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Presumptive catecholaminergic ganglion cells in the pigeon retina

Published online by Cambridge University Press:  02 June 2009

Kent T. Keyser
Affiliation:
Department of Neurosciences, University of California, San Diego, La Jolla
Luiz R. G. Britto
Affiliation:
Department of Physiology and Biophysics, Institute of Biomedical Sciences, Sao Paulo State University, 05508 Sao Paulo, SP, Brazil
Jong-Inn Woo
Affiliation:
Laboratory of Molecular Neurobiology, Cornell University Medical College, Burke Rehabilitation Center, White Plains
Dong H. Park
Affiliation:
Laboratory of Molecular Neurobiology, Cornell University Medical College, Burke Rehabilitation Center, White Plains
Tung H. Joh
Affiliation:
Laboratory of Molecular Neurobiology, Cornell University Medical College, Burke Rehabilitation Center, White Plains
Harvery J. Karten
Affiliation:
Department of Neurosciences, University of California, San Diego, La Jolla

Abstract

An antiserum directed against tyrosine hydroxylase (TH), the rate-limiting enzyme in the synthesis of dopamine, was used to study the pigeon retina. Labeled cells were observed in both the inner nuclear layer (INL) and ganglion cell layer (GCL). Two populations of TH-immunoreactive neurons were observed in the INL. Some of these cells were 7−10 μ in diameter and gave rise to processes that arborized in three Layers of the inner plexiform layer (IPL). These cells appeared similar to the dopaminergic amacrine cells described previously (Marc, 1988). Other labeled cells in the INL were 12−20 μ in diameter and were recognizable as a previously described subpopulation of TH-immunoreactive displaced ganglion cells (Britto et al., 1988).

A population of labeled cells was observed in the GCL. Counts of these cells in two retinae revealed 5000 and 7000 cells, respectively. They ranged in size from 8−15 μ in diameter in the central retina and from 8−20 m in diameter in the peripheral retina. The density of labeled cells was highest in the central retina and red field and lowest in the retinal periphery. The difference in cell size and cell density as a function of eccentricity is characteristic of the total population of ganglion cells in the avian retina (Ehrlich, 1981; Hayes, 1982). Some of the TH-positive cells in the GCL could be classified as ganglion cells for two reasons: (1) The axons of many of the TH-positive cells in the GCL were TH-immunoreactive as well and could be followed to the optic nerve head. (2) The injection of rhodamine-labeled microspheres into the nucleus geniculatus lateralis, pars ventralis (GLv), resulted in the retrograde labeling of many of the TH-positive cells in the contralateral retina.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1990

