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Autoradiographic localization of 3H-γ-aminobutyric acid uptake in the lamina ganglionaris of Musca and Drosophila

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Summary

The uptake of 3H-GABA in the visual system of half-head preparations of Musca and Drosophila was studied by means of light and electron microscope autoradiography. Of all three ganglia, only the first synaptic region, the lamina ganglionaris, showed accumulation of radioactive grains, and there a preferential glial uptake could be found. Under normal light conditions at incubation (constant light flux of 100 Lux) the maximum of radio-activity was found in the marginal glia cells. Increasing the time of incubation produced also an increase in the number of grains per surface unit in the marginal glia cells. After changing the light intensity during incubation, quantitative modifications of the distribution of radio-activity were observed: incubating with stroboscopic illumination, the number of grains diminished in the marginal glia cells and remained constant in the epithelial cells; incubated in darkness, the epithelial cells became more intensely labelled whilst the number of grains decreased in the marginal cells.

The possibility is discussed that the receptor axons 1–6 are the neurological elements of the lamina which use GABA as a transmitter. This hypothesis is lent some support from results of similar experiments with neurological mutants of Drosophila. In opm 18 there was a delayed uptake of 3H-GABA whereas in opm 3 and ebony the results were comparable to those found in Musca incubated in darkness. Behavioral studies on these mutants have demonstrated a defect, most probably related to the receptor system 1–6.

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References

  • Alawi, A. A., Jennings, V., Grossfield, J., Pak, W. L.: Photogransduction mutants of Drosophila melanogaster. In: The visual system: Neurophysiology, Biophysics and their clinical applications, ed. by G. B. Arden, p. 1–21. New York: Plenum Publ. Corp. 1972

    Google Scholar 

  • Arnett, D. W.: Spatial and temporal integration properties of units in first optic ganglion of Dipterans. J. Neurophysiol. 35, 429–444 (1972)

    Google Scholar 

  • Autrum, H., Zettler, F., Järvilehto, M.: Postsynaptic potentials from a single monopolar neuron of the ganglion opticum I of the blowfly Calliphora. Z. vergl. Physiol. 70, 414–424 (1970)

    Google Scholar 

  • Bloom, F. E., Iversen, L. L.: Localizing 3H-GABA in nerve terminals of rat cerebral cortex by electron microscopic autoradiography. Nature (Lond.) 229, 528–630 (1971)

    Google Scholar 

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

    Google Scholar 

  • Boschek, C. B.: Synaptology of the lamina ganglionaris in the fly. In: Information processing in the visual system of Arthropods, ed. by R. Wehner, p. 17–22. Berlin-Heidelberg-New York: Springer 1972

    Google Scholar 

  • Braitenberg, V.: Patterns of projections in the visual system of the fly. 1. Retina-lamina projections. Exp. Brain Res. 3, 271–298 (1967)

    Google Scholar 

  • Braitenberg, V.: Ordnung und Orientierung der Elemente im Sehsystem der Fliege. Kybernetik 7, 235–242 (1969)

    Google Scholar 

  • Brebbia, D. R., Ludwig, D.: Saline solutions for maintaining the isolated heart of the house fly, Musca domestica L. Ann. Ent. Soc. Amer. 55, 131–135 (1962)

    Google Scholar 

  • Burkhardt, D.: Spectral sensitivity and other response characteristics of single visual cells in the arthropod eye. Symp. Soc. exp. Biol. 16, 86–109 (1962)

    Google Scholar 

  • Cajal, S. R.: Nota sobre la retina de la mosca (M. vomitoria L.). Trab. Lab. Invest. Biol. Univ. Madrid 7, 217–257 (1909)

    Google Scholar 

  • Campos-Ortega, J. A., Strausfeld, N. J.: The columnar organization of the second synaptic region of the visual system of Musca domestica L. I. Receptor terminals in the medulla. Z. Zellforsch. 124, 561–585 (1972)

    Google Scholar 

  • Campos-Ortega, J. A., Strausfeld, N. J.: Synaptic connections of intrinsic cells and basket arborizations in the external plexiform layer of the fly's eye. Brain Res. 59, 119–136 (1973)

    Google Scholar 

  • Colonnier, M.: Synaptic patterns of different cell types in the different laminae of the cat visual cortex. An electron microscope study. Brain Res. 9, 268–287 (1968)

    Google Scholar 

  • Curtis, D. R., Johnston, G. A. R.: Amino acid transmitters. In: Handbook of neurochemistry, ed. by A. Latjah, Vol. IV, p. 115–134. New York-London: Plenum Press (1970)

    Google Scholar 

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

    Google Scholar 

  • Eckert, H.: Die spektrale Empfindlichkeit des Komplexauges von Musca (Bestimmungen aus Messungen der optomotorischen Reaktion). Kybernetik 9, 145–156 (1971)

