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Postembryonic development of serotonin-immunoreactive neurons in the central nervous system of the blowfly, Calliphora erythrocephala

I. The optic lobes

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Summary

The postembryonic development of serotonin-immunoreactive (5-HTi) neurons was studied in the optic lobe of the blowfly. In the adult fly there are 24 5-HTi neurons invading each optic lobe. The perikarya of two of these neurons are situated in the dorso-caudal part of the protocerebrum (LBO-5HT neurons; large bilateral optic lobe 5-HTi neurons). The cell bodies of the remaining 22 neurons are located anteriorly at the medial base of the medulla (2 innervating the lobula, LO-5HT neurons; and 20 neurons innervating the medulla, ME-5HT neurons). The two central neurons (LBO-5HT neurons) are derived from metamorphosing larval neurons, while the ME- and LO-5HT neurons are imaginai optic lobe neurons differentiating during pupal development.

The 5-HTi neurons of the optic lobe seem to have different ancestors. The LBO-5HT neurons are probably derived from segmental protocerebral neuroblasts, whereas the ME-and LO-5HT neurons are most likely derived from the inner optic anlage. The first 5-HTi fibers to reach the imaginal optic lobes are seen in the late third instar larva and are derived from the LBO-5HT neurons. The first ME- and LO-5HT neurons become immunoreactive at 24 h (10%) pupal development. At about 96 h (40%) of pupal development all the 5-HTi neurons of the optic lobes have differentiated and attained their basic adult morphology. The further development mainly entails increase in volume of arborizations and number of finer processes. The differentiation and outgrowth of 5-HTi processes follows that of, e.g., columnar neurons in the optic lobe neuropils. Hence, 5-HTi processes invade neuropil relatively late in the differentiation of the optic lobe.

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References

  1. Anderson H (1978a) Postembryonic development of the visual system of the locust Schistocerca gregaria I. Patterns of growth and developmental interactions in the retina and optic lobe. J Embryol Exp Morphol 45:55–83

  2. Anderson H (1978b) Postembryonic development of the visual system of the locust Schistocerca gregaria. II. An experimental investigation of the formation of the retina-lamina projection. J Embryol Exp Morphol 46:147–170

  3. Burden HW, Lawrence IE (1973) Precence of biogenic amines in early rat development. Am J Anat 136:251–257

  4. Campos-Ortega JA (1980) On compound eye development in Drosophila melanogaster. In: Hunt RK (ed) Current topics in dev biol, vol 15, Academic Press, New York, pp 347–371

  5. Campos-Ortega JA, Hartenstein V (1985) Development of the nervous system. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology biochemistry and pharmacology, vol 5, Pergamon Press, New York, pp 49–84

  6. Cantera R, Nässel DR (1987) Postembryonic development of serotonin-immunoreactive neurons in the central nervous system of the blowfly. II. The thoracico-abdominal ganglia. Cell Tissue Res (in press)

  7. Fischbach KF (1983) Neural cell types surviving congenital sensory deprivation in the optic lobes of Drosophila melanogaster. Dev Biol 95:1–18

  8. Frölich A, Meinertzhagen IA (1982) Synaptogenesis in the first optic neuropil of the fly's visual system. J Neurocytol 11:159–180

  9. Goodman CS, Bastiani MJ, Doc CQ, Du Lac S, Helfand SL, Kuwada JY, Thomas JB (1984) Cell recognition during neuronal development. Science 222:1271–1279

  10. Gundersen RW, Larsen JR (1978) Postembryonic development of the optic lobes of Phormia regina Meigen (Diptera:Calliphoriae). Int J Insect Morphol Embryol 7:121–136

  11. Hildebrand JG (1985) Metamorphosis of the insect nervous system: Influences of the periphery on the postembryonic development of the antennal sensory pathway in the brain of Manduca sexta. In: Selverston AI (ed) Model neural networks and behavior, Plenum Press, New York, pp 124–148

  12. Lauder JM, Wallace JA, Krebs H, Petrusz P, McCarthy K (1982) In vivo and in vitro development of serotonergic neurons. Brain Res 9:605–625

  13. Levine RB (1984) Changes in neuronal circuits during insect metamorphosis. J Exp Biol 112:27–44

  14. Levine RB, Truman JW (1982) Metamorphosis of the insect nervous system: Changes in morphology and synaptic interaction of identified neurons. Nature 299:250–252

  15. Levine RB, Truman JW (1985) Fate of abdominal motorneurons during metamorphosis of the moth, Manduca sexta. J Neurosci 5:2424–2431

  16. Levine RB, Pak C, Linn D (1985) The structure, function and metamorphic reorganization of somatotopically projecting sensory neurons in Manduca sexta. J Comp Physiol 157:1–13

