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Cholinergic amacrine neurons of the dogfish retina

Published online by Cambridge University Press:  02 June 2009

Christopher Brandon
Christopher Brandon
Affiliation:
Department of Cell Biology and Anatomy, The Chicago Medical School, North Chicago
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Abstract

In the mammalian retina, the dendritic arbors of cholinergic amacrine neurons have a unique starburst shape; these arbors lie in narrow sublaminae within the inner plexiform layer, where they provide input to a wide variety of ganglion cell types. Immunocytochemistry has been used to identify cholinergic cells in one poikilotherm, the goldfish (Tumosa et al., 1984), but there has been no description of the detailed dendritic morphology of these cells in the lower vertebrates. In the present study, cholinergic neurons have been characterized, by immunocytochemistry and dye filling, in the retina of the Pacific Coast dogfish, Squalus acanthias.

The inner nuclear layer contained two populations of choline acetyltransferase-immunoreactive amacrine cells, of different sizes (average soma diameters 12.2 vs. 16.3 μm); 70% of the immunoreactive cells were of the smaller type. Cholinergic dendrites from these two cell populations formed two narrow strata within the inner plexiform layer, at depths of 14% and 31%. In the ganglion cell layer, 40% of the cells were immunoreactive for choline acetyltransferase (ChAT); these cells were very homogeneous in size, had an average diameter of 12.6 μm, and appeared to represent a single class of cholinergic amacrine. The dendrites of these cells formed a single, narrow stratum within the inner plexiform layer, at a depth of 59%.

In living preparations, the smallest cell bodies in the ganglion cell layer were filled iontophoretically with Lucifer Yellow, under microscopic control. Such cells invariably had a stellate morphology; in many cases, they appeared quite similar to the starburst cholinergic amacrine cells described in rabbit and rat (Vaney, 1984; Voigt, 1986). Although double-label experiments failed to demonstrate ChAT immunoreactivity in specific dye-filled cells, the dendritic arbors of individual dye-filled stellate dogfish amacrines did co-stratify precisely with the proximal ChAT-immunoreactive sublamina of the inner plexiform layer. In addition, dye injection and ChAT immunocytochemistry appeared to label the same population of dogfish neurons, as suggested by the close structural similarity, and similar numerical proportion, of the cells identified with these two techniques.

Similarities between the displaced cholinergic amacrine neurons of the dogfish retina, and the cholinergic, “starburst” amacrine neurons of the rabbit retina, are discussed.

Keywords

DogfishAcetylcholineAmacrine neuronDye injectionStarburst amacrine
Type
Research Articles
Information
Visual Neuroscience , Volume 6 , Issue 6 , June 1991 , pp. 553 - 562
Copyright
Copyright © Cambridge University Press 1991