    Google Scholar 

  • Ehinger, B.: Autoradiographic identification of rabbit retinal neurons that take up GABA. Experienta (Basel) 26, 1063–1964 (1970)

    Google Scholar 

  • Ehinger, B.: Cellular location of the uptake of some amino acids into the rabbit retina. Brain Res. 46, 297–311 (1972)

    Google Scholar 

  • Faeder, I. R., Salpeter, M. M.: Glutamate uptake by a stimulated insect nerve muscle preparation. J. Cell Biol. 46, 300–307 (1970)

    Google Scholar 

  • Frontali, N., Pierantoni, R.: Autoradiographic localization of 3H-GABA in the cockroach brain. Comp. Biochem. Physiol. 44, 1369–1372 (1973)

    Google Scholar 

  • Gerschenfeld, H. M.: Chemical transmission in invertebrate central nervous systems and neuromuscular junctions. Physiol. Rev. 53, 1–119 (1973)

    Google Scholar 

  • Guillery, R. W., Colonnier, M.: Synaptic patterns in the dorsal lateral geniculate nucleus of the monkey. Z. Zellforsch. 103, 90–108 (1970)

    Google Scholar 

  • Hebb, C.: CNS at the cellular level: identity of transmitter agents. Ann. Rev. Physiol. 32, 165–192 (1970)

    Google Scholar 

  • Heisenberg, M.: Isolation of mutants lacking the optomotor response. Drosophila Information Service 46, 68 (1971a)

    Google Scholar 

  • Heisenberg, M.: Separation of receptor and lamina potentials in the electroretinogram of normal and mutant Drosophila. J. exp. Biol. 55, 85–100 (1971b)

    Google Scholar 

  • Heisenberg, M.: Behavioural diagnostics; a way to analyse visual mutants of Drosophila. In: Information processing in the visual system of Arthropods. ed. by R. Wehner, 265–268. Berlin-Heidelberg-New York: Springer 1972a

    Google Scholar 

  • Heisenberg, M.: Comparative behavioural studies on two visual mutants of Drosophila. J. comp. Physiol. 80, 119–136 (1972b)

    Google Scholar 

  • Henn, F. A., Hamberger, A.: Glial cell function: Uptake of transmitter substances. Proc. nat. Acad. Sci. (Wash.) 68, 2686–2690 (1971)

    Google Scholar 

  • Hildebrand, J. G., Barker, D. L., Herbert, E., Kravitz, E. A.: Screening for neurotransmitters: a rapid radiochemical procedure. J. Neurobiol. 2, 231–246 (1971)

    Google Scholar 

  • Hökfelt, T., Ljungdahl, A.: Autoradiographic identification of cerebral and cerebellar cortical neurons accumulating labelled gamma-amino-butyric acid (3H-GABA). Exp. Brain Res. 13, 354–263 (1972)

    Google Scholar 

  • Hösli, E., Ljungdahl, A., Hökfelt, T., Hösli, L.: Spinal cord tissue cultures, a model for autoradiographic studies on uptake of putative neurotransmitters such as glycine and GABA. Experientia (Basel) 28, 1342–1344 (1972)

    Google Scholar 

  • Hotta, Y., Benzer, S.: Abnormal electroretinograms in visual mutants of Drosophila. Nature (Lond.) 222, 354–356 (1969)

    Google Scholar 

  • Iversen, L. L.: Neurotransmitters, neurohormones and other small molecules in neurons In: The neurosciences. Second study program, ed. by F. O. Schmitt, p. 768–781. New York: The Rockefeller Univ. Press 1971

    Google Scholar 

  • Iversen, L. L., Bloom, F. E.: Studies of the uptake of 3H-GABA and 3H-glycine in slices and homogenates of rat brain and spinal-cord by electron microscopic autoradiography. Brain Res. 41, 131–143 (1972)

    Google Scholar 

  • Karnovsky, M. J.: A formaldehyde-glutaraldehyde fixative of high osmolarity for use in electronmicroscopy. J. Cell Biol. 27, 137A (1965)

  • Kirschfeld, K.: Das neurale Superpositionsauge. Fortschr. Zool. 21, 229–257 (1973)

    Google Scholar 

  • Kirschfeld, K., Franceschini, N.: Optische Eigenschaften der Ommatidien im Komplexauge von Musca. Kybernetik 5, 47–52 (1968)

    Google Scholar 

  • Kirschfeld, K., Reichardt, W.: Optomotorische Versuche an Musca mit linear polarisiertem Licht. Z. Naturforsch. 25b, 228 (1970)

    Google Scholar 

  • Krnjević, K., Schwartz, S.: Is γ-aminobutyric acid an inhibitory transmitter? Nature (Lond.) 211, 1372–1374 (1966)

    Google Scholar 

  • Krnjević, K., Schwartz, S.: The action of γ-aminobutyric acid on cortical neurons. Exp. Brain Res. 3, 320–336 (1967)

