Table of Contents Author Guidelines Submit a Manuscript
Advances in Artificial Intelligence
Volume 2010 (2010), Article ID 478107, 9 pages
http://dx.doi.org/10.1155/2010/478107
Review Article

Investigating the Underlying Intelligence Mechanisms of the Biological Olfactory System

Research Institute of Electrical Communication, Tohoku University, 2-1-1 Katahira, Aoba-ku, Sendai 980-8577, Japan

Received 8 September 2009; Revised 11 November 2009; Accepted 9 December 2009

Academic Editor: Naoyuki Sato

Copyright © 2010 Yoshinari Makino and Masafumi Yano. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. Chase and B. Tolloczko, “Tracing neural pathways in snail olfaction: from the tip of the tentacles to the brain and beyond,” Microscopy Research and Technique, vol. 24, no. 3, pp. 214–230, 1993. View at Publisher · View at Google Scholar · View at Scopus
  2. G. Laurent, “Olfactory network dynamics and the coding of multidimensional signals,” Nature Reviews Neuroscience, vol. 3, no. 11, pp. 884–895, 2002. View at Publisher · View at Google Scholar · View at Scopus
  3. K. Mori, Y. K. Takahashi, K. M. Igarashi, and M. Yamaguchi, “Maps of odorant molecular features in the mammalian olfactory bulb,” Physiological Reviews, vol. 86, no. 2, pp. 409–433, 2006. View at Publisher · View at Google Scholar · View at Scopus
  4. L. B. Vosshall and R. F. Stocker, “Molecular architecture of smell and taste in Drosophila,” Annual Review of Neuroscience, vol. 30, pp. 505–533, 2007. View at Publisher · View at Google Scholar · View at Scopus
  5. G. M. Shepherd, Neurobiology, Oxford University Press, New York, NY, USA, 2nd edition, 1988.
  6. L. Buck and R. Axel, “A novel multigene family may encode odorant receptors: a molecular basis for odor recognition,” Cell, vol. 65, no. 1, pp. 175–187, 1991. View at Google Scholar · View at Scopus
  7. R. Vassar, S. K. Chao, R. Sitcheran, J. M. Nunez, L. B. Vosshall, and R. Axel, “Topographic organization of sensory projections to the olfactory bulb,” Cell, vol. 79, no. 6, pp. 981–991, 1994. View at Google Scholar · View at Scopus
  8. L. B. Vosshall, A. M. Wong, and R. Axel, “An olfactory sensory map in the fly brain,” Cell, vol. 102, no. 2, pp. 147–159, 2000. View at Google Scholar · View at Scopus
  9. R. W. Friedrich and S. I. Korsching, “Combinatorial and chemotopic odorant coding in the zebrafish olfactory bulb visualized by optical imaging,” Neuron, vol. 18, no. 5, pp. 737–752, 1997. View at Publisher · View at Google Scholar · View at Scopus
  10. C. G. Galizia, S. Sachse, A. Rappert, and R. Menzel, “The glomerular code for odor representation is species specific in the honeybee Apis mellifera,” Nature Neuroscience, vol. 2, no. 5, pp. 473–478, 1999. View at Publisher · View at Google Scholar · View at Scopus
  11. B. D. Rubin and L. C. Katz, “Optical imaging of odorant representations in the mammalian olfactory bulb,” Neuron, vol. 23, no. 3, pp. 499–511, 1999. View at Publisher · View at Google Scholar · View at Scopus
  12. N. Uchida, Y. K. Takahashi, M. Tanifuji, and K. Mori, “Odor maps in the mammalian olfactory bulb: domain organization and odorant structural features,” Nature Neuroscience, vol. 3, no. 10, pp. 1035–1043, 2000. View at Publisher · View at Google Scholar · View at Scopus
  13. R. Chase, “The olfactory sensitivity of snails, Achatina fulica,” Journal of Comparative Physiology A, vol. 148, no. 2, pp. 225–235, 1982. View at Publisher · View at Google Scholar · View at Scopus
  14. R. Chase, “Structure and function in the cerebral ganglion,” Microscopy Research and Technique, vol. 49, no. 6, pp. 511–520, 2000. View at Publisher · View at Google Scholar · View at Scopus
