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Communicating junctions of the human sensory retina

A freeze-fracture study

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Albrecht von Graefes Archiv für klinische und experimentelle Ophthalmologie Aims and scope Submit manuscript

Summary

Using the freeze-fracture technique communicating junctions could be identified between the cells of the adult human sensory retina. Communicating junctions with particles arranged in linear or circular rows as well as in small aggregates were found between adjacent photoreceptor endings. Communicating junctions with particles forming plaques were localized in the inner plexiform layer. They were isolated between unidentified cell processes or lay close to active sites of chemical synapses, thus suggesting the occurrence of “mixed” (chemical and electrical) synapses in this layer. Furthermore, communicating junctions were detected between portions of Müller's cells.

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References

  • Baylor, D.A., Fuortes, M.G.F., O'Bryan, P.M.: Receptive fields of cones in the retina of the turtle. J. Physiol. 214, 265–294 (1971)

    Google Scholar 

  • Bennett, M.V.L.: Function of electrotonic junctions in embryonic and adult tissues. Fed. Proc. 32, 65–75 (1973)

    Google Scholar 

  • Branton, D., Bullivant, S., Gilula, N.B., Karnovsky, M.J., Moor, H., Mühlethaler, K., Northcote, D.H., Paker, L., Satir, B., Satir, P., Speth, V., Staehelin, L.A., Steere, R.L., Weinstein, R.S.: Freeze-etching nomenclature. Science 190, 54–56 (1975)

    Google Scholar 

  • Brightman, M.W., Reese, T.S.: Junctions between intimately apposed cell membranes in the vertebrate brain. J. Cell Biol. 40, 648–677 (1969)

    Google Scholar 

  • Brightman, M.W., Reese, T.S.: Membrane specializations of ependymal cells and astrocytes. In: The Nervous System, D.B. Tower, ed., Vol. 1, The Basic Neurosciences, pp. 267–277. New York: Raven Press 1975

    Google Scholar 

  • Cohen, A.I.: Some electron microscopic observations on interreceptor contacts in the human and macaque retinae. J. Anat. 99, 595–610 (1965)

    Google Scholar 

  • Custer, N.V.: Structurally specialized contacts between the photoreceptors of the retina of the Axolotl. J. Comp. Neurol. 151, 35–56 (1973)

    Google Scholar 

  • Dermietzel, R.: Visualization by freeze-fracturing of regular structures in glial cell membranes. Naturwissensch. 60, 208 (1973)

    Google Scholar 

  • Dermietzel, R.: Junctions in the central nervous system of the cat. III. Gap junctions and membrane-associated orthogonal particle complexes (MOPC) in astrocytic membranes. Cell Tiss. Res. 149, 121–135 (1974)

    Google Scholar 

  • Dowell, W.C.T.: Die Entwicklung geeigneter Folien für elektronenmikroskopische Präparatträger großen Durchlaßbereiches und ihre Verwendung zur Untersuchung von Kristallen. Optik 21, 47–58 (1964)

    Google Scholar 

  • Dowling, J.E.: Organization of vertebrate retinas. Invest. Ophthal. 9, 655–680 (1970)

    Google Scholar 

  • Dowling, J.E., Boycott, B.B.: Neural connection of the retina: fine structure of the inner plexiform layer. Cold Spring Habor Symp. Quant. Biol. 30, 393–402 (1965)

    Google Scholar 

  • Dowling, J.E., Boycott, B.B: Retinal ganglion cells: a correlation of anatomical and physiological approaches. In: The Retina; Morphology, Function and Clinical Characteristics, B.R. Straatsma, M.O. Hall, R.A. Allen, F. Crescitelli, eds., pp. 145–161. Berkeley — Los Angeles: University of California Press 1969

    Google Scholar 

  • Dowling, J.E., Werblin, F.S.: Synaptic organization of vertebrate retina. Vis. Res., Suppl. 3, 1–15 (1971)

    Google Scholar 

  • Fain, G.L., Gold, G.H., Dowling, J.E.: Receptor coupling in the toad retina. Cold Spring Harbor Symp. Quant. Biol. 40, 547–561 (1976)

    Google Scholar 

  • Gilula, N.B.: Junctions between cells. In: Cell communication, R.P. Cox, ed., pp. 1–29. New York: Wiley 1974

    Google Scholar 

  • Gilula, N.B.: Junctional membrane structure. In: The Nervous System, D.B. Tower, ed., Vol. 1, The Basic Neurosciences, pp. 1–11. New York: Raven Press 1975

    Google Scholar 

  • Hanna, R.B., Hirano, A., Pappas, G.D.: Membrane specializations of dendritic spines and glia in the weaver mouse cerebellum: a freeze-fracture study. J. Cell Biol. 68, 403–410 (1976)

