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Cholinoceptive neurons in the retina of the chick: an immunohistochemical study of the nicotinic acetylcholine receptors

Published online by Cambridge University Press:  02 June 2009

K.T. Keyser ,
T.E. Hughes ,
P.J. Whiting ,
J.M. Lindstrom  and
H.J. Karten
K.T. Keyser
Affiliation:
Department of Neurosciences, University of California, San Diego, La Jolla
T.E. Hughes
Affiliation:
Department of Neurosciences, University of California, San Diego, La Jolla
P.J. Whiting
Affiliation:
Receptor Biology Laboratory, The Salk Institute for Biological Studies, La Jolla
J.M. Lindstrom
Affiliation:
Receptor Biology Laboratory, The Salk Institute for Biological Studies, La Jolla
H.J. Karten
Affiliation:
Receptor Biology Laboratory, The Salk Institute for Biological Studies, La Jolla
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Abstract

Monoclonal antibodies directed against nicotinic acetylcholine receptors (nAChRs) were used to identify and characterize cholinoceptive neurons in the chick retina. Two monoclonal antibodies (mAbs), mAb 210 and mAb 270, stained many neurons in both the inner nuclear layer (INL) and ganglion cell layer (GCL). A class of large labeled cells in the inner INL were positioned at the INL/IPL (inner plexiform layer) border and resembled displaced ganglion cells (DGCs). Their identity was confirmed with injections of rhodamine-labeled microspheres into the ventral tectum and nucleus of the basal optic root (nBOR). Four days after the injection, large nAChR-positive neurons in the inner INL were labeled with beads. The distribution of these cells matched that reported for DGCs in the chicken and pigeon (Reiner et al., 1979; Fite et al., 1981). Many smaller cells in the INL also exhibited nAChR immunoreactivity. These cells were not retrogradely labeled after bead injections into retinal recipient areas. Their processes entered the IPL where they arborized in a band comprised of the inner leaflet of lamina 1 and all of lamina 2. In some instances, a process continued inward to lamina 4. These neurons were tentatively identified as amacrine cells because of their position and branching pattern.

Approximately 12–18% of the cells in the GCL exhibited nAChR immunoreactivity. Many of these cells could be classified as ganglion cells as their axons were also labeled following exposure to nAChR antibodies. Their distribution mirrored that of all ganglion cells with a higher density of cells in the central retina than in the periphery (Ehrlich, 1981). A “double label” technique was used to compare the distribution of nAChR-positive neurons with that of the choline acetyltransferase-positive (ChAT), cholinergic neurons in the chick retina. The two antigens were visualized with two different fluorophores: FITC and RITC. We were unable to find any cells in either the INL or GCL that exhibited both ChAT- and nAChR-like immunoreactivity. The nAChR-positive cells and the ChAT-positive cells both arborized in two bands within the IPL. The patterns were in perfect register in the inner IPL (lamina 4). But, in the outer IPL, the nAChR-positive dendrites were observed in the inner leaflet of lamina 1 and in all of lamina 2 while the ChAT-positive dendrites did not extend into the innermost portion of lamina 2.

