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Glutamate immunoreactivity in the cat retina: A quantitative study

Published online by Cambridge University Press:  02 June 2009

Ljubomir Jojich  and
Roberta G. Pourcho
Ljubomir Jojich
Affiliation:
Department of Anatomy and Cell Biology, Wayne State University, Detroit
Roberta G. Pourcho
Affiliation:
Department of Anatomy and Cell Biology, Wayne State University, Detroit
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Abstract

Immunocytochemical methods were used to visualize glutamate immunoreactivity in the cat retina and to compare its localization with that of aspartate, GABA, and glycine. The cellular and subcellular distribution of glutamate was analyzed at the light-microscopic level by optical densitometry and at the electron-microscopic level by immunogold quantification. The findings were consistent with the proposed role for glutamate as the neurotransmitter of photoreceptors and bipolar cells as particularly high concentrations of staining were found in synaptic terminals of these cells. Ganglion cells were also consistently stained. Aspartate was totally colocalized with glutamate in neuronal cell bodies but the synaptic levels of aspartate were much lower than for glutamate. In addition to the staining of photoreceptor, bipolar, and ganglion cells, glutamate immunoreactivity was also observed in approximately 60% of the amacrine cells. These cells exhibited colocalization with either GABA or glycine. The elevated levels of Glu in amacrine cells may reflect its role as a transmitter precursor in GABAergic cells and as an energy source for mitochondria in glycinergic cells.

Keywords

GlutamateRetinaImmunocytochemistryDensitometryNeurotransmitter
Type
Research Articles
Information
Visual Neuroscience , Volume 13 , Issue 1 , January 1996 , pp. 117 - 133
Copyright
Copyright © Cambridge University Press 1996

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References

REFERENCES

Abdullah, L.H., Ordronneau, P. & Petrusz, P. (1992). Molecular requirements for hapten binding to antibodies against glutamate and aspartate. Neuroscience 51, 729–738.Google Scholar
Altschuler, R.A., Mosinger, J.L., Harmison, G.G. & Parakkal, G.G. (1982). Aspartate aminotransferase-like immunoreactivity as a marker for aspartate/glutamate in guinea pig photoreceptors. Nature 298, 657–659.Google Scholar
Ariel, M. & Daw, N.W. (1982). Pharmacological analysis of directionally sensitive rabbit retinal ganglion cells. Journal of Physiology 324, 161–185.CrossRefGoogle ScholarPubMed
Ayoub, G.S., Korenbrot, J.I. & Copenhagen, D.R. (1989). Release of endogenous glutamate from isolated cone photoreceptors of the lizard. Neuroscience Research (Suppl.) 10, 47–56.Google ScholarPubMed
Berger, S.J., McDaniel, M.L., Carter, J.G. & Lowry, H. (1977). Distribution of four potential transmitter amino acids in monkey retina. Journal of Neurochemistry 28, 159–163.CrossRefGoogle ScholarPubMed
Bloomfield, S.A. & Dowling, J.E. (1985 a). Roles of aspartate and glutamate in synaptic transmission in rabbit retina. I. Outer plexi-form layer. Journal of Neurophysiology 53, 699–713.CrossRefGoogle Scholar
Bloomfield, S.A. & Dowling, J.E. (1985 b). Roles of aspartate and glutamate in synaptic transmission in rabbit retina. II. Inner plexi-form layer. Journal of Neurophysiology 53, 714–725.Google Scholar
Brandon, C. & Lam, D.M.K. (1983). L-Glutamic acid: A neurotransmitter candidate for cone photoreceptors in human and rat retinas. Proceedings of the National Academy of Sciences of the U.S.A. 80, 5117–5121.Google Scholar
