Apidologie

, Volume 43, Issue 3, pp 322–333 | Cite as

The molecular signalling processes underlying olfactory learning and memory formation in honeybees

Original article

Abstract

The honeybee Apis mellifera provides the opportunity to study molecular signalling processes underlying olfactory learning and memory formation in intact animals. Applying innovative techniques to monitor and manipulate signalling processes in vivo during learning led to the identification of dynamic signalling events that contribute to different facets of olfactory learning and memory formation. these techniques opened novel insights into how different training strengths change the dynamics of individual molecular signalling processes, resulting in the induction and maintenance of distinct memory phases. To date, the major contributors were believed to be the mushroom bodies, as shown in Drosophila. This in vivo work now adds the insight that processes localised in the antennal lobes also contribute considerably to the memory processes. In addition, it shows that the effects of satiation on appetitive learning and memory is most likely mediated by so far unidentified molecular signalling pathways, as the aforementioned evolutionarily conserved and well-known pathways are only partially involved.

Keywords

learning memory second messenger translation transcription 

Notes

ACKNOWLEDGEMENT

I thank Dr. S. Meuser for help with the manuscript.

REFERENCES

  1. Arnold, G., Masson, C., Budharugsa, S. (1985) Comparative study of the antennal lobes and their afferent pathway in the worker bee and the drone (Apis mellifera). Cell Tissue Res. 242, 593–605CrossRefGoogle Scholar
  2. Barbara, G.S., 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 Neuroethol. Sens. Neural Behav. Physiol. 191, 823–836PubMedCrossRefGoogle Scholar
  3. Ben-Shahar, Y. (2005) The foraging gene, behavioral plasticity, and honeybee division of labor. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 191, 987–994PubMedCrossRefGoogle Scholar
  4. Ben-Shahar, Y., Robinson, G.E. (2001) Satiation differentially affects performance in a learning assay by nurse and forager honey bees. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 187, 891–899PubMedCrossRefGoogle Scholar
  5. Ben-Shahar, Y., Robichon, A., Sokolowski, M.B., Robinson, G.E. (2002) Influence of gene action across different time scales on behavior. Science 296, 741–744PubMedCrossRefGoogle Scholar
  6. Bicker, G., Schäfer, S., Ottersen, O.P., Storm-Mathisen, J. (1988) Glutamate-like immunoreactivity in identified neuronal populations of insect nervous systems. J. Neurosci. 8, 2108–2122PubMedGoogle Scholar
  7. Bitterman, M.E., Menzel, R., Fietz, A., Schäfer, S. (1983) Classical olfactory conditioning of proboscis extension in honeybees (Apis mellifera). J. Comp. Physiol. 97, 107–119Google Scholar
  8. Bloch, G. (2010) The social clock of the honeybee. J. Biol. Rhythms 25, 307–317PubMedCrossRefGoogle Scholar
  9. Brand, A.H., Perrimon, N. (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401–415PubMedGoogle Scholar
  10. Braun, G., Bicker, G. (1992) Habituation of an appetitive reflex in the honeybee. J. Neurophysiol. 67, 588–598PubMedGoogle Scholar
  11. Burke, C.J., Waddell, S. (2011) Remembering nutrient quality of sugar in Drosophila. Curr. Biol. 21, 746–750PubMedCrossRefGoogle Scholar
  12. Chabaud, M.A., Devaud, J.M., Pham-Delègue, M.H., Preat, T., Kaiser, L. (2006) Olfactory conditioning of proboscis activity in Drosophila melanogaster. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 192, 1335–1348PubMedCrossRefGoogle Scholar
  13. Claridge-Chang, A., Roorda, R.D., Vrontou, E., Sjulson, L., Li, H., Hirsh, J., Miesenböck, G. (2009) Writing memories with light-addressable reinforcement circuitry. Cell 139, 405–415PubMedCrossRefGoogle Scholar
  14. Collett, T.S., Collett, M. (2000) Path integration in insects. Curr. Opin. Neurobiol. 10, 757–762PubMedCrossRefGoogle Scholar
  15. Davis, R.L. (2011) Traces of Drosophila memory. Neuron 70, 8–19PubMedCrossRefGoogle Scholar