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References

Anderson, K.J., Borja, M.A., Cotman, C.W., Moffett, J.R., Namboodiri, M.A.A. & Neale, J.H. (1987). N-acetylaspartylglutamate identified in the rat retinal ganglion cells and their projections to the brain. Brain Research 411, 172177.CrossRefGoogle ScholarPubMed
Baughman, R.W. & Bader, C.R. (1977). Biochemical characterization of the cholinergic system in the chicken retina. Brain Research 138, 469485.CrossRefGoogle ScholarPubMed
Beaudet, A., Burkhalter, A., Reubi, J.C. & Cuenod, M. (1981). Selective bidirectional transport of [3H\-aspartate in the pigeon retinotectal pathway. Neuroscience 6, 20212034.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
Britto, L.R.G., Keyser, K.T., Hamassaki, D.E., & Karten, H.J. (1988). Catecholaminergic subpopulation of retinal displaced ganglion cells projects to the accessory optic nucleus in the pigeon (Columba livia). Journal of Comparative Neurology 269, 109117.CrossRefGoogle Scholar
Britto, L.R.G., Keyser, K.T., Hamassaki, D.E. & Shimizu, T. & Karten, H.J. (1989). Chemically specific retinal ganglion cells collateralize to the pars ventralis of the lateral geniculate and optic tectum in the pigeon (Columba livia). Visual Neuroscience 3, 477482.CrossRefGoogle Scholar
Brunken, W.J., Witovsky, P. & Karten, H.J. (1986). Retinal neurochemistry of three elasmobranch species: an immunohistochemical approach. Journal of Comparative Neurology 243, 112.CrossRefGoogle ScholarPubMed
Cohen, J. & Hadjiconstantinou, M. (1984). Identification of epinephrine and phenylethanolamine N-methyltransferase activity in rat retina. Proceedings of the Federation of American Societies for Experimental Biology 43, 27252728.Google ScholarPubMed
Cowan, W.M., Adamson, L. & Powell, T.P.S. (1961). An experimental study of the avian visual system. Journal of Anatomy 95, 545563.Google Scholar
Da, Prada M. (1977). Dopamine content and synthesis in retina and N. accumbens septi: pharmacological and light-induced modifications. In Advances in Biochemical Psychopharmacology, Vol. 16: Nonstriatal Dopaminergic Neurons, ed. Costa, E. & Gessa, G.L., pp. 311319. New York: Raven Press.Google Scholar
Daw, N.W., Brunken, W.J. & Parkinson, D. (1989). The function of synaptic transmitters in the retina. Annual Review of Neuroscience 12, 205225.CrossRefGoogle ScholarPubMed
Dowling, J.E. & Ehinger, B. (1975). Synaptic organization of the amine-containing interplexiform cells of the goldfish and Cebus monkey retinas. Science 188, 270273.Google Scholar
Dowling, J.E. & Ehinger, B. (1978). The interplexiform cell system, I: Synapses of the dopaminergic neurons of the goldfish retina. Proceedings of the Royal Society B (London) 201, 726.Google Scholar
Dowling, J.E. & Ehinger, B. & Hedden, W.L. (1976). The interplexiform cell: a new type of retinal neuron. Investigative Ophthalmology 15, 916926.Google Scholar
Ehinger, B. (1966). Adrenergic retinal neurons. Zeitschrift fϜr Zellforschung Mikroskopic Anatomy 71, 146152.CrossRefGoogle Scholar
Ehinger, B., Falck, B. & Laties, A.M. (1969). Adrenergic neurons inteleost retina. Zeitschrift fϜr Zellforschung Mikroskopic Anatomy 97, 285297.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, 643657.Google Scholar
Ehrlich, D. & Marc, R.E. (1984). Retinal topography of primary visual centres in the brain of the chick. Journal of Comparative Neurology 223, 611625.CrossRefGoogle ScholarPubMed
Ehrlich, D., Keyser, K.T. & Karten, H.J. (1987). Distribution of substance P-like immunoreactive retinal ganglion cells and their pattern of termination in the optic tectum of chick (Gallusgallus). Journal of Comparative Neurology 266, 220233.CrossRefGoogle Scholar
Eldred, W.D. & Cheung, K. (1989). Immunocytochemical localization of glycine in the retina of the turtle (Pseudemys scripta). Visual Neuroscience 2, 331338.CrossRefGoogle ScholarPubMed
Eldred, W.D., Isayama, T., Reiner, A. & Carraway, R. (1988). Ganglion cells in the turtle retina contain the neuropeptide LANT-6. Journal of Neuroscience 8, 119132.Google Scholar
Foster, G.A., Hokfelt, T., Coyle, J.T. & Goldstein, M. (1985). Immunohistochemical evidence for Phenylethanolamine-N-methyltransferase-positive/tyrosine hydroxylase-negative neurons in the retina and the posterior hypothalamus of the rat. Brain Research 330, 183188.CrossRefGoogle ScholarPubMed
Frederick, J.M., Rayborn, M.E., Laties, A.M., Lam, D.M.K. & Hollyfield, J.G. (1982). Dopaminergic neurons in the human retina. Journal of Comparative Neurology 210, 6579.CrossRefGoogle ScholarPubMed
