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

Apidologie

Volumn 43, Issue 3, 2012, Pages 322-333

  Müller, Uli ^a  

^a SAARLAND UNIVERSITY   (Germany)

Author keywords

Learning; Memory; Second messenger; Transcription; Translation

Indexed keywords

EVOLUTIONARY BIOLOGY; FLY; GENE EXPRESSION; HONEYBEE; INNOVATION; LEARNING; MEMORY; MOLECULAR ANALYSIS; MONITORING SYSTEM; OLFACTION; SIGNALING;

EID: 84862665197     PISSN: 00448435     EISSN: 12979678     Source Type: Journal    
DOI: 10.1007/s13592-011-0115-8     Document Type: Article

References (81)

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, 593-605 (Pubitemid 16202968)
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, 823-836
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, 987-994 (Pubitemid 41586771)
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, 891-899 (Pubitemid 34124435)
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, 741-744 (Pubitemid 34442003)
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, 2108-2122
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, 107-119
8. Bloch, G. (2010) The social clock of the honeybee. J. Biol. Rhythms 25, 307-317
9. Brand, A.H., Perrimon, N. (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415 (Pubitemid 23214028)
10. Braun, G., Bicker, G. (1992) Habituation of an appetitive reflex in the honeybee. J. Neurophysiol. 67, 588-598
11. Burke, C.J., Waddell, S. (2011) Remembering nutrient quality of sugar in Drosophila. Curr. Biol. 21, 746-750
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, 1335-1348 (Pubitemid 44749645)
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, 405-415
14. Collett, T.S., Collett, M. (2000) Path integration in insects. Curr. Opin. Neurobiol. 10, 757-762 (Pubitemid 32052543)
15. Davis, R.L. (2011) Traces of Drosophila memory. Neuron 70, 8-19
16. Davis, H.P., Squire, L.R. (1984) Protein synthesis and memory: a review. Psychol. Bull. 96, 518-559
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, 861-869
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, 316-24 (Pubitemid 34279811)
19. Erber, J., Kierzek, S., Sander, E., Grandy, K. (1998) Tactile learning in the honeybee. J. Comp. Physiol. A 183, 737-744 (Pubitemid 29020021)
20. Erber, J., Masuhr, T., Menzel, R. (1980) Localization of short-term memory in the brain of the bee, Apis mellifera. Physiol. Entomol. 5, 343-358
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, 355-365 (Pubitemid 27414152)
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, 5370-5380 (Pubitemid 36793266)
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, 145-159
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, 4460-4468 (Pubitemid 38608157)
25. Fujita, M., Tanimura, T. (2011) Drosophila evaluates and learns the nutritional value of sugars. Curr. Biol. 21, 751-755
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, 190-194 (Pubitemid 38446669)
27. Galizia, C.G., Menzel, R. (2000) Odour perception in honeybees: coding information in glomerular patterns. Curr. Opin. Neurobiol. 10, 504-510 (Pubitemid 30614512)
28. Gauthier, M. (2010) State of the art on insect nicotinic acetylcholine receptor function in learning and memory. Adv. Exp. Med. Biol. 683, 97-115
29. Giurfa, M. (2003) Cognitive neuroethology: dissecting non-elemental learning in a honeybee brain. Curr. Opin. Neurobiol. 13, 726-735 (Pubitemid 37518461)
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, 4384-4392 (Pubitemid 28243831)
31. Hammer, M. (1993) An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees. Nature 366, 59-63 (Pubitemid 23345235)
32. Hammer, M., Menzel, R. (1995) Learning and memory in the honeybee. J. Neurosci. 15, 1617-1630
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, 146-156 (Pubitemid 29108277)
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), 735-745 (Pubitemid 40876357)
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), 523-535 (Pubitemid 46852865)
36. Heisenberg, M., Borst, A., Wagner, S., Byers, D. (1985) Drosophila mushroom body mutants are deficient in olfactory learning. J. Neurogenet. 2, 1-30 (Pubitemid 15148068)
37. Hildebrandt, H., Müller, U. (1995a) PKA activity in the antennal lobe of honeybees is regulated by chemosensory stimulation in vivo. Brain Res. 679, 281-288
38. Hildebrandt, H., Müller, U. (1995b) Octopamine mediates rapid stimulation of protein kinase A in the antennal lobe of honeybees. J. Neurobiol. 27, 44-50
39. Kandel, E.R. (2001) The molecular biology of memory storage: a dialogue between genes and synapses. Science 294, 1030-1038 (Pubitemid 33041851)
