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Glial membrane specializations and the compartmentalization of the lamina ganglionaris of the housefly compound eye

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Journal of Neurocytology

Summary

Membrane specializations in the lamina ganglionaris of the housefly are investigated using conventional thin-section EM, freeze-fracture replication and the diffusion of colloidal lanthanum. All glial cells in the lamina are coupled by gap junctions. Desmosomes also link all glia except the epithelial glia. Extensive glia-glial and glia-neuronal septate junctions are present in the pseudocartridge zone and nuclear layer. Septate junctions in the nuclear layer intermingle with bands of interglial and glia-neuronal tight junctions. Tight junctions are also found between satellite and epithelial glia at the border of the nuclear and plexiform layers, between adjacent epithelial glial cells in the plexiform layer, between epithelial and marginal glia at the proximal boundary of the optic neuropil, between marginal glial cells, and between marginal glia and axons. Colloidal lanthanum, introduced through an incision in the cornea, penetrates the retina but is occluded from the neuropil by septate junctions in the pseudocartridge zone. The disposition of tight and septate junctions is described in relation to the compartmentalization of the lamina. Two major compartments are delineated. The first represents the nuclear layer and contains the cell bodies of second-order visual neurons (monopolar neurons). The second compartment constitutes the plexiform layer of the lamina. Within the plexiform layer, each optic cartridge is partitioned into a separate subcompartment. Also, tracheoles and axons of long visual fibres are isolated from the optic cartridges by glial tight junctions. Morphological evidence for compartmentalization is correlated with previously established electrical properties of the insect lamina ganglionaris.

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References

  • Autrum, H., Zettler, F. &Järvilheto, M. (1970) Postsynaptic potentials from a single monopolar neuron of the ganglion opticum I of the blowflyCalliphora.Zeitschrift für vergleichende Physiologie 70, 414–24.

    Google Scholar 

  • Bennet, M. V. L. (1977) Electrical transmission: a functional analysis and comparison to chemical transmission. InHandbook of Physiology. Section 1: The Nervous System Vol. 1 (edited byBrookhart, J. M., Mountcastle, V. B., Kandel, E. R. &Geiger, S. R.), pp. 357–416. Bethesda: American Physiological Society.

    Google Scholar 

  • Boschek, C. B. (1971) On the fine structure of the peripheral retina and lamina ganglionaris of the fly,Musca domestica.Zeitschrift für Zellforschung und mikroskopische Anatomie 118, 369–409.

    Google Scholar 

  • Brightman, M. W. &Reese, T. S. (1969) Junctions between intimately apposed cell membranes in the vertebrate brain.Journal of Cell Biology 40, 648–77.

    Google Scholar 

  • Bullivant, S. &Loewenstein, W. R. (1968) Structure of coupled and uncoupled cell junctions.Journal of Cell Biology 37, 621–32.

    Google Scholar 

  • Burtt, E. T. &Catton, W. T. (1964) The potential profile of the insect compound eye and optic lobe.Journal of Insect Physiology 10, 689–710.

    Google Scholar 

  • Carlson, S. D., Saint Marie, R. L. &Chi, C. (1982) Freeze-fracture replication and the interpretation of glial and neuronal structures in insect nervous tissue. InNeuroanatomical Techniques. Insect Nervous Systems Vol. 2 (edited byStrausfeld, N. J.), Berlin: Springer-Verlag (in press).

    Google Scholar 

  • Carlson, S. D., Saint Marie, R. L. &Chi, C. (1983) The photoreceptor cells. InInsect Ultrastructure Vol. 2 (edited byKing, R. C. &Akai, H.), New York: Plenum Press (in press).

    Google Scholar 

  • Chi, C. &Carlson, S. D. (1980a) Membrane specializations in the first optic neuropil of the housefly,Musca domestica L. I. Junctions between neurons.Journal of Neurocytology 9, 429–49.

    Google Scholar 

  • Chi, C. &Carlson, S. D. (1980b) Membrane specializations in the first optic neuropil of the housefly,Musca domestica L. II. Junctions between glial cells.Journal of Neurocytology 9, 451–69.

