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Localization of substance P and GABA in retinotectal ganglion cells of the larval tiger salamander

Published online by Cambridge University Press:  02 June 2009

Carl B. Watt ,
Patricia A. Glazebrook  and
Valarie J. Florack
Carl B. Watt
Affiliation:
Alice R. McPherson Laboratory of Retina Research, Center for Biotechnology, Baylor College of Medicine, The Woodlands
Patricia A. Glazebrook
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 the transmitter specificity of neuronal populations in the larval tiger salamander retina. Backfill-labeling of ganglion cells from the optic tectum was combined with double-label immunofluorescence histochemistry to determine if substance P and GABA are localized to ganglion cell populations in the tiger salamander retina. The triple-label analysis revealed the presence of substance P- and GABA-ganglion cells in both central and peripheral regions of the retina. Substance P-immunoreactive ganglion cells comprised 2% of the total population of backfill-labeled ganglion cells, while less than 1% of backfill-labeled ganglion cells expressed GABA immunoreactivity. Ganglion cells were not found to co-label for both substance P and GABA. Backfill-labeled displaced ganglion cells, which comprised 1.4% of the ganglion cell population, were not observed to be immunoreactive for either substance P or GABA. Forty-six point nine percent of substance P-cells in the ganglion cell layer were backfill-labeled and were identified as ganglion cells. GABA ganglion cells comprised less than 1% of GABA-immunoreactive cells in the ganglion cell layer.

Keywords

Triple-labelAMCAImmunocytochemistryBackfillCoexistenceNeuropeptideClassical neurotransmitter
Type
Research Articles
Information
Visual Neuroscience , Volume 11 , Issue 2 , March 1994 , pp. 355 - 362
Copyright
Copyright © Cambridge University Press 1994

