APIS - A novel approach for conditioning honey bees

Frontiers in Behavioral Neuroscience

Volumn , Issue MAR, 2013, Pages

  Kirkerud, Nicholas H ^a   Wehmann, Henja Niniane ^a   Giovanni Galizia, C ^a,b   Gustav, David ^a  

^a UNIVERSITY OF KONSTANZ   (Germany)

^b UNIVERSITY OF ROME TOR VERGATA   (Italy)

Author keywords

Automatic conditioning; Automatic tracking; Aversive learning; Behaviour; Honey bee; Olfaction; Proboscis extension response; Short term memory

Indexed keywords

LINALOOL; NONANOL; PHEROMONE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; APPETITE; ARTICLE; ASSOCIATION; AUTOANALYSIS; AUTOMATIC PERFORMANCE INDEX SYSTEM; AVERSIVE BEHAVIOR; BEHAVIOR CONTROL; BEHAVIORAL SCIENCE; CONDITIONING; DATA PROCESSING; DECISION MAKING; ELECTRIC SHOCK; ESCAPE BEHAVIOR; HABITUATION; HONEYBEE; HORMONE RELEASE; INTERMETHOD COMPARISON; LEARNING; MENTAL CAPACITY; MOVEMENT (PHYSIOLOGY); NERVOUS SYSTEM PARAMETERS; NONHUMAN; ODOR; PROBOSCIS EXTENSION RESPONSE CONDITIONING; QUANTITATIVE ANALYSIS; REACTION TIME; REINFORCEMENT; RESPONSE TIME; SHORT TERM MEMORY; SOCIAL DISTANCE; STIMULUS RESPONSE; VELOCITY;

EID: 84875947528     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2013.00029     Document Type: Article

References (63)

