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The optic lobe of Drosophila melanogaster. I. A Golgi analysis of wild-type structure

Summary

Golgi studies of the neurons in the optic lobes of Drosophila melanogaster reveal a large number of neuronal cell types. These can be classified as either columnar or tangential. Columnar elements establish the retinotopic maps of the lamina, medulla, and lobula-complex neuropiles. They are classified according to the position of their cell bodies, the number, width, and level of their arborizations, and their projection areas. Tangential elements are oriented perpendicularly to the columns. The arborizations of different tangential neurons are restricted to different layers of the optic neuropiles, within such layers their dendritic fields may span the entire retinotopic field or only part of it. The abundance of cell types inside each of the columnar units of the optic lobe is discussed with regard to its possible functional significance. By means of their stratified arborizations the columnar neurons form what appear to be multiple sets of retinotopically organized parallel information processing networks. It is suggested that these parallel networks filter different kinds of visual information and thus represent structurally separated functional subunits of the optic lobe. Such a parallel organization of visual functions increases the sites for function-specific gene actions and may explain the behavioral phenotypes of recently isolated structural mutants of the optic lobe.

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References

  1. Aceves-Piña EO, Booker R, Duerr JS, Livingstone MS, Quinn WG, Smith RF, Sziber PP, Tempel BL, Tully TP (1983) Learning and memory in Drosophila studied with mutants. Cold Spring Harbor Symp Quant biol 48:831–840

  2. Armett-Kibel C, Meinertzhagen IA, Dowling JE (1977) Cellular and synaptic organization in the lamina of the dragon-fly Sympetrum rubicundulum. Proc R Soc Lond [Biol] 196:385–413

  3. Bausenwein B (1988) Neuronale Aktivitätsmarkierung während visueller Flugsteuerung von Drosophila melanogaster. Dissertation. Julius-Maximilians-Universität Würzburg, FRG

  4. Benzer S (1971) From the gene to behavior. J Am Med Assoc 218:1015–1022

  5. Blest AD (1961) Some modifications of Holme's silver method for insect central nervous system. Q J Micr Sci 102:413–417

  6. Blondeau J, Heisenberg M (1982) The three-dimensional optomotor torque system of Drosophila melanogaster. Studies on wildtype and the mutant optomotor blindH13. J Comp Physiol 145:321–329

  7. Borst A, Fischbach K-F (1987) Golgi and degeneration studies of the antennal lobes of Drosophila melanogaster. J Neurogenetics 4:115–117

  8. Boschek CR (1971) On the fine structure of the peripheral retina and the lamina of the fly Musca domestica. Z Zellforsch 110:336–349

  9. Boschert U, Ramos R GP, Tix S, Technau GM, Fischbach K-F (1989) Genetic and developmental analysis of irreC, a genetic function required for optic chiasm formation in Drosophila. J Neurogenetics (submitted)

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

  11. Braitenberg V, Debbage P (1974) A regular net of reciprocal synapses in the visual system of the fly, Musca domestica. J Comp Physiol 90:25–31

  12. Braitenberg V, Strausfeld NJ (1970) The compound eye of the fly (Musca domestica): Connections between the cartridges of the lamina ganglionaris. Z vergl Physiol 70:95–104

  13. Buchner E, Buchner S, Bülthoff I (1984) Deoxyglucose mapping of nervous activity induced in Drosophila brain by visual movement. J Comp Physiol [A] 155:471–483

  14. Buchner E, Buchner S, Crawford G, Mason WT, Salvaterra PM, Sattelle DB (1986) Choline acetyltransferase-like immunoreactivity in the brain of Drosophila melanogaster. Cell Tissue Res 246:57–62

  15. Buchner E, Bader R, Buchner S, Cox J, Emson PC, Flory E, Heizmann CW, Hemm S, Hofbauer A, Oertel WH (1988) Cell-specific immunoprobes for the brain of normal and mutant Drosophila melanogaster. Cell Tissue Res 253:357–370

  16. Bülthoff I, Buchner E (1985) Deoxyglucose mapping of nervous activity induced in Drosophila brain by visual movement. II. optomotor blindH31 and lobula plate-less N684, visual mutants. J Comp Physiol [A] 156:25–34

  17. Burkhardt W, Braitenberg V (1976) Some peculiar synaptic complexes in the first visual ganglion of the fly Musca domestica. Cell Tissue Res 173:287–308