  16. Davis, H.P., Squire, L.R. (1984) Protein synthesis and memory: a review. Psychol. Bull. 96, 518–559PubMedCrossRefGoogle Scholar
  17. de Brito Sanchez, M.G., Chen, C., Li, J., Liu, F., Gauthier, M., Giurfa, M. (2008) Behavioral studies on tarsal gustation in honeybees: sucrose responsiveness and sucrose-mediated olfactory conditioning. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 194, 861–869PubMedCrossRefGoogle Scholar
  18. Drier, E.A., Tello, M.K., Cowan, M., Wu, P., Blace, N., Sacktor, T.C., Yin, J.C. (2002) Memory enhancement and formation by atypical PKM activity in Drosophila melanogaster. Nat. Neurosci. 5, 316–24PubMedCrossRefGoogle Scholar
  19. Erber, J., Kierzek, S., Sander, E., Grandy, K. (1998) Tactile learning in the honeybee. J. Comp. Physiol. A 183, 737–744CrossRefGoogle Scholar
  20. Erber, J., Masuhr, T., Menzel, R. (1980) Localization of short-term memory in the brain of the bee, Apis mellifera. Physiol. Entomol. 5, 343–358CrossRefGoogle Scholar
  21. Erber, J., Pribbenow, B., Grandy, K., Kierzek, S. (1997) Tactile motor learning in the antennal system of the honeybee (Apis mellifera). J. Comp. Physiol. A 181, 355–365CrossRefGoogle Scholar
  22. Farooqui, T., Robinson, K., Vaessin, H., Smith, B.H. (2003) Modulation of early olfactory processing by an octopaminergic reinforcement pathway in the honeybee. J. Neurosci. 23, 5370–5380PubMedGoogle Scholar
  23. Flanagan, D., Mercer, A.R. (1989) An atlas and 3-D reconstruction of the antennal lobes in the worker honeybee, Apis mellifera L. Int. J. Insect Morphol. Embryol. 18, 145–159CrossRefGoogle Scholar
  24. 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, 4460–4468PubMedCrossRefGoogle Scholar
  25. Fujita, M., Tanimura, T. (2011) Drosophila evaluates and learns the nutritional value of sugars. Curr. Biol. 21, 751–755PubMedCrossRefGoogle Scholar
  26. Funada, M., Yasuo, S., Yoshimura, T., Ebihara, S., Sasagawa, H., Kitagawa, Y., Kadowaki, T. (2004) Characterization of the two distinct subtypes of metabotropic glutamate receptors from honeybee, Apis mellifera. Neurosci. Lett. 359, 190–194PubMedCrossRefGoogle Scholar
  27. Galizia, C.G., Menzel, R. (2000) Odour perception in honeybees: coding information in glomerular patterns. Curr. Opin. Neurobiol. 10, 504–510PubMedCrossRefGoogle Scholar
  28. Gauthier, M. (2010) State of the art on insect nicotinic acetylcholine receptor function in learning and memory. Adv. Exp. Med. Biol. 683, 97–115PubMedCrossRefGoogle Scholar
  29. Giurfa, M. (2003) Cognitive neuroethology: dissecting non-elemental learning in a honeybee brain. Curr. Opin. Neurobiol. 13, 726–735PubMedCrossRefGoogle Scholar
  30. Grünbaum, L., Müller, U. (1998) Induction of a specific olfactory memory leads to a long-lasting activation of protein kinase C in the antennal lobe of the honeybee. J. Neurosci. 18, 4384–4392PubMedGoogle Scholar
  31. Hammer, M. (1993) An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees. Nature 366, 59–63CrossRefGoogle Scholar
  32. Hammer, M., Menzel, R. (1995) Learning and memory in the honeybee. J. Neurosci. 15, 1617–1630PubMedGoogle Scholar
  33. Hammer, M., Menzel, R. (1998) Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees. Learn. Mem. 5, 146–156PubMedGoogle Scholar
  34. Haupt, S.S. (2004) Antennal sucrose perception in the honey bee (Apis mellifera L.): behaviour and electrophysiology. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 190(9), 735–745PubMedGoogle Scholar
  35. Haupt, S.S. (2007) Central gustatory projections and side-specificity of operant antennal muscle conditioning in the honeybee. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 193(5), 523–535PubMedCrossRefGoogle Scholar
  36. Heisenberg, M., Borst, A., Wagner, S., Byers, D. (1985) Drosophila mushroom body mutants are deficient in olfactory learning. J. Neurogenet. 2, 1–30PubMedCrossRefGoogle Scholar
  37. Hildebrandt, H., Müller, U. (1995a) PKA activity in the antennal lobe of honeybees is regulated by chemosensory stimulation in vivo. Brain Res. 679, 281–288PubMedCrossRefGoogle Scholar
