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Neurotransmitter Systems in the Honey Bee Brain: Functions in Learning and Memory

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Honeybee Neurobiology and Behavior

Abstract

Synaptic correlates of olfactory learning within the honey bee brain ­utilize several transmitters and receptors. Experiments unraveled distinct roles of these transmitter systems in cognitive processes. Cholinergic synaptic transmission is involved in acquisition and retrieval processes. At least two subtypes of nicotinic acetylcholine receptors exist in the honey bee brain, one involved in retrieval processes and another one linked to the formation of long-term memory. The electrophysiological and pharmacological properties of the underlying nicotinic acetylcholine receptors (nAChR) are well described whereas muscarinic acetylcholine receptors (mAChR) are physiologically unknown. The reward processing pathway largely depends on octopaminergic neuromodulation. Serotonin (5-HT) impairs the conditioned response during acquisition. Whether dopamine (DA) mediates aversive learning while octopamine (OA) mediates appetitive learning remains to be analyzed. Several studies indicated that GABA receptors play a role during odor learning, but the specific function of inhibition is not yet clear. Both inhibitory and excitatory glutamate receptors are required for certain forms of learning and for memory retrieval.

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Abbreviations

α-BGT:

α-Bungarotoxin

HA:

Histamine

5-HT:

Serotonin (5-hydroxy-tryptamine)

ACh:

Acetylcholine

AChE:

Acetylcholine esterase

AmTYR1:

Honey bee TA receptor

CR:

Conditioned response

CS:

Conditioned stimulus

DA:

Dopamine

GluCl:

Glutamate-gated chloride channel

mAChR:

Muscarinic ACh receptor (metabotropic G-protein-coupled receptors)

nAChR:

Nicotinic ACh receptor

OA:

Octopamine

PER:

Proboscis extension reflex

siRNA:

Small interfering RNA

TA:

Tyramine

US:

Unconditioned stimulus

References

  1. Bernadou A, Demares F, Couret-Fauvel T, Sandoz JC, Gauthier M (2009) Effect of fipronil on side-specific antennal tactile learning in the honeybee. J Insect Physiol 55(12):1099–1106

    Article  PubMed  CAS  Google Scholar 

  2. Bicker G (1999) Biogenic amines in the brain of the honeybee: cellular distribution, development, and behavioral functions. Microsc Res Tech 44(2–3):166–178

    Article  PubMed  CAS  Google Scholar 

  3. Bicker G (1999) Histochemistry of classical neurotransmitters in antennal lobes and mushroom bodies of the honeybee. Microsc Res Tech 45:174–183

    Article  PubMed  CAS  Google Scholar 

  4. Blenau W, Balfanz S, Baumann A (2000) Amtyr1: characterization of a gene from honeybee (Apis mellifera) brain encoding a functional tyramine receptor. J Neurochem 74:900–908

    Article  PubMed  CAS  Google Scholar 

  5. Cano Lozano V, Armengaud C, Gauthier M (1995) Implication of the cholinergic system in memory processes in the honeybee: role and distribution of cholinergic receptors. In: 23rd Göttingen Neurobiology conference, Göttingen, p 79

    Google Scholar 

  6. Cano Lozano V, Armengaud C, Gauthier M (2001) Memory impairment induced by cholinergic antagonists injected into the mushroom bodies of the honeybee. J Comp Physiol A 187:249–254

    Article  Google Scholar 

  7. Cano Lozano V, Bonnard E, Gauthier M, Richard D (1996) Mecamylamine-induced impairment of acquisition and retrieval of olfactory conditioning in the honeybee. Behav Brain Res 81:215–222

    Article  Google Scholar 

  8. Cano Lozano V, Gauthier M (1998) Effects of the muscarinic antagonists atropine and pirenzepine on olfactory conditioning in the honeybee. Pharmacol Biochem Behav 59(4):903–907

    Article  PubMed  CAS  Google Scholar 

  9. Cazzamali G, Klaerke DA, Grimmelikhuijzen CJP (2005) A new family of insect tyramine receptors. Biochem Biophys Res Commun 338:1189–1196

