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Journal of Comparative Physiology A

, Volume 193, Issue 8, pp 801–824 | Cite as

Behavioral and neural analysis of associative learning in the honeybee: a taste from the magic well

  • Martin Giurfa
Review

Abstract

Equipped with a mini brain smaller than one cubic millimeter and containing only 950,000 neurons, honeybees could be indeed considered as having rather limited cognitive abilities. However, bees display a rich and interesting behavioral repertoire, in which learning and memory play a fundamental role in the framework of foraging activities. We focus on the question of whether adaptive behavior in honeybees exceeds simple forms of learning and whether the neural mechanisms of complex learning can be unraveled by studying the honeybee brain. Besides elemental forms of learning, in which bees learn specific and univocal links between events in their environment, bees also master different forms of non-elemental learning, including categorization, contextual learning and rule abstraction, both in the visual and in the olfactory domain. Different protocols allow accessing the neural substrates of some of these learning forms and understanding how complex problem solving can be achieved by a relatively simple neural architecture. These results underline the enormous richness of experience-dependent behavior in honeybees, its high flexibility, and the fact that it is possible to formalize and characterize in controlled laboratory protocols basic and higher-order cognitive processing using an insect as a model.

Keywords

Perception Cognition Learning Memory Honeybee 

Abbreviations

AL

Antennal lobe

CS

Conditioned stimulus

DMTS

Delayed matching-to-sample

DNMTS

Delayed non matching-to-sample

MB

Mushroom body

mRNA

Messenger ribonucleic acid

PER

Proboscis extension reflex

RNAi

Ribonucleic acid interference

SER

Sting extension reflex

US

Unconditioned stimulus

VUMmx1

Ventral unpaired median neuron of the maxillary neuromere 1

Notes

Acknowledgments

I thank JM Devaud, JC Sandoz and R Menzel for helpful criticisms on previous versions of this manuscript. I also thank all the members of my research team at the University of Toulouse for providing a stimulating and productive environment. Thanks are also due to the CNRS, the University of Toulouse and the Institut Universitaire de France for much support.