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, 3103-3113 (Pubitemid 351442287)
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, 71-84 (Pubitemid 19201152)
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, 583-595 (Pubitemid 24297784)
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, 399-405 (Pubitemid 30064526)
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, 458-464
45. Leboulle, G., Müller, U. (2004) Synergistic activation of insect cAMP-dependent protein kinase A (type II) by cyclicAMP and cyclicGMP. FEBS Lett. 576, 216-220 (Pubitemid 39330486)
46. Lima, S.Q., Miesenböck, G. (2005) Remote control of behavior through genetically targeted photostimulation of neurons. Cell 121, 141-152
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, 11614-11618 (Pubitemid 43098454)
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, 49-53
49. McGuire, S.E., Roman, G., Davis, R.L. (2004) Gene expression systems in Drosophila: a synthesis of time and space. Trends Genet. 20, 384-391 (Pubitemid 38943029)
50. Menzel, R. (1999) Memory dynamics in the honeybee. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 185, 323-340 (Pubitemid 29532282)
51. Menzel, R. (2001) Searching for the memory trace in a mini-brain, the honeybee. Learn. Mem. 8, 53-62 (Pubitemid 32297801)
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.
53. Menzel, R., Giurfa, M. (2006) Dimensions of cognition in an insect, the honeybee. Behav. Cogn. Neurosci. Rev. 5, 24-40 (Pubitemid 43987739)
54. Menzel, R., Müller, U. (1996) Learning and memory in honeybees: from behavior to neural substrates. Annu. Rev. Neurosci. 19, 379-404 (Pubitemid 26080833)
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.
56. Müller, U. (1996) Inhibition of nitric oxide synthase impairs a distinct form of long-term memory in the honeybee, Apis mellifera. Neuron 16, 541-549 (Pubitemid 26101105)
57. Müller, U. (1997) The nitric oxide system in insects. Prog. Neurobiol. 51, 363-381 (Pubitemid 27143803)
58. Müller, U. (2000) Prolonged activation of cAMPdependent protein kinase during conditioning induces long-term memory in honeybees. Neuron 27, 159-168
59. Müller, U. (2002) Learning in honeybees: from molecules to behaviour. Zoology 105, 313-320
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, 2240-2248
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, 7817-7825
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, 1104-1107 (Pubitemid 24293080)
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, 489-500 (Pubitemid 28190207)
64. Rehder, V. (1989) Sensory pathways and motoneurons of the proboscis reflex in the suboesophageal ganglion of the honeybee. J. Comp. Neurol. 279, 499-513 (Pubitemid 19033001)
65. Riedel, G., Platt, B., Micheau, J. (2003) Glutamate receptor function in learning and memory. Behav. Brain Res. 140, 1-47 (Pubitemid 36313239)
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, 133-144
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, 1767-1779 (Pubitemid 39265913)
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, 1106-1117 (Pubitemid 34670872)
69. Sacktor, T.C. (2008) PKMzeta, LTP maintenance, and the dynamic molecular biology of memory storage. Prog. Brain Res. 169, 27-40 (Pubitemid 351451897)
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, 138-150 (Pubitemid 32802849)
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, 191-197 (Pubitemid 38125150)
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, 345-356
73. Srinivasan, M.V. (2011) Honeybees as a model for the study of visually guided flight, navigation, and biologically inspired robotics. Physiol. Rev. 91, 413-460
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, 3303-3313 (Pubitemid 41504770)
75. Toth, A.L., Robinson, G.E. (2007) Evo-devo and the evolution of social behavior. Trends Genet. 23, 334-341 (Pubitemid 46962801)
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), e288
77. Witthöft, W. (1967) Absolute Anzahl und Verteilung der Zellen im Hirn der Honigbiene. Z. Morphol. Oekol. Tiere. 61, 160-184
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, 4024-4033 (Pubitemid 350275042)
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, 2742-2745 (Pubitemid 28362582)
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, 603-615
81. Zannat, M.T., Locatelli, F., Rybak, J., Menzel, R., Leboulle, G. (2006) Identification and localization of the NR1 sub-unit homologue of the NMDA glutamate receptor in the honeybee brain. Neurosci. Lett. 398, 274-279 (Pubitemid 44274991)