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Neural organization of the retina of the turtle Mauremys caspica: a light microscope and Golgi study

Published online by Cambridge University Press:  02 June 2009

Helga Kolb ,
Ido Perlman  and
Richard A. Normann
Helga Kolb
Affiliation:
Physiology Department, University of Utah School of Medicine
Ido Perlman
Affiliation:
Department of Physiology, Technion-Israel Institute of Technology, Haifa, Israel
Richard A. Normann
Affiliation:
Bioengineering Department, University of Utah, Salt Lake City
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Abstract

The organization of the retina of the turtle species Mauremys caspica, found in fresh water ponds of Israel, has been examined by light microscopical techniques including examination of fresh wholemount retina, one micron blue-stained vertical sections and Golgi-stained material. The anatomical findings on Mauremys retina have been compared with those of the Pseudemys retina (Kolb, 1982) which is more commonly used for electrophysiological and neurochemical studies in the USA. The photoreceptors of Mauremys are similar in type and oil droplet content to Pseudemys photoreceptors except for the double cone in Mauremys. This cone type appears more abundant than in Pseudemys and the principal member contains a yellow oil droplet instead of an orange oil droplet. Golgi staining reveals that all the cell types that have been seen in Pseudemys are found in Mauremys with identical morphology. In addition, two amacrine cell types that were not before described for Pseudemys have been added to the classification. One of these is the tristratified dopaminergic amacrine cell described in immunocytochemical studies (Witkovsky et al., 1984; Nguyen-Legros et al., 1985; Kolb et al., 1987). We have used these anatomical studies on Pseudemys and Mauremys retina to form a catalogue of neural types for the turtle retina in general. We conclude with an attempt to combine findings from anatomy, electrophysiology, and neurochemistry to form an overview of the organization of this reptilian retina.

Keywords

Turtle retinaphotoreceptorsGolgi techniqueamarcine cells
Type
Research Articles
Information
Visual Neuroscience , Volume 1 , Issue 1 , January 1988 , pp. 47 - 72
Copyright
Copyright © Cambridge University Press 1988

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References

Amthor, F.R., Oyster, C.W. & Takahashi, E.S. (1984). Morphology of on-off direction-selective ganglion cells in the rabbit retina. Brain Research 298, 187–190.CrossRefGoogle ScholarPubMed
Ariel, M. & Adolph, A.R. (1985). Neurotransmitter inputs to directionally sensitive turtle retinal ganglion cells. Journal of Neurophysiology 54, 1123–1143.CrossRefGoogle ScholarPubMed
Arnold, K. & Neumeyer, C. (1987). Wavelength discrimination in the turtle (Pseudemys scripta elegans). Vision Research 27, 1501–1511.CrossRefGoogle ScholarPubMed
Baylor, D.A. & Fuortes, M.G.F. (1970). Electrical responses of single cones in the retina of the turtle. Journal of Physiology (London) 207, 77–92.CrossRefGoogle ScholarPubMed
Baylor, D.A., Fuortes, M.G.F. & O'Bryan, P.M. (1971). Receptive field of cones in the retina of the turtle. Journal of Physiology (London) 214, 265–294.Google Scholar
Baylor, D.A. & Fettiplace, R. (1979). Synaptic drive and impulse generation in ganglion cells of turtle retina. Journal of Physiology (London) 288, 107–127.Google Scholar
Bowling, D.B. (1980). Light responses of ganglion cells in the retina of the turtle. Journal of Physiology (London) 299, 173–196.Google Scholar
Cajal, S.R.Y. (1933). Die Retina der Wirbeltiere. Wiesbaden: Bergmann. The Structure of the Retina. Translation by Thorpe, S.A. and Glickstein, M. (1972). Thomas, Springfield.Google Scholar
