Cell and Tissue Research

, Volume 257, Issue 2, pp 343–366 | Cite as

Neuronal architecture of the central complex in Drosophila melanogaster

  • U. Hanesch
  • K. -F. Fischbach
  • M. Heisenberg
Article

Summary

On the basis of 1200 Golgi-impregnated brains the structure of the central complex of Drosophila melanogaster was analyzed at the cellular level. The four substructures of the central complex — the ellipsoid body, the fanshaped body, the noduli, and the protocerebral bridge — are composed of (a) columnar small-field elements linking different substructures or regions in the same substructure and (b) tangential large-field neurons forming strata perpendicular to the columns. At least some small-field neurons belong to isomorphic sets, which follow various regular projection patterns. Assuming that the blebs of a neuron are presynaptic and the spines are postsynaptic, the Golgi preparations indicate that small-field neurons projecting to the ventral bodies (accessory area) are the main output from the central complex and that its main input is through the large-field neurons. These in turn are presumed to receive input in various neuropils of the brain including the ventral bodies. Transmitters can be attributed immunocytochemically to some neuron types. For example, GABA is confined to the R1–R4 neurons of the ellipsoid body, whereas these cells are devoid of choline acetyltransferase-like immunore-activity. It is proposed that the central complex is an elaboration of the interhemispheric commissure serving the fast exchange of data between the two brain hemispheres in the control of behavioral activity.

