Skip to main content
SpringerLink
Log in

Serotonin-immunoreactive brain interneurons persist during metamorphosis of an insect: a developmental study of the brain of Tenebrio molitor L. (Coleoptera)

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

Serotonin-immunoreactive neurons in the brain of Tenebrio molitor L. have been demonstrated and mapped throughout metamorphosis. Most serotonin-immunoreactive brain neurons persist throughout metamorphosis; their fate can be followed during development because of their characteristic cell body locations and arborization patterns. The detailed morphology of the persisting neurons, however, changes during metamorphosis, probably to accommodate architectural changes of the different brain centers. Serotonin-immunoreactivity in the optic lobes allows a subset of neurons that is newly differentiated during metamorphosis to be identified. Phylogenetic homology of serotonin-immunoreactive brain interneurons of different insect species is discussed. The serotonin-immunoreactive brain neurons comprise a phylogenetically conserved neuronal population. Serial homologous abdomino-thoracic and brain serotonin-immunoreactive neurons were characterized, allowing a comparison of some basic structural features of these neurons.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Balling A, Technau GM, Heisenberg M (1987) Are the structural changes in adult Drosophila mushroom bodies memory traces? Studies on biochemical learning mutants. J Neurogenet 4:65–73

    Google Scholar 

  • Bishop CA, O'Shea M (1983) Serotonin immunoreactive neurons in the central nervous system of an insect (Periplaneta americana). J Neurobiol 14:251–269

    Google Scholar 

  • Breidbach O (1987a) The fate of persisting thoracic neurons during metamorphosis of the meal beetle, Tenebrio molitor (Insecta, Coloeptera). Roux's Arch Dev Biol 196:93–100

    Google Scholar 

  • Breidbach O (1987b) Constancy and variation of the serotonin-like immunoreactive neurons in the metamorphosing ventral nerve cord of the meal beetle, Tenebrio molitor L. (Coleoptera, Tenebrionidae). Int J Insect Morphol Embryol 16:17–26

    Google Scholar 

  • Breidbach O (1987c) Constancy of ascending projections in the metamorphosing brain of the meal-beetle Tenebrio molitor L. (Insecta, Coloeptera). Roux's Arch Dev Biol 196:450–459

    Google Scholar 

  • Breidbach O (1987d) Absence of sensory input does not affect persistent neurons in Tenebrio molitor metamorphosis (Insecta, Coloeptera). Roux's Arch Dev Biol 196:486–491

    Google Scholar 

  • Breidbach O (1988) Reorganization of identified neurons during the metamorphosis of the meal beetle—aspects for an analysis of neuronal regeneration. Monogr Dev Biol 21:105–111

    Google Scholar 

  • Breidbach O (1989) Fate of descending interneurons in the metamorphosing brain of an insect, the beetle Tenebrio molitor L. J Comp Neurol (in press)

  • Breidbach O, Dircksen H (1989) Proctolin-immunoreactive neurons persist during metamorphosis of an insect: a developmental study of the ventral nerve cord of Tenebrio molitor L. (Coleoptera). Cell Tissue Res 257:217–225

    Google Scholar 

  • 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

    Google Scholar 

  • 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 250:449–459

    Google Scholar 

  • Davis NT (1985) Serotonin-immunoreactive visceral nerves and neurohemal system in the cockroach Periplaneta americana (L.). Cell Tissue Res 240:593–600

    Google Scholar 

  • Davis NT (1987) Neurosecretory neurons and their projections to the serotonin neurohemal system of the cockroach Periplaneta americana (L.), and identification of mandibular and maxillary motor neurons associated with this system. J Comp Neurol 259:604–621

    Google Scholar 

  • Elekes K, Hustert R, Geffard M (1987) Serotonin-immunoreactive and dopamine-immunoreactive neurons in the terminal ganglia of the cricket. Acheta domestica: light- and electron-microscopic immunocytochemistry. Cell Tissue Res 250:167–180

    Google Scholar 

  • Granger NA, Homberg U, Henderson P, Towle A, Lauder JM (1989) Serotonin-immunoreactive neurons in the brain of Manduca sexta during larval development and larval-pupal metamorphosis. Int J Dev Neurosci 7:55–72

    Google Scholar 

  • 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 behaviour. Plenum Press, New York, pp 124–148

    Google Scholar 

  • Homberg U, Hildebrand JG (1989) Serotonin-immunoreactive neurons in the median protocerebrum and suboesophageal ganglion of the sphinx moth Manduca sexta. Cell Tissue Res 258:1–24

    Google Scholar 

  • Hustert R, Topel U (1986) Localisation and major postembryonic changes of identified 5HT-immunoreactive neurones in the terminal ganglion of a cricket (Acheta domesticus). Cell Tissue Res 245:615–621

    Google Scholar 

  • Kent KS, Levine RB (1988) Neural control of leg movements in a metamorphic insect: persistence of larval leg motor neurons to innervate the adult legs of Manduca sexta. J Comp Neurol 276:30–43

    Google Scholar 

  • Kent KS, Hoskins SG, Hildebrand JG (1987) A novel serotoninimmunoreactive neuron in the antennal lobe of the sphinx moth Manduca sexta persists throughout postembryonic life. J Neurobiol 18:451–465

    Google Scholar 

  • Klemm N, Sundler F (1983) Organization of catecholamine and serotonin-immunoreactive neurons in the corpora pedunculata of the desert locust, Schistoceraca gregaria Forsk. Neurosci Lett 36:13–17