Brandstätter, J.H., Hartveit, E., Sassoè-Pognetto, M. & Wässle, H. (1994). Expression of NMDA and high-affinity kainate receptor subunit mRNAs in the adult rat retina. European Journal of Neuroscience 6, 1100–1112.CrossRefGoogle ScholarPubMed
Castel, M., Belenky, M., Cohen, S., Ottersen, O.P. & Storm-Mathisen, J. (1993). Glutamate-like immunoreactivity in retinal terminals of the mouse suprachiasmatic nucleus. European Journal of Neuroscience 5, 368–381.Google Scholar
Chen, B. & Pourcho, R.G. (1995). Morphological diversity and glutamate immunoreactivity of retinal terminals in the suprachiasmatic nucleus of the cat. Journal of Comparative Neurology 361, 108–118.Google Scholar
Cohen, E. & Sterling, P. (1986). Accumulation of (3H)glycine by cone bipolar neurons in the cat retina. Journal of Comparative Neurology 250, 1–7.CrossRefGoogle ScholarPubMed
Copenhagen, D.R. & Jahr, C.E. (1989). Release of endogenous excitatory amino acids from turtle photoreceptors. Nature 341, 536–539.CrossRefGoogle ScholarPubMed
Crooks, J. & Kolb, H. (1992), Localization of GABA, glycine, gluta-mate and tyrosine hydroxylase in the human retina. Journal of Comparative Neurology 315, 287–302.CrossRefGoogle Scholar
Cunningham, J.R. & Neal, M.J. (1985). Effect of excitatory amino acids on γ-aminobutyric acid release from frog horizontal cells. Journal of Physiology (London) 362, 51–67.Google Scholar
Davanger, S., Ottersen, O.P. & Storm-Mathisen, J. (1991). Gluta-mate, GABA, and glycine in the human retina: An immunocyto-chemical investigation. Journal of Comparative Neurology 311, 483–494.CrossRefGoogle Scholar
Davanger, S., Ottersen, O.P. & Storm-Mathisen, J. (1994). Colo-calization of glutamate and glycine in bipolar cell terminals of the human retina. Experimental Brain Research 98, 342–354.Google Scholar
Docherty, M., Bradford, H.F. & Wu, J.Y. (1987). Co-release of glutamate and aspartate from cholinergic and GABAergic synapto-somes. Nature 350, 64–66.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.CrossRefGoogle ScholarPubMed
Eliasof, S. & Werblin, F. (1993). Characterization of the glutamate transporter in retinal cones of the tiger salamander. Journal of Neuroscience 13, 402–411.Google Scholar
Erecinska, M. & Silver, I.A. (1990). Metabolism and role of glutamate in mammalian brain. Progress in Neurobiology 35, 245–296.Google Scholar
Famiglietti, E.V. (1987). Starburst amacrine cells in cat retina are associated with bistratified, presumed directionally selective, ganglion cells. Brain Research 413, 404–408.Google Scholar
Fisher-Bovenkerk, C., Kish, P.E. & Ueda, T. (1988). ATP-dependent glutamate uptake into synaptic vesicles from cerebellar mutant mice. Journal of Neurochemistry 51, 1054–1059.CrossRefGoogle Scholar
Fykse, E.M. & Fonnum, E. (1989). Regional distribution of γ-amino-butyrate and L-glutamate uptake into synaptic vesicles isolated from rat brain. Neuroscience Letters 99, 300–304.CrossRefGoogle Scholar
Galigher, A.E. & Kozloff, E.N. (1971). Nitrocellulose method. In Essentials of Practical Microtechnique, ed. Galigher, A.E. & Kozloff, E.N., pp. 255–270. Philadelphia, Pennsylvania: Lea & Febiger.Google Scholar
Hamassaki-Britto, D.E., Hermans-Borgmeyer, I., Heinemann, S. & Hughes, T.E. (1993). Expression of glutamate receptor genes in the mammalian retina: The localization of GluRl through GluR7 mRNAs. Journal of Neuroscience 13, 1888–1898.CrossRefGoogle Scholar
Hartveit, E., Brandstätter, J.H., Sassoè-Pognetto, M., Laurie, D.J., Seeburg, P.H. & Wässle, H. (1994). Localization and developmental expression of the NMDA receptor subunit NR2A in the mammalian retina. Journal of Comparative Neurology 348, 570–582.CrossRefGoogle ScholarPubMed
