Advertisement

Dynamics of Odor-Evoked Activity Patterns in the Olfactory System

  • Thomas Nowotny
  • Paul Szyszka
Chapter
Part of the Nonlinear Systems and Complexity book series (NSCH, volume 20)

Abstract

Olfaction, the sense of smell, has the reputation of being slow compared to other senses such as vision and hearing. Consequently, constant stimuli are commonly used in olfaction research. However, in natural conditions, animals encounter fine-scale temporal patterns of odorant stimuli, which contain information not only about odor identity but also about the distance and number of odorant sources. New tools for monitoring and controlling stimulus dynamics in the lab have promoted our understanding of how temporal stimulus cues are processed in the olfactory system. In this chapter we contrast classic and recent studies on olfactory coding, and discuss some physiological and behavioral constraints on a neural code for odor identity, concentration, and temporal stimulus structure.

Keywords

Olfaction Odor stimulus dynamics Olfactory coding 

References

  1. 1.
    Hildebrand, J.G., Shepherd, G.M.: Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu. Rev. Neurosci. 20, 595–631 (1997)CrossRefGoogle Scholar
  2. 2.
    Nakagawa, T., Vosshall, L.B.: Controversy and consensus: noncanonical signaling mechanisms in the insect olfactory system. Curr. Opin. Neurobiol. 19 (3), 284–292 (2009)CrossRefGoogle Scholar
  3. 3.
    Sato, K., Pellegrino, M., Nakagawa, T., Nakagawa, T., Vosshall, L.B., Touhara, K.: Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature 452 (7190), 1002–1006 (2008)CrossRefGoogle Scholar
  4. 4.
    Silbering, A.F., Benton, R.: Ionotropic and metabotropic mechanisms in chemoreception: ‘chance or design’? EMBO Rep. 11 (3), 173–179 (2010)CrossRefGoogle Scholar
  5. 5.
    Vosshall, L.B., Hansson, B.S.: A unified nomenclature system for the insect olfactory coreceptor. Chem. Senses 36 (6), 497–498 (2011)CrossRefGoogle Scholar
  6. 6.
    Wicher, D., Schäfer, R., Bauernfeind, R., Stensmyr, M.C., Heller, R., Heinemann, S.H., Hansson, B.S.: Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels. Nature 452 (7190), 1007–1011 (2008)CrossRefGoogle Scholar
  7. 7.
    Clyne, P.J., Warr, C.G., Freeman, M.R., Lessing, D., Kim, J., Carlson, J.R.: A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron 22 (2), 327–338 (1999)CrossRefGoogle Scholar
  8. 8.
    Vosshall, L.B., Wong, A.M., Axel, R.: An olfactory sensory map in the fly brain. Cell 102, 147–159 (2000)CrossRefGoogle Scholar
  9. 9.
    Hallem, E.A., Ho, M.G., Carlson, J.R.: The molecular basis of odor coding in the Drosophila antenna. Cell 117 (7), 965–979 (2004)CrossRefGoogle Scholar
  10. 10.
    Gao, Q., Yuan, B., Chess, A.: Convergent projections of Drosophila olfactory neurons to specific glomeruli in the antennal lobe. Nat. Neurosci. 3, 780–785 (2000)CrossRefGoogle Scholar
  11. 11.
    Galizia, C.G., Menzel, R.: Odour perception in honeybees: coding information in glomerular patterns. Curr. Opin. Neurobiol. 10, 504–510 (2000)CrossRefGoogle Scholar
  12. 12.
    Hansson, B.S., Carlsson, M.A., Kalinová, B.: Olfactory activation patterns in the antennal lobe of the sphinx moth, manduca sexta. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 189 (4), 301–308 (2003)Google Scholar
  13. 13.
    Joerges, J., Küttner, A., Galizia, C.G., Menzel, R.: Representations of odour mixtures visualized in the honeybee brain. Nature 387, 285–288 (1997)CrossRefGoogle Scholar
  14. 14.
    Wilson, R., Mainen, Z.F.: Early events in olfactory processing. Annu. Rev. Neurosci. 29, 163–201 (2006)CrossRefGoogle Scholar
  15. 15.
    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 (4), 385–399 (1993)CrossRefGoogle Scholar
  16. 16.