References

  1. Abel R, Rybak J, Menzel R (2001) Structure and response patterns of olfactory interneurons in the honeybee, Apis mellifera. J Comp Neurol 437:363–383PubMedCrossRefGoogle Scholar
  2. Alvarado MC, Bachevalier J (2005) Selective neurotoxic damage to the hippocampal formation impairs performance of the transverse patterning and location memory tasks in rhesus macaques. Hippocampus 15:118–131PubMedCrossRefGoogle Scholar
  3. Altman JS, Kien J (1987) Functional organization of the subesophageal ganglion in arthropods. In: Gupta AP (ed) Arthropod brain: its evolution, development, structure and function. Wiley, New York, pp 265–301Google Scholar
  4. Benard J, Giurfa M (2004) A test of transitive inferences in free-flying honeybees: unsuccessful performance due to memory constraints. Learn Mem 11:328–336PubMedCrossRefGoogle Scholar
  5. Benard J, Stach S, Giurfa M (2006) Categorization of visual stimuli in the honeybee Apis mellifera. Anim Cogn 9:257–270PubMedCrossRefGoogle Scholar
  6. Bitterman ME, Menzel R, Fietz A, Schäfer S (1983) Classical conditioning of proboscis extension in honeybees (Apis mellifera). J Comp Psychol 97:107–119PubMedCrossRefGoogle Scholar
  7. Blaser RE, Couvillon PA, Bitterman ME (2004) Backward blocking in honeybees. Q J Exp Psychol B 57:349–360PubMedCrossRefGoogle Scholar
  8. Bolles RC (1970) Specifies-specific defense reactions and avoidance learning. Psychol Rev 77:32–48CrossRefGoogle Scholar
  9. Borlikova GG, Elbers NA, Stephens DN(2006). Repeated withdrawal from ethanol spares contextual fear conditioning and spatial learning but impairs negative patterning and induces over-responding: evidence for effect on frontal cortical but not hippocampal function? Eur J Neurosci 24:205–216PubMedCrossRefGoogle Scholar
  10. Bucci DJ, Saddoris MP, Burwell RD (2002) Contextual fear discrimination is impaired by damage to the postrhinal or perirhinal cortex. Behav Neurosci 116:479–488PubMedCrossRefGoogle Scholar
  11. Buffon (Leclerc G.L.a) (1749a) Histoire naturelle générale et particulière: avec la description du cabinet du Roy. Imprimerie Royale, Paris, vol IIGoogle Scholar
  12. Buffon (Leclerc G.L.b) (1749b) Histoire naturelle générale et particulière: avec la description du cabinet du Roy. Imprimerie Royale, Paris, vol IVGoogle Scholar
  13. Chandra S, Smith BH (1998) An analysis of synthetic processing of odor mixtures in the honeybee. J Exp Biol 201:3113–3121PubMedGoogle Scholar
  14. Chittka L, Thomson JD, Waser NM (1999) Flower constancy, insect psychology, and plant evolution. Naturwissenschaften 86:361–377CrossRefGoogle Scholar
  15. Cheng K, Wignall AE (2006) Honeybees (Apis mellifera) holding on to memories: response competition causes retroactive interference effects. Anim Cogn 9:141–150PubMedCrossRefGoogle Scholar
  16. Collett TS, Collett M (2002) Memory use in insect visual navigation. Nat Rev Neurosci 3:542–552PubMedCrossRefGoogle Scholar
  17. Collett TS, Graham P, Durier V (2003) Route learning by insects. Curr Opin Neurobiol 13:718–725PubMedCrossRefGoogle Scholar
  18. Couvillon PA, Bitterman ME (1980) Some phenomena of associative learning in honey bees. J Comp Physiol Psychol 94:878–885CrossRefGoogle Scholar
  19. Couvillon PA, Klosterhalfen S, Bitterman ME (1983) Analysis of overshadowing in honeybees. J Comp Psychol 97:154–166CrossRefGoogle Scholar
  20. Couvillon PA, Arakaki L, Bitterman ME (1997) Intramodal blocking in honeybees. Anim Learn Behav 25:277–282Google Scholar
  21. Dacher M, Lagarrigue A, Gauthier M (2005) Antennal tactile learning in the honeybee: effect of nicotinic antagonists on memory dynamics. Neuroscience 130:37–50PubMedCrossRefGoogle Scholar
