Abstract
The effects of the widely used neurotoxic pyrethroid insecticides on neuronal development or plasticity are unclear. To expand knowledge about the influence of the pyrethroid fenvalerate on neuronal development, metamorphic remodelling of the primary olfactory neuropil of the beetle Tenebrio molitor has been studied. The antennal lobe is subdivided into distinct glomeruli before metamorphosis. This is in contrast to that which occurs in other well-studied holometabolous insects such as the moth Manduca sexta and the honeybee. As an indicator of antennal lobe interneurons, locusta-tachykinin immunoreactive neurons have been used. They project into the antennal lobes and form tufted arbors in larval and adult stages within glomeruli throughout the neuropil. These glomerular structures are invaded by glomerular sensory afferent axons and are surrounded by processes of glia cells. With pupation, the glomerulization is lost and no locusta-tachykinin or substance P immunoreactivity is visible in the antennal lobe. The immunoreactivity reappears during metamorphosis, starting with diffusely branched arbors that later become tufted. Application of the neurotoxic insecticide fenvalerate at pupation in sublethal concentrations resulted in a loss or reduction of glomerular pattern formation by neurons and glia cells during metamorphosis. Labelling of antennal sensory axons revealed that the olfactory neuropil was not deafferented, and also that the sensory axons were not organized into a normal glomerular pattern. In addition to the morphological differences, fenvalerate treatment caused locusta-tachykinin immunoreactivity to reappear prematurely during metamorphosis. Possible reasons for fenvalerate-induced alterations in antennal lobe development and their implications for normal development are discussed.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
Similar content being viewed by others
References
Aldridge, W. N. (199o) An assessment of the toxicological properties of pyrethroids and their neurotoxicity. Crit. Rev. Toxicol. 21: 89–104
Baumann, P.M., Oland, L.A., Tolbert, L.P. (1996) Glial cells stabilize axonal protoglomeruli in the developing olfactory lobe of the moth Manduca sexta. J. Comp. Neurol. 373: 118–128
Becker, M., Breidbach, O. (1993) Distribution of GABA-like immunoreactivity throughout metamorphosis of the supraoesophageal ganglion of the beetle Tenebrio molitor L. (Coleoptera, Tenebrinoidae). In: Elsner, N., Heisenberg, M. (eds)Proc. Gött. Neurobiol. Conf Thieme, Stuttgart, p. 738
Breidbach, O., Marx, J.M. (1990) Antennale sensorische Projektionen im Zentralnervensystem der Larve des Mehlkäfers Tenebrio molitor L. (Insecta, Coleoptera). Z. Ang. Zool. 77: 291–310
Breidbach, O., Wegerhoff, R. (1994) FMRFamide-like immunoreactive neurons in the brain of the beetle, Tenebrio molitor L. 1758 (Coleoptera: Tenebrinoidae): constancies and variations in development from embryo to the adult. Int. J. Insect Morphol. Embryol. 23: 383–404
Breidbach, O., Dennis, R., Marx, J., Görlach, C., Wiegand, H., Wegerhoff, R. (1992) Insect glial cells show differential expression of a glycolipid-derived, glucuronic acid-containing epitope throughout neurogenesis: detection during postembyogenesis and regeneration in the central nervous system of Tenebrio molitor L. Neurosci. Lett. 147: 5–8
Brown, L.D., Narahashi, T. (1992) Modulation of nerve membrane sodium channel activation by deltamethrin. Brain Res. 584: 71–76
Eriksson, P., Fredriksson, A. (1991) Neurotoxic effects of two different pyrethroids. Bioallethrin and Deltamethrin, on immature and adult mice: changes in behavioural and muscarinic receptor variables. Toxicol. Appl. Pharmacol. 108: 78–85
