Cognitive Architecture of a Mini-Brain

  • Martin Giurfa
  • Randolf Menzel


Honeybees have small brains but their behavioural repertoire is impressive. The concept of modularity of cognitive functions is used to characterise levels of complexity in an insect brain. We focus on the question to what extent adaptive behaviour in honeybees exceeds elementary forms of learning. Non-elemental forms of associative learning are studied in an olfactory conditioning paradigm. Examples of occasion setting and categorical learning of visual cues are demonstrated for freely flying bees. Memory is found to be highly dynamic, involving several sequential phases of learning-induced processing. Navigation is based both on stereotypical behavioural routines and a flexible form of topographic memory. These analyses show that independent functions of vertically arranged domain specific processing modules cannot explain the richness and complexity of honeybee behaviour rather horizontal integration in a central state is required. Neural mechanisms are discussed which may underlie domain specific processing modules and central integration. We conclude that the honeybee may serve as a model for the study of intermediate levels of complexity in cognitive functions and for the identification of their neural substrates.


Context Link Visual Stimulus Mushroom Body Cognitive Architecture Differential Conditioning Comparative Physiology 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Bitterman, M. E., Menzel, R., Fietz, A., and Schäfer, S. (1983) Classical conditioning of proboscis extension in honeybees (Apis mellifera). Journal of Comparative Psychology 97, 107–119.CrossRefGoogle Scholar
  2. 2.
    Capaldi, E. A. Robinson, G. E. and Fahrbach, S. E. (1999) Neuroethology of spatial learning: the bird and the bees. Annual Review of Psychology 50, 651–682.CrossRefGoogle Scholar
  3. 3.
    Capaldi, E. A., Smith, A. D., Osborne, J. L., Fahrbach, S. E., Farris, S. M., Reynolds, D. R., Edwards, A. S., Martin, A., Robinson, G. E., Poppy, G. M., Riley, J. R. (2000) Ontogeny of orientation flight in the honeybee revealed by harmonic radar. Nature 403, 537–540.CrossRefADSGoogle Scholar
  4. 4.
    Cheng, K. (2000) How Honeybees find a place: lessons from a simple mind. Animal Learning and Behavior 28, 1–15.CrossRefGoogle Scholar
  5. 5.
    Chittka, L. and Geiger, K. (1995) Can honeybees count landmarks? Animal Behaviour 49, 159–164.CrossRefGoogle Scholar
  6. 6.
    Collett, T. S. (1996) Insect navigation en route to the goal: multiple strategies for the use of landmarks. Journal of Experimental Biology 199, 227–235.CrossRefGoogle Scholar
  7. 7.
    Collett, T. S. and Baron, J. (1995) Learnt sonsory-motor mappings in honeybees: interpolation and its possible relevance to navigation. Journal of Comparative Physiology A 177, 287–298.Google Scholar
  8. 8.
    Collett, T. S. and Zeil, J. (1998) Places and landmarks: an arthropod perspective. In Spatial Representation in Animals, edited by S. Healy. Oxford University Press, Oxford, pp. 18–53.Google Scholar
  9. 9.
    Collett, T. S., Fry, S. N., and Wehner, R. (1993) Sequence learning by honeybees. Journal of Comparative Physiology A 172, 693–706.Google Scholar
  10. 10.
    Collett, T. S. Fauria, K. Dale, K. and Baron, J. (1997) Places and patterns–a study of context learning in honeybees. Journal of Comparative Physiology A 181, 343–353.CrossRefGoogle Scholar
  11. 11.
    Coltheart, M. (1999) Modularity and cognition. Trends in Cognitive Sciences 3, 115–120.CrossRefGoogle Scholar
  12. 12.
    Dyer, F. C. (1998) Cognitive ecology of navigation. In Cognitive Ecology, edited by R. Dukas, Chicago University Press, Chicago, pp. 201–260.Google Scholar
  13. 13.