    Article  PubMed  CAS  Google Scholar 

  10. Consortium (2006) Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443:931–949

    Article  Google Scholar 

  11. Dacher M, Gauthier M (2008) Involvement of NO-synthase and nicotinic receptors in learning in the honeybee. Physiol Behav 95:200–207

    Article  PubMed  CAS  Google Scholar 

  12. Dacher M, Lagarrigue A, Gauthier M (2005) Antennal tactile learning in the honeybee: effect of nicotinic antagonists on memory dynamics. Neuroscience 130:37–50

    Article  PubMed  CAS  Google Scholar 

  13. Decourtye A, Devillers J, Aupinel P, Brun F, Bagnis C et al (2011) Honeybee tracking with microchips: a new methodology to measure the effects of pesticides. Ecotoxicology 20(2):429–437

    Article  PubMed  CAS  Google Scholar 

  14. Decourtye A, Lefort S, Devillers J, Gauthier M, Aupinel P et al (2009) Sublethal effects of fipronil on the ability of honeybees (Apis mellifera L.) to orientate in a complex maze. Julius-Kühn-Archiv 423:75–83

    Google Scholar 

  15. Dupuis JP, Gauthier M, Raymond Delpech V (2011) Expression patterns of nicotinic subunits a2, a7, a8 and b1 affect the kinetics and pharmacology of ACh-induced currents in the adult bee olfactory neuropiles. J Neurophysiol 106:1604–1613

    Article  PubMed  Google Scholar 

  16. 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(1):30–39

    Article  PubMed  Google Scholar 

  17. 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(2):91–100

    Article  PubMed  Google Scholar 

  18. El Hassani AK, Giurfa M, Gauthier M, Armengaud C (2008) Inhibitory neurotransmission and olfactory memory in honeybees. Neurobiol Learn Mem 90(4):589–595

    Article  PubMed  Google Scholar 

  19. Farooqui T, Robinson K, Vaessin H, Smith BH (2003) Modulation of early olfactory processing by an octopaminergic reinforcement pathway in the honeybee. J Neurosci 23(12):5370–5380

    PubMed  CAS  Google Scholar 

  20. Ganeshina O, Menzel R (2001) GABA-immunoreactive neurons in the mushroom bodies of the honeybee: an electron microscopic study. J Comp Neurol 437(3):335–349

    Article  PubMed  CAS  Google Scholar 

  21. Gauthier M (2010) State of the art on insect nicotinic acetylcholine receptor function in learning and memory. Adv Exp Med Biol 681:143–149

    Article  Google Scholar 

  22. Gauthier M, Cano Lozano V, Zaoujal A, Richard D (1994) Effects of intracranial injections of scopolamine on olfactory conditioning retrieval in the honeybee. Behav Brain Res 63(2):145–149

    Article  PubMed  CAS  Google Scholar 

  23. Gauthier M, Dacher M, Thany SH, Niggebrügge C, Déglise P et al (2006) Involvement of a-bungarotoxin-sensitive nicotinic receptors in long-term memory formation in the honeybee (Apis mellifera). Neurobiol Learn Mem 86:164–174

    Article  PubMed  CAS  Google Scholar 

  24. Hammer M (1993) An identified neuron mediates the unconditioned stimulus in associative learning in honeybees. Nature 366:59–63

    Article  Google Scholar 

  25. 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

    PubMed  CAS  Google Scholar 

  26. Hauser F, Cazzamali G, Williamson M, Blenau W, Grimmelikhuijzen CJP (2006) A review of neurohormone GPCRs present in the fruitfly Drosophila melanogaster and the honeybee Apis mellifera. Prog Neurobiol 80:1–19

    Article  PubMed  CAS  Google Scholar 

  27. Ismail N, Christine S, Robinson GE, Fahrbach SE (2008) Pilocarpine improves recognition of nestmates in young honey bees. Neurosci Lett 439(2):178–181

