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Associative learning modifies neural representations of odors in the insect brain

Abstract

Recording brain activity in vivo during learning is fundamental to understanding how memories are formed. We used functional calcium imaging to track odor representations in the primary chemosensory center of the honeybee, the antennal lobe, while training animals to discriminate a rewarded odor from an unrewarded one. Our results show that associative learning transforms odor representations and decorrelates activity patterns for the rewarded versus the unrewarded odor, making them less similar. Additionally, activity for the rewarded but not for the unrewarded odor is increased. These results indicate that neural representations of the environment may be modified through associative learning.

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Figure 1: Quantitative changes in odor–evoked activity patterns in the bee brain induced by learning.
Figure 2: Quantitative analysis reveals analogous results for imaging and behavioral data.
Figure 3: Learning leads to a qualitative change in odor representations.

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References

  1. Karni, A. et al. Functional MRI evidence for adult motor cortex plasticity during motor skill learning. Nature 377, 155– 158 (1995).

    Article  CAS  Google Scholar 

  2. Recanzone, G. H. et al. Topographic reorganization of the hand representation in cortical area 3b of owl monkeys trained in a frequency–discrimination task. J. Neurosci. 67, 1031– 1056 (1992).

    CAS  Google Scholar 

  3. Shadmehr, R. & Holcomb, H. H. Neural correlates of motor memory consolidation. Science 277, 821– 825 (1997).

    Article  CAS  Google Scholar 

  4. Brennan, P. A. et al. Changes in neurotransmitter release in the main olfactory bulb following an olfactory conditioning procedure in mice. Neuroscience 3, 583–590 ( 1998).

    Article  Google Scholar 

  5. Wilson, M. A. & McNaughton, B. L. Dynamics of the hippocampal ensemble code for space. Science 261, 1055 –1058 (1993).

    Article  CAS  Google Scholar 

  6. Rogan, T. R., Stäubli, U. V. & LeDoux, J. E. Fear conditioning induces associative long–term potentiation in the amygdala. Nature 390, 604–610 (1997).

    Article  CAS  Google Scholar 

  7. Schoenbaum, G. & Eichenbaum, H. Information coding in the rodent prefrontal cortex. I. single–neuron activity in orbitofrontal cortex compared with that in pyriform cortex. J. Neurophysiol. 74, 733–750 (1995).

    Article  CAS  Google Scholar 

  8. Hawkins, R. D., Abrams, T. W., Carew, T. J. & Kandel, E. R. A cellular mechanism of classical conditioning in Aplysia: activity–dependent amplification of presynaptic facilitation. Science 219, 400–405 (1983).

    Article  CAS  Google Scholar 

  9. Mauelshagen, J. Neural correlates of olfactory learning paradigms in an identified neuron in the honeybee brain. J. Neurophysiol. 69, 609–625 (1993).

    Article  CAS  Google Scholar 

  10. Hammer, M. An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees. Nature 366, 59– 63 (1993).

    Article  CAS  Google Scholar 

  11. Joerges, J., Küttner, A., Galizia, G. & Menzel, R. Representations of odours and odour mixtures visualized in the honeybee brain. Nature 387, 285–288 (1997).

    Article  CAS  Google Scholar 

  12. Hildebrand, J. G. & Shepherd, G. M. Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu. Rev. Neurosci. 20, 595– 631 (1997).

    Article  CAS  Google Scholar 

  13. Galizia, C. G., Nägler, K., Hölldobler, B. & Menzel, R. Odour coding is billaterally symmetrical in the antennal lobes of honeybees (Apis mellifera). Eur. J. Neurosci. 10, 2964–2974 (1998).

    Article  CAS  Google Scholar 

  14. Bitterman, M. E., Menzel, R., Fietz, A. & Schäfer, S. Classical conditioning of proboscis extension in the honeybees (Apis mellifera). J. Comp. Physiol. 97, 107– 119 (1983).

    CAS  Google Scholar 

  15. Menzel, R. & Müller, U. Learning and memory in honeybees: From behavior to neural substrates. Annu. Rev. Neurosci. 19, 379–404 (1996).

    Article  CAS  Google Scholar 

  16. Galizia, G., McIlwrath, S. L. & Menzel, R. A digital 3D atlas of the honeybee antennal lobe based on optical sections acquired using confocal microscopy. Cell Tissue Res. (in press).