Eriksson, P., Nordberg, A. (199o) Effects of two pyrethroids, bioallethrin and deltamethrin, on subpopulations muscarinic and nicotinic receptors in the mouse brain. Toxicol. Appl. Pharmacol. 102: 446–463
Hähnlein, I., Bicker, G. (1996) Morphology of neuroglia in the antennal lobes and mushroom bodies of the brain of the honeybee. J. Comp. Neurol. 367: 235–245
Hähnlein, I., Härtig, W., Bicker, G. (1996) Datura stramonium lectin staining of glial associated extracellular material in insect brains. J. Comp. Neurol. 376: 175–187
Hartzell, A., Scudder, H. I. (1942) Histological effects of pyrethrum and an activator on the central nervous system of the housefly. J. Econ. Entomol. 35: 428–433
Hassouna, I., Wickert, H., El-Elaimy, I., Zimmermann, M., Herdegen, T. (1996) Systemic application of pyrethroid insecticides evokes differential expression of c-Fos and c-Jun proteins in rat brain. Neurot. Toxicol. 17: 415–432
Hemming, H., Flodstrom, S., Warngard, L. (1993) Enhancement of altered hepatic foci in rat liver and inhibition of intercellular communication in vitro by the pyrethroid insecticides fenvalerate, flucythrinate and cypermethrin. Carcinogenesis 14: 2531–2535
Hildebrand, J.G. (1985) Metamorphosis of the insect nervous system: influence of the periphery on the postembryonic development of the antennal sensory pathway in the brain of Manduca sexta. In: Selverstone, A.I. (ed)Model neuronal networks and behaviour. Plenum, New York, pp. 124–148
Kutsch, W., Schneider, H. (1987) Histological characterization of neurons innervating functionally different muscles of Locusta. J. Comp. Neurol. 261: 515–528
Levine, R.B. (1984) Changes in neuronal circuits during insect metamorphosis. J. Exp. Biot. 112: 27–44
Malun, D., Oland, L.A., Tolbert, L.P. (1994) Uniglomerular projection neurons participate in early developmet of olfactory glomeruli in the moth Manduca sexta. J. Comp. Neuro1. 350: 1–22
Muren, J.E., Lundquist, C.T., Nässel, D.R. (1995) Abundant distribution of locustatachykinin-like peptide in the nervous system and intestine of the cockroach Leucophaea maderae. Philos. Trans. R. Soc. Lond. [Biol]. 348: 423-444
Narahashi, T. (1996a) Toxins that modulate the sodium channel gating mechanism. Ann. N. Y. Acad. Sci. 479: 133–151
Narahashi, T. (1996b) Transmitter-activated ion channels as the target of chemical agents. Adv. Exp. Med. Biot. 287: 61–73
Nässel, D.R. (1993) Neuropeptides in the insect brain: a review. Cell Tissue Res. 273: 1–29
Naumann, K. (199o) Synthetic pyrethroid insecticides. In:Structure and properties. Springer, Berlin Heidelberg New York
Nordlander, R.H., Edwards, J.S. (1970) Postembryonic brain development in the monarch butterfly, Danaus plexippus plexippus L. III. Morphogenesis of centers other than the optic lobes. Wilhelm Roux. Arch. 164: 247–260
Oland, L.A., Tolbert, L.P. (1987) Glial patterns during early development of antennal lobes of Manduca sexta: a comparison between normal lobes and lobes of deprived of antennal axons. J. Comp. Neurol. 255: 196–207
Oland, L.A., Tolbert, L.P. (1996) Multiple factors shape development of olfactory glomeruli: insights from an insect model system. J. Neurobiol. 30: 92–109
Oland, L.A., Pott, W.M., Bukhman, G., Sun, X.J., Tolbert, L. P. (1996) Activity blockade does not prevent the construction of olfactory glomeruli in the moth Manduca sexta. Int. J. Deli. Neurosci. 14: 983–996