  22. de Brito Sanchez MG, Giurfa M, de Paula Mota TR, Gauthier M (2005) Electrophysiological and behavioural characterization of gustatory responses to antennal ‘bitter’ taste in honeybees. Eur J Neurosci 22:3161–3170PubMedCrossRefGoogle Scholar
  23. Deisig N, Lachnit H, Hellstern F, Giurfa M (2001) Configural olfactory learning in honeybees: negative and positive patterning discrimination. Learn Mem 8:70–78PubMedCrossRefGoogle Scholar
  24. Deisig N, Lachnit H, Giurfa M (2002) The effect of similarity between elemental stimuli and compounds in olfactory patterning discriminations. Learn Mem 9:112–121PubMedCrossRefGoogle Scholar
  25. Deisig N, Lachnit H, Sandoz JC, Lober K, Giurfa M (2003) A modified version of the unique cue theory accounts for olfactory compound processing in honeybees. Learn Mem 10:199–208PubMedCrossRefGoogle Scholar
  26. Deisig N, Giurfa M, Lachnit H, Sandoz JC (2006) Neural representation of olfactory mixtures in the honeybee antennal lobe. Eur J Neurosci 24:1161–1174PubMedCrossRefGoogle Scholar
  27. Delius JD, Jitsumori M, Siemann M (2000) Stimulus equivalences through discrimination reversals. In: Heyes C, Huber L (eds) The evolution of cognition. MIT Press, Cambridge, pp 103–122Google Scholar
  28. Erber J, Kierzek S, Sander E, Grandy K (1998) Tactile learning in the honeybee. J Comp Physiol A 183:737–744CrossRefGoogle Scholar
  29. Faber T, Joerges J, Menzel R (1999) Associative learning modifies neural representations of odors in the insect brain. Nature Neurosci 2:74–78PubMedCrossRefGoogle Scholar
  30. Faber T, Menzel R (2001) Visualizing mushroom body response to a conditioned odor in honeybees. Naturwissenschaften 88:472–476PubMedCrossRefGoogle Scholar
  31. Fanselow MS (1980) Conditioned and unconditional components of post-shock freezing. Pavlov J Biol Sci 15:177–182PubMedGoogle Scholar
  32. Farina W, Gruter C, Diaz PC (2005) Social learning of floral odours inside the honeybee hive. Proc Biol Sci 272:1923–1928PubMedCrossRefGoogle Scholar
  33. Farina W, Gruter C, Acosta L, Mc Cabe S (2006) Honeybees learn floral odors while receiving nectar from foragers within the hive. Naturwissenschaften 94:55–60PubMedCrossRefGoogle Scholar
  34. Farooqui T, Robinson K, Vaessin H, Smith BH (2003) Modulation of early olfactory processing by an octopaminergic reinforcement pathway in the honeybee. J Neurosci 23:5370–5380PubMedGoogle Scholar
  35. Fersen Lv, Wynne CDL, Delius JD (1990) Deductive reasoning in pigeons. Naturwissenschaften 77:548–549CrossRefGoogle Scholar
  36. Fiala A, Müller U, Menzel R (1999) Reversible down regulation of protein kinase A during olfactory learning using antisense technique impairs long-term memory formation in the honeybee Apis mellifera. J Neurosci 19:10125–10134PubMedGoogle Scholar
  37. Frisch Kv (1914) Der Farbensinn und Formensinn der Biene. Zool Jb Physiol 37:1–238Google Scholar
  38. Frisch Kv (1962) Dialects in the language of the bees. Sci Amer 207:78–87CrossRefGoogle Scholar
  39. Frisch Kv (1967) The dance language and orientation of bees. Belknap Press, CambridgeGoogle Scholar
  40. Galizia CG, Menzel R (2000) Odour perception in honeybees: coding information in glomerular patterns. Curr Opin Neurobiol 10:504–510PubMedCrossRefGoogle Scholar
  41. Galizia CG, Nägler K, Hölldobler B, Menzel R (1998) Odour coding is bilaterally symmetrical in the antennal lobes of honeybees (Apis mellifera). Eur J Neurosci 10:2964–2974PubMedCrossRefGoogle Scholar
  42. Galizia CG, Sachse S, Rappert A, Menzel R (1999) The glomerular code for odor representation is species specific in the honeybee Apis mellifera. Nat Neurosci 2:473–478PubMedCrossRefGoogle Scholar
  43. Gerber B, Ullrich J (1999) No evidence for olfactory blocking in honeybee classical conditioning. J Exp Biol 202:1839–1854PubMedGoogle Scholar
