Skip to main content
SpringerLink
Log in

Glutamate Neurotransmission in the Honey Bee Central Nervous System

  • Chapter
  • First Online:
Honeybee Neurobiology and Behavior

Abstract

There is increasing evidence that a glutamatergic neurotransmission is present in the honey bee central nervous system. Besides the localization of glutamate in the brain, membrane and vesicular glutamate transporters as well as specific receptors have been characterized. Glutamate receptors homologous to their vertebrate counterparts (NMDA, non-NMDA and metabotropic) have been identified. In addition, there are inhibitory currents mediated by glutamate-gated chloride channels, specific to invertebrates. Glutamate neurotransmission is widespread in the brain, but it is probably less important in the mushroom body. Several studies show that the activation of different components of the neurotransmission is required during or shortly after conditioning for the formation of specific memory phases. In addition, different regions of the brain are differently implicated in memory processes.

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

AMPA:

Amino-3-hydroxy-5-methylisoxazole-4-propionic acid

CS:

Conditioned stimulus

eLTM:

Early long-term memory

GABA:

g-aminobutyric acid

Glu-ir:

Glutamate-like immunoreactivity

GluCl:

Glutamate-gated chloride

lLTM:

Late long-term memory

LTM:

Long-term memory

LTP:

Long-term potentiation

MTM:

Mid-term memory

NMDA:

N-Methyl-D-aspartic acid

PER:

Proboscis extension reflex

RNAi:

RNA interference

US:

Unconditioned stimulus

References

  1. 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 191:823–836

    Article  PubMed  Google Scholar 

  2. Bicker G, Schäfer S, Ottersen OP, Storm-Mathisen J (1988) Glutamate-like immunoreactivity in identified neuronal populations of insect nervous systems. J Neurosci 8:2108–2122

    PubMed  CAS  Google Scholar 

  3. Bitterman ME, Menzel R, Fietz A, Schäfer S (1983) Classical conditioning of proboscis extension in honeybees (Apis mellifera). J Comp Psychol 97:107–119

    Article  PubMed  CAS  Google Scholar 

  4. Breer H, Sattelle DB (1987) Molecular-properties and functions of insect acetylcholine-receptors. J Insect Physiol 33:771–790

    Article  CAS  Google Scholar 

  5. Cain DP (1997) LTP, NMDA, genes and learning. Curr Opin Neurobiol 7:235–242

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  7. Colomb J, Kaiser L, Chabaud MA, Preat T (2009) Parametric and genetic analysis of Drosophila appetitive long-term memory and sugar motivation. Genes Brain Behav 8:407–415

    Article  PubMed  CAS  Google Scholar 

  8. Daniels RW, Gelfand MV, Collins CA, DiAntonio A (2008) Visualizing glutamatergic cell bodies and synapses in Drosophila larval and adult CNS. J Comp Neurol 508:131–152

    Article  PubMed  CAS  Google Scholar 

  9. Dingledine R, Borges K, Bowie D, Traynelis SF (1999) The glutamate receptor ion channels. Pharmacol Rev 51:7–61

    PubMed  CAS  Google Scholar 

  10. El Hassani AK, Dacher M, Gauthier M, Armengaud C (2005) Effects of sublethal doses of fipronil on the behavior of the honeybee (Apis mellifera). Pharmacol Biochem Behav 82:30–39

    Article  PubMed  Google Scholar 

  11. El Hassani AK, Dupuis JP, Gauthier M, Armengaud C (2009) Glutamatergic and GABAergic effects of fipronil on olfactory learning and memory in the honeybee. Invert Neurosci 9:91–100

    Article  PubMed  Google Scholar 

  12. El Hassani AK, Giurfa M, Gauthier M, Armengaud C (2008) Inhibitory neurotransmission and olfactory memory in honeybees. Neurobiol Learn Mem 90:589–595

    Article  PubMed  Google Scholar 

  13. Farris SM, Abrams AI, Strausfeld NJ (2004) Development and morphology of class II Kenyon cells in the mushroom bodies of the honey bee, Apis mellifera. J Comp Neurol 474:325–339

