Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-19T18:01:46.081Z Has data issue: false hasContentIssue false
  • English
  • Français

Synaptic microcircuitry of bipolar and amacrine cells with serotonin-like immunoreactivity in the retina of the turtle, Pseudemys scripta elegans

Published online by Cambridge University Press:  02 June 2009

Lawrence B. Hurd II  and
William D. Eldred
Lawrence B. Hurd II
Affiliation:
Department of Anatomy and Neurobiology, Boston University School of Medicine, Boston
William D. Eldred
Affiliation:
Department of Biology, Boston University, Boston
Get access Rights & Permissions [Opens in a new window]

Abstract

Although serotonin is thought to be a neurotransmitter in a number of retinal systems, much of the precise synaptic connectivity of serotonergic neurons is unknown. To address this issue, we used an antiserum directed against serotonin to label serotonergic bipolar and amacrine cells in the turtle retina. Light-microscopic analysis of labeled amacrine and bipolar cells indicated that both had bistratified dendritic arborizations primarily in stratum 1 and in strata 4/5 of the inner plexiform layer.

Ultrastructural analysis of the neurocircuitry of these cells indicated that the processes of labeled bipolar cells in the outer plexiform layer made basal junction contacts with photoreceptor terminals. Only in rare instances did labeled bipolar cells processes invaginate near photoreceptor ribbon synapses. Processes of labeled bipolar cells received both conventional and small ribbon synaptic contacts in the outer plexiform layer. Bipolar cell processes in stratum 1 of the inner plexiform layer synapsed onto either amacrine/amacrine or amacrine/ganglion cell dyads, and made rare ribbon synaptic contacts onto labeled amacrine cell processes. Synaptic inputs to serotonergic bipolar cells in stratum 1 were from unlabeled bipolar and amacrine cells. Bipolar cell contacts in strata 4/5 were similar to those in stratum 1, but were fewer in number and no bipolar cell inputs were seen.

Labeled amacrine cell output in both strata was onto other unlabeled amacrine cells and ganglion cells; but synaptic outputs to unlabeled bipolar cells were only seen in strata 4/5. In both strata 1 and 4/5, synaptic inputs to labeled amacrine cells were from both unlabeled amacrine cells and labeled bipolar cells. The serotonergic amacrine cells had many more synaptic interactions in stratum 1 than in strata 4/5 which supports the role of serotonergic bipolar cells in the OFF pathway of retinal processing. Interactions between serotonergic bipolar and amacrine cells may play an important role in visual processing.

Keywords

IndoleaminesVertebrate retina5-HydroxytryptamineNeurocircuitry
Type
Articles
Information
Visual Neuroscience , Volume 10 , Issue 3 , May 1993 , pp. 455 - 471
Copyright
Copyright © Cambridge University Press 1993

