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Enkephalin-immunoreactive ganglion cells in the pigeon retina

Published online by Cambridge University Press:  02 June 2009

Luiz R. G. Britto  and
Dȃnia E. Hamassaki-Britto
Luiz R. G. Britto
Affiliation:
Neurosciences and Behavior Research Nucleus and Department of Physiology and Biophysics, Institute for Biomedical Sciences, University of Sao Paulo, Brazil
Dȃnia E. Hamassaki-Britto
Affiliation:
Neurosciences and Behavior Research Nucleus and Department of Physiology and Biophysics, Institute for Biomedical Sciences, University of Sao Paulo, Brazil
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Abstract

A small number of enkephalin-like immunoreactive cells were observed in the ganglion cell layer of the pigeon retina. Many of these neurons were identified as ganglion cells, since they were retrogradely labeled after injections of fluorescent latex microspheres in the contralateral optic tectum. These ganglion cells were mainly distributed in the inferior retina, and their soma sizes ranged from 12–26 μm in the largest axis. The enkephalin-containing ganglion cells appear to represent only a very small percentage of the ganglion cells projecting to the optic tectum (less than 0.1%). Two to 7 weeks after removal of the neural retina, there was an almost complete elimination of an enkephalin-like immunoreactive plexus in layer 3 of the contralateral, rostrodorsal optic tectum. These data provide evidence for the existence of a population of enkephalinergic retinal ganglion cells with projections to the optic tectum.

Keywords

EnkephalinsNeuropeptidesNeurotransmittersOpioidsOptic tectum
Type
Research Articles
Information
Visual Neuroscience , Volume 9 , Issue 3-4 , October 1992 , pp. 389 - 398
Copyright
Copyright © Cambridge University Press 1992

