Odour aversion after olfactory conditioning of the sting extension reflex in honeybees

Journal of Experimental Biology

Volumn 212, Issue 5, 2009, Pages 620-626

  Carcaud, Julie ^a   Roussel, Edith ^a   Giurfa, Martin ^a   Sandoz, Jean Christophe ^a  

^a CNRS   (France)

Author keywords

Appetitive learning; Aversive learning; Avoidance; Classical conditioning; Honeybee; Olfaction

Indexed keywords

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; ASSOCIATION; BEE; CONDITIONED REFLEX; ELECTROSTIMULATION; ODOR; PHYSIOLOGY; REFLEX; STIMULATION;

ANIMALS; BEES; BEHAVIOR, ANIMAL; CONDITIONING, CLASSICAL; CUES; ELECTRIC STIMULATION; ODORS; REFLEX; SMELL; STIMULATION, CHEMICAL;

ANIMALIA; APIS MELLIFERA; APOIDEA; HEXAPODA;

EID: 62849107371     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.026641     Document Type: Article

References (44)

1. Arenas, A., Fernandez, V. M. and Farina, W. M. (2007). Floral odor learning within the hive affects honeybees' foraging decisions. Naturwissenschaften 94, 218-222.
2. Bakchine-Huber, E., Pham-Delègue, M. H., Patte, F. and Masson, C. (1992). Modification d'une préférence olfactive après apprentissage chez l'abeille: influence de la nature du signal appris. C. R. Acad. Sci. III 314, 325-330.
3. Balderrama, N., Núñez, J., Guerrieri, F. and Giurfa, M. (2002). Different functions of two alarm substances in the honeybee. J. Comp. Physiol. A 188, 485-491.
4. Bitterman, M. E., Menzel, R., Fietz, A. and Schäfer, S. (1983). Classical conditioning of proboscis extension in honeybees (Apis mellifera). J. Comp. Psychol. 97, 107-119.
5. Breed, M. D., Guzman-Novoa, E. and Hunt, G. J. (2004). Defensive behavior of honey bees: organization, genetics, and comparison with other bees. Annu. Rev. Entomol. 49, 271-298.
6. Chaffiol, A., Laloi, D. and Pham-Delègue, M. H. (2005). Prior classical olfactory conditioning improves odour-cued flight orientation of honeybees in a wind tunnel. J. Exp. Biol. 208, 3731-3737.
7. Dupuy, F., Sandoz, J. C., Giurfa, M. and Josens, R. (2006). Individual olfactory learning in Camponotus ants. Anim. Behav. 72, 1081-1091.
8. Farina, W. M., Grüter, C. and Diaz, P. C. (2005). Social learning of floral odours inside the honeybee hive. Proc. Biol. Sci. 272, 1923-1928.
9. Farooqui, T., Robinson, K., Vaessin, H. and Smith, B. H. (2003). Modulation of early olfactory processing by an octopaminergic reinforcement pathway in the honeybee. J. Neurosci. 23, 5370-5380.
10. Frings, H. (1944). The loci of olfactory end-organs in the honey-bee, Apis mellifera L. J. Exp. Zool. 97, 123-134.
11. Gerber, B., Geberzahn, N., Hellstern, F., Klein, J., Kowalsky, O., Wüstenberg, D. and Menzel, R. (1996). Honey bees transfer olfactory memories established during flower visits to a proboscis extension paradigm in the laboratory. Anim. Behav. 52, 1079-1085.
12. Gerber, B., Tanimoto, H. and Heisenberg, M. (2004). An engram found? Evaluating the evidence from fruit flies. Curr. Opin. Neurobiol. 14, 737-744.
13. Gil, M. and De Marco, R. J. (2005). Olfactory learning by means of trophallaxis in Apis mellifera. J. Exp. Biol. 208, 671-680.
14. Giurfa, M. (2007). Behavioral and neural analysis of associative learning in the honeybee: a taste from the magic well. J. Comp. Physiol. A 193, 801-824.
15. Guerrieri, F., Schubert, M., Sandoz, J. C. and Giurfa, M. (2005). Perceptual and neural olfactory similarity in honeybees. PLOS Biol. 3, 1-14.
16. Hammer, M. and Menzel, R. (1998). Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees. Learn. Mem. 5, 146-156.
17. Haney, J. and Lukowiak, K. (2001). Context learning and the effect of context on memory retrieval in Lymnaea. Learn. Mem. 8, 35-43.
18. Kilpatrick, L. and Cahill, L. (2003). Modulation of memory consolidation for olfactory learning by reversible inactivation of the basolateral amygdala. Behav. Neurosci. 117, 184-188.
19. Kirsch, I., Lynn, S. J., Vigorito, M. and Miller, R. R. (2004). The role of cognition in classical and operant conditioning. J. Clin. Psychol. 60, 369-392.