Hirano, A.A., Hirsch, J.A. & Macleish, P.R. (1988). Glutamate responses in solitary bipolar cells from salamander retina. Society for Neuroscience Abstracts 14, 986.Google Scholar
Hughes, T.E., Hermanns-Borgmeyer, I. & Heinemann, S. (1992). Differential expression of glutamate receptor genes (GluR1–5) in the rat retina. Visual Neuroscience 8, 49–55.Google Scholar
Ikeda, H., Daws, E. & Hankins, M. (1992). Spontaneous firing level distinguishes the effects of NMDA and non-NMDA receptor antagonists on the ganglion cells in the cat retina. European Journal of Pharmacology 210, 53–59.Google Scholar
Ikeda, H., Kay, C.D. & Robbins, J. (1990). Excitatory amino acid receptors on sustained retinal ganglion cells in the kitten during the critical period of development. Developmental Brain Research 51, 85–91.Google Scholar
Ishida, A.T., Kaneko, A. & Tachibana, M. (1984). Responses of solitary retinal horizontal cells from Carassius auratus to L-glutamate and related amino acids. Journal of Physiology (London) 348, 255–270.CrossRefGoogle ScholarPubMed
Israël, M., Lesbats, B. & Bruner, J. (1993). Glutamate and acetylcholine release from cholinergic nerve terminals, a calcium control of the specificity of the release mechanism. Neurochemistry International 22, 53–58.Google Scholar
Johnson, J. W. & Ascher, P. (1987). Glycine potentiates the NMDA response in cultured mouse brain neurons. Nature 325, 529–531.Google Scholar
Jojich, L. & Pourcho, R.G. (1992). Quantitative immunogold analysis reveals high glutamate levels in retinocollicular projections in rat, rabbit and cat. Investigative Ophthalmology and Visual Science (Suppl.) 33, 1689.Google Scholar
Lasater, E.M. & Dowling, J.E. (1982). Carp horizontal cells in culture respond selectively to L-glutamate and its agonists. Proceedings of the National Academy of Sciences of the U.S.A. 79, 936–940.Google Scholar
Lin, C-T., Li, H-Z. & Wu, J-K. (1983). Immunocytochemical localization of L-glutamate decarboxylase, gamma-aminobutyric acid transaminase, cysteine sulfinic acid decarboxylase, aspartate aminotransferase and somatostatin in rat retina. Brain Research 270, 273–283.Google Scholar
Liu, C.J., Grandes, P., Matute, C., Cuenod, M. & Streit, P. (1989). Glutamate-like immunoreactivity revealed in rat olfactory bulb, hippocampus and cerebellum by monoclonal antibody and sensitive staining method. Histochemistry 90, 427–445.Google Scholar
Marc, R.E. & Lam, D.M.K. (1981). Uptake of aspartic and glutamic acid by photoreceptors in goldfish retina. Proceedings of the National Academy of Sciences of the U.S.A. 78, 7185–7189.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.CrossRefGoogle ScholarPubMed
Marc, R.E., Stell, W.K., Bok, D. & Lam, D.M.K. (1978). GABAergic pathways in the goldfish retina. Journal of Comparative Neurology 182, 221–246.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.N. & Chader, C.J., pp. 399–425. Oxford, England: Pergamon.Google Scholar
Massey, S.C. & Miller, R.F. (1990). N-Methyl-D-aspartate receptors of ganglion cells in rabbit retina. Journal of Neurophysiology 63, 16–30.Google Scholar
McMahon, H.T. & Nicholls, D.G. (1991). Transmitter glutamate release from isolated nerve terminals: Evidence for biphasic release and triggering by localized Ca2+. Journal of Neurochemistry 56, 86–94.CrossRefGoogle ScholarPubMed
Miller, R.F. & Slaughter, M.M. (1986). Excitatory amino acid receptors of the retina: Diversity of subtypes and conductance mechanisms. Trends in Neuroscience 9, 211–218.CrossRefGoogle Scholar
Mize, R.R. (1994). Quantitative image analysis for immunocytochemistry and in situ hybridization. Journal of Neuroscience Methods 54, 219–237.CrossRefGoogle ScholarPubMed
