vaney, D.I., Young, H.M. & Gynther, I.C. (1991 b). The rod circuit in the rabbit retina. Visual Neuroscience 7, 141154.
Voigt, T. (1986). Cholinergic amacrine cells in the rat retina. Journal of Comparative Neurology 248, 1935.
Wässle, H., Schäfer-Trenkler, I. & Voigt, T. (1986). Analysis of a glycinergic inhibitory pathway in the cat retina. Journal of Neuroscience 6, 594604.
Wässle, H., Yamashita, U., Greferath, U., Grünert, U. & Müller, F. (1991). The rod bipolar cell of the mammalian retina. Visual Neuroscience 7, 99112.
Wässle, H., Grünert, U. & Röhrenbeck, J. (1993). Immunocytochemical staining of AII-amacrine cells in the rat retina with antibodies against parvalbumin. Journal of Comparative Neurology 332, 407420.
Wässle, H., Grünert, U., Chun, M.-H. & Boycott, B.B. (1995). The rod pathway of the macaque monkey retina: Identification of AII-amacrine cells with antibodies against calretinin. Journal of Comparative Neurology 361, 537551.
West, R.W. (1976). Light and electron microscopy of the ground squirrel retina: Functional considerations. Journal of Comparative Neurology 168, 355378.
Wright, L.L., Pow, D.V., Macqueen, C.L. & Vaney, D.I. (1994). Glycinergic amacrine cells in the rabbit retina: A combined immunocytochemical and tracer-coupling study on retinal wholemounts. Proceedings of the Australian Neuroscience Society 5, 203.
Wright, L.L., Pow, D.V. & Vaney, D.I. (1996). A quantitative immunocytochemical analysis of the distribution of glycinergic and GABAergic amacrine cells in wholemount rabbit retina. Proceedings of the Australian Neuroscience Society 7, 213.
Wyatt, H.J. & Daw, N.W. (1976). Specific effects of neurotransmitter antagonists on ganglion cells in rabbit retina. Science 191, 204205.
Young, H.M., Elston, G., Dann, J.F. & Vaney, D.I. (1990). “DAPI-3” cells in rabbit retina: Glycine-accumulating amacrine cells that costratify with cholinergic amacrine cells. Society for Neuroscience Abstracts 16, 466.
Zhang, L., Kalloniatis, M., Marc, R.E. & Kolb, H. (1996). Calretinin immunostaining in the monkey fovea. Investigative Ophthalmology and Visual Science 37, S950.
Zhou, Z.J. & Fain, G.L. (1995). Neurotransmitter receptors of starburst amacrine cells in rabbit retinal slices. Journal of Neuroscience 15, 53345345.

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The DAPI-3 amacrine cells of the rabbit retina

  • Layne L. Wright, Colin L. Macqueen, Guy N. Elston, Heather M. Young, David V. Pow and David I. Vaney (a1)...

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