  17. Levine RB, Truman JW, Linn D, Bate CM (1986) Endocrine regulation of the form and function of axonal arbors during insect metamorphosis. J Neurosci 6(1):293–299

  18. Meinertzhagen IA (1973) Development of compound eye and optic lobe of insects. In: Young D (ed) Developmental neurobiology of arthropods, London, Cambridge University Press, pp 51–104

  19. Meinertzhagen IA, Fröhlich A (1983) The regulation of the synapse formation in the fly's visual system. Trends Neurosci 6:223–228

  20. Meyerowitz EM, Kankel DR (1978) A genetic analysis of visual system development in Drosophila melanogaster. Dev Biol 62:112–142

  21. Nässel DR (1987) Serotonin and serotonin-immunoreactive neurons in the nervous system of insects. Prog Neurobiol (In press)

  22. Nässel DR, Cantera R (1985) Serotonin-immunoreactive neurons in the larval nervous system of Calliphora erythrocephala and Sarcophaga bullata. A comparison with ventral ganglia in adult animals. Cell Tissue Res 239:423–434

  23. Nässel DR, Elekes K (1984) Ultrastructural demonstration of serotonin-immunoreactivity in the nervous system of an insect (Call iphora erythrocephala). Neurosci Lett 48:203–210

  24. Nässel DR, Geiger G (1983) Neuronal organization in the fly optic lobes altered by laser ablations early in development or by mutations of the eye. J Comp Neurol 217:86–102

  25. Nässel DR, Klemm N (1983) Serotonin-like immunoreactivity in the optic lobes of three insect species. Cell Tissue Res 232:129–140

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

  27. Nässel DR, Hagberg M, Seyan H (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

  28. 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

  29. Nässel DR, Ohlsson LG, Sivasubramanian P (1987) Postembryonic differentiation of serotonin-immunoreactive neurons in fleshfly optic lobes developing in situ or cultured in vivo without eye discs. J Comp Neurol 255:327–340

  30. Nordlander RH, Edwards JS (1969) Postembryonic brain development in the monarch butterfly, Danaus plexippus plexippus L II. The optic lobes. Wilhelm Roux Arch Entw Mech Org 163:197–220

  31. Olsson L, Seiger Å (1972) Early prenatal ontogeny of central monoamine neurons in the rat: fluorescence histochemical observations. Z Anat Entwgesch 137:301–316

  32. Raper JA, Bastiani MJ, Goodman CS (1983) Pathfinding by neuronal growth cones in grasshopper embryos. I. Divergent choices made by growth cones of sibling neurones. J Neurosci 3:20–30

  33. Strausfeld NJ, Nässel DR (1980) Neuroarchitecture of brain regions that subserve compound eyes of Crustacea and insects. In: Autrum H (ed) Handbook of sensory physiology, VII/6B. Springer, Berlin Heidelberg New York, pp 1–132

  34. Taghert PH, Goodman CS (1984) Cell determination and differentiation of identified serotonin-immunoreactive neurons in the grasshopper embryo. J Neurosci 4:984–1000

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

  36. Trujillo-Cenoz O, Melamed J (1973) The development of the retina-lamina complex in muscoid flies. J Ultrastruct Res 42:554–581

  37. Truman JW, Reiss SE (1976) Dendritic reorganization of an identified motorneuron during metamorphosis of the tobacco hornworm moth. Science 192:477–479

  38. Venkatesh TR, Zipursky SL, Benzer S (1985) Molecular analysis of the development of the compound eye in Drosophila. Trends Neurosci 8:251–257

  39. Wallace JA (1982) Monoamines in the early chick embryo: demonstration of serotonin synthesis and the regional distribution of serotonin-concentrating cells during morphogenesis. Am J Anat 165:261–276

  40. Wallace JA, Lauder JM (1983) Development of the serotoninergic system in the rat embryo: an immunocytochemical study. Brain Res 10:459–479

  41. Weisblat DA, Kristan Jr WB (1985) The development of serotoninontaining neurons in the leech. In: Selverston AI (ed) Model neural networks and behavior. Plenum Press, New York, pp 175–190

  42. White K, Kankel DR (1978) Patterns of cell division and cell movement in the formation of the imginal nervous system in Drosophila melanogaster. Dev Biol 65:296–321

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Correspondence to Lennart G. Ohlsson.

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Ohlsson, L.G., Nässel, D.R. Postembryonic development of serotonin-immunoreactive neurons in the central nervous system of the blowfly, Calliphora erythrocephala . Cell Tissue Res. 249, 669–679 (1987). https://doi.org/10.1007/BF00217339

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Key words

  • Serotonin (5-HT)
  • Optic lobes
  • Insect CNS
  • Postembryonic development
  • Blowly, Calliphora erythrocephala