Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-05T01:47:34.601Z Has data issue: false hasContentIssue false
  • English
  • Français

Neurotransmitter-specific identification and characterization of neurons in the all-cone retina of Anolis carolinensis II: Glutamate and aspartate

Published online by Cambridge University Press:  02 June 2009

David M. Sherry  and
Robert J. Ulshafer
David M. Sherry
Affiliation:
Departments of Neuroscience and Ophthalmology, University of Florida, Gainesville
Robert J. Ulshafer
Affiliation:
Departments of Neuroscience and Ophthalmology, University of Florida, Gainesville
Get access Rights & Permissions [Opens in a new window]

Abstract

Immunocytochemical and autoradiographic methods were used to identify neurons in the pure cone retina of the lizard (Anolis carolinensis) that are likely to employ glutamate (GLU) or aspartate (ASP) as a neurotransmitter.

GLU immunocytochemistry demonstrated high levels of endogenous GLU in all cone types and numerous bipolar cells. Moderate GLU levels were found in horizontal and ganglion cells. Müller cells and most amacrine cells had very low GLU levels. GLU immunoreactivity (GLU-IR) in the cones was present from the inner segment to the synaptic pedicle. A large spherical cell type with moderate GLU-IR was identified in the proximal inner plexiform layer (IPL). These cells also contain ASP and have been tentatively identified as amacrine cells. Uptake of [3H]-L-GLU labeled all retinal layers. All cone types and Müller cells sequestered [3H]-D-ASP, a substrate specific for the GLU transporter.

Anti-ASP labeling was observed in cones, horizontal cells, amacrine cells, and cells in the ganglion cell layer. ASP immunoreactivity (ASP-IR) in the cones was confined to the inner segment. One ASP-containing pyriform amacrine cell subtype ramifying in IPL sublamina b was identified.

Analysis of GLU-IR, ASP-IR, and GABA-IR on serial sections indicated that there were two distinct populations of horizontal cells in the Anolis retina: one containing GABA-IR, GLU-IR, and ASP-IR; and another type containing only GLU-IR and ASP-IR. Light GLU-IR was frequently found in GABA-containing amacrine cells but ASP-IR was not.

The distinct distributions of GLU and ASP may indicate distinctly different roles for these amino acids. GLU, not ASP, is probably the major neurotransmitter in the cone-biploar-ganglion cell pathway of the Anolis retina. Both GLU and ASP are present in horizontal cells and specific subpopulations of amacrine cells, but it is unclear if GLU or ASP have a neurotransmitter role in these cells.

Keywords

GlutamateAspartateNeurotransmitterAutoradiographyImmunocytochemistryBipolar cellCone photoreceptorAnolis carolinensisRetina
Type
Research Articles
Information
Visual Neuroscience , Volume 9 , Issue 3-4 , October 1992 , pp. 313 - 323
Copyright
Copyright © Cambridge University Press 1992