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

Ammermüller, J., Kolb, H., Normann, R.A. & Weiler, R. (1991). Physiological sublamination of the inner plexiform layer (IPL) in the turtle retina. Society for Neuroscience Abstracts 17, 1014.Google Scholar
Ammermüller, J. & Weiler, R. (1988). Physiological and morphological characterization of OFF-center amacrine cells in the turtle retina. Journal of Comparative Neurology 273, 137–148.CrossRefGoogle ScholarPubMed
Baumgarten, H.G., Klemm, H.P. & Schlossberger, H.G. (1984). In vivo metabolism of 14C-5-HT, 14C-5,6-DHT and 14C-5,7-DHT by MAO/COMT/Aldehyde dehydrogenase in rat brain. In Progress in Tryptophan and Serotonin Research, ed. Schlossberger, H.G., Kochen, W., Linzen, B. & Steihart, H., pp. 214–249. Berlin, New York: W. de Gruyter.Google Scholar
Brunken, W.J., Witkovsky, P. & Sytsma, V.M. (1984). Retinal neurochemistry of three elasmobranch species: An immunohistochemical approach. Journal of Comparative Neurology 243, 1–12.Google Scholar
Bruun, A., Ehinger, B. & Sytsma, V.M. (1984). Neurotransmitter localization in the skate retina. Brain Research 295, 233–248.CrossRefGoogle ScholarPubMed
Cajal, S.R.y. (1933). Die retina der wirbeltiere. Wiesbaden: Bergmann. (Translation: Thorpe, S.A. & Glickstein, M. (1972). The Structure of the Retina. Springfield: Thomas).Google Scholar
Cuenca, N. & Kolb, H. (1989). Morphology and distribution of neurons immunoreactive for substance P in the turtle retina. Journal of Comparative Neurology 290, 391–411.CrossRefGoogle ScholarPubMed
Dacheux, R.F. (1982). Connections of the small bipolar cells with the photoreceptors in the turtle. An electron-microscope study of Golgi-impregnated, gold-toned retinas. Journal of Comparative Neurology 205, 55–62.CrossRefGoogle ScholarPubMed
Dowling, J.E., Ehinger, B. & Floren, I. (1980). Fluorescence and electron-microscopical observations on the amine-accumulating neurons of the cebus monkey retina. Journal of Comparative Neurology 192, 665–685.CrossRefGoogle ScholarPubMed
Ehinger, B. & Floren, I. (1976). Indoleamine-accumulating neurons in the retina of rabbit, cat and goldfish. Cell and Tissue Research 175, 37–48.CrossRefGoogle Scholar
Ehinger, B. & Holmgren, I. (1979). Electron microscopy of the indoleamine-accumulating neurons in the retina of the rabbit. Cell and Tissue Research 197, 175–194.CrossRefGoogle ScholarPubMed
Ehinger, B., Hansson, C. & Tornqvist, K. (1981). 5-Hydroxytrypta-mine in the retina of some mammals. Experimental Eye Research 33, 663–672.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 232, 36–42.CrossRefGoogle Scholar
Eldred, W.D., Zucker, C., Karten, H.J. & Yazulla, S. (1983). Comparison of fixation and penetration enhancement techniques for use in ultrastructural immunocytochemistry. Journal of Histochemistry and Cytochemistry 31(2), 285–292.CrossRefGoogle ScholarPubMed
Eldred, W.D. & Carraway, R.E. (1987). Neurocircuitry of two types of neurotensin-containing amacrine cells in the turtle retina. Neuroscience 21(2), 603–618.CrossRefGoogle ScholarPubMed
Eldred, W.D., Li, H.-B., Carraway, R.E. & Dowling, J.E. (1987). Immunocytochemical localization of LANT-6-like immunoreactivity within neurons in the inner nuclear and ganglion cell layers in vertebrate retinas. Brain Research 424, 361–370.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
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
Famiglietti, E.V., Kaneko, A. & Tachibana, M. (1977). Neuronal architecture of ON- and OFF-pathways to ganglion cells in carp retina. Science 198, 1267–1269.CrossRefGoogle Scholar
Famiglietti, E.V. Jr, & Kolb, H. (1976). Structural basis for ON- and OFF-center responses in retinal ganglion cells. Science 194, 193–195.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. Jr, (1981). Functional architecture of cone bipolar cells in mammalian retina. Vision Research 21, 1559–1563.CrossRefGoogle ScholarPubMed
Frederick, J.M., Rayborn, M.E., & Hollyfield, J.G. (1989). Sero-tonergic neurons in the retina of Xenopus laevis: Selective staining, identification, development, and content. Journal of Comparative Neurology 281, 516–531.CrossRefGoogle Scholar