    Edwards, D. H. Heitler, W. J. and Krasne, F. B. (1999) Fifty years of a command neuron: the neurobiology of escape behavior in the crayfish. Trends in Neurosciences 22 153–161.Google Scholar
  14. 14.
    Faber, T., Joerges, J., and Menzel, R. (1999) Associative learning modifies neural representations of odors in the insect brain. Nature neuroscience 2, 74–78.Google Scholar
  15. 15.
    Fanselow, M. S. (1998) Pavlovian conditioning, negative feedback, and blocking: mechanisms that regulate association formation. Neuron 20, 625–627.CrossRefGoogle Scholar
  16. 16.
    Flanagan, D. and Mercer, A. R. (1989) An atlas and 3-D reconstruction of the antennal lobes in the worker honey bee, Apis mellifera L. (Hymenoptera: Apidae). International Journal of Insect Morphology and Embryology 18, 145–159.CrossRefGoogle Scholar
  17. 17.
    Fodor, J. A. (1983) The Modularity of Mind. MIT Press, Cambridge, Massachusetts.Google Scholar
  18. 18.
    Frisch, K. von (1967) The Dance Language and Orientation of Bees. Harvard University Press, Cambridge.Google Scholar
  19. 19.
    Galizia, C. G. and Menzel, R. (2000) Odour perception in honeybees: coding information in glomerular patterns. Current Opinion in Neurobiology 10, 504–510.CrossRefGoogle Scholar
  20. 20.
    Galizia, C. G. and Menzel, R. (2001) The role of glomeruli in the neural representation of odours: results from optical recording studies. Journal of Insect Physiology 47, 115–129.CrossRefGoogle Scholar
  21. 21.
    Galizia, C. G., Mcllwrath, S. L. and Menzel. R. (1999a) A digital 3D atlas of the honeybee antennal lobe based on optical sections acquired using confocal microscopy. Cell Tissue Research 295, 383–394, 1999.Google Scholar
  22. 22.
    Galizia, C. G., Sachse, S., Rappert, A. and Menzel, R. (1999b) The glomerular code for odor representation is species specific in the honeybee Apis mellifera. Nature Neuroscience 2, 473–478.CrossRefGoogle Scholar
  23. 23.
    Getz, W. M. and Akers, R. P. (1994) Honeybee olfactory sensilla behave as integrated processing units. Behavioral Neural Biology 61, 191–195.CrossRefGoogle Scholar
  24. 24.
    Getz, W. M. and Akers, R. P. (1995) Partitioning non-linearities in the response of olfactory neurons to binary odors. BioSystems 34, 27–40, 1995.CrossRefGoogle Scholar
  25. 25.
    Gerber, B. and Ullrich, J. (1999) No evidence for olfactory blocking in honeybee classical conditioning. Journal of Experimental Biology 202, 1839–1854.Google Scholar
  26. 26.
    Giger, A. D. and Srinivasan, M. V. (1995) Pattern recognition in honeybees: eidetic imagery and orientation discrimination. Journal of Comparative Physiology A 176, 791–795.CrossRefGoogle Scholar
  27. 27.
    Giurfa, M. and Menzel, R. (1997) Insect visual perception: complex ability of simple nervous systems. Current Opinion in Neurobiology 7, 505–513.CrossRefGoogle Scholar
  28. 28.
    Giurfa, M. and Capaldi, E. A. (1999) Vectors, routes and maps: new discoveries about navigation in insects. Trends in Neurosciences 22, 237–242.CrossRefGoogle Scholar
  29. 29.
    Giurfa, M. and Lehrer, M. (2001) Honeybee vision and floral displays: from detection to close-up recognition. In Cognitive Ecology of Pollination, edited by L. Chittka and R. Thompson. Cambridge University Press, Cambridge, pp. 61–82.CrossRefGoogle Scholar
  30. 30.
    Giurfa, M., Backhaus, W. and Menzel, R. (1995) Colour and angular orientation in the discrimination of bilateral symmetric patterns in the honeybee. Naturwissenschaften, 82, 198201.Google Scholar
  31. 31.
