Neuroscience and Behavioral Physiology

, Volume 44, Issue 2, pp 156–162 | Cite as

Morphological Basis of a Conditioned Reflex in the Honeybee Apis Mellifera L.

  • A. V. Shvetsov
  • T. G. Zachepilo

This review summarizes studies directed to seeking the neuroanatomical basis of associative learning (conditioned olfactory proboscis-extension feeding reflex) in honeybees. Data on the structure of the bee brain are presented. Parallel pathways involved in responses to conditioned and unconditioned stimuli are demonstrated. The contributions of various brain structures and specific neurons (VUMmx1, PE1) to forming the conditioned reflex are addressed.


conditioned reflex honeybee mushroom bodies associative learning 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    A. K. Voskresenskaya, “The role of the mushroom bodies of the supraesophageal ganglion in conditioned reflexes in the honeybee,” Dokl. Akad. Nauk. SSSR, 112, 964–967 (1957).Google Scholar
  2. 2.
    Yu. Konorski, Integrative Brain Activity [Russian translation], Mir, Moscow (1970).Google Scholar
  3. 3.
    I. A. Levchenko, Information Transmission on the Coordinates of Food Sources in Honeybees [in Russian], Naukova Dumka, Kiev (1976).Google Scholar
  4. 4.
    M. E. Lobashev, “Parallel studies – analogous and homologous series of the development of the main properties of nervous activity in animal phylogenesis,” in: Proc. 2nd Sci. Conf. Evolutionary Physiology in Memory of Academician L. A. Orbeli [in Russian], Leningrad (1960), pp. 16–23.Google Scholar
  5. 5.
    M. E. Lobashev, N. G. Lopatina, I. A. Nikitina, and E. G. Chesnokova, “Orientation of honeybees using visual above-ground stimuli,” Pchelovodstvo, 10, 31–33 (1961).Google Scholar
  6. 6.
    N. G. Lopatina, Signal Activity in the Honeybee Family [in Russian], Nauka, Leningrad (1971).Google Scholar
  7. 7.
    N. G. Lopatina and E. G. Chesnokova, “Conditioned reflexes and memory in the honeybee,” Zh. Vyssh. Nerv. Deyat., 42, No. 5, 890–903 (1992).Google Scholar
  8. 8.
    G. A. Mazokhin-Porshnyakov, S. A. Semenova, and I. A. Milevskaya, “Similarity in the behavior of insects and vertebrates in solving difficult visual tasks,” Zh. Vyssh. Nerv. Deyat., 29, No. 1, 101–107 (1979).Google Scholar
  9. 9.
    I. P. Pavlov, Lectures on the Functioning of the Cerebral Cortex. Complete Collection of Works [in Russian], USSR Academy of Sciences, Moscow (1927), Vol. 4.Google Scholar
  10. 10.
    A. Fessar, The Role of Neural Networks in the Transmission of Sensory Information. A Theory of Associations in Sensory Systems [Russian translation], G. D. Smirnov (ed.), Mir, Moscow (1964), pp. 81–99.Google Scholar
  11. 11.
    R. Abel, J. Rybak, and R. Menzel, “Structure and response patterns of olfactory interneurons in the honeybee, Apis mellifera,” J. Comp. Neurol., 37, 363–383 (2001).CrossRefGoogle Scholar
  12. 12.
    G. Arnold, C. Masson, and S. Budharugsa, “Comparative study of the antennal lobes and their afferent pathway in the worker bee and the drone Apis mellifera,” Cell Tiss. Res., 242, 593–605 (1985).CrossRefGoogle Scholar
  13. 13.
    N. Balderrama, “One trial learning in the American cockroach, Periplaneta americana,” J. Insect Physiol., 26, 4990504 (1980).CrossRefGoogle Scholar
  14. 14.
    E. A. Bernays and J. Lee, “Food aversion learning in the polyphagous grasshopper Schistocerca americana,” Physiol. Entomol., 13, 131–137 (1988).CrossRefGoogle Scholar
  15. 15.
    G. Bicker, “Histochemistry of classical neurotransmitters in antennal lobes and mushroom bodies of the honeybee,” Miscosc. Res. Tech., 45, 175–183 (1999).Google Scholar
  16. 16.
    G. Bicker, S. Schafer, and T. J. Kingan, “Mushroom body feedback interneurons in the honeybee show GABA-like immunoreactivity,” Brain Res., 60, 394–397 (1985).CrossRefGoogle Scholar
  17. 17.
    M. E. Bitterman, R. Menzel, A. Fietz, and S. Schäfer, “Classical conditioning of proboscis extension in honeybee (Apis mellifera),” J. Comp. Physiol., 97, 107–119 (1983).Google Scholar
  18. 18.
