Skip to main content
SpringerLink
Log in

Cellular Physiology of the Honey Bee Brain

  • Chapter
  • First Online:
Honeybee Neurobiology and Behavior

Abstract

Membrane-bound ion channels determine the electrical activity of ­excitable cells. In this respect honey bee neurons within the olfactory pathways are among the physiologically best studied insect cells. Several ionic currents were characterized from identified central neurons in vitro, in particular mushroom body Kenyon cells (KCs) and antennal lobe (AL) neurons. They express voltage-sensitive Na+ and Ca2+ currents that depolarize the neurons upon activation. Outward K+ currents are rather diverse. At least four types exist: a delayed rectifier, a rapidly inactivating A-type, a slowly inactivating and a Ca2+-dependent K+ current. This diversity of K+ channels determines the threshold and shapes of single spikes and spike trains. Based on sequence analyses the honey bee genome contains genes coding for nine nicotinic acetylcholine receptor α-subunits, three GABA receptor subunits, one glutamate-chloride channel, three NMDA receptor subtypes, and two histamine-chloride channels. Acetylcholine-, GABA-, and glutamate-induced currents have been physiologically characterized. The ionotropic nicotinic cholinergic receptor is one of the major excitatory receptors of the olfactory pathway. It is involved during olfactory learning and therefore a good candidate for inducing learning-dependent synaptic plasticity (see Chap. 3.3). GABA-induced Cl− currents provide the major inhibitory system. In addition, glutamate-sensitive Cl− channels provide a parallel inhibitory network within the honey bee ALs. KCs express functional cation-selective AMPA-like receptors, whereas no physiological data exist on functioning NMDA-like receptors. Integrating the cell physiological data into a working model to explain experience-dependent neuronal plasticity is challenging, because the interactions of the various currents and signaling cascades and their contribution to experience-dependent plasticity remain to be analysed.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

4-AP:

4-aminopyridine

AMPA:

2-amino-3-(5-methyl-3-oxo-1,2-oxazol-4-yl) propanoic acid

cAMP:

Cyclic adenosine monophosphate

MLA:

Methyllycaconitine

NMDA:

N-Methyl-D-aspartate

OA:

Octopamine

TTX:

Tetrodotoxin

References

  1. Barbara GS, Grünewald B, Paute S, Gauthier M, Raymond-Delpech V (2008) Study of nicotinic acetylcholine receptors on cultured antennal lobe neurones from adult honeybee brains. Invert Neurosci 8(1):19–29

    Article  PubMed  CAS  Google Scholar 

  2. Barbara GS, Zube C, Rybak J, Gauthier M, Grünewald B (2005) Acetylcholine, GABA and glutamate induce ionic currents in cultured antennal lobe neurons of the honeybee, Apis ­mellifera. J Comp Physiol A 191(9):823–836

    Article  PubMed  Google Scholar 

  3. Bicker G, Kreissl S (1994) Calcium imaging reveals nicotinic acetylcholine receptors on cultured mushroom body neurons. J Neurophysiol 71(2):808–810

    PubMed  CAS  Google Scholar 

  4. Bicker G, Schäfer S, Kingan TG (1985) Mushroom body feedback interneurones in the honeybee show GABA-like immunoreactivity. Brain Res 360(1–2):394–397

    Article  PubMed  CAS  Google Scholar 

  5. Bornhauser BC, Meyer EP (1997) Histamine-like immunoreactivity in the visual system and brain of an orthopteran and a hymenopteran insect. Cell Tissue Res 287(1):211–221

    Article  PubMed  CAS  Google Scholar 

  6. Cleland TA (1996) Inhibitory glutamate receptor channels. Mol Neurobiol 13(2):97–136

    Article  PubMed  CAS  Google Scholar 

  7. Collet C, Belzunces L (2007) Excitable properties of adult skeletal muscle fibres from the honeybee Apis mellifera. J Exp Biol 210(Pt 3):454–464