    Giurfa, M., Eichmann, B., and Menzel, R. (1996) Symmetry perception in an insect. Nature 382, 458–461.Google Scholar
  32. 32.
    Giurfa, M., Nûiïez, J. A., Chittka, L. and Menzel, R. (1995) Colour preferences of flower-naive honeybees. Journal of Comparative Physiology A 177, 247–259.CrossRefGoogle Scholar
  33. 33.
    Giurfa, M., Zhang, S. W., Jennett, A., Menzel, R. and Srinivasan, M. V. (2001) The concepts of sameness and difference in an insect. Nature 410, 930–933.CrossRefADSGoogle Scholar
  34. 34.
    Giurfa, M., Hammer, M., Stach, S., Stollhoff, N., Müller-Deisig, N. and Mizyrycki, C. (1999) Pattern learning by honeybees: conditioning procedure and recognition strategy. Animal Behaviour 57, 315–324.CrossRefGoogle Scholar
  35. 35.
    Gould, J. L. (1985) How bees remember flower shapes. Science 227, 1492–1494.Google Scholar
  36. 36.
    Gould, J. L. (1986) Pattern learning by honey bees. Animal Behaviour 34, 990–997.CrossRefGoogle Scholar
  37. 37.
    Grünewald, B. (1999) Physiological properties and response modulations of mushroom body feedback neurons during olfactory learning in the honeybee Apis mellifera. Journal of Comparative Physiology A 185, 565–576.CrossRefGoogle Scholar
  38. 38.
    Guerrieri, F., Krause, G., Komischke, B. Gerber, B., Malun, D. and Giurfa, M. (2001) Blocking and odour similarity in olfactory conditioning of honeybees. Proceedings of the 28th Göttingen Neurobiology Conference,660.Google Scholar
  39. 39.
    Gumbert, A. (2000) Color choices by bumble bees (Bombus terrestris): innate preferences and generalization after learning. Behavioral Ecology Sociobiology 48, 36–43.CrossRefGoogle Scholar
  40. 40.
    Hammer, M. (1993) An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees. Nature 366, 59–63.CrossRefADSGoogle Scholar
  41. 41.
    Hammer, M. (1997) The neural basis of associative reward learning in honeybees. Trends in Neurosciences 20, 245–252.CrossRefGoogle Scholar
  42. 42.
    Hammer, M. and Menzel, R. (1994) Neuromodulation, instruction and behavioral plasticity. In Flexibility And Constraint in Behavioral Systems, edited by R. Greenspan and B. Kyriacou. J. Wiley & Sons, Chichester, pp. 109–118.Google Scholar
  43. 43.
    Hammer, M. and Menzel, R. (1995) Learning and memory in the honeybee. Journal of Neuroscience 15, 1617–1630.Google Scholar
  44. 44.
    Hammer, M. and Menzel, R. (1998) Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees. Learning and Memory 5, 146156.Google Scholar
  45. 45.
    Hateren, J. H. van, Srinivasan, M. V., and Wait, P. B. (1990) Pattern recognition in bees; orientation discrimination. Journal of Comparative Physiology A 167, 649–654.CrossRefGoogle Scholar
  46. 46.
    Hertz, M. (1933) Über figurale Intensitäten and Qualitäten in der optischen Wahrnehmung der Biene. Biologisches Zentralblatt 53, 10–40.Google Scholar
  47. 47.
    Hildebrand, J. G. and Shepherd, G. M. (1997) Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annual Review of Neuroscience 20, 595–631.CrossRefGoogle Scholar
  48. 48.
    Homberg, U. and Erber, J. (1979) Response Characteristics and Identification of Extrinsic Mushroom Body Neurons of the Bee. Zoologische Naturforschung 34, 612–615.Google Scholar
  49. 49.
    Horridge, A. (1997) Pattern discrimination by the honeybee: disruption as a cue. Journal of Comparative Physiology A 181, 267–277.CrossRefGoogle Scholar
  50. 50.