  44. Gil M, de Marco RJ (2005) Olfactory learning by means of trophallaxis in Apis mellifera. J Exp Biol 208:671–680PubMedCrossRefGoogle Scholar
  45. Gil M, de Marco RJ (2006) Apis mellifera bees acquire long-term olfactory memories within the colony. Biol Lett 2:98–100PubMedCrossRefGoogle Scholar
  46. Giurfa M (2003) Cognitive neuroethology: dissecting non-elemental learning in a honeybee brain. Curr Opin Neurobiol 13:726–735PubMedCrossRefGoogle Scholar
  47. Giurfa M (2006) Associative learning: the instructive function of biogenic amines. Curr Biol 16:R892–R895PubMedCrossRefGoogle Scholar
  48. Giurfa M, Malun D (2004) Associative mechanosensory conditioning of the proboscis extension reflex in honeybees. Learn Mem 11:294–302PubMedCrossRefGoogle Scholar
  49. Giurfa M, Menzel R (1997) Insect visual perception: complex abilities of simple nervous systems. Curr Opin Neurobiol 7:505–513PubMedCrossRefGoogle Scholar
  50. Giurfa M, Lehrer M (2001) Honeybee vision and floral displays: from detection to close-up recognition. In: Chittka L, Thomson J (eds) Cognitive ecology of pollination. Cambridge University Press, Cambridge, pp 61–82Google Scholar
  51. Giurfa M, Eichmann B, Menzel R (1996) Symmetry perception in an insect. Nature 382:458–461CrossRefPubMedGoogle Scholar
  52. Giurfa M, Núñez JA, Chittka L, Menzel R (1995). Colour preferences of flower-naive honeybees. J Comp Physiol A 177:247–259CrossRefGoogle Scholar
  53. Giurfa M, Hammer M, Stach S, Stollhoff N, Müller-Deisig N, Mizyrycki C (1999) Pattern learning by honeybees: conditioning procedure and recognition strategy. Anim Behav 57:315–324PubMedCrossRefGoogle Scholar
  54. Giurfa M, Zhang S, Jenett A, Menzel R, Srinivasan MV (2001) The concepts of ‘sameness’ and ‘difference’ in an insect. Nature 410:930–933PubMedCrossRefGoogle Scholar
  55. Giurfa M, Schubert M, Reisenman C, Gerber B, Lachnit H (2003) The effect of cumulative experience on the use of elemental and configural visual discrimination strategies in honeybees. Behav Brain Res 145:161–169PubMedCrossRefGoogle Scholar
  56. Grant V (1951) The fertilization of flowers. Sci Amer 12:1–6Google Scholar
  57. Guerrieri F, Schubert M, Sandoz JC, Giurfa M (2005a) Perceptual and neural olfactory similarity in honeybees. PLoS Biol 3(4):e60PubMedCrossRefGoogle Scholar
  58. Guerrieri F, Lachnit H, Gerber B, Giurfa M (2005b) Olfactory blocking and odorant similarity in the honeybee. Learn Mem 12:86–95PubMedCrossRefGoogle Scholar
  59. Hammer M (1993) An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees. Nature 366:59–63CrossRefGoogle Scholar
  60. 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
  61. Harnard S (1987) Categorical perception. The groundwork of cognition. Cambridge University Press, CambridgeGoogle Scholar
  62. Hateren JH v, Srinivasan MV, Wait PB (1990) Pattern recognition in bees: orientation discrimination. J Comp Physiol A 197:649–654Google Scholar
  63. Haupt SS (2004) Antennal sucrose perception in the honey bee (Apis mellifera L.): behaviour and electrophysiology. J Comp Physiol A 190:735–745CrossRefGoogle Scholar
  64. Hellstern F, Wüstenberg D, Hammer M (1995) Contextual learning in honeybees under laboratory conditions. In: Elsner N, Menzel R (eds) Proceedings of the 23rd Göttingen Neurobiology Conference on Learning and Memory. Georg Thieme Verlag, Stuttgart, p. 30Google Scholar
  65. Hori S, Takeuchi H, Arikawa K, Kinoshita M, Ichikawa N, Sasaki M, Kubo T (2006) Associative visual learning, color discrimination, and chromatic adaptation in the harnessed honeybee Apis mellifera L. J Comp Physiol A 192:691–700CrossRefGoogle Scholar
  66. Hosler JS, Smith BH (2000) Blocking and the detection of odor components in blends. J Exp Biol 203:2797–2806PubMedGoogle Scholar
