Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-25T06:01:44.223Z Has data issue: false hasContentIssue false

Displaced cholinergic, GABAergic amacrine cells in the rabbit retina also contain adenosine

Published online by Cambridge University Press:  02 June 2009

Christine Blazynski
Affiliation:
Departments of Biochemistry and Molecular Biophysics, Ophthalmology, and Anatomy-Neurbiology, Washington University School of Medicine, St. Louis

Abstract

It is generally accepted that the purine nucleoside, adenosine, plays a neuromodulatory role in the central nervous system (CNS) (Daly et al., 1981; Phillis ' Wu, 1983; Williams, 1986; Williams, 1987; Snyder, 1985). Adenosine is thought to exert its primary effects presynaptically, by inhibiting the release of neurotransmitters including ³-aminobutyric acid (GABA) and acetylcholine (ACh) (Phillis ' Barraco, 1985; Proctor ' Dunwiddie, 1987). In mammalian retina, cell bodies that are strongly labeled for adenosine-like immunoreactivity (ALIR) have been localized to the ganglion cell layer (GCL) (Braas et al., 1987; Blazynski et al., 1989). Rabbit retinal cells that are labeled by markers for both ACh and GABA are located in the GCL and inner nuclear layer (INL) (Tauchi ' Masland, 1984; Vaney ' Young, 1988b; Brecha et al., 1988). It is now demonstrated in the rabbit retina that approximately 50% of the cells labeled for ALIR within the GCL represent true ganglion cells, with the remainder presumed to be displaced cholinergic amacrine cells (DAPI accumulating). In addition, some of these same cells also demonstrate immunoreactivity to glutamate decarboxylase (GAD), involved in the biosynthesis of the neurotransmitter GABA. Thus, in a particular class of retinal neurons, two fast-acting neurotransmitters as well as a putative neuromodulator have been co-localized.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1989