1. Abbott, K.R. (2006). Bumblebees avoid flowers containing evidence of past predation events. Canadian Journal of Zoology-Revue Canadienne De Zoologie 84, 1240-1247.
2. Abbott, K.R., and Dukas, R. (2009). Honeybees consider flower danger in their waggle dance. Animal Behaviour 78, 633-635.
3. Abramson, C.I. (1986). Aversive conditioning in honeybees (Apis mellifera). Journal of Comparative Psychology 100, 108-116.
4. Abramson, C.I., and Boyd, B.J. (2001). An automated apparatus for conditioning proboscis extension in honey bees, Apis mellifera L. Journal of Entomological Science 36, 78-92.
5. Abramson, C.I., Miler, J., and Mann, D.W. (1982). An olfactory shuttle box and runway for insects. Journal of Mind and Behavior 3, 151-159.
6. Agarwal, M., Giannoni Guzmán, M., Morales-Matos, C., Del Valle Díaz, R.A., Abramson, C.I., and Giray, T. (2011). Dopamine and octopamine influence avoidance learning of honey bees in a place preference assay. PLoS ONE 6, e25371.
7. Bates, D., Maechler, M., and Bolker, B. (2011). lme4: Linear mixed-effects models using S4 classes, in: R package version 0.999375-42.).
8. Bhagavan, S., and Smith, B.H. (1997). Olfactory conditioning in the honey bee, Apis mellifera: Effects of odor intensity. Physiology & Behavior 61, 107-117.
9. Bitterman, M.E., Menzel, R., Fietz, A., and Schäfer, S. (1983). Classical conditioning of proboscis extension in honeybees (Apis mellifera). The journal of Comparative Psychology 97, 107-119.
10. Brembs, B. (2003). Operant conditioning in invertebrates. Current Opinion in Neurobiology 13, 710-717.
11. Brembs, B. (2008). Operant learning of Drosophila at the torque meter. Journal of Visualized Experiments, 731.
12. Butler, C.G., and Free, J.B. (1951). The behaviour of worker honeybees at the hive entrance. Behaviour 4, 262-291.
13. Carcaud, J., Roussel, E., Giurfa, M., and Sandoz, J.C. (2009). Odour aversion after olfactory conditioning of the sting extension reflex in honeybees. Journal of Experimental Biology 212, 620-626.
14. Cervantes-Sandoval, I., and Davis, R.L. (2012). Distinct traces for appetitive versus aversive olfactory memories in DPM neurons of Drosophila. Current Biology 22, 1247-1252.
15. Chabaud, M.A., Devaud, J.M., Pham-Delegue, M.H., Preat, T., and Kaiser, L. (2006). Olfactory conditioning of proboscis activity in Drosophila melanogaster. Journal of Comparative Physiology A 192, 1335-1348.
16. Chittka, L., and Niven, J. (2009). Are bigger brains better? Current Biology 19, R995-R1008.
17. Clarac, F., and Pearlstein, E. (2007). Invertebrate preparations and their contribution to neurobiology in the second half of the 20th century. Brain Research Reviews 54, 113-161.
18. Claridge-Chang, A., Roorda, R.D., Vrontou, E., Sjulson, L., Li, H., Hirsh, J., and Miesenbock, G. (2009). Writing memories with light-addressable reinforcement circuitry. Cell 139, 405-415.
19. Collins, A.M., and Blum, M.S. (1982). Bioassay of compounds derived from the honeybee sting. Journal of Chemical Ecology 8, 463-470.
20. Dukas, R. (2001). Effects of perceived danger on flower choice by bees. Ecology Letters 4, 327-333.
21. Dukas, R., and Morse, D.H. (2003). Crab spiders affect flower visitation by bees. Oikos 101, 157-163.
22. Eisenhardt, D., and Menzel, R. (2007). Extinction learning, reconsolidation and the internal reinforcement hypothesis. Neurobiology of Learning and Memory 87, 167-173.
23. Frost, E.H., Shutler, D., and Hillier, N.K. (2011). Effects of cold immobilization and recovery period on honeybee learning, memory, and responsiveness to sucrose. Journal of Insect Physiology 57, 1385-1390.
24. Gelman, A., Su, Y.-S., Yajima, M., Hill, J., Pittau, M.G., Kerman, J., and Zheng, T. (2012). arm: Data Analysis Using Regression and Multilevel/Hierarchical Models, in: R package version 1.5-05.).
25. Ghirlanda, S., and Enquist, M. (2003). A century of generalization. Animal Behaviour 66, 15-36.
26. Giurfa, M. (2003). Cognitive neuroethology: dissecting non-elemental learning in a honeybee brain. Current Opinion in Neurobiology 13, 726-735.
27. Giurfa, M., Fabre, E., Flaven-Pouchon, J., Groll, H., Oberwallner, B., Vergoz, V., Roussel, E., and Sandoz, J.C. (2009). Olfactory conditioning of the sting extension reflex in honeybees: Memory dependence on trial number, interstimulus interval, intertrial interval, and protein synthesis. Learning & Memory 16, 761-765.
28. Giurfa, M., and Sandoz, J.-C. (2012). Invertebrate learning and memory: Fifty years of olfactory conditioning of the proboscis extension response in honeybees. Learning & Memory 19, 54-66.
29. Grossmann, K.E. (1973). Continuous, fixed-ratio, and fixed-interval reinforcement in honey bees. Journal of the Experimental Analysis of Behavior 20, 105-109.
30. Guerrieri, F., Schubert, M., Sandoz, J.C., and Giurfa, M. (2005). Perceptual and neural olfactory similarity in honeybees. Plos Biology 3, 718-732.
31. Honjo, K., and Furukubo-Tokunaga, K. (2009). Distinctive neuronal networks and biochemical pathways for appetitive and aversive memory in Drosophila larvae. Journal of Neuroscience 29, 852-862.
32. Ings, T.C., and Chittka, L. (2008). Speed-accuracy tradeoffs and false alarms in bee responses to cryptic predators. Current Biology 18, 1520-1524.