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References

Arkin, M.S. & Miller, R.F. (1988). Mudpuppy retinal ganglion cell morphology revealed by an HRP impregnation technique which provides Golgi-like staining. Journal of Comparative Neurology 270, 185–208.CrossRefGoogle ScholarPubMed
Ball, A.K. & Dickson, D.H. (1983). Displaced amacrine and ganglion cells in the newt retina. Experimental Eye Research 36, 199–213.Google Scholar
Brecha, N. (1983). Retinal neurotransmitters: Histochemical and biochemical studies. In Chemical Neuroanatomy, ed. Emson, P.C., pp. 85–129. New York: Raven.Google Scholar
Brecha, N., Johnson, D., Bolz, J., Sharma, S., Parnevelas, J.G. & Lieberman, A.R. (1987). Substance P-immunoreactive retinal ganglion cells and their central axon terminals in the rabbit. Nature 327, 155–158.Google Scholar
Britto, L.R.G. & Hamasaki, 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. & Hamasaki-Britto, D.E. (1991). Cholecystokinin-like immunoreactive ganglion cells project to the ventral lateral geniculate nucleus in pigeons. Brain Research 557, 322–326.Google Scholar
Caruso, D.M., Orczarzak, M.T., Hazlett, J.C. & Pourcho, R.G. (1989). GABA-immunoreactive ganglion cells in the rat retina project to the superior colliculus. Brain Research 476, 129–134.CrossRefGoogle Scholar
Caruso, D.M., Orczarzak, 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
Dick, E. & Miller, R.F. (1981). Peptides influence retinal ganglion cells. Neuroscience Letters 26, 131–135.CrossRefGoogle ScholarPubMed
Ehrlich, D., Keyser, K., Manthorpe, M., Varon, S. & Karten, H.J. (1990). Differential effects of axotomy on substance P-containing and nicotinic acetylcholine receptor-containing retinal ganglion cells: Time course of degeneration and effects of nerve growth factor. Neuroscience 36, 699–723.CrossRefGoogle ScholarPubMed
Freund, T. & Antal, M. (1988). GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature 336, 170–173.CrossRefGoogle ScholarPubMed
Gabriel, R., Straznicky, C. & Wye-Dvorak, J. (1992). GABA-like immunoreactive neurons in the retina of Bufo marinus: Evidence for the presence of GABA-containing ganglion cells. Brain Research 571, 175–179.Google Scholar
Glazebrook, P.A., Fry, K.R. & Watt, C.B. (1993). Interaction between enkephalin and GABA in the chicken retina: A double-label immunoelectron microscopic analysis. Society for Neuroscience Abstracts 19, 115.Google Scholar
Glickman, R.D., Adolph, A.R. & Dowling, J.E. (1982). Inner plexiform layer of the carp retina: Effects of cholinergic agonists, GABA and substance P on the ganglion cells. Brain Research 234, 81–99.CrossRefGoogle Scholar
Hurd, L.B. & Eldred, W.D. (1989). Localization of GABA- and GAD-like immunoreactivity in the turtle retina. Visual Neuroscience 3, 9–20.Google Scholar
Hutsler, J.J., White, C.A. & Chalupa, L.M. (1991). Neuropeptide Y identifies a subgroup of gamma-type ganglion cells in the cat retina. Society for Neuroscience Abstracts 17, 343.Google Scholar
Lasansky, A. (1973). Organization of the outer synaptic layer in the retina of the larval tiger salamander retina. Philosophical Transactions of the Royal Society (London) 265, 471–489.Google Scholar
Leresche, N., Hardy, D., Audinat, E. & Jassik-Gerschenfeld, D. (1986). Synaptic organization of inhibitory circuits in the pigeon’s optic tectum. Brain Research 265, 383–387.CrossRefGoogle Scholar
Li, H.B., Chen, N.X., Watt, C.B. & Lam, D.M.K. (1986). The light microscopic localization of substance P- and somatostatin-like immunoreactive cells in the larval tiger salamander retina. Experimental Brain Research 63, 93–101.Google Scholar
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 Research 31, 262–271.Google ScholarPubMed
Lugo-Garcia, N. & Blanco, R.E. (1991). Localization of GAD- and GABA-like immunoreactivity in ground squirrel retina: Retrograde labeling demonstrates GAD-positive ganglion cells. Brain Research 564, 19–26.Google Scholar
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
Massey, S.C. & Redburn, D.A. (1987). Transmitter circuits in the vertebrate retina. Progress in Neurobiology 28, 55–96.Google Scholar
Miceli, D., Reperant, J., Marchand, L. & Rio, J.-P. (1993). Retrograde transneuronal transport of the fluorescent dye rhodamine B-isothiocyanate from the primary and centrifugal visual systems in the pigeon. Brain Research 601, 289–298.CrossRefGoogle ScholarPubMed
Pourcho, R.G. & Goebel, D.J. (1988). Colocalization of substance P and gamma-aminobutyric acid in amacrine cells of cat retina. Brain Research 447, 164–168.CrossRefGoogle ScholarPubMed
Sawaki, Y. (1979). Suprachiasmatic nucleus neurons: Excitation and inhibition mediated by the direct retino-hypothalamic projection in female rats. Experimental Brain Research 37, 127–138.Google Scholar
Schmidt, A., Roth, G. & Ernst, M. (1989). Distribution of substance P-like, leucine enkephalin-like and bombesine-like immunoreactivity and acetylcholinesterase activity in the visual system of salamanders. Journal of Comparative Neurology 288, 123–135.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. Proceedings of the Royal Society (London) 237, 471–488.Google Scholar
Watt, C.B., Li, H.B., Fry, K.R. & Lam, D.M.K. (1985). Localization of enkephalin-like immunoreactive neurons in the larval tiger salamander retina. Journal of Comparative Neurology 241, 171–179.Google Scholar
Watt, C.B., Li, T., Wu, S.M. & Lam, D.M.K. (1987). Interactions between enkephalin and GABA in the larval tiger salamander retina. Brain Research 408, 258–262.Google Scholar
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). The 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.Google Scholar
Watt, C.B. & Wilson, E.A. (1990). Synaptic organization of serotonin-like immunoreactive amacrine cells in the larval tiger salamander retina. Neuroscience 35, 351–354.CrossRefGoogle ScholarPubMed
Watt, C.B. (1991). A re-examination of enkephalin’s coexistence with gamma-aminobutyric acid in the larval tiger salamander retina. Brain Research 551, 351–354.CrossRefGoogle ScholarPubMed
Watt, C.B. (1992). 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.Google Scholar
Watt, C.B. & Florack, V.J. (1992). 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. (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.Google Scholar
Watt, C.B. & Florack, V.J. (1993 a). Colocalization of glycine in substance P-amacrine cells of the larval tiger salamander retina. Visual Neuroscience 10, 899–906.CrossRefGoogle ScholarPubMed
Watt, C.B. & Florack, V.J. (1993 b). Double-label analyses of the somatostatin’s coexistence with GABA and glycine in amacrine cells of the larval tiger salamander retina. Brain Research 617, 131–137.CrossRefGoogle ScholarPubMed
White, C.A. & Chalupa, L.M. (1991). Subgroup of alpha ganglion cells in the adult cat retina is immunoreactive for somatostatin. Journal of Comparative Neurology 304, 1–13.Google Scholar
Williamson, D.E. & Elbred, W.D. (1989). Amacrine and ganglion cells with corticotropin-releasing factor-like immunoreactivity in the turtle retina. Journal of Comparative Neurology 280, 424–435.CrossRefGoogle ScholarPubMed
Wong-Riley, M.M.T. (1974). Synaptic organization of the inner plexiform layer in the retina of the tiger salamander. 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.Google Scholar
Yang, C.Y. & Yazulla, S. (1988 a). Localization of putative GABAergic neurons in the larval tiger salamander retina by immunocytochemical and autoradiographical methods. Journal of Comparative Neurology 277, 96–108.CrossRefGoogle Scholar
Yang, C.Y. & Yazulla, S. (1988 b). 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, Lukasiewicz, P., Maguire, G., Werblin, F.S. & Yazulla, S. (1991). Amacrine cells in the larval tiger salamander retina: Morphology, physiology and neurotransmitter identification. Journal of Comparative Neurology 312, 19–32.CrossRefGoogle Scholar
Yang, S.Z., Watt, C.B. & Lam, D.M.K. (1988). Localization of neurotensin-like immunoreactive amacrine cells in the larval tiger 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.Google Scholar
Yazulla, S. (1986). GABAergic mechanisms in the retina. In Progress in Retinal Research, Vol. 5, ed. Osborne, N.N. & Chader, G.J., pp. 1–52. Oxford: Pergamon.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.Google Scholar
Yu, B.C., Watt, C.B., Lam, D.M.K. & Fry, K.R. (1988). GABAergic ganglion cells in the rabbit retina. Brain Research 439, 376–382.CrossRefGoogle ScholarPubMed
Zalutsky, R.A. & Miller, R.F. (1990). The physiology of substance P in the rabbit retina. Journal Neuroscience 10, 394–402.CrossRefGoogle ScholarPubMed