Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-27T05:09:48.814Z Has data issue: false hasContentIssue false

Synaptic inputs to physiologically defined turtle retinal ganglion cells

Published online by Cambridge University Press:  02 June 2009

Jay F. Muller
Affiliation:
Department of Physiology, University of Utah School of Medicine, Salt Lake City
Josef Ammermüller
Affiliation:
Department of Neurobiology, University of Oldenburg, Oldenburg, Germany
Richard A. Normann
Affiliation:
Department of Physiology, University of Utah School of Medicine, Salt Lake City Department of Bioengineering, University of Utah, Salt Lake City
Helga Kolb
Affiliation:
Department of Physiology, University of Utah School of Medicine, Salt Lake City

Abstract

Two physiologically distinct, HRP-marked turtle retinal ganglion cells were examined for their morphology, GABAergic, glycinergic, and bipolar cell synaptic inputs, using electron-microscopic autoradiography and postembedding immunocytochemistry. One cell was a color-opponent, transient ON/OFF ganglion cell. Its center response to red was a sustained hyperpolarization, and its center response to green was a depolarization with increased spiking at onset. The HRP-injected cell most resembled G6, from previous Golgi-impregnation studies (Kolb, 1982; Kolb et al., 1988). It was a narrow-field bistratified cell, whose two broad dendritic strata peaked at approximately levels L20–25 (sublamina a) and L60 (sublamina b) of the inner plexiform layer. Bipolar cell synapses onto G6 were found evenly distributed between its distal and proximal dendritic strata, spanning L20–75. These inputs probably originated from several different bipolar cells, reflecting the complexity of the center response. GABAergic inputs were found onto both the distal and proximal strata, from near L20–L85. Only a few glycinergic inputs, confined to dendrites at L50–70, were observed.

A second ganglion cell type that we physiologically characterized and HRP-injected had sustained ON-center, sustained OFF-surround responses. Two examples were studied; both were bistratified in sublamina b, near L60–70 and L85–100, with branches up to near L40. They resembled G10, from previous Golgi-impregnation studies (Kolb, 1982; Kolb et al., 1988). One cell was partially reconstructed to look at the distributions of GABAergic and glycinergic amacrine cell, and bipolar cell inputs. Although synapses from bipolar cells were equally divided between the two major dendritic strata of G10, the inputs to the distal stratum were close to the soma, and the inputs to the more proximal stratum were on the peripheral dendrites. This arrangement may reflect input from two distinct types of ON-bipolar cell. GABAergic and glycinergic inputs to G10 costratified to both strata and to the distal branches; but where glycinergic inputs were found distributed throughout the arbor, GABAergic inputs appeared to be confined to peripheral dendrites. We hypothesize on the neural elements involved and the circuitry that may underlie the physiologically recorded receptive fields of these two very different ganglion cell types in the turtle retina.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1991

