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Colocalization of glycine in substance P-amacrine cells of the larval tiger salamander retina

Published online by Cambridge University Press:  02 June 2009

Carl B. Watt  and
Valarie J. Florack
Carl B. Watt
Affiliation:
Alice R. McPherson Laboratory of Retina Research, Center for Biotechnology, Baylor College of Medicine, The Woodlands
Valarie J. Florack
Affiliation:
Alice R. McPherson Laboratory of Retina Research, Center for Biotechnology, Baylor College of Medicine, The Woodlands
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Abstract

The present study was performed as part of a systematic examination of glycine's coexistence with other classical transmitters and neuropeptides in neuronal populations of the larval tiger salamander retina. Substance P immunocytochemistry was combined with either glycine immunocytochemistry or autoradiography of glycine high-affinity uptake to examine whether tiger salamander substance P-amacrine cells express these glycine markers. Double-label analyses revealed two populations of substance P-amacrine cells that express glycine immunoreactivity and glycine high-affinity uptake. The large majority of double-labeled cells were situated in the innermost cell row of the inner nuclear layer, while a smaller number were located in the inner nuclear layer in the second cell row distal to the inner plexiform layer. Double-label immunocytochemistry revealed that these double-labeled cells accounted for 91.7% of substance P-immunoreactive amacrine cells. A slightly lower percentage (90.1%) of substance P-amacrine cells were found to exhibit a glycine high-affinity uptake mechanism. Substance P-amacrine cells that did not co-label for markers of glycine activity were situated in the innermost cell row of the inner nuclear layer. Substance P-immunoreactive displaced amacrine cells were not observed to co-label for either glycine immunoreactivity or glycine high-affinity uptake.

The present study reveals that the large majority of substance P-amacrine cells in the larval tiger salamander retina co-express markers of glycine activity. This finding suggests a functional diversity in the population of tiger salamander substance P-amacrine cells relative to their coexisting relationship with a major inhibitory neurotransmitter.

Keywords

GABANeuropeptidesClassical transmittersCoexistenceImmunocytochemistryAutoradiography
Type
Research Articles
Information
Visual Neuroscience , Volume 10 , Issue 5 , September 1993 , pp. 899 - 906
Copyright
Copyright © Cambridge University Press 1993

