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The ultrastructure of retinula cell endings in the compound eye of the crayfish

  • Published:
Journal of Neurocytology

Summary

The retinula cell axons entering the synaptic region of the optic lamina in the crayfish form large expanded bag-like terminals which are organized with other neural elements into structural units called ‘cartridges’. The cytoplasm of the terminals contains synaptic and coated vesicles, ER cisternae, clusters of tubular elements, and mitochondria. Several mitochondria are often found associated with a single large rod-shaped inclusion present within each terminal. The rod-like formation could be demonstrated in both light and EM material, it is composed of 85–95 Å filaments and averages I μm in width and 6.5 μm in length.

The terminal synaptic contacts are characterized by a bar-shaped presynaptic density and three postsynaptic elements. Some synaptic vesicles appear aligned along the bar density which measures approximately 800 Å in width and 0.75 μm in length. Each terminal synapse has three postsynaptic elements which have an electron-dense fringe along their membrane bordering the synaptic cleft. From the planes of section through this contact a composite reconstruction is presented.

Also present along the central border of the terminals are numerous small invaginated processes, some of which extend almost to the middle of the terminal. No membrane specializations were found along these processes and they have been tentatively identified as neuronal.

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References

  • Bernhard, H. (1916) Der Bau des Komplexauges von Astacus fiuviatilis (Potamobius astacus L.). Ein Beitrag zur Morphologie der Decapoden.Zeitschrift fuer Wissenschaftliche Zoologie 114, 650–707.

    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 

  • Boycott, B. B. andDowling, J. E. (1969) Organization of the primate retina: light microscopy.Philosophical Transactions of the Royal Society of London Series B 255, 109–84.

    Google Scholar 

  • Boycott, B. B., Gray, E. G. andGuillery, R. W. (1961) Synaptic structure and its alterations with environmental temperature: a study by light and electron microscopy of the central nervous system in lizards.Proceedings of the Royal Society of London Series B 154, 151–72.

    Google Scholar 

  • Braitenberg, V. (1967) Patterns of projection in the visual system of the fly. I. Retina-lamina projections.Brain Research 3, 271–98.

    Google Scholar 

  • Bunt, A. H. (1973) Paracrystalline inclusions in optic nerve terminals following intraocular injection of vinblastine.Brain Research 53, 29–39.

    PubMed  Google Scholar 

  • Coggeshall, R. E. andFawcett, D. W. (1964) The fine structure of the central nervous system of the leechHirudo medicinalis.Journal of Neurophysiology 27, 229–89.

    PubMed  Google Scholar 

  • Cuénod, M., Sandri, C. andAkert, K. (1972) Enlarged synaptic vesicles in optic nerve terminals induced by intraocular injection of colchicine.Brain Research 39, 285–96.

    PubMed  Google Scholar 

  • Dowling, J. E. andBoycott, B. B. (1965) Neural connections of the retina: fine structure of the inner plexiform layer.Cold Spring Harbor Symposium 30, 393–402.

    Google Scholar 

  • Dowling, J. E. andBoycott, B. B. (1966) Organization of the primate retina: electron microscopy.Proceedings of the Royal Society of London Series B 166, 80–111.

    Google Scholar 

  • Eakin, R. andBrandenburger, J. L. (1970) Osmic staining of amphibian and gastropod photoreceptors.Journal of Ultrastructure Research 30, 619–41.

    PubMed  Google Scholar 

  • Ebbesson, S. O. E. (1970) The selective silver-impregnation of degenerating axons and their synaptic endings in nonmammalian species. InContemporary Research Methods in Neuroanatomy (edited byNauta, W. J. H. andEbbesson, S. O. E.) pp. 132–61. New York: Springer-Verlag.

    Google Scholar 

  • Eccles, J. C., Ito, M., andSzentágothai, J. (1967)The Cerebellum as a Neuronal Machine, Chapter VII, pp. 116–55. New York: Springer-Verlag.

    Google Scholar 

  • Gray, E. G. andGuillery, R. W. (1963a) An electron microscopical study of the ventral nerve cord of the leech.Zeitschrift für Zellforschung and Mikroskopische Anatomie 60, 826–49.

    Google Scholar 

  • Gray, E. G. andGuillery, R. W. (1963b) On nuclear structure in the ventral nerve cord of the leech (Hirudo medicinalis).Zeitschrift für Zellforschung und Mikroskopische Anatomie 59, 738–45.

    Google Scholar 

  • Gray, E. G. andPease, H. L. (1971) On understanding the organization of the retinal receptor synapses.Brain Research 35, 1–15.

    PubMed  Google Scholar 

  • Gray, E. G. andWillis, R. A. (1970) On synaptic vesicles, complex vesicles and dense projections.Brain Research 24, 149–68.

    PubMed  Google Scholar 

  • Hafner, G. S. (1974) The neural organization of the lamina ganglionaris in the crayfish: A Golgi and EM study.Journal of Comparative Neurology 152, 255–80.

    Google Scholar 

  • Hamóri, J. andHorridge, G. A. (1966a) The lobster optic lamina. I. General organization.Journal of Cell Science 1, 249–56.

    Google Scholar 

  • Hamóri, J. andHorridge, G. A. (1966b) The lobster optic lamina. II. Types of synapse.Journal of Cell Science 1, 257–70.

    Google Scholar 

  • Hamóri, J. andHorridge, G. A. (1966c) The lobster optic lamina. III. Degeneration of retinula cell endings.Journal of Cell Science 1, 271–4.

    PubMed  Google Scholar 

  • Hamóri, J. andHorridge, G. A. (1966d) The lobster optic lamina. IV. Glial cells.Journal of Cell Science 1, 275–80.