Colonnier, M. (1964). The tangential organization of the visual cortex. Journal of Anatomy 98, 327–344.Google Scholar
Criswell, M.H. & Brandon, C.J. (1987). Immunocytochemical evidence that turtle cones are cholinergic. Investigative Ophthalmology and Visual Science (Suppl.) 28, 278.Google Scholar
Dacheux, R.F. & Raviola, E. (1986). The rod pathway in the rabbit retina: a depolarizing bipolar and amacrine cell. Journal of Neuroscience 6, 331–345.CrossRefGoogle ScholarPubMed
Dalton, A.J. (1955). A chrome-osmium fixative for electron microscopy. Anatomical Record 121, 281–287.Google Scholar
Eldred, W.D. & Karten, H.J. (1983). Characterization and quantification of peptidergic amacrine cells in the turtle retina: enkephalin, neurotensin, and glucagon. Journal of Comparative Neurology 221, 371–381.Google Scholar
Eldred, W.D. & Karten, H.J. (1985). Ultrastructure and synaptic contacts of enkephalinergic amacrine cells in the retina of turtle (Pseudemys scripta). Journal of Comparative Neurology 232, 36–42.Google Scholar
Eldred, W.D. & Carraway, R.E. (1987). Neurocircuitry of two types of neurotensin containing amacrine cells in the turtle retina. Neuroscience 21, 603–618.CrossRefGoogle ScholarPubMed
Eldred, W.D., Howard, E. & Polak, J.M. (1985). Quantitative analysis of neuropeptide-Y containing amacrine cells in the turtle retina. Society for Neuroscience Abstracts 1216.Google Scholar
Eldred, W.D., Isayama, T., Reiner, A. & Carraway, R.E. (1987). Ganglion cells in the turtle retina contain the neuropeptide LANT-6. Journal of Neuroscience (in press).Google Scholar
Eldred, W.A. & Williamson, D. (1987). Corticotropin releasing factor containing amacrine cells in turtle retina. Investigative Ophthalmology and Visual Science (Suppl.) 28, 351.Google Scholar
Famglietti, E.V. (1987). The ganglion cells of the rabbit retina: shape, stratification of dendritic trees, and relationship to cholinergic amacrine cells. Investigative Ophthalmology and Visual Science (Suppl.) 28, 279.Google Scholar
Fujimoto, K., Yanase, T. & Hanaoka, T. (1957). Spectral transmittance of retinal colored oil globules reexamined with microspectrophotometer. Japanese Journal of Physiology 7, 339–346.Google Scholar
Fulbrook, J.E. (1982). Motion sensitivity of optic nerve axons in turtle Pseudemys scripta elegans. Dissertation, University of Delaware.Google Scholar
Fuortes, M.G.F. & Simon, E.J. (1974). Interactions leading to horizontal cell responses in the turtle retina. Journal of Physiology (London) 240, 177–198.Google Scholar
Gerschenfeld, H.M. & Piccolino, M. (1977). Muscarinic antagonists block cone to horizontal cell transmission in the turtle retina. Nature 268, 257–259.CrossRefGoogle ScholarPubMed
Gerschenfeld, H.M., Neyton, J., Piccolino, M. & Witkovsky, P. (1982). L-horizontal cells of the turtle: network organization and coupling modulation. Biomedical Research 3, 21–34.Google Scholar
Itzhaki, A. & Perlman, I. (1984). Light adaptation in luminosity horizontal cells in the turtle retina. Vision Research 24, 1119–1126.Google Scholar
Itzhaki, A. & Perlman, I. (1987). Light adaptation of red cones and LI horizontal cells in the turtle retina: effects of the background spatial pattern. Vision Research 27, 685–696.CrossRefGoogle Scholar
James, W.M. & Klein, W.L. (1985). α-Bungarotoxin receptors on neurons isolated from turtle retina: molecular heterogeneity of bipolar cells. Journal of Neuroscience 5, 352–361.CrossRefGoogle ScholarPubMed
Jensen, R.J. & DeVoe, R.D. (1982). Ganglion cells and (dye-coupled) amacrine cells in the turtle retina that have possible synaptic connection. Brain Research 240, 146–150.CrossRefGoogle ScholarPubMed