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, 280–292.CrossRefGoogle ScholarPubMed
Holmgren-Taylor, I. (1982). Electron-microscopical observations on the indoleamine accumulating neurons and their synaptic connections in the retina of the cat. Journal of Comparative Neurology 208, 144–156.CrossRefGoogle ScholarPubMed
Holmgren-Taylor, I. (1983). Synaptic organization of the indoleamine-accumulating neurons in the cyprinid retina. Cell and Tissue Research 229, 317–335.Google ScholarPubMed
Hurd, L.B. & Eldred, W.D. (1989). Localization of GABA- and GAD-like immunoreactivity in the turtle retina. Visual Neuroscience 3, 9–20.CrossRefGoogle ScholarPubMed
Isayama, T. & Eldred, W.D. (1988). Neuropeptide Y-immunoreactive amacrine cells in the retina of the turtle Pseudemys scripta elegans. Journal of Comparative Neurology 271, 56–66.CrossRefGoogle ScholarPubMed
Isayama, T., Polak, J. & Eldred, W.D. (1988). Synaptic analysis of amacrine cells with neuropeptide Y-like immunoreactivity in turtle retina. Journal of Comparative Neurology 275, 452–459.CrossRefGoogle ScholarPubMed
Jaffe, E.H., Urbina, M., Ayala, C. & Chemello, M.E. (1987). Serotonin containing neurons in the retina of the teleost Eugenes plumieri. Vision Research 27(12), 2015–2026.CrossRefGoogle Scholar
Kolb, H. (1979). The inner plexiform layer of the cat: Electron microscopic observations. Journal of Neurocytology 8, 295–329.CrossRefGoogle ScholarPubMed
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, 355–393.Google ScholarPubMed
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., Wang, H.H. & Jones, J. (1986). Cone synapses with Golgi-stained 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, 510–520.CrossRefGoogle 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(5), 577–588.CrossRefGoogle ScholarPubMed
Kolbinger, W. & Weiler, R. (1990). Glutaminergic and serotonergic modulation of endogenous dopamine release in the turtle retina. Investigative Ophthalmology and Visual Science (Suppl.) 31(4), 334 (ARVO Abstract).Google Scholar
Lasansky, A. (1969). Basal junctions at synaptic endings of turtle visual cells. Journal of Cell Biology 40, 577–581.CrossRefGoogle ScholarPubMed
Lasansky, A. (1971). Synaptic organization of cone cells in the turtle retina. Philosophical Transactions of the Royal Society B (London) 262, 365–381.Google Scholar
Lasansky, A. (1972). Cell junctions at the outer synaptic layer of the retina. Investigative Ophthalmology 11(5), 265–275.Google ScholarPubMed
Mangel, S.C. & Brunken, W. J. (1992). The effects of serotonin drugs on horizontal and ganglion cells in the rabbit retina. Visual Neuroscience 8, 213–218.CrossRefGoogle ScholarPubMed
Marc, R.E. (1986). Neurochemical stratification in the inner plexiform layer of the vertebrate retina. Vision Research 22, 589–608.CrossRefGoogle Scholar
Marc, R.E., Liu, W.-L.S., Scholz, K. & Muller, J.F. (1988). Serotonergic and serotonin-accumulating neurons in the goldfish retina. Journal of Neuroscience 8(9), 3427–3450.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
Mariani, A.P. (1987). Neuronal and synaptic organization of the outer plexiform layer of the pigeon retina. American Journal of Anatomy 179, 25–39.CrossRefGoogle ScholarPubMed
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. (1980). Functional stratification of cone bipolar cells in the cat retina. Investigative Ophthalmology and Visual Science (Suppl.) 19, 130 (Abstract).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.CrossRefGoogle ScholarPubMed
Osborne, N.N. (1984). Indoleamines in the eye with special reference to the serotonergic neurones of the retina. In Progress in Retinal Research, Vol. 3, ed. Osborne, N.N. & Chader, G., pp. 61–103. Oxford, New York, Toronto, Sydney, Paris, Frankfurt: Pergamon Press.Google Scholar
Osborne, N.N. (1982). Evidence for serotonin being a neurotransmitter in the retina. In The Biology of Serotonergic Transmission, ed. Osborne, N.N., pp. 401–430. New York: John Wiley & Sons.Google Scholar
Osborne, N.N. & Barnett, N.L. (1990). What constitutes a serotonergic neurone in the retina? Neurochemistry International 17, 177–187.CrossRefGoogle ScholarPubMed