    M. Denker, R. Finke, F. Schaupp, et al., “Neural correlates of odor learning in the honeybee,” Eur. J. Neurosci., 31, 119–133 (2010).PubMedCrossRefGoogle Scholar
  19. 19.
    J. C. Eccles, The Neurophysiological Basis of Mind. The Principles of Neurophysiology, Oxford University Press, Oxford (1953).Google Scholar
  20. 20.
    B. Ehmer and W. Gronenberg, “Segregation of visual input to the mushroom bodies in honeybee (Apis mellifera)” J. Comp. Neurol., 451, 362–373 (2002).PubMedCrossRefGoogle Scholar
  21. 21.
    J. Erber, T. Masuhr, and R. Menzel, “Localization of short-term memory in the brain of the bee, Apis mellifera,” Physiol. Entomol., 5, 343–358 (1980).CrossRefGoogle Scholar
  22. 22.
    T. Faber and R. Menzel, “Visualizing a mushroom body response to a conditioned odor in honeybees,” Naturwissenschaften, 88, 472–476 (2001).PubMedCrossRefGoogle Scholar
  23. 23.
    R.-J. Fan, P. Anderson, and B. S. Hansson, “Behavioural analysis of olfactory conditioning in the moth Spodoptera littoralis (Boisd.) (Lepidoptera: Noctuidae),” J. Exp. Biol., 200, 2969–2976 (1997).PubMedGoogle Scholar
  24. 24.
    R.-J. Fan and B. S. Hansson, “Olfactory conditioning in the moth Spodoptera littoralis,” Physiol. Behav., 72, 159–165 (2001).PubMedCrossRefGoogle Scholar
  25. 25.
    K. Frisch, “Der Farbensinn und Formensinn der Biene,” Zool. Jahrb. Physiol. Abt., 35, 1–88 (1915).Google Scholar
  26. 26.
    G. C. Galizia, S. L. McIlwrath, and R. Menzel, “A digital threedimensional atlas of the honeybee antennal lobe based on optical sections acquired by confocal microscopy,” Cell Tiss. Res., 295, 383–394 (1999).CrossRefGoogle Scholar
  27. 27.
    O. Ganeshina and R. Menzel, “GABA-immunoreactive neurons in the mushroom bodies of the honeybee: an electron microscope study,” J. Comp. Neurol., 437, 335–349 (2001).PubMedCrossRefGoogle Scholar
  28. 28.
    J. Gascuel and C. Masson, “A quantitative ultrastructural study of the honeybee antennal lobe,” Tiss. Cell, 23, 341–355 (1991).CrossRefGoogle Scholar
  29. 29.
    M. Guirfa, “Behavioral and neural analysis of associative learning in the honeybee: a taste from the magic well,” J. Comp. Physiol. Ser. A. Neuroethol. Sens. Neural. Behav. Physiol., 193, No. 8, 801–824 (2007).CrossRefGoogle Scholar
  30. 30.
    W. Gronenberg, “Subdivisions of hymenopteran mushroom body calyces by their afferent supply,” J. Comp. Neurol., 435, 474–489 (2001).PubMedCrossRefGoogle Scholar
  31. 31.
    B. Grünewald, “Morphology of feedback neurons in the mushroom body of the honeybee, Apis mellifera,” J. Comp. Neurol., 404, 114–126 (1999).PubMedCrossRefGoogle Scholar
  32. 32.
    B. Grünewald, “Physiological properties and response modulations of mushroom body feedback neurons during olfactory learning in the honeybee Apis mellifera,” J. Comp. Physiol. Ser. A, 185, 565–576 (1999).CrossRefGoogle Scholar
  33. 33.
    M. Haehnel and R. Menzel, “Sensory representation and learningrelated plasticity in mushroom body extrinsic feedback neurons of the protocerebral tract,” Front. Syst. Neurosci., 4, Art. 161, 1–16 (2010).CrossRefGoogle Scholar
  34. 34.
    M. Hammer, “An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees,” Nature, 366, 59–63 (1993).PubMedCrossRefGoogle Scholar
  35. 35.
    M. Hammer, “The neural basis of associative reward learning in honeybees,” Trends Neurosci., 20, 245–252 (1997).PubMedCrossRefGoogle Scholar
  36. 36.
    M. Hammer and R. Menzel, “Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees,” Learn, Mem., 5, 146–156 (1998).Google Scholar
  37. 37.
    D. O. Hebb, The Organization of Behavior. A Neuropsychological Theory, Wiley, New York (1949).Google Scholar
  38. 38.