    Hosler, J. S. and Smith, B. S. (2000) Blocking and the detection of odor components in blends. Journal of Experimental Biology 203, 2797–2806.Google Scholar
  51. 51.
    Huber, F. (1990) Nerve cells and insect behavior–studies on crickets. American Zoologist 30, 609–627.Google Scholar
  52. 52.
    Joerges, J., Küttner, A., Galizia, C. G., and Menzel, R. (1997) Representation of odours and odour mixtures visualized in the honeybee brain. Nature 387, 285–288.CrossRefADSGoogle Scholar
  53. 53.
    Kramer, E. (1976) The orientation of walking honeybees in odour fields with small concentration gradients. Physiological Entomology 1, 27–37.CrossRefGoogle Scholar
  54. 54.
    Laska, M., Galizia, C. G., Giurfa, M., and Menzel, R. (1999) Olfactory discrimination ability and odor structure-activity relationships in honeybees. Chemical Senses 24, 429–438.CrossRefGoogle Scholar
  55. 55.
    Lehrer, M. (1997) Honeybees’ visual spatial orientation at the feeding site. In Detection and Comunication in Arthropods, edited by M. Lehrer. Birkhäuser, Basel, pp. 115–144.Google Scholar
  56. 56.
    Lehrer, M., Horridge, G. A., Zhang, S. W. and Gadagkar, R. (1995) Shape vision in bees: innate preference for flower-like patterns. Philosophical Transactions of the Royal Society London B 347, 123–137.CrossRefADSGoogle Scholar
  57. 57.
    Lehrer, M., Srinivasan, M. V., Zhang, S. W. and Horridge, G. A. (1988) Motion cues provide the bee’s visual world with a third dimension. Nature 332, 356–357.CrossRefADSGoogle Scholar
  58. 58.
    Malun, D. (1998) Early development of mushroom bodies in the brain of the honeybee Apis mellifera as revealed by BrdU incorporation and ablation experiments. Learning and Memory 5, 90–101.Google Scholar
  59. 59.
    Malun, D., Giurfa, M., Galizia, G., Plath, N., Brandt, R., Gerber, B. and Eisermann, B. (2002) Hydroxyurea-induced partial mushroom body ablation does not affect acquisition and retention of olfactory differential conditioning in honeybees. Journal of Neurobiology 53, 343–360.CrossRefGoogle Scholar
  60. 60.
    Mauelshagen, J. (1993) Neural correlates of olfactory learning in an identified neuron in the honey bee brain. Journal of Neurophysiology 69 609–625.Google Scholar
  61. 61.
    Menzel, R. (1967) Untersuchungen zum Erlernen von Spektralfarben durch die Honigbiene (Apis mellifica). Zeitschrift für vergleichende Physiologie 56, 22–62.CrossRefGoogle Scholar
  62. 62.
    Menzel, R. (1968) Das Gedächtnis der Honigbiene für Spektralfarben. I. Kurzzeitiges and langzeitiges Behalten. Zeitschrift für vergleichende Physiologie 60, 82–102.CrossRefGoogle Scholar
  63. 63.
    Menzel, R. (1969) Das Gedächtnis der Honigbiene für Spektralfarben. II. Umlernen and Mehrfachlernen. Zeitschrift für vergleichende Physiologie 63, 290–309.CrossRefGoogle Scholar
  64. 64.
    Menzel, R. (1985) Learning in honey bees in an ecological and behavioral context. In Experimental Behavioral Ecology, edited by B. Hölldobler and M. Lindauer. Gustav Fischer, Stuttgart, pp. 55–74.Google Scholar
  65. 65.
    Menzel, R. (1990) Learning, memory, and ‘cognition’ in honey bees. In Neurobiology of comparative cognition, edited by R. P. Kesner and D. S. Olton. Erlbaum, Hillsdale, pp. 237–292.Google Scholar
  66. 66.
    Menzel, R. (1999) Memory dynamics in the honeybee. Journal of Comparative Physiology A 185, 323–340.CrossRefGoogle Scholar
  67. 67.