    Google Scholar 

  • Chi, C., Carlson, S. D. &Saint Marie, R. L. (1979) Membrane specializations in the peripheral retina of the houseflyMusca domestica L.Cell and Tissue Research 198, 501–20.

    Google Scholar 

  • Claude, P. (1978) Morphological factors influencing transepithelial permeability: a model for the resistance of theZonula occludens.Journal of Membrane Biology 39, 219–32.

    Google Scholar 

  • Claude, P. &Goodenough, D. A. (1973) Fracture faces ofZonulae occludentes from ‘tight’ and ‘leaky’ epithelia.Journal of Cell Biology 58, 390–400.

    Google Scholar 

  • Cosens, D. J. (1967) Extracellular potentials in the locust eye and optic lobe.Journal of Insect Physiology 13, 1373–86.

    Google Scholar 

  • Filshie, B. K. &Flower, N. E. (1977) Junctional structures in Hydra.Journal of Cell Science 23, 151–72.

    Google Scholar 

  • Gilula, N. B. (1974) Junctions between cells. InCell Communication (edited byCox, R. P.), pp. 1–29. New York: Wiley.

    Google Scholar 

  • Gilula, N. B. (1977) Gap junctions and cell communication. InInternational Cell Biology 1976–77 (edited byBrinkley, B. R. &Porter, K. R.), pp. 61–9. New York: Rockefeller University Press.

    Google Scholar 

  • Gilula, N. B. (1979) Electrotonic junctions. InThe Neurosciences: Fourth Study Program (edited bySchmitt, F. O. &Worden, F. G.), pp. 359–66. Cambridge, Mass: MIT Press.

    Google Scholar 

  • Hand, A. R. &Gobel, S. (1972) The structural organization of the septate and gap junctions ofHydra.Journal of Cell Biology 52, 397–408.

    Google Scholar 

  • Harris, W. A., Stark, W. S. &Walker, J. A. (1976) Genetic dissection of the photoreceptor system in the compound eye ofDrosophila melanogaster.Journal of Physiology 256, 415–39.

    Google Scholar 

  • Heisenberg, M. (1971) Separation of receptor and lamina potentials in the electroretinogram of normal and mutantDrosophila.Journal of Experimental Biology 55, 85–100.

    Google Scholar 

  • Ioannides, A. C. &Walcott, B. (1971) Graded illumination potentials from retinula cell axons in the bugLethocerus.Zeitschrift für vergleichende Physiologie 71, 315–25.

    Google Scholar 

  • Järvilheto, M. &Moring, J. (1976) Spectral and polarization sensitivity of identified retinal cells of the fly. InNeural Principles in Vision (edited byZettler, F. &Weiler, R.), pp. 214–26. Berlin: Springer-Verlag.

    Google Scholar 

  • Järvilheto, M. &Zettler, F. (1971) Localized intracellular potentials from pre- and postsynaptic components in the external plexiform layer of an insect retina.Zeitschrift für vergleichende Physiologie 75, 422–40.

    Google Scholar 

  • Järvilheto, M. &Zettler, M. (1973) Electrophysiological-histological studies on some functional properties of visual cells and second order neurons of an insect retina.Zeitschrift für Zellforschung und mikroskopische Anatomie 136, 291–306.

    Google Scholar 

  • Josephson, R. K. &Macklin, M. (1967) Transepithelial potentials inHydra.Science 156, 1629–31.

    Google Scholar 

  • Josephson, R. K. &Macklin, M. (1969) Electrical properties of body wall ofHydra.Journal of General Physiology 53, 638–65.

    Google Scholar 

  • Lane, N. J. (1972) Fine structure of a lepidopteran nervous system and its accessibility to peroxidase and lanthanum.Zeitschrift für Zellforschung und mikroskopische Anatomie 131, 205–22.

    Google Scholar 

  • Lane, N. J. (1978) Intercellular junctions and cell contacts in invertebrates. InProceedings of the Ninth International Congress on Electron Microscopy, Toronto Vol. 3 (edited bySturgess, J. M.), pp. 673–91. Toronto: Microscopical Society of Canada.