20. Lewis, W. J. and Takasu, K. (1990). Use of learned odors by a parasitic wasp in accordance with host and food needs. Nature 348, 635-636.
21. Lunney, G. H. (1970). Using analysis of variance with a dichotomous dependent variable: an empirical study. J. Educ. Meas. 7, 263-269.
22. Menzel, R. (1999). Memory dynamics in the honeybee. J. Comp. Physiol. A 185, 323-340.
23. Núñez, J., Maldonado, H., Miralto, A. and Balderrama, N. (1983). The stinging response of the honeybee: effects of morphine, naloxone and some opioid peptides. Pharmacol. Biochem. Behav. 19, 921-924.
24. Núñez, J., Almeida, L., Balderrama, N. and Giurfa, M. (1998). Alarm pheromone induces stress analgesia via an opioid system in the honeybee. Physiol. Behav. 63, 75-80.
25. Okutani, F., Yagi, F. and Kaba, H. (1999). Gabaergic control of olfactory learning in young rats. Neurosci. 93, 1297-1300.
26. Page, R. E., Scheiner, R., Erber, J. and Amdam, G. V. (2006). The development and evolution of division of labor and foraging specialization in a social insect (Apis mellifera L.). Curr. Top. Dev. Biol. 74, 253-286.
27. Reinhard, J., Srinivasan, M. V., Guez, D. and Zhang, S. W. (2004). Floral scents induce recall of navigational and visual memories in honeybees. J. Exp. Biol. 207, 4371-4381.
28. Rescorla, R. A. (1988). Behavioral studies of Pavlovian conditioning. Annu. Rev. Neurosci. 11, 329-352.
29. Roussel, E., Carcaud, J., Sandoz, J. C. and Giurfa, M. (2009). Reappraising social insect behavior through aversive responsiveness and learning. PLoS ONE 4, e4197.
30. Sandoz, J. C., Roger, B. and Pham-Delègue, M. H. (1995). Olfactory learning and memory in the honeybee: comparison of different classical conditioning procedures of the proboscis extension response. C. R. Acad. Sci. III 318, 749-755.
31. Sandoz, J. C., Laloi, D., Odoux, J. F. and Pham-Delègue, M. H. (2000). Olfactory information transfer in the honey bees: compared efficiency of classical conditionning and early exposure. Anim. Behav. 59, 1025-1034.
32. Scheiner, R., Erber, J. and Page, R. E., Jr (1999). Tactile learning and the individual evaluation of the reward in honey bees (Apis mellifera L.). J. Comp. Physiol. A 185, 1-10.
33. Scheiner, R., Page, R. E., Jr and 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.
34. Schroll, C., Riemensperger, T., Bucher, D., Ehmer, J., Völler, T., Erbguth, K., Gerber, B., Hendel, T., Nagel, G., Buchner, E. et al. (2006). Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae. Curr. Biol. 16, 1471-1747.
35. Schwärzel, M., Monastirioti, M., Scholz, H., Friggi-Grelin, F., Birman, S. and Heisenberg, M. (2003). Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila. J. Neurosci. 23, 10495-10502.
36. Seeley, T. D. (1995). The Wisdom of the Hive. Cambridge, MA: Harvard University Press.
37. Shafir, S., Wiegmann, D. D., Smith, B. H. and Real, L. A. (1999). Risk-sensitive foraging: choice behaviour of honeybees in response to variability in volume of reward. Anim. Behav. 57, 1055-1061.
38. Takeda, K. (1961). Classical conditioned response in the honeybee. J. Insect Physiol. 6, 168-179.
39. Tully, T. and Quinn, W. G. (1985). Classical conditioning and retention in normal and mutant Drosophila melanogaster. J. Comp. Physiol. A 157, 263-277.
40. Unoki, S., Matsumoto, Y. and Mizunami, M. (2005). Participation of octopaminergic reward system and dopaminergic punishment system in insect olfactory learning revealed by pharmacological study. Eur. J. Neurosci. 22, 1409-1416.
41. Unoki, S., Matsumoto, Y. and Mizunami, M. (2006). Roles of octopaminergic and dopaminergic neurons in mediating reward and punishment signals in insect visual learning. Eur. J. Neurosci. 24, 2031-2038.
42. Vergoz, V., Roussel, E., Sandoz, J. C. and Giurfa, M. (2007). Aversive learning in honeybees revealed by the olfactory conditioning of the sting extension reflex. PLoS One 3, e288.
43. von Frisch, K. (1946). Die Tänze der Bienen. Öst. Zool. Zeitschr. 1, 1-48.
44. Winston, M. L. (1987). The Biology of the Honey Bee. Cambridge, MA: Harvard University Press.