  15. A. Gelperin, “Rapid food aversion learning by a terrestrial mollusk,” Science, vol. 189, no. 4202, pp. 567–570, 1975. View at Google Scholar · View at Scopus
  16. C. Sahley, J. W. Rudy, and A. Gelperin, “An analysis of associative learning in a terrestrial mollusc—I. Higher-order conditioning, blocking and a transient US pre-exposure effect,” Journal of Comparative Physiology A, vol. 144, no. 1, pp. 1–8, 1981. View at Publisher · View at Google Scholar · View at Scopus
  17. C. L. Sahley, K. A. Martin, and A. Gelperin, “Analysis of associative learning in the terrestrial mollusc Limax maximus—II. Appetitive learning,” Journal of Comparative Physiology A, vol. 167, no. 3, pp. 339–345, 1990. View at Google Scholar · View at Scopus
  18. A. Yamada, T. Sekiguchi, H. Suzuki, and A. Mizukami, “Behavioral analysis of internal memory states using cooling-induced retrograde amnesia in Limax flavus,” Journal of Neuroscience, vol. 12, no. 3, pp. 729–735, 1992. View at Google Scholar
  19. H. Suzuki, T. Sekiguchi, A. Yamada, and A. Mizukami, “Sensory preconditioning in the terrestrial mollusk, Limax flavus,” Zoological Science, vol. 11, pp. 121–125, 1994. View at Google Scholar
  20. T. Teyke, “Food-attraction conditioning in the snail, Helix pomatia,” Journal of Comparative Physiology A, vol. 177, no. 4, pp. 409–414, 1995. View at Publisher · View at Google Scholar · View at Scopus
  21. D. Kleinfeld, K. R. Delaney, M. S. Fee, J. A. Flores, D. W. Tank, and A. Gelperin, “Dynamics of propagating waves in the olfactory network of a terrestrial mollusk: an electrical and optical study,” Journal of Neurophysiology, vol. 72, no. 3, pp. 1402–1419, 1994. View at Google Scholar · View at Scopus
  22. S. Kawahara, S. Toda, Y. Suzuki, S. Watanabe, and Y. Kirino, “Comparative study on neural oscillation in the procerebrum of the terrestrial slugs Incilaria bilineata and Limax marginatus,” Journal of Experimental Biology, vol. 200, no. 13, pp. 1851–1861, 1997. View at Google Scholar · View at Scopus
  23. S. Toda, S. Kawahara, and Y. Kirino, “Image analysis of olfactory responses in the procerebrum of the terrestrial slug Limax marginatus,” Journal of Experimental Biology, vol. 203, no. 19, pp. 2895–2905, 2000. View at Google Scholar · View at Scopus
  24. E. S. Nikitin and P. M. Balaban, “Optical recording of odor-evoked responses in the olfactory brain of the naive and aversively trained terrestrial snails,” Learning and Memory, vol. 7, no. 6, pp. 422–432, 2000. View at Publisher · View at Google Scholar · View at Scopus
  25. S. Watanabe, S. Shimozono, and Y. Kirino, “Optical recording of oscillatory neural activities in the molluscan brain,” Neuroscience Letters, vol. 359, no. 3, pp. 147–150, 2004. View at Publisher · View at Google Scholar · View at Scopus
  26. H. Makinae, Y. Makino, T. Obara, and M. Yano, “Specific spatio-temporal activities in the cerebral ganglion of Incilaria fruhstorferi in response to superior and inferior tentacle nerve stimulation,” Brain Research, vol. 1231, pp. 47–62, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. T. Kimura, S. Toda, T. Sekiguchi, S. Kawahara, and Y. Kirino, “Optical recording analysis of olfactory response of the procerebral lobe in the slug brain,” Learning and Memory, vol. 4, no. 5, pp. 389–400, 1998. View at Google Scholar · View at Scopus
  28. R. Chase and R. P. Croll, “Tentacular function in snail olfactory orientation,” Journal of Comparative Physiology A, vol. 143, no. 3, pp. 357–362, 1981. View at Publisher · View at Google Scholar · View at Scopus
