Advertisement

Acta Biologica Hungarica

, Volume 55, Issue 1–4, pp 3–12 | Cite as

Neuromodulatory Octopaminergic Neurons and Their Functions During Insect Motor Behaviour

The Ernst Florey Memory Lecture
  • H.-J. PflüGerEmail author
  • C. Duch
  • E. Heidel
Article

Abstract

In this article we describe recent advances in functional studies on the role of octopamine released in the periphery by efferent dorsal or ventral unpaired median neurons. In addition to the previously described modulatory effects on the neuromuscular junction, we describe a metabolic regulatory role for these neurons. Due to their activity glycolytic rates in target tissues, such as muscles, are increased. In flight muscles that use carbohydrate catabolism only at take-off but have to switch to lipid oxidation during prolonged flight, these neurons are only active at rest but are inhibited as soon as flight motor patterns are selected.

Keywords

Locusts unpaired median neurons flight signalling pathways metabolism 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Ballantyne, D., Rathmayer, W. (1981) On the function of the common inhibitory neurone in the walking legs of the crab, Eriphia spinifrons. J. Comp. Physiol. A 145, 111–122.CrossRefGoogle Scholar
  2. 2.
    Baudoux, S., Burrows, M. (1998) Synaptic activation of efferent neuromodulatory neurones in the locust Schistocerca gregaria. J. Exp. Biol. 201, 3339–3354.PubMedPubMedCentralGoogle Scholar
  3. 3.
    Baudoux, S., Duch, C., Morris, O. T. (1998) Coupling of efferent neuromodulatory neurons to rhythmical leg motor activity in the locust. J. Neurophysiol. 79, 361–370.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Bazemore, A., Elliott, K. A. C., Florey, E. (1956) Factor I and gamma-aminobutyric acid. Nature 178, 1052–1053.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Blau, C., Wegener, G. (1994) Metabolic integration in locust flight: The effect of octopamine on fructose 2,6-bisphosphate content of flight muscle in vivo. J. Comp. Physiol. [B] 164, 11–15.CrossRefGoogle Scholar
  6. 6.
    Bräunig, P. (1991) Suboesophageal DUM neurones innervate the principal neuropiles of the locust brain. Philos. Trans. R. Soc. Lond. [B] 322, 221–240.Google Scholar
  7. 7.
    Bräunig, P. (2003) The morphology of descending dorsal unpaired median (DUM) neurons of the locust suboesophageal ganglion. In: Elsner, N., Zimmermann, H. (eds), Proc. 29th Göttingen Neurobiology Conference. Thieme, Stuttgart, 726 (Nr. 678).Google Scholar
  8. 8.
    Bräunig, P., Eder, M. (1998) Locust dorsal unpaired median (DUM) neurones directly innervate and modulate hindleg proprioceptors. J. Exp. Biol. 201, 3333–3338.Google Scholar
  9. 9.
    Bräunig P., Pflüger, H.-J. (2001) The unpaired median neurons of insects. Adv. Insect Physiol. 28, 185–266.CrossRefGoogle Scholar
  10. 10.
    Bräunig, P., Stevenson, P. A., Evans, P. D. (1994) A locust octopamine immunoreactive dorsal unpaired median neurone forming terminal networks on sympathetic nerves. J. Exp. Biol. 192, 225–238.Google Scholar
  11. 11.
    Burrows, M. (1996) The neurobiology of an insect brain. Oxford University Press. Oxford.CrossRefGoogle Scholar
  12. 12.
    Burrows, M., Pflüger, H.-J. (1995) Action of locust neuromodulatory neurons is coupled to specific motor patterns. J. Neurophysiol. 74, 347–357.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Condron, B. G., Zinn, K. (1994) The grasshopper median neuroblast is a multipotent progenitor cell that generates glia and neurons in distinct temporal phases. J. Neurosci. 14, 5766–5777.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Duch, C., Pflüger, H. J. (1999) DUM neurons in locust flight: a model system for amine-mediated peripheral adjustments to the requirements of a central motor program. J. Comp. Physiol. [A] 184, 489–499.CrossRefGoogle Scholar
