Learning in honeybees: From molecules to behaviour

Zoology

Volumn 105, Issue 4, 2002, Pages 313-320

  Müller, Uli ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Antennal lobes; Associative learning; Memory; Protein kinases; Second messenger cascades

Indexed keywords

ANIMALIA; APIS MELLIFERA; AVES; HEXAPODA; INSECTA; MAMMALIA; MOLLUSCA;

EID: 0036997058     PISSN: 09442006     EISSN: None     Source Type: Journal    
DOI: 10.1078/0944-2006-00075     Document Type: Conference Paper

References (40)

1. Abel, T., P. V. Nguyen, M. Barad, T. A. S. Deuel, E. R. Kandel and R. Bourtchouladze. 1997. Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory. Cell 88: 615-626.
2. Abel, T., K. C. Martin, D. Bartsch and E. R. Kandel. 1998. Memory suppressor genes: Inhibitory constraints on the storage of long-term memory. Science 279: 338-341.
3. Bitterman, M. E., R. Menzel, A. Fietz and S. Schäfer. 1983. Classical olfactory conditioning of proboscis extension in honeybees (Apis mellifera). J. Comp. Physiol. 97: 107-119.
4. Byrne, J. H. and E. R. Kandel. 1996. Presynaptic facilitation revisited: state and time dependence. J. Neurosci. 16: 425-435.
5. Carew, T. J. 1996. Molecular enhancement of memory formation. Neuron 16: 5-8.
6. Davis, R. L. 1993. Mushroom bodies and Drosophila learning. Neuron 11: 1-14.
7. Davis, R. L. 1996. Physiology and biochemistry of Drosophila learning mutants. Physiol. Rev. 76: 299-317.
8. DeZazzo, J. and T. Tully. 1995. Dissection of memory formation: from behavioral pharmacology to molecular genetics. Trends Neurosci. 18: 212-218.
9. Dubnau, J. and T. Tully. 1998. Gene discovery in Drosophila: New insights for learning and memory. Annu. Rev. Neurosci. 21: 407-444.
10. Ebbinghaus, M. 1885. Über das Gedächtnis. Buehler, Leipzig.
11. Erber, J., T. Masuhr and R. Menzel. 1980. Localization of short-term memory in the brain of the bee, Apis mellifera. Physiol. Entomol. 5: 343-358.
12. Frey, U., Y. Y. Huang and E. R. Kandel. 1993. Effect of cAMP simulates a late stage of LTP in hippocampal CA1 neurons. Science 260: 1661-1664.
13. Galizia, C. G. and R. Menzel. 2000. Odour perception in honey bees: coding information in glomerular patterns. Curr. Opin. Neurobiol. 10: 504-510.
14. Grünbaum, L. and U. Müller. 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.
15. Hammer, M. 1993. An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees. Nature 366: 59-63.
16. Hammer, M. and R. Menzel. 1995. Learning and memory in the honeybee. J. Neurosci. 15: 1617-1630.
17. Hammer, M. and R. Menzel. 1998. Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees. Learn. Mem. 5: 146-156.
18. Hildebrandt, H. and U. Müller. 1995a. Octopamine mediates rapid stimulation of PKA in the antennal lobe of honeybees. J. Neurobiol. 27: 44-50.
19. Hildebrandt, H. and U. Müller. 1995b. PKA activity in the antennal lobe of honeybees is regulated by chemosensory stimulation in vivo. Brain Res. 679: 281-288.
20. Huang, Y.-Y., E. R. Kandel, L. Varshavsky, E. P. Brandon, M. Qi, R. L. Idzerda, G. S. McKnight and R. Bourtchouladze. 1995. A genetic test of the effects of mutations in PKA of mossy fiber LTP and its relation to spatial and contextual learning. Cell 83: 1211-1222.
21. Joerges, J., A. Küttner, G. Galizia and R. Menzel. 1997. Representations of odours and odour mixtures visualized in the honeybee brain. Nature 387: 285-288.
22. Kogan, J. H., P. W. Frankland, J. A. Blendy, J. Coblentz, Z. Marowitz, G. Schütz and A. J. Silva. 1997. Spaced training induces normal long-term memory in CREB mutant mice. Curr. Biol. 7: 1-11.
23. Kuwabara, M. 1957. Bildung des bedingten Reflexes von Pavlov Typus bei der Honigbiene, Apis mellifera. J. Fac. Sci. Hokkaido Univ. Ser. VI Zool. 13: 458-464.
24. Kreissl, S., S. Eichmüller, G. Bicker, J. Rapus and M. Eckert. 1994. Octopamine-like immunoreactivity in the brain and suboesophageal ganglion of the honeybee. J. Comp. Neurol. 348: 583-595.
25. Menzel, R. 1990. Learning, memory and "cognition" in honey bees. In: Neurobiology of Comparative Cognition (R.P. Kesner and D.S. Olten, eds.). Erlbaum, Inc., Hillsdale NY, pp. 237-292.
26. Menzel, R. 1999. Memory dynamics in the honeybee. J. Comp. Physiol. A 185: 323-340.
27. Menzel, R. and U. Müller. 1996. Learning and memory in honeybees: from behavior to neural substrates. Annu. Rev. Neurosci. 19: 379-404.
28. Menzel, R., J. Erber and T. Masuhr. 1974. Learning and memory in the honeybee. In: Experimental analysis of insect behaviour (L.B. Browne, ed.). Springer Verlag, Berlin, pp. 195-217.
29. 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.
30. 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: 33-44.
31. Müller, U. 2000. Prolonged activation of cAMP-dependent protein kinase during conditioning induces long-term memory in honeybees. Neuron 27: 159-168.
32. Müller, U. and T. J. Carew. 1998. Serotonin induces temporally and mechanistically distinct phases of persistent PKA activity in Aplysia sensory neurons. Neuron 21: 1423-1434.
33. Olds J. L., S. Golski, D. L. McPhie, D. Olton, M. Mishkin and D. L. Alkon. 1990. Discrimination learning alters the distribution of protein kinase C in the hippocampus of rats. J. Neurosci. 10: 3707-3713.
34. Roberson, E. D., J. D. English and J. D. Sweatt. 1996. A biochemist's view of long-term potentiation. Learn. Mem. 3: 1-24.
35. Silva A. J., J. H. Kogan, P. W. Frankland and S. Kida. 1998. CREB and memory. Annu. Rev. Neurosci. 21: 127-148.
36. Sutton, M. A., J. Ide, S. E. Masters and T. J. Carew. 2002. Interaction between amount and pattern of training in the induction of intermediate- and long-term memory for sensitization in Aplysia. Learn. Mem. 9: 29-40.
37. Tully, T., T. Preat, S. C. Boynton and M. Del Vecchio. 1994. Genetic dissection of consolidated memory in Drosophila. Cell 79: 35-47.
38. Van der Zee E. A., J. C. Compaan, M. de Boer and P. G. M. Luiten. 1992 Changes in PKC immunoreactivity in mouse hippocampus induced by spatial discrimination learning. J. Neurosci. 12: 4808-4815.
39. von Frisch, K. 1967. The dance language and orientation of bees. Harvard Univ. Press, Cambridge, MA.
40. Yin, J. C. P. and T. Tully. 1996. CREB and the formation of long-term memory. Curr. Opin. Neurobiol. 6: 264-268.