  67. Huber R (2005). Amines and motivated behaviors: a simpler systems approach to complex behavioral phenomena. J Comp Physiol A 191:231–239CrossRefGoogle Scholar
  68. Jacobs LF (2006) From movement to transitivity: the role of hippocampal parallel maps in configural learning. Rev Neurosci 17:99–109PubMedGoogle Scholar
  69. Joerges J, Küttner A, Galizia CG, Menzel R (1997) Representation of odours and odour mixtures visualized in the honeybee brain. Nature 387:285–288CrossRefGoogle Scholar
  70. Kien J, Menzel R (1977) Chromatic properties of interneurons in the optic lobes of the bee. II. Narrow band and colour opponent neurons. J Comp Physiol A 113:35–53CrossRefGoogle Scholar
  71. Kisch J, Erber J (1999) Operant conditioning of antennal movements in the honey bee. Behav Brain Res 99:93–102PubMedCrossRefGoogle Scholar
  72. Komischke B, Sandoz JC, Lachnit H, Giurfa M (2003) Non-elemental processing in olfactory discrimination tasks needs bilateral input in honeybees. Behav Brain Res 145:135–143PubMedCrossRefGoogle Scholar
  73. Komischke B, Sandoz JC, Malun D, Giurfa M (2005) Partial unilateral lesions of the mushroom bodies affect olfactory learning in honeybees Apis mellifera L. Eur J Neurosci 21:477–485PubMedCrossRefGoogle Scholar
  74. 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
  75. 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
  76. Laurent G, Wehr M, Davidowitz H (1996) Temporal representations of odors in an olfactory network. J Neurosci 16:3837–3847PubMedGoogle Scholar
  77. Leadbeater E, Chittka L (2005) A new mode of information transfer in foraging bumblebees? Curr Biol 15:R447–R448PubMedCrossRefGoogle Scholar
  78. Lehrer M (1997) Honeybee’s visual orientation at the feeding site. In: Lehrer M (eds) Orientation and communication in arthropods. Birkhäuser, Basel, pp 115–144Google Scholar
  79. Libersat F, Pflüger HJ (2004) Monoamines and the orchestration of behavior. Bioscience 54:17–25CrossRefGoogle Scholar
  80. Malun D (1998) Early development of mushroom bodies in the brain of the honeybee Apis mellifera as revealed by BrdU incorporation and ablation experiments. Learn Mem 5:90–101PubMedGoogle Scholar
  81. Malun D, Giurfa M, Galizia CG, Plath N, Brandt R, Gerber B, Eisermann B (2002) Hydroxyurea-induced partial mushroom body ablation does not affect acquisition and retention of olfactory differential conditioning in honeybees. J Neurobiol 53:343–360PubMedCrossRefGoogle Scholar
  82. Menzel R (1967) Untersuchungen zum Erlernen von Spektralfarben durch die Honigbiene (Apis mellifica). Z vergl Physiol 56:22–62CrossRefGoogle Scholar
  83. Menzel R (1968) Das Gedächtnis der Honigbiene für Spektralfarben. I. Kurzzeitiges und langzeitiges Behalten. Z vergl Physiol 60:82–102CrossRefGoogle Scholar
  84. Menzel R (1985) Learning in honey bees in an ecological and behavioral context. In: Hölldobler B, Lindauer M (eds) Experimental behavioral ecology and sociobiology. Fischer, Stuttgart, pp 55–74Google Scholar
  85. Menzel R (1999) Memory dynamics in the honeybee. J Comp Physiol A 185:323–340CrossRefGoogle Scholar
  86. Menzel R (2001) Searching for the memory trace in a mini-brain, the honeybee. Learn Mem 8:53–62PubMedCrossRefGoogle Scholar
  87. Menzel R, Backhaus W (1991) Colour vision in insects. In: Gouras P (ed) Vision and visual dysfunction. The perception of colour. MacMillan Press, London, pp 262–288Google Scholar
  88. Menzel R, Erber J (1978) Learning and memory in bees. Sci Amer 239:80–87Google Scholar
  89. Menzel R, Giurfa M (2001) Cognitive architecture of a mini-brain: the honeybee. Trends Cogn Sci 5:62–71PubMedCrossRefGoogle Scholar
  90. Menzel R, Manz G, Menzel R, Greggers U (2001) Massed and spaced learning in honeybees: the role of CS, US, the intertrial interval, and the test interval. Learn Mem 8:198–208PubMedCrossRefGoogle Scholar