    Article  PubMed  CAS  Google Scholar 

  28. Ismail N, Robinson GE, Fahrbach SE (2006) Stimulation of muscarinic receptors mimics experience-dependent plasticity in the honey bee brain. Proc Natl Acad Sci USA 103(1):207–211

    Article  PubMed  CAS  Google Scholar 

  29. 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 16:1422–1430

    Article  PubMed  CAS  Google Scholar 

  30. 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 

  31. Kirschner S, Kleineidam CJ, Zube C, Rybak J, Grünewald B et al (2006) Dual olfactory pathway in the honeybee, Apis mellifera. J Comp Neurol 499:933–952

    Article  PubMed  Google Scholar 

  32. Lingueglia E, Deval E, Lazdunski M (2006) FRMFamide-gated sodium channels and ASIC channels: a new class of ionotropic receptors for FRMFamide and related peptides. Peptides 5:1138–1152

    Article  Google Scholar 

  33. 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(50):11614–11618

    Article  PubMed  CAS  Google Scholar 

  34. 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 

  35. 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

    Article  PubMed  CAS  Google Scholar 

  36. Mustard JA, Kurshan PT, Hamilton IS, Blenau W, Mercer A (2005) Developmental expression of a tyramine receptor gene in the brain of the honey bee, Apis mellifera. J Comp Neurol 483(1):66–75

    Article  PubMed  CAS  Google Scholar 

  37. Raymond-Delpech V, Augier A, Paute S, Sandoz JC (2008) Functional study of two populations of projection neurons in the antennal lobe of adult honeybee. In: Club de Neurobiologie des Invertébrés, Toulouse

    Google Scholar 

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

    PubMed  Google Scholar 

  39. 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 

  40. Sasaki K, Nagao T (2002) Brain tyramine and reproductive states of workers in honeybees. J Insect Physiol 48(12):1075–1085

    Article  PubMed  CAS  Google Scholar 

  41. Schäfer S, Bicker G, Ottersen OP, Storm-Mathisen J (1988) Taurine-like immunoreactivity in the brain of the honeybee. J Comp Neurol 268(1):60–70

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  43. Schlenstedt J, Balfanz S, Baumann A, Blenau W (2006) Am5-HT7: molecular and pharmacological characterization of the first serotonin receptor of the honeybee (Apis mellifera). J Neurochem 98(6):1985–1998

    Article  PubMed  CAS  Google Scholar 

  44. Schröter U, Malun D, Menzel R (2007) Innervation pattern of suboesophageal ventral unpaired median neurones in the honeybee brain. Cell Tissue Res 327:647–667

    Article  PubMed  Google Scholar 

  45. Schürmann FW, Erber J (1990) FMRFamide-like immunoreactivity in the brain of the honeybee (Apis mellifera). A light-and electron microscopical study. Neuroscience 38(3):797–807

    Article  PubMed  Google Scholar 

  46. 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 

  47. Strausfeld NJ, Homberg U, Kloppenburg P (2000) Parallel organization in honey bee mushroom bodies by peptidergic Kenyon cells. J Comp Neurol 424(1):179–195

    Article  PubMed  CAS  Google Scholar 

  48. Szyszka P, Ditzen M, Galkin A, Galizia CG, Menzel R (2005) Sparsening and temporal sharpening of olfactory representations in the honeybee mushroom bodies. J Neurophysiol 94(5):3303–3313

    Article  PubMed  Google Scholar 

  49. Thamm M, Balfanz S, Scheiner R, Baumann A, Blenau W (2010) Characterization of the 5-HT1A receptor of the honeybee (Apis mellifera) and involvement of serotonin in phototactic behavior. Cell Mol Life Sci 67:2467–2479

    Article  PubMed  CAS  Google Scholar 

  50. 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 

  51. 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 

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Correspondence to Monique Gauthier .

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Gauthier, M., Grünewald, B. (2012). Neurotransmitter Systems in the Honey Bee Brain: Functions in Learning and Memory. In: Galizia, C., Eisenhardt, D., Giurfa, M. (eds) Honeybee Neurobiology and Behavior. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-2099-2_13

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