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References

Adolph, A.R. (1989). Pharmacological actions of peptides and indoleamines on turtle retinal ganglion cells. Visual Neuroscience 3, 411–423.CrossRefGoogle ScholarPubMed
Altschuler, R.A., Mosinger, J.W., Hoffman, D.W. & Parakkal, M.H. (1982). Immunocytochemical localization of enkephalin-like immunoreactivity of the retina of the guinea pig. Proceedings of the National Academy of Sciences of the U.S.A. 79, 2398–2400.Google Scholar
Bayon, A., Koda, L., Battenberg, E., Aarens, R. & Bloom, F.E. (1980). Regional distribution of endorphin, met5-enkephalin and leus-enkephalin in the pigeon brain. Neuroscience Letters 16, 75–80.CrossRefGoogle ScholarPubMed
Blahser, S. & Dubois, M.P. (1980). Immunocytochemical demonstration of met-enkephalin in the central nervous system of the domestic fowl. Cell and Tissue Research 213, 53–68.Google Scholar
Brecha, N. (1983). Retinal neurotransmitters: Histochemical and biochemical studies. In Chemical Neuroanatomy, ed Emson, P.C., pp. 85–129. New York: Raven Press.Google Scholar
Brecha, N.C., Eldred, W., Kuijis, R.O. & Karten, H.J. (1984). Identification and localization of biologically active peptides in the vertebrate retina. In Progress in Retinal Research, Vol. 3, ed. Osborne, N. & Chader, G., pp. 185–226. Oxford: Pergamon Press.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, 155–158.CrossRefGoogle ScholarPubMed
Brecha, N.C. & Karten, H.J. (1985). Localization of biologically active peptides in the retina. In Retinal Transmitters and Modulators: Models for the Brain, Vol. I, ed. Morgan, W.W., pp. 93–118. Boca Raton, Florida: CRC Press.Google Scholar
Brecha, N., Karten, H.J. & Laverack, C. (1979). Enkephalin-containing amacrine cells in the avian retina: Immunohistochemical localization. Proceedings of the National Academy of Sciences of the U.S.A. 76, 3010–3014.Google Scholar
Britto, L.R.G. & Hamassaki, D.E. (1991). A subpopulation of displaced ganglion cells of the pigeon retina exhibits substance P-like immunoreactivity. Brain Research 546, 61–68.Google Scholar
Britto, L.R.G. & Hamassaki-Britto, D.E. (1991). Cholecystokinin-like immunoreactive retinal ganglion cells project to the ventral lateral geniculate nucleus in pigeons. Brain Research 557, 322–326.Google Scholar
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, 109–117.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 nucleus and optic tectum in the pigeon (Columba livia). Visual Neuroscience 3, 477–482.CrossRefGoogle Scholar
Cajal, S.R. (1911). Histologie du Systeme Nerveux, Vol. 2. Paris: Maloine.Google Scholar
Caruso, D.M., Owczarzak, M.T. & Pourcho, R.G. (1990). Colocalization of substance P and GABA in retinal ganglion cells: A computer-assisted visualization. Visual Neuroscience 5, 389–394.CrossRefGoogle ScholarPubMed
Clarke, P.G.H. & Whitteridge, D. (1976). The projection of the retina, including the “red area,” on to the optic tectum of the pigeon. Quarterly Journal of Experimental Physiology 61, 351–358.CrossRefGoogle Scholar
Cuenca, N. & Kolb, H. (1989). Morphology and distribution of neurons immunoreactive for substance P in the turtle retina. Journal of Comparative Neurology 290, 391–411.CrossRefGoogle ScholarPubMed
De Lanerolle, N.C., Elde, R.P., Sparber, S.B. & Fricke, M. (1981). Distribution of methionine-enkephalin immunoreactivity in the chick brain: An immunohistochemical study. Journal of Comparative Neurology 199, 513–533.CrossRefGoogle Scholar
Eberhardt, L. (1967). Some developments in “distance sampling.” Biometrics 23, 207–216.Google Scholar
Ehinger, B., Ottersen, O.P., Storm-Mathisen, J. & Dowling, J.E. (1988). Bipolar cells in the turtle retina are strongly immunoreactive for glutamate. Proceedings of the National Academy of Sciences of the U.S.A. 85, 8321–8325.Google Scholar
Ehrlich, D., Keyser, K.T. & Karten, H.J. (1987). The distribution of substance P-like immunoreactive retinal ganglion cells and their pattern of termination in the optic tectum of chick (Gallus gallus). Journal of Comparative Neurology 266, 220–233.Google Scholar
Ehrlich, D. & Mark, R.F. (1984). Retinal topography of primary visual centres in the brain of the chick (Callus gallus). Journal of Comparative Neurology 223, 611–625.CrossRefGoogle Scholar
Eldred, W.D. & Cheung, K. (1989). Immunocytochemical localization of glycine in the retina of the turtle (Pseudemys scripta). Visual Neuroscience 2, 331–338.Google Scholar
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, 119–132.Google Scholar