Keywords

AcetylcholineNicotinic acetylcholine receptorRetinaCholine acetyltransferaseGanglion cells
Type
Research Articles
Information
Visual Neuroscience , Volume 1 , Issue 4 , July 1988 , pp. 349 - 366
Copyright
Copyright © Cambridge University Press 1988

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References

Ames, A. & Pollen, D.A. (1969). Neurotransmission in central nervous tissue: a study of isolated rabbit retina. Journal of Neurophysiology 32, 424–442.CrossRefGoogle ScholarPubMed
Amthor, F.R., Oyster, C.W. & Takahashi, E.S. (1984). Morphology of ON-OFF direction-selective ganglion cells in the rabbit retina. Brain Research 298, 187–190.CrossRefGoogle ScholarPubMed
Ariel, M. & Daw, N.W. (1982 a). Effects of cholinergic drugs on receptive field properties of rabbit retinal ganglion cells. Journal of Physiology 324, 135–160.CrossRefGoogle ScholarPubMed
Ariel, M. & Daw, N.W. (1982b). Pharmacological analysis of direc-tionally sensitive rabbit retinal ganglion cells. Journal of Physiology (London) 324, 161–186.CrossRefGoogle ScholarPubMed
Baughman, R.W. & Bader, C.R. (1977). Biochemical characterization and cellular localization of the cholinergic system in the chicken retina. Brain Research 138, 469–485.CrossRefGoogle ScholarPubMed
Bloomfield, S.A. & Miller, R.F. (1986). A functional organization of ON and OFF pathways in the rabbit retina. Journal of Neuro-science 6, 1–13.Google Scholar
Brecha, N., Francis, A. & Schechter, N. (1979). Rapid loss of nicotine-cholinergic receptor binding activity in the deafferented avian optic lobe. Brain Research 167, 273–280.CrossRefGoogle ScholarPubMed
Chiapinelli, V.A. (1985). Actions of snake venom toxins on neuronal nicotinic receptors and other neuronal receptors. Pharmacology and Therapeutics 31, 1–32.CrossRefGoogle Scholar
Coleman, P.A. & Miller, R.F. (1984). The electroanatomy of the rabbit ON-OFF amacrine cell. Society for Neuroscience Abstracts 10, 325.Google Scholar
Conley, M., Fitzpatrick, D. & Lachica, E.A. (1986). Laminar asymmetry in the distribution of choline acetyltransferase-immunoreative neurons in the retina of the tree shrew (Tupaia belangeri). Brain Research 399, 332–338.CrossRefGoogle ScholarPubMed
Cuello, A.C. & Sofroniew, M.V. (1984). The anatomy of the CNS cholinergic neurons. Trends in Neuroscience 7, 74–78.CrossRefGoogle Scholar
Dogiel, A.S. (1888). Uber das Verhalten der nervosen Elemente in der Retina der Ganoiden, Reptilien, Vogel und Saugetiere. Anatomis-cher Anzeiger 3, 133–143.Google Scholar
Eckenstein, F. & Thoenen, H. (1982). Production of specific antisera and monoclonal antibodies to choline acetyltransferase: characterization and use for identification of cholinergic neurons. EMBO Journal 1, 363–368.CrossRefGoogle ScholarPubMed
Eckenstein, F., Baughman, R.W., Sofroniew, M.V. & Thibault, J. (1983). A comparison of the distribution of choline acetyltransferase and tyrosine hydroxylase immunoreactivities in rat retina. Society for Neuroscience Abstracts 9, 80.Google Scholar
Ehrlich, D. (1981). Regional specialization of the chick retina as revealed by the size and density of neurons in the ganglion cell layer. Journal of Comparative Neurology 195, 643–657.CrossRefGoogle ScholarPubMed
Erichsen, J.T., Reiner, A. & Karten, H.J. (1982). Co-occurrence of substance P-like and leucine-enkephalin-like immunoreactivities in neurones and fibres of avian nervous system. Nature 295, 407–410.CrossRefGoogle Scholar
Famiglietti, E.V. & Kolb, H. (1976). Structural basis for the ON- and OFF-center responses in retinal ganglion cells. Science 194, 193–195.CrossRefGoogle ScholarPubMed
Famiglietti, E.V., Kaneko, A. & Tachibana, M. (1977). Neuronal architecture of ON and OFF pathways to ganglion cells of the carp retina. Science 198, 1267–1269.CrossRefGoogle Scholar
Famiglietti, E.V. (1983). ON and OFF pathways through amacrine cells in mammalian retina: the synaptic connections of “starburst” amacrine cells. Vision Research 23, 1265–1279.CrossRefGoogle ScholarPubMed