    M. Heisenberg, “Genetic approach to learning and memory (mnemogenetics) in Drosophila melanogaster,” in: Fundamentals of Memory Formation: Neuronal Plasticity and Brain Function, B. Rahmann (ed.), Gustav Fischer Verlag, Stuttgart (1989), pp. 3–45.Google Scholar
  39. 39.
    M. Heisenberg, “What do the mushroom bodies do for the insect brain? An introduction,” Learn. Mem., 5, No. 1, 1–10 (1998).PubMedGoogle Scholar
  40. 40.
    U. Homberg, “Processing of antennal information in extrinsic mushroom body neurons of the bee brain,” J. Comp. Physiol. Ser. A, 154, 825–836 (1984).CrossRefGoogle Scholar
  41. 41.
    Y. Homberg and J. Erber, “Response characteristics and identification of extrinsic mushroom body neurons of the bee,” Z. Naturforsch., 34, 612–615 (1979).Google Scholar
  42. 42.
    B. Hourcade, T. Muenz, J.-C. Sandoz, et al., “Long-term memory leads to synaptic reorganization in the mushroom bodies: A memory trace in the insect brain?” J. Neurosci., 30, No. 18, 6461–6465 (2010).PubMedCrossRefGoogle Scholar
  43. 43.
    E. R. Kandel, “The molecular biology of memory storage: a dialogue between genes and synapses,” Science, 294, 1030–1038 (2001).PubMedCrossRefGoogle Scholar
  44. 44.
    F. C. Kenyon, “The brain of the bee. A preliminary contribution to the morphology of the nervous system of the arthropoda,” J. Comp. Neurol., 6, 133–210 (1896).CrossRefGoogle Scholar
  45. 45.
    S. Kirschner, C. J. Kleineidam, C. Zube, et al., “Dual olfactory pathway in the honeybee Apis mellifera,” J. Comp. Neurol., 499, 933–952 (2006).PubMedCrossRefGoogle Scholar
  46. 46.
    M. Kuwabara, “Bildung des bedingten Reflexes von Pavlovs Typus bei der Honigbiene, Apis mellifica,” J. Fac. Sci. Hokkaido Univ. (Ser VI. Zool.), 13, 458–464 (1957).Google Scholar
  47. 47.
    D. Laloi, J. S. Sandoz, A. L. Picard-Nizou, et al., “Olfactory conditioning of the proboscis extension in bumble bees,” Entomol. Exp. Appl., 90, 123–129 (1999).CrossRefGoogle Scholar
  48. 48.
    M. Lindauer, “General sensory physiology. Orientation in space,” Fortschr. Zool., 16, 58–140 (1963).PubMedGoogle Scholar
  49. 49.
    J. Mauelshagen, “Neural correlates of olfactory learning in an identified neuron in the honey bee brain,” J. Neurophysiol., 69, 609–625 (1993).PubMedGoogle Scholar
  50. 50.
    R. Menzel, “Searching for the memory trace in a minibrain, the honeybee,” Learn. Mem., 8, 53–62 (2001).PubMedCrossRefGoogle Scholar
  51. 51.
    R. Menzel, “Memory dynamics in the honeybee,” J. Comp. Physiol. (Ser. A), 185, 323–340 (1999).CrossRefGoogle Scholar
  52. 52.
    R. Menzel, C. Durst, J. Erber, et al., “The mushroom bodies in the honeybee: from molecules to behavior. Neural basis for adaptations,” in: Fortschritte der Zoologie, K. Schildberger and N. Elsner (eds.), Gustav Fischer Verlag, Stuttgart (1993), Vol. 39, pp. 81–102.Google Scholar
  53. 53.
    R. Menzel and M. Giurfa, “Cognitive architecture of a minibrain: The honeybee,” Trends Cogn. Sci., 5, 62–71 (2001).PubMedCrossRefGoogle Scholar
  54. 54.
    R. Menzel, M. Giurfa, B. Gerber, and F. Hellstern, “Elementary and configural forms of memory in an insect: the honeybee,” in: Learning: Rule Extraction and Representation, A. D. Friederici and R. Menzel (eds.), Walter de Gruyter, Berlin (1999), pp. 259–282.Google Scholar
  55. 55.
    R. Menzel and G. Manz, “Neural plasticity of mushroom bodyextrinsic neurons in the honeybee brain,” J. Exp. Biol., 208, No. 22, 4317–4332 (2005).PubMedCrossRefGoogle Scholar
  56. 56.
    T. Menzel and U. Müller, “Learning and memory in honeybees: from behavior to neural substrates,” Annu. Rev. Neurosci., 19, 379–404 (1996).PubMedCrossRefGoogle Scholar
  57. 57.