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Agardh, E., Brunn, A., Ehinger, B. & Storm-Mathisen, J. (1986). GABA immunoreactivity in the retina. Investigative Ophthalmology and Visual Science 27, 674–678.Google ScholarPubMed
Altschuler, R.A., Mosinger, J.L., Harmison, G.G., Parakkal, M.H. & Wenthold, R.J., (1982). Aspartate aminotransferase-like immunoreactivity as a marker for glutamate/aspartate in guinea pig photoreceptors. Nature 298, 657–659.CrossRefGoogle Scholar
Ammermüller, J. & Weiler, R. (1989). Correlation between electrophysiological response and morphological classes of turtle retinal amacrine cells. In Neurobiology of the Inner Retina, ed. Weiler, R. & Osborne, N.N., pp. 117–132. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Attwell, D., Mobbs, P., Tessier-Lavinge, M. & Wilson, M. (1987). Neurotransmitter-induced currents in retinal bipolar cells of the axolotl, Ambystoma mexicanum. Journal of Physiology 387, 125–161.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
Blanks, J.C. & Roffler-Tarlov, S. (1982). Differential localization of radioactive gamma-aminobutyric acid and muscimol in isolated and in vivo mouse retina. Experimental Eye Research 35, 573–584.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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
Cajal, S.R. (1893). La retine des vertebres. In The Vertebrate Retina: Principles of Structure and Function, trans. Rodieck, R.W. & Maguire, D., pp. 775–904. San Francisco, California: W.H. Freeman and Co.Google Scholar
Copenhagen, D.R. & Jahr, C.E. (1989). Release of endogenous excitatory amino acids from turtle photoreceptors. Nature 341, 536–539.CrossRefGoogle ScholarPubMed
Crescitelli, F. (1972). The visual cells and visual pigments of the vertebrate eye. In Handbook of Sensory Physiology, Vol. VII/I, ed. Dartnall, H.J.A., pp. 245–363. New York: Springer-Verlag.Google Scholar
Ehinger, B. (1977). Glial and neuronal uptake of GABA, glutamic acid, glutamine and glutathione in the rabbit retina. Experimental Eye Research 25, 221–234.CrossRefGoogle ScholarPubMed
Ehinger, B. (1981). [3H]-D-aspartate accumulation in the retina of pigeon, guinea pig and rabbit. Experimental Eye Research 33, 381–391.CrossRefGoogle 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
Eldred, W.D. & Cheung, K. (1989). Immunocytochemical localization of glycine in the retina of the turtle (Pseudemys scripta). Visual Neuroscience 2, 331–338.CrossRefGoogle ScholarPubMed
Eldred, W.D. & Yaqub, A. (1989). The diverse localization of aspartate-like immunoreactivity in the turtle retina. Investigative Ophthalmology and Visual Science (Suppl.) 30, 321.Google Scholar
Engbretson, G.A. & Battelle, B.A. (1987). Serotonin and dopamine in the retina of a lizard. Journal of Comparative Neurology 257, 140–147.CrossRefGoogle ScholarPubMed
Engbretson, G.A., Anderson, K.J. & Wu, J.-Y. (1989). GABA as a potential transmitter in lizard photoreceptors: Immunocytochemical and biochemical evidence. Journal of Comparative Neurology 278, 461–471.CrossRefGoogle Scholar
Famiglietti, E.V. Jr, Kaneko, A. & Tachibana, M. (1977). Neuronal architecture of On and Off pathways to ganglion cells in carp retina. Science 198, 1267–1269.CrossRefGoogle Scholar
Fowlkes, D.H., Karwoski, C.J. & Proenza, L.M. (1984). Endogenous circadian rhythm in electroretinogram of free-moving lizards. Investigative Ophthalmology and Visual Science 25, 121–124.Google ScholarPubMed
Hare, W.A., Lowe, J.S. & Owen, G. (1986). Morphology of physiologically identified bipolar cells in the retina of the tiger salamander, Ambystoma tigrinum. Journal of Comparative Neurology 252, 130–138.CrossRefGoogle ScholarPubMed
Hodgekinson, P.E. & Still, A.W. (1980). Color and brightness preferences in the lizard Anolis carolinensis. Perception 9, 61–68.CrossRefGoogle Scholar
Hurd, L.B. II & Eldred, W.D. (1989). Localization of GABA- and GAD-like immunoreactivity in the turtle retina. Visual Neuroscience 3, 9–20.CrossRefGoogle ScholarPubMed
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 348, 255–270.CrossRefGoogle ScholarPubMed
Keyser, K.T., Britto, L.R.G., Woo, J.-L., Park, D.H., Joh, T.H. & Karten, H.J. (1990). Presumptive catecholaminergic ganglion cells in the pigeon retina. Visual Neuroscience 4, 225–236.CrossRefGoogle ScholarPubMed
Lam, D.M.K. & Hollyfield, J.G. (1980). Localization of putative amino acid neurotransmitters in the human retina. Experimental Eye Research 31, 729–732.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Leeper, H. (1978). Horizontal cells of the turtle retina: Light microscopy of Golgi preparations. Journal of Comparative Neurology 182, 777–794.CrossRefGoogle ScholarPubMed
Lukasiewicz, P.D. & McReynolds, J.S. (1985). Synaptic transmission at the N-methyl-D-aspartate receptors in the proximal retina of the mudpuppy. Journal of Physiology 367, 99–115.CrossRefGoogle ScholarPubMed