  18. Cajal SR, Sánchez D (1915) Contribucion al conocimiento de los centros nerviosos de los insectos. Parte I, retina y centros opticos. Trab Lab Invest Biol Univ Madr 13:1–168

  19. Campos-Ortega JA, Strausfeld NJ (1972a) Columns and layers in the second synaptic region of the fly's visual system. The case for two superimposed neuronal architectures. In: Wehner R (ed) Information processing in the visual system of arthropods. Springer, Berlin Heidelberg New York

  20. Campos-Ortega JA, Strausfeld NJ (1972b) 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

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

  22. Colonnier M (1964) The tangential organization of the visual cortex. J Anat 98:327–344

  23. Datum K-H, Weiler R, Zettler F (1986) Immunocytochemical demonstration of γ-amino butyric acid and glutamic acid decarboxylase in R7 photoreceptors and C2 centrifugal fibers in the blowfly visual system. J Comp Physiol 159:241–249

  24. Dumont JPC, Robertson RM (1986) Neuronal circuits: An evolutionary perspective. Science 233:849–853

  25. Ewer J, Rosbash M, Hall JC (1988) An inducible promoter fused to the period gene in Drosophila conditionally rescues adult per-mutant arrhythmicity. Nature 333:82–84

  26. Fischbach K-F (1983a) Neural cell types surviving congenital sensory deprivation in the optic lobes of Drosophila melanogaster. Dev Biol 95:1–18

  27. Fischbach K-F (1983b) Neurogenetik am Beispiel des visuellen Systems von Drosophila melanogaster. Habilitation Thesis. University of Würzburg

  28. Fischbach K-F, Bausenwein B (1988) Habituation and sensitization of the landing response of Drosophila melanogaster: II. Receptive field size of habituating units. In: Hertting G, Spatz H Ch (eds) Modulation of synaptic transmission and plasticity in nervous systems. NATO ASI Series, Springer, Berlin Heidelberg New York, pp 369–385

  29. Fischbach K-F, Götz CR (1981) Das Experiment. Ein Blick ins Fliegengehirn: Golgi gefärbte Nervenzellen bei Drosophila. BiuZ 11:183–187

  30. Fischbach K-F, Heisenberg M (1981) Structural brain mutant of Drosophila melanogaster with reduced cell number in the medulla cortex and with normal optomotor yaw response. Proc Natl Acad Sci USA 78:1105–1109

  31. Fischbach K-F, Heisenberg M (1984) Neurogenetics and behaviour in insects. J Exp Biol 112:65–93

  32. Fischbach K-F, Lyly-Hünerberg I (1983) Genetic dissection of the anterior optic tract. Cell Tissue Res 231:551–563

  33. Fischbach K-F, Technau G (1984) Cell degeneration in the developing optic lobes of the sine oculis and small optic lobes mutants of Drosophila melanogaster. Dev Biol 104:219–239

  34. Fischbach K-F, Technau G (1987) Mutant analysis of optic lobe development in Drosophila. In: Elsner N, Creutzfeld O (ed) New frontiers in brain research. Georg Thieme Verlag, Stuttgart New York

  35. Fischbach KF, Barleben F, Boschert U, Dittrich APM, Gschwander B, Houbé B, Jäger R, Kaltenbach E, Ramos RGP, Schlosser G (1989) Developmental studies on the optic lobe of Drosophila melanogaster using structural brain mutants. In: Singh RN, Strausfeld NJ (eds) Neurobiology of sensory systems. Plenum Press

  36. Franceschini N, Hardie R, Ribi W, Kirschfeld K (1981) Sexual dimorphism in a photoreceptor. Nature 291:241–244

  37. Garen SH, Kankel DR (1983) Golgi and genetic mosaic analyses of visual system mutants in Drosophila melanogaster. Dev Biol 96:445–466

  38. Goodman CS (1977) Neuron duplications and deletions in locust clones and clutches. Science 197:1384–1386

  39. Goodman CS, Raper JA, Ho RK, Chang S (1982) Pathfinding of neuronal growth cones in grasshopper embryos. In: Subtelny S, Green PB (eds) Developmental order: its origin and regulation. Alan R Liss, New York, pp 275–316