    Google Scholar 

  • Lane, N. J. (1979a) Tight junctions in a fluid-transporting epithelium of an insect.Science 204, 91–3.

    Google Scholar 

  • Lane, N. J. (1979b) Freeze-fracture and tracer studies on the intercellular junctions of insect rectal tissues.Tissue and Cell 11, 481–506.

    Google Scholar 

  • Lane, N. J. (1981) Vertebrate-like tight junctions in the insect eye.Experimental Cell Research 132, 482–8.

    Google Scholar 

  • Lane, N. J. &Skaer, H. Le B. (1980) Intercellular junctions in insect tissues. InAdvances in Insect Physiology Vol. 15 (edited byBerridge, M.),Treherne, J. E. &Wigglesworth, V. B.), pp. 35–213. London: Academic Press.

    Google Scholar 

  • Lane, N. J., Skaer, H. Le B. &Swales, L. S. (1975) Junctional complexes in insect nervous systems.Journal of Cell Biology 67, 233A.

    Google Scholar 

  • Lane, N. J., Skaer, H. Le B. &Swales, L. S. (1977) Intercellular junctions in the central nervous system.Journal of Cell Science 26, 175–99.

    Google Scholar 

  • Lane, N. J. &Swales, L. S. (1976) Dynamics of cell junctions in the differentiating insect nervous system.Journal of Cell Biology 70, 590A.

    Google Scholar 

  • Lane, N. J. &Swales, L. S. (1977) Differentiation of intercellular junctions in the CNS of developing insects.Journal of Cell Biology 75, 56A.

    Google Scholar 

  • Lane, N. J. &Swales, L. S. (1978a) Changes in the blood-brain barrier of the central nervous system in the blowfly during development, with special reference to the formation and disaggregation of gap and tight junctions. I. Larval development.Developmental Biology 62, 389–414.

    Google Scholar 

  • Lane, N. J. &Swales, L. S. (1978b) Changes in the blood-brain barrier of the central nervous system in the blowfly during development, with special reference to the formation and disaggregation of gap and tight junctions. II. Pupal development and adult flies.Developmental Biology 62, 415–31.

    Google Scholar 

  • Lane, N. J. &Swales, L. S. (1979) Intercellular junctions and the development of the blood-brain barrier inManduca sexta.Brain Research 168, 227–45.

    Google Scholar 

  • Lane, N. J. &Treherne, J. E. (1972) Studies on perineurial junctional complexes and the sites of uptake of microperoxidase and lanthanum in the cockroach central nervous system.Tissue and Cell 4, 427–36.

    Google Scholar 

  • Langer, H. &Thorell, B. (1966a) Microspectrophotometry of single rhabdomeres in the insect eye.Experimental Cell Research 41, 673–7.

    Google Scholar 

  • Langer, H. &Thorell, B. (1966b) Microspectrophotometric assay of visual pigments in single rhabdomeres of the insect eye. InThe functional Organization of the Compound Eye (edited byBernhard, C. G.), pp. 145–9. London: Pergamon.

    Google Scholar 

  • Laughlin, S. B. (1974) Neural integration in the first optic neuropile of dragonflies. II. Receptor signal interactions in the lamina.Journal of Comparative Physiology 92, 357–75.

    Google Scholar 

  • Laughlin, S. B. (1975) The function of the lamina ganglionaris. InThe Compound Eye and Vision in Insects (edited byHorridge, G. A.), pp. 341–58. London: Oxford University Press.

    Google Scholar 

  • Laughlin, S. B. (1976) Adaptations of the dragonfly retina for contrast detection and the elucidation of neural principles in the peripheral visual system. InNeural Principles in Vision (edited byZettler, F. &Weiler, R.), pp. 175–93. Berlin: Springer-Verlag.

    Google Scholar 

  • Laughlin, S. (1981) Neural principles in the peripheral visual systems of invertebrates. InHandbook of Sensory Physiology Vol. VII/6B (edited byAutrum, H.), pp. 133–280. Berlin: Springer-Verlag.

