Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-18T20:00:10.879Z Has data issue: false hasContentIssue false
  • English
  • Français

The DAPI-3 amacrine cells of the rabbit retina

Published online by Cambridge University Press:  02 June 2009

Layne L. Wright ,
Colin L. Macqueen ,
Guy N. Elston ,
Heather M. Young ,
David V. Pow  and
David I. Vaney
David I. Vaney
Affiliation:
Vision Touch and Hearing Research CentreDepartments of Physiology and PharmacologyThe University of QueenslandBrisbane 4072 QueenslandAustrialia
Get access Rights & Permissions [Opens in a new window]

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.

Keywords

Rabbit retinaGlycinergic amacrine cellsNeurobiotin tracer couplingImmunocytochemistryDirectional selectivity
Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 3 , May 1997 , pp. 473 - 492
Copyright
Copyright © Cambridge University Press 1997

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., Oyster, C.W. & Takahashi, E.S. (1983). Quantitative morphology of rabbit retinal ganglion cells. Proceedings of the Royal Society B (London), 217, 341–355.Google ScholarPubMed
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, 187–190.CrossRefGoogle ScholarPubMed
Bloomfield, S.A. (1992). Relationship between receptive and dendritic field size of amacrine cells in the rabbit retina. Journal of Neurophysiology 68, 711–725.CrossRefGoogle ScholarPubMed
Bolz, J., Thier, P., Voigt, T. & Wässle, H. (1985). Action and localization of glycine and taurine in the cat retina. Journal of Physiology 362, 395–413.CrossRefGoogle ScholarPubMed
Brandon, C. (1987). Cholinergic neurons in the rabbit retina: Dendritic branching and ultrastructural connectivity. Brain Research 426, 119–130.CrossRefGoogle ScholarPubMed
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, 6187–6191.CrossRefGoogle ScholarPubMed
Cajal, S.R. (1933). Die Retina der Wirbeltiere. Wiesbaden: Bergman.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 276, 277–298.CrossRefGoogle ScholarPubMed
Crooks, J. & Kolb, H. (1992). Localization of GABA, glycine, glutamate and tyrosine hydroxylase in the human retina. Journal of Comparative Neurology 315, 287–302.CrossRefGoogle ScholarPubMed
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, 563–577.CrossRefGoogle ScholarPubMed
Cunningham, J.R., Dawson, C. & Neal, M.J. (1983). Evidence for a cholinergic feedback mechanism in the rabbit retina. Journal of Physiology 340, 455–468.CrossRefGoogle ScholarPubMed
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.Google Scholar
Famiglietti, E.V. (1983). ‘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. (1987). Starburst amacrine cells in cat retina are associated with bistratified, presumed directionally selective, ganglion cells. Brain Research 413, 404–408.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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, 322–335.CrossRefGoogle Scholar
Famiglietti, E.V. & Kolb, H. (1975). A bistratified amacrine cell and synaptic circuitry in the inner plexiform layer of the retina. Brain Research 84, 293–300.CrossRefGoogle Scholar
Famiglietti, E.V. & Tumosa, N. (1987). Immunocytochemical staining of cholinergic amacrine cells in rabbit retina. Brain Research 413, 398–403.CrossRefGoogle ScholarPubMed
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, 4911–4922.CrossRefGoogle ScholarPubMed
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, 473–487.CrossRefGoogle ScholarPubMed
Hughes, A. (1985). New perspectives in retinal organization. Progress in Retinal Research 4, 243–313.CrossRefGoogle Scholar
Ikeda, H. & Sheardown, M.J. (1983). Transmitters mediating inhibition of ganglion cells in the cat retina: Iontophoretic studies in vivo. Neuroscience 8, 837–853.CrossRefGoogle ScholarPubMed
Kittila, C.A. & Massey, S.C. (1995). Effect of ON pathway blockade on directional selectivity in the rabbit retina. Journal of Neurophysiology 73, 703–712.CrossRefGoogle Scholar
Kolb, H. & Famiglietti, E.V. (1974). Rod and cone pathways in the inner plexiform layer of cat retina. Science 186, 47–49.CrossRefGoogle ScholarPubMed
Kolb, H., Nelson, R. & Mariani, A. (1981). Amacrine cells, bipolar cells and ganglion cells of the cat retina: A Golgi study. Vision Research 21, 1081–1114.CrossRefGoogle ScholarPubMed