  40. Hall JC (1982) Genetics of the nervous system in Drosophila. Q Rev Biophys 15:223–479

  41. Hall JC (1984) Genetic analysis of behavior in insects. In: Kerkut GA, Gilbert LI (eds) Comprehensive Insect Physiology Biochemistry and Pharmacology 9:287–373

  42. Hanesch U (1986) Der Zentralkomplex von Drosophila melanogaster. PHD Thesis, University of Würzburg

  43. Hanesch U, Fischbach KF, Heisenberg M (1989) Neuronal architecture of the central complex in Drosophila melanogaster. Cell Tissue Res 257:343–366

  44. Hanström B (1928) Vergleichende Anatomie des Nervensystems der wirbellosen Tiere. Springer, Berlin Heidelberg New York

  45. Hardie RC (1983) Projection and connectivity of sex-specific photoreceptors in the compound eye of the male housefly (Musca domestica). Cell Tissue Res 233:1–21

  46. Hardie RC (1984) Properties of photoreceptors R7 and R8 in dorsal marginal ommatidia in the compound eyes of Musca and Calliphora. J Comp Physiol 154:157–165

  47. Hardie RC (1986) The photoreceptor array of the dipteran retina. TINS 9:419–423

  48. Hardie RC (1987) Is histamine a neurotransmitter in insect photoreceptors? J Comp Physiol 161:201–213

  49. Harris WS, Stark WS, Walker JA (1976) Genetic dissection of the photoreceptor system in the compound eye of Drosophila melanogaster. J Physiol (Lond) 256:415–439

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

  51. Hausen K (1981) Monocular and binocular compution of motion in the lobula plate of the fly. Verh Dtsch Zool Ges 49–70

  52. Hausen K, Strausfeld NJ (1980) Sexually dimorphic interneuron arrangements in the fly visual system. Proc R Soc Lond [Biol] 208:57–71

  53. Hauser-Holschuh H (1975) Vergleichend quantitative Untersuchungen an den Sehganglien der Fliegen Musca domestica and Drosophila melanogaster. Dissertation Tübingen

  54. Heisenberg M (1980) Mutants of brain structure and function: What is the significance of the mushbroom bodies for behavior? In: Siddiqi O, Babu P, Hall LM, Hall JC (eds) Development and Neurobiology of Drosophila. Plenum Press, New York, pp 373–390

  55. Heisenberg M, Buchner E (1977) The rôle of retinula cell types in visual behavior of Drosophila melanogaster. J Comp Physiol 117:127–162

  56. Heisenberg M, Wolf R (1984) Vision in Drosophila. Genetics of microbehavior. Springer, Berlin Heidelberg New York

  57. Heisenberg M, Wonneberger R, Wolf R (1978) Optomotor blindH31 — A Drosophila mutant of the lobula plate giant neurons. J Comp Physiol [A] 124:287–296

  58. Hofbauer A (1979) Die Entwicklung der optischen Ganglien bei Drosophila melanogaster. Dissertation, Universität Freiburg

  59. Hu KG, Stark WS (1977) Specific receptor input into spectral preference in Drosophila. J comp Physiol 121:241–252

  60. Jacob KG, Willmund R, Folkers E, Fischbach KF, Spatz H Ch (1977) T-maze phototaxis of Drosophila melanogaster and several mutants in the visual system. J Comp Physiol 116:209–225

  61. Kirschfeld K (1967) Die Projektion der optischen Umwelt auf das Raster der Rhabdomere im Komplexauge von Musca. Exp Brain Res 3:248–270

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

  63. Konopka R, Wells S, Lee T (1983) Mosaic analysis of a Drosophila clock mutant. Mol Gen Genetics 190:284–288

  64. Kral K, Meinertzhagen IA (1989) Anatomical plasticity of synapses in the lamina of the optic lobe of the fly. Philos Trans R Soc Lond [Biol] 323:155–183

  65. Land MF, Collett TS (1974) Chasing behavior of houseflies (Fannia cannicularis). J Comp Physiol 89:331–357

  66. Macagno ER, Lopresti V, Levinthal C (1973) Structure and development of neuronal connections in isogenic organisms. Variation and similarities in the optic system of Daphnia. Proc Natl Acad Sci USA 70:57–61

  67. Meinertzhagen IA (1973) Development of the compound eye and optic lobe of insects. In: Young D (ed) Developmental neurobiology of arthropods. Cambridge University Press