Jensen, R.J. & DeVoe, R.D. (1983). Comparisons of directionally selective with other ganglion cells of the turtle retina: intracellular recording and staining. Journal of Comparative Neurology 217, 271–287.Google Scholar
Kaneko, A., Tachibana, M. & Ohtsuka, T. (1985). GABA sensitivity in solitary turtle cones: evidence for the feedback pathways from horizontal cells to cones. In Neurocircuilry of the Retina: A Cajal memorial, eds. Gallego, A. & Gouras, P., pp. 89–98. New York: Elsevier.Google Scholar
Kaneko, A. & Tachibana, M. (1987). Effects of L-glutamate on isolated turtle photoreceptors. Investigative Ophthalmology and Visual Science (Suppl.) 28, 50.Google Scholar
Kolb, H. (1982). The morphology of the bipolar cells, amacrine cells, and ganglion cells in the retina of the turtle (Pseudemys scripta elegans). Philosophical Transactions of the Royal Society B 298, 355–393.Google ScholarPubMed
Kolb, H., Nelson, R. & Mariani, A. (1981). Amacrine cells, bipolar cells, and ganglion cells of the cat retina: a Golgi study. Vision Research 21, 1081–1114.Google Scholar
Kolb, H. & Jones, J. (1982). Light and electron microscopy of the photoreceptors in the retina of the red-eared slider (Pseudemys scripta elegans). Journal of Comparative Neurology 209, 331–338.CrossRefGoogle ScholarPubMed
Kolb, H. & Jones, J. (1984). Synaptic organization of the outer plexiform layer of the turtle retina: an electron microscope study of serial sections. Journal of Neurocytology 13, 567–591.CrossRefGoogle ScholarPubMed
Kolb, H. & Nelson, R. (1985). Functional neurocircuitry of amacrine cells in the cat retina. In Neurocircuitry of the Retina: A Cajal Memorial, eds. Gallego, A. & Gouras, P., pp. 215–232. New York: Elsevier Press.Google Scholar
Kolb, H., Wang, H.H. & Jones, J. (1986 a). Cone synapses with Golgistained bipolar cells that are morphologically similar to a center-hyperpolarizing and a center-depolarizing cell type in the turtle retina. Journal of Comparative Neurology 250, 510–520.CrossRefGoogle Scholar
Kolb, H., Linberg, K.A. & Fisher, S.K. (1986 b). A Golgi study of ganglion cells in the human retina. Investigative Ophthalmology and Visual Science (Suppl.) 27, 203.Google Scholar
Kolb, H. & Jones, J. (1987). The distinction by light and electron microscopy of two types of cone containing colorless oil droplets in the retina of the turtle. Vision Research 27, 1445–1458.Google Scholar
Kolb, H., Cline, C, Wang, H.H. & Brecha, N. (1987). The distribution of dopaminergic amacrine cells in the retina of the turtle (Pseudemys scripta elegans). Journal of Neurocytology 16, 577–588.Google Scholar
Lam, D.M.K. (1972). The biosynthesis of acetylcholine in turtle photoreceptors. Proceedings of the National Academy of Science of the U.S.A. 69, 1987–1991.CrossRefGoogle ScholarPubMed
Lam, D.M.K., Lasater, E.M. & Naka, K-I. (1978). 7-aminobutyric acid: a neurotransmitter candidate for cone horizontal cells of the catfish retina. Proceedings of the National Academy of Science of the U.S.A. 75, 6310–6313.Google Scholar
Lasansky, A. (1971). Synaptic organization of cone cells in the turtle retina. Philosophical Transactions of the Royal Society B 262, 365–381.Google Scholar
Leeper, H.F. (1978 a). Horizontal cells of the turtle retina. I. Light microscopy of Golgi preparations. Journal of Comparative Neurology 182, 777–794.Google Scholar
Leeper, H.F. (1978 b). Horizontal cells of the turtle retina. II. Analysis of interconnections between photoreceptor cells and horizontal cells by light microscopy. Journal of Comparative Neurology 182, 795–810.CrossRefGoogle ScholarPubMed
Leeper, H.F. & Copenhagen, D.R. (1979). Mixed rod-cone responses in horizontal cells of snapping turtle retina. Vision Research 19, 407–412.CrossRefGoogle ScholarPubMed