Kolb, H., Linberg, K.A. & Fisher, S.K. (1992). Neurons of the human retina: A Golgi study. Journal of Comparative Neurology 318, 147–187.CrossRefGoogle ScholarPubMed
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, 2617–2628.CrossRefGoogle Scholar
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, 605–617.CrossRefGoogle ScholarPubMed
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, 173–216.3.0.CO;2-2>CrossRefGoogle ScholarPubMed
Maranto, A.R. (1982). Neuronal mapping: a photooxidation reaction makes Lucifer yellow useful for electron microscopy. Science 217, 953–955.CrossRefGoogle ScholarPubMed
Marc, R.E. (1989). The role of glycine in the mammalian retina. Progress in Retinal Research 8, 67–107.CrossRefGoogle Scholar
Marc, R.E. & Liu, W.-L.S. (1985). (3H)glycine-accumulating neurons of the human retina. Journal of Comparative Neurology 232, 241–260.CrossRefGoogle Scholar
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, 4006–4034.CrossRefGoogle ScholarPubMed
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.Google Scholar
Marc, R.E., Murry, R.F. & Basinger, S.F. (1995 b). Pattern recognition of amino acid signatures in retinal neurons. Journal of Neuroscience 15, 5106–5129.CrossRefGoogle ScholarPubMed
Mariani, A.P. (1990). Amacrine cells of the rhesus monkey retina. Journal of Comparative Neurology 301, 382–400.CrossRefGoogle ScholarPubMed
Mariani, A.P. & Hersh, L.B. (1988). Synaptic organization of cholinergic amacrine cells in the rhesus monkey retina. Journal of Comparative Neurology 267, 269–280.CrossRefGoogle ScholarPubMed
Masland, R.H. & Tauchi, M. (1986). The cholinergic amacrine cell. Trends in Neurosciences 9, 218–223.CrossRefGoogle 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 B (London) 223, 79–100.Google ScholarPubMed
Massey, S.C. (1990). Cell types using glutamate as a neurotransmitter in the vertebrate retina. Progress in Retinal Research 9, 399–425.CrossRefGoogle Scholar
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, 1607–1613.CrossRefGoogle ScholarPubMed
Millar, T.J. & Morgan, I.G. (1987). Cholinergic amacrine cells in the rabbit retina synapse onto other cholinergic amacrine cells. Neuroscience Letters 74, 281–285.CrossRefGoogle ScholarPubMed
Mills, S.L. & Massey, S.C. (1991). Labeling and distribution of AII amacrine cells in the rabbit retina. Journal of Comparative Neurology 304, 491–501.CrossRefGoogle ScholarPubMed
Müller, F., Wässle, H. & Voigt, T. (1988). Pharmacological modulation of the rod pathway in the cat retina. Journal of Neurophysiology 59, 1657–1672.CrossRefGoogle ScholarPubMed
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, 363–372.CrossRefGoogle ScholarPubMed
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, 301–305.CrossRefGoogle ScholarPubMed
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, 43–53.CrossRefGoogle ScholarPubMed
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, 3414–3418.CrossRefGoogle ScholarPubMed
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, 1394–1408.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, 579–608.CrossRefGoogle ScholarPubMed
Pourcho, R.G. (1980). Uptake of [3H]glycine and [3H]GABA by amacrine cells in the cat retina. Brain Research 198, 333–346.CrossRefGoogle ScholarPubMed
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, 473–480.CrossRefGoogle ScholarPubMed
Pourcho, R.G. & Goebel, D.J. (1987). Visualization of endogenous glycine in cat retina: An immunocytochemical study with Fab fragments. Journal of Neuroscience 7, 1189–1197.CrossRefGoogle ScholarPubMed
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. 355–389. New York: John Wiley & Sons.Google Scholar
Pourcho, R.G. & Osman, K. (1986). Acetylcholinesterase localization in cat retina: A comparison with choline acetyltransferase. Experimental Eye Research 43, 585–594.CrossRefGoogle ScholarPubMed
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, 199–209.CrossRefGoogle ScholarPubMed
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, 115–123.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, 121–164.CrossRefGoogle ScholarPubMed