  68. Meinertzhagen IA (1989) Fly photoreceptor synapses: their development, evolution and plasticity. J Neurobiol 20:276–294

  69. Meinertzhagen IA, O'Neil S (1988) The lamina cartridge in the optic lobe of Drosophila. Soc Neurosci [Abstr] 14:376

  70. Nässel DR (1988a) Serotonin and serotonin-immunoreactive neurons in the nervous system of insects. Prog Neurobiol 30:1–85

  71. Nässel DR (1988b) Immunocytochemistry of putative neuroactive substances in the insect brain. In: Salanki J, Rósza KS (eds) Neurobiology of invertebrates: Transmitters, modulators and receptors. Akadémiai Kiadó, Budapest

  72. Nässel DR, Sivasubramanian P (1983) Neural differentiation in fly CNS transplants cultured in vivo. J Exp Zool 225:301–310

  73. Nässel DR, Hagberg M, Seyan HS (1983) A new, possibly serotonergic neuron in the lamina of the blowfly optic lobe: an immunocytochemical and Golgi-EM study. Brain Res 280:361–367

  74. Nässel DR, Meyer EP, Klemm N (1985) Mapping and ultrastructure of serotonin-immunoreactive neurons in the optic lobes of three insect species. J Comp Neurol 232:190–204

  75. Nässel DR, Ohlsson L, Sivasubramanian P (1987) Differentiation of serotonin-immunoreactive neurons in fly optic lobes developing in situ or cultured in vivo without eye discs. J Comp Neurol 255:327–340

  76. Nässel Dr, Holmquist MH, Hardie RC, Håkanson R, Sundler F (1988) Histamine-like immunoreactivity in photoreceptors of the compound eyes and ocelli of the flies (Calliphora erythrocephala and Musca domestica). Cell Tissue Res 253:639–646

  77. Nicol D, Meinertzhagen IA (1982) An analysis of the number and composition of the synaptic populations formed by photoreceptors of the fly. J Comp Neurol 207:29–44

  78. Ohlsson LG, Nässel DR (1987) Postembryonic development of serotonin-immunoreactive neurons in the central nervous system of the blowfly, Calliphora erythrocephala. I. The optic lobes. Cell Tissue Res 249:669–679

  79. Paulus HF (1979) Eye structure and the monophyly of the Arthropoda. In: Gupta AP (ed) Arthropod phylogeny. Van Nostrand Reinhold Comp, New York, pp 299–383

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

  81. Power ME (1943) The effect of reduction in numbers of ommatidia upon the brain of Drosophila melanogaster. J Exp Zool 94:33–71

  82. Ribi WA (1981) The first optic ganglion of the bee. IV. Synaptic fine structure and connectivity patterns of receptor cell axons and first order interneurones. Cell Tissues Res 215:443–464

  83. Shaw SR (1981) Anatomy and physiology of identified non-spiking cells in the photoreceptor-lamina complex of the compound eye of insects especially Diptera. In: Roberts A, Bush BMH (eds) Neurons without Impulses. Cambridge University Press

  84. Shaw SR (1984) Early visual processing in insects. J Exp Biol 112:225–251

  85. Shaw SR, Meinertzhagen IA (1986) Evolutionary progression at synaptic connections made by identified homologous neurons. Proc Natl Acad Sci USA 83:7961–7965

  86. Steller H, Fischbach K-F, Rubin G (1987) Disconnected: A locus required for neuronal pathway formation. Cell 50:1139–1153

  87. Stent GS (1981) Strength and weakness of the genetic approach to the development of the nervous system. Annu Rev Neurosci 4:163–194

  88. Stocker RF, Singh RN, Schorderet M, Siddiqi O (1983) Projection patterns of different types of antennal sensilla in the antennal glomeruli of Drosophila melanogaster. Cell Tissue Res 232:237–248

  89. Strausfeld NJ (1970) Golgi studies on insects. Part II. The optic lobes of Diptera. Philos Trans R Soc Lond 258:135–223

  90. Strausfeld NJ (1971) The organization of the insect visual system (light microscopy). II. The projection of fibres across the first optic chiasm. Z Zellforsch 121:442–454

  91. Strausfeld NJ (1976) Atlas of an insect brain. Springer, Berlin Heidelberg New York

  92. Strausfeld NJ (1979) The representation of a receptor map within retinotopic neuropil of the fly. Verh Dtsch Zool Ges 72:167–179

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

  94. Strausfeld NJ (1980b) The Golgi method. Its application to the insect nervous system and the phenomenon of stochastic impregnation. In: Strausfeld NJ, Miller TA (eds) Neuroanatomical techniques. Insect nervous system. Springer, Berlin Heidelberg New York

  95. Strausfeld NJ (1984) Functional neuroanatomy of the blowfly's visual system. In: Ali MA (ed) Photoreception and vision in invertebrates. Plenum Publishing Corporation.