    Christensen, T.A., Waldrop, B.R., Hildebrand, J.G.: Gabaergic mechanisms that shape the temporal response to odors in moth olfactory projection neurons. Ann. N. Y. Acad. Sci. 855, 475–481 (1998)CrossRefGoogle Scholar
  17. 17.
    Christensen, T.A., Waldrop, B.R., Hildebrand, J.G.: Multitasking in the olfactory system: context-dependent responses to odors reveal dual gaba-regulated coding mechanisms in single olfactory projection neurons. J. Neurosci. 18 (15), 5999–6008 (1998)Google Scholar
  18. 18.
    Sachse, S., Galizia, C.G.: Role of inhibition for temporal and spatial odor representation in olfactory output neurons: a calcium imaging study. J. Neurophysiol. 87, 1106–1117 (2002)CrossRefGoogle Scholar
  19. 19.
    Wilson, R.I., Laurent, G.: Role of gabaergic inhibition in shaping odor-evoked spatiotemporal patterns in the Drosophila antennal lobe. J. Neurosci. 25, 9069–79 (2005)CrossRefGoogle Scholar
  20. 20.
    Olsen, S.R., Bhandawat, V., Wilson, R.: Excitatory interactions between olfactory processing channels in the Drosophila antennal lobe. Neuron 54 (1), 89–103 (2007)CrossRefGoogle Scholar
  21. 21.
    Shang, Y., Claridge-Chang, A., Sjulson, L., Pypaert, M., Miesenböck, G.: Excitatory local circuits and their implications for olfactory processing in the fly antennal lobe. Cell 128 (3), 601–612 (2007)CrossRefGoogle Scholar
  22. 22.
    Silbering, A.F., Galizia, C.G.: Processing of odor mixtures in the Drosophila antennal lobe reveals both global inhibition and glomerulus-specific interactions. J. Neurosci. 27 (44), 11966–11977 (2007)CrossRefGoogle Scholar
  23. 23.
    Silbering, A.F., Okada, R., Ito, K., Galizia, C.G.: Olfactory information processing in the Drosophila antennal lobe: anything goes? J. Neurosci. 28 (49), 13075–13087 (2008)CrossRefGoogle Scholar
  24. 24.
    Davis, R.L.: Mushroom bodies and Drosophila learning. Neuron 11, 1–14 (1993)CrossRefGoogle Scholar
  25. 25.
    Davis, R.L.: Traces of Drosophila memory. Neuron 70 (1), 8–19 (2011)CrossRefGoogle Scholar
  26. 26.
    Heisenberg, M.: Mushroom body memoir: from maps to models. Nat. Rev. Neurosci. 4 (4), 266–275 (2003)CrossRefGoogle Scholar
  27. 27.
    Menzel, R.: Searching for the memory trace in a mini-brain, the honeybee. Learn. Mem. 8 (2), 53–62 (2001)CrossRefGoogle Scholar
  28. 28.
    de Bruyne, M., Clyne, P.J., Carlson, J.R.: Odor coding in a model olfactory organ: the Drosophila maxillary palp. J. Neurosci. 19 (11), 4520–4532 (1999)Google Scholar
  29. 29.
    Nowotny, T., de Bruyne, M., Berna, A.Z., Warr, C.G., Trowell, S.C.: Drosophila olfactory receptors as classifiers for volatiles from disparate real world applications. Bioinspir. Biomim. 9 (4), 046007 (2014)CrossRefGoogle Scholar
  30. 30.
    Galizia, C.G., Joerges, J., Küttner, A., Faber, T., Menzel, R.: A semi-in-vivo preparation for optical recording of the insect brain. J. Neurosci. Methods 76 (1), 61–69 (1997)CrossRefGoogle Scholar
  31. 31.
    Galizia, C.G., Sachse, S., Rappert, A., Menzel, R.: The glomerular code for odor representation is species specific in the honeybee Apis mellifera. Nat. Neurosci. 2, 473–478 (1999)CrossRefGoogle Scholar
  32. 32.
    Sachse, S., Rappert, A., Galizia, C.G.: The spatial representation of chemical structures in the antennal lobes of honeybees: steps toward the olfactory code. Eur. J. Neurosci. 11, 3970–3982 (1999)CrossRefGoogle Scholar
  33. 33.
    Galizia, C.G., Kimmerle, B.: Physiological and morphological characterization of honeybee olfactory neurons combining electrophysiology, calcium imaging and confocal microscopy. J. Comp. Physiol. A 190, 21–38 (2004)CrossRefGoogle Scholar
  34. 34.