Gamlin, P.D. & Cohen, D.H. (1988). Projections of the retino-recipient pretectal nuclei in the pigeon (Columba livia). Journal of Comparative Neurology 269, 1846.CrossRefGoogle ScholarPubMed
Guiloff, G.D., Maturana, H.R. & Varela, F.J. (1987). Cytoarchitecture of the avian ventral lateral geniculate nucleus. Journal of Comparative Neurology 264, 509526.CrossRefGoogle ScholarPubMed
Hadjiconstantinou, M., Mariani, A.P., Panula, P., Joh, T.H. & Neff, N.H. (1984). Immunohistochemical evidence for epinephrinecontaining retinal amacrine cells. Neuroscience 13, 547551.CrossRefGoogle ScholarPubMed
Hale, P.T. & Sefton, A.J. (1978). A comparison of the visual and electrical response properties of cells in the dorsal and ventral lateral geniculate nuclei. Brain Research 153, 591595.CrossRefGoogle ScholarPubMed
Hayes, B.P. (1982). The structural organization of the pigeon retina. Progress in Retinal Research 1, 197226.CrossRefGoogle Scholar
Hokfelt, T., Foster, G., Coyle, J. & Goldstein, M. (1985). Immunohistochemical evidence for PNMT-positive/TH-negative cells in the retina and posterior hypothalamus. Brain Research 330, 183188.Google Scholar
Hollander, H., Egensperger, R. & Dirlich, G. (1989). Size distribution of rhodamine-labeled microspheres retrogradely transported in cultured neurons. Journal of Neuroscience Methods 29, 14.CrossRefGoogle Scholar
Hughes, C.P. & Chi, D.Y.K. (1983). Visual function in the ventral lateral geniculate nucleus of the cat. Experimental Neurology 79, 611621.CrossRefGoogle ScholarPubMed
Jensen, R.J. & Daw, N.W. (1984). Effects of dopamine antagonists on receptive fields of brisk cells and directionally selective cells in the rabbit retina. Journal of Neuroscience 4, 29722985.Google Scholar
Jones, E.G. (1985). The Thalamus. New York: Plenum Press.Google Scholar
Karten, H.J. & Hodos, W. (1967). A Stereotactic Atlas of the Brainof the Pigeon (Columba livia). Baltimore, Maryland: Johns Hopkins Press.Google Scholar
Karten, H.J., Hodos, W., Nauta, W.J.H. & Revzin, A.M. (1973). Neural connections of the “visual wulst” of the avian telencephalon. Experimental studies in the pigeon (Columba livia) and owl (Speotyto cunicularia). Journal of Comparative Neurology 150, 253277.CrossRefGoogle ScholarPubMed
Kalz, L.C., Burkhalter, A. & Dreyer, W.J. (1984). Fluorescent latex microspheres as a retrograde marker for in vivo and in vitro studies of visual cortex. Nature 310, 498500.Google Scholar
Kemp, J.A. & Sollito, A.M. (1982). The nature of the excitatory transmitter mediating X and Y cells inputs to the cat dorsal lateral geniculate nucleus. Journal of Physiology 323, 377391.Google Scholar
Keyser, K.T., Karten, H.J., Katz, B. & Bohn, M.C. (1987). Catecholaminergic horizontal and amacrine cells in the ferret retina. Journal of Neuroscience 7, 39964004.Google Scholar
Kramer, S.G. (1971). Dopamine: a retinal neurotransmitter, I: Retinal uptake, storage, and light-stimulated release of [H3\-dopamine in the retina. Investigative Ophthalmology 10, 617624.Google ScholarPubMed
Kuljis, R.O. & Karten, H.J. (1983). Modifications in the laminar organization of peptide-like immunoreactivity in the anuran optic tecturm following retinal deafferentation. Journal of Comparative Neurology 217, 239251.Google Scholar
Kuljis, R.O. & Karten, H.J. (1986). Substance P-containing ganglion cells become progressively less detectable during retinotectal development in the frog (Rana pipiens). Proceedings of the National Academy of Sciences of the U.S.A. 83, 57365740.CrossRefGoogle ScholarPubMed
Marc, R.E. (1988). Neurochemical stratification in the inner plexiform layer of the vertebrate retina. Vision Research 26, 223238.Google Scholar
Mariani, A.P. & HoKoc, J.N. (1988). Two types of tyrosine hydroxylase-immunoreactive amacrine cell in the rhesus monkey retina. Journal of Comparative Neurology 276,8191.Google Scholar
Massey, S.C. & Redburn, D.A. (1987). Transmitter circuits in the vertebrate retina. Progress in Neurobiology 28, 5596.CrossRefGoogle ScholarPubMed
Maturana, H.R. & Varela, F.J. (1982). Color-opponent responses in the avian lateral geniculate: a study in the quail (Coturnix coturnix japonica). Brain Research 247, 227241.Google Scholar
Millar, T.J., Ishimoto, I., Johnson, C.D., Epstein, M.L., Chubb, I.W. & Morgan, I.G. (1985). Cholinergic and acetyl cholinesterasecontaining neurons of the chicken retina. Neuroscience Letters 61, 311316.Google Scholar
Millar, T.J., Ishimoto, I., Chubb, I.W., Epstein, M.L., Johnson, C.D. & Morgan, I.G.. (1987 a). Cholinergic amacrine cells of the chicken retina: a light and electron-microscope study. Neuroscience 21, 725743.Google Scholar