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References

Brecha, N., Johnson, D., Peichl, L. & Wässle, H. (1988). Cholinergic amacrine cells of the rabbit retina contain glutamate decarboxylase and gamma-aminobutyrate immunoreactivity. Proceedings of the National Academy of Sciences of the U.S.A. 85, 6187–6191.CrossRefGoogle ScholarPubMed
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
Davanger, S., Ottersen, O.P. & Storm-Mathisen, J. (1991). Glutamate, GABA, and glycine in the human retina: An immunohisto-chemical investigation. Journal of Comparative Neurology 311 483–494.CrossRefGoogle Scholar
Dick, E. & Miller, R.F. (1981). Peptides influence retinal ganglion cells. Neuroscience Letters 26, 131–135.CrossRefGoogle ScholarPubMed
Glickman, R.D., Adolph, A.R. & Dowling, J.E. (1982). Inner plexi-form circuits in the carp retina: Effects of cholinergic agonists, GABA, and substance P on the ganglion cells. Brain Research 234, 81–99.CrossRefGoogle Scholar
Hokfelt, T., Holets, V.R., Staines, W., Meister, B., Melander, T., Schalling, M., Schultzberg, M., Freedman, J., Bjorklund, H., Olson, L., Lindh, B., Elfvin, L.G., Lundberg, J.M., Lindgren, J.A., Samuelsson, B., Pernow, B., Terenius, L., Post, C, Everitt, B. & Goldstein, M. (1986). Coexistence of neuronal messengers: An overview. In Progress in Brain Research, Vol. 68, ed. Hokfelt, T., Fuxe, K. & Pernow, B., pp. 33–70. Berlin: Elsevier Science Publisher.CrossRefGoogle Scholar
Katayama-Kumoi, Y., Kiyama, H., Manabe, R., Shatani, Y. & Tohyama, M. (1985 a). Coexistence of glucagon- and substance P-like immunoreactivity in the chicken retina. Neuroscience 16, 417–424.CrossRefGoogle ScholarPubMed
Katayama-Kumoi, Y., Kiyama, H., Emson, P.C., Kimmel, J.R. & Tohyama, M. (1985 b). Coexistence of pancreatic polypeptide and substance P in the chicken retina. Brain Research 361, 25–35.CrossRefGoogle ScholarPubMed
Kosaka, T., Tauchi, M. & Dahl, J.L. (1988). Cholinergic amacrine cells containing GABA-like and/or glutamic acid decarboxylase-like immunoreactivities in various brain regions of the rat. Experimental Brain Research 70, 605–617.CrossRefGoogle ScholarPubMed
Lasansky, A. (1973). Organization of the outer synaptic layer in the retina of the larval tiger retina. Philosophical Transactions of the Royal Society B (London) 265, 471–489.Google ScholarPubMed
Li, H.B., Watt, C.B. & Lam, D.M.K. (1986 a). The light-microscopic localization of substance P- and somatostatin-like immunoreactive cells in the larval tiger salamander retina. Experimental Brain Research 63, 93–101.CrossRefGoogle ScholarPubMed
Li, H.B., Marshak, D.W., Dowling, J.E. & Lam, D.M.K. (1986 b). Colocalization of immunoreactive substance P and neurotensin in amacrine cells of the goldfish retina. Brain Research 366, 307–313.Google ScholarPubMed
Li, T., Wu, S.M., Lam, D.M.K. & Watt, C.B. (1990). Localization of classical neurotransmitters in interneurons of the larval tiger salamander retina. Investigative Ophthalmology and Visual Science 31, 262–271.Google ScholarPubMed
Lukasiewicz, P.D. & Werblin, F.S. (1990). The spatial distribution of excitatory and inhibitory inputs to ganglion cell dendrites in the tiger salamander retina. Journal of Neuroscience 10, 210–221.CrossRefGoogle ScholarPubMed
Marc, R.E. (1985). The role of glycine in retinal circuitry. In Retinal Transmitters and Modulators: Model for the Brain, ed. Morgan, W., pp. 120–158. Boca Raton, Florida: CRC Press.Google Scholar
Marc, R.E. (1989). The role of glycine in the mammalian retina. In Progress in Retinal Research, Vol. 8, ed. Osborne, N.N. & Chader, G.J., pp. 67–107. Oxford: Pergamon Press.Google Scholar
O'Malley, D.M., Sandell, J.H. & Masland, R.H. (1992). Co-release of acetylcholine and GABA by starburst amacrine cells. Journal of Neuroscience 12, 1394–1408.CrossRefGoogle ScholarPubMed
Pourcho, R.G. & Goebel, D.J. (1988). Colocalization of substance P and gamma-aminobutyric acid in amacrine cells of the cat retina. Brain Research 447, 164–167.CrossRefGoogle ScholarPubMed
Pourcho, R.G. & Owczarzak, M.T. (1991). Connectivity of glycine-immunoreactive amacrine cells in the cat retina. Journal of Comparative Neurology 307, 549–561.CrossRefGoogle ScholarPubMed
Vaney, D.I. & Young, H.M. (1988). GABA-like immunoreactivity in cholinergic amacrine cells of the rabbit retina. Brain Research 438, 369–373.CrossRefGoogle ScholarPubMed
Vaney, D.I., Whitington, G.E. & Young, H.M. (1989). The morphology and topographic distribution of substance P-like immunoreactive amacrine cells in the cat retina. Proceeding of the Royal Society B (London) 237, 471–488.Google ScholarPubMed
Vaney, D.I. (1990). The mosaic of amacrine cells in the mammalian retina. In Progress in Retinal Research, Vol. 9, ed. Osborne, N.N. & Chader, G.J., pp. 1–46. Oxford: Pergamon Press.Google Scholar
Watt, C.B., Su, Y.Y.T. & Lam, D.M.K. (1984). Interactions between enkephalin and GABA in the avian retina. Nature 311, 761–763.CrossRefGoogle ScholarPubMed
Watt, C.B., Li, H.B., Fry, K.R. & Lam, D.M.K. (1985 a). Localization of enkephalin-like immunoreactive amacrine cells in the larval tiger salamander retina. Journal of Comparative Neurology 241, 172–179.Google ScholarPubMed