    Galán, R.F., Sachse, S., Galizia, C.G., Herz, A.V.M.: Odor-driven attractor dynamics in the antennal lobe allow for simple and rapid olfactory pattern classification. Neural Comput. 16, 999–1012 (2004)zbMATHCrossRefGoogle Scholar
  35. 35.
    Schmuker, M., Yamagata, N., Nawrot, M.P., Menzel, R.: Parallel representation of stimulus identity and intensity in a dual pathway model inspired by the olfactory system of the honeybee. Front. Neuroeng. 4, 17 (2011)CrossRefGoogle Scholar
  36. 36.
    Sachse, S., Galizia, C.G.: The coding of odour-intensity in the honeybee antennal lobe: local computation optimizes odour representation. Eur. J. Neurosci. 18, 2119–2132 (2003)CrossRefGoogle Scholar
  37. 37.
    Guerrieri, F., Schubert, M., Sandoz, J.-C., Giurfa, M.: Perceptual and neural olfactory similarity in honeybees. PLoS Biol. 3 (4), e60 (2005)CrossRefGoogle Scholar
  38. 38.
    Baker, T.C., Fadamiro, H.Y., Cosse, A.A.: Moth uses fine tuning for odour resolution. Nature 393 (6685), 530–530 (1998)CrossRefGoogle Scholar
  39. 39.
    Szyszka, P., Stierle, J.S., Biergans, S., Galizia, C.G.: The speed of smell: odor-object segregation within milliseconds. PLoS One 7 (4), e36096 (2012)CrossRefGoogle Scholar
  40. 40.
    Badel, L., Ohta, K., Tsuchimoto, Y., Kazama, H.: Decoding of context-dependent olfactory behavior in Drosophila. Neuron 91 (1), 155–167 (2016)CrossRefGoogle Scholar
  41. 41.
    Laurent, G., Wehr, M., Davidowitz, H.: Temporal representations of odors in an olfactory network. J. Neurosci. 16, 3837–3847 (1996)Google Scholar
  42. 42.
    Laurent, G., MacLeod, K., Wehr, M.: Spatiotemporal structure of olfactory inputs to the mushroom bodies. Learn. Mem. 5, 124–132 (1998)Google Scholar
  43. 43.
    Adrian, E.D.: Olfactory reactions in the brain of the hedgehog. J. Physiol. 100 (4), 459–473 (1942)CrossRefGoogle Scholar
  44. 44.
    Freeman, W.J.: The physiology of perception. Sci. Am. 264 (2), 78–85 (1991)CrossRefGoogle Scholar
  45. 45.
    Gelperin, A., Tank, D.W.: Odour-modulated collective network oscillations of olfactory interneurons in a terrestrial mollusc. Nature 345 (6274), 437–440 (1990)CrossRefGoogle Scholar
  46. 46.
    Heinbockel, T., Kloppenburg, P., Hildebrand, J.G.: Pheromone-evoked potentials and oscillations in the antennal lobes of the sphinx moth manduca sexta. J. Comp. Physiol. A 182 (6), 703–714 (1998)CrossRefGoogle Scholar
  47. 47.
    Stopfer, M., Bhagavan, S., Smith, B.H., Laurent, G.: Impaired odour discrimination on desynchronization of odour-encoding neural assemblies. Nature 390 (6655), 70–74 (1997)CrossRefGoogle Scholar
  48. 48.
    Nusser, Z., Kay, L.M., Laurent, G., Homanics, G.E., Mody, I.: Disruption of gaba(a) receptors on gabaergic interneurons leads to increased oscillatory power in the olfactory bulb network. J. Neurophysiol. 86 (6), 2823–2833 (2001)Google Scholar
  49. 49.
    Biergans, S.D., Jones, J.C., Treiber, N., Galizia, C.G., Szyszka, P.: Dna methylation mediates the discriminatory power of associative long-term memory in honeybees. PLoS One 7 (6), e39349 (2012)CrossRefGoogle Scholar
  50. 50.
    Lotka, A.J.: Contribution to the theory of periodic reaction. J. Phys. Chem. 14 (3), 271–274 (1910)CrossRefGoogle Scholar
  51. 51.
    May, R.M., Leonard, W.J.: Nonlinear aspects of competition between three species. SIAM J. Appl. Math. 29, 243–253 (1975)MathSciNetzbMATHCrossRefGoogle Scholar
  52. 52.
