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The synaptic organization of visual interneurons in the lobula complex of flies

A light and electron microscopical study using silver-intensified cobalt-impregnations

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Summary

The synaptic organization of three classes of cobalt-filled and silver-intensified visual interneurons in the lobula complex of the blowfly Calliphora (Col A cells, horizontal cells and vertical cells) was studied electron microscopically. The Col A cells are regularly spaced, columnar, small field neurons of the lobula, which constitute a plexus of arborizations at the posterior surface of the neuropil and the axons of which terminate in the ventrolateral protocerebrum. They show postsynaptic specializations in the distal layer of their lobula-arborizations and additional presynaptic sites in a more proximal layer; their axon terminals are presynaptic to large descending neurons projecting into the thoracic ganglion. The horizontal and vertical cells are giant tangential neurons, the arborizations of which cover the anterior and posterior surface of the lobula plate, respectively, and which terminate in the perioesophageal region of the protocerebrum. Both classes of these giant neurons were found to be postsynaptic in the lobula plate and pre- and postsynaptic at their axon terminals and axon collaterals. The significance of these findings with respect to the functional properties of the neurons investigated is discussed.

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References

  • Altman JS, Shaw MK, Tyrer NM (1979) Visualization of synapses of physiologically identified cobalt-filled neurones in the locust. J Physiol 296:2P

    Google Scholar 

  • Barlow HB, Levick WR (1965) The mechanism of directionally sensitive units in the rabbit's retina. J Physiol 178:477–504

    Google Scholar 

  • Boschek CB (1971) On the fine structure of the peripheral retina and lamina ganglionaris of the fly, Musca domestica. Z Zellforsch 118:369–409

    Google Scholar 

  • Braitenberg V (1970) Ordnung und Orientierung der Elemente im Sehsystem der Fliege. Kybernetik 7:235–242

    Google Scholar 

  • Buchner E, Buchner S, Hengstenberg R (1979) 2-deoxy-D-glucose maps movement — specific nervous activity in the second visual ganglion of Drosophila. Science 205:687–688

    Google Scholar 

  • Bullock TH, Horridge GA (1965) Structure and function in the nervous systems of invertebrates. WH Freeman and Company, San Francisco and London

    Google Scholar 

  • Case R (1957) Differentiation of the effects of pH and CO2 on the spiracular function of insects. J Cell Comp Physiol 49:103–113

    Google Scholar 

  • Dvorak DR, Bishop LG, Eckert HE (1975) On the identification of movement detectors in the fly optic lobe. J Comp Physiol 100:5–23

    Google Scholar 

  • Eckert H, Bishop LG (1978) Anatomical and physiological properties of the vertical cells in the third optic ganglion of Phaenicia sericata (Diptera, Calliphoridae). J Comp Physiol 126:57–86

    Google Scholar 

  • Hassenstein B, Reichardt W (1956) Systemtheoretische Analyse der Zeit-, Reihenfolgen- und Vorzeichenauswertung bei der Bewegungsperzeption des Rüsselkäfers Chlorophanus. Z Naturforsch 116:513–524

    Google Scholar 

  • Hausen K (1976a) Struktur, Funktion und Konnektivität bewegungsempfindlicher Interneuronen im dritten optischen Neuropil der Schmeißfliege Calliphora erytrocephala. Doctoral Dissertation. University of Tübingen

  • Hausen K (1976b) Functional characterization and anatomical identification of motion sensitive neurons in the lobula plate of the blowfly Calliphora erythrocephala. Z Naturforsch 31c:629–633

    Google Scholar 

  • Hausen K (1976c) Funktion, Struktur und Konnektivität bewegungsempfindlicher Interneurone in der Lobula plate von Dipteren. Verh Dtsch Zool Ges 69:254

    Google Scholar 

  • Hausen K (1977) Signal processing in the insect eye. In: GS Stent (ed) Function and Formation of Neural Systems. Abakon Verlagsgesellschaft, Berlin

    Google Scholar 

  • Hausen K (1979) Neural circuitry of visual orientation behavior in flies: Structure and function of the lobula-complex. Invest Ophthalmol Visual Sci 18:(Suppl) 109

    Google Scholar 

  • Hausen K, Strausfeld NJ (in press, 1980) Sexually dimorphic interneuron arrangements in the fly visual system. Proc R Soc Lond B

  • Hausen K, Wolburg-Buchholz K (1980) An improved cobalt-sulphide silver-intensification method for electron microscopy. Brain Res 187:462–466

