Journal of Computational Neuroscience

, Volume 32, Issue 2, pp 197–212 | Cite as

A model of non-elemental olfactory learning in Drosophila

  • Jan Wessnitzer
  • Joanna M. Young
  • J. Douglas Armstrong
  • Barbara Webb


The pathways for olfactory learning in the fruitfly Drosophila have been extensively investigated, with mounting evidence that that the mushroom body is the site of the olfactory associative memory trace (Heisenberg, Nature 4:266–275, 2003; Gerber et al., Curr Opin Neurobiol 14:737–744, 2004). Heisenberg’s description of the mushroom body as an associative learning device is a testable hypothesis that relates the mushroom body’s function to its neural structure and input and output pathways. Here, we formalise a relatively complete computational model of the network interactions in the neural circuitry of the insect antennal lobe and mushroom body, to investigate their role in olfactory learning, and specifically, how this might support learning of complex (non-elemental; Giurfa, Curr Opin Neuroethol 13:726–735, 2003) discriminations involving compound stimuli. We find that the circuit is able to learn all tested non-elemental paradigms. This does not crucially depend on the number of Kenyon cells but rather on the connection strength of projection neurons to Kenyon cells, such that the Kenyon cells require a certain number of coincident inputs to fire. As a consequence, the encoding in the mushroom body resembles a unique cue or configural representation of compound stimuli (Pearce, Psychol Rev 101:587–607, 1994). Learning of some conditions, particularly negative patterning, is strongly affected by the assumption of normalisation effects occurring at the level of the antennal lobe. Surprisingly, the learning capacity of this circuit, which is a simplification of the actual circuitry in the fly, seems to be greater than the capacity expressed by the fly in shock-odour association experiments (Young et al. 2010).


Computational model Olfactory pathways Mushroom body Coincidence detection Non-elemental 