    Laurent, G., Stopfer, M., Friedrich, R.W., Rabinovich, M.I., Abarbanel, H.D.I.: Odor encoding as an active, dynamical process: Experiments, computation, and theory. Annu. Rev. Neurosci. 24, 263–297 (2001)CrossRefGoogle Scholar
  53. 53.
    Rabinovich, M. Volkovskii, A., Lecanda, P., Huerta, R., Abarbanel, H.D.I., Laurent, G.: Dynamical encoding by networks of competing neuron groups: winnerless competition. Phys. Rev. Lett. 87 (6), 068102 (2001)CrossRefGoogle Scholar
  54. 54.
    Mazor, O., Laurent, G.: Transient dynamics versus fixed points in odor representations by locust antennal lobe projection neurons. Neuron 48, 661 (2005)CrossRefGoogle Scholar
  55. 55.
    Rabinovich, M.I., Huerta, R., Varona, P., Afraimovich, V.S.: Generation and reshaping of sequences in neural systems. Biol. Cybern. 95 (6), 519–536 (2006)MathSciNetzbMATHCrossRefGoogle Scholar
  56. 56.
    Nowotny, T., Rabinovich, M.I.: Dynamical origin of independent spiking and bursting activity in neural microcircuits. Phys. Rev. Lett. 98, 128106 (2007)CrossRefGoogle Scholar
  57. 57.
    Ashwin, P., Karabacak, O., Nowotny, T.: Criteria for robustness of heteroclinic cycles in neural microcircuits. J. Math. Neurosci. 1 (1), 13 (2011)MathSciNetzbMATHCrossRefGoogle Scholar
  58. 58.
    Ashwin, P., Swift, J.W.: The dynamics of n weakly coupled identical oscillators. J. Nonlinear Sci. 2, 69–108 (1992)MathSciNetzbMATHCrossRefGoogle Scholar
  59. 59.
    Hansel, D., Mato, G., Meunier, C.: Clustering and slow switching in globally coupled phase oscillators. Phys. Rev. E 48 (5), 3470–3477 (1993)CrossRefGoogle Scholar
  60. 60.
    Buckley, C.L., Nowotny, T.: Transient dynamics between displaced fixed points: an alternate nonlinear dynamical framework for olfaction. Brain Res. 1434, 62–72 (2012)CrossRefGoogle Scholar
  61. 61.
    Buckley, C.L., Nowotny, T.: Multiscale model of an inhibitory network shows optimal properties near bifurcation. Phys. Rev. Lett. 106 (23), 238109 (2011)CrossRefGoogle Scholar
  62. 62.
    Vetter, R.S., Sage, A.E., Justus, K.A., Cardé, R.T., Galizia, C.G.: Temporal integrity of an airborne odor stimulus is greatly affected by physical aspects of the odor delivery system. Chem. Senses 31 (4), 359–369 (2006)CrossRefGoogle Scholar
  63. 63.
    Uchida, N., Mainen, Z.F.: Speed and accuracy of olfactory discrimination in the rat. Nat. Neurosci. 6, 1224–1229 (2003)CrossRefGoogle Scholar
  64. 64.
    Resulaj, A., Rinberg, D.: Novel behavioral paradigm reveals lower temporal limits on mouse olfactory decisions. J. Neurosci. 35 (33), 11667–11673 (2015)CrossRefGoogle Scholar
  65. 65.
    Ditzen, M., Evers, F., Galizia, C.G.: Odor similarity does not influence the time needed for odor processing. Chem. Senses 28, 781–789 (2003)CrossRefGoogle Scholar
  66. 66.
    Wright, G.A., Carlton, M., Smith, B.H.: A honeybee’s ability to learn, recognize, and discriminate odors depends upon odor sampling time and concentration. Behav. Neurosci. 123 (1), 36–43 (2009)CrossRefGoogle Scholar
  67. 67.
    Murlis, J., Elkinton, J.S., Cardé, R.T.: Odor plumes and how insects use them. Annu. Rev. Entomol. 37, 505–532 (1992)CrossRefGoogle Scholar
  68. 68.
    Celani, A., Villermaux, E., Vergassola, M.: Odor landscapes in turbulent environments. Phys. Rev. X 4, 041015 (2014)Google Scholar
  69. 69.