  91. Menzel R, Greggers U, Hammer M (1993) Functional organization of appetitive learning and memory in a generalist pollinator, the honey bee. In: Papaj D, Lewis AC (eds) Insect learning: ecological and evolutionary perspectives. Chapman and Hall, New York, pp 79–125Google Scholar
  92. Moses SN, Cole C, Driscoll I, Ryan J (2005) Differential contributions of hippocampus, amygdala and perirhinal cortex to recognition of novel objects, contextual stimuli and stimulus relationships. Brain Res Bull 67:62–76PubMedCrossRefGoogle Scholar
  93. Müller D, Gerber B, Hammer M, Menzel R (2000) Sensory preconditioning in honeybees. J Exp Biol 203:1351–1356PubMedGoogle Scholar
  94. Müller D, Abel R, Brandt R, Zöckler M, Menzel R (2002) Differential parallel processing of olfactory information in the honeybee, Apis mellifera L. J Comp Physiol A 188:359–370CrossRefGoogle Scholar
  95. Núñez JA, Almeida L, Balderrama N, Giurfa M (1997) Alarm pheromone induces stress analgesia via an opioid system in the honeybee. Physiol Behav 63:75–80PubMedCrossRefGoogle Scholar
  96. Núñez JA (1982) Honeybee foraging strategies at a food source in relation to its distance from the hive and the rate of sugar flow. J Apicult Res 21:139–150Google Scholar
  97. O’Reilly RC, Rudy JW (2001) Conjunctive representations in learning and memory: Principles of cortical and hippocampal function. Psychol Rev 108:311–345PubMedCrossRefGoogle Scholar
  98. Pavlov IP (1927) Lectures on conditioned reflexes. International publishers, New YorkGoogle Scholar
  99. Pearce JM (1994) Similarity and discrimination: a selective review and a connectionist model. Psychol Rev 101:587–607PubMedCrossRefGoogle Scholar
  100. Peele P, Ditzen M, Menzel R, Galizia G (2006) Appetitive odor learning does not change olfactory coding in a subpopulation of honeybee antennal lobe neurons. J Comp Physiol A 192:1083–1103CrossRefGoogle Scholar
  101. Raine NE, Ings T, Dornhaus A, Saleh N, Chittka L (2006) Adaptation, genetic drift, pleiotropy, and history in the evolution of bee foraging behavior. Adv Study Behav 36:305–354Google Scholar
  102. Rescorla RA, Wagner AR (1972) A theory of Pavlovian conditioning: variations in the effectiveness of reinforcement and nonreinforcement. In: Black AH, Prokasy WF (eds) Classical conditioning II. Appleton-Century-Crofts, New York, pp 64–99Google Scholar
  103. Riemensperger T, Völler T, Stock P, Buchner E, Fiala (2005). Punishment prediction by dopaminergic neurons in Drosophila. Curr Biol 15:1953–1960PubMedCrossRefGoogle Scholar
  104. Robertson I (2001) Problem solving. Psychology Press, HoveGoogle Scholar
  105. Rudy JW, Sutherland RJ (1992) Configural and elemental associations and the memory coherence problem. J Cognit Neurosci 4:208–216CrossRefGoogle Scholar
  106. Rudy JW, Sutherland RJ (1995) Configural association theory and the hippocampal formation: an appraisal and reconfiguration. Hippocampus 5:375–389PubMedCrossRefGoogle Scholar
  107. Sachse S, Galizia CG (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
  108. Sandoz JC, Menzel R (2001) Side-specificity of olfactory learning in the honeybee: generalization between odors and sides. Learn Mem 8:286–294PubMedCrossRefGoogle Scholar
  109. Sandoz JC, Galizia CG, Menzel R (2003) Side-specific olfactory conditioning leads to more specific odor representations between sides but not within sides in the honeybee antennal lobes. Neuroscience 120:1137–1148PubMedCrossRefGoogle Scholar
  110. Scheiner R, Erber J, Page RE Jr (1999) Tactile learning and the individual evaluation of the reward in honey bees (Apis mellifera L.). J Comp Physiol A 185:1–10PubMedCrossRefGoogle Scholar
  111. Scheiner R, Page RE Jr, Erber J (2001a) The effects of genotype, foraging role, and sucrose responsiveness on the tactile learning performance of honey bees (Apis mellifera L.). Learn Mem 76:138–150CrossRefGoogle Scholar