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  1. Armstrong, D., & van Hemert, J. (2009). Towards a virtual fly brain. Philosophical Transactions of the Royal Society Mathematical, Physical and Engineering Sciences, 367, 2387–2397.CrossRefGoogle Scholar
  2. Aso, Y., Gruebel, K., Busch, S., Friedrich, A., Siwanowicz, I., et al. (2009). The mushroom body of adults Drosophila characterized by GAL4 drivers. Journal of Neurogenetics, 23, 156–172.PubMedCrossRefGoogle Scholar
  3. Assisi, C., Stopfer, M., Laurent, G., & Bazhenov, M. (2007). Adaptive regulation of sparseness by feedforward inhibition. Nature Neuroscience, 10, 1176–1184.PubMedCrossRefGoogle Scholar
  4. Brembs, B., & Wiener, J. (2006). Context and occasion setting in Drosophila visual learning. Learning and Memory, 13, 618–628.PubMedCrossRefGoogle Scholar
  5. Busto, G., Cervantes-Sandoval, I., & Davis, R. (2010). Olfactory learning in Drosophila. Physiology, 25, 338–346.PubMedCrossRefGoogle Scholar
  6. Cassenaer, S., & Laurent, G. (2007). Hebbian STDP in mushroom bodies facilitates the synchronous flow of olfactory information in locusts. Nature, 448, 709–713. doi:10.1038/nature05973.PubMedCrossRefGoogle Scholar
  7. Chittka, L., & Niven, J. (2009). Are bigger brains better? Current Biology, 19, R995–R1008.CrossRefGoogle Scholar
  8. Chou Y. H., Spletter, M., Yaksi, E., Leong, J., Wilson, R., et al. (2010). Diversity and wiring variability of olfactory local interneurons in the Drosophila antennal lobe. Nature Neuroscience, 13, 439–449.PubMedCrossRefGoogle Scholar
  9. Claridge-Chang, A., Roorda, R., Vrontou, E., Sjulson, L., Li, H., et al. (2009). Writing memories with light-addressable reinforcement circuitry. Cell, 139, 405–415.PubMedCrossRefGoogle Scholar
  10. Cleland, T., & Linster, C. (1999). Concentration tuning mediated by spare receptor capacity in olfactory sensory neurons: A theoretical study. Neural Computation, 11, 1673–1690.PubMedCrossRefGoogle Scholar
  11. Couto, A., Alenius, M., & Dickson, B. (2005). Molecular, anatomical, and functional organization of the Drosophila olfactory system. Current Biology, 17, 1535–1547.CrossRefGoogle Scholar
  12. Deisig, N., Lachnit, H., Giurfa, M., & Hellstern, F. (2001). Configural olfactory learning in honeybees: Negative and positive patterning discrimination. Learning and Memory, 8, 70–78.PubMedCrossRefGoogle Scholar
  13. Gerber, B., Tanimoto, H., & Heisenberg, M. (2004). An engram found? Evaluating the evidence from fruit flies. Current Opinion in Neurobiology, 14, 737–744.PubMedCrossRefGoogle Scholar
  14. Giurfa, M. (2003). Cognitive neuroethology: Dissecting non-elemental learning in a honeybee brain. Current Opinion in Neuroethology, 13, 726–735.CrossRefGoogle Scholar
  15. Gutierrez-Osuna, R. (2002). A self-organizing model of chemotopic convergence for olfactory coding. In Proceedings of the second joint EMBS/BMES conference (pp. 236–237). Houston, TX, USA.Google Scholar
  16. Hallem, E., Dahanukar, A., & Carlson, J. (2006). Insect odor and taste receptors. Annual Review of Entomology, 51, 113–135.PubMedCrossRefGoogle Scholar
  17. Heisenberg, M. (2003). Mushroom body memoir: From maps to models. Nature, 4, 266–275.Google Scholar
  18. Huang, J., Zhang, W., Qiao, W., Hu, A., & Wang, Z. (2010). Functional connectivity and selective odor responses of excitatory local interneurons in Drosophila antennal lobe. Neuron, 67, 1021–1033.PubMedCrossRefGoogle Scholar
  19. Huerta, R., & Nowotny, T. (2009). Fast and robust learning by reinforcement signals: Explorations in the insect brain. Neural Computation, 21, 2123–2151.PubMedCrossRefGoogle Scholar
  20. Huerta, R., Nowotny, T., Garcia-Sanchez, M., Abarbanel, H., & Rabinovich, M. (2004). Learning classification in the olfactory system of insects. Neural Computation, 16, 1601–1640.PubMedCrossRefGoogle Scholar
  21. Ito, I., Bazhenov, M., Ying Ong R.C., Raman, B., & Stopfer, M. (2009). Frequency transitions in odor-evoked neural oscillations. Neuron, 64, 692–706.PubMedCrossRefGoogle Scholar
  22. Izhikevich, E. (2007a). Dynamical systems in neuroscience: The geometry of excitability and bursting. Cambridge, MIT Press.Google Scholar