    Riffell, J.A., Shlizerman, E., Sanders, E., Abrell, L., Medina, B., Hinterwirth, A.J., Kutz, J.N.: Sensory biology. flower discrimination by pollinators in a dynamic chemical environment. Science 344 (6191), 1515–1518 (2014)Google Scholar
  70. 70.
    Soltys, M.A., Crimaldi, J.P.: Joint probabilities and mixing of isolated scalars emitted from parallel jets. J. Fluid Mech. 769, 130–153, 003 (2015)Google Scholar
  71. 71.
    Hopfield, J.J.: Olfactory Computation and Object Perception. Proc. Natl. Acad. Sci. U. S. A. 88 (15), 6462–6466 (1991)CrossRefGoogle Scholar
  72. 72.
    Fadamiro, H.Y., Baker, T.C.: Reproductive performance and longevity of female European corn borer, Ostrinia nubilalis: effects of multiple mating, delay in mating, and adult feeding. J. Insect Physiol. 45 (4), 385–392 (1999)CrossRefGoogle Scholar
  73. 73.
    Nikonov, A.A., Leal, W.S.: Peripheral coding of sex pheromone and a behavioral antagonist in the Japanese beetle, Popillia japonica. J. Chem. Ecol. 28 (5), 1075–1089 (2002)CrossRefGoogle Scholar
  74. 74.
    Saha, D., Leong, K., Li, C., Peterson, S., Siegel, G., Raman, B.: A spatiotemporal coding mechanism for background-invariant odor recognition. Nat. Neurosci. 16 (12), 1830–1839 (2013)CrossRefGoogle Scholar
  75. 75.
    Broome, B., Jayaraman, V., Laurent, G.: Encoding and decoding of overlapping odor sequences. Neuron 51, 467–482 (2006)CrossRefGoogle Scholar
  76. 76.
    Stierle, J., Galizia, C.G., Szyszka, P.: Millisecond stimulus onset-asynchrony enhances information about components in an odor mixture. J. Neurosci. 33 (14), 6060–6069 (2013)CrossRefGoogle Scholar
  77. 77.
    Andersson, M.N., Binyameen, M., Sadek, M.M., Schlyter, F.: Attraction modulated by spacing of pheromone components and anti-attractants in a bark beetle and a moth. J. Chem. Ecol. 37 (8), 899–911 (2011)CrossRefGoogle Scholar
  78. 78.
    Andersson, M.N., Larsson, M.C., Blazenec, M., Jakus, R., Zhang, Q.-H., Schlyter, F.: Peripheral modulation of pheromone response by inhibitory host compound in a beetle. J. Exp. Biol. 213 (Pt 19), 3332–3339 (2010)CrossRefGoogle Scholar
  79. 79.
    Su, C.-Y., Menuz, K., Reisert, J., Carlson, J.R.: Non-synaptic inhibition between grouped neurons in an olfactory circuit. Nature 492 (7427), 66–71 (2012)CrossRefGoogle Scholar
  80. 80.
    O’connell, R.J., Grant, A.J., Mayer, M.S., Mankin, R.W.: Morphological correlates of differences in pheromone sensitivity in insect sensilla. Science 220 (4604), 1408–1410 (1983)CrossRefGoogle Scholar
  81. 81.
    Nowotny, T., Stierle, J.S., Galizia, C.G., Szyszka, P.: Data-driven honeybee antennal lobe model suggests how stimulus-onset asynchrony can aid odour segregation. Brain Res. 1536, 119–134 (2013)CrossRefGoogle Scholar
  82. 82.
    Linster, C., Sachse, S., Galizia, C.G.: Computational modeling suggests that response properties rather than spatial position determine connectivity between olfactory glomeruli. J. Neurophysiol. 93 (6), 3410–3417 (2005)CrossRefGoogle Scholar
  83. 83.
    Shanbhag, S.R., Müller, B., Steinbrecht, R.A.: Atlas of olfactory organs of Drosophila melanogaster 2. Internal organization and cellular architecture of olfactory sensilla. Arthropod Struct. Dev. 29 (3), 211–229 (2000)Google Scholar
  84. 84.
    Getchell, T.V., Margolis, F.L., Getchell, M.L.: Perireceptor and receptor events in vertebrate olfaction. Prog. Neurobiol. 23 (4), 317–345 (1984)CrossRefGoogle Scholar
  85. 85.
    Pelosi, P.: Perireceptor events in olfaction. J. Neurobiol. 30 (1), 3–19 (1996)CrossRefGoogle Scholar
  86. 86.