Raviola, E. (1972). Intercellular junctions in the outer plexiform layer of the retina. Investigative Ophthalmology 15(11), 881–894.Google Scholar
Redburn, D.A. (1984). Serotonin systems in the inner and outer plexiform layers of the vertebrate retina. Federation Proceedings 43, 2699–2703.Google ScholarPubMed
Sandell, J.H. & Masland, R.H. (1986). A system of indoleamine-accumulating neurons in the rabbit retina. Journal of Neuroscience 6(11), 3331–3347.CrossRefGoogle ScholarPubMed
Sandell, J.H., Masland, R.H., Raviola, E. & Dacheux, R.F. (1989). Connections of indoleamine-accumulating cells in the rabbit retina. Journal of Comparative Neurology 283, 303–313.CrossRefGoogle ScholarPubMed
Schütte, M. & Witkovsky, P. (1990). Serotonin-like immunoreactivity in the retina of the clawed frog Xenopus laevis. Journal of Neurocytology 19, 504–518.CrossRefGoogle ScholarPubMed
Schütte, 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.CrossRefGoogle Scholar
Schütte, M. & Weiler, R. (1988). Mesencephalic innervation of the turtle retina by a single serotonin-containing neuron. Neuroscience Letters 91, 289–294.CrossRefGoogle ScholarPubMed
Tauchi, M. (1989). Displaced and indoleamine-accumulating bipolar cells in the turtle retina. Neuroscience Research 10, s57–S66.Google ScholarPubMed
Tauchi, M. (1990). Single cell shape and population densities of indoleamine-accumulating and displaced bipolar cells in Reeves’ turtle retina. Proceedings of the Royal Society B (London) 238, 351–367.Google ScholarPubMed
Tornqvist, K., Hansson, C. & Ehinger, B. (1983). Immunohistochemical and quantitative analysis of 5-hydroxytryptamine in the retina of some vertebrates. Neurochemistry International 5, 299–308.CrossRefGoogle ScholarPubMed
Vaney, D.I. (1986). Morphological identification of serotonin-accumulating neurons in the living retina. Science 233, 444–446.Google ScholarPubMed
Wässle, H., Voigt, T. & Patel, B. (1987). Morphological and immunocytochemical identification of indoleamine-accumulating neurons in the cat retina. Journal of Neuroscience 7(5), 1574–1585.CrossRefGoogle ScholarPubMed
Watt, C.B. & Wilson, E.A. (1990). Synaptic organization of serotonin-like immunoreactive amacrine cells in the larval tiger salamander retina. Neuroscience 35, 715–723.CrossRefGoogle 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, 459–464.Google Scholar
Weiler, R. & Ball, A.K. (1984). Co-localization of neurotensin-like immunoreactivity and 3H-glycine uptake system in sustained amacrine cells of turtle retina. Nature 311(5988), 759–761.CrossRefGoogle ScholarPubMed
Weiler, R. & Schütte, M. (1985 a). Kainic acid-induced release of serotonin from OFF-bipolar cells in the turtle retina. Brain Research 360, 379–383.CrossRefGoogle ScholarPubMed
Weiler, R. & Schütte, M. (1985 b). Morphological and pharmacological analysis of putative serotonergic bipolar and amacrine cells in the retina of a turtle, Pseudemys scripta elegans. Cell and Tissue Research 241, 373–382.CrossRefGoogle ScholarPubMed
Weiler, R. & Ammermüller, J. (1986). Immunocytochemical localization of serotonin in intracellularly analyzed and dye-injected ganglion cells of the turtle retina. Neuroscience Letters 72, 147–152.Google ScholarPubMed
Williamson, D.E. & Eldred, 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
Williamson, D. & Eldred, W.D. (1991). The synaptic organization of two types of amacrine cells with CRF-like immunoreactivity in the turtle retina. Visual Neuroscience 6, 257–269.CrossRefGoogle ScholarPubMed
Witkovsky, P., Eldred, W.D. & Karten, H.J. (1984). Catecholamine-and indoleamine-containing neurons in the turtle retina. Journal of Comparative Neurology 228, 217–225.CrossRefGoogle ScholarPubMed
Witkovsky, P., Alines, V. & Piccolino, M. (1987). Morphological changes induced in turtle retinal neurons by exposure to 6-hydroxy-dopamineand 5,6-dihydroxytryptamine. Journal of Neurocytology 16, 55–67.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Zhu, B. & Straznicky, C. (1990). Morphology and distribution of serotonin-like immunoreactive amacrine cells in the retina of Bufo Marinus. Visual Neuroscience 5, 371–378.CrossRefGoogle ScholarPubMed