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

Ariel, M. & Daw, N.W. (1982 a). 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. (1982 b). Pharmacological analysis of directionally sensitive rabbit retinal ganglion cells. Journal of Physiology 324, 161185.CrossRefGoogle ScholarPubMed
Blazynski, C., Kinscherf, A.D., Geary, K.M. & Ferrendelli, J.A (1986). Adenosine-mediated regulation of cyclic AMP levels in isolated incubated retinas. Brain Research 366, 224229.Google Scholar
Blazynski, C. (1987). Adenosine A1 receptor-mediated inhibition of adenylate cyclase in rabbit retina. Journal of Neuroscience 7, 25222528.Google Scholar
Blazynski, C., Mosinger, J.L. ' Cohen, A.I. (1989). A comparison of endogenous adenosine-containing cells and adenosine uptake in mammalian retinas. Visual Neuroscience 2, 109116.Google Scholar
Braas, K.M., Newby, A.C., Wilson, V.S. & Snyder, S.H. (1986). Adenosine-containing neurons in the brain localized by immunocytochemistry. Journal of Neuroscience 6, 19521961.Google Scholar
Braas, K.M., Zarbin, M.A. & Snyder, S.H. (1987). Endogenous adenosine and adenosine receptors localized to ganglion cells of the retina. Proceedings of the National Academy of Sciences of the U.S.A. 84, 39063910.Google Scholar
Brecha, N., Johnson, D., Bolz, J., Sharma, S., Parnavelas, J.G. & Lieberman, A.R(1987). Substance P-immunoreactive retinal ganglion cells and their central axon terminals in the rabbit. Nature 327, 155158.CrossRefGoogle ScholarPubMed
Brecha, N., Johnson, D., Peichi, L. & Wassle, H. (1988). Cholinergic amacrine cells of the rabbit retina contain glutamate decarboxylase and ³-aminobutyrate immunoreactivity. Proceedings of the National Academy of Sciences of the U.S.A. 85, 61876191.CrossRefGoogle Scholar
Daly, J.W., Bruns, R.F. & Snyder, S.H. (1981). Adenosine receptors in the central nervous system: relationship to the central actions of methylxanthines. Life Sciences 28, 20832097.Google Scholar
De Mello, M.C.F., Ventura, A.L.M., Paes, De Carvalho R., Klein, W.L. & De, Mello F.G. (1982). Regulation of dopamine- and adenosine-dependent adenylate cyclase systems of chicken embryo retina cells in culture. Proceedings of the National Academy of Sciences of the U.S.A. 79, 57085712.Google Scholar
Ehinger, B. & Perez, M.T.R (1984). Autoradiography of nucleoside uptake into the retina. Neurochem. Int. 6, 369381.CrossRefGoogle ScholarPubMed
Goodman, R.R., Kuhar, M.J., Hester, L. & Snyder, S.H. (1983). Adenosine receptors: autoradiographic evidence for their location on axon terminals of excitatory neurons. Science 220, 967969.Google Scholar
Krupin, T., Podos, S.M. & Becker, B. (1970). Effect of optic nerve transection on osmotic alterations of intraocular pressure. American Journal of Ophthalmology 70, 214220.CrossRefGoogle ScholarPubMed
Masland, R.H. & Livingstone, C.J. (1976). Effect of stimulation with light on synthesis and release of acetylcholine by an isolated mammalian retina. Journal of Neurophysiology 39, 12101218.Google Scholar
Masland, R.H., Mills, J.W. & Cassidy, C. (1984 a). The functions of acetylcholine in the rabbit retina. Proceedings of the Royal Society (London) 223, 121139.Google ScholarPubMed
Masland, R.H., Mills, J.W. & Hayden, S.A. (1984 b). Acetylcholinesynthesizing amacrine cells: identification and selective staining by using radioautography and fluorescent markers. Proceedings of the Royal Society (London) 223, 79100.Google Scholar
Massey, S.C. & Neal, M.J. (1979). The light-evoked release of acetylcholine from the rabbit retina in vivo and its inhibition by ³-aminobutyric acid. Journal of Neurochemistry 32, 13271329.Google Scholar
Massey, S.C. & Redburn, D.A. (1982). A tonic ³-aminobutyric acid- mediated inhibition of cholinergic amacrine cells in rabbit retina. Journal of Neuroscience 2, 16331643.Google Scholar
Miller, R.F. (1988). Are single retinal neurons both excitatory and inhibitory? Nature 336, 517518.CrossRefGoogle ScholarPubMed
Mosinger, J. & Yazulla, S. (1987). Double-label analysis of GAD- and GABA-like immunoreactivity in the rabbit retina. Vision Research 27, 2330.Google Scholar
Mosinger, J.L. & Yazulla, S. (1985). Co-localization of GAD-like immunoreactivity and [3H]-GABA uptake in amacrine cells of rabbit retina. Journal of Comparative Neurology 240, 396406.CrossRefGoogle Scholar
