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Organization and Plasticity of the Olfactory System of the Honeybee, Apis mellifera

  • Claudine Masson
  • Gérard Arnold

Abstract

From a neurobiological point of view, the olfactory system of the honeybee is of considerable interest. Many adult behavioral responses, such as olfactory conditioning through food reward, suggest plasticity of the nervous system involved in olfactory processing. It seems likely that adult olfactory plasticity may be dependent on the olfactory history of individuals. Here we have selected recently obtained data which suggest that the olfactory system in the bee is especially suitable for an analysis of neuronal plasticity during post-embryonic development. Both normal development, and the role of epigenetic factors in the stabilization of the synapses are considered with respect to their impact on adult behavior. The organization of the antennal system is described in detail to provide a reference point for the developmental studies.

Keywords

Olfactory System Mushroom Body Antennal Lobe Olfactory Pathway Postembryonic Development 
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.

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References

  1. (1).
    Arnold, G., and Masson, C. 1983. Mise en place des connexions synaptiques de la voie afférente antennaire au cours du développement nymphal de l’ouvrière d’abeille Apis mellifica ligustica. C.R. Acad Se Paris III: 131–136.Google Scholar
  2. (2).
    Arnold, G.; Masson, C.; and Budharugsa, S. 1983. Organisation spatiale du système nerveux antennaire de l’abeille étudiée au moyen d’une technique de marquage aux ions cobalt. Apidologie 14 (2): 127–135.CrossRefGoogle Scholar
  3. (3).
    Arnold, G.; Masson, C; and Budharugsa, S. 1984. Demonstration of a sexual dimorphism in the olfactory pathways of the drones (Apis mellifica L., Hymenoptera, Apidae). Experientia 40: 723–725.CrossRefGoogle Scholar
  4. (4).
    Arnold, G.; Masson, C.; and Budharugsa, S. 1985. Comparative study of the antennal afferent pathway of the workerbee and the drone ( Apis mellifera L.) Cell Tiss. Res. 242: 593–605.CrossRefGoogle Scholar
  5. (5).
    Arnold, G.; Masson, C.; and Budharugsa, S. 1986. Spatial organization of the antennal lobe in the queen honeybee. Int. J. Insect Morphol. Empryol., in press.Google Scholar
  6. (6).
    Arnold, G.; Masson, C.; and Denizot, J.P. 1986. Immunocytochemical demonstration of GABA in the honeybee brain. In Proc. Symp. Invertebrate Peptides and Amines. Bordeaux: Soc. Exp. Biol., in press.Google Scholar
  7. (7).
    Barbier, M., and Lederer, E. 1960. Structure chimique de la substance royale de la reine d’abeille. C.R. Acad. Se. Paris 250: 4467–4469.Google Scholar
  8. (8).
    Blum, M.S.; Fales, H.M.; Tucker, K.W.; and Collins, A.M. 1978. Chemistry of the sting apparatus of the worker honeybee. J. Apic. Res. 17 (4): 218–221.Google Scholar
  9. (9).
    Boeckh, J., and Boeckh, V. 1979. Threshold and odor specificity of pheromone sensitive neurons in the deutocerebrum of Antherea pernyi and Antherea polyphemus. J. Comp. Phys. 132 (3): 235–242.CrossRefGoogle Scholar
  10. (10).
    Boeckh, J.; Boeckh, V.; and Kuhn, A. 1977. Further data on the topography and physiology of central olfactory neurons in insects. In Inter. Symp. Olfaction and Taste VI, eds. J. Le Magnen and P. Mac Leod, pp. 315–322. London: IRL.Google Scholar
  11. (11).
    Blum, M.S.; Fales, H.M.; Tucker, K.W.; and Collins, A.M. 1978. Chemistry of the sting apparatus of the worker honeybee. J. Apic. Res. 17 (4): 218–221.Google Scholar
  12. (12).
    Brandon, J.G., and Coss, R.G. 1982. Rapid dendritic spine stem shortening during one-trial learning: the honeybee’s first orientation flight. Brain Research 252: 51–61.PubMedCrossRefGoogle Scholar
  13. (13).
    Burrows, M.; Boeckh, J., and Esslen, J. 1982. Physiological and morphological properties of interneurones in the DTC of male cockroaches which respond to female pheromones. J. Comp. Physiol. 145: 447–457.CrossRefGoogle Scholar
  14. (14).
    Callow, R.K.; Chapman, J.R.; and Paton, P.N. 1964. Pheromones of the honeybee: chemical studies of the mandibular gland secretion of the queen. J. Apic. Res. 3 (2): 77–89.Google Scholar