Fite, K.V., Brecha, N., Karten, H.J. & Hunt, S.P. (1981). Displaced ganglion cells and the accessory optic system of the pigeon. Journal of Comparative Neurology 195, 279–288.CrossRefGoogle ScholarPubMed
Hare, W.A., Lowe, J.S. & Owen, J. (1986). Morphology of physiologically identified bipolar cells in the retina of the tiger salamander, Ambystoma tigrinum. Journal of Comparative Neurology 252, 130–138.CrossRefGoogle ScholarPubMed
Henley, J.M., Linstrom, J.M. & Oswald, R.E. (1986). Acetylcholine receptor synthesis in retina and transport to optic tectum in goldfish. Science 232, 1627–1629.CrossRefGoogle ScholarPubMed
Hughes, T.E., Keyser, K.T., Whiting, P.J., Lindstrom, J.M. & Karten, H.J. (1987). Cholinoceptive neurons in the retina of the chicken: an immunohistochemical study of the nicotinic acetylcholine receptors. Society for Neuroscience Abstracts 13, 1058.Google Scholar
Jacob, M., Berg, D. & Lindstrom, J. (1984). Shared antigenic determinant between Electrophorus acetylcholine receptor and a synaptic component on chicken ciliary ganglion neurons. Proceedings of the National Academy of Sciences (USA) 81, 3223–3227.CrossRefGoogle Scholar
Jacob, M.H., Lindstrom, J.M. & Berg, D.D. (1986). Surface and in-tracellular distribution of a putative neuronal nicotinic actetylcholine receptor. Journal of Cell Biology 103, 205–214.CrossRefGoogle Scholar
James, W.M. & Klein, W.L. (1985). a-bungarotoxin receptors on neurons isolated from turtle retina: molecular heterogeneity of bipolar cells. Journal of Neuroscience 5, 352–361.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
Karten, H.J., Fite, K.V. & Brecha, N. (1977). Specific projection of displaced retinal ganglion cells upon the accessory optic system in the pigeon Columba livia. Proceedings of the National Academy of Sciences (USA) 74, 1753–1756.CrossRefGoogle Scholar
Karten, H.J., Keyser, K.T., Whiting, P.J. & Lindstrom, J.M. (1987). Nicotinic acetylcholine receptors in the developing and adult avian retina: an immunohistochemical study. Investigative Ophtalmology and Visual Science Suppl. 28, 348.Google Scholar
Large, T.H., Cho, N.J., Demello, F.G. & Klein, W.L. (1985 a). Molecular alteration of a muscarinic acetylcholine receptor system during synaptogenesis. Journal of Biological Chemistry 260, 8873–8881.CrossRefGoogle ScholarPubMed
Large, T.H., Rauh, J.J., Demello, F.G. & Klein, W.L. (1985 b). Two molecular weight forms of muscarinic acetylcholine receptors in the avian central nervous system: switch in predominant form during differentiation of synapses. Proceedings of the National Academy of Sciences (USA) 82, 8785–8789.CrossRefGoogle ScholarPubMed
Lindstrom, J.M. (1986). Probing nicotinic acetylcholine receptors with monoclonal antibodies. Trends in Neuroscience 9, 401–407.CrossRefGoogle Scholar
Lindstrom, J.M., Schoepfer, R. & Whiting, P. (1987). Molecular studies of the neuronal nicotinic acetylcholine receptor family. Molecular Neurbiology 1, 281–337.CrossRefGoogle ScholarPubMed
Ma, P.M. & Grant, P. (1984). Choline acetyltransferase and cho-linesterases in the developing Xenopus retina. Journal of Neurochemistry 42, 1328–1337.CrossRefGoogle ScholarPubMed
Marchisio, A.M., Palomba, M., Mulas, M.L. & Gremo, F. (1985). Heterogeneity of muscarinic cholinergic receptors in the developing chick embryo retina. Brain Research 325, 381–384.CrossRefGoogle ScholarPubMed
Masland, R.H. & Ames, A. (1976). Responses to acetylcholine of ganglion cells in an isolated mammalian retina. Journal of Neurophysiology 32, 424–442.Google Scholar
Masland, R.H. & Mills, J.W. (1979). Autoradiographic identification of acetylcholine in the rabbit retina. Journal of Cell Biology 81, 159–178.CrossRefGoogle Scholar
Masland, R.H., Mills, J.W. & Hayden, S.A. (1984). The functions of acetylcholine in the rabbit retina. Proceedings of the Royal Society (London), Series B 223, 121–139.Google ScholarPubMed