Eldred, W. & Karten, H.J. (1984). Characterization and quantification of peptidergic amacrine cells in the turtle retina: Enkephalin, neurotensin and glucagon. Journal of Comparative Neurology 221, 371–378.CrossRefGoogle Scholar
Ferro, E.S., Camargo, A.C.M., Hamassaki, D.E. & Britto, L.R.G. (1991). Endo-oligopeptidase A, a putative enkephalin-synthesizing enzyme, in the vertebrate retina. Journal of Neurochemistry 57, 1643–1649.Google Scholar
Graybiel, A.M., Brecha, N. & Karten, H.J. (1984). Cluster-and-sheet pattern of enkephalin-like immunoreactivity in the superior colliculus of the cat. Neuroscience 12, 191–214.Google Scholar
Hamano, K., Katayama-Kumoi, Y., Kiyama, H., Ishimoto, I., Manabe, R. & Tohyama, M. (1989). Coexistence of enkephalin and somatostatin in the chicken retina. Brain Research 489, 254–260.CrossRefGoogle ScholarPubMed
Hayes, B.P. (1982). The structural organization of the pigeon retina. In Progress in Retinal Research, Vol. I, ed. Osborne, N. & Chader, C., pp. 197–226. Oxford: Pergamon Press.Google Scholar
Hurd, L.B. & Eldred, W.D. (1989). Localization of GABA- and GAD-like immunoreactivity in the turtle retina. Visual Neuroscience 3, 9–20.CrossRefGoogle ScholarPubMed
Isayama, T., McLaughlin, P.J. & Zagon, I.S. (1991). Endogenous opioids regulate cell proliferation in the retina of the developing rat. Brain Research 544, 79–85.CrossRefGoogle ScholarPubMed
Kageyama, G.H. & Meyer, R.L. (1989). Glutamate immunoreactivity in the retinal and optic tectum of goldfish. Brain Research 503, 118–127.Google Scholar
Karten, H.J., Keyser, K.T. & Brecha, N.C. (1990). Biochemical and morphological heterogeneity of retinal ganglion cells. In Vision and the Brain: The Organization of the Central Visual System, ed. Cohen, B. & Bodis-Wollner, I., pp. 19–34. New York: Raven Press.Google Scholar
Karten, H.J., Reiner, A. & Brecha, N. (1982). Laminar organization and origins of neuropeptides in the avian retina and optic tectum. In Cytochemical Methods in Neuroanatomy, ed. Palay, S.L. & Chan-Palay, V., pp. 189–204. New York: Alan R. Liss.Google Scholar
Katz, L.C., Burkhalter, A. & Dreyer, W.J. (1984). Fluorescent latex microspheres as a retrograde neuronal marker for in vivo and in vitro studies of visual cortex. Nature 310, 498–500.Google Scholar
Katz, L.C. & Iarovici, D.M. (1990). Green fluorescent latex microspheres: A new retrograde tracer. Neuroscience 34, 511–520.Google Scholar
Keyser, K.T., Britto, L.R.G., Woo, J-I., Park, D.H., Joh, T.H. & Karten, H.J. (1990). Presumptive catecholaminergic ganglion cells in the pigeon retina. Visual Neuroscience 4, 225–235.Google Scholar
Keyser, K.T., Karten, H.J. & Ehriich, D. (1988). “Bullwhip” association amacrine cells in the pigeon retina: Morphology and histochemical heterogeneity. Investigative Ophthalmology and Visual Sciences (Supl.) 29, 196.Google Scholar
Kuljis, R.O. & Karten, H.J. (1983). Modifications in the laminar organization of peptide-like immunoreactivity in the anuran optic tectum following retinal deafferentation. Journal of Comparative Neurology 217, 239–251.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, 5736–5740.CrossRefGoogle ScholarPubMed
Kuljis, R.O. & Karten, H.J. (1988). Neuroactive peptides as markers of retinal ganglion cell populations that differ in anatomical organization and function. Visual Neuroscience 1, 73–81.Google Scholar
Kuljis, R.O., Krause, J.E. & Karten, H.J. (1984). Peptide-like immunoreactivity in anuran optic nerve fibers. Journal of Comparative Neurology 226, 222–237.Google Scholar
Li, H.-B., Watt, C.B. & Lam, D.M.-K. (1990). Double-label analyses of somatostatin's coexistence with enkephalin and gamma-aminobutyric acid in amacrine cells of the chicken retina. Brain Research 525, 304–309.Google 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.Google Scholar
Massey, S.C. (1990). Cell types using glutamate as a neurotransmitter in the vertebrate retina. In Progress in Retinal Research, Vol. 9, ed. Osborne, N. & Chader, G., pp. 399–425. Oxford: Pergamon Press.Google Scholar
McGill, J.I., Powell, T.P.S. & Cowan, W.M. (1966). The retinal representation upon the optic tectum and the isthmo-optic nucleus in the pigeon. Journal of Anatomy 100, 5–33.Google Scholar
Miguel-Hidalgo, J.J., Senba, E., Takatsuji, K. & Tohyama, M. (1990). Substance P and enkephalins in the superficial layers of the rat superior colliculus: Differential plastic effects of retinal deafferentation. Journal of Comparative Neurology 299, 389–404.CrossRefGoogle ScholarPubMed
Mize, R.R. (1989). Enkephalin-like immunoreactivity in the cat superior colliculus: Distribution, ultrastructure, and colocalization with GABA. Journal of Comparative Neurology 285, 133–155.Google Scholar
