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The Visual System of Flies: Analysis of the Number, Specificity, Plasticity, and Phylogeny of Identified Synapses

  • René Marois
  • I. A. Meinertzhagen
Part of the NATO ASI Series book series (NSSA, volume 192)

Abstract

The functional interactions of a neural circuit are established primarily by its pattern of synaptic connections. Understanding the process of synapse formation and its regulation is therefore paramount to an analysis of circuit organization. To formulate the rules for the assembly of synaptic microcircuits requires as a minimum a simple system that nonetheless possesses the major architectural principles of all nervous systems, and that is easily amenable to precise, detailed analysis. The first neuropil of the fly’s optic lobe, the lamina, meets many of these requirements. As background, the structural organization and ontogeny of the defined circuits of this highly stereotyped neuropil have already been thoroughly investigated. This chapter presents recent studies that have exploited these advantages to decipher the operational steps in the formation of synaptic microcircuits and their regulation, plasticity, and evolution.

Keywords

Amacrine Cell Synapse Formation Optic Lobe Pupal Development Synaptic Site 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Bennett, M. R., and Pettigrew, A. G., 1975, The formation of neuromuscular synapses, Cold Spring Harb. Symp. Quant. Biol., 40:409.CrossRefGoogle Scholar
  2. Brandstätter, J. H., Shaw, S. R., and Meinertzhagen, I. A., 1989, Synaptic disassembly after photo-degeneration of receptor terminals in the lamina of the fly’s optic lobe, Soc. Neurosci. Abstr., 15:1388.Google Scholar
  3. Bullock, T. H., 1978, Identifiable and addressed neurons in the vertebrates, in: “Neurobiology of the Mauthner Cell,” D. Faber and H. Korn, eds., Raven Press, New York, p. 1.Google Scholar
  4. Burry, R. W., Kniss, D. A., and Scribner, L. R., 1984, Mechanisms of synapse formation and maturation, Curr. Topics Neurosci. Res. Synapses, 1:1.Google Scholar
  5. Campbell, G., and Frost, D. O., 1987, Target-controlled differentiation of axon terminals and synaptic organization, Proc. Natl. Acad. Sci. USA, 84:6929.PubMedCrossRefGoogle Scholar
  6. Constantine-Paton, M., and Norden, J. J., 1986, Synapse regulation in the developing visual system, in: “Development of Order in the Visual System,” S. R. Hilfer, and J. B. Sheffield, eds., Springer-Verlag, New York, p. 1.CrossRefGoogle Scholar
  7. Cotman, C. W., and Nieto-Sampedro, M., 1984, CeU biology of synaptic plasticity, Science, 225:1287.PubMedCrossRefGoogle Scholar
  8. Dowling, J. E., and Boycott, B. B., 1966, Organization of the primate retina: Electron microscopy, Proc. R. Soc. Lond. [Biol.], 166:80.CrossRefGoogle Scholar
  9. Easter, S. S., Purves, D., Rakic, P., and Spitzer, N. C., 1985, The changing view of neural specificity, Science, 230:507.PubMedCrossRefGoogle Scholar
  10. Ferrus, A., and Garcia-Bellido, A., 1976, Morphogenetic mutants detected in mitotic recombination clones, Nature, 260:425.PubMedCrossRefGoogle Scholar
  11. Fröhlich, A., and Meinertzhagen, I. A., 1983, Quantitative features of synapse formation in the fly’s visual system. I. The presynaptic photoreceptor terminal, J. Neurosci., 3:2336.PubMedGoogle Scholar
  12. Fröhlich, A., and Meinertzhagen, I. A., 1987, Regulation of synaptic frequency: Comparison of the effects of hypoinnervation with those of hyperinnervation in the fly’s compound eye, J. Neurobiol., 18:343.PubMedCrossRefGoogle Scholar
  13. Hertel, H., 1982, The effect of spectral light deprivation on the spectral sensitivity of the honeybee, J. Comp. Physiol. (A), 147:365.CrossRefGoogle Scholar
  14. Hertel, H., 1983, Change of synapse frequency in certain photoreceptors of the honey bee after chromatic deprivation, J. Comp. Physiol. (A), 151:477.CrossRefGoogle Scholar
  15. John, B., and Miklos, G., 1988, “The Eukaryote Genome in Development and Evolution,” Allen and Unwin, London.Google Scholar
  16. Kral, K., and Meinertzhagen, I. A., 1989, Anatomical plasticity of synapses in the lamina of the optic lobe of the fly, Phil. Trans. R. Soc. Lond. [Biol.], 323:155.CrossRefGoogle Scholar
  17. Laughlin, S., 1981, Neural principles in the peripheral visual systems of invertebrates, in: “Handbook of Sensory Physiology,” Vol. VII/6B, Comparative Physiology and Evolution of Vision in Invertebrates, H. Autrum, ed., Springer-Verlag, New York.Google Scholar