  15. 15.
    Duch, C., Mentel, T., Pflüger, H. J. (1999) Distribution and activation of different types of octopaminergic DUM neurons in the locust. J. Comp. Neurol. 403, 119–134.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Eckert, M., Rapus, J., Nürnberger, A., Penzlin, H. (1992) A new specific antibody reveals octopamine-like immunoreactivity in cockroach ventral nerve cord. J. Comp. Neurol. 322, 1–15.Google Scholar
  17. 17.
    Evans, P. D., O’Shea, M. (1977) An octopaminergic neurone modulates neuromuscular transmission in the locust. Nature 270, 257–259.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Evans, P. D., O’Shea, M. (1978) The identification of an octopaminergic neurone and the modulation of a myogenic rhythm in the locust. J. Exp. Biol. 73, 235–260.Google Scholar
  19. 19.
    Florey, E. (1967) Neurotransmitters and modulators in the animal kingdom. Fed. Proc. 26, 1164–1178.PubMedPubMedCentralGoogle Scholar
  20. 20.
    Heidel, E., Pflüger, H.-J. (2003) Transient potassium currents in identified subtypes of octopaminergic dorsal unpaired median (DUM-) neurons isolated from locust thoracic ganglia. In: Elsner, N., Zimmermann, H. (eds) Proc. 29th Göttingen Neurobiology Conference. Thieme, Stuttgart, p. 212 (Nr. 97).Google Scholar
  21. 21.
    Hoyle, G. (1974) A function for neurons (DUM) neurosecretory on skeletal muscle of insects. J. Exp. Zool. 189, 401–406.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Hoyle, G. (1978) The dorsal, unpaired, median neurones of the locust metathoracic ganglion. J. Neurobiol. 9, 43–57.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Hoyle, G. (1985) Generation of motor activity and control of behavior: the roles of neuromodulator octopamine, and the orchestration hypothesis. In: Kerkut, G. A., Gilbert, L. I. (eds) Comprehensive Insect Physiology, Biochemistry and Pharmacology, Vol. 5. Pergamon Press, Oxford, pp. 607–621.Google Scholar
  24. 24.
    Johnston, R. M., Consoulas, C., Pflüger, H.-J., Levine, R. B. (1999) Patterned activation of unpaired median neurons during fictive crawling in Manduca sexta larvae. J. Exp. Biol. 202, 103–113.PubMedPubMedCentralGoogle Scholar
  25. 25.
    Konings, P. N. M., Vullings, H. G. B., Geffard, M., Buijs, R. M., Diederen, J. H. B., Jansen, W. F. (1988) Immunocytochemical demonstration of octopamine-immunoreactive cells in the nervous system of Locusta migratoria and Schistocerca gregaria. Cell Tissue Res. 251, 371–379.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Mentel, T., Duch, C., Stypa, H., Müller, U., Wegener, G., Pflüger, H.-J. (2003) Central modulatory neurons control fuel selection in flight muscle of migratory locust. J. Neurosci. 23, 1109–1113.CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Morris, O. T., Duch, C., Stevenson, P. A. (2000) Differential activation of octopaminergic (DUM) neurones via proprioceptors responding to flight muscle contractions in the locust. J. Exp. Biol. 203, 3555–3564.Google Scholar
  28. 28.
    O’Shea, M., Evans, P. D. (1979) Potentiation of neuromuscular transmission by an octopaminergic neurone in the locust. J. Exp. Biol. 79, 169–190.Google Scholar
  29. 29.
    Ramirez, J. M., Orchard, I. (1990) Octopaminergic modulation of the forewing stretch receptor in the locust Locusta migratoria. J. Exp. Biol. 149, 255–279.Google Scholar
  30. 30.
    Ramirez, J.-M., Pearson, K. G. (1991) Octopaminergic modulation of interneurons in the flight system of the locust. J. Neurophysiol. 66, 1522–1537.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Rathmayer, W. (1978) Venoms of Sphecidae, Pompilidae, Mutilidae and Bethylidae. In: Bettini, P. (ed.) Handbook of Experimental Pharmacology, Vol. 48. Arthropod venoms. Springer, Heidelberg, pp. 661–6Google Scholar