Mize, R.R., Holdefer, R.N. & Nabors, L.R. (1988). Quantitative immunocytochemistry using an image analyzer. 1. Hardware evaluation, image processing and data analysis. Journal of Neuroscience Methods 26, 1–24.Google Scholar
Montero, M.M. (1990). Quantitative immunogold analysis reveals high glutamate levels in synaptic terminals of retino-geniculate, cortico-geniculate, and geniculo-cortical axons of the cat. Visual Neuroscience 4, 437–443.CrossRefGoogle ScholarPubMed
Morjaria, B. & Voaden, M.J. (1979). The formation of glutamate, aspartate and GABA in the rat retina: Glucose and glutamine as precursors. Journal of Neurochemistry 33, 541–551.Google Scholar
Mosinger, J.L. & Altschuler, R.A. (1985). Aspartate aminotrans-ferase-like immunoreactivity in the guinea pig and monkey retinas. Journal of Comparative Neurology 233, 255–268.Google Scholar
Muller, F., Greferath, U., Wässle, H., Widsen, W. & Seeburg, P. (1992). Glutamate receptor expression in the rat retina. Neuroscience Letters 138, 179–182.Google Scholar
Murakami, M., Ohtsuka, T. & Shimazaki, H. (1975). Effects of aspartate and glutamate on the bipolar cells in the carp retina. Vision Research 15, 456–458.CrossRefGoogle ScholarPubMed
Nabors, L.B., Songu-Mize, E. & Mize, R.R. (1988). Quantitative immunocytochemistry using an image analyzer. II. Concentration standards for transmitter immunocytochemistry. Journal of Neuroscience Methods 26, 25–34.CrossRefGoogle ScholarPubMed
Naito, S. & Ueda, T. (1985). Characterization of glutamate uptake into synaptic vesicles. Journal of Neurochemistry 44, 99–109.Google Scholar
Nakajima, Y., Iwakabe, H., Akazawa, C., Nawa, H., Shigemoto, R., Mizuno, N. & Nakanishi, S. (1993). Molecular characterization of a novel retinal metabotropic glutamate receptor mGLUR6 with a high selectivity for L-2–amino-4–phosphonobutyrate. Journal of Biological Chemistry 268, 11868–11873.Google Scholar
Nawy, S. & Jahr, C.E. (1990). Time-dependent reduction of glutamate current in retinal bipolar cells. Neuroscience Letters 108, 279–283.CrossRefGoogle ScholarPubMed
Neal, M.J. & Cunningham, J.R. (1989). L-Homocysteicacid-a possible bipolar cell transmitter in rabbit retina. Neuroscience Letters 102, 114–119.Google Scholar
Osborne, N.N., Patel, S., Beaton, D.W. & Neuhoff, V. (1986). GABA neurons in retina of different species and their postnatal development in situ and in culture in the rabbit retina. Cell and Tissue Research 243, 117–123.Google Scholar
Ottersen, O.P. (1987). Postembedding light- and electron-microscopic immunocytochemistry of amino acids: Description of a new model system allowing identical conditions for specificity testing and tissue processing. Experimental Brain Research 69, 167–174.CrossRefGoogle ScholarPubMed
Ottersen, O.P. (1989). Postembedding immunogold labeling of fixed glutamate: An electron microscopic analysis of the relationship between gold particle density and antigen concentration. Journal of Chemical Neuroanatomy 2, 57–67.Google ScholarPubMed
Pourcho, R.G. (1980). Uptake of [3H]-glycine and [3H]-GABA by amacrine cells in the cat retina. Brain Research 198, 333–346.Google Scholar
Pourcho, R.G. & Goebel, D.J. (1985). A combined Golgi and autoradiographic study of (3H)-glycine-accumulating amacrine cells in the cat retina. Journal of Comparative Neurology 233, 473–480.Google Scholar
Pourcho, R.G. & Goebel, D.J. (1987 a). A combined golgi and autoradiographic study of 3H-glycine-accumulating cone bipolar cells in the cat retina. Journal of Neuroscience 7, 1178–1188.Google Scholar
Pourcho, R.G. & Goebel, D.J. (1987 b). Visualization of endogenous glycine in cat retina: An immunocytochemical study with Fab fragments. Journal of Neuroscience 7, 1189–1197.CrossRefGoogle ScholarPubMed