    Google Scholar 

  • Hogan, M.J., Alvarado, J.A., Weddel, J.E.: Histology of the human eye. An atlas and textbook. Philadelphia-London-Toronto: Saunders 1971

    Google Scholar 

  • Kaneko, A.: Electrical connexions between horizontal cells in the dogfish retina. J. Physiol. 213, 95–105 (1971)

    Google Scholar 

  • Kolb, H., Famiglietti, E.V., Jr.: Rod and cone pathways in the inner plexiform layer of cat retina. Science 186, 47–49 (1974)

    Google Scholar 

  • Kolb, H., Famiglietti, E.V., Jr.: Rod and cone pathways in the retina of the cat. Invest. Ophthal. 15, 935–946 (1976)

    Google Scholar 

  • Landis, D.M.D., Reese, T.S.: Arrays of particles in freeze-fractured astrocytic membranes. J. Cell Biol. 60, 316–320 (1974)

    Google Scholar 

  • Lasansky, A.: Functional implications of structural findings in retinal glial cells. Progr. Brain Res. 15, 48–72 (1965)

    Google Scholar 

  • Lasansky, A.: Cell junctions at the outer synaptic layer of the retina. Invest. Ophthal. 11, 265–275 (1972)

    Google Scholar 

  • Lasansky, A.: Synaptic actions on retinal photoreceptors: structural aspects. Fed. Proc. 33, 1069–1073 (1974)

    Google Scholar 

  • Lasansky, A.: Interactions between horizontal cells of the salamander retina. Invest. Ophthal. 15, 909–916 (1976)

    Google Scholar 

  • McNutt, N.S.: Freeze-fracture techniques and applications to the structural analysis of the mammalian plasma membrane. In: Dynamic Aspects of Cell Surface Organization, G. Poste, G.L. Nicolson, eds., pp. 75–126. Elsevier/North-Holland: Biomedical Press 1977

    Google Scholar 

  • McNutt, N.S., Weinstein, R.S.: The ultrastructure of the nexus. A correlated thin-section and freezecleave study. J. Cell Biol. 47, 666–688 (1970)

    Google Scholar 

  • Miller, R.F., Dowling, J.E.: Intracellular responses of the Müller (glial) cells of mudpuppy retina: their relation to b-wave of the electroretinogram. J. Neurophysiol. 33, 323–341 (1970)

    Google Scholar 

  • Missotten, L.: The ultrastructure of the human retina. Editions Arscia, Bruxelles 1965

    Google Scholar 

  • Moore, H., Mühlethaler, K.: Fine structure in frozen-etched yeast cells. J. Cell Biol. 17, 609–628 (1963)

    Google Scholar 

  • Nabeshima, S., Reese, T.S., Landis, D.M.D., Brightman, M.W.: Junctions in the meninges and marginal glia. J. Comp. Neurol. 164, 127–170 (1975)

    Google Scholar 

  • Naka, K.I., Rushton, W.A.H.: The generation and spread of S-potentials in fish (cyprinidae). J. Physiol. 192, 437–461 (1967)

    Google Scholar 

  • O'Daly, J.A.: ATPase activity at the functional contacts between retinal cells which produce S-potential. Nature 216, 1329–1331 (1967)

    Google Scholar 

  • Ogden, T.E.: Intraretinal slow potentials evoked by brain stimulation in the primate. J. Neurophysiol. 29, 898–908 (1966)

    Google Scholar 

  • Pannese, E., Luciano, L., Iurato, S., Reale, E.: Intercellular junctions and other membrane specializations in developing spinal ganglia: a freeze-fracture study. J. Ultrastruct. Res. 60, 169–180 (1977)

    Google Scholar 

  • Peters, A., Palay, S.L., Webster, H. de F.: The fine structure of the nervous system: the neurons and supporting cells. Philadelphia-London-Toronto: Saunders 1976

    Google Scholar 

  • Prescott, L., Brightman, M.W.: The sarcolemma of Aplysia smooth muscle in freeze-fracture preparations. Tissue and Cell 8, 241–258 (1976)

    Google Scholar 

  • Raviola, E.: Intercellular junctions in the outer plexiform layer of the retina. Invest. Ophthal. 15, 881–895 (1976)

    Google Scholar 

  • Raviola, E., Gilula, N.B.: Gap junctions between photoreceptor cells in the vertebrate retina. Proc. Nat. Acad. Sci. (USA) 70, 1677–1681 (1973)