    Google Scholar 

  • Leutscher-Hazelhoff, J. T. &Kuiper, J. W. (1964) Responses of the blowflyCalliphora erythrocephala to light flashes and to sinusoidally modulated light.Documenta Ophthalmologica 18, 275–83.

    Google Scholar 

  • Loewenstein, W. R. &Kanno, Y. (1964) Studies on epithelial gland cell junction. I. Modifications of surface membrane permeability.Journal of Cell Biology 22, 565–86.

    Google Scholar 

  • Lord, B. A. P. &Dibona, D. R. (1976) Role of the septate junction in the regulation of paracellular transepithelial flow.Journal of Cell Biology 71, 967–72.

    Google Scholar 

  • McCann, G. D. &Arnett, D. W. (1972) Spectral and polarization sensitivity of the dipteran visual system.Journal of General Physiology 59, 534–58.

    Google Scholar 

  • McNutt, N. S. &Weinstein, R. S. (1973) Membrane ultrastructure at mammalian intercellular junctions.Progress in Biophysics and Molecular Biology 26, 47–101.

    Google Scholar 

  • Mote, M. I. (1970) Focal recordings of response evoked by light in the lamina ganglionaris of the flySarcophaga bullata.Journal of Experimental Zoology 175, 149–57.

    Google Scholar 

  • Newell, P. F. &Skelding, J. M. (1973) Structure and permeability of the septate junction in the kidney sac ofHelix pomatia L.Zeitschrift für Zellforschung und mikroskopische Anatomie 147, 31–9.

    Google Scholar 

  • Noirot-Timothée, C., Smith, D. S., Cayer, M. L. &Noirot, C. (1978) Septate junctions in insects: comparison between intercellular and intramembranous structures.Tissue and Cell 10, 125–36.

    Google Scholar 

  • Revel, J. P. &Karnovsky, M. J. (1967) Hexagonal array of subunits in intercellular junctions of the mouse heart and liver.Journal of Cell Biology 33, C7.

    Google Scholar 

  • Saint Marie, R. L. &Carlson, S. D. (1980) Glia-glial and glia-axonal tight junctions: possible substrate for lateral electrical inhibition at the fly photoreceptor synapse.Investigative Ophthalmology and Visual Science 11, Suppl. 246.

  • Saint Marie, R. L. &Carlson, S. D. (1982) Synaptic vesicle activity in stimulated and unstimulated photoreceptor axons in the housefly. A freeze-fracture study.Journal of Neurocytology 11, 747–61.

    Google Scholar 

  • Saint Marie, R. L. &Carlson, S. D. (1983) The fine structure of neuroglia in the lamina ganglionaris of the housefly,Musca domestica L.Journal of Neurocytology 12, 213–41.

    Google Scholar 

  • Scholes, J. (1969) The electrical responses of the retinal receptors and the lamina in the visual system of the flyMusca.Kybernetik 6, 149–62.

    Google Scholar 

  • Shaklai, M. &Tavassoli, M. (1977) A modified technique to obtain uniform precipitation of lanthanum tracer in the extracellular space.Journal of Histochemistry and Cytochemistry 25, 1013–15.

    Google Scholar 

  • Shaw, S. R. (1968) Organization of the locust retina.Symposium of the Zoological Society of London 23, 135–63.

    Google Scholar 

  • Shaw, S. R. (1975) Retinal resistance barriers and electrical lateral inhibition.Nature 255, 480–3.

    Google Scholar 

  • Shaw, S. R. (1977) Restricted diffusion and extracellular space in the insect retina.Journal of Comparative Physiology 113, 257–82.

    Google Scholar 

  • Shaw, S. R. (1978) The extracellular space and blood-eye barrier in an insect retina: an ultrastructural study.Cell and Tissue Research 188, 35–61.

    Google Scholar 

  • Shaw, S. R. (1979) Signal transmission by graded slow potentials in the arthropod peripheral visual system. InThe Neurosciences: Fourth Study Program (edited bySchmitt, F. O. &Worden, F. G.), pp. 275–95. Cambridge, Mass: MIT Press.