  15. (15).
    Chambille, I.; Rospars, J. P.; and Masson, C. 1980. The deutocerebrum of the cockroach Blaberus craniifer Burm. Spatial organization of the sensory glomeruli. J. Neurobiol. 11: 1–23.Google Scholar
  16. (16).
    Changeux, J.P.; Heidmann, T.; and Patte, P. 1984. Learning by selection. In The Biology of Learning, eds. P. Marler and H.S. Terrace, pp. 115–133. Berlin: Springer-Verlag.Google Scholar
  17. (17).
    Coss, R.G.; Brandon, J.G.; and Globus, A. 1980. Changes in morphology of dendritic spines on honeybee calycal interneurons associated with cumulative nursing and foraging experiences. Brain Research 192; 49–59.PubMedCrossRefGoogle Scholar
  18. (18).
    Eassa, Y.E.C. 1963. Metamorphosis of the cranial capsule and its appendages in the cabbage butterfly, Pieris brassicae. Ann. Entomol. Soc. Amer. 56: 510–521.Google Scholar
  19. (19).
    Erber, J. 1981. Neural correlates of learning in the honeybee. Trends in Neurosci. 4 (11): 270–273.CrossRefGoogle Scholar
  20. (20).
    Ernst, K.D., and Boeckh, J. 1983. A neuroanatomical study on the organization of the central antennal pathways in insects. Cell Tissue Res. 229: 1–22.PubMedCrossRefGoogle Scholar
  21. (21).
    Esslen, J., and Kaissling, K.E. 1976. Zahl und Verteilung antennaler Sensillen bei der Honigbiene. Zoomorph. 83: 227–251.CrossRefGoogle Scholar
  22. (22).
    Hertel, H. 1983. Change of synapse frequency in certain photoreceptors of the honeybee after chromatic deprivation. J. Comp. Physiol. 151: 477–482.Google Scholar
  23. (23).
    Hildebrand, J.G., and Maxwell, G.D. 1980. Neurochemical explorations of the central nervous system of the moth Manduca sexta and especially of the antennal and visual pathways. In Insect Neurobiology and Pesticide Action (NEUROTOX 79), pp. 101–107. London: Society of Chemical Industry.Google Scholar
  24. (24).
    Hildebrand, J.G.; Hall, L.M. and Osmond, B.C. 1979. Distribution of binding sites for 125 I- labelled bungarotoxin in normal and deafferented antennal lobes of Manduca sexta. Proc. Natl. Acad. Sci. USA 76 (1): 499–503.PubMedCrossRefGoogle Scholar
  25. (25).
    Jawlowski, H. 1957. Nerve tracts in bee (Apis mellifica) running from the sight and antennal organs to the brain. Ann. Univ. Mariae Curie Sklodowska XII, 22: 307–322.Google Scholar
  26. (26).
    Kaissling, K.E., and Thorson, J. 1980. Insect olfactory sensilla: structural chemical and electrical aspects of the functional organization. In Receptors for Neurotransmitters, Hormones and Pheromones in Insects, eds. O.B. Satelle et al., pp. 261–281. Amsterdam: Else vier/North Holland Biomedical Press.Google Scholar
  27. (27).
    Klemm, N. 1974. Vergleichend-histochemische Untersuchungen über die Verteilung monoamin-haltiger Strukturen im Oberschlundganglion von Angehörigen verschiedener Insektenordungen. Ent. germ. J 1: 21–49.Google Scholar
  28. (28).
    Lacher, V. 1964. Elektrophysiologische Untersuchungen an einzelnen Rezeptoren für Geruch, Kohlendioxid, Luftfeuchtigkeit und Temperatur auf den Antennen der Arbeitsbienen und der Drohne (Apis mellifica L.). Z. vergl. Physiol. 48: 587–623.Google Scholar
  29. (29).
    Mc Indoo, N. E. 1922. The auditory sense of the honeybee. Neurol. 34: 173–199.Google Scholar
  30. (30).
    Masson, C. 1977. Central olfactory pathways and plasticity of responses to odorous stimuli in insects. In Int. Symp. Olfaction and Taste VI, eds. J. LeMagnen and P. MacLeod, pp. 315–322. London: IRL.Google Scholar
  31. (31).
    Masson, C. 1984. Neural basis of olfaction in insects. In Comparative Physiology: Sensory Physiology, eds. K. Schmidt-Nielsen, L. Bolis, and S.H.P. Maddrell, pp. 245–255. Cambridge: University Press.Google Scholar
  32. (32).
    Masson, C., and Arnold, G. 1984. Ontogeny, maturation and plasticity of the olfactory system in the workerbee. J. Insect Physiol. 30: 7–14.CrossRefGoogle Scholar
  33. (33).
    Masson, C., and Brossut, R. 1981. La communication chimique chez les insectes. La Recherche 121: 406–416.Google Scholar
  34. (34).
    Masson, C., and Mustaparta, H. 1986. Chemical information processing in the olfactory systems of insects. Physiological Reviews, in press.Google Scholar
  35. (35).