Watt, C.B., Su, Y.Y.T. & Lam, D.M.K. (1985 b). The presence of three neuroactive peptides in putative glycinergic amacrine cells of the chicken retina. Brain Research 348, 187–191.CrossRefGoogle Scholar
Watt, C.B., Li, T., Wu, S.M. & Lam, D.M.K. (1987). Interactions between enkephalin and gamma-aminobutyric acid in the larval tiger salamander retina. Brain Research 408, 258–262.CrossRefGoogle ScholarPubMed
Watt, C.B., Yang, S.Z., Lam, D.M.K. & Wu, S.M. (1988). Localization of tyrosine hydroxylase-like immunoreactive amacrine cells in the larval tiger salamander retina. Journal of Comparative Neurology 272, 114–126.CrossRefGoogle ScholarPubMed
Watt, C.B. & Lam, D.M.K. (1989). Coexistence of multiple neuroactive substances in the retina. In Neurobiology of the Inner Retina, ed. Weiler, R. & Osborne, N.N., pp. 275–293. Berlin: Springer.CrossRefGoogle Scholar
Watt, C.B. & Wilson, E.A. (1990). Synaptic organization of serotonin-like immunoreactive amacrine cells in the larval tiger salamander retina. Neuroscience 35, 715–723.CrossRefGoogle ScholarPubMed
Watt, C.B. (1991). A re-examination of enkephalin's coexistence with gamma-aminobutyric acid in amacrine cells of the larval tiger salamander retina. Brain Research 551, 351–354.CrossRefGoogle ScholarPubMed
Watt, C.B., Glazebrook, P.A. & Li, H.B. (1991). Coexistence of somatostatin and neurotensin in amacrine cells of the chicken retina. Brain Research 546, 166–170.CrossRefGoogle ScholarPubMed
Watt, C.B. & Florack, V.J. (1992 a). A double-label study demonstrating that all serotonin-like immunoreactive amacrine cells in the larval tiger salamander retina express GABA-like immunoreactivity. Brain Research 583, 336–339.CrossRefGoogle ScholarPubMed
Watt, C.B. & Florack, V.J. (1992 b). Double-label analysis demonstrating the non-coexistence of tyrosine hydroxylase- and GABA-like immunoreactivities in amacrine cells of the larval tiger salamander retina. Neuroscience Letters 148, 47–50.CrossRefGoogle ScholarPubMed
Watt, C.B., Florack, V.J. & Walker, R.B. (1992). Coexisting relationships of substance P-amacrine cells in the larval tiger salamander retina. Society for Neuroscience Abstracts 18, 1027.Google Scholar
Watt, C.B., Florack, V.J. & Walker, R.B. (1993). Quantitative analyses of the coexistence of gamma-aminobutyric acid in substance P-amacrine cells of the larval tiger salamander retina. Brain Research 603, 111–116.CrossRefGoogle ScholarPubMed
Watt, C.B. & Glazebrook, P.A. (1993). Synaptic organization of dopaminergic amacrine cells in the larval tiger salamander retina. Neuroscience 53, 27–36.CrossRefGoogle ScholarPubMed
Weiler, R. & Ball, A.K. (1984). Colocalization of neurotensin-like immunoreactivity and [3H]-glycine uptake system in sustained amacrine cells of the chicken retina. Nature 311, 759–761.CrossRefGoogle Scholar
Wenthold, R.J., (1987). Evidence for a glycinergic pathway connecting the two cochlear nuclei: An immunocytochemical and retrograde transport study. Brain Research 415, 183–187.CrossRefGoogle ScholarPubMed
Wong-Riley, M.T.T. (1974). Synaptic organization of the inner plexi-form layer in the retina of the tiger salamander retina. Journal of Neurocytology 3, 1–33.CrossRefGoogle Scholar
Wu, S.M. (1987). Synaptic connections among retinal neurons in living slices. Journal of Neuroscience Methods 20, 139–149.CrossRefGoogle ScholarPubMed
Yang, C.Y. & Yazulla, S. (1986). Neuropeptide-like immunoreactive cells in the retina of the larval tiger salamander: Attention to the symmetry of dendritic projections. Journal of Comparative Neurology 248, 105–118.CrossRefGoogle Scholar
Yang, C.Y. & Yazulla, S. (1988 a). 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.CrossRefGoogle ScholarPubMed
Yang, C.Y. & Yazulla, S. (1988 b). Localization of putative GABAergic neurons in the larval tiger salamander retina by immunocytochemical and autoradiographical methods. Journal of Comparative Neurology 272, 96–108.CrossRefGoogle Scholar
Yang, C.Y., Lukasiewicz, P., Maguire, G., Werblin, F.S. & Yazulla, S. (1991). Amacrine cells in the tiger salamander retina: Morphology, physiology, and neurotransmitter identification. Journal of Comparative Neurology 312, 19–32.CrossRefGoogle ScholarPubMed
Yang, S.Z., Watt, C.B. & Lam, D.M.K. (1988). Localization of neurrotensin-like immunoreactive amacrine cells in the larval tiger sala mander retina. Experimental Brain Research 70, 33–42.CrossRefGoogle Scholar
Yang, S.Z., Watt, C.B. & Lam, D.M.K. (1988). Localization of neurotensin-like immunoreactive amacrine cells in the larval tiger salamander retina. Experimental Brain Research 70, 33–42.CrossRefGoogle ScholarPubMed
Yang, S.Z., Lam, D.M.K. & Watt, C.B. (1989). Localization of serotonin-like immunoreactive amacrine cells in the larval tiger salamander retina. Journal of Comparative Neurology 287, 28–37.CrossRefGoogle Scholar
Yazulla, S. (1986). GABAergic mechanisms in the retina. In Progress in Retinal Research, Vol. 6, ed. Osborne, N.N. & Chader, G., pp. 1–52. Oxford: Pergamon Press.Google Scholar
Yazulla, S. & Yang, C.Y. (1988). Colocalization of GABA and glycine immunoreactivities in a subset of retinal neurons in the tiger salamander retina. Neuroscience Letters 95, 37–41.CrossRefGoogle Scholar
Zalutsky, R.A. & Miller, R.F. (1990). The physiology of substance P in the rabbit retina. Journal of Neuroscience 10, 394–402.CrossRefGoogle ScholarPubMed