    Menzel, R. and Backhaus, W. (1991) Color vision in insects. In Vision and Visual Dysfunction. The Perception of Colour, edited by P. Gouras. MacMillan Press, London, pp. 262–288.Google Scholar
  68. 68.
    Menzel, R. and Giurfa, M. (2001) The cognitive architecture of a mini brain: the honeybee. Trends in Cognitive Sciences 5, 62–71.CrossRefGoogle Scholar
  69. 69.
    Menzel, R. and Müller, U. (1996) Learning and memory in honeybees: from behavior to neural substrates. Annual Review of Neuroscience 19, 379–404.CrossRefGoogle Scholar
  70. 70.
    Menzel, R., Greggers, U., and Hammer, M. (1993) Functional organization of appetitive learning and memory in a generalist pollinator, the honey bee. In Insect Learning: Ecological and Evolutionary Perspectives, edited by D. Papaj, and A.C. Lewis. Chapman & Hall, New York, pp. 79–125.CrossRefGoogle Scholar
  71. 71.
    Menzel, R., Geiger, K., Chittka, L., Joerges, J., Kunze, J. and Müller, U. (1996) The knowledge base of bee navigation. Journal of Experimental Biology 199, 141–146.Google Scholar
  72. 72.
    Menzel, R., Giurfa, M., Gerber, B., and Hellstem, F. (1999). Elementary and configural forms of memory in an insect: the honeybee. In Learning: Rule Extraction And Representation, edited by A. D. Friederici and R. Menzel. Walter de Gruyter, Berlin, pp. 259–282.Google Scholar
  73. 73.
    Menzel, R., Geiger, K., Müller, U., Joerges, J. and Chit-tka, L. (1998) Bees travel novel homeward routes by integrat-ing separately acquired vector memories. Animal Behaviour 55, 139–152.CrossRefGoogle Scholar
  74. 74.
    Menzel, R, Brandt, R., Gumbert, A., Komischke, B. and Kunze, J. (2000) Two spatial memories for honeybee navigation. Proceedings of the Royal Society of London B 267, 961–968.CrossRefGoogle Scholar
  75. 75.
    Mobbs, P. G. (1982) The brain of the honeybee Apis mellifera I. The connections and spatial organization of the mushroom bodies. Philosophical Transactions of the Royal Society of London B 298, 309–354.CrossRefADSGoogle Scholar
  76. 76.
    Rescorla, R. A. and Wagner, A. R. (1972) A theory of classical conditioning: variations in the effectiveness of reinforcement and non-reinforcement. In Classical Conditioning II: Current Research and Theory, edited by A. H. Black and W. F. Prokasy. Appleton- Century-Crofts, New York, pp. 64–99.Google Scholar
  77. 77.
    Riley, J. R. Smith, A. D., Reynolds, D. R., Edwards, A. S., Osborne, J. L., Williams, I. H., Carreck, N. L. and Poppy, G. M. (1996) Tracking bees with harmonic radar. Nature 379, 29–30.CrossRefADSGoogle Scholar
  78. 78.
    Ronacher, B. (1998) How do bees learn and recognize visual patterns? Biological Cybernetic 79, 477–485.CrossRefGoogle Scholar
  79. 79.
    Ronacher, B. and Duft, U. (1996) An image-matching mechanism describes a generalization task in honeybees. Journal of Comparative Physiology A, 178, 803–812.CrossRefGoogle Scholar
  80. 80.
    Rudy, J. W. and Sutherland, R. J. (1992) Configural and elemental associations and the memory coherence problem. Journal of Cognitive Neuroscience 4,3, 208–216.CrossRefGoogle Scholar
  81. 81.
    Sachse, S,. Rappert, A. and Galizia, C. G. (1999) The Spatial representation of chemical structures in the antennal lobe of honeybees: steps towards the olfactory code. European Journal of Neuroscience 11, 3970–3982.CrossRefGoogle Scholar
  82. 82.