Newby, A.C. & Sala, G.B. (1982). A new procedure for haptenizing adenosine leading to a more specific radioimmunoassay method. Biochemistry Journal 208, 603610.CrossRefGoogle ScholarPubMed
Malley, D.M. & Masland, R.H. (1988). Co-release of acetylcholine and GABA by a retinal neuron. Investigative Ophthalmology and Visual Science (Abstract) 29, 273.Google Scholar
Oertel, W.H., Tappaz, I.J., Kopin, I.J., Ranson, D.H. & Schmechel, D.E. (1980). Production of an antiserum to rat brain glutamate (GAD)/cysteine sulfinate (CSD) decarboxylase. Brain Research Bulletin 5, 713719.Google Scholar
Carvalho, R. Paes De & De Mello, F.G. (1982). Adenosine-elicited accumulation of adenosine 3&,5&-cyclic monophosphate in the chick embryo retina. Journal of Neurochemistry 38, 493500.Google Scholar
Paes, Ee Carvalho R. & De Mello, F.G. (1985). Expression of A1 adenosine receptors modulating dopamine-dependent cyclic AMP accumulation in the chick embryo retina. Journal of Neurochemistry 44, 845851.Google Scholar
Perez, M.T.R. & Bruun, A. (1987). Co-localization of [3H]-adeno- sine accumulation and GABA immunoreactivity in the chicken and rabbit retinas. Histochemistry 87, 413417.CrossRefGoogle Scholar
Phillis, J.W. & Barraco, R.A. (1985). Adenosine, adenylate cyclase, and transmitter release. Advances in Cyclic Nucleotide Protein Phosphorylation Research 19, 243257.Google ScholarPubMed
Phillis, J.W. & Wu, P.H. (1983). Roles of adenosine and adenine nucleotides in the central nervous system. In Physiology and Pharmacology of Adenosine Derivatives, ed. Daly, J.W., Kuroda, Y., Phillis, J.W., Shimizu, H. & Ui, M., pp. 219236. New York: Raven Press.Google Scholar
Proctor, W.R. & Dunwiddie, T.V. (1987). Pre- and postsynaptic actions of adenosine in the in vitro rat hippocampus. Brain Research 426, 187190.Google Scholar
Sagar, S.M. (1987). Somatostatin-like immunoreactive material in the rabbit retina: immunohistochemical staining using monoclonal antibodies. Journal of Comparative Neurology 266, 291299.CrossRefGoogle ScholarPubMed
Snyder, S.H. (1985). Adenosine as a neuromodulator. Annual Review of Neuroscience 8, 103124.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 (London) 223, 101119.Google Scholar
Trussell, L.O. & Jackson, M.B. (1985). Adenosine-activated potassium conductance in cultured striatal neurons. Proceedings of the National Academy of Sciences of the U.S.A. 82, 48574861.CrossRefGoogle ScholarPubMed
Trussell, L.O. & Jackson, M.B. (1987). Dependence of an adenosine activated potassium current on a GTP-binding protein in mammalian central neurons. Journal of Neuroscience 7, 33063316.CrossRefGoogle ScholarPubMed
Vaney, D.I. (1980). A quantitative comparison between the ganglion cell populations and axonal outflows of the visual streak and periphery of the rabbit retina. Journal of Comparative Neurology 189, 215233.Google Scholar
Vaney, D.I. (1984). ‘Coronate’ amacrine cells in the rabbit retina have the ‘starburst’ dendritic morphology. Proceedings of the Royal Society (London) 220, 501508.Google Scholar
Vaney, D.I. & Young, H.M. (1988 a). GABA-like immunoreactivity in NADPH-diaphorase amacrine cells of the rabbit retina. Brain Research 474, 380385.CrossRefGoogle ScholarPubMed
Vaney, D.I. & Young, H.M. (1988 b). GABA-like immunoreactivity in cholinergic amacrine cells of the rabbit retina. Brain Research 438, 369373.Google Scholar
Williams, M. (1986). Purinergic receptors in the CNS. In Neuromethods, ed. Boulton, A.A., Baker, G.B. & Hrdina, P.D., pp. 365413. Clifton: Humana Press.Google Scholar
Williams, M. (1987). Purinergic receptors and central nervous system function. In Psychopharmacology. The Third Generation of Progress, ed. Meltzer, H.Y., pp. 289301. New York: Raven Press.Google Scholar
Yazulla, S., Studholme, K. & Zucker, C. (1985). Synaptic organization of substance-P like immunoreactive amacrine cells in the goldfish retina. Journal of Comparative Neurology 231, 232238.Google Scholar
Zucker, C.L., Yazulla, S. & Wu, J.-Y. (1984). Non-correspondence of [3H]-GABA uptake and GAD localization in goldfish amacrine cells. Brain Research 298, 154158.Google Scholar