  32. 32.
    Roeder, T. (1999) Octopamine in invertebrates. Prog. Neurobiol. 59, 533–561.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Sinakevitch, I. G., Geffard, M., Pelhate, M., Lapied, B. (1994) Octopamine-like immunoreactivity in the dorsal unpaired median (DUM) neurons innervating the accessory gland of the male cockroach Periplaneta americana. Cell Tissue Res. 276, 15–21.CrossRefGoogle Scholar
  34. 34.
    Sinakevitch, I. G., Geffard, M., Pelhate, M., Lapied, B. (1995) Octopaminergic dorsal unpaired median (DUM) neurones innervating the colleterial glands of the female cockroach Periplaneta americana. J. Exp. Biol. 198, 1539–1544.PubMedPubMedCentralGoogle Scholar
  35. 35.
    Sinakevitch, I. G., Geffard, M., Pelhate, M., Lapied, B. (1996) Anatomy and targets of dorsal unpaired median neurones in the terminal abdominal ganglion of the male cockroach Periplaneta americana L. J. Comp. Neurol. 367, 147–163.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Sombati, S., Hoyle, G. (1984) Generation of specific behaviors in a locust by local release into neuropil of the natural neuromodulator octopamine. J. Neurobiol. 15, 481–506.CrossRefGoogle Scholar
  37. 37.
    Stern, M., Thompson, K. S. J., Zhou, P., Watson, D. G., Midgley, J. M., Gewecke, M., Bacon, J. P. (1995) Octopaminergic neurons in the locust brain: Morphological, biochemical and electrophysiological characterisation of potential modulators of the visual system. J. Comp. Physiol. A 177, 611–625.CrossRefGoogle Scholar
  38. 38.
    Stevenson, P. A., Kutsch, W. (1988) Demonstration of functional connectivity of the flight motor system in all stages of the locust. J. Comp. Physiol. A 162, 247–259.CrossRefGoogle Scholar
  39. 39.
    Stevenson, P. A., Spörhase-Eichmann, U. (1995) Localization of octopaminergic neurones in insects. Comp. Biochem. Physiol. 110A, 203–215.Google Scholar
  40. 40.
    Stevenson, P. A., Pflüger, H.-J., Eckert, M., Rapus, J. (1992) Octopamine immunoreactive cell populations in the locust thoracic-abdominal nervous system. J. Comp. Neurol. 315, 382–397.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Stevenson, P. A., Pflüger, H.-J., Eckert, M., Rapus, J. (1994) Octopamine-like immunoreactive neurones in locust genital abdominal ganglia. Cell Tissue Res. 275, 299–308.CrossRefGoogle Scholar
  42. 42.
    Walther, C., Zittlau, K. E. (1998) Resting membrane properties of locust muscle and their modulation II. Actions of the biogenic amine octopamine. J. Neurophysiol. 80, 785–797.CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Walther, C., Zittlau, K. E., Murck, H., Voigt, K. (1998) Resting membrane properties of locust muscle and their modulation I. Actions of the neuropeptides YGGFMRFamide and proctolin. J. Neurophysiol. 80, 771–784.CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Watson, A. H. D. (1984) The dorsal unpaired median neurons of the locust metathoracic ganglion: neuronal structure and diversity, and synapse distribution. J. Neurocytol. 13, 303–327.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Wegener, G. (1996) Flying insects: Model systems in exercise physiology. Experientia 52, 404–412.CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Wicher, D., Walther, C., Wicher, C. (2001) Non-synaptic ion channels in insects-basic properties of currents and their modulation in neurons and skeletal muscles. Prog. Neurobiol. 64, 431–525.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Akadémiai Kiadó, Budapest 2004

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors and Affiliations

  1. 1.Freie Universität Berlin, FB BCPInstitut für Biologie, NeurobiologieBerlinGermany

Personalised recommendations