    Matsumoto, S.G., and Hildebrand, J.G. 1981. Olfactory mechanisms in the moth manduca sexta: response characteristics and morphology of central neurons in the antennal lobes. Proc. Roy. Soc. Lond. B. 213: 249–277.Google Scholar
  36. (36).
    Menzel, R.; Erber, J. and Masuhr, T. 1974. Learning and memory in the honeybee. In Experimental Analysis of Insect Behaviour, ed. L. Barton Browne, pp. 195–217. Berlin, Heidelberg, New York: Springer-Verlag.Google Scholar
  37. (37).
    Mercer, A. R.; Mobbs, P. G.; Davenport, A. P. and Evans, P. D. 1983. Biogenic amines in the brain of the honeybee. Cell Tissue Res. 234: 655–677.PubMedCrossRefGoogle Scholar
  38. (38).
    Mobbs, P.G. 1982. The brain of the honeybee Apis mellifica. I. The connections and spatial organization of the mushroom bodies. Phil. Trans. R. Soc. Lond. 298: 309–354.Google Scholar
  39. (39).
    Mobbs, P.G. 1984. Neural networks in the mushroom bodies of the honeybee. J. Insect Physiol. 30 (1): 43–58.CrossRefGoogle Scholar
  40. (40).
    Palka, J. 1984. Precision and plasticity in the insect nervous system. Trends in Neurosci. 7 (12): 455–456.CrossRefGoogle Scholar
  41. (41).
    Panov, A.A. 1961. The structure of the insect brain at successive stages in postembryonic development. 4. The olfactory center. Ent. Rev. 40: 140-145.Google Scholar
  42. (42).
    Pareto, A. 1972. Die zentrale Verteilung der Fühlerafferenz bei Arbeiterrinnen der Honigbiene Apis mellifera L. Z. Zellforsch. Micro. Anat. 131: 109–146.Google Scholar
  43. (43).
    Pham-Delegue, M.H.; Fonta, C.; and Masson, C. 1983. L’apprentissage olfactif chez l’abeille et le bourdon: une étude comparée par conditionnement associatif. C.R. Acad. Sci. Paris, III, 296: 501–506.Google Scholar
  44. (44).
    Pham-Delegue, M.H.; Masson, C.; and Etievant, P. 1986. Selective olfactory choices among food scents by honeybee, a study by coupled associative conditioning and chemical analysis. J. Chem. Ecol. 12 (3): 781–793.CrossRefGoogle Scholar
  45. (45).
    Pickett, J.A.; Williams, I.H.; Martin, A.P. and Smith, M.C. 1980. Nasonov pheromone of the honey bee, Apis mellifera L. (Hymenoptera: Apidae) Part I. Chemical characterization. J. Chem. Ecol. 6 (2): 425–434.CrossRefGoogle Scholar
  46. (46).
    Sanes, J.R., and Hildebrand, J.G. 1976. Structure and development of antennae in the moth Manduca sexta. Developmental Biology 51: 282–299.CrossRefGoogle Scholar
  47. (47).
    Sanes, J.R.; Hildebrand, J.G.; and Prescott, D.J. 1976. Differentiation of insect sensory neurons in the absence of their normal synaptic targets. Developmental Biology 52: 121–127.PubMedCrossRefGoogle Scholar
  48. (48).
    Schäfer, S., and Bicker, G. 1986. Distribution of GABA-like immunoreactivity in the brain of the honeybee. J. Comp. Neurol. 246: 287–300.PubMedCrossRefGoogle Scholar
  49. (49).
    Schneidermann, A.M., and Hildebrand, J.G. 1985. Sexually dimorphism development of the insect olfactory pathway. Trends in Neurosci. 8 (11): 494–499.CrossRefGoogle Scholar
  50. (50).
    Schurmann, F.W. and Klemm, N. 1984. Serotonin-immunoreactive neurons in the brain of the honeybee. J. Comp. Neurol. 225: 570–580.PubMedCrossRefGoogle Scholar
  51. (51).
    Schweitzer, E.S.; Sanes, J.R.; and Hildebrand, J.G. 1976. Ontogeny of electroantennogram responses in the moth, Manduca sexta. J. Insect Physiol. 22: 955–960.Google Scholar
  52. (52).
    Suzuki, H. 1975. Antennal movements induced by odour and central projection of the antennal neurones in the honey bee. J. Insect Physiol. 21: 831–847.CrossRefGoogle Scholar
  53. (53).
    Tolbert, L.P.; Matsumoto, S.G.; and Hildebrand, J.G. 1983. Development of synapses in the antennal lobes of the moth Manduca sexta during metamorphosis. J. Neurosci. 3 (6): 1158–1175.PubMedGoogle Scholar
  54. (54).
    Vareschi, E. 1971. Duftunterscheidung bei der Honigbiene. Einzelzellableitungen und Verhaltensreaktionen. Z. vergl. Physiol. 75: 143–173.Google Scholar

Copyright information

© Springer-Verlag Berlin Heildelberg 1987

Authors and Affiliations

  • Claudine Masson
    • 1
  • Gérard Arnold
    • 1
  1. 1.Laboratoire de Neurobiologie Comparée des InvertebresINRA-CNRS (UA 1190)Bures-sur-YvetteFrance

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