    P. G. Mobbs, “The brain of the honeybee Apis mellifera. I. The connections and spatial organization of the mushroom bodies,” Phil. Trans Roy. Soc. (Ser. B), 298, 309–354 (1982).CrossRefGoogle Scholar
  58. 58.
    R. Okada, J. Rybak, G. Manz, and R. Menzel, “Learning-related plasticity in PE1 and other mushroom body-extrinsic neurons in the honeybee brain,” J. Neurosci., 27, 11736–11747 (2007).PubMedCrossRefGoogle Scholar
  59. 59.
    S. Oleskevich, J. D. Clements, and M. V. Srinivasan, “Long-term synaptic plasticity in the honeybee,” J. Neurophysiol., 78, No. 1, 528–532 (1997).PubMedGoogle Scholar
  60. 60.
    D. Raubenheimer and J. Blackshaw, “Locusts learn to associate visual stimuli with drinking,” J. Insect Behav., 7, 569–575 (1994).CrossRefGoogle Scholar
  61. 61.
    J. Rybak and J. Mauelshagen, “The PE1 neuron of the honeybee – an efferent pathway from the mushroom bodies to the protocerebral lobe,” in: Proc. 22nd Gottingen Neurobiol. Conf., N. Elsner and H. Breer (eds.), Georg Thieme, Stuttgart (1994), Vol. II.Google Scholar
  62. 62.
    J. Rybak and R. Menzel, “Anatomy of the mushroom bodies in the honeybee brain: the neuronal connections of the alpha-lobe,” J. Comp. Neurol., 334, 444–465 (1993).PubMedCrossRefGoogle Scholar
  63. 63.
    J. Rybak and R. Menzel, “Integrative properties of the Pe1-neuron, a unique mushroom body output neuron,” Learn. Mem., 5, 133–145 (1998).PubMedGoogle Scholar
  64. 64.
    J. Rybak and R. Menzel, “Mushroom body of the honeybee,” in: Handbook of Brain Microcircuits, M. Gordon et al. (eds.), Oxford University Press, Oxford (2010), pp. 433–438.CrossRefGoogle Scholar
  65. 65.
    M. Sakura and M. Mizunami, “Olfactory learning and memory in the cockroach Periplaneta americana,” Zool. Sci., 18, 21–28 (2001).CrossRefGoogle Scholar
  66. 66.
    U. Schroter, D. Malun, and R. Menzel, “Innervation pattern of suboesophageal VUM neurons in the honeybee brain,” Cell Tiss. Res., 326, No. 3, 647–667 (2007).CrossRefGoogle Scholar
  67. 67.
    U. Schroter and R. Menzel, “A new ascending sensory tract to the calyces of the honeybee mushroom body, the subesophageal-calycal tract,” J. Comp. Neurol., 465, 168–178 (2003).PubMedCrossRefGoogle Scholar
  68. 68.
    I. Sinakevitch, S. Birman, and B. H. Smith, “An octopamine receptor (AmOA1/OAMB) is expressed in inhibitory neurons in olfactory learning and memory centers in the honeybee and the fruit fly,” Neuroscience 2009, Abstr. No. 350.6/V31, Society for Neuroscience, Chicago.Google Scholar
  69. 69.
    N. J. Strausfeld, “Organization of the honey bee mushroom body: representation of the calyx within the vertical and gamma lobes,” J. Comp. Neurol., 450, 4–33 (2002).PubMedCrossRefGoogle Scholar
  70. 70.
    P. Szyszka, M. Ditzen, A. Galkin, et al., “Sparsening and temporal sharpening of olfactory representations in the honeybee mushroom bodies,” J. Neurophysiol., 94, 3303–3313 (2005).PubMedCrossRefGoogle Scholar
  71. 71.
    P. Szyszka, A. Galkin, and R. Menzel, “Associative and non-associative plasticity in Kenyon cells of the honeybee mushroom body,” Front. Syst. Neurosci., 2, 1–10 (2008).CrossRefGoogle Scholar
  72. 72.
    K. Takeda, “Classical conditioned response in the honey bee,” J. Insect Physiol., 6, 168–179 (1961).CrossRefGoogle Scholar
  73. 73.
    W. H. Thorpe, Learning and Instinct in Animals, Methuen, London (1963).Google Scholar
  74. 74.
    T. Tully and W. G. Quinn, “Classical conditioning and retention in normal and mutant Drosophila melanogaster,” J. Comp. Physiol. A, 157, No. 2, 263–277 (1985).PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  1. 1.I. P. Pavlov Institute of PhysiologySt. PetersburgRussia

Personalised recommendations