    Google Scholar 

  • Raviola, E., Gilula, N.B.: Intramembrane organization of specialized contacts in the outer plexiform layer of the retina. J. Cell Biol. 65, 192–222 (1975)

    Google Scholar 

  • Raviola, E., Raviola, G.: Difference in internal structure of the postsynaptic membrane at ribbon and conventional synapses in the inner plexiform layer of the retina. J. Cell Biol. 67, 355a (1975)

    Google Scholar 

  • Raviola, G.: The structural basis of the blood-ocular barriers. Exp. Eye Res., Suppl. 25, 27–63 (1977)

    Google Scholar 

  • Reale, E., Luciano, L., Spitznas, M.: Introduction to freeze-fracture method in retinal research. Albrecht v. Graefes Arch. Ophthalm. 192, 73–87 (1974)

    Google Scholar 

  • Reale, E., Spitznas, M.: Freeze-fracture analysis of junctional complexes in human ciliary epithelia. Albrecht v. Graefes Arch. Ophthalm. 195, 1–16 (1975)

    Google Scholar 

  • Revel, J.-P., Karnovsky, M.J.: Hexagonal array of subunits in intercellular junctions of the mouse heart and liver. J. Cell Biol. 33, C7-C12 (1967)

    Google Scholar 

  • Sandri, C., Akert, K., Livingston, R.B., Moor, H.: Particle aggregations at specialized sites in freeze-etched post-synaptic membranes. Brain Res. 41, 1–16 (1972)

    Google Scholar 

  • Sandri, C., van Buren, J.M., Akert, K.: Membrane morphology of the vertebrate nervous system. A study with freeze-etch technique. Progr. Brain Res. 46, 1–384 (1977)

    Google Scholar 

  • Simon, E.J.: Two types of luminosity horizontal cells in the retina of the turtle. J. Physiol. 230, 199–211 (1973)

    Google Scholar 

  • Spitznas, M.: Zur Feinstruktur der sog. Membrana limitans externa der menschlichen Retina. Albrecht v. Graefes Arch. Ophthalm. 180, 44–56 (1970)

    Google Scholar 

  • Staehelin, L.A.: Structure and function of intercellular junctions. Internat. Rev. Cytol. 39, 191–283 (1974)

    Google Scholar 

  • Stell, W.K.: The morphological organization of the vertebrate retina. In: Handbook of Sensory Physiology, M.G.F. Fuortes, ed., Vol. VII/2, pp. 111–213. Berlin-Heidelberg-New York: Springer 1972

    Google Scholar 

  • Uga, S., Nakao, F., Mimura, M., Ikui, H.: Some new findings in the fine structure of the human photoreceptor cells. J. Electr. Micros. 19, 71–84 (1970)

    Google Scholar 

  • Uga, S., Smelser, G.K.: Comparative study of the fine structure of retinal Müller cells in various vertebrates. Invest. Ophthal. 12, 434–448 (1973)

    Google Scholar 

  • Weinstein, R.S., Merk, F.B., Alroy, J.: The structure and function of intercellular junctions in cancer. In: Advances in Cancer Research, G. Klein, S. Weinhouse, eds., Vol. 23, pp. 23–89. New York: Academic Press 1976

    Google Scholar 

  • Witkovsky, P., Dowling, J.E.: Synaptic relationships in the plexiform layers of carp retina. Z. Zellforsch. 100, 60–82 (1969)

    Google Scholar 

  • Witkovsky, P., Shakib, M., Ripps, H.: Interreceptoral junctions in the teleost retina. Invest. Ophthal. 13, 996–1009 (1974)

    Google Scholar 

  • Witkovsky, P., Stell, W.K.: Gross morphology and synaptic relationships of bipolar cells in the retina of the smooth dogfish Mustelus canis. Anat. Rec. 169, 456–457 (1971)

    Google Scholar 

  • Yamada, E., Ishikawa, T.: Fine structure of the horizontal cells in some vertebrate retinae. Cold Spring Harbor Symp. Quant. Biol. 30, 383–392 (1965)

    Google Scholar 

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Authors and Affiliations

  1. Laboratory of Electron Microscopy, School of Medicine, Karl-Wiechert-Allee 9, D-3000, Hannover, Germany

    Enrico Reale & Liliana Luciano

  2. University Eye Hospital, Hufelandstr. 55, D-4300, Essen, Germany

    Manfred Spitznas

Authors
  1. Enrico Reale
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  2. Liliana Luciano
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  3. Manfred Spitznas
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Reale, E., Luciano, L. & Spitznas, M. Communicating junctions of the human sensory retina. Albrecht von Graefes Arch. Klin. Ophthalmol. 208, 77–92 (1978). https://doi.org/10.1007/BF00406984

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