  17. Hammer, M., Braun, G. & Mauelshagen, J. Food induced arousal and nonassociative learning in honeybees: dependence of sensitization on the application site and duration of food stimulation. Behav. Neural Biol. 62, 210–223 (1994).

    Article  CAS  Google Scholar 

  18. Rehder, V. Quantification of the honeybee's proboscis reflex by electromyographic recordings. J. Insect Physiol. 33, 501– 507 (1987).

    Article  Google Scholar 

  19. Smith, B. The olfactory memory in the honeybee apis mellifera I. odorant modulation of short– and intermediate–term memory after single–trial conditioning. J. Exp. Biol. 161, 367– 382 (1991).

    Google Scholar 

  20. Rescorla, R. A. & Wagner, A. R. in Classical conditioning II Theory and Research (eds Black, A. H. & Prolcasy, W. F.) 64–99 (Appleton–Century–Crafts, New York, 1972).

    Google Scholar 

  21. Menzel, R. in Neurobiology of Comparative Cognition (eds Kesner, R. P. & Olton, D. S.) 237–292 (Lawrence Erlbaum, Hillsdale, New Jersey, 1990).

    Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  24. Hawkins, R. D., Kandel, E. R. & Siegelbaum, S. A. Learning to modulate transmitter release: themes and variations in synaptic plasticity. Annu. Rev. Neurosci. 16, 626–665 (1993).

    Article  Google Scholar 

  25. Yuste, R. & Denk, W. Dendritic spines as basic functional units of neuronal integration. Nature 375, 682–684 (1995).

    Article  CAS  Google Scholar 

  26. Linster, C. & Hasselmo, M. Modulation of inhibition in a model of olfactory bulb reduces overlap in the neural representation of olfactory stimuli. Behav. Brain Res. 84, 117– 127 (1997).

    Article  CAS  Google Scholar 

  27. Laurent, G. & Davidowitz, H. Encoding of olfactory information with oscillating neural assemblies. Science 265, 1872–1875 (1994).

    Article  CAS  Google Scholar 

  28. Laurent, G., Wehr, M. & Davidowitz, H. Temporal representations of odors in an olfactory network. J. Neurosci. 16, 3837– 3847 (1996).

    Article  CAS  Google Scholar 

  29. Stopfer, M., Bhagavan, S., Smith, B. H. & Laurent, G. Impaired odour discrimination on desynchronization of odour–encoding neural assemblies. Nature 390, 70– 74 (1997).

    Article  CAS  Google Scholar 

  30. Davis, R. L. Mushroom bodies and drosophila learning. Neuron 11, 1–14 (1993).

    Article  CAS  Google Scholar 

  31. de Belle, J. S. & Heisenberg, M. Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science 263, 692– 695 (1994).

    Article  CAS  Google Scholar 

  32. Heisenberg, M., Borst, A., Wagner, S. & Byers, D. Drosophila mushroom body mutants are deficient in olfactory learning. J. Neurogenet. 2, 1–30 (1985 ).

    Article  CAS  Google Scholar 

  33. Connolly, J. B. et al. Associative learning disrupted by impaired Gs signaling in Drosophila mushroom bodies. Science 275, 2104–2107 (1996).

    Article  Google Scholar 

  34. Menzel, R. et al. The mushroom bodies in the honeybee: From molecules to behavior. Fortschritte Zoologie 39, 81– 102 (1994).

    CAS  Google Scholar 

  35. Hammer, M. & Menzel, R. Multiple sites of associative odor learning as revealed by local brain microinjections of octopamin in honeybees. Learn. Mem. 5, 146–156 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Galizia, G. C. et al. A semi–in–vivo preparation for optical recording of the insect brain. J. Neurosci. Methods 76, 61–69 (1997).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Thanks to M. Giurfa for statistical advice and comments. We also thank G. Galizia, B. Gerber, P. Stevenson and S. Sachse for discussions and comments on the manuscript and G. Manz for technical support in the behavioral experiments.

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Correspondence to Till Faber.

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Faber, T., Joerges, J. & Menzel, R. Associative learning modifies neural representations of odors in the insect brain. Nat Neurosci 2, 74–78 (1999). https://doi.org/10.1038/4576

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