Summary
Neurons immunoreactive with antibodies to serotonin (5-HT) were mapped in the thoracico-abdominal ganglia of the blowfly, Calliphora erythrocephala, during postembryonic development. Reconstructions from serial sections of tissue processed with a preincubation PAP-method permitted a detailed analysis of the morphological changes occurring in 5-HT-immunoreactive (5-HTi) neurons.
All the 5-HTi cell bodies in the thoracico-abdominal ganglia of the 3rd instar larva, except two in the metathoracic ganglion, retain their immunochemical phenotype throughout pupal development. Hence, all the adult 5-HTi neurons in these ganglia differentiate during embryonic development. The finer processes of the larval 5-HTi neurons undergo a substantial regression during the first 24 h of pupal development, and thereafter new branches form on the primary processes of the same cell bodies. The slight change in relative position of 5-HTi cell bodies and the reorganization of the neuropil into an adult pattern occur during the first half of pupal development. The neuropil mass and extent of 5-HTi processes continue to increase during the following days and appear to be fully developed two days (80% of pupal development) before hatching.
On the basis of the presented data, some of the basic processes are discussed that lead to the transformation of the larval nervous system into its adult form.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bate CM (1976) Embryogenesis of an insect nervous system. I. A map of the thoracic and abdominal in Locusta migratoria. J Embryol Exp Morphol 35:107–123
Bate CM, Goodman CS, Spitzer NC (1981) Embryonic development of identified neurons: segment-specific differences in the H cell homologues. J Neurosci 1:103–106
Bishop CA, O'Shea M (1982) Neuropeptide proctolin (H-Arg-Tyr-Leu-Pro-Thr-OH): immunocytochemical mapping of neurons in the central nervous system of the cockroach. J Comp Neurol 207:223–238
Duve H, Thorpe A (1981) Gastrin/cholecystokinin (CCK)-like immunoreactive neurones in the brain of the blowfly, Calliphora erythrocephala (Diptera). Gen Comp Endocrinol 43:381–391
Duve H, Thorpe A (1984) Immunocytochemical mapping of gastrin/CCK-like peptides in the neuroendocrine system of the blowfly Calliphora erythrocephala (Diptera). Cell Tissue Res 237:309–320
Copenhaver PF, Truman JW (1986) Metamorphosis of the cerebral neuroendocrine system in the moth Manduca sexta. J Comp Neurol 249:186–204
Edwards J (1969) Postembryonic development and regeneration of the insect nervous system. Adv Insect Physiol 6:97–137
Ekström P, Nyberg L, Van Veen T (1985) Ontogenetic development of serotonergic neurons in the brain of a teleost, the threespined stickleback. An immunohistochemical analysis. Dev Brain Res 17:209–224
Goodman CS, Bate M, Spitzer NC (1981) Embryonic development of identified neurons: Origin and transformation of the H cell. J Neurosci 1:94–102
Heinertz R (1976) Untersuchungen am thorakalen Nervensystem von Antheraea polyphemus (Lepidoptera) unter besonderer Berücksichtigung der Metamorphose. Rev Suisse Zool 83:216–242
Hustert R, Topel U (1986) Location and major postembryonic changes of identified 5-HT-immunoreactive neurons in the terminal ganglion of a cricket Acheta domesticus. Cell Tissue Res 245:615–621
Keshishian H, O'Shea M (1985) The distribution of a peptide neurotransmitter in the postembryonic grasshopper central nervous system. J Neurosci 5(4):992–1004
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 locust and crickets (Orthoptera, Insecta). Neuroscience 1(1):247–261
Eevine R (1984) Changes in neuronal circuits during insect metamorphosis J Exp Biol 112:27–44
Eevine R, Truman JW (1982) Metamorphosis of the insect nervous system: changes in morphology and synaptic interactions of identified neurones. Nature 299:250–252
Eevine R, Truman JW (1985) Fate of abdominal motorneurons during metamorphosis of the moth. Maduca sexta. J Neurosci 5:2424–2431
Levine R (1986) Reorganization of the insect nervous system during metamorphosis. Trends Neurosci 9(7):315–319
Myers CM, Evans PD (1985a) An FMRFamide antiserum differentiates between populations of antigens in the ventral nervous system of the locust, Schistocerca gregaria. Cell Tissue Tes 242:109–114
Myers CM, Evans PD (1985b) The distribution of bovine pancreatic polypeptide FMRFamide-like immunoreactivity in the ventral nervous system of the locust. J Comp Neurol 234:1–16
Nässel DR (1986a) Serotonin and scrotonin-immunoreactive neurons in the nervous system of insects. Progr Neurobiol (in press)
Nässel DR (1986b) Neuroactive substances in the insect CNS. In: Ali MA (ed): Invertebrate nervous systems. Plenum Press, New York (in press)
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
Nässel DR, Elekes K (1985) Serotonergic terminals in the neural sheath of the blowfly nervous system: ultrastructural immunocytochemicstry and 5,7-dihydroxytryptamine labelling. Neuroscience 15:293–307
Nässel DR, Klemm N (1983) Serotonin-like immunoreactivity in the optic lobes of three insect species. Cell Tissue Res 232:129–140
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
Nässel DR, Ohlsson EG, Sivasubramanian P (1986) Differentiation of serotonin-immunoreactive neurons in fly optic lobes developing in situ or cultured in vivo without eye discs. J Comp Neurol (in press)
Nordlander RM, 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
Ohlsson EG, Nässel DR (1987) Postembryonic development of serotonin-immunoreactive neurons in the central nervous system of the blowfly. I. The optic lobes. Cell Tissue Res (in press)
Power ME (1952) A quantitative study of the growth of the central nervous system of a holometabolous insect, Drosophila melanogaster. J Morphol 91:389–411
Sivasubramanian P, Biagi M (1983) Morphology of the pupal stages of the fleshfly, Sacrophaga bullata. Int J Insect Morphol Embryol 12 (5/6):355–359
Taghert PH, Goodman CS (1984) Cell determination and differentiation of identified serotonin-immunoreactive neurons in the grasshopper embryo. J Neurosci 4:989–1000
Taylor HM, Truman JW (1974) Metamorphosis of the abdominal ganglia of the tobacco hornworm, Manduca sexta. J Comp Physiol 90:367–388
Technau G, Heisenberg M (1982) Neural reorganization during metamorphosis of the corpora pedunculata in Drosophila melanogaster. Nature 295:405–406
Trimmer BA (1985) Serotonin and the control of salivation in the blowfly Calliphora. J Exp Biol 114:307–328
Truman JW (1984) Cell death in invertebrate nervous systems. Ann Rev Neurosci 7:171–188
Truman JW, Reiss S (1976) Dendritic reorganization of an identified motoneuron during metamorphosis of the tobacco hornworm moth. Science 192:477–479
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
Valles AM, White K (1986) Development of serotonin-containing neurons in Drosophila mutants unable to synthesize serotonin. J Neurosci 6(5):1482–1491
White K, Kankel D (1978) Patterns of cell division and cell movement in the formation of the imaginai nervous system in Drosophila melanogaster. Dev Biol 65:296–321
White K, Hurteau T, Punsal P (1986) Neuropeptide-FMRFamidelike immunoreactivity in Drosophila: development and distribution. J Comp Neurol 247:430–438
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Cantera, R., Nässel, D.R. Postembryonic development of serotonin-immunoreactive neurons in the central nervous system of the blowfly. Cell Tissue Res. 250, 449–459 (1987). https://doi.org/10.1007/BF00219091
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00219091