  23. Izhikevich, E. (2007b). Solving the distal reward problem through linkage of STDP and dopamine signaling. Cerebral Cortex, 17, 2443–2452.PubMedCrossRefGoogle Scholar
  24. Jayaraman, V., & Laurent, G. (2009). Olfactory system: Circuit dynamics and neural coding in the locust. In Encyclopedia of neuroscience (pp. 187–196).Google Scholar
  25. Keene, A., & Waddell, S. (2007). Drosophila olfactory memory: Single genes to complex neural circuits. Nature Reviews Neuroscience, 8, 341–354.PubMedCrossRefGoogle Scholar
  26. Kohonen, T. (1990). The self-organizing map. Proceedings of the IEEE, 78, 1464–1480.CrossRefGoogle Scholar
  27. Komischke, B., Sandoz, J. C., Lachnit, H., & Giurfa, M. (2003). Non-elemental processing in olfactory discrimination tasks needs bilateral input in honeybees. Behavioral Brain Research, 145, 135–143.CrossRefGoogle Scholar
  28. Krashes, M., Keene, A., Leung, B., Armstrong, D., & Waddell, S. (2007). Sequential use of mushroom body neuron subsets during Drosophila odor memory processing. Neuron, 53, 103—115.PubMedCrossRefGoogle Scholar
  29. Laissue, P., Reiter, C., Hiesinger, P., Halter, S., Fischbach, K., et al. (1999) Three-dimensional reconstruction of the antennal lobe in Drosophila melanogaster. Journal of Comparative Neurology, 405, 543–552.PubMedCrossRefGoogle Scholar
  30. Lancet, D., Sadovsky, E., & Seidemann, E. (1993). Probability model for molecular recognition in biological receptor repertoires: Significance to the olfactory system. Proceedings of the National Academy of Sciences (PNAS), 90, 3715–3719.CrossRefGoogle Scholar
  31. Liang, L., & Luo, L. (2010). The olfactory circuit of the fruit fly Drosophila melanogaster. Science China Life Sciences, 53, 472–484.PubMedCrossRefGoogle Scholar
  32. Linster, C., Sachse, S., & Galizia, G. (2005). Computational modeling suggests that response properties rather than spatial position determine connectivity between olfactory glomeruli. Journal of Neurophysiology, 93, 3410–3417.PubMedCrossRefGoogle Scholar
  33. Martinez, D., & Montejo, N. (2008). A model of stimulus-specific neural assemblies in the insect antennal lobe. PLoS Computational Biology, 4, e1000139.PubMedCrossRefGoogle Scholar
  34. Masuda-Nakagawa, L., Tanaka, N., & O’Kane, C. (2005). Stereotypic and random patterns of connectivity in the larval mushroom body calyx of Drosophila. Proceedings of the National Academy of Sciences (PNAS), 102, 19027–19032.CrossRefGoogle Scholar
  35. Matsumoto, Y., & Mizunami, M. (2004). Context-dependent olfactory learning in an insect. Learning and Memory, 11, 288–293.PubMedCrossRefGoogle Scholar
  36. Mizunami, M., Unoki, S., Mori, Y., Hirashima, D., Hatano, A., et al. (2009). Roles of octopaminergic and dopaminergic neurons in appetitive and aversive memory recall in an insect. BMC Biology, 7, 46.PubMedCrossRefGoogle Scholar
  37. Murthy, M., Fiete, I., & Laurent, G. (2008). Testing odor response stereotypy in the Drosophila mushroom body. Neuron, 59, 1009–1023.PubMedCrossRefGoogle Scholar
  38. Nowotny, T., Huerta, R., Abarbanel, H., & Rabinovich, M. (2005). Self-organization in the olfactory system: One shot odor recognition in insects. Biological Cybernetics, 93, 436–446.PubMedCrossRefGoogle Scholar
  39. Olsen, S., Bhandawat, V., & Wilson, R. (2010). Divisive normalization in olfactory population codes. Neuron, 66, 287–299.PubMedCrossRefGoogle Scholar
  40. Pearce, J. (1994). Similarity and discrimination: A selective review and a connectionist model. Psychological Review, 101, 587–607.PubMedCrossRefGoogle Scholar
  41. Rescorla, R. (1973). Evidence for “unique stimulus” account of configural conditioning. Journal of Comparative and Physiological Psychology, 85, 331–338.CrossRefGoogle Scholar
  42. Sato, C., Matsumoto, Y., Sakura, M., & Mizunami, M. (2006). Contextual olfactory learning in cockroaches. NeuroReport, 17, 553–557.PubMedCrossRefGoogle Scholar
  43. Schubert, M., Lachnit, H., Francucci, S., & Giurfa, M. (2002). Non-elemental visual learning in honeybees. Animal Behaviour, 64, 175–184.CrossRefGoogle Scholar
  44. Schwaerzel, M., Heisenberg, M., & Zars, T. (2002). Extinction antagonizes olfactory memory at the subcellular level. Neuron, 35, 951–960.PubMedCrossRefGoogle Scholar
