Advertisement

Acta Biologica Hungarica

, Volume 55, Issue 1–4, pp 53–63 | Cite as

Learning Channels. Cellular Physiology of Odor Processing Neurons Within the Honeybee Brain

  • B. GrünewaldEmail author
  • Anna Wersing
  • D. G. Wüstenberg
Article

Abstract

To understand the cellular mechanisms of olfactory learning in the honeybee brain we study the physiology of identified neurons within the olfactory pathway. Here, we review data on the voltage-sensitive and ligand-gated ionic currents of mushroom body Kenyon cells and antennal lobe neurons in vitro and in situ. Both cell types generate action potentials in vitro, but have different voltage-sensitive K+ currents. They express nicotinic acetylcholine receptors and ionotropic GABA receptors, representing the major transmitter systems in the insect olfactory system. Our data are interpreted with respect to learningdependent plasticity in the honeybee brain.

Keywords

Voltage-sensitive currents Kenyon cells acetylcholine receptor GABA receptor insects 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Benjamin, P. R. (2000) A systems approach to the cellular analysis of associative learning in the pond snail Lymnaea. Learn. Mem. 7, 124–131.Google Scholar
  2. 2.
    Bicker, G., Schäfer, S., Kingan, T. G. (1985) Mushroom body feedback interneurons in the honeybee show GABA-like immunoreactivity. Brain Res. 360, 394–397.CrossRefGoogle Scholar
  3. 3.
    Cleland, T. A. (1996) Inhibitory glutamate receptor channels. Mol. Neurobiol. 13, 97–136.CrossRefGoogle Scholar
  4. 4.
    Goldberg, F., Grünewald, B., Rosenboom, H., Menzel, R. (1999) Nicotinic acetylcholine currents of cultured Kenyon cells from the mushroom bodies of the honey bee Apis mellifera. J. Physiol. 514, 759–768.CrossRefGoogle Scholar
  5. 5.
    Grohmann, L., Blenau, W., Erber, J., Ebert, P. R., Strünkes, T., Baumann, A. (2003) Molecular and functional characterization of an octopamine receptor from honeybee (Apis mellifera) brain. J. Neurochem. 86, 725–735.CrossRefGoogle Scholar
  6. 6.
    Gronenberg, W. (1987) Anatomical and physiological properties of feedback neurons of the mushroom bodies in the bee brain. Exp. Biol. 46, 115–125.Google Scholar
  7. 7.
    Grünewald, B. (1999) Morphology of feedback neurons in the mushroom body of the honeybee, Apis mellifera. J. Comp. Neurol. 404, 114–126.CrossRefGoogle Scholar
  8. 8.
    Grünewald, B. (1999) Physiological properties and response modulations of mushroom body feedback neurons during olfactory learning in the honeybee, Apis mellifera. J. Comp. Phys. A, 185, 565–576.Google Scholar
  9. 9.
    Grünewald, B. (2003) Differential expression of voltage-sensitive K+ and Ca2+ currents in neurons of the honeybee olfactory pathway. J. Exp. Biol. 206, 117–129.CrossRefGoogle Scholar
  10. 10.
    Gundelfinger, E. D., Schulz, R. (2000) Insect nicotinic acetylcholine receptors: Genes, structure, physiological and pharmacological properties. In: Clementi, F. (ed.), Handbook of experimental pharmacology. Springer-Verlag, Heidelberg. pp. 497–521.Google Scholar
  11. 11.
    Hammer, M. (1993) An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees. Nature 366, 59–63.CrossRefGoogle Scholar
  12. 12.
    Hammer, M., Menzel, R. (1998) Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees. Learn. Mem. 5, 146–156.PubMedPubMedCentralGoogle Scholar
  13. 13.
    Heisenberg, M. (2003) Mushroom body memoir: from maps to models. Nat. Rev. Neurosci. 4, 266–275.CrossRefGoogle Scholar
  14. 14.
    Heisenberg, M., Borst, A., Wagner, S., Byers, D. (1985) Drosophila mushroom body mutants are deficient in olfactory learning. J. Neurogenetics 2, 1–30.CrossRefGoogle Scholar
  15. 15.
    Hosie, A. M., Aronstein, K., Sattelle, D. B., ffrench-Constant, R. H. (1997) Molecular biology of insect neuronal GABA receptors. Trends Neurosci. 20, 578–583.CrossRefGoogle Scholar
  16. 16.
    Kandel, E. R. (2001) The molecular biology of memory storage: A dialogue between genes and synapses. Science 294, 1030–1038.CrossRefGoogle Scholar
  17. 17.