Linberg, K.A., Fisher, S.K. & Kolb, H. (1986). A Golgi study of amacrine cells in the human retina. Investigative Ophthalmology and Visual Science (Suppl.) 27, 203.Google Scholar
Liebman, P.A. (1972). Microspectrophotometry of photoreceptors. In Handbook of Sensory Physiology, vol. VII/I, pp. 481–528. Berlin: Springer.Google Scholar
Liebman, P.A. & Granda, A.M. (1971). Microspectrophotometric measurements of visual pigments of two species of turtle (Pseudemys scripta and Chelonia mydas). Vision Research 11, 105–114.Google Scholar
Lipetz, L.E. (1985). Some neuronal circuits of the turtle retina. In The Visual System, eds. Fein, A. & Levine, J.S., pp. 107–132. New York: Alan R. Liss, Inc.Google Scholar
Lipetz, L.E. & MacNichol, E.F. Jr. (1982 a). Photoreceptor types and their visual pigments in a turtle. Investigative Ophthalmology and Visual Science (Suppl.) 22, 120.Google Scholar
Lipetz, L.E. & MacNichol, E.F. Jr. (1982 b). Photoreceptors of freshwater turtles: cell types and visual pigments. Biology Bulletin 163, 396.Google Scholar
Lipetz, L.E. & MacNichol, E.F. Jr. (1983). Visual pigments of two freshwater turtles. Biophysical Journal 41 (2/2), 26a.Google Scholar
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
Marchlafava, P.L. (1979). The responses of retinal ganglion cells to stationary and moving visual stimuli. Vision Research 19, 1203–1212.CrossRefGoogle Scholar
Marchiafava, P.L. (1983). The organization of inputs establishes two functional and morphologically identifiable classes of ganglion cells in the retina of the turtle. Vision Research 23, 325–338.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 of London B 208, 103–113.Google Scholar
Marchiafava, P.L. & Weiler, R. (1982). The photoresponses of structurally identified amacrine cells in the turtle retina. Proceedings of the Royal Society of London B 214, 403–415.Google ScholarPubMed
Massey, S.C. & Redburn, D.A. (1987). Transmitter circuits in the vertebrate retina. Progress in Neurobiology 28, 55–96.Google Scholar
Miller, W.H., Hashimoto, Y., Saito, T. & Tomita, T. (1973). Physiological and morphological identification of L- and C-type S-potentials in the turtle retina. Vision Research 13, 443–447.CrossRefGoogle ScholarPubMed
Miller, R.F. & Bloomfteld, S.A. (1983). Electroanatomy of a unique amacrine cell in the rabbit retina. Proceedings of the National Academy of Science of the U.S.A. 80, 3069–3073.Google Scholar
Miller, R.F. & Slaughter, M.M. (1985). Excitatory amino acid receptors in the vertebrate retina. In Retinal Transmitters and Modulators: Models for the Brain, ed. Morgan, W.W., vol. II, pp. 123–160. Boca Raton, Florida: CRC Press.Google Scholar
Nelson, R., Famiglietti, E.V. & Kolb, H. (1978). Intracellular staining reveals different levels of stratification for on- and off-center ganglion cells in cat retina. Journal of Neurophysiology 41, 472–483.CrossRefGoogle ScholarPubMed
Nelson, R. (1982). All amacrine cells quicken time course of rod signals in the cat retina. Journal of Neurophysiology 47, 928–947.Google Scholar
Nelson, R. & Kolb, H. (1985). A17: a broad-field amacrine cell in the rod system of the cat retina. Journal of Neurophysiology 54, 592–614.Google Scholar
Nguyen-Legros, J., Versaux-Botteri, C, Vigny, A. & Raoux, N. (1985). Tyrosine hydroxylase immunohistochemistry fails to demonstrate dopaminergic interplexiform cells in the turtle retina. Brain Research 339, 323–328.Google Scholar
Normann, R.A., Perlman, I. & Daly, S.J. (1986). The effects of continuous superfusion of L-aspartate and L-glutamate on horizontal cells of the turtle retina. Vision Research 26, 259–268.CrossRefGoogle ScholarPubMed
Ohtsuka, T. (1978). Combination of oil droplets with different types of photoreceptor in a fresh-water turtle (Geoclemys reevesii). Sensory Processes 2, 321–325.Google Scholar