  45. Seki, Y., Rybak, J., Wicher, D., Sachse, S., & Hansson, B. (2010). Physiological and morphological characterization of local interneurons in the Drosophila antennal lobe. Journal of Neurophysiology, 104, 1007–1019.PubMedCrossRefGoogle Scholar
  46. Silbering, A., & Galizia, G. (2007). Processing of odor mixtures in the Drosophila antennal lobe reveals both global inhibition and glomerulus-specific interactions. Journal of Neuroscience, 27, 11966–11977.PubMedCrossRefGoogle Scholar
  47. Smith, D., Wessnitzer, J., & Webb, B. (2008). A model of associative learning in the mushroom body. Biological Cybernetics, 99, 89–103.PubMedCrossRefGoogle Scholar
  48. Song, S., Miller, K., & Abbott, L. (2000). Competitive Hebbian learning through spike-timing-dependent synaptic plasticity. Nature Neuroscience, 3, 919–926.PubMedCrossRefGoogle Scholar
  49. Tanaka, N., Tanimoto, H., & Ito, K. (2008). Neuronal assemblies of the Drosophila mushroom body. Journal of Comparative Neurology, 508, 711–755.PubMedCrossRefGoogle Scholar
  50. Thum, A., Jenett, A., Ito, K., Heisenberg, M., & Tanimoto, H. (2007). Multiple memory traces for olfactory reward learning in Drosophila. Journal of Neuroscience, 27, 11132–11138.PubMedCrossRefGoogle Scholar
  51. Tomchik, S., & Davis, R. (2009). Dynamics of learning-related camp signaling and stimulus integration in the Drosophila olfactory pathway. Neuron, 64, 510–521.PubMedCrossRefGoogle Scholar
  52. Turner, G., Bazhenov, M., & Laurent, G. (2008). Olfactory representations by Drosophila mushroom body neurons. Journal of Neurophysiology, 99, 734–746.PubMedCrossRefGoogle Scholar
  53. Waddell, S. (2010). Dopamine reveals neural circuit mechanisms of fly memory. Trends in Neurosciences, 33, 457–464.PubMedCrossRefGoogle Scholar
  54. Wang, J., Wong, A., Flores, J., Vosshall, L., & Axel, R. (2003). Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell, 112, 271–282.PubMedCrossRefGoogle Scholar
  55. Wessnitzer, J., Webb, B., & Smith, D. (2007). A model of non-elemental associative learning in the Mushroom Body neuropil of the insect brain. In Proceedings of the international conference on adaptive and natural computing algorithms ICANNGA’07 (pp. 488–497). Warsaw, Poland.Google Scholar
  56. Wilson, R., Turner, G., & Laurent, G. (2004). Transformation of olfactory representations in the Drosophila antennal lobe. Science, 303, 366–370.PubMedCrossRefGoogle Scholar
  57. Wuestenberg, D., Boytcheva, M., Gruenewald, B., Byrne, J., Menzel, R., et al. (2004) Current- and voltage-clamp recordings and computer simulations of Kenyon cells in the honeybee. Journal of Neurophysiology, 92, 2589–2603.CrossRefGoogle Scholar
  58. Yamagata, N., Schmuker, M., Szyszka, P., Mizunami, M., & Menzel, R. (2009). Differential odor processing in two olfactory pathways in the honeybee. Frontiers in Systems Neuroscience, 3, Article 16, 1–13.CrossRefGoogle Scholar
  59. Yarali, A., Hendel, T., & Gerber, B. (2006). Olfactory learning and behaviour are ‘insulated’ against visual processing in larval Drosophila. Journal of Comparative Physiology A, 192, 1133–1145.CrossRefGoogle Scholar
  60. Yarali, A., Mayerle, M., Nawroth, C., & Gerber, B. (2008). No evidence for visual context-dependency of olfactory learning in Drosophila. Naturwissenschaften, 95, 767–774.PubMedCrossRefGoogle Scholar
  61. Young, J., Wessnitzer, J., Armstrong, J., & Webb, B. (2010). Can flies learn complex olfactory associations? In International congress on neuroethology abstract. Salamanca, Spain.Google Scholar
  62. Yu, D., Ponomarev, A., & Davis, R. (2004). Altered representation of the spatial code for odors after olfactory classical conditioning: Memory trace formation by synaptic recruitment. Neuron, 42, 437–449.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Jan Wessnitzer
    • 1
  • Joanna M. Young
    • 1
    • 2
  • J. Douglas Armstrong
    • 2
  • Barbara Webb
    • 1
  1. 1.Institute of Perception, Action and Behaviour, School of InformaticsUniversity of EdinburghEdinburghUK
  2. 2.Institute for Adaptive Neural Computation, School of InformaticsUniversity of EdinburghEdinburghUK

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