  96. Strausfeld NJ, Bassimir UK (1983) Cobalt-coupled neurons of a giant fibre system in Diptera. J Neurocytol 12:971–991

  97. Strausfeld NJ, Blest AD (1970) Golgi study on insects. Part I. The optic lobes of Lepidoptera. Philos Trans R Soc Lond [Biol] 258:81–134

  98. Strausfeld NJ, Campos-Ortega JA (1972) Some interrelationships between the first and second synaptic regions of the fly's (Musca domestica) visual system. In: Wehner R (ed) Information processing in the visual system of arthropods. Springer, Berlin Heidelberg New York

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

  100. Strausfeld NJ, Campos-Ortega JA (1973b) L3, the 3rd 2nd order neuron of the 1st visual ganglion in the “neural superposition” eye of Musca domestica. Z Zellforsch 139:397–403

  101. Strausfeld NJ, Campos-Ortega JA (1977) Vision in insects. Pathways possibly underlying neural adaptation and lateral inhibition. Science 195:894–897

  102. Strausfeld NJ, Hausen K (1977) The resolution of neuronal assemblies after cobalt injection into neuropil. Proc R Soc Lond 1998:463–476

  103. Strausfeld NJ, Nässel DR (1981) Neuroarchitecture of brain regions that subserve the compound eyes of crustacia and insects. In: Handbook of sensory physiology Vol. VII/6B. Springer, Berlin Heidelberg New York

  104. Strausfeld NJ, Wunderer H (1985) Optic lobe projections of marginal ommatidia in Calliphora erythrocephala specialized forthe detection of polarized light. Cell Tissue Res 242:163–178

  105. Strausfeld NJ, Bassemir UK, Singh RN, Bacon JP (1984) Organizational principles of outputs from dipteran brains. J Insect Physiol 30:73–93

  106. Stürmer CAO (1988) The trajectories of regenerating retinal axons in the goldfish. II. Exploratory branches and growth cones on axons at early regeneration stages. J Comp Neurol 267:69–91

  107. Tanouye MA, Wyman R (1980) Motor outputs of giant nerve fibres in Drosophila. J. Neurophysiol 44:405–421

  108. Technau GM (1984) Fiber number in the mushroom bodies of adult Drosophila melanogaster depends on age, sex and experience. J Neurogenetics 1:113–126

  109. Technau GM, Heisenberg M (1982) Neural reorganization during metamorphosis of the corpora pedunculata in Drosophila melanogaster. Nature 295:405–407

  110. Tix S, Minden JS, Technau GM (1989) Pre-existing neuronal pathways in the developing optic lobes of Drosophila. Development 105:739–746

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

  112. Tully T (1988) On the road to a better understanding of learning and memory in Drosophila melanogaster. In: Hertting G, Spatz H Ch (eds) Modulation of synaptic transmission and plasticity in nervous system. NATO ASI Series, Springer, Berlin Heidelberg New York

  113. Wada S (1974) Spezielle randzonale Ommatidien von Calliphora erythrocephala Meig. (Diptera, Calliphoridae): Architektur der zentralen Rhabdomeren-Kolumne und Topographie im Komplexauge. Int J Insect Morphol Embryol 3:397–424

  114. Wehner R (1983) Celestial and terrestrial navigations: Human strategies — insect strategies. In: Huber F, Markl H (eds) Neuroethology and behavioural physiology. Springer, Berlin Heidelberg New York, pp 366–381

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Fischbach, K.-., Dittrich, A.P.M. The optic lobe of Drosophila melanogaster. I. A Golgi analysis of wild-type structure. Cell Tissue Res. 258, 441–475 (1989). https://doi.org/10.1007/BF00218858

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Key words

  • Optic lobe
  • Neurons
  • Cell types
  • Structurae mutanto
  • Drosophila melanogaster (Insecta)