Pourcho, R.G. & Osman, K. (1986). Cytochemical identification of cholinergic amacrine cells in cat retina. Journal of Comparative Neurology 247, 497–504.Google Scholar
Pourcho, R.G. & Owczarzak, M.T. (1989). Distribution of GABA immunoreactivity in the cat retina: A light- and electron-microscopic study. Visual Neuroscience 2, 425–435.CrossRefGoogle ScholarPubMed
Pow, D.V. & Robinson, S.R. (1994). Glutamate in some retinal neurons is derived solely from glia. Neuroscience 60, 335–366.Google Scholar
Riepe, R.E. & Norenberg, M.D. (1977). Müller cell localization of glu-tamine synthetase in rat retina. Nature 268, 654–655.CrossRefGoogle ScholarPubMed
Roberts, W.A., Eaton, S.A. & Salt, T.E. (1991). Excitatory amino acid receptors mediate synaptic responses to visual stimuli in superior colliculus neurones of the rat. Neuroscience Letters 129, 161–164.Google Scholar
Robinson, M.B., Blakely, R.D., Cuoto, R. & Coyle, J.T. (1987). Hydrolysis of the brain dipeptide N-acetyl-L-aspartyl-L-glutamate: Identification of a novel N-acetylated α-linked dipeptidase activity from rat brain. Journal of Biological Chemistry 262, 14498–14506.Google Scholar
Sakurai, T., Miyamoto, T. & Okada, Y. (1990). Reduction of glutamate content in rat superior colliculus after retino-tectal denervation. Neuroscience Letters 109, 299–303.Google Scholar
Sarthy, P.V., Hendrickson, A.E. & Wu, J.Y. (1986). L-glutamate: A neurotransmitter candidate for cone photoreceptors in the monkey retina. Journal of Neuroscience 6, 637–643.CrossRefGoogle ScholarPubMed
Sassoè-Pognetto, M., Wässle, H. & Grünert, U. (1994). Glyciner-gic synapses in the rod pathway of the rat retina: Cone bipolar cells express the α 1 subunit of the glycine receptor. Journal of Neuroscience 8, 5131–5146.Google Scholar
Schwarz, S., Zhou, G.Z., Kaatki, A.G. & Rodbard, D. (1990). L-homocysteate stimulates [3H]MK-801 binding to the phencycli-dine recognition site and is thus an agonist for the N-methyl-d aspartate-operaled cation channel. Neuroscience 37, 193–200.Google Scholar
Sekiguchi, M., Okamoto, K. & Sakai, Y. (1987). Excitatory action of N-acetylaspartylglutamate on Purkinje cells in guinea pig cerebellar slices: An intrasomatic study. Brain Research 423, 23–33.Google Scholar
Sherry, D.M. & Ulshafer, R.J. (1992). Neurotransmitter-specific identification and characterization of neurons in the all-cone retina of Anolis carolinensis, 11: Glutamate and aspartate. Visual Neuroscience 9, 313–323.Google Scholar
Shiells, R.A. & Falk, G. (1990). Glutamate receptors of rod bipolar cells are linked to a cyclic GMP cascade via a G-protein. Proceedings of the Royal Society B (London) 242, 91–94.Google Scholar
Slaughter, M.M. & Miller, R.F. (1983 a). The role of excitatory amino acid transmitters in the mudpuppy retina: An analysis with kainic acid and N-methyl aspartate. Journal of Neuroscience 3, 1701–1711.CrossRefGoogle ScholarPubMed
Slaughter, M.M. & Miller, R.F. (1983 b). Bipolar cells in the mud-puppy retina use an excitatory amino acid neurotransmitter. Nature 303, 537–538.CrossRefGoogle Scholar
Slusher, B.S., Tsai, G., Yoo, G. & Coyle, J.T. (1992). Immunocytochemical localization of the N-acetyl-aspartyl-glutamate (NAAG) hydrolyzing enzyme N-acetylated-alpha-linked acidic dipeptidase (NAALADase). Journal of Comparative Neurology 315(2), 217–229.Google Scholar
Somogyi, P., Halasy, K., Somogyi, J., Storm-Mathisen, J. & Ottersen, O.P. (1986). Quantification of immunogold labeling reveals enrichment of glutamate in mossy and parallel fibre terminals in cat cerebellum. Neuroscience 19, 1045–1050.Google Scholar