McReynolds, J.S. & Miyachi, E. (1986). The effect of cholinergic agonists and antagonists on ganglion cells in the mudpuppy retina. Neuroscience Research (Suppl.) 4, S153–S161.CrossRefGoogle ScholarPubMed
Millar, T.J., Ishimoto, I., Johnson, C.D., Epstein, M.L., Chubb, l.W. & Morgan, l.G. (1985). Cholinergic and acetylcholinesterase-containing neurons of the chicken retina. Neuroscience Letters 61, 311–316.CrossRefGoogle ScholarPubMed
Millar, T.J. & Morgan, l.G. (1987). Cholinergic amacrine cells in the rabbit retina synapse onto other cholinergic amacrine cells. Neuroscience Letters 74, 281–285.CrossRefGoogle ScholarPubMed
Morley, B.J. & Kemp, G.E. (1981). Characterization of a putative nicotinic acetylcholine receptor in mammalian brain. Brain Research Review 3, 81–104.CrossRefGoogle Scholar
Nelson, R., Famiglietti, E.V. & Kolb, H. (1978). Intracellular staining reveals different levels of stratification for ON- and OFF-center ganglion cells in cat retina. Journal of Neurophysiology 41, 472–484.CrossRefGoogle ScholarPubMed
Nichols, C.W. & Koelle, G.B. (1968). Comparison of the localization of acetylcholinesterase and nonspecific cholinesterase activities in mammalian and avian retinas. Journal of Comparative Neurology 133, 1–15.CrossRefGoogle ScholarPubMed
Noell, W.K. & Lasansky, A. (1959). Effects of electrophoretically applied drugs and electric currents on ganglion cells of the retina. Federation Proceedings 18, 115.Google Scholar
Peichl, L. & Wassle, H. (1981). Morphological identification of ON-and OFF-center brisk transient (Y) cells in the cat retina. Journal of Physiology (London) 212, 139–156.Google Scholar
Polans, A.S., Hutchins, J.B. & Werblin, F.S. (1985). Muscarinic cholinergic receptors in the retina of the larval tiger salamander. Brain Research 340, 355–362.CrossRefGoogle ScholarPubMed
Polyak, S.L. (1942). The Reina. Chicago, Illinois: University of Chicago Press.Google Scholar
Pourcho, R.G. (1979). Localization of cholinergic synapses in mammalian retina with peroxidase-conjugated a-bungarotoxin. Vision Research 19, 287–292.CrossRefGoogle Scholar
Ramon, Y., Cajal, S. (1972). The Structure of the Retina (Thorpe, S.A. & Glickstein, M. trans.) Springfield, Illinois: Charles C. Thomas.Google Scholar
Reiner, A., Brecha, N. & Karten, H.J. (1979). A specific projection of retinal ganglion cells to the nucleus of the basal optic root in the chicken. Neuroscience 4, 1679–1688.CrossRefGoogle Scholar
Sargent, P.B., Pike, S.H., Nadel, D.B. & Lindstrom, J.M. (In press). Nicotinic acetylcholine receptor-like molecules in the retina, retinotectal pathway and optic tectum of the frog. j. Neuroscience.Google Scholar
Spira, A.W., Millar, T.J., Ishimoto, I., Epstein, M.L., Johnson, C.D, Dahl, J.L. & Morgan, l.G. (1987). Localization of choline acetyltransferase-like immunoreactivity in the embryonic chick retina. Journal of Comparative Neurology 260, 526–538.CrossRefGoogle ScholarPubMed
Stell, W.K., Ishida, A. & Lightfoot, D. (1977). Structural basis for ON- and OFF-center responses in retinal bipolar cells. Science 198, 1269–1271.CrossRefGoogle ScholarPubMed
Stollberg, J. & Berg, D.K. (1987). Neuronal acetylcholine receptors: fate of surface and internal pools in cell culture. Journal of Neuroscience, 1809–1815.CrossRefGoogle ScholarPubMed
Straschill, M. (1968). Action of drugs on single neurons in the cat's retina. Vision Research 8, 35–47.CrossRefGoogle Scholar
Straschill, M. & Perwien, J. (1973). The effect of iontophoretically applied acetylcholine upon the cat's retinal ganglion cells. Pflugers Archiv. European Journal of Physiology 339, 289–298.CrossRefGoogle ScholarPubMed
Sugiyama, H., Daniels, M.P. & Nirenberg, M. (1977). Muscarinic acetylcholine receptors of the developing retina. Proceedings of the National Academy of Sciences (USA) 12, 5524–5528.CrossRefGoogle Scholar