    Scheiner, R., Weiß, A., Malun, D. and Erber, J. (2001) Learning in honey bees with brain lesions: how partial mushroom-body ablations affect sucrose responsiveness and tactile antennal learning. Animal Cognition 4, 227–235.CrossRefGoogle Scholar
  83. 83.
    Seeley, T.D. (1995) The Wisdom of the Hive. Harvard University Press, Cambridge, MAGoogle Scholar
  84. 84.
    Shettleworth, S. J. (1998) Cognition, Evolution and Behavior. 1–688. New York, Oxford University Press.Google Scholar
  85. 85.
    Shettleworth, S. J. (2001) Animal cognition and animal behaviour. Animal Behaviour 61, 277–286.CrossRefGoogle Scholar
  86. 86.
    Smith, B. H. (1997) An analysis of blocking in binary odorant mixtures: an increase but not a decrease in intensity of reinforcement produces unblocking. Behavioral Neuroscience. 111, 57–69.Google Scholar
  87. 87.
    Smith, B. H. and Cobey, S. (1994) The olfactory memory of the honey bee, Apis mellifera. II. Blocking between odorants in binary mixtures. Journal of Experimental Biology 195, 91–108.Google Scholar
  88. 88.
    Srinivasan, M. V. (1994) Pattern recognition in the honeybee: recent progress. Journal of Insect Physiology 40, 183–194.CrossRefGoogle Scholar
  89. 89.
    Srinivasan, M. V. and Zhang, S. W. (1998) Honeybees link sights to smells. Nature 39, 637–638.CrossRefADSGoogle Scholar
  90. 90.
    Srinivasan, M. V., Lehrer, M., and Horridge, G. A. (1990) Visual figure-ground discrimination in the honeybee: the role of motion parallax at boundaries. Proceedings of the Royal Society London B 238, 331–350.CrossRefADSGoogle Scholar
  91. 91.
    Srinivasan, M. V., Poteser, M. and Kral, K. (1999) Motion detection in insect orientation and navigation. Vision Research 39, 2749–2766.CrossRefGoogle Scholar
  92. 92.
    Takeda, K (1961) Classical conditioned response in the honey bee. Journal of Insect Physiology 6, 168–179.CrossRefGoogle Scholar
  93. 93.
    Wehner, R. (1972) Dorsoventral asymmetry in the visual field of the be, Apis mellifica. Journal of Comparative Physiology, 77, 256–277.CrossRefGoogle Scholar
  94. 94.
    Wehner, R. (1981) Spatial vision in arthropods. In Handbook of sensory Physiology VIc, edited by H. J. Autrum. Springer, Berlin, pp. 287–616.Google Scholar
  95. 95.
    Wehner, R. and Menzel, R. (1990) Do insects have cognitive maps? Annual Review of Neuroscience 13, 403–414.CrossRefGoogle Scholar
  96. 96.
    Wehner, R. Michel, B. and Antonsen, P. (1996) Visual navigation in insects: coupling of egocentric and geocentric information. Journal of Experimental Biology 199 129–140.Google Scholar
  97. 97.
    Withers, G. S., Fahrbach, S. E. and Robinson, G. E. (1993) Selective neuroanatomical plasticity and division of labour in the honey bee (Apis mellifera). Nature 364, 238–240.CrossRefADSGoogle Scholar
  98. 98.
    Wilson, E. O. and Hölldobler, B. (1987) Causes of ecological success: the case of the ants. Ecology 56, 1–9.Google Scholar
  99. 99.
    Zhang, S. W., Bartsch, K. and Srinivasan, M. V. (1996) Maze learning by honeybees. Neurobiology of Learning and Memory 66, 267–282.CrossRefGoogle Scholar
  100. 100.
    Zhang, S. W., Lehrer, M., and Srinivasan, M. V. (1999) Honeybee memory: navigation by associative grouping and recall of visual stimuli. Neurobiology of Learning and Memory 72, 180–201.CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2003

Authors and Affiliations

  • Martin Giurfa
  • Randolf Menzel

There are no affiliations available

Personalised recommendations