Ohtsuka, T. (1983). Axons connecting somata and axon terminals of luminosity-type horizontal cells in the turtle retina: receptive field studies and intracellular injections of HRP. Journal of Comparative Neurology 220, 191–198.Google Scholar
Ohtsuka, T. (1985 a). Relation of spectral types to oil droplets in cones of turtle retina. Science 229, 874–877.Google Scholar
Ohtsuka, T. (1985 b). Spectral sensitivities of seven morphological types of photoreceptors in the retina of the turtle (Geoclemys reevesii). Journal of Comparative Neurology 237, 145–154.CrossRefGoogle ScholarPubMed
Ohtsuka, T. & Kouyama, N. (1986). Electron microscopic study of synaptic contacts between photoreceptors and HRP-filled horizontal cells in the turtle retina. Journal of Comparative Neurology 250, 141–156.CrossRefGoogle ScholarPubMed
Perlman, I. & Normann, R.A. (1979). Short-wavelength input to luminosity-type horizontal cells in the turtle retina. Vision Research 19, 903–906.Google Scholar
Perlman, I., Normann, R.A. & Anderton, P.J. (1987). The effects of prolonged superfusions with acidic amino acids and their agonists on field potentials and horizontal cell photoresponses in the turtle retina. Journal of Neurophysiology, 57, 1022–1032.CrossRefGoogle ScholarPubMed
Sarthy, P.V. & Lam, D.M.K. (1979 b). Endogenous levels of neurotransmitter candidates in photoreceptor cells of the turtle retina. Journal of Neurochemistry 32, 455–461.Google Scholar
Schutte, M. & Weiler, R. (1987). Morphometric analysis of serotonergic bipolar cells in the retina and its implications for retinal image processing. Journal of Comparative Neurology 260, 619–626.Google Scholar
Tachibana, M. & Kaneko, A. (1984). γ-aminobutyric acid acts at axon terminals of turtle photoreceptors: difference in sensitivity among cell types. Proceedings of the National Academy of Science of the U.S.A. 81, 7961–7964.CrossRefGoogle ScholarPubMed
Wagner, H.-J. & Wagner, E. (1987). Differentiation and layering of amacrine cells in the roach. Investigative Ophthalmology and Visual Science (Suppl.) 28, 262.Google Scholar
Weiler, R. (1985). Afferent and efferent peptidergic pathways in the turtle retina. In Neurocircuitry of the Retina: A Cajal Memorial, eds. Gallego, A. & Gouras, P., pp. 245–256. New York: Elsevier.Google Scholar
Weiler, R. & Marchiafava, P.L. (1981). Physiological and morphological study of the inner plexiform layer in the turtle retina. Vision Research 21, 1635–1638.CrossRefGoogle ScholarPubMed
Weiler, R. & Ball, A.K. (1984). Colocalization of neurotensin-like immunoreactivity and 3H-glycine uptake system in sustained amacrine cells of turtle retina. Nature 311, 759–761.Google Scholar
Weiler, R. & Schutte, M. (1985). Morphological and pharmacological analysis of putative serotonergic bipolar and amacrine cells in the retina of a turtle (Pseudemys scripta elegans). Cell Tissue Research 241, 373–382.Google Scholar
Weiler, R. & Ammermuller, J. (1986). Immunocytochemical localization of serotonin in intracellularly analyzed and dye-injected ganglion cells of the turtle retina. Neuroscience Letters 72, 147–152.CrossRefGoogle ScholarPubMed
Witkovsky, P., Eldred, W. & Karten, H.J. (1984). Catecholamine and indoleamine-containing neurons in the turtle retina. Journal of Comparative Neurology 228, 217–225.Google Scholar
Witkovsky, P., Alones, V. & Piccolino, M.Morphological changes induced in turtle retinal neurons by exposure to 6-hydroxydopamine and 5–6-dihydroxytryptamine. Journal of Neurocytology 16, 55–67.Google Scholar
Yazulla, S. (1976). Cone input to horizontal cells in the turtle retina. Vision Research 16, 727–735.Google Scholar
Yazulla, S. (1986). GABAergic mechanisms in the retina. Progress in Retinal Research 5, 1–52.Google Scholar