  112. Scheiner R, Weiß A, Malun D, Erber J (2001b) Learning in honey bees with brain lesions: how partial mushroom-body ablations affect sucrose responsiveness and tactile antennal learning. Anim Cogn 4:227–235CrossRefGoogle Scholar
  113. Schroll C, Riemensperger T, Bucher D, Ehmer J, Völler T, Erbguth K, Gerber B, Hendel T, Nagel G, Buchner E, Fiala A (2006) Light-induced activation of distinct modulatory neurons substitutes for appetitive or aversive reinforcement during associative learning in larval Drosophila. Curr Biol 16:1741–1747PubMedCrossRefGoogle Scholar
  114. Schroter U, Malun D, Menzel R (2007) Innervation pattern of suboesophageal ventral unpaired median neurones in the honeybee brain. Cell Tissue Res 327:647–667PubMedCrossRefGoogle Scholar
  115. Schubert M, Francucci S, Lachnit H, Giurfa M (2005) Nonelemental visual learning in honeybees. Anim Behav 64:175–184CrossRefGoogle Scholar
  116. Schultz W, Dickinson A (2000) Neuronal coding of prediction errors. Annu Rev Neurosci 23:473–500PubMedCrossRefGoogle Scholar
  117. Schwaerzel M, Müller U (2006) Dynamic memory networks: dissecting molecular mechanisms underlying associative memory in the temporal domain. Cell Mol Life Sci 63:989–998CrossRefGoogle Scholar
  118. Schwaerzel M, Monastirioti M, Scholz H, Friggi-Grelin F, Birman S, Heisenberg M (2003) Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila. J Neurosci 23:10495–10502PubMedGoogle Scholar
  119. Seeley TD (1989) The honey bee colony as a superorganism. Amer Sci 77:546–553Google Scholar
  120. Seeley TD (1995) The wisdom of the hive—the social physiology of honey bee colonies. Harvard University Press, LondonGoogle Scholar
  121. Seeley TD, Visscher K (2004) Quorum sensing during nest site selection by honeybee swarms. Behav Ecol Sociobiol 56:594–601CrossRefGoogle Scholar
  122. Skinner BF (1938) The behavior of organisms. Appleton, New YorkGoogle Scholar
  123. Smith BH (1998) Analysis of interaction in binary odorant mixtures. Physiol Behav 65:397–407PubMedCrossRefGoogle Scholar
  124. Smith BH, Cobey S (1994) The olfactory memory of the honeybee Apis mellifera. II. Blocking between odorants in binary mixtures. J Exp Biol 195:91–108PubMedGoogle Scholar
  125. Southwick EE (1983) The honey bee cluster as a homeothermic superorganism. Comp Biochem Physiol 75:641–645CrossRefGoogle Scholar
  126. Srinivasan MV (1994) Pattern recognition in the honeybee: recent progress. J Insect Physiol 40:183–194CrossRefGoogle Scholar
  127. Srinivasan MV, Zhang SW (1997) Visual control of honeybee flight. In: Lehrer M (ed) Orientation and communication in arthropods. Birkhäuser, Basel, pp 95–114Google Scholar
  128. Srinivasan MV, Poteser M, Kral K (1999) Motion detection in insect orientation and navigation. Vision Res 39:2749–2766PubMedCrossRefGoogle Scholar
  129. Stach S, Giurfa M (2005) The influence of training length on generalization of visual feature assemblies in honeybees. Behav Brain Res 161:8–17PubMedCrossRefGoogle Scholar
  130. Stach S, Benard J, Giurfa M (2004) Local-feature assembling in visual pattern recognition and generalization in honeybees. Nature 429:758–761PubMedCrossRefGoogle Scholar
  131. Stopfer M, Bhagavan S, Smith BH, Laurent G (1997) Impaired odour discrimination on desynchronization of odour-encoding neural assemblies. Nature 390:70–74PubMedCrossRefGoogle Scholar
  132. Szyszka P, Ditzen M, Galkin A, Galizia G, Menzel R (2005) Sparsening and temporal sharpening of olfactory representations in the honeybee mushroom bodies. J Neurophysiol 94:3303–3313PubMedCrossRefGoogle Scholar
  133. Takeda K (1961) Classical conditioned response in the honey bee. J Insect Physiol 6:168–179CrossRefGoogle Scholar