    PubMed  Google Scholar 

  • Heimer, L. (1969) Silver impregnation of degenerating axons and their terminals on Epon-Araldite sections.Brain Research 12, 246–9.

    PubMed  Google Scholar 

  • Heimer, L. (1970) Selective silver impregnation of degenerating axoplasm. In:Contemporary Research Methods in Neuroanatomy (edited byNauta, W. J. H. andEbbesson, S. O. E.) pp. 106–31. New York: Springer-Verlag.

    Google Scholar 

  • Heuser, J. E. andReese, T. S. (1973) Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction.Journal of Cell Biology 57, 315–444.

    PubMed  Google Scholar 

  • Iraldi, A. P. de andSuburo, A. M. (1971) Osmium tetroxide-zinc iodide reactive rites in the photoreceptor cells.Vision Research Supplement No. 3, 27–31.

    Google Scholar 

  • Kanaseki, T. andKadota, K. (1969) The ‘vesicle in a basket’. A morphological study of the coated vesicle isolated from the nerve endings of the guinea pig brain with special reference to the mechanism of membrane movements.Journal of Cell Biology 42, 202–20.

    PubMed  Google Scholar 

  • Lovas, B. (1971) Tubular networks in the terminal endings of the visual receptor cells in the human, the monkey, the cat and the dog.Zeitschrift für Zellforschung und Mikroskopische Anatomie 121, 341–57.

    Google Scholar 

  • Parker, G. H. (1897) The retina and optic ganglia in decapods, especially in Astacus.Mitteilungen aus der Zoologischen Station zu Neapel 12, 1–73.

    Google Scholar 

  • Potter, H. D. (1973) Alterations in neurofibrillar rings in the lizard brain during cold acclimation.Journal of Neurocytology 2, 29–45.

    PubMed  Google Scholar 

  • Potter, H. D. andHafner, G. S. (1974) Sequence of changes in neurofibrils (neurofilaments) induced in synaptic regions of bullfrogs by environmental temperature changes. In preparation.

  • Reynolds, E. S. (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy.Journal of Cell Biology 17, 208–12.

    PubMed  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 ofDiptera.Zeitschrift für Zellforschung und Mikroskopische Anatomie 121, 377–441.

    Google Scholar 

  • Strausfeld, N. J. andBlest, A. D. (1970) Golgi studies on insects. Part I. The optic lobes of Lepidoptera.Philosophical Transactions of the Royal Society of London Series B 258, 81–134.

    Google Scholar 

  • Szentägothai, J. (1970) The morphological identification of active synaptic regions: Aspects of general arrangement, of geometry and topology. In:Excitatory Synaptic Mechanisms (edited byAndersen, P. andJansen, J. K. S.) pp. 9–26. Oslo, Norway: Universitetsforlaget.

    Google Scholar 

  • Trujillo-Cenóz, O. (1962) Some aspects of the structural organization of the arthropod ganglia.Zeitschrift für Zellforschung und Mikroskopische Anatomie 56, 649–82.

    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.

    PubMed  Google Scholar 

  • Trujillo-Cenóz, O. (1972) The structural organization of the compound eye in insects. In:Physiology of Photoreceptor Organs. Handbook of Sensory Physiology, Vol. VII (edited byFuortes, M. G. F.) pp. 5–63. New York: Springer-Verlag.

    Google Scholar 

  • Trujillo-Cenóz, O. andMelamed, J. (1973) The development of the retina-lamina complex in muscoid flies.Journal of Ultrastructure Research 42, 554–81.

    PubMed  Google Scholar 

  • Trujillo-Cenöz, O. andMelamed, J. (1963) On the fine structure of the photoreceptor-second order neuron synapse in the insect retina.Zeitschrift für Zellforschung und Mikroskopische Anatomie 59, 71–7.

    Google Scholar 

  • Trujillo-Cenöz, O. andMelamed, J. (1967) The fine structure of the visual system ofLycosa (Araneae: Lycosidae). Part II. Primary visual centers.Zeitschrift für Zellforschung und Mikroskopische Anatomie 76, 377–88.

    Google Scholar 

  • Van Harreveld, A. (1936) A physiological solution for fresh-water crustaceans.Proceedings of the Society for Experimental Biology 34, 428–32.

    Google Scholar 

  • Viallanes, H. (1892) Contribution á l'histologie du systéme nerveux des invertébrés, La lame ganglionaire de la langouste.Annales des Sciences Naturelles Séries 7, Zoologie 13-14, 385–98.

    Google Scholar 

  • Wolff, J. R. andGüldner, F. H. (1970) Über die Ultrastruktur des ‘Nervus opticus’ und des Ganglion opticum I vonDaphnia pulex.Zeitschrift für Zellforschung und Mikroskopische Anatomie 103, 526–43.

    Google Scholar 

  • Yamada, E. (1965) Some observations on the membrane-limited structure within the retinal element. In:Intracellular Membranous Structure (edited bySeng, S. andCowdry, E. V.) pp. 49–63. Okayama Japan: Japanese Society of Cell Biology.

    Google Scholar 

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Author notes

  1. Gary S. Hafner

    Present address: Department of Anatomy, University of California Medical Centre, School of Medicine, 90024, Los Angeles, California

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  1. Department of Anatomy and Physiology, Indiana University, Bloomington, Indiana

    Gary S. Hafner

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Hafner, G.S. The ultrastructure of retinula cell endings in the compound eye of the crayfish. J Neurocytol 3, 295–311 (1974). https://doi.org/10.1007/BF01097915

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  • DOI: https://doi.org/10.1007/BF01097915

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