    Kloppenburg, P., Kirchhof, B. S., Mercer, A. R. (1999) Voltage-activated currents from adult honeybee (Apis mellifera) antennal motor neurons recorded in vitro and in situ. J. Neurophysiol. 81, 39–48.CrossRefGoogle Scholar
  18. 18.
    Kreissl, S., Bicker, G. (1989) Histochemistry of acetylcholinesterase and immunocytochemistry of an acetylcholine receptor-like antigen in the brain of the honeybee. J. Comp. Neurol. 286, 71–84.CrossRefGoogle Scholar
  19. 19.
    Masuhr, T., Menzel, R. (1972) Learning experiments on the use of sidespecific information in the olfactory and visual system in the honeybee of (Apis mellifica). In: Wehner, R. (ed.) Information processing in the visual systems of arthropods. Springer, Berlin–Heidelberg–New York, pp. 315–322.CrossRefGoogle Scholar
  20. 20.
    McGuire, S. E., Le, P. T., Davis, R. L. (2001) The role of Drosophila mushroom body signaling in olfactory memory. Science 293, 1330–1333.CrossRefGoogle Scholar
  21. 21.
    Menzel, R. (2001) Searching for the memory trace in a mini-brain, the honeybee. Learning and Memory 8, 853–862.Google Scholar
  22. 22.
    Menzel, R., Heyne, A., Kinzel, C., Gerber, B., Fiala, A. (1999) Pharmacological dissociation between the reinforcing, sensitizing, and response-releasing functions of reward in honeybee classical conditioning. Behav. Neurosci. 113, 744–754.CrossRefGoogle Scholar
  23. 23.
    Müller, U. (2000) Prolonged activation of cAMP-dependent protein kinase during conditioning induces long-term memory in honeybees. Neuron 27, 159–168.CrossRefGoogle Scholar
  24. 24.
    Müller, U. (2002) Learning in honeybees: from molecules to behaviour. Zoology 105, 313–320.CrossRefGoogle Scholar
  25. 25.
    Pelz, C., Jander, J., Rosenboom, H., Hammer, M., Menzel, R. (1999) IA in Kenyon cells of the mushroom body of honeybees resembles shaker currents: kinetics, modulation by K+, and simulation. J. Neurophysiol. 81, 1749–1759.CrossRefGoogle Scholar
  26. 26.
    Rogero, O., Hämmerle, B., Tejedor, F. J. (1997) Diverse expression and distribution of Shaker potassium channels during the development of the Drosophila nervous system. J. Neurosci. 17, 5108–5118.CrossRefGoogle Scholar
  27. 27.
    Schäfer, S., Rosenboom, H., Menzel, R. (1994) Ionic currents of Kenyon cells from the mushroom body of the honeybee. J. Neurosci. 14, 4600–4612.CrossRefGoogle Scholar
  28. 28.
    Schröter, U., Malun, D. (2000) Formation of antennal lobe and mushroom body neuropils during metamorphosis in the honeybee, Apis mellifera. J. Comp. Neurol. 422, 229–245.CrossRefGoogle Scholar
  29. 29.
    Wersing, A., Grünewald, B. (2003) An ionotropic GABA receptor in cultured mushroom body Kenyon cells of the honeybee and its modulation by intracellular calcium. J. Exp. Biol. (submitted).Google Scholar
  30. 30.
    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. Neurobio. 64, 431–525.CrossRefGoogle Scholar
  31. 31.
    Wüstenberg, D., Boytcheva, M., Grünewald, B., Baxter, D. A., Menzel, R., Byrne, J. H. (2003) Current and voltage-clamp analyses and computer simulations of Kenyon cells in the honeybee. J. Neuphysiol. (in press).Google Scholar
  32. 32.
    Wüstenberg, D., Grünewald, B. (2003) The neuronal acetylcholine receptor of the honeybee: a nicotinic receptor with an unusual pharmacology. J. Comp. Physiol. A. (in press).Google Scholar
  33. 33.
    Yusuyama, K., Meinertzhagen, I. A., Schürmann, F.-W. (2002) Synaptic organization of the mushroom body calyx in Drosophila melanogaster. J. Comp. Neurol. 445, 211–226.CrossRefGoogle Scholar
  34. 34.
    Zars, T., Wolf, R., Davis, R. L., Heisenberg, M. (2000) Tissue-specific expression of a type I adenylyl cyclase rescues the rutabaga mutant memory defect: in search of the engram. Learning and Memory 7, 18–31.CrossRefGoogle 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

  • B. Grünewald
    • 1
    Email author
  • Anna Wersing
    • 1
  • D. G. Wüstenberg
    • 2
  1. 1.Institut für Biologie, NeurobiologieFreie Universität BerlinBerlinGermany
  2. 2.Department of Neurobiology & AnatomyUniversity of Texas, Houston Medical SchoolHoustonUSA

Personalised recommendations