  134. Terrace HS, McGonigle B (1994) Memory and representation of serial order by children, monkeys and pigeons. Curr Dir Psychol Sci 3:180–185CrossRefGoogle Scholar
  135. Theraulaz G, Gautrais J, Camazine S, Deneubourg JL (2003) The formation of spatial patterns in social insects: from simple behaviours to complex structures. Philos Trans R Soc Lond A 361:1263–1282CrossRefGoogle Scholar
  136. Troje F, Huber L, Loidolt M, Aust U, Fieder M (1999) Categorical learning in pigeons: the role of texture and shape in complex static stimuli. Vis Res 39:353–366PubMedCrossRefGoogle Scholar
  137. Tully T, Quinn WG (1985) Classical conditioning and retention in normal and mutant Drosophila melanogaster. J Comp Physiol Psychol 156:263–277Google Scholar
  138. Unoki S, Matsumoto Y, Mizunami M (2005) Participation of octopaminergic reward system and dopaminergic punishment system in insect olfactory learning revealed by pharmacological study. Eur J Neurosci 22:1409–1416PubMedCrossRefGoogle Scholar
  139. Unoki S, Matsumoto Y, Mizunami M (2006) Roles of octopaminergic and dopaminergic neurons in mediating reward and punishment signals in insect visual learning. Eur J Neurosci 24:2031–2038PubMedCrossRefGoogle Scholar
  140. Vareschi E (1971) Duftunterscheidung bei der Honigbiene - Einzelzell-Ableitungen und Verhaltensreaktionen. Z vergl Physiol 75:143–173Google Scholar
  141. Vergoz V, Roussel E, Sandoz JC, Giurfa M (2007) Aversive learning in honeybees revealed by the olfactory conditioning of the sting extension reflex. PLoS One 2(3):e288PubMedCrossRefGoogle Scholar
  142. Wehner R. (1981) Spatial vision in arthropods. In: Autrum HJ (ed) Handbook of sensory physiology VIc. Springer, Berlin, pp 287–616Google Scholar
  143. Wehr M, Laurent G (1996) Temporal combinatorial encoding of odours with oscillations. Nature 384:162–166PubMedCrossRefGoogle Scholar
  144. Whitehead AT (1978) Electrophysiological response of honey bee labial palp contact chemoreceptors to sugars and electrolytes. Physiol Entomol 3:241–248Google Scholar
  145. Whitehead AT, Larsen JR (1976) Electrophysiological responses of galeal contact chemoreceptors of Apis mellifera to selected sugars and electrolytes. J Insect Physiol 22:1609–1616PubMedCrossRefGoogle Scholar
  146. Whitlow JW, Wagner AR (1972) Negative patterning in classical conditioning: summation of response tendencies to isolable and configural components. Psychon Sci 27:299–301Google Scholar
  147. Wittstock S, Menzel R (1994) Color learning and memory in honey bees are not affected by protein synthesis inhibition. Behav Neural Biol 62:224–229PubMedCrossRefGoogle Scholar
  148. Wüstenberg D, Gerber B, Menzel R (1998) 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
  149. Yang EC, Maddess T (1997) Orientation-sensitive neurons in the brain of the honey bee (Apis mellifera). J Insect Physiol 43:329–336PubMedCrossRefGoogle Scholar
  150. Yang EC, Lin HC, Hung YS (2004) Patterns of chromatic information processing in the lobula of the honeybee, Apis mellifera L. J Insect Physiol 50:913–925PubMedCrossRefGoogle Scholar
  151. Zentall TR, Galizio M, Critchfield TS (2002) Categorization, concept learning and behavior analysis: an introduction. J Exp Anal Behav 78:237–248PubMedCrossRefGoogle Scholar
  152. Zhang SW, Srinivasan MV, Zhu H, Wong J (2004) Grouping of visual objects by honeybees. J Exp Biol 207:3289–3298PubMedCrossRefGoogle Scholar
  153. Zhang S, Bock F, Si A, Tautz J, Srinivasan M (2005) Visual working memory in decision making by honey bees. Proc Natl Acad Sci USA 102:5250–5255PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  1. 1.Research Centre on Animal CognitionCNRS – University Paul SabatierToulouse cedex 9France

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