    Article  PubMed  CAS  Google Scholar 

  8. Deglise P, Grünewald B, Gauthier M (2002) The insecticide imidacloprid is a partial agonist of the nicotinic receptor of honeybee Kenyon cells. Neurosci Lett 321(1–2):13–16

    Article  PubMed  CAS  Google Scholar 

  9. Devaud JM, Blunk A, Podufall J, Giurfa M, Grünewald B (2007) Using local anaesthetics to block neuronal activity and map specific learning tasks to the mushroom bodies of an insect brain. Eur J Neurosci 26(11):3193–3206

    Article  PubMed  Google Scholar 

  10. Dupuis JP, Bazelot M, Barbara GS, Paute S, Gauthier M et al (2010) Homomeric RDL and heteromeric RDL/LCCH3 GABA receptors in the honeybee antennal lobes: two candidates for inhibitory transmission in olfactory processing. J Neurophysiol 103(1):458–468

    Article  PubMed  CAS  Google Scholar 

  11. Goldberg F, Grünewald B, Rosenboom H, Menzel R (1999) Nicotinic acetylcholine currents of cultured Kkenyon cells from the mushroom bodies of the honey bee Apis mellifera. J Physiol 514(Pt 3):759–768

    Article  PubMed  CAS  Google Scholar 

  12. Grohmann L, Blenau W, Erber J, Ebert PR, Strunker T et al (2003) Molecular and functional characterization of an octopamine receptor from honeybee (Apis mellifera) brain. J Neurochem 86(3):725–735

    Article  PubMed  CAS  Google Scholar 

  13. 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

    Article  Google Scholar 

  14. Grünewald B (2003) Differential expression of voltage-sensitive K  +  and Ca2+ currents in neurons of the honeybee olfactory pathway. J Exp Biol 206(Pt 1):117–129

    Article  PubMed  Google Scholar 

  15. Grünewald B, Wersing A (2008) An ionotropic GABA receptor in cultured mushroom body Kenyon cells of the honeybee and its modulation by intracellular calcium. J Comp Physiol A 194(4):329–340

    Article  PubMed  Google Scholar 

  16. Grünewald B, Wersing A, Wustenberg DG (2004) Learning channels. Cellular physiology of odor processing neurons within the honeybee brain. Acta Biol Hung 55(1–4):53–63

    Article  PubMed  Google Scholar 

  17. Gundelfinger ED, Schulz R (2000) Insect nicotinic acetylcholine receptors: Genes, structure, physiological and pharmacological properties. In: Clementi F, Fornasari D, Gotti C (eds) Handbook of experimental pharmacology. Springer, Heidelberg, pp 497–521

    Google Scholar 

  18. Hammer M, Menzel R (1998) Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees. Learn Mem 5(1–2):146–156

    PubMed  CAS  Google Scholar 

  19. Hosie AM, Aronstein K, Sattelle DB, Ffrench-Constant RH (1997) Molecular biology of insect neuronal GABA receptors. Trends Neurosci 20(12):578–583

    Article  PubMed  CAS  Google Scholar 

  20. Ikeno H, Usui S (1999) Mathematical description of ionic currents of the Kenyon cell in the mushroom body of honeybee. Neurocomputing 26–27:177–184

    Article  Google Scholar 

  21. Jones AK, Raymond-Delpech V, Thany SH, Gauthier M, Sattelle DB (2006) The nicotinic acetylcholine receptor gene family of the honey bee, Apis mellifera. Genome Res 16(11):1422–1430

    Article  PubMed  CAS  Google Scholar 

  22. Jones AK, Sattelle DB (2006) The cys-loop ligand-gated ion channel superfamily of the honeybee, Apis mellifera. Invert Neurosci 6(3):123–132

    Article  PubMed  CAS  Google Scholar 

  23. Kloppenburg P, Kirchhof BS, Mercer AR (1999) Voltage-activated currents from adult honeybee (Apis mellifera) antennal motor neurons recorded in vitro and in situ. J Neurophysiol 81(1):39–48