  29. A. Friedrich and T. Teyke, “Identification of stimuli and input pathways mediating food-attraction conditioning in the snail, Helix,” Journal of Comparative Physiology A, vol. 183, no. 2, pp. 247–254, 1998. View at Publisher · View at Google Scholar · View at Scopus
  30. T. Kimura, S. Toda, T. Sekiguchi, and Y. Kirino, “Behavioral modulation induced by food odor aversive conditioning and its influence on the olfactory responses of an oscillatory brain network in the slug Limax marginatus,” Learning and Memory, vol. 4, no. 5, pp. 365–375, 1998. View at Google Scholar · View at Scopus
  31. T. Kimura, A. Iwama, and T. Sekiguchi, “Contributions of superior and inferior tentacles to learned food-avoidance behavior in Limax marginatus,” Zoological Science, vol. 16, no. 4, pp. 595–602, 1999. View at Google Scholar · View at Scopus
  32. M. E. Egan and A. Gelperin, “Olfactory inputs to a bursting serotonergic interneuron in a terrestrial mollusk,” Journal of Molluscan Studies, vol. 47, pp. 80–88, 1981. View at Google Scholar
  33. T. Teyke and A. Gelperin, “Olfactory oscillations augment odor discrimination not odor identification by Limax CNS,” NeuroReport, vol. 10, no. 5, pp. 1061–1068, 1999. View at Google Scholar · View at Scopus
  34. Y. Makino, H. Makinae, T. Obara, H. Miura, and M. Yano, “Observations of olfactory information flows within brain of the terrestrial slug, Inciralia fruhstorferi,” in Proceedings of IEEE International Conference on Neural Networks (IJCNN '06), pp. 3874–3881, Vancouver, Canada, July 2006. View at Scopus
  35. R. Chase and B. Tolloczko, “Interganglionic dendrites constitute an output pathway from the procerebrum of the snail Achatina fulica,” Journal of Comparative Neurology, vol. 283, no. 1, pp. 143–152, 1989. View at Google Scholar · View at Scopus
  36. R. Chase, “Responses to odors mapped in snail tentacle and brain by [14C]-2-deoxyglucose autoradiography,” Journal of Neuroscience, vol. 5, no. 11, pp. 2930–2939, 1985. View at Google Scholar · View at Scopus
  37. A. Galperin and D. W. Tank, “Odour-modulated collective network oscillations of olfactory interneurons in a terrestrial mollusc,” Nature, vol. 345, no. 6274, pp. 437–440, 1990. View at Publisher · View at Google Scholar · View at Scopus
  38. T. Kimura, H. Suzuki, E. Kono, and T. Sekiguchi, “Mapping of interneurons that contribute to food aversive conditioning in the slug brain,” Learning and Memory, vol. 4, no. 5, pp. 376–388, 1998. View at Google Scholar · View at Scopus
  39. A. Schütt, E. Başar, and T. H. Bullock, “Power spectra of ongoing activity of the snail brain can discriminate odorants,” Comparative Biochemistry and Physiology A, vol. 123, no. 1, pp. 95–110, 1999. View at Publisher · View at Google Scholar · View at Scopus
  40. Y. Kasai, S. Watanabe, Y. Kirino, and R. Matsuo, “The procerebrum is necessary for odor-aversion learning in the terrestrial slug Limax valentianus,” Learning and Memory, vol. 13, no. 4, pp. 482–488, 2006. View at Publisher · View at Google Scholar · View at Scopus
  41. S. A. Siegelbaum, J. S. Camardo, and E. R. Kandel, “Serotonin and cyclic AMP close single K+ channels in Aplysia sensory neurones,” Nature, vol. 299, no. 5882, pp. 413–417, 1982. View at Google Scholar · View at Scopus
  42. M. Hammer, “An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees,” Nature, vol. 366, no. 6450, pp. 59–63, 1993. View at Publisher · View at Google Scholar · View at Scopus
  43. W. Schultz, P. Apicella, and T. Ljungberg, “Responses of monkey dopamine neurons to reward and conditioned stimuli during successive steps of learning a delayed response task,” Journal of Neuroscience, vol. 13, no. 3, pp. 900–913, 1993. View at Google Scholar · View at Scopus