    Kaissling, K.-E.: Kinetics of olfactory responses might largely depend on the odorant-receptor interaction and the odorant deactivation postulated for flux detectors. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 199 (11), 879–896 (2013)CrossRefGoogle Scholar
  87. 87.
    Leal, W.S.: Odorant reception in insects: roles of receptors, binding proteins, and degrading enzymes. Annu. Rev. Entomol. 58, 373–391 (2013)CrossRefGoogle Scholar
  88. 88.
    Vogt, R.G., Riddiford, L.M.: Pheromone binding and inactivation by moth antennae. Nature 293 (5828), 161–163 (1981)CrossRefGoogle Scholar
  89. 89.
    Benton, R., Sachse, S., Michnick, S.W., Vosshall, L.B.: Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo. PLoS Biol. 4 (2), e20 (2006)CrossRefGoogle Scholar
  90. 90.
    Schneider, D., Lacher, V., Kaissling, K.E.: Die Reaktionsweise und das Reaktionsspektrum von Riechzellen bei Antheraea pernyi (Lepidoptera, Saturniidae). Z. Vgl. Physiol. 48, 632–662 (1964)CrossRefGoogle Scholar
  91. 91.
    Szyszka, P., Gerkin, R.C., Galizia, C.G., Smith, B.H.: High-speed odor transduction and pulse tracking by insect olfactory receptor neurons. Proc. Natl. Acad. Sci. U. S. A. 111 (47), 16925–16930 (2014)CrossRefGoogle Scholar
  92. 92.
    Semmelroch, P., Grosch, W.: Studies on character impact odorants of coffee brews. J. Agric. Food Chem. 44, 537–543 (1996)CrossRefGoogle Scholar
  93. 93.
    Knudsen, J.T., Tollsten, L., Bergström, L.G.: Floral scents - a checklist of volatile compounds isolated by head-space techniques. Phytochemistry 33, 253–280 (1993)CrossRefGoogle Scholar
  94. 94.
    Root, C.M., Masuyama, K., Green, D.S., Enell, L.E., Nässel, D.R., Lee, C.-H., Wang, J.W.: A presynaptic gain control mechanism fine-tunes olfactory behavior. Neuron 59 (2), 311–321 (2008)CrossRefGoogle Scholar
  95. 95.
    Girardin, C.C., Kreissl, S., Galizia, C.G.: Inhibitory connections in the honeybee antennal lobe are spatially patchy. J. Neurophysiol. 109 (2), 332–343 (2013)CrossRefGoogle Scholar
  96. 96.
    Hong, E.J., Wilson, R.I.: Olfactory neuroscience: normalization is the norm. Curr. Biol. 23 (24), R1091–R1093 (2013)CrossRefGoogle Scholar
  97. 97.
    Hong, E.J., Wilson, R.I.: Simultaneous encoding of odors by channels with diverse sensitivity to inhibition. Neuron 85 (3), 573–589 (2015)CrossRefGoogle Scholar
  98. 98.
    Deisig, N., Giurfa, M., Lachnit, H., Sandoz, J.-C.: Neural representation of olfactory mixtures in the honeybee antennal lobe. Eur. J. Neurosci. 24 (4), 1161–1174 (2006)CrossRefGoogle Scholar
  99. 99.
    Deisig, N., Giurfa, M., Sandoz, J.-C.: Antennal lobe processing increases separability of odor mixture representations in the honeybee. J. Neurophysiol. 103 (4), 2185–2194 (2010)CrossRefGoogle Scholar
  100. 100.
    Smith, B.H.: Analysis of interaction in binary odorant mixtures. Physiol. Behav. 65 (3), 397–407 (1998)CrossRefGoogle Scholar
  101. 101.
    Chandra, S., Smith, B.H.: An analysis of synthetic processing of odor mixtures in the honeybee (Apis mellifera). J. Exp. Biol. 201 (Pt 22), 3113–3121 (1998)Google Scholar
  102. 102.
    Deisig, N., Lachnit, H.,Giurfa, M., Hellstern, F.: Configural olfactory learning in honeybees: negative and positive patterning discrimination. Learn. Mem. 8 (2), 70–78 (2001)CrossRefGoogle Scholar
  103. 103.