    Article  PubMed  Google Scholar 

  14. Featherstone DE et al (2005) An essential Drosophila glutamate receptor subunit that functions in both central neuropil and neuromuscular junction. J Neurosci 25:3199–3208

    Article  PubMed  CAS  Google Scholar 

  15. Friedrich A, Thomas U, Müller U (2004) Learning at different satiation levels reveals parallel functions for the cAMP-protein kinase A cascade in formation of long-term memory. J Neurosci 24:4460–4468

    Article  PubMed  CAS  Google Scholar 

  16. Funada M et al (2004) Characterization of the two distinct subtypes of metabotropic glutamate receptors from honeybee, Apis mellifera. Neurosci Lett 359:190–194

    Article  PubMed  CAS  Google Scholar 

  17. Hannon GJ (2002) RNA interference. Nature 418:244–251

    Article  PubMed  CAS  Google Scholar 

  18. Jan LY, Jan YN (1976) L-glutamate as an excitatory transmitter at the Drosophila larval neuromuscular junction. J Physiol 262:215–236

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  20. Krashes MJ et al (2009) A neural circuit mechanism integrating motivational state with memory expression in Drosophila. Cell 139:416–427

    Article  PubMed  CAS  Google Scholar 

  21. Krashes MJ, Keene AC, Leung B, Armstrong JD, Waddell S (2007) Sequential use of mushroom body neuron subsets during Drosophila odor memory processing. Neuron 53:103–115

    Article  PubMed  CAS  Google Scholar 

  22. Kucharski R, Ball EE, Hayward DC, Maleszka R (2000) Molecular cloning and expression analysis of a cDNA encoding a glutamate transporter in the honeybee brain. Gene 242:399–405

    Article  PubMed  CAS  Google Scholar 

  23. Kucharski R, Mitri C, Grau Y, Maleszka R (2007) Characterization of a metabotropic glutamate receptor in the honeybee (Apis mellifera): implications for memory formation. Invert Neurosci 7:99–108

    Article  PubMed  CAS  Google Scholar 

  24. Locatelli F, Bundrock G, Müller U (2005) Focal and temporal release of glutamate in the mushroom bodies improves olfactory memory in Apis mellifera. J Neurosci 25:11614–11618

    Article  PubMed  CAS  Google Scholar 

  25. Lopatina NG, Ryzhova IV, Chesnokova EG, Dmitrieva LA (2000) N-Methyl-D-aspartate receptors in the short-term memory development in the honey bee Apis mellifera. Zh Evol Biokhim Fiziol 36:223–228

    PubMed  CAS  Google Scholar 

  26. Maleszka R, Helliwell P, Kucharski R (2000) Pharmacological interference with glutamate re-uptake impairs long-term memory in the honeybee, Apis mellifera. Behav Brain Res 115:49–53

    Article  PubMed  CAS  Google Scholar 

  27. Malinow R, Malenka RC (2002) AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25:103–126

    Article  PubMed  CAS  Google Scholar 

  28. Marrus SB, Portman SL, Allen MJ, Moffat KG, DiAntonio A (2004) Differential localization of glutamate receptor subunits at the Drosophila neuromuscular junction. J Neurosci 24:1406–1415

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  30. Menzel R, Manz G (2005) Neural plasticity of mushroom body-extrinsic neurons in the honeybee brain. J Exp Biol 208:4317–4332

    Article  PubMed  Google Scholar 

  31. Müßig L et al (2010) Acute disruption of the NMDA receptor subunit NR1 in the honeybee brain selectively impairs memory formation. J Neurosci 30:7817–7825

    Article  PubMed  Google Scholar 

  32. Okada R, Rybak J, Manz G, Menzel R (2007) Learning-related plasticity in PE1 and other mushroom body-extrinsic neurons in the honeybee brain. J Neurosci 27:11736–11747