  44. E. Marder and S. Hooper, “Neurotransmitter modulation of the stomatogastric ganglion of decapod crustaceans,” in Model Neural Networks and Behavior, A. I. Selverston, Ed., pp. 319–337, Plenum Press, New York, NY, USA, 1985. View at Google Scholar
  45. R. E. Flamm and R. M. Harris-Warrick, “Aminergic modulation in lobster stomatogastric ganglion—I. Effects on motor pattern and activity of neurons within the pyloric circuit,” Journal of Neurophysiology, vol. 55, no. 5, pp. 847–865, 1986. View at Google Scholar
  46. Y. Makino, M. Akiyama, and M. Yano, “Emergent mechanisms in multiple pattern generation of the lobster pyloric network,” Biological Cybernetics, vol. 82, no. 6, pp. 443–454, 2000. View at Google Scholar · View at Scopus
  47. A. Gelperin, L. D. Rhines, J. Flores, and D. W. Tank, “Coherent network oscillations by olfactory interneurons: modulation by endogenous amines,” Journal of Neurophysiology, vol. 69, no. 6, pp. 1930–1939, 1993. View at Google Scholar · View at Scopus
  48. L. D. Rhines, P. G. Sokolove, J. Flores, D. W. Tank, and A. Gelperin, “Cultured olfactory interneurons from Limax maximus: optical and electrophysiological studies of transmitter-evoked responses,” Journal of Neurophysiology, vol. 69, no. 6, pp. 1940–1947, 1993. View at Google Scholar · View at Scopus
  49. M. Peschel, V. Straub, and T. Teyke, “Consequences of food-attraction conditioning in Helix: a behavioral and electrophysiological study,” Journal of Comparative Physiology A, vol. 178, no. 3, pp. 317–327, 1996. View at Google Scholar · View at Scopus
  50. S. A. Prescott, N. Gill, and R. Chase, “Neural circuit mediating tentacle withdrawal in Helix aspersa, with specific reference to the competence of the motor neuron C3,” Journal of Neurophysiology, vol. 78, no. 6, pp. 2951–2965, 1997. View at Google Scholar · View at Scopus
  51. E. S. Nikitin, I. S. Zakharov, E. I. Samarova, G. Kemenes, and P. M. Balaban, “Fine tuning of olfactory orientation behaviour by the interaction of oscillatory and single neuronal activity,” European Journal of Neuroscience, vol. 22, no. 11, pp. 2833–2844, 2005. View at Publisher · View at Google Scholar · View at Scopus
  52. G. Laurent, M. Wehr, and H. Davidowitz, “Temporal representations of odors in an olfactory network,” Journal of Neuroscience, vol. 16, no. 12, pp. 3837–3847, 1996. View at Google Scholar · View at Scopus
  53. R. W. Friedrich and G. Laurent, “Dynamic optimization of odor representations by slow temporal patterning of mitral cell activity,” Science, vol. 291, no. 5505, pp. 889–894, 2001. View at Publisher · View at Google Scholar · View at Scopus
  54. M. Stopfer, V. Jayaraman, and G. Laurent, “Intensity versus identity coding in an olfactory system,” Neuron, vol. 39, no. 6, pp. 991–1004, 2003. View at Publisher · View at Google Scholar · View at Scopus
  55. J. Perez-Orive, O. Mazor, G. C. Turner, S. Cassenaer, R. I. Wilson, and G. Laurent, “Oscillations and sparsening of odor representations in the mushroom body,” Science, vol. 297, no. 5580, pp. 359–365, 2002. View at Publisher · View at Google Scholar · View at Scopus
  56. J. Hegdé and D. C. Van Essen, “Temporal dynamics of shape analysis in macaque visual area V2,” Journal of Neurophysiology, vol. 92, no. 5, pp. 3030–3042, 2004. View at Publisher · View at Google Scholar · View at Scopus
  57. M. D. Menz and R. D. Freeman, “Stereoscopic depth processing in the visual cortex: a coarse-to-fine mechanism,” Nature Neuroscience, vol. 6, no. 1, pp. 59–65, 2003. View at Publisher · View at Google Scholar · View at Scopus
  58. R. D. Luce, Vision, Freeman, New York, NY, USA, 1982.
  59. R. O. Duda, P. E. Hart, and D. G. Stork, Pattern Classification, John Wiley & Sons, New York, NY, USA, 2nd edition, 2001.