Swanson, L.W., Lindstrom, J., Tzartos, S., Schmued, L., 'Leary, D.D. & Cowan, W.M. (1983). Immunohistochemical localization of monoclonal antibodies to the nicotinic acetylcholine receptor in the midbrain of the chick. Proceedings of the National Academy of Sciences (USA) 80, 4532–4536.CrossRefGoogle Scholar
Swanson, L.W., Simmons, D.M., Whiting, P.J. & Lindstrom, J. (1987). Immunohistochemical localization of neuronal nicotinic receptors in the rodent central nervous system. Journal of Neuroscience 7, 3334–3342.CrossRefGoogle ScholarPubMed
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
Tzartos, S., Rand, D., Einarson, B. & Lindstrom, J. (1981). Mapping surface structures of acetylcholine receptor using monoclonal antibodies. Journal of Biological Chemistry 256, 185–194.CrossRefGoogle ScholarPubMed
Tzartos, S., Hochschwender, S., Vasquez, P. & Lindstrom, J. (1987). Passive transfer of experimental autoimmune myesthenia gravis by monoclonal antibodies to the main immunogenic region of the acetylcholine receptor. Journal of Neuroimmunoiogy 15, 185–194.CrossRefGoogle Scholar
Vogel, Z. & Nirenberg, M. (1976). Localization of acetylcholine receptors during synaptogenesis in retina. Proceedings of the National Academy of Sciences (USA) 73, 1806–1810.CrossRefGoogle ScholarPubMed
Vogel, Z., Maloney, G.J., Ling, A. & Daniels, M.P. (1977). Identification of synaptic acetylchoine receptor sites in retina with per-oxidase-labeled a-bungarotoxin. Proceedings of the National Academy of Sciences (USA) 74, 3268–3272.CrossRefGoogle Scholar
Voigt, T. (1986). Cholinergic amacrine cells in the rat retina. Journal of Comparative Neurology 248, 19–35.CrossRefGoogle ScholarPubMed
Watson, J., Adkins-Regan, E., Whiting, P., Lindstrom, J. & Podleski, T. (1988) (in preparation). Autoradiographic determination of the distribution of nicotinic acetylcholine receptors in the zebra finch brain.Google Scholar
Whiting, P. & Lindstrom, J. (1986). Purification and characterization of a nicotinic acetylcholine receptor from chick brain. Biochemistry 25, 2082–2093.CrossRefGoogle ScholarPubMed
Whiting, P. & Lindstrom, J. (1987). Purification and characterization of a nicotinic acetylcholine receptor from rat brain. Proceedings of the National Academy of Sciences (USA) 84, 595–599.CrossRefGoogle ScholarPubMed
Whiting, P. & Lindstrom, J. (1988). Characterization of bovine and human neuronal nicotinic acetylcholine receptors using monoclonal antibodies. Journal of Neuroscience (in press).CrossRefGoogle ScholarPubMed
Whiting, P., Liu, R., Morley, B. & Lindstrom, J. (1987) Structurally different neuronal nicotinic acetylcholine receptor subtypes purified and characterized using monoclonal antibodies. Journal of Neuroscience, 4005–4016.CrossRefGoogle ScholarPubMed
Wunk, D.F. & Werblin, F.S. (1979). Synaptic inputs to the ganglion cells in the tiger salamander retina. Journal of General Physiology 73, 265–286.CrossRefGoogle Scholar
Yazulla, S. (1979). Synaptic layers of the retina: A comparative analysis with (125I)-α-bungarotoxin. In Neural Mechanisms of Behavior in the Pigeon, ed. Granda, A.M. & Maxwell, J.H., pp. 350–370. New York: Plenum Press.Google Scholar
Yazulla, S. & Schmidt, J. (1976). Radioautographic localization of (125I)-α-bungarotoxin binding sites in the retinas of goldfish and turtle. Vision Research 16, 878–880.CrossRefGoogle Scholar
Yazulla, S. & Schmidt, J. (1977). Two types of receptors for bungarotoxin in the synaptic layers of the pigeon retina. Brain Research 138, 45–57.CrossRefGoogle ScholarPubMed
Zucker, C. & Yazulla, S. (1982). Localization of synaptic and non-synaptic nicotinic-acetylcholine receptors in the goldfish retina. Journal of Comparative Neurology 204, 188–195.CrossRefGoogle Scholar
Zimmerman, R.P. & Dowling, J.E. (1979). Functional stratification of the IPL of the mudpuppy retina. Investigative Ophthalmology and Visual Science (Suppl.) 18, 35.Google Scholar