    Google Scholar 

  • Kuhar, M. J., Aghajanian, G. K.: Selective accumulation of 3H-serotonin by nerve terminals of raphe neurons: an autoradiographic study. Nature (Lond.) New Biol. 241, 187–189 (1973)

    Google Scholar 

  • Lam, D.M.K., Steinman, L.: The uptake of (γ-3H) aminobutyric acid in the goldfish retina. Proc. nat. Acad. Sci. (Wash.) 68, 2777–2781 (1971)

    Google Scholar 

  • Langer, H.: Grundlagen der Wahrnehmung von Wellenlängen und Schwingungsebene des Lichtes. Göttingen, Verh. Dtsch Zool. Ges., S. 195–233, 1966

  • Ljungdahl, A., Hökfelt, T.: Accumulation of 3H-glycine in interneurons of the cat spinal cord. Histochemie 33, 277–280 (1973)

    Google Scholar 

  • Llinas, R.: Neurobiology of cerebellar evolution and development, Editor. American Medical Association, Chicago, Ill. 1969

    Google Scholar 

  • Matus, A. I., Dennison, M. E.: An autoradiography study of uptake of exogenous glycine by vertebrate spinal cord slices in vitro. J. Neurocytol. 1, 27–34 (1972)

    Google Scholar 

  • Melamed, J., Trujillo-Cenóz, O.: The fine structure of the central cell in the ommatidia of Dipterans. J. Ultrastruct. Res. 21, 313–334 (1968)

    Google Scholar 

  • Miller, R. F.: Role of K+ in generation of b-wave of electroretinogram. J. Neurophysiol. 36, 28–38 (1973)

    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 

  • Neal, M. J., Iversen, I. L.: Autoradiographic localization of 3H-GABA in rat retina. Nature (Lond.) New Biol. 235, 217–218 (1972)

    Google Scholar 

  • Obata, K., Ito, M., Ochi, R., Sato, N.: Pharmacological properties of the postsynaptic inhibition by Purkinje cell axons and the action of γ-amino-butyric acid on Deiters neurons. Exp. Brain Res. 4, 43–57 (1967)

    Google Scholar 

  • Orkand, P. M., Kravitz, E. A.: Localization of the sites of γ-aminobutyric acid (GABA) up-take in lobster nerve-muscle preparations. J. Cell Biol. 49, 75–89 (1971)

    Google Scholar 

  • Pak, W. L., Grossfield, J., White, N. V.: Nonphototactic mutants in a study of vision of Drosophila. Nature (Lond.) 222, 351–354 (1969)

    Google Scholar 

  • Schon, F., Iversen, L. L.: Selective accumulation of 3H-GABA by stellate cells in rat cerebellar cortex in vivo. Brain Res. 42, 503–507 (1972)

    Google Scholar 

  • Sotelo, C., Privat, A., Drian, M.-J.: Localization of 3H-GABA in tissue culture of rat cerebellum using electron microscopy autoradiography. Brain Res. 45, 302–308 (1972)

    Google Scholar 

  • Strausfeld, N. J.: The organization of the insect visual system (light microscopy). I. Projections and arrangements of neurons in the lamina ganglionaris of Diptera. Z. Zellforsch. 121, 377–441 (1971)

    Google Scholar 

  • Strausfeld, N. J., Campos-Ortega, J. A.: Some interrelationships between the first and second synaptic regions of the fly's (Musca domestica L.) visual system. In: Information processing in the visual system of arthropods, ed. by R. Wehner, p. 23–30. Berlin-Heidelberg-New York: Springer 1972

    Google Scholar 

  • Strausfeld, N. J., Campos-Ortega, J. A.: The L4 monopolar neurone: a substrate for lateral interaction in the visual system of the fly Musca domestica (L.). Brain Res. 59, 97–117 (1973)

    Google Scholar 

  • Trujillo-Cenóz, O.: Some aspects of the structural organization of the intermediate retina of Dipterans. J. Ultrastruct. Res. 13, 1–33 (1965)

    Google Scholar 

  • Uchizono, K.: Characteristics of excitatory and inhibitory synapses in the central nervous system of the cat. Nature (Lond.) 207, 642–643 (1965)

    Google Scholar 

  • Valvidia, O.: Methods of fixation and the morphology of synaptic vesicles. J. comp. Neurol. 142, 257–274 (1971)

    Google Scholar 

  • Zettler, F., Järvilehto, M.: Decrement-free conduction of graded potentials along the axon of a monopolar neuron. Z. vergl. Physiol. 75, 402–421 (1971)

    Google Scholar 

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Campos-Ortega, J.A. Autoradiographic localization of 3H-γ-aminobutyric acid uptake in the lamina ganglionaris of Musca and Drosophila . Z.Zellforsch 147, 415–431 (1974). https://doi.org/10.1007/BF00307474

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