Mangel, S.C., Ariel, M. & Dowling, J.E. (1985). Effects of acidic amino acid antagonists upon the spectral properties of carp horizontal cells: Circuitry of the outer retina. Journal of Neuroscience 5, 2839–2850.CrossRefGoogle ScholarPubMed
Marc, R.E. (1985). The role of glycine in retinal circuitry. In Retinal Transmitters and Modulators: Models for the Brain, ed. Morgan, W.W., pp. 119–158. Boca Raton, Florida: CRC Press, Inc.Google Scholar
Marc, R.E. (1986). Neurochemical stratification in the IPL of the vertebrate retina. Vision Research 26, 223–238.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
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
Marchiafava, P.L. & Weiler, R. (1980). Intracellular analysis and structural correlates of the organization of inputs to ganglion cells in the retina of the turtle. Proceedings of the Royal Society B (London) 208, 103–113.Google ScholarPubMed
Masland, R.H., Mills, J.W. & Cassidy, C. (1984). The functions of acetylcholine in the rabbit retina. Proceedings of the Royal Society B (London) 223, 121–139.Google ScholarPubMed
Massey, S.C. (1990). Cell types using glutamate as a neurotransmitter in the vertebrate retina. Progress in Retinal Research 9, 399–425.CrossRefGoogle Scholar
Mosinger, J.L. & Altschuler, R.A. (1985). Aspartate aminotransferase-like immunoreactivity in the guinea pig and monkey retinas. Journal of Comparative Neurology 233, 255–268.CrossRefGoogle ScholarPubMed
Murakami, M., Ohtsu, K. & Ohtsuka, T. (1972). Effects of chemicals on receptors and horizontal cells in the retina. Journal of Physiology 111, 899–913.CrossRefGoogle Scholar
Naka, K.-I. (1977). Functional Organization Of Catfish Retina. Journal of Neurophysiology 40, 26–43.CrossRefGoogle ScholarPubMed
Nawy, S. & Copenhagen, D.R. (1987). Multiple classes of glutamate receptor on depolarizing bipolar cells in retina. Nature 325, 56–58.CrossRefGoogle ScholarPubMed
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 tis- sue processing. Experimental Brain Research 69, 167–174.CrossRefGoogle Scholar
Ross, C.D. & Godfrey, D.A. (1985). Distributions of aspartate aminotransferase and malate dehydrogenase activities in rat retinal layers. Journal of Histochemistry and Cytochemistry 33, 624–630.CrossRefGoogle ScholarPubMed
Ross, C.D. & Godfrey, D.A. (1987). Distribution of activities of aspartate aminotransferase and malate dehydrogenase in guinea pig retina layers. Journal of Histochemistry and Cytochemistry 35, 669–674.CrossRefGoogle Scholar
Ross, C.D., Bowers, M. & Godfrey, D.A. (1987). Distributions of the activities of aspartate aminotransferase in rat retinal layers. Neuroscience Letters 74, 205–210.CrossRefGoogle ScholarPubMed
Roth, J. (1983). The colloidal gold marker system for light and electron miscroscopic cytochemistry. In Techniques in Immunocytochemistry, Vol. 2, ed. Bullock, G.R. & Petrusz, P., pp. 217–284. London: Academic Press.Google Scholar
Rubinson, K., Yazulla, S. & Studholme, K.M. (1990). Horizontal cells in the developing lamprey retina. Investigative Ophthalmology and Visual Science (Suppl.) 31, 159.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
Sarthy, P.V. & Lam, D.M.K. (1978). Biochemical studies of isolated glial (Miiller) cells from the turtle retina. Journal of Cell Biology 78, 675–684.CrossRefGoogle Scholar
Sherry, D.M. & Ulshafer, R.J. (1988). Immunocytochemical localization of putative neurotransmitters in the ”all-cone” Anolis retina. Investigative Ophthalmology and Visual Science (Suppl.) 29, 195.Google Scholar
Sherry, D.M. & Ulshafer, R.J. (1992). Neurotransmitter-specific identification and characterization of neurons in the all-cone retina of Anolis carolinensis. I: GABA. Visual Neuroscience 8, 515–529.CrossRefGoogle Scholar
Slaughter, M.M. & Miller, R.F. (1983a). 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. (1983b). Bipolar cells in the mudpuppy retina use an excitatory amino acid neurotransmitter. Nature 303, 537–538.CrossRefGoogle ScholarPubMed
Stell, W.K. & Lightfoot, D.O. (1975). Color-specific interconnections of cones and horizontal cells in the retina of the goldfish. Journal of Comparative Neurology 159, 473–502.CrossRefGoogle ScholarPubMed
Underwood, G. (1951). Reptilian retinas. Nature 167, 183–185.CrossRefGoogle ScholarPubMed
Weiler, R. (1981). The distribution of center-depolarizing and centerhyperpolarizing bipolar cell ramifications within the inner plexiform layer of the turtle retina. Journal of Comparative Physiology 144, 459–464.CrossRefGoogle Scholar
Weiler, R. & Ammermuller, J. (1987). Immunocytochemical localization of serotonin in intracellularly analyzed and dye-injected ganglion cells in the turtle retina. Neuroscience Letters 72, 147–152.CrossRefGoogle Scholar
Yazulla, S. (1985). Evoked efflux of [3H]-GABA from goldfish retina in the dark. Brain Research 325, 171–180.CrossRefGoogle ScholarPubMed
Yazulla, S. (1986). GABAergic mechanisms in the retina. Progress in Retinal Research 5, 1–52.CrossRefGoogle Scholar