    Article  PubMed  CAS  Google Scholar 

  33. Pascual A, Preat T (2001) Localization of long-term memory within the Drosophila mushroom body. Science 294:1115–1117

    Article  PubMed  CAS  Google Scholar 

  34. Petersen SA, Fetter RD, Noordermeer JN, Goodman CS, DiAntonio A (1997) Genetic analysis of glutamate receptors in Drosophila reveals a retrograde signal regulating presynaptic transmitter release. Neuron 19:1237–1248

    Article  PubMed  CAS  Google Scholar 

  35. Qin G et al (2005) Four different subunits are essential for expressing the synaptic glutamate receptor at neuromuscular junctions of Drosophila. J Neurosci 25:3209–3218

    Article  PubMed  CAS  Google Scholar 

  36. Raymond V, Sattelle DB (2002) Novel animal-health drug targets from ligand-gated chloride channels. Nat Rev Drug Discov 1:427–436

    Article  PubMed  CAS  Google Scholar 

  37. Schuster CM et al (1991) Molecular cloning of an invertebrate glutamate receptor subunit expressed in Drosophila muscle. Science 254:112–114

    Article  PubMed  CAS  Google Scholar 

  38. 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 77:191–197

    Article  PubMed  CAS  Google Scholar 

  39. Sinakevitch I, Grau Y, Strausfeld NJ, Birman S (2010) Dynamics of glutamatergic signaling in the mushroom body of young adult Drosophila. Neural Dev 5:10

    Article  PubMed  Google Scholar 

  40. Strausfeld NJ (2002) Organization of the honey bee mushroom body: representation of the calyx within the vertical and gamma lobes. J Comp Neurol 450:4–33

    Article  PubMed  Google Scholar 

  41. The Honeybee Genome Sequencing Consortium (2006) Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443:931–949

    Article  Google Scholar 

  42. Tsacopoulos M, Poitry-Yamate CL, Poitry S, Perrottet P, Veuthey AL (1997) The nutritive function of glia is regulated by signals released by neurons. Glia 21:84–91

    Article  PubMed  CAS  Google Scholar 

  43. Ultsch A et al (1992) Glutamate receptors of Drosophila melanogaster: cloning of a kainate-selective subunit expressed in the central nervous system. Proc Natl Acad Sci USA 89:10484–10488

    Article  PubMed  CAS  Google Scholar 

  44. van Swinderen B, Brembs B (2010) Attention-like deficit and hyperactivity in a Drosophila memory mutant. J Neurosci 30:1003–1014

    Article  PubMed  Google Scholar 

  45. Volkner M, Lenz-Bohme B, Betz H, Schmitt B (2000) Novel CNS glutamate receptor subunit genes of Drosophila melanogaster. J Neurochem 75:1791–1799

    Article  PubMed  CAS  Google Scholar 

  46. Weinberg RJ (1999) Glutamate: an excitatory neurotransmitter in the mammalian CNS. Brain Res Bull 50:353–354

    Article  PubMed  CAS  Google Scholar 

  47. Wu CL et al (2007) Specific requirement of NMDA receptors for long-term memory consolidation in Drosophila ellipsoid body. Nat Neurosci 10:1578–1586

    Article  PubMed  CAS  Google Scholar 

  48. Zannat T, 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 398:274–279

    Article  PubMed  CAS  Google Scholar 

  49. Zars T, Fischer M, Schulz R, Heisenberg M (2000) Localization of a short-term memory in Drosophila. Science 288:672–675

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Neurobiologie, Freie Universität Berlin, Berlin, Germany

    Gérard Leboulle

Authors
  1. Gérard Leboulle
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gérard Leboulle .

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

Leboulle, G. (2012). Glutamate Neurotransmission in the Honey Bee Central Nervous System. In: Galizia, C., Eisenhardt, D., Giurfa, M. (eds) Honeybee Neurobiology and Behavior. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-2099-2_14

Download citation

Publish with us

Policies and ethics

Search

Navigation