    PubMed  CAS  Google Scholar 

  24. 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(1):71–84

    Article  PubMed  CAS  Google Scholar 

  25. Laurent S, Masson C, Jakob I (2002) Whole-cell recording from honeybee olfactory receptor neurons: ionic currents, membrane excitability and odourant response in developing workerbee and drone. Eur J Neurosci 15(7):1139–1152

    Article  PubMed  Google Scholar 

  26. Mauelshagen J (1993) Neural correlates of olfactory learning paradigms in an identified neuron in the honeybee brain. J Neurophysiol 69(2):609–625

    PubMed  CAS  Google Scholar 

  27. Müller U (1997) Neuronal cAMP-dependent protein kinase type II is concentrated in mushroom bodies of Drosophila melanogaster and the honeybee Apis mellifera. J Neurobiol 33(1):33–44

    Article  PubMed  Google Scholar 

  28. Müssig L, Richlitzki A, Rössler R, Eisenhardt D, Menzel R et al (2010) Acute disruption of the NMDA receptor subunit NR1 in the honeybee brain selectively impairs memory formation. J Neurosci 30(23):7817–7825

    Article  PubMed  Google Scholar 

  29. Nässel DR (1999) Histamine in the brain of insects: a review. Microsc Res Tech 44(2–3):121–136

    Article  PubMed  Google Scholar 

  30. Nauen R, Ebbinghaus-Kintscher U, Schmuck R (2001) Toxicity and nicotinic acetylcholine receptor interaction of imidacloprid and its metabolites in Apis mellifera (Hymenoptera: Apidae). Pest Manag Sci 57(7):577–586

    Article  PubMed  CAS  Google Scholar 

  31. 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(4):1749–1759

    PubMed  CAS  Google Scholar 

  32. Perk CG, Mercer AR (2006) Dopamine modulation of honey bee (Apis mellifera) antennal-lobe neurons. J Neurophysiol 95(2):1147–1157

    Article  PubMed  CAS  Google Scholar 

  33. Sachse S, Galizia CG (2002) Role of inhibition for temporal and spatial odor representation in olfactory output neurons: a calcium imaging study. J Neurophysiol 87(2):1106–1117

    PubMed  Google Scholar 

  34. Sachse S, Peele P, Silbering AF, Guhmann M, Galizia CG (2006) Role of histamine as a putative inhibitory transmitter in the honeybee antennal lobe. Front Zool 3:22

    Article  PubMed  Google Scholar 

  35. Schäfer S, Bicker G (1986) Distribution of GABA-like immunoreactivity in the brain of the honeybee. J Comp Neurol 246(3):287–300

    Article  PubMed  Google Scholar 

  36. Schäfer S, Rosenboom H, Menzel R (1994) Ionic currents of Kenyon cells from the mushroom body of the honeybee. J Neurosci 14(8):4600–4612

    PubMed  Google Scholar 

  37. Scheidler A, Kaulen P, Bruning G, Erber J (1990) Quantitative autoradiographic localization of [125I] alpha-bungarotoxin binding sites in the honeybee brain. Brain Res 534(1–2):332–335

    Article  PubMed  CAS  Google Scholar 

  38. Scheiner R, Baumann A, Blenau W (2006) Aminergic control and modulation of honeybee behaviour. Curr Neuropharmacol 4(4):259–276

    Article  PubMed  CAS  Google Scholar 

  39. Si A, Helliwell P, Maleszka R (2004) Effects of NMDA receptor antagonists on olfactory learning and memory in the honeybee (Apis mellifera). Pharmacol Biochem Behav 77(2):191–197

    Article  PubMed  CAS  Google Scholar 

  40. Stopfer M, Bhagavan S, Smith BH, Laurent G (1997) Impaired odour discrimination on desynchronization of odour-encoding neural assemblies. Nature 390(6655):70–74