Ramon, P. (1898). Centros opticos de las aves. Revista Trimestral Micrografica 4, 141–197.Google Scholar
Reiner, A., Brauth, S.E., Kitt, C.A. & Quirion, R. (1989). Distribution of mu, delta and kappa opiate receptor types in the forebrain and midbrain of pigeons. Journal of Comparative Neurology 280, 359–382.CrossRefGoogle ScholarPubMed
Reiner, A., Karten, H.J. & Brecha, N.C. (1982). Enkephalin-mediated basal ganglia influences over the optic tectum: Immunohistochemistry of the tectum and the lateral spiriform nucleus in pigeon. Journal of Comparative Neurology 208, 37–53.CrossRefGoogle ScholarPubMed
Sandell, J.H. & Masland, R.H. (1989). Shape and distribution of an unusual retinal neuron. Journal of Comparative Neurology 280, 489–497.CrossRefGoogle ScholarPubMed
Studholme, K.M., Yazulla, S. & Phillips, C.J. (1987). Interspecific comparisons of immunohistochemical localization of retinal neurotransmitters in four species of bats. Brain, Behavior, and Evolution 30, 160–173.Google Scholar
Su, Y.-Y.T., Fry, K.R., Lam, D.M.-K. & Watt, C.B. (1986). Enkephalin in the goldfish retina. Cellular and Molecular Neurobiology 6, 331–347.CrossRefGoogle ScholarPubMed
Su, Y.-Y. & Watt, C.B. (1987). Interaction between enkephalin and dopamine in the avian retina. Brain Research 423, 63–70.Google ScholarPubMed
Su, Y.-Y.T., Watt, C.B. & Lam, D.M.-K. (1985). Opioid pathways in an avian retina. I. The content, biosynthesis, and release of Met5-enkephalin. Journal of Neuroscience 5, 851–856.Google Scholar
Van Haesendonck, E. & Missotten, L. (1990). Glutamate-like immunoreactivity in the retina of a marine teleost, the dragonet. Neuroscience Letters 111, 281–286.Google Scholar
Wässle, H. & Riemann, H.J. (1978). The mosaic of nerve cells in the mammalian retina. Proceedings of the Royal Society B (London) 200, 441–460.Google ScholarPubMed
Watt, C.B. (1989). Synaptic organizations of enkephalinlike-immunoreactive amacrine cells in the goldfish retina. Journal of Comparative Neurology 283, 333–341.Google Scholar
Watt, C.B. (1991). A re-examination of enkephalins coexistence with gamma-aminobutyric acid in amacrine cells of the larval tiger salamander retina. Brain Research 551, 351–354.Google Scholar
Watt, C.B., Li, T., Lam, D.M.K. & Wu, S.M. (1987). Interactions between enkephalin and γ-aminobutyric acid in the larval tiger salamander retina. Brain Research 408, 258–262.Google Scholar
Watt, C.B., Li, T., Lam, D.M.K. & Wu, S.M. (1988). Quantitative studies of enkephalin's coexistence with γ-aminobutyric acid, glycine and neurotensin in amacrine cells of the chicken retina. Brain Research 444, 366–370.Google Scholar
Watt, C.B., Su, Y.-Y.T. & Lam, D.M.-K. (1984). Interactions between enkephalin and GABA in avian retina. Nature 311, 761–763.Google Scholar
Watt, C.B., Su, Y.-Y.T. & Lam, D.M.-K. (1985a). Opioid pathways in an avian retina. II. Synaptic organization of enkephalin-immunoreactive amacrine cells. Journal of Neuroscience 5, 857–865.Google Scholar
Watt, C.B., Su, Y.-Y.T. & Lam, D.M.-K. (1985b). Enkephalins in the vertebrate retina. In Progress in Retinal Research, Vol. 4, ed. Osborne, N. & Chader, G., pp. 221–242. Oxford: Pergamon Press.Google Scholar
Weiler, R. & Ammermuller, J. (1986). lmmunocytochemical localization of serotonin in intracellularly analyzed and dye-injected ganglion cells of the turtle retina. Neuroscience Letters 72, 147–152.CrossRefGoogle Scholar
Weiler, R. & Ball, A.K. (1989). Enkephalinergic modulation of the dopamine system in the turtle retina. Visual Neuroscience 3, 455–461.CrossRefGoogle ScholarPubMed
White, C.A., Chalupa, L.M., Johnson, D. & Brecha, N.C. (1990). Somatostatin-immunoreactive cells in the adult cat retina. Journal of Comparative Neurology 293, 134–150.Google Scholar
Williamson, D.E. & Eldred, W.D. (1989). Amacrine and ganglion cells with corticotropin-releasing-factor-like immunoreactivity in the turtle retina. Journal of Comparative Neurology 280, 424–435.Google Scholar
Yang, C.-Y. & Yazulla, S. (1988a). Light microscopic localization of putative glycinergic neurons in the larval tiger salamander retina by immunocytochemical and autoradiographical methods. Journal of Comparative Neurology 272, 343–357.Google Scholar
Yang, C.-Y. & Yazulla, S. (1988b). Localization of putative GABAergic neurons in the larval tiger salamander retina by immunocytochemical and autoradiographic methods. Journal of Comparative Neurology 277, 96–108.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, 376–382.Google Scholar