Millar, T.J., Ishimoto, I., Boelen, M., Epstein, M.L., Johnson, C.D. & Morgan, I.G.. (1987 b). The toxic effects of ethylcholine mustard aziridinium ion on cholinergic cells in the chicken retina. Journal of Neuroscience 7, 343356.CrossRefGoogle ScholarPubMed
Mitrofanis, J., Vigny, A. & Sotne, J. (1988). Distribution of catecholaminergic cells in the retina of the rat, guinea pig, cat, and rabbit: independence from ganglion cell distribution. Journal of Comparative Neurology 267, 114.Google Scholar
Negishi, K., Kato, S., Teranishi, T., Kiyama, H., Katayama, V. & Tohyama, M. (1985). So-called interplexiform cells immunoreactive to tyrosine hydroxylase or somatostatin in rat retina. Brain Research 346, 136140.Google Scholar
O'leary, J.L. (1940). A structural analysis of the lateral geniculate nucleus of the cat. Journal of Comparative Neurology 73, 405430.Google Scholar
Osborne, N.N. & Nesselhut, T. (1983). Adrenaline: occurrence in the bovine retina. Neuroscience Letters 39, 3336.CrossRefGoogle ScholarPubMed
Oyster, C.W., Takahashi, E.S., Cilluffo, M. & Brecha, N. (1985). Morphology and distribution of tyrosine hydroxylase-like immunoreactive neurons in the cat retina. Proceedings of the National Academy of Sciences of the U.S.A. 82, 63356339.CrossRefGoogle ScholarPubMed
Park, D.H., Teitelman, G., Evinger, M.J., Woo, J.l., Ruggiero, D.A., Albert, V.R., Baetge, E.E., Pickel, V.M., Reis, D.J. & Joh, T.H. (1986). Phenyl ethanolamine N-methyltransferase-containing neurons in rat retina: immunohistochemistry, immunochemistry, and molecular biology. Journal of Neuroscience 6, 11081113.Google Scholar
Reiner, A. & Karten, H.J. (1982). Laminar distribution of the cells of origin of the descending tectofugal pathways in the bird. Journal of Comparative Neurology 204, 165187.CrossRefGoogle Scholar
Reperant, J. (1973). Nouvelles donnees sur les projections visuelles chez le pigeon. Journal fϜr Hirnforschung 14, 151186.Google Scholar
Rickman, D., Johnson, D., Sharma, S. & Brecha, N. (1986). Distribution of substance P and somatostatin immunoreactive cells in the rabbit retina. Society for Neuroscience Abstracts 12, 641.Google Scholar
Ritchie, T.C. & Leonard, R.B. (1983). Immunocytochemical demonstration of serotoninergic neurons and processes in the retina and optic nerve of the stingray (Dasyatis sabina). Brain Research 267, 352356.CrossRefGoogle ScholarPubMed
Spear, P.D., Smith, D.C. & Williams, L.L. (1977). Visual receptive- field properties of single neurons in cat's ventral-lateral geniculate nucleus. Journal of Neurophysiology 40, 390409.CrossRefGoogle ScholarPubMed
Sumitomo, I., Sugitani, M., Fukuda, Y. & Iwama, K. (1979). Properties of cells responding to visual stimuli in the rat ventral lateral geniculate nucleus. Experimental Neurology 66, 721736.CrossRefGoogle ScholarPubMed
Tieman, S.B., Cangro, C.B. & Neale, J.H. (1987 a). N-acetyl aspartylglutamate immunoreactivity in neurons of the cat's visual system. Brain Research 420, 188193.CrossRefGoogle Scholar
Tieman, S.B., Hamilton, C.R., Vermeire, B.A., Namboodiri, M.A.A. & Neale, J.H. (1987 b). N-acetyl aspartylglutamate immunoreactivity in neurons of the monkey's visual pathway. Society for Neuroscience Abstracts 13, 992.Google Scholar
Versaux-Botteri, C., Martin-Martinelli, E., Nguyen-Legros, J., Geffard, M., Vigny, A. & Denoroy, L. (1986). Regional specialization of the rat retina: catecholamine-containing amacrine cell characterization and distribution. Journal of Comparative Neurology 243, 422433.CrossRefGoogle ScholarPubMed
Voigt, T. & Wässle, H. (1987). Dopaminergic innervation of All amacrine cells in the mammalian retina. Journal of Neuroscience 7, 41154128.Google Scholar
Wässle, H., Voigt, T., Schmidt, M. & Humphrey, M. (1986). Action and localization of neurotransmitters in the cat retina. Neuroscience Research (Suppl.) 4, S181S195.CrossRefGoogle ScholarPubMed
Watling, K.J. & Iversen, L.L. (1981). Comparison of the binding of [3H\-spiperone and [3H\-domperidone in homogenates of mammalian retina and caudate nucleus. Journal of Neurochemistry 37, 11301143.CrossRefGoogle Scholar
Weller, R. & Ammermuller, J. (1987). Immunocytochemical localization of serotonin in intracellularly analyzed and dye-injected ganglion cells in the turtle retina. Neuroscience Letters 72, 147152.Google Scholar
Yu, B.C., Watt, C.B., Lam, D.M. & Fry, K.R. (1988). GABAergic ganglion cells in the rabbit retina. Brain Research 439, 376382.CrossRefGoogle ScholarPubMed