Key words

Central complex Golgi impregnation Neurotransmitters Protocerebrum, insect Immunocytochemistry Drosophila melanogaster (Insecta) 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Bausenwein B (1988) Neuronale Aktivitätsmarkierung während visueller Flugsteuerung von Drosophila melanogaster. Dissertation WürzburgGoogle Scholar
  2. Blest AD (1961) Some modifications of Holme's silver method for insect central nervous system. Q J Microsc Sci 102:413–417Google Scholar
  3. Buchner E, Buchner S (1984) Neuroanatomical mapping of visually induced nervous activity in insects by 3H-deoxyglucose. In: Ali MA (ed) Photoreception and vision in invertebrates. Plenum Press New York, pp 623–634Google Scholar
  4. 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 246:57–62Google Scholar
  5. 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 253:357–370Google Scholar
  6. Colonnier M (1964) The tangential organization of the visual cortex. J Anat 98:327–344Google Scholar
  7. Drescher W (1960) Regenerationsversuche am Gehirn von Periplaneta americana unter Berücksichtigung von Verhaltensänderungen und Neurosekretion. Z Morphol Ökol Tiere 48:576–649Google Scholar
  8. Duve H, Thorpe A, Strausfeld NJ (1983) Cobalt-immunocytochemical identification of peptidergic neurons in Calliphora innervating central and peripheral targets. J Neurocytol 12:847–861Google Scholar
  9. Fischbach KF, Götz C (1981) Das Experiment: ein Blick ins Fliegenhirn: Golgi-gefärbte Nervenzellen bei Drosophila. Biu Z 11:183–187Google Scholar
  10. Fischbach KF, Heisenberg M (1981) Structural brain mutant of Drosophila melanogaster with reduced cell number in the medulla cortex and with normal optomotor response. Proc Natl Acad Sci USA 78:1105–1109Google Scholar
  11. Goll W (1967) Strukturuntersuchungen am Gehirn von Formica. Z Morphol Ökol Tiere 59:143–210Google Scholar
  12. Goodman CS, Williams JLD (1976) Anatomy of the ocellar interneurons of acridid grasshoppers. II. The small interneurons. Cell Tissue Res 175:203–207Google Scholar
  13. Gorczyca M, Hall J (1987) Immunocytochemical localization of choline acetyltransferase during development and in mutant Drosophila melanogaster. Soc Neurosci Abstr 12:245Google Scholar
  14. Hanesch U (1987) Der Zentralkomplex von Drosophila melanogaster. Dissertation WürzburgGoogle Scholar
  15. Hanström B (1928) Vergleichende Anatomie des Nervensystems der wirbellosen Tiere. Springer, Berlin Heidelberg New YorkGoogle Scholar
  16. Hauusen K (1981) Monocular and binocular computation of motion in the lobula plate of the fly. Verh Dtsch Zool Ges 1981:49–70Google Scholar
  17. Heisenberg M, Wonneberger R, Wolf R (1978) optomotor-blindH31 — a Drosophila mutant of the lobula plate giant neurons. J Comp Physiol 124:287–296Google Scholar
  18. Heisenberg M, Borst A, Wagner S, Byers D (1985) Drosophila mushroom body mutants are deficient in olfactory learning. J Neurogenet 2:1–30Google Scholar
  19. Hertweck H (1931) Anatomie und Variabilität des Nervensystems und der Sinnesorgane von Drosophila melanogaster. Z Wiss Zool 139:559–663Google Scholar
  20. Hofbauer A (1987) Monoclonal antibodies reveal anatomical details in the Drosophila brain. In: Elsner N, Creutzfeldt O (eds) New frontiers in brain research. Thieme, Stuttgart New YorkGoogle Scholar
  21. Homberg U (1985) Interneurons of the central complex in the bee brain (Apis mellifica L.). J Insect Physiol 31:251–264Google Scholar
  22. Homberg U (1987) Structure and functions of the central complex in insects. In: Gupta AP (ed) Arthropod brain. Wiley, New York Chichester Brisbane Toronto SingaporeGoogle Scholar
  23. Honegger HW, Schürmann FWE (1975) Cobalt sulphide staining of optic fibres in the brain of the cricket, Gryllus compestris. Cell Tissue Res 159:213–225Google Scholar
  24. Horridge GA (1965) Arthropod A: General anatomy. In: Bullock TH, Horridge GA (eds) Structure and function in the nervous system of invertebrates vol 2. Freeman, San FranciscoGoogle Scholar
  25. Huber F (1955) Sitz und Bedeutung nervöser Zentren für Instinkthandlungen beim Männchen von Gryllus campestris. Z Tierpsychol 12:12–18Google Scholar
  26. Huber F (1960) Untersuchungen über die Funktion des Zentralnervensystems und insbesondere des Gehirns bei der Fortbewegung und Lauterzeugung der Grillen. Z Vergl Physiol 44:60–132Google Scholar
  27. Meyer EP, Matute C, Streit P, Nässel DR (1986) Insect optic lobe neurons identifiable with monoclonal antibodies to GABA. Histochemistry 84:207–216Google Scholar
  28. Otto D (1971) Untersuchungen zur zentralnervösen Kontrolle der Lauterzeugung von Grillen. Z Vergl Physiol 74:227–271Google Scholar
  29. Power ME (1943) The brain of Drosophila melanogaster J Morphol 72:517–559Google Scholar
  30. Schäfer S, Bicker G (1986) Distribution of GABA-like immunoreactivity in the brain of the honeybee. J Comp Neurol 246:287–300Google Scholar
  31. Schildberger K (1982) Untersuchungen zur Struktur und Funktion von Interneuronen im Pilzkörperbereich des Gehirns der Hausgrille Acheta domesticus. Dissertation GöttingenGoogle Scholar
  32. Schildberger K (1983) Local interneurons associated with the mushroom bodies and the central body in the brain of Acheta domesticus. Cell Tissue Res 230:573–586Google Scholar
  33. Schürmann FW (1974) Bemerkungen zur Funktion der Corpora pedunculata im Gehirn der Insekten aus morphologischer Sicht. Exp Brain Res 19:406–432Google Scholar
  34. 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) Neurones without impulses. Cambridge University Press, CambridgeGoogle Scholar
  35. Strausfeld N (1976) Atlas of an insect brain. Springer, Berlin Heidelberg New YorkGoogle Scholar
  36. Viallanes H (1886) La structure du cerveau des hymenopteres. Bull Soc Philom Paris 10:82–83Google Scholar
  37. Williams JLD (1972) Some observations on the neuronal organization of the supraoesophageal ganglion in Schistocerca gregaria with particular reference to the central complex. Dissertation CardiffGoogle Scholar
  38. Williams JLD (1975) Anatomical studies of the insect nervous system: A ground-plan of the midbrain and an introduction of the central complex in the locust, Schistocerca gregaria (Orthoptera). J Zool Lond 176:67–86Google Scholar

Copyright information

© Springer-Verlag 1989

Authors and Affiliations

  • U. Hanesch
    • 1
  • K. -F. Fischbach
    • 1
  • M. Heisenberg
    • 1
  1. 1.Institut für Genetik und MikrobiologieWürzburgGermany

Personalised recommendations