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, 5131–5146.CrossRefGoogle Scholar
Scharfman, H.E., Kunkel, D.D. & Schwartzkroin, P.A. (1989). Intracellular dyes mask immunoreactivity of hippocampal interneurons. Neuroscience Letters 96, 23–28.CrossRefGoogle ScholarPubMed
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, 623–642.CrossRefGoogle Scholar
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, 101–119.Google ScholarPubMed
Tauchi, M. & Masland, R.H. (1985). Local order among the dendrites of an amacrine cell population. Journal of Neuroscience 5, 2494–2501.CrossRefGoogle ScholarPubMed
Taylor, W.R. & Wässle, H. (1995). Receptive field properties of starburst cholinergic amacrine cells in the rabbit retina. European Journal of Neuroscience 7, 2308–3221.CrossRefGoogle ScholarPubMed
Vaney, D.I. (1984). ‘Coronate’ amacrine cells in the rabbit retina have the ‘starburst’ dendritic morphology. Proceedings of the Royal Society B (London) 220, 501–508.Google ScholarPubMed
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, 475–488.Google ScholarPubMed
Vaney, D.I. (1990). The mosaic of amacrine cells in the mammalian retina. Progress in Retinal Research 9, 49–100.CrossRefGoogle Scholar
Vaney, D.I. (1991). Many diverse types of retinal neurons show tracer coupling when injected with biocytin or Neurobiotin. Neuroscience Letters 125, 187–190.CrossRefGoogle ScholarPubMed
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, 217–223.CrossRefGoogle ScholarPubMed
Vaney, D.I. (1994 a). Patterns of neuronal coupling in the retina. Progress in Retinal and Eye Research 13, 301–355.CrossRefGoogle Scholar
Vaney, D.I. (1994 b). Territorial organization of direction-selective ganglion cells in rabbit retina. Journal of Neuroscience 14, 6301–6316.CrossRefGoogle ScholarPubMed
Vaney, D.I. & Hughes, A.A. (1990). Is there more than meets the eye? In Vision: Coding and Efficiency, ed. Blakemore, C., pp. 74–83. Cambridge: Cambridge University Press.Google Scholar
Vaney, D.I. & Young, H.M. (1988 a). GABA-like immunoreactivity in cholinergic amacrine cells of the rabbit retina. Brain Research 438, 369–373.CrossRefGoogle ScholarPubMed
Vaney, D.I. & Young, H.M. (1988 b). GABA-like immunoreactivity in NADPH-diaphorase amacrine cells of the rabbit retina. Brain Research 474, 380–385.CrossRefGoogle ScholarPubMed
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, 373–391.CrossRefGoogle ScholarPubMed
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. 157–168. Berlin: Springer Verlag.CrossRefGoogle Scholar
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, 154–169.CrossRefGoogle ScholarPubMed
Vaney, D.I., Young, H.M. & Gynther, I.C. (1991 b). The rod circuit in the rabbit retina. Visual Neuroscience 7, 141–154.CrossRefGoogle ScholarPubMed
Voigt, T. (1986). Cholinergic amacrine cells in the rat retina. Journal of Comparative Neurology 248, 19–35.CrossRefGoogle ScholarPubMed
Wässle, H., Schäfer-Trenkler, I. & Voigt, T. (1986). Analysis of a glycinergic inhibitory pathway in the cat retina. Journal of Neuroscience 6, 594–604.CrossRefGoogle ScholarPubMed
Wässle, H., Yamashita, U., Greferath, U., Grünert, U. & Müller, F. (1991). The rod bipolar cell of the mammalian retina. Visual Neuroscience 7, 99–112.CrossRefGoogle ScholarPubMed
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, 407–420.CrossRefGoogle ScholarPubMed
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, 537–551.CrossRefGoogle ScholarPubMed
West, R.W. (1976). Light and electron microscopy of the ground squirrel retina: Functional considerations. Journal of Comparative Neurology 168, 355–378.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.Google Scholar
Wyatt, H.J. & Daw, N.W. (1976). Specific effects of neurotransmitter antagonists on ganglion cells in rabbit retina. Science 191, 204–205.CrossRefGoogle ScholarPubMed
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.Google Scholar
Zhang, L., Kalloniatis, M., Marc, R.E. & Kolb, H. (1996). Calretinin immunostaining in the monkey fovea. Investigative Ophthalmology and Visual Science 37, S950.Google Scholar
Zhou, Z.J. & Fain, G.L. (1995). Neurotransmitter receptors of starburst amacrine cells in rabbit retinal slices. Journal of Neuroscience 15, 5334–5345.CrossRefGoogle ScholarPubMed