Sterling, P. (1983). Microcircuitry of the cat retina. Annual Review of Neuroscience 6, 149–185.Google Scholar
Storm-Mathisen, J., Leknes, A.K., Bore, A.T., Vaaland, J.L., Edminson, P., Haug, F.-M.S. & Ottersen, O.P. (1983). First visualization of glutamate and GABA in neurones by immunocytochemistry. Nature 301, 517–520.Google Scholar
Storm-Mathisen, J. & Ottersen, O.P. (1990). Immunocytochemistry of glutamate at the synaptic level. Journal of Histochemistry and Cytochemistry 38, 1733–1743.CrossRefGoogle ScholarPubMed
Storm-Mathisen, J., Ottersen, O.P., Fu-Long, T., Gundersen, V., Laake, J.H. & Nordbo, G. (1986). Metabolism and transport of amino acids studied by immunocytochemistry. Medical Biology 101, 683–688.Google Scholar
Taschenberger, H. & Grantyn, R. (1995). Several types of Ca2+ channels mediate glutamatergic synaptic responses to activation of single Thy-1–immunolabeled rat retinal ganglion neurons. Journal of Neuroscience 15(3), 2240–2254.Google Scholar
Tian, N. & Slaughter, M.M. (1994). Pharmacological similarity between the retinal APB receptor and the family of metabotropic glutamate receptors. Journal of Neurophysiology 71, 2258–2268.Google Scholar
Tieman, S.B., Cangro, C.B. & Neale, J.H. (1987). N-acetylaspartylglutamate immunoreactivity in neurons of the cat's visual system. Brain Research 420, 188–193.CrossRefGoogle ScholarPubMed
Tieman, S.B., Moffett, J.R. & Irtenkauf, S.M. (1991). Effect of eye removal on N-acetylaspartyl glutamate immunoreactivity in retinal targets of the cat. Brain Research 562, 318–322.Google Scholar
van den Pol, A.N. (1991). Glutamate and aspartate immunoreactivity in hypothalamic presynaptic axons. Journal of Neuroscience 11, 2087–2101.CrossRefGoogle ScholarPubMed
Vaney, D.I. (1985). The morphology and topographic distribution of An amacrine cells in the cat retina. Proceedings of the Royal Society B (London) 224, 475–488.Google Scholar
Vaney, D.I. & Young, H.M. (1989). GABA-like immunoreactivity in cholinergic amacrine cells of the rabbit retina. Brain Research 438, 369–373.CrossRefGoogle Scholar
Vyes, S. & Bradford, H.F. (1987). Co-release of acetylcholine, glutamate and taurine from synaptosomes of Torpedo electric organ. Neuroscience Letters 82, 58–64.Google Scholar
Waerhaug, O. & Ottersen, O.P. (1993). Demonstration of glutamate-like immunoreactivity at rat neuromuscular junctions by quantitative electron microscopic immunocytochemistry. Anatomy and Embryology 188, 501–513.Google Scholar
Wang, Y. & Floor, E. (1994). Dynamic storage of glutamate in rat brain synaptic vesicles. Neuroscience Letters 180, 175–178.Google Scholar
Watanabe, M., Mishina, M. & Inoue, Y. (1994). Differential distributions of the NMDA receptor channel subunit mRNAs in the mouse retina. Brain Research 634, 328–332.Google Scholar
Williamson, L.C. & Neale, J.H. (1988 a). Ultrastructural localization of N-acetylaspartyl-glutamate in synaptic vesicles of retinal neurons. Brain Research 456, 375–381.Google Scholar
Williamson, L.C. & Neale, J.H. (1988 b). Calcium-dependent release of N-acetylaspartyl-glutamate from retinal neurons upon depolarization. Brain Research 475, 151–155.Google Scholar
Williamson, L.C. & Neale, J.H. (1992). Uptake, metabolism, and release of N-[3H]-acetylaspartyl glutamate by avian retina. Journal of Neurochemistry 58, 2191–2199.Google Scholar
Winkler, B.S. & Orselli, S.M. (1994). Glutamate oxidation by retinal mitochondria. Investigative Ophthalmology and Visual Science 35, 503.Google Scholar
Yaqub, A. & Eldred, W.D. (1991). Localization of aspartate-like immunoreactivity in the retina of the turtle (Pseudemys scripta). Journal of Comparative Neurology 312, 584–598.Google Scholar