    Google Scholar 

  • Shaw, S. R. &Stowe, S. (1982) Freeze-fracture evidence for gap junctions connecting the axon terminals of Dipteran photoreceptors.Journal of Cell Science 53, 115–41.

    Google Scholar 

  • Snyder, A. W. (1973) Polarization sensitivity of individual retinular cells.Journal of Comparative Physiology 83, 331–60.

    Google Scholar 

  • Snyder, A. W. &Pask, C. (1973) Spectral sensitivity of dipteran retinular cells.Journal of Comparative Physiology 84, 59–76.

    Google Scholar 

  • Staehelin, L. A. (1974) Structure and function of intercellular junctions. InInternational Review of Cytology Vol. 39 (edited byBourne, G. H. &Danielli, J. F.), pp. 191–283. New York: Academic Press.

    Google Scholar 

  • Strausfeld, N. J. (1971) The organization of the insect visual system (light microscopy). I. Projections and arrangements of neurons in the lamina ganglionaris of Diptera.Zeitschrift für Zellforschung und mikroskopische Anatomie 121, 377–441.

    Google Scholar 

  • Strausfeld, N. J. (1976a) Mosaic organizations, layers, and visual pathways in the insect brain. InNeural Principles in Vision (edited byZettler, J. &Weiler, R.), pp. 245–79. Berlin: Springer-Verlag.

    Google Scholar 

  • Strausfeld, N. J. (1976b)Atlas of an Insect Brain Berlin: Springer-Verlag.

    Google Scholar 

  • Strausfeld, N. J. &Campos-Ortega, J. A. (1977) Vision in insects: pathways possibly underlying neural adaptation and lateral inhibition.Science 195, 894–7.

    Google Scholar 

  • Strausfeld, N. J. &Nässel, D. R. (1981) Neuroarchitecture of brain regions that subserve the compound eye of crustacea and insects. InHandbook of Sensory Physiology Vol. VII/6B (edited byAutrum, H.), pp. 1–132. Berlin: Springer-Verlag.

    Google Scholar 

  • Szöllösi, A. &Marcaillou, C. (1977) Electron microscope study of the blood-testis barrier in an insect:Locuste migratoria.Journal of Ultrastructure Research 59, 158–72.

    Google Scholar 

  • Trujillo-Cenóz, O. (1965) Some aspects of the structural organization of the intermediate retina of dipterans.Journal of Ultrastructure Research 13, 1–33.

    Google Scholar 

  • Wood, R. L. (1959) Intercellular attachment in the epithelium ofHydra as revealed by electron microscopy.Journal of Biophysical and Biochemical Cytology 6, 343–52.

    Google Scholar 

  • Zettler, F. &Järvilheto, M. (1971) Decrement-free conduction of graded potentials along the axon of a monopolar neuron.Zeitschrift für vergleichende Physiologie 75, 402–21.

    Google Scholar 

  • Zettler, F. &Järvilheto, M. (1972) Lateral inhibition in an insect eye.Zeitschrift für vergleichende Physiologie 76, 233–44.

    Google Scholar 

  • Zettler, F. &Järvilheto, M. (1973) Active and passive axonal propagation of non-spike signals in the retina ofCalliphora.Journal of Comparative Physiology 85, 89–104.

    Google Scholar 

  • Zimmerman, R. P. (1978) Field potential analysis and the physiology of second-order neurons in the visual system of the fly.Journal of Comparative Physiology 126, 297–316.

    Google Scholar 

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  1. Richard L. Saint Marie

    Present address: Department of Anatomy, Boston University, School of Medicine, 80E. Concord St., 02118, Boston, MA, USA

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  1. Neurosciences Training Program and Department of Entomology, University of Wisconsin, 53706, Madison, Wisconsin, USA

    Richard L. Saint Marie & Stanley D. Carlson

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Submitted by R. L. Saint Marie in partial fulfilment of the requirements for the degree of PhD, University of Wisconsin, Madison.

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Saint Marie, R.L., Carlson, S.D. Glial membrane specializations and the compartmentalization of the lamina ganglionaris of the housefly compound eye. J Neurocytol 12, 243–275 (1983). https://doi.org/10.1007/BF01148464

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