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

Adolph, A.R. (1989). Pharmacological actions of peptides and indoleamines on turtle retinal ganglion cells. Visual Neuroscience 3, 411423.CrossRefGoogle ScholarPubMed
Ammermüller, J. & Weiler, R. (1988). Physiological and morphological characterization of OFF-center amacrine cells in the turtle retina. Journal of Comparative Neurology 273, 137148.CrossRefGoogle ScholarPubMed
Ammermüller, J. & Weiler, R. (1989). Correlation between electro-physiological responses and morphological classes of turtle retinal amacrine cells. In Neurobiology of the Inner Retina, ed. Weiler, R. & Osborne, N., pp. 117132. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Ariel, M. & Adolph, A.R. (1985). Neurotransmitter inputs to directionally sensitive turtle retinal ganglion cells. Journal of Neurophysiology 54, 11231143.CrossRefGoogle ScholarPubMed
Bouteille, M. (1976). The “LIGOP” method for routine ultrastructural autoradiography: a combination of single grid coating, gold laten-sification, and phenidon development. Journal de Microscopie et de Biologie Celluaire 27, 121128.Google Scholar
Bowling, D.B. (1980). Light responses of ganglion cells in the retina of the turtle. Journal of Physiology 299, 173196.CrossRefGoogle ScholarPubMed
Daw, N.W. (1968). Colour-coded ganglion cells in the goldfish retina: extension of their receptive fields by way of new stimuli. Journal of Physiology 197, 567592.CrossRefGoogle Scholar
Djamgoz, M.B.A. & Ruddock, K.H. (1983). Spectral characteristics of transient amacrine cells in a cyprinid fish (roach) retina in vitro. Journal of Physiology (London) 339, 19P.Google Scholar
Djamgoz, M.B.A., Spadavecchia, L., Usai, C. & Vallerga, S. (1990). Variability of light-evoked response pattern and morphological characterization of amacrine cells in goldfish retina. Journal of Comparative Neurology 301, 171190.CrossRefGoogle ScholarPubMed
Eldred, W.D. & Cheung, K. (1989). Immunocytochemical localization of glycine in the retina of the turtle (Pseudemys scripta). Visual Neuroscience 2, 331338.CrossRefGoogle ScholarPubMed
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, 371381.CrossRefGoogle ScholarPubMed
Fain, G.L. (1977). The threshold signal of photoreceptors. In Vertebrate Photoreceptors, ed. Barlow, H.B., pp. 305323. London: Academic.Google Scholar
FamigliettiE.V., Jr. E.V., Jr., Kaneko, A. & Tachibana, M. (1977). Neuronal architecture of on and off pathways to ganglion cells of the carp retina. Science 198, 12671269.CrossRefGoogle Scholar
Frumkes, T.E., Miller, R.F., Slaughter, M. & Dacheux, R.F. (1981). Physiological and pharmacological basis of GABA and glycine action on neurons of the mudpuppy retina. III. Amacrine-mediated inhibitory influences on ganglion cell receptive field organization: a model. Journal of Neurophysiology 45, 783805.CrossRefGoogle ScholarPubMed
Gouras, P. (1968). Identification of cone mechanisms in monkey ganglion cells. Journal of Physiology 199, 533547.CrossRefGoogle ScholarPubMed
Granda, A.M. & Fulbrook, J.E. (1989). Classification of turtle retinal ganglion cells. Journal of Neurophysiology 62, 723737.CrossRefGoogle ScholarPubMed
Guiloff, G.D., Jones, J. & Kolb, H. (1988). Organization of the inner plexiform layer of the turtle retina: an electron microscopic study. Journal of Comparative Neurology 272, 280292.CrossRefGoogle ScholarPubMed
Hare, W.A., Lowe, J.S. & Owen, G. (1986). Morphology of physio-logically identified bipolar cells in the retina of the tiger salamander, Ambystoma tigrinum. Journal of Comparative Neurology 252, 130138.CrossRefGoogle Scholar
Hendrickson, A.E., Koontz, M.A., Pourcho, R.G., Sarthy, P.V. & Goebel, D.J. (1988). Localization of glycine-containing neurons in the Macaca monkey retina. Journal of Comparative Neurology 273, 473487.CrossRefGoogle ScholarPubMed