33. Jones, E.I., and Dornhaus, A. (2011). Predation risk makes bees reject rewarding flowers and reduce foraging activity. Behavioral Ecology and Sociobiology 65, 1505-1511.
34. Ken, T., Hepburn, H.R., Radloff, S.E., Yu, Y.S., Liu, Y.Q., Zhou, D.Y., and Neumann, P. (2005). Heat-balling wasps by honeybees. Naturwissenschaften 92, 492-495.
35. Knudsen, J.T., Tollsten, L., and Bergstrom, L.G. (1993). Floral scents - a checklist of volatile compounds isolated by headspace techniques. Phytochemistry 33, 253-280.
36. Krashes, M.J., Dasgupta, S., Vreede, A., White, B., Armstrong, J.D., and Waddell, S. (2009). A neural circuit mechanism integrating motivational state with memory expression in Drosophila. Cell 139, 416-427.
37. Krashes, M.J., and Waddell, S. (2008). Rapid consolidation to a radish and protein synthesis-dependent long-term memory after single-session appetitive olfactory conditioning in Drosophila. Journal of Neuroscience 28, 3103-3113.
38. Matsumoto, Y., Menzel, R., Sandoz, J.C., and Giurfa, M. (2012). Revisiting olfactory classical conditioning of the proboscis extension response in honey bees: A step toward standardized procedures. Journal of Neuroscience Methods 211, 159-167.
39. Menzel, R. (1983). Neurobiology of learning and memory: the honeybee as a model system. Naturwissenschaften 70, 504-511.
40. Menzel, R. (1990). Learning, memory, and cognition in honey bees, in Neurobiology of comparative cognition - Comparative cognition and neuroscience, eds. R.P. Kesner & D.S. Olton. (Hillsdale, N.J.: L. Erlbaum Associates), 237-292.
41. Menzel, R. (2001). Searching for the memory trace in a mini-brain, the honeybee. Learning & Memory 8, 53-62.
42. Menzel, R., and Giurfa, M. (2001). Cognitive architecture of a mini-brain: the honeybee. Trends in Cognitive Sciences 5, 62-71.
43. Menzel, R., Manz, G., and Greggers, U. (2001). Massed and spaced learning in honeybees: the role of CS, US, the intertrial interval, and the test interval. Learning & Memory 8, 198-208.
44. Mota, T., Roussel, E., Sandoz, J.C., and Giurfa, M. (2011). Visual conditioning of the sting extension reflex in harnessed honeybees. Journal of Experimental Biology 214, 3577-3587.
45. Nieh, J.C. (2010). A negative feedback signal that is triggered by peril curbs honey bee recruitment. Current Biology 20, 310-315.
46. Núñez, J.A. (1970). The relationship between sugar flow and foraging and recruiting behaviour of honey bees (Apis mellifera L.). Animal Behaviour 18, Part 3, 527-538.
47. Núñez, J.A., Almeida, L., Balderrama, N., and Giurfa, M. (1997). Alarm pheromone induces stress analgesia via an opioid system in the honeybee. Physiology & Behavior 63, 75-80.
48. Pankiw, T., and Page, R.E. (2003). Effect of pheromones, hormones, and handling on sucrose response thresholds of honey bees (Apis mellifera L.). Journal of Comparative Physiology A 189, 675-684.
49. Pessotti, I. (1972). Discrimination with light stimuli and a lever-pressing response in Melipona rufiventris. Journal of Apicultural Research 11, 89-93.
50. Putz, G., and Heisenberg, M. (2002). Memories in Drosophila heat-box learning. Learning & Memory 9, 349-359.
51. R-Core-Team (2012). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
52. Sandoz, J.C., and Pham-Delegue, M.H. (2004). Spontaneous recovery after extinction of the conditioned proboscis extension response in the honeybee. Learning & Memory 11, 586-597.
53. Sattelle, D.B., and Buckingham, S.D. (2006). Invertebrate studies and their ongoing contributions to neuroscience. Invertebrate Neuroscience 6, 1-3.
54. Schwaerzel, 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. Journal of Neuroscience 23, 10495-15502.
55. Sigurdson, J.E. (1981). Automated discrete-trials techniques of appetitive conditioning in honey bees. Behavior Research Methods & Instrumentation 13, 1-10.
56. Smith, B.H., and Menzel, R. (1989). The use of electromyogram recordings to quantify odorant discrimination in the honey bee, Apis mellifera. Journal of Insect Physiology 35, 369-375.
57. Sokolowski, M.B.C., and Abramson, C.I. (2010). From foraging to operant conditioning: A new computer-controlled Skinner box to study free-flying nectar gathering behavior in bees. Journal of Neuroscience Methods 188, 235-242.
58. Stollhoff, N., Menzel, R., and Eisenhardt, D. (2005). Spontaneous recovery from extinction depends on the reconsolidation of the acquisition memory in an appetitive learning paradigm in the honeybee (Apis mellifera). Journal of Neuroscience 25, 4485-4492.
59. Tinbergen, N. (1932). Über die Orientierung des Bienenwolfes (Philanthus triangulum Fabr.). Zeitschrift für vergleichende Physiologie 16, 305-334.
60. Tully, T., and Quinn, W.G. (1985). Classical conditioning and retention in normal and mutant Drosophila melanogaster. Journal of Comparative Physiology A 157, 263-277.
61. Urlacher, E., Frances, B., Giurfa, M., and Devaud, J.-M. (2010). An alarm pheromone modulates appetitive olfactory learning in the honeybee (Apis mellifera). Frontiers in Behavioral Neuroscience 4, 1-10.
62. Vareschi, E. (1971). Duftunterscheidung bei der Honigbiene - Einzelzell-Ableitungen und Verhaltensreaktionen. Zeitschrift für vergleichende Physiologie 75, 143-173.
63. 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 2, e288.