    Deisig, N., Lachnit, H., Giurfa, M.: The effect of similarity between elemental stimuli and compounds in olfactory patterning discriminations. Learn. Mem. 9 (3), 112–121 (2002)CrossRefGoogle Scholar
  104. 104.
    Deisig, N., Lachnit, H., Sandoz, J.-C., Lober, K., Giurfa, M.: A modified version of the unique cue theory accounts for olfactory compound processing in honeybees. Learn. Mem. 10 (3), 199–208 (2003)CrossRefGoogle Scholar
  105. 105.
    Kamin, L.J.: Predictability, surprise, attention, and conditioning. Punishment and Aversive Behavior, pp. 279–296. Appleton-Century-Crofts, New York (1969)Google Scholar
  106. 106.
    Rescorla, R.A., Wagner, A.R., et al.: A theory of pavlovian conditioning: variations in the effectiveness of reinforcement and nonreinforcement. Classical Conditioning II: Current Research and Theory, vol. 2, pp. 64–99. Appleton-Century Crofts, New York (1972)Google Scholar
  107. 107.
    Hosler, J.S., Smith, B.H.: Blocking and the detection of odor components in blends. J. Exp. Biol. 203 (Pt 18), 2797–2806 (2000)Google Scholar
  108. 108.
    Smith, B.H.: An analysis of blocking in odorant mixtures: an increase but not a decrease in intensity of reinforcement produces unblocking. Behav. Neurosci. 111 (1), 57–69 (1997)CrossRefGoogle Scholar
  109. 109.
    Smith, B.H., Cobey, S.: The olfactory memory of the honeybee Apis mellifera. II. Blocking between odorants in binary mixtures. J. Exp. Biol. 195, 91–108 (1994)Google Scholar
  110. 110.
    Gerber and Ullrich: No evidence for olfactory blocking in honeybee classical conditioning. J. Exp. Biol. 202 (Pt 13), 1839–1854 (1999)Google Scholar
  111. 111.
    Guerrieri, F., Lachnit, H., Gerber, B., Giurfa, M.: Olfactory blocking and odorant similarity in the honeybee. Learn. Mem. 12 (2), 86–95 (2005)CrossRefGoogle Scholar
  112. 112.
    Zars, T., Fischer, M., Schulz, R., Heisenberg, M.: Localization of a short-term memory in Drosophila. Science 288 (5466), 672–675 (2000)CrossRefGoogle Scholar
  113. 113.
    Becher, P.G., Bengtsson, M., Hansson, B.S., Witzgall, P.: Flying the fly: long-range flight behavior of Drosophila melanogaster to attractive odors. J. Chem. Ecol. 36 (6), 599–607 (2010)CrossRefGoogle Scholar
  114. 114.
    Strutz, A., Soelter, J., Baschwitz, A., Farhan, A., Grabe, V., Rybak, J., Knaden, M., Schmuker, M., Hansson, B.S., Sachse, S.: Decoding odor quality and intensity in the Drosophila brain. Elife 3, e04147 (2014)CrossRefGoogle Scholar
  115. 115.
    Huerta, R., Nowotny, T., Garcia-Sanchez, M., Abarbanel, H.D.I., Rabinovich, M.I.: Learning classification in the olfactory system of insects. Neural Comput. 16, 1601–1640 (2004)zbMATHCrossRefGoogle Scholar
  116. 116.
    Perez-Orive, J., Mazor, O., Turner, G.C., Cassenaer, S., Wilson, R., Laurent, G.: Oscillations and sparsening of odor representations in the mushroom body. Science 297 (5580), 359–365 (2002)CrossRefGoogle Scholar
  117. 117.
    Szyszka, P., Ditzen, M., Galkin, A., Galizia, C.G., Menzel, R.: Sparsening and temporal sharpening of olfactory representations in the honeybee mushroom bodies. J. Neurophysiol. 94 (5), 3303–3313 (2005)CrossRefGoogle Scholar
  118. 118.
    Lin, A.C., Bygrave, A.M., de Calignon, A., Lee, T., Miesenböck, G.: Sparse, decorrelated odor coding in the mushroom body enhances learned odor discrimination. Nat. Neurosci. 17 (4), 559–568 (2014)CrossRefGoogle Scholar
  119. 119.
    Nowotny, T., Huerta, R., Abarbanel, H.D.I., Rabinovich, M.I.: Self-organization in the olfactory system: rapid odor recognition in insects. Biol Cybern. 93, 436–446 (2005)zbMATHCrossRefGoogle Scholar
  120. 120.