    Google Scholar 

  • Heisenberg M, Wonneberger R, Wolf R (1978) Optomotor-blind H31 — a Drosophila mutant of the lobula plate giant neurons. J Comp Physiol 124:287–296

    Google Scholar 

  • Hengstenberg R (1977) Spike responses of “non-spiking” visual interneurones. Nature 270:338–340

    Google Scholar 

  • Hengstenberg R (in press, 1980) Drehspezifität von Vertikalzellen in der Lobula plate. Verh Dtsch Zool Ges

  • Kirschfeld K (1972) The visual system of Musca: Studies on optics, structure and function. In: R Wehner (ed) Information Processing in the Visual Systems of Arthropods. Springer-Verlag, Berlin Heidelberg New York

    Google Scholar 

  • Kirschfeld K (1979) The visual system of the fly: Physiological optics and functional anatomy as related to behavior. In: FO Schmitt, FG Worden (eds) The Neurosciences, Fourth Study Program. The MIT Press, Cambridge, Mass. London, England, pp 297–310

    Google Scholar 

  • La Vail JH, La Vail MM (1972) Retrograde axonal transport in the central nervous system. Science 176:1416–1417

    Google Scholar 

  • Lillie RD (1965) Histopathologic technique and practical histochemistry. McGraw Hill, New York Toronto Sydney London

    Google Scholar 

  • Pierantoni R (1976) A look into the cockpit of the fly. The architecture of the lobular plate. Cell Tissue Res 171:101–122

    Google Scholar 

  • Pitman RM, Tweedle CD, Cohen MJ (1972) Branching of central neurons: Intracellular cobalt injection for light and electron microscopy. Science 176:412–414

    Google Scholar 

  • Poggio T, Reichardt W (1976) Visual control of orientation behaviour in the fly. Toward the underlying neural interactions. Quart Rev Biophys 9:377–438

    Google Scholar 

  • Reichardt W (1957) Autokorrelationsauswertung als Funktionsprinzip des Zentralnervensystems. Z Naturforsch 12b:448–457

    Google Scholar 

  • Reichardt W, Poggio T (1976) Visual control of orientation behaviour in the fly. Part I: A quantitative analysis. Quart Rev Biophys 9:311–375

    Google Scholar 

  • Ribi WA (1976) The first optic ganglion of the bee. II. Topographical relationships of the monopolar cells within and between cartridges. Cell Tissue Res 171:359–373

    CAS  PubMed  Google Scholar 

  • Ribi WA, Berg GJ (1980) Light and electron microscopic structure of Golgi-stained neurons in the vertebrate brain (New rapid Golgi procedure). Cell Tissue Res 205:1–10

    Google Scholar 

  • Stewart WW (1978) Functional connections between cells as revealed by dye-coupling with a highly fluorescent naphtalimide tracer. Cell 14:741–759

    Google Scholar 

  • Strausfeld NJ (1980) Male and female neurons in dipterous insects. Nature 283:381–383

    Google Scholar 

  • Strausfeld NJ (1976) Atlas of an Insect Brain. Springer-Verlag, Berlin Heidelberg New York

    Google Scholar 

  • Strausfeld NJ, Obermayer M (1976) Resolution of intraneuronal and transsynaptic migration of cobalt in the insect visual and nervous systems. J Comp Physiol 110:1–12

    Google Scholar 

  • Strausfeld NJ, Hausen K (1977) The resolution of neuronal assemblies after cobalt injection into neuropil. Proc R Soc Lond B 199:463–476

    Google Scholar 

  • Stretton AOW, Kravitz EA (1968) Neuronal geometry. Determination with a technique of intracellular dye injection. Science 162:132–134

    Google Scholar 

  • Torre V, Poggio T (1978) A synaptic mechanism possibly underlying directional selectivity to motion. Proc R Soc London B 202:409–416

    Google Scholar 

  • Tyrer NM, Bell EM (1974) The intensification of cobalt-filled neurone profiles using a modification of Timm's sulphide-silver method. Brain Res 73:151–155

    Google Scholar 

  • Wässle H, Hausen K (1980) Extracellular marking and retrograde labelling of neurons. In: Ch Heym, WG Forssmann (eds) Techniques in Neuroanatomical Research. Springer-Verlag, Heidelberg Berlin New York

    Google Scholar 

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Hausen, K., Wolburg-Buchholz, K. & Ribi, W.A. The synaptic organization of visual interneurons in the lobula complex of flies. Cell Tissue Res. 208, 371–387 (1980). https://doi.org/10.1007/BF00233871

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