  60. J. J. Hopfield, “Pattern recognition computation using action potential timing for stimulus representation,” Nature, vol. 376, no. 6535, pp. 33–36, 1995. View at Google Scholar · View at Scopus
  61. R. D. Luce, Response Times, Oxford University Press, Oxford, UK, 1986.
  62. N. M. Abraham, H. Spors, A. Carleton, T. W. Margrie, T. Kuner, and A. T. Schaefer, “Maintaining accuracy at the expense of speed: stimulus similarity defines odor discrimination time in mice,” Neuron, vol. 44, no. 5, pp. 865–876, 2004. View at Publisher · View at Google Scholar · View at Scopus
  63. D. Rinberg, A. Koulakov, and A. Gelperin, “Speed-accuracy tradeoff in olfaction,” Neuron, vol. 51, no. 3, pp. 351–358, 2006. View at Publisher · View at Google Scholar · View at Scopus
  64. K. Mori and G. M. Shepherd, “Emerging principles of molecular signal processing by mitral/tufted cells in the olfactory bulb,” Seminars in Cell and Developmental Biology, vol. 5, no. 1, pp. 65–74, 1994. View at Google Scholar · View at Scopus
  65. M. Wachowiak, L. B. Cohen, and M. R. Zochowski, “Distributed and concentration-invariant spatial representations of odorants by receptor neuron input to the turtle olfactory bulb,” Journal of Neurophysiology, vol. 87, no. 2, pp. 1035–1045, 2002. View at Google Scholar · View at Scopus
  66. S. Sachse and C. G. Galizia, “The coding of odour-intensity in the honeybee antennal lobe: local computation optimizes odour representation,” European Journal of Neuroscience, vol. 18, no. 8, pp. 2119–2132, 2003. View at Publisher · View at Google Scholar · View at Scopus
  67. C. D. Brody and J. J. Hopfield, “Simple networks for spike-timing-based computation, with application to olfactory processing,” Neuron, vol. 37, no. 5, pp. 843–852, 2003. View at Publisher · View at Google Scholar · View at Scopus
  68. S. Sachse, A. Rappert, and C. G. Galizia, “The spatial representation of chemical structures in the antennal lobe of honeybees: steps towards the olfactory code,” European Journal of Neuroscience, vol. 11, no. 11, pp. 3970–3982, 1999. View at Publisher · View at Google Scholar · View at Scopus
  69. F. Guerrieri, M. Schubert, J. C. Sandoz, and M. Giurfa, “Perceptual and neural olfactory similarity in honeybees,” PLoS Biology, vol. 3, no. 4, article e60, 2005. View at Google Scholar
  70. M. Laska, C. G. Galizia, M. Giurfa, and R. Menzel, “Olfactory discrimination ability and odor structure-activity relationships in honeybees,” Chemical Senses, vol. 24, no. 4, pp. 429–438, 1999. View at Publisher · View at Google Scholar · View at Scopus
  71. C. Linster and M. E. Hasselmo, “Behavioral responses to aliphatic aldehydes can be predicted from known electrophysiological responses of mitral cells in the olfactory bulb,” Physiology & Behavior, vol. 66, no. 3, pp. 497–502, 1999. View at Publisher · View at Google Scholar · View at Scopus
  72. Y. Makino, M. Yasuike, Y. Naka, H. Miura, and M. Yano, “Olfactory computation using spatiotemporal pattern of network activity for odor representation,” Neuroscience Research, vol. 58, supplement, p. S103, 2007. View at