    Huerta, R., Nowotny, T.: Fast and robust learning by reinforcement signals: explorations in the insect brain. Neural Comput. 21, 2123–2151 (2009)zbMATHCrossRefGoogle Scholar
  121. 121.
    Finelli, L.A., Haney, S., Bazhenov, M., Stopfer, M., Sejnowski, T.J.: Synaptic learning rules and sparse coding in a model sensory system. PLoS Comput. Biol. 4 (4), e1000062 (2008)MathSciNetCrossRefGoogle Scholar
  122. 122.
    Szyszka, P., Galkin, A., Menzel, R.: Associative and non-associative plasticity in Kenyon cells of the honeybee mushroom body. Front. Syst. Neurosci. 2, 3 (2008)CrossRefGoogle Scholar
  123. 123.
    Smith, D., Wessnitzer, J., Webb, B.: A model of associative learning in the mushroom body. Biol. Cybern. 99 (2), 89–103 (2008)MathSciNetzbMATHCrossRefGoogle Scholar
  124. 124.
    Wessnitzer, J., Young, J.M., Armstrong, J.D., Webb, B.: A model of non-elemental olfactory learning in Drosophila. J. Comput. Neurosci. 32 (2), 197–212 (2012)CrossRefGoogle Scholar
  125. 125.
    Bazhenov, M., Huerta, R., Smith, B.H.: A computational framework for understanding decision making through integration of basic learning rules. J. Neurosci. 33 (13), 5686–5697 (2013)CrossRefGoogle Scholar
  126. 126.
    Perry, C.J., Barron, A.B., Cheng, K.: Invertebrate learning and cognition: relating phenomena to neural substrate. Wiley Interdiscip. Rev. Cogn. Sci. 4 (5), 561–582 (2013)CrossRefGoogle Scholar
  127. 127.
    Papadopoulou, M., Cassenaer, S., Nowotny, T., Laurent, G.: Normalization for sparse encoding of odors by a wide-field interneuron. Science 332 (6030), 721–725 (2011)CrossRefGoogle Scholar
  128. 128.
    Assisi, C., Stopfer, M., Laurent, G., Bazhenov, M.: Adaptive regulation of sparseness by feedforward inhibition. Nat. Neurosci. 10 (9), 1176–1184 (2007)CrossRefGoogle Scholar
  129. 129.
    Gupta, N., Stopfer, M.: Functional analysis of a higher olfactory center, the lateral horn. J. Neurosci. 32 (24), 8138–8148 (2012)CrossRefGoogle Scholar
  130. 130.
    Kee, T., Sanda, P., Gupta, N., Stopfer, M., Bazhenov, M.: Feed-forward versus feedback inhibition in a basic olfactory circuit. PLoS Comput. Biol. 11 (10), e1004531 (2015)CrossRefGoogle Scholar
  131. 131.
    Grünewald, B.: Morphology of feedback neurons in the mushroom body of the honeybee, Apis mellifera. J. Comp. Neurol. 404, 114–126 (1999)CrossRefGoogle Scholar
  132. 132.
    Andrew, S.C., Perry, C.J., Barron, A.B., Berthon, K., Peralta, V., Cheng, K.: Peak shift in honeybee olfactory learning. Anim. Cogn. 17 (5), 1177–1186 (2014)CrossRefGoogle Scholar
  133. 133.
    Campbell, R.A.A., Honegger, K.S., Qin, H., Li, W., Demir, E., Turner, G.C.: Imaging a population code for odor identity in the Drosophila mushroom body. J. Neurosci. 33 (25), 10568–10581 (2013)CrossRefGoogle Scholar
  134. 134.
    Nowotny, T., Rabinovich, M.I., Huerta, R., Abarbanel, H.D.I.: Decoding temporal information through slow lateral excitation in the olfactory system of insects. J. Comput. Neurosci. 15, 271–281 (2003)CrossRefGoogle Scholar
  135. 135.
    Nowotny, T., Berna, A.Z., Binions, R., Trowell, S.: Optimal feature selection for classifying a large set of chemicals using metal oxide sensors. Sens. Actuators B 187, 471–480 (2013); Selected Papers from the 14th International Meeting on Chemical Sensors.Google Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.University of SussexBrightonUK
  2. 2.Department of BiologyUniversity of KonstanzKonstanzGermany

Personalised recommendations