Hurd, L.D., II & Eldred, W.D. (1989). Localization of GABA- and GAD-like immunoreactivity in the turtle retina. Visual Neuroscience 3, 920.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, 146150.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, 271287.CrossRefGoogle ScholarPubMed
Kelly, J.S. & Weitsch-Dick, F. (1978). Critical evaluation of the use of radioautography as a tool in the localization of amino acids in the mammalian nervous system. In Amino Acids as Chemical Transmitters, ed. Fonnum, F., pp. 102121. New York: Plenum.Google Scholar
Kleinschmidt, J. & Yazulla, S. (1984). Uptake of 3H-glycine in the outer plexiform layer of the toad (Bufo marinus). Journal of Comparative Neurology 230, 352360.CrossRefGoogle ScholarPubMed
Koch, C., Poggio, T. & Torre, V. (1986). Computations in the vertebrate retina: gain enhancements, differentiation, and motion discrimination. Trends in Neuroscience 9, 204210.CrossRefGoogle 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 (London) 298, 355393.Google Scholar
Kolb, H. & Nelson, R. (1985). Functional neurocircuitry of amacrine cells in the cat retina. In Neurocircuitry of the Retina: A Cajal Memorial, ed. Gallego, A., pp. 215232. New York: Elsevier.Google Scholar
Kolb, H., Perlman, I. & Normann, R.A. (1988). Neural organization of the retina of the turtle Mauremys capsica: a light-microscope and Golgi study. Visual Neuroscience 1, 4772.CrossRefGoogle Scholar
Kolb, H.K., Wang, H.H. & Jones, J. (1986). Cone synapses with Golgistained bipolar cells that are morphologically similar to a center-hyperpolarizing and a center-depolarizing bipolar cell type in the turtle retina. Journal of Comparative Neurology 250, 510520.CrossRefGoogle Scholar
Lipetz, L.E. & Hill, R.M. (1970). Discrimination characteristics of the turtle's retinal ganglion cells. Experientia 26, 373374.CrossRefGoogle ScholarPubMed
Maguire, G., Lukasiewicz, P., Wu, S. & Werblin, F. (1989). Physiological characterization of biochemically and morphologically identified sustained amacrine cells in the tiger salamander retina. Investigative Ophthalmology and Visual Science (Suppl.) 30, 62.Google Scholar
Marc, R.E. (1985). The role of glycine in retinal circuitry. In Retinal Neurotransmitters and Modulators: Models for the Brain Vol. 2, ed. Morgan, W.W., pp. 119158. Boca Raton, Florida: CRC Press.Google Scholar
Marc, R.E. (1986). Neurochemical stratification of the inner plexiform layer of the vertebrate retina. Vision Research 26, 223238.CrossRefGoogle ScholarPubMed
Marc, R.E. (1989). The anatomy of multiple GABAergic and glycinergic pathways in the inner plexiform layer of the goldfish retina. In The Neurobiology of the Inner Retina, ed. Weiler, R. & Osborne, N., pp. 5364. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Marc, R.E. & Lam, D.M.K. (1981). Glycinergic pathways in the goldfish retina. Journal of Neuroscience 1, 152165.CrossRefGoogle ScholarPubMed
Marc, R.E. & Liu, W.-L. (1985). (3H) Glycine-accumulating neurons of the human retina. Journal of Comparative Neurology 232, 241260.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, 221246.CrossRefGoogle ScholarPubMed
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, 325338.CrossRefGoogle ScholarPubMed
Marchiafava, P.L. & Wagner, H.G. (1981). Interactions leading to color opponency in ganglion cells of the turtle retina. Proceedings of the Royal Society B (London) 211, 261267.Google Scholar
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, 103113.Google Scholar
Mariani, A.P. & Caserta, M.T. (1986). Electron microscopy of glutamate decarboxylase (GAD) immunoreactivity in the inner plexiform layer of the rhesus monkey retina. Journal of Neurocytology 15, 645655.CrossRefGoogle ScholarPubMed
Marshak, D., Ariel, M. & Brown, E. (1988). Distribution of synaptic inputs onto goldfish retinal ganglion cell dendrites. Experimental Eye Research 46, 965978.CrossRefGoogle ScholarPubMed