    Article  PubMed  CAS  Google Scholar 

  41. Thany SH (2010) Insect nicotinic acetylcholine receptors, vol 683, Advances in experimental medicine and biology. Springer, New York

    Book  Google Scholar 

  42. Thany SH, Crozatier M, Raymond-Delpech V, Gauthier M, Lenaers G (2005) Apisalpha2, Apisalpha7-1 and Apisalpha7-2: three new neuronal nicotinic acetylcholine receptor alpha-subunits in the honeybee brain. Gene 344:125–132

    Article  PubMed  CAS  Google Scholar 

  43. Thany SH, Lenaers G, Crozatier M, Armengaud C, Gauthier M (2003) Identification and localization of the nicotinic acetylcholine receptor alpha3 mRNA in the brain of the honeybee, Apis mellifera. Insect Mol Biol 12(3):255–262

    Article  PubMed  CAS  Google Scholar 

  44. Tomizawa M, Casida JE (2003) Selective toxicity of neonicotinoids attributable to specificity of insect and mammalian nicotinic receptors. Annu Rev Entomol 48:339–364

    Article  PubMed  CAS  Google Scholar 

  45. Usherwood PNR (1994) Insect glutamate receptors. Adv Insect Physiol 24:309–341

    Article  CAS  Google Scholar 

  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(5):431–525

    Article  PubMed  CAS  Google Scholar 

  47. Wüstenberg DG, Boytcheva M, Grünewald B, Byrne JH, Menzel R et al (2004) Current- and voltage-clamp recordings and computer simulations of Kenyon cells in the honeybee. J Neurophysiol 92(4):2589–2603

    Article  PubMed  Google Scholar 

  48. Wüstenberg DG, Grünewald B (2004) Pharmacology of the neuronal nicotinic acetylcholine receptor of cultured Kenyon cells of the honeybee, Apis mellifera. J Comp Physiol A 190(10):807–821

    Article  PubMed  Google Scholar 

  49. Zachepilo TG, Il’inykh YF, Lopatina NG, Molotkov DA, Popov AV et al (2008) Comparative analysis of the locations of the NR1 and NR2 NMDA receptor subunits in honeybee (Apis mellifera) and fruit fly (Drosophila melanogaster, Canton-S wild-type) cerebral ganglia. Neurosci Behav Physiol 38(4):369–372

    Article  PubMed  CAS  Google Scholar 

  50. Zannat MT, Locatelli F, Rybak J, Menzel R, Leboulle G (2006) Identification and localisation of the NR1 sub-unit homologue of the NMDA glutamate receptor in the honeybee brain. Neurosci Lett 398(3):274–279

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Fachbereich Biowissenschaften, Institut für Bienenkunde, Polytechnische Gesellschaft Frankfurt am Main, Goethe-Universität Frankfurt am Main, Karl-von-Frisch-Weg 2, D-61440, Oberursel, Germany

    Bernd Grünewald

Authors
  1. Bernd Grünewald
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bernd Grünewald .

Editor information

Editors and Affiliations

  1. , Department of Neurobiology, Universität Konstanz, Universitätsstrasse 10, Konstanz, 78457, Germany

    C. Giovanni Galizia

  2. , Department of Neurobiology, Freie Universität Berlin, Königin-Luise-Str. 28-30, Berlin, 14195, Germany

    Dorothea Eisenhardt

  3. , Centre de Recherches sur la Cognition An, CNRS - Université Paul Sabatier, Route de Narbonne 118, Toulouse Cedex 9, 31062, France

    Martin Giurfa

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Grünewald, B. (2012). Cellular Physiology of the Honey Bee Brain. In: Galizia, C., Eisenhardt, D., Giurfa, M. (eds) Honeybee Neurobiology and Behavior. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-2099-2_15

Download citation

Publish with us

Policies and ethics

Search

Navigation