  38. Hildebrandt, H., Müller, U. (1995b) Octopamine mediates rapid stimulation of protein kinase A in the antennal lobe of honeybees. J. Neurobiol. 27, 44–50PubMedCrossRefGoogle Scholar
  39. Kandel, E.R. (2001) The molecular biology of memory storage: a dialogue between genes and synapses. Science 294, 1030–1038PubMedCrossRefGoogle Scholar
  40. Krashes, M.J., Waddell, S. (2008) Rapid consolidation to a radish and protein synthesis-dependent long-term memory after single-session appetitive olfactory conditioning in Drosophila. J. Neurosci. 28, 3103–3113PubMedCrossRefGoogle Scholar
  41. 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, 71–84PubMedCrossRefGoogle Scholar
  42. Kreissl, S., Eichmüller, S., Bicker, G., Rapus, J., Eckert, M. (1994) Octopamine-like immunoreactivity in the brain and suboesophageal ganglion of the honeybee. J. Comp. Neurol. 348, 583–595PubMedCrossRefGoogle Scholar
  43. Kucharski, R., Ball, E., Hayward, D., Maleszka, R. (2000) Molecular cloning and expression analysis of a cDNA encoding a glutamate transporter in the honeybee brain. Gene 244, 399–405CrossRefGoogle Scholar
  44. Kuwabara, M. (1957) Bildung des bedingten Reflexes von Pavlovs Typus bei der Honigbiene, Apis mellifica. J. Fac. Sci. Hokkaido Univ. Ser. VI Zool. 13, 458–464Google Scholar
  45. Leboulle, G., Müller, U. (2004) Synergistic activation of insect cAMP-dependent protein kinase A (type II) by cyclicAMP and cyclicGMP. FEBS Lett. 576, 216–220PubMedCrossRefGoogle Scholar
  46. Lima, S.Q., Miesenböck, G. (2005) Remote control of behavior through genetically targeted photostimulation of neurons. Cell 121, 141–152PubMedCrossRefGoogle Scholar
  47. 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, 11614–11618PubMedCrossRefGoogle Scholar
  48. 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, 49–53PubMedCrossRefGoogle Scholar
  49. McGuire, S.E., Roman, G., Davis, R.L. (2004) Gene expression systems in Drosophila: a synthesis of time and space. Trends Genet. 20, 384–391PubMedCrossRefGoogle Scholar
  50. Menzel, R. (1999) Memory dynamics in the honeybee. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 185, 323–340CrossRefGoogle Scholar
  51. Menzel, R. (2001) Searching for the memory trace in a mini-brain, the honeybee. Learn. Mem. 8, 53–62PubMedCrossRefGoogle Scholar
  52. Menzel R., Erber J., Masuhr T. (1974) Learning and memory in the honeybee. In: Experimental analysis of insect behaviour. (ed. L. B. Browne), pp. 195–217, Springer, Berlin.Google Scholar
  53. Menzel, R., Giurfa, M. (2006) Dimensions of cognition in an insect, the honeybee. Behav. Cogn. Neurosci. Rev. 5, 24–40PubMedCrossRefGoogle Scholar
  54. Menzel, R., Müller, U. (1996) Learning and memory in honeybees: from behavior to neural substrates. Annu. Rev. Neurosci. 19, 379–404PubMedCrossRefGoogle Scholar
  55. Mobbs P. G. (1982) The brain of the honeybee Apis mellifera I. The connections and spatial organization of the mushroom bodies. Philos Trans R Soc Lond B 298: 309–354.Google Scholar
  56. Müller, U. (1996) Inhibition of nitric oxide synthase impairs a distinct form of long-term memory in the honeybee, Apis mellifera. Neuron 16, 541–549PubMedCrossRefGoogle Scholar
  57. Müller, U. (1997) The nitric oxide system in insects. Prog. Neurobiol. 51, 363–381PubMedCrossRefGoogle Scholar
  58. Müller, U. (2000) Prolonged activation of cAMP-dependent protein kinase during conditioning induces long-term memory in honeybees. Neuron 27, 159–168PubMedCrossRefGoogle Scholar
  59. Müller, U. (2002) Learning in honeybees: from molecules to behaviour. Zoology 105, 313–320PubMedCrossRefGoogle Scholar
  60. Müller, U., Hildebrandt, H. (1995) The nitric oxide/cGMP system in the antennal lobe of Apis mellifera is implicated in integrative processing of chemosensory stimuli. Eur. J. Neurosci. 7, 2240–2248PubMedCrossRefGoogle Scholar
  61. Müssig, L., Richlitzki, A., Rössler, R., Eisenhardt, D., Menzel, R., Leboulle, G. (2010) Acute disruption of the NMDA receptor subunit NR1 in the honeybee brain selectively impairs memory formation. J. Neurosci. 30, 7817–7825PubMedCrossRefGoogle Scholar