Massey, S.C. & Miller, R.F. (1988). Glutamate receptors of ganglion cells in the rabbit retina: evidence for glutamate as a bipolar cell transmitter. Journal of Physiology 405, 635655.CrossRefGoogle ScholarPubMed
Miller, R.F. (1979). The neuronal basis of ganglion cell receptive field organization and the physiology of amacrine cells. In The Neurosciences Fourth Study Program, ed. Schmitt, F.O., pp. 227245. Cambridge, Massachusetts: MIT Press.Google Scholar
Miller, R.F. & Dacheux, R.F. (1976). Synaptic organization and ionic basis of on and off channels in mudpuppy retina. III. A model of ganglion cell receptive field organization based on chloride-free experiments. Journal of General Physiology 67, 679690.CrossRefGoogle Scholar
Miller, R.F. & Slaughter, M.M. (1986). Excitatory amino acid receptors of the retina: diversity of subtypes and conductive mechanisms. Trends in Neuroscience 9, 211213.CrossRefGoogle Scholar
Mosinger, J.L., Yazulla, S. & Studholme, K.M. (1986). GABA-like immunoreactivity in the vertebrate retina: a species comparison. Experimental Eye Research 42, 631644.CrossRefGoogle ScholarPubMed
Muller, J.F. & Marc, R.E. (1984). Three distinct morphological classes of receptors in fish olfactory organs. Journal of Comparative Neurology 222, 482495.CrossRefGoogle ScholarPubMed
Muller, J.F. & Marc, R.E. (1990). GABAergic and glycinergic pathways in the inner plexiform layer of the goldfish retina. Journal of Comparative Neurology 291, 281304.CrossRefGoogle ScholarPubMed
Muller, J.F., Ammermüller, J., Kolb, H. & Normann, R.A. (1989). Physiological, anatomical and neurochemical studies on turtle amacrine and ganglion cells. Investigative Ophthalmology and Visual Science (Suppl.) 30, 122.Google Scholar
Nelson, R., Famiglietti, E.V. Jr & Kolb, H. (1978). Intracellular staining reveals different levels of stratification for on- and off-center ganglion cells in cat retina. Journal of Neurophysiology 41, 472483.CrossRefGoogle ScholarPubMed
Pourcho, R.G. & Goebel, D.J. (1987). Visualization of endogenous glycine in cat retina: an immunocytochemical study with Fab fragments. Journal of Neuroscience 7, 11891197.CrossRefGoogle ScholarPubMed
Pourcho, R.G. & Owczarzak, M.T. (1989). Distribution of GABA immunoreactivity in the cat retina: a light and electron microscopic study. Visual Neuroscience 2, 425435.CrossRefGoogle ScholarPubMed
Slaughter, M.M. & Miller, R.F. (1981). 2-Amino-4-phosphonobutyric acid: a new pharmacological tool for retina research. Science 211, 182184.CrossRefGoogle ScholarPubMed
Slaughter, M.M. & Miller, R.F. (1983a). An excitatory amino-acid antagonist blocks cone input to sign-conserving second-order retinal neurons. Science 219, 12301232.CrossRefGoogle ScholarPubMed
Slaughter, M.M. & Miller, R.F. (1983b). Bipolar cells in the mudpuppy retina use an excitatory amino acid neurotransmitter. Nature 303, 537538.CrossRefGoogle ScholarPubMed
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, 79617964.CrossRefGoogle ScholarPubMed
Watanabe, S.-I. & Murakami, M. (1985). Electrical properties of on-off transient amacrine cells in the carp retina. Neuroscience Research (Suppl.) 2, S201–S210.Google ScholarPubMed
Weiler, R. (1981). The distribution of center-depolarizing and center-hyperpolarizing bipolar cell ramifications within the inner plexiform layer of turtle retina. Journal of Comparative Physiology A 144, 459464.CrossRefGoogle Scholar
Yazulla, S. (1976). Cone input to bipolar cells in the turtle retina. Vision Research 16, 737744.CrossRefGoogle ScholarPubMed
Yazulla, S. (1986). GABAergic mechanisms in the retina. In Progress in Retinal Research, Vol. 5, ed. Osborne, N., pp. 152. Oxford: Pergamon.Google Scholar
Yazulla, S. & Studholme, K.M. (1990). Multiple subtypes of glycineimmunoreactive neurons in the goldfish retina: single and double-label studies. Visual Neuroscience 4, 299309.CrossRefGoogle ScholarPubMed