Rodrigues, V., Pinto, L. (1988) The antennal glomerulus as a functional unit of odor coding in Drosophila melanogaster. In: Singh, R.N., Strausfeld, N.J. (eds) Neurobiology of sensory systems. Plenum, New York, pp. 387–396
Salecker, I., Boeckh, J. (1995) Embryonic development of the antennal lobes of a hemimetabolous insect, the cockroach Periplaneta americana: light and electron microscopic observations. J. Comp. Neurol. 352: 33-54
Salecker, I., Boeckh, J. (1996) Influence of receptor axons on the formation of olfactory glomeruli in a hemimetabolous insect, the cockroach Periplaneta americana. J. Comp. Neurol. 370: 262–279
Sanes, J.R., Prescott, D.J., Hildebrand, J.G. (1977) Cholinergic neurochemical development of normal and deafferented antennal lobes during metamorphosis of the moth Manduca sexta. Brain Res. 119: 389–402
Schatz, C.J. (1990) Impulse activity and the patterning of connections during CNS development. Neuron 5: 745–756
Schatz, C.J. (1995) Brain waves and brain wiring. In: Elsner, N., Menzel, R. (eds) Gött. Neurobiol. Rep. Thieme, Stuttgart, pp. 159–187
Sheets, L.P., Doherty, J.D., Law, M.W., Reiter, L.W., Crofton, K.M. (1994) Age-dependent differences in the susceptibility of rats to deltamethrin. Toxicol. Appl. Pharmacol. 126: 186–190
Tateno, C., Ito, S., Tanaka, M.,Yoshitake, A. (1993) Effects of pyrethroid insecticides on gap junctional intercellular communications in Balb/c3T3 cells by dye-transfer assay. Cell Biol. Toxiol. 9: 215–221
Technau, G. M., Heisenberg, M. (1982) Neuronal reorganization during metamorphosis of the corpora pedunculata inDrosophila melanogaster. Nature 295: 405–407
Veenstra, J.A., Lau, G.W., Agricola, H.J., Petzel, D.H. (1995) Immunohistochemical localization of regulatory peptides in the midgut of the female mosquito Aedes aegypti. Histochem. Cell Bio!. 104: 337-347
Vijverberg, H.P.M., Van den Berken, J. (1990) Neurotoxicological effects and the mode of action of pyrethroid insecticides. Crit. Rev. Toxicol. 21: 105–126
Wegerhoff, R. (1996) Pyrethroide: Unbedenkliche Insektizide?. PHi 3: 94–97
Wegerhoff, R., Breidbach, O. (1991) Distribution of GABA like immunoreactivity throughout postembryogenesis of the midbrain in the beetle Tenebrio molitor L. (Insecta, Coleoptera). In: Elsner, N., Penzlin, H. (eds) Proc. Gött. Neurobiol. Conf. Thieme, Stuttgart, p. 511
Wegerhoff, R., Breidbach, O. (1992) Structure and development of the larval central complex in a holometabolous insect, the beetle Tenebrio molitor. Cell Tissue Res. 268: 341–358
Wegerhoff, R., Breidbach, 0., Lobemeier, M. (1996a) Tachykinin and FMRFamide like immunopositive neurons in the developing central complex of the beetle Tenebrio molitor. In: Krisch, B., Mentlein, R.(eds) The peptidergic neuron. Birkhäuser, Basel, pp. 205–211
Wegerhoff, R., Breidbach, O., Lobemeier, M. (1996b) Development of Locustatachykinin immunopositive neurons in the central complex of the beetle Tenebrio molitor. J. Comp. Neurol. 375: 157–166
Author information
Authors and Affiliations
Rights and permissions
Copyright information
© 1998 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Wegerhoff, R. (1998). Metamorphic development of locusta-tachykinin immunoreactive neurons of the antennal lobes of the beetle Tenebrio molitor and the effect of fenvalerate application. In: EBO — Experimental Biology Online Annual 1996/97. EBO — Experimental Biology Online Annual, vol 1996/1997. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-662-00932-1_24
Download citation
DOI: https://doi.org/10.1007/978-3-662-00932-1_24
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-662-00934-5
Online ISBN: 978-3-662-00932-1
eBook Packages: Springer Book Archive