Representations of odours and odour mixtures visualized in the honeybee brain

Abstract

Most animals depend on the identification of odours to locate food or to find mating partners. To accomplish this, the olfactory system must recognize relative concentrations of a large number of substances by analysing complex patterns of chemoreceptor activations1,2, but how these patterns are represented in the brain is not well understood. Previous studies indicated that odours evoke specific patterns of activity in olfactory sensory centres3–7 and led to the hypothesis that single glomeruli in the olfactory bulb of mammals respond to particular receptor types8–10. We made optical recordings in vivo in the honeybee brain to investigate neuronal population responses to odorants delivered naturally to the animal. We report here that odours evoked specific spatio–temporal excitation patterns in the antennal lobe, the structural and functional analogue of the olfactory bulb11. Specific ensembles of active glomeruli represent odours in a combinatorial manner. A comparison between different individuals shows remarkable similarities for a pheromone component, but not for general flower odours. Mixtures evoked patterns that were combinations of the single odorant responses. These combinations were not fully additive, however, indicating inhibitory effects on single glomeruli. Such interactions could be crucial for the formation of singular codes for complex odour blends.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1

    Shepherd, G. M. in Olfaction: A Model System for Computational Neurosdence (eds Davis, J. & Eichenbaum, H.) 3–41 (MIT Press, Cambridge, MA, 1991).

  2. 2

    Laurent, G. Odor Images and Tunes. Neuron 16, 473–476 (1996).

  3. 3

    Stewart, W. B., Kauer, J. S. & Shepherd, G. M. Functional organization of rat olfactory bulb analyzed by the 2-deoxyglucose method. J. Comp. Neurol. 185, 715–734 (1979).

  4. 4

    Kauer, J. S. Real-time imaging of evoked activity in local circuits of the salamander olfactory bulb. Nature 331, 166–168 (1988).

  5. 5

    Rodrigues, V. spatial coding of olfactory information in the antennal lobe of Drosophila melanogaster. Brain Res. 453, 299–307 (1988).

  6. 6

    Lieke, E. Optical recording of neuronal activity in the insect central nervous system: odorant coding by the antennal lobes of honeybees. Eur. J. Neurosd. 5, 49–55 (1993).

  7. 7

    Cinelli, A. R., Hamilton, K. A. & Kauer, J. S. Salamander olfactory bulb neuronal activity observed by video rate, voltage-sensitive dye imaging. III. Spatial and temporal properties of responses evoked by odorant stimulation. J. Neurophysiol. 73, 2053–2071 (1995).

  8. 8

    Vassar, R. et al. Topographic organization of sensory projections in the olfactory bulb. Cell 79, 981–991 (1994).

  9. 9

    Ressler, K. J., Sullivan, K. J. & Buck, L. B. Information coding in the olfactory system: evidence for a stereotyped and highly organized epitope map in the olfactory bulb. Cell 79, 1245–1255 (1994).

  10. 10

    Mombaerts, P. et al. Visualizing an olfactory sensory map. Cell 87, 675–686 (1996).

  11. 11

    Boeckh, J., Distler, P., Ernst, K. D., Hösl, M. & Malun, D. in Chemosensory Information Processing (ed. Schild, D.) 201–227 (Springer, Berlin, 1990).

  12. 12

    Firestein, S., Picco, C. & Menini, A. The relation between stimulus and response in olfactory receptor cells of the tiger salamander. J. Physiol. 468, 1–10 (1993).

  13. 13

    Schild, D. Signal integration in the olfactory system. Trends Neurosci. 17, 366–367 (1994).

  14. 14

    Christensen, T. A., Waldrop, B. R., Harrow, I. D. & Hildebrand, J. G. Local interneurons and information processing in the olfactory glomeruli of the moth Manduca sexta. J. Comp. Physiol. A 173, 385–399 (1993).

  15. 15

    Sun, X., Fonta, C. & Masson, C. Odour quality processing by bee antennal lobe interneurones. Chem. Senses 18, 355–377 (1993).

  16. 16

    Mori, K. & Yoshihara, Y. Molecular recognition and olfactory processing in the mammalian olfactory system. Progr. Neurobiol 45, 585–619 (1995).

  17. 17

    Wehr, M. & Laurent, G. Odour encoding by temporal sequences of firing in oscillating neural assemblies. Nature 384, 162–166 (1996).

  18. 18

    Flanagan, D. & Mercer, A. R. An atlas and 3-D reconstruction of the antennal lobes in the worker honeybee, Apis mellifera. Int. J. Insect Morphol. Embryol. 18, 145–159 (1989).

  19. 19

    Christensen, T. A., Hildebrand, J. G., Tumlinson, J. H. & Doolittle, R. E. Sex pheromone blend of Manduca sexta: responses of central olfactory interneurons to antennal stimulation in male moths. Arch. Insect Biochem. Physiol. 10, 281–291 (1989).

  20. 20

    Tank, D. W., Gelperin, A. & Kleinfeld, D. Odors, oscillations, and waves: does it all compute? Science 265, 1819–1820 (1994).

  21. 21

    Hanson, B. S., Ljungberg, H., Hallberg, E. & Löfstedt, C. Functional specialization of olfactory glomeruli in a moth. Science 256, 1313–1315 (1992).

  22. 22

    Pelz, C., Gerber, B. & Menzel, R. Odorant intensity as a determinant for olfactory conditioning in honeybees: roles in discrimination, overshadowing and memory consolidation. J. Exp. Biol. 200, 837–847 (1997).

  23. 23

    Yuste, R. & Katz, L. C. Control of postsynaptic Ca++ influx in developing neocortex by excitatory and inhibitory neurotransmitters. Neuron 6, 333–344 (1991).

  24. 24

    O'Donovan, M. J., Ho, S., Sholomenko, G. & Yee, W. Realtime imaging of neurons retrogradely and anterogradely labelled with calcium-sensitive dyes. J. Neurosci. Meth. 46, 91–106 (1993).

  25. 25

    Akers, R. P. & Getz, W. M. Response of olfactory receptor neurons in honey bees to odorants and their binary mixtures. J. Comp. Physiol. A 173, 169–185 (1993).

  26. 26

    Distler, P. GABA-immunohistochemistry as a label for identifying types of local interneurons and their synaptic contacts in the antennal lobes of the american cockroach. Histochemistry 93, 617–626 (1990).

  27. 27

    Hansson, B. S., Anton, S. & Christensen, T. A. Structure and function of antennal lobe neurons in the male turnip moth, Agrotis segetum. J. Comp. Physiol. A 175, 547–562 (1994).

  28. 28

    Ache, B. W. Towards a common strategy for transducing olfactory information. Semin. Cell Biol. 5, 55–63 (1994).

  29. 29

    Hammer, M. & Menzel, R. Learning and memory in the honeybee. J. Neurosci. 15, 1617–1630 (1995).

  30. 30

    Kendrick, K. M., Levy, F. & Keverne, E. B. Changes in the sensory processing of olfactory signals induced by birth in sheep. Science 256, 833–836 (1992).

  31. 31

    Friedrich, R. W. & Karsching, S. I. Neuron 833–836 (in the press).

Download references

Author information

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Joerges, J., Küttner, A., Galizia, C. et al. Representations of odours and odour mixtures visualized in the honeybee brain. Nature 387, 285–288 (1997). https://doi.org/10.1038/387285a0

Download citation

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.