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References

Adams, J.C. (1981). Heavy metal intensification of DAB-based HRP reaction product. Journal of Histochemistry and Cytochemistry 29, 775.CrossRefGoogle ScholarPubMed
Ariel, M. & Daw, N.W. (1982). Pharmacological analysis of directionally sensitive rabbit retinal ganglion cells. Journal of Physiology 324, 161–185.CrossRefGoogle ScholarPubMed
Brandon, C. (1985). Improved immunocytochemical staining through the use of primary Fab fragments, Fab-specific second antibody, and FabHRP. Journal of Histochemistry Cytochemistry 33, 715–719.CrossRefGoogle Scholar
Brandon, C. (1987). Cholinergic neurons in the rabbit retina: dendritic branching and ultrastructural connectivity. Brain Research 426, 119–130.CrossRefGoogle ScholarPubMed
Brown, R.N. Jr & Hitchcock, P.F. (1989). Dendritic growth of DAPI-accumulating amacrine cells in the retina of the goldfish. Developmental Brain Research 50, 123–128.CrossRefGoogle ScholarPubMed
Cohen, J.L (1985). Effects of glycine and GABA on the ganglion cells of the retina of the skate (Raja erinacea). Brain Research 332, 169–173.CrossRefGoogle ScholarPubMed
Collin, S.P. (1988). The retina of the shovel-nosed ray, Rhinobatos batillum (Rhinobatidae): morphology and quantitative analysis of the ganglion, amacrine, and bipolar cell populations. Experimental Biology 47, 195–207.Google ScholarPubMed
Conley, M., Fitzpatrick, D. & Lachica, E.A. (1986). Laminar asymmetry in the distribution of choline acetyltransferase-immunoreactive neurons in the retina of the tree shrew (Tupaia belangeri). Brain Research 399, 332–338.CrossRefGoogle ScholarPubMed
Famiglitti, E.V. & Tumosa, N. (1987).Immunocytochemical staining of cholinergic amacrine cells in rabbit retina. Brain Research 413, 398–403.CrossRefGoogle Scholar
Johnson, C.D. & Epstein, M.L. (1986). Monoclonal antibodies and polyvalent antiserum to chicken choline acetyltransferase. Journal of Neurochemistry 46, 968–976.CrossRefGoogle ScholarPubMed
Maren, T.H. (1967). Special body fluids of the elasmobranch. In Sharks, Skates, and Rays, ed. Gilbert, P.W., Mathewson, R. & Rall, D.P. pp. 287–292. Baltimore, MD: Johns Hopkins Press.Google Scholar
Masland, R.H. & Ames, A. (1976). Responses to acetylcholine of ganglion cells in an isolated mammalian retina. Journal of Neurophysiology 39, 1220–1235.CrossRefGoogle Scholar
Masland, R.H. & Mills, J.W. (1979). Autoradiographic identification of acetylcholine in the rabbit retina. Journal of Cell Biology 83, 159–178.CrossRefGoogle ScholarPubMed
Masland, R.H., Mills, J.W. & Hayden, S.A. (1984 a). Acetylcholinesynthesizing amacrine cells: identification and selective staining by using radioautography and fluorescent markers. Proceedings of the Royal Society B (London) 223, 79–100.Google ScholarPubMed
Masland, R.H., Mills, J.W. & Cassidy, C. (1984 b). The functions of acetylcholine in the rabbit retina. Proceedings of the Royal Society B (London) 223, 121–139.Google ScholarPubMed
Millar, T., Ishimoto, I., Johnson, C.D., Epstein, M.L., Chubb, I.W. & Morgan, I.G. (1985). Cholinergic and acetylcholinesterase-containing neurons of the chicken retina. Neuroscience Letters 61, 311–316.CrossRefGoogle ScholarPubMed
Millar, T., Ishimoto, I., Chubb, I.W., Epstein, M.L., Johnson, C.D. & Morgan, I.G. (1987). Cholinergic amacrine cells of the chicken retina: a light- and electron-microscope immunocytochemical study. Neuroscience 21, 725–743.CrossRefGoogle ScholarPubMed
Mitrofanis, J. & Stone, J. (1988). Distribution of cholinergic amacrine cells in the retinas of normally pigmented and hypopigmented strains of rat and cat. Visual Neuroscience 1, 367–376.CrossRefGoogle ScholarPubMed
Naka, K-I. & Carraway, N.R.G. (1975). Morphological and functional identifications of catfish retinal neurons, 1: Classical morphology. Journal of Neurophysiology 38, 53–71.CrossRefGoogle ScholarPubMed
Rodieck, R.W. (1989). Starburst amacrine cells of the primate retina. Journal of Comparative Neurology 285, 18–37.CrossRefGoogle ScholarPubMed
Schmidt, M., Humphrey, M.F. & Wassle, H. (1987). Action and localization of acetylcholine in the cat retina. Journal of Neurophysiology 58, 997–1015.CrossRefGoogle ScholarPubMed
Slemmon, J.R., Salvaterra, P.M. & Saito, K. (1980). Preparation and characterization of peroxidase:antiperoxidase-Fab complex. Journal of Histochemistry and Cytochemistry 28, 10–18.CrossRefGoogle ScholarPubMed
Stell, W.K., Wagner, H.G. & Wolbarsht, M.L. (1970). Receptive-field organization of ganglion cells in the retina of the smooth dogfish (Mustelus canis). Biological Bulletin 139, 437–438.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 B (London) 223, 101–119.Google ScholarPubMed
Tauchi, M. & Masland, R.H. (1985). Local order among the denrites of an amacrine cell population. Journal of Neuroscience 5, 2494–2501.CrossRefGoogle Scholar
Tumosa, N., Eckenstein, F. & Stell, W.K. (1984). Immunocytochemical localization of putative cholinergic neurons in the goldfish retina. Neuroscience Letters 48, 255–259.CrossRefGoogle ScholarPubMed
Vallerga, S., Kock, J.-H. & Usai, C. (1987), DAPI staining of neurons in the vertebrate retina. Abstracts of the Association for Research in Vision and Ophthalmology 28, 351.Google Scholar
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. (1990). The mosaic of amacrine cells in the mammalian retina. Progress in Retinal Research 9, 1–46.CrossRefGoogle Scholar
Voigt, T. (1986). Cholinergic amacrine cells in the rat retina. Journal of Comparative Neurology 248, 19–35.CrossRefGoogle ScholarPubMed