    Google Scholar 

  • Klemm N, Steinbusch HWM, Sundler F (1984) Serotonin-immunoreactive neurons and their projections in the brain of the cockroach, Periplaneta americana. J Comp Neurol 225:387–395

    Google Scholar 

  • Klemm N, Hustert R, Cantera R, Nässel DR (1986) Neurons reactive to antibodies against serotonin in the stomatogastric nervous system and in the alimentary canal of locusts and crickets (Orthoptera, Insecta). Neuroscience 17:247–261

    Google Scholar 

  • Konings PNM, Vullings HGB, Siebinga R, Diederen JHB, Jansen WF (1988) Serotonin-immunoreactive neurones in the brain of Locusta migratoria innervating the corpus cardiacum. Cell Tissue Res 254:147–153

    Google Scholar 

  • Lange AB, Orchard I, Lloyd RJ (1988) Immunohistochemical and electrochemical detection of serotonin in the nervous system of the blood-feeding bug, Rhodnius prolixus. Arch Insect Biochem Physiol 8:187–201

    Google Scholar 

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

    Google Scholar 

  • Levine RB (1986) Reorganization of the insect nervous system during metamorphosis. Trends Neurosci 6:315–319

    Google Scholar 

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

    Google Scholar 

  • Longley AJ, Longley RD (1986) Serotonin immunoreactivity in the nervous system of the dragonfly nymph. J Neurobiol 17:329–338

    Google Scholar 

  • Meinertzhagen IA (1984) The rules of synaptic assembly in the developing insect lamina. In: Ali MA (ed) Photoreception and vision in invertebrates. Plenum, New York, pp 635–660

    Google Scholar 

  • Nässel DR (1987) Serotonin and serotonin-immunoreactive neurons in the nervous system of insects. Prog Neurobiol 30:1–85

    Google Scholar 

  • Nässel DR, Cantera R (1985) Mapping of serotonin-immunoreactive neurons in the larval nervous system of the flies Calliphora erythrocephala and Sarcophaga bullata. Cell Tissue Res 239:423–434

    Google Scholar 

  • Nässel DR, Elekes K (1985) Serotinergic terminals in the neural sheath of the blowfly nervous system: electron microscopical immunocytochemistry and 5,7-dihydroxytryptamine labelling. Neuroscience 15:293–307

    Google Scholar 

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

    Google Scholar 

  • 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

    Google Scholar 

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

    Google Scholar 

  • Nordlander RH, Edwards JS (1968) Morphology of the larval and adult brains of monarch butterfly, Danaus plexippus plexippus L. J Morphol 126:67–94

    Google Scholar 

  • Nordlander RH, Edwards JS (1969a) Postembryonic brain development in the monarch butterfly Danaus plexippus plexippus L. I. Cellular events during brain morphogenesis. Wilhelm Roux Arch Entwicklungsmech Org 162:197–217

    Google Scholar 

  • Nordlander RH, Edwards JS (1969b) Postembryonic brain development in the monarch buterfly Danaus pelxippus plexippus L. II. The optic lobes. Wilhelm Roux Arch Entwicklungsmech Org 163:197–220

    Google Scholar 

  • Nordlander RH, Edwards JS (1970) Postembryonic brain development in the monarch buterfly Danaus plexippus plexippus L. III. Morphogenesis of centers others than the optic lobes. Wilhelm Roux Arch Entwicklungsmech Org 164:247–260

    Google Scholar 

  • Pipa RL (1978) Patterns of neural reorganization during the postembryonic development of insects. Int Rev Cytol 7:403–438

    Google Scholar 

  • Rehder V, Bicker G, Hammer M (1987) Serotonin-immunoreactive neurons in the antennal lobes and suboesophageal ganglion of the honeybee. Cell Tissue Res 247:59–66

    Google Scholar 

  • Schürmann FW, Klemm N (1984) Serotonin-immunoreactive neurons in the brain of the honeybee. J Comp Neurol 225:570–580

    Google Scholar 

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

    Google Scholar 

  • Taghert PH, Goodman CS (1984) Cell determination and differentiation of identified serotonin-immunoreactive neurons in the grasshopper embryo. J Neurosci 4:989–1000

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Truman JW, Levine RB (1983) Cellular events in the nervous system during metamorphosis in the moth Manduca sexta. In: Barker JL (ed) Current methods in cellular neurobiology. Plenum, New York, pp 16–48

    Google Scholar 

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

    Google Scholar 

  • Tyrer NM, turner JD, Altman JS (1984) Identifiable neurons in the locust central nervous system that react with antibodies to serotonin. J Comp Neurol 227:313–330

    Google Scholar 

  • Vallés AM, White K (1986) Development of serotonin-containing neurons in Drosophila mutants unable to synthesize serotonin. J Neurosci 6:1482–1491

    Google Scholar 

  • Vallés AM, White K (1988) Serotonin-containing neurons in Drosophila melanogaster: development and distribution. J Comp Neurol 268:414–428

    Google Scholar 

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

    Google Scholar 

  • White K, Vallés AM (1983) Immunohistochemical and genetic studies of serotonin and neuropeptides in Drosophila. In: Edelmann GM (ed) Molecular basis of neural development. Wiley, New York, pp 547–564

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institut für Angewandte Zoologie der Universität Bonn, Bonn, Federal Republic of Germany

    Olaf Breidbach

Authors
  1. Olaf Breidbach
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Breidbach, O. Serotonin-immunoreactive brain interneurons persist during metamorphosis of an insect: a developmental study of the brain of Tenebrio molitor L. (Coleoptera). Cell Tissue Res 259, 345–360 (1990). https://doi.org/10.1007/BF00318458

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00318458

Key words

Search

Navigation