  18. Macagno, E. R., 1984, Formation of ordered connections in the visual system of Daphnia magna, Bioscience, 34:308.CrossRefGoogle Scholar
  19. Masland, R. H., 1988, Amacrine cells, Trends Neurosci., 11:405.PubMedCrossRefGoogle Scholar
  20. Meinertzhagen, I. A., 1973, Development of the compound eye and optic lobe of insects, in: “Developmental Neurobiology of Arthropods,” D. Young, ed., Cambridge University Press, Cambridge, p. 51.Google Scholar
  21. Meinertzhagen, I. A., 1984, The rules of synaptic assembly in the developing insect lamina, in: “Photoreception and Vision in Invertebrates,” M. A. Ali, ed., NATO ASI Series A, Vol. 74, Plenum Press, New York, p. 635.Google Scholar
  22. Meinertzhagen, I. A., 1989, Fly photoreceptor synapses: Their development, evolution, and plasticity, J. Neurobiol, 20:276.PubMedCrossRefGoogle Scholar
  23. Meinertzhagen, I. A., and Fröhlich, A., 1983, The regulation of synapse formation in the fly’s visual system, Trends Neurosci., 6:223.CrossRefGoogle Scholar
  24. Meyerowitz, E. M., and Kankel, D.R., 1978, A genetic analysis of visual system development in Drosophila melanogaster, Dev. Biol., 62:112.PubMedCrossRefGoogle Scholar
  25. Mimura, K., 1986, Development of visual pattern discrimination in the fly depends on light experience, Science, 232: 83.PubMedCrossRefGoogle Scholar
  26. Mimura, K., 1987, Persistence and extinction of the effect of visual pattern deprivation in the fly, Exp. Biol., 46:155.PubMedGoogle Scholar
  27. Murphey, R. K., 1986, The myth of the inflexible invertebrate: Competition and synaptic remodelling in the development of invertebrate nervous systems, J. Neurobiol, 17:585.PubMedCrossRefGoogle Scholar
  28. Nicol, D., and Meinertzhagen, I. A., 1982a, An analysis of the number and composition of the synaptic populations formed by photoreceptors of the fly, J. Comp. Neurol., 207:29.PubMedCrossRefGoogle Scholar
  29. Nicol, D., and Meinertzhagen, I. A., 1982b, Regulation in the number of fly photoreceptor synapses: The effects of alterations in the number of presynaptic cells, J. Comp. Neurol., 207:45.PubMedCrossRefGoogle Scholar
  30. Rauschecker, J. P., and Marier, P., 1987, “Imprinting and Cortical Plasticity: Comparative Aspects of Sensitive Periods,” Wiley, New York.Google Scholar
  31. Shaw, S. R., 1981, Anatomy and physiology of identified non-spiking cells in the photoreceptor-lamina complex of the compound eye of insects, especially Diptera, in: “Neurones without Impulses,” A. Roberts, and B. M. H. Bush, eds., Society Exptl. Biol. Seminar Series, Vol. 6, Cambridge University Press, Cambridge, UK, p. 61.Google Scholar
  32. Shaw, S. R., 1984, Early visual processing in insects, J. Exp. Biol., 112:225.PubMedGoogle Scholar
  33. Shaw, S. R., and Meinertzhagen, I. A., 1986, Evolutionary progression at synaptic connections made by identified homologous neurones, Proc. Natl. Acad. Sci. USA, 83:7961.PubMedCrossRefGoogle Scholar
  34. Stent, G. S., and Weisblat, D. A., 1985, Cell lineage in the development of invertebrate nervous systems, Anna. Rev. Neurosci., 8:45.CrossRefGoogle Scholar
  35. Stevens, C. F., 1989, Strengthening the synapses, Nature, 338:460.PubMedCrossRefGoogle Scholar
  36. Strausfeld, N. J., and Campos-Ortega, J. A., 1977, Vision in insects: Pathways possibly underlying neural adaptation and lateral inhibition, Science, 195:894.PubMedCrossRefGoogle Scholar
  37. Strausfeld, N. J., and Nässei, D. R., 1981, Neuroarchitectures serving compound eyes of Crustacea and insects, in: “Handbook of Sensory Physiology,” Vol. VII/6B, “Comparative Physiology and Evolution of Vision in Invertebrates,” H. Autrum, ed., Springer-Verlag, New York, p. 1.CrossRefGoogle Scholar
  38. Trujillo-Cenóz, O., 1965, Some aspects of the structural organization of the intermediate etina of dipterans, J. Ultrastruct. Res., 13:1.PubMedCrossRefGoogle Scholar
  39. Trujillo-Cenóz, O., and Melamed, J., 1973, The development of the retina-lamina complex in muscoid flies, J. Ultrastruct. Res., 42:554.PubMedCrossRefGoogle Scholar
  40. Watson, A. H. D., and Burrows, M., 1982, The ultrastructure of identified locust motor neurone and their synaptic relationships, J. Comp. Neurol., 205:383.PubMedCrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1990

Authors and Affiliations

  • René Marois
    • 1
  • I. A. Meinertzhagen
    • 2
  1. 1.Department of PsychologyYale UniversityNew HavenUSA
  2. 2.Life Sciences CentreDalhousie UniversityHalifaxCanada

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