  62. Nguyen, P.V., Abel, T., Kandel, E.R. (1994) Requirement of a critical period of transcription for induction of a late phase of LTP. Science 265, 1104–1107PubMedCrossRefGoogle Scholar
  63. Page Jr., R.E., Erber, J., Fondrk, M.K. (1998) The effect of genotype on response thresholds to sucrose and foraging behavior of honey bees (Apis mellifera L.). J. Comp. Physiol. A 182, 489–500PubMedCrossRefGoogle Scholar
  64. Rehder, V. (1989) Sensory pathways and motoneurons of the proboscis reflex in the suboesophageal ganglion of the honeybee. J. Comp. Neurol. 279, 499–513PubMedCrossRefGoogle Scholar
  65. Riedel, G., Platt, B., Micheau, J. (2003) Glutamate receptor function in learning and memory. Behav. Brain Res. 140, 1–47PubMedCrossRefGoogle Scholar
  66. Root, C.M., Ko, K.I., Jafari, A., Wang, J.W. (2011) Presynaptic facilitation by neuropeptide signaling mediates odor-driven food search. Cell 145, 133–144PubMedCrossRefGoogle Scholar
  67. Rueppell, O., Pankiw, T., Nielsen, D.I., Fondrk, M.K., Beye, M., Page Jr., R.E. (2004) The genetic architecture of the behavioral ontogeny of foraging in honeybee workers. Genetics 167, 1767–1779PubMedCrossRefGoogle Scholar
  68. Sachse, S., Galizia, C.G. (2002) The role of inhibition for temporal and spatial odor representation in olfactory output neurons: A calcium imaging study. J. Neurophysiol. 87, 1106–1117PubMedGoogle Scholar
  69. Sacktor, T.C. (2008) PKMzeta, LTP maintenance, and the dynamic molecular biology of memory storage. Prog. Brain Res. 169, 27–40PubMedCrossRefGoogle Scholar
  70. Scheiner, R., Page Jr., R.E., Erber, J. (2001) The effects of genotype, foraging role, and sucrose responsiveness on the tactile learning performance of honey bees (Apis mellifera L.). Neurobiol. Learn. Mem. 76, 138–150PubMedCrossRefGoogle Scholar
  71. 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, 191–197PubMedCrossRefGoogle Scholar
  72. Smith, B.H., Abramson, C.I., Tobin, T.R. (1991) Conditional withholding of proboscis extension in honeybees (Apis mellifera) during discriminative punishment. J. Comp. Psychol. 105, 345–356PubMedCrossRefGoogle Scholar
  73. Srinivasan, M.V. (2011) Honeybees as a model for the study of visually guided flight, navigation, and biologically inspired robotics. Physiol. Rev. 91, 413–460PubMedCrossRefGoogle Scholar
  74. Szyszka, P., Ditzen, M., Galkin, A., Galizia, C.G., Menzel, R. (2005) Sparsening and temporal sharpening of olfactory representations in the honeybee mushroom bodies. J. Neurophysiol. 94, 3303–3313PubMedCrossRefGoogle Scholar
  75. Toth, A.L., Robinson, G.E. (2007) Evo-devo and the evolution of social behavior. Trends Genet. 23, 334–341PubMedCrossRefGoogle Scholar
  76. Vergoz, V., Roussel, E., Sandoz, J.C., Giurfa, M. (2007) Aversive learning in honeybees revealed by the olfactory conditioning of the sting extension reflex. PLoS One 2(3), e288PubMedCrossRefGoogle Scholar
  77. Witthöft, W. (1967) Absolute Anzahl und Verteilung der Zellen im Hirn der Honigbiene. Z. Morphol. Oekol. Tiere. 61, 160–184Google Scholar
  78. Wright, G.A., Mustard, J.A., Kottcamp, S.M., Smith, B.H. (2007) Olfactory memory formation and the influence of reward pathway during appetitive learning in honey bees. J. Exp. Biol. 210, 4024–4033PubMedCrossRefGoogle Scholar
  79. Wüstenberg, D., Gerber, B., Menzel, R. (1998) Short communication: long- but not medium-term retention of olfactory memories in honeybees is impaired by actinomycin D and anisomycin. Eur. J. Neurosci. 10, 2742–2745PubMedCrossRefGoogle Scholar
  80. Xia, S., Miyashita, T., Fu, T.F., Lin, W.Y., Wu, C.L., Pyzocha, L., Lin, I.R., Saitoe, M., Tully, T., Chiang, A.S. (2005) NMDA receptors mediate olfactory learning and memory in Drosophila. Curr. Biol. 15, 603–615PubMedCrossRefGoogle Scholar
  81. Zannat, M.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, 274–279PubMedCrossRefGoogle Scholar

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© INRA, DIB and Springer-Verlag, France 2012

Authors and Affiliations

  1. 1.Natural Sciences and Technology III, Dept. 8.3 – Biosciences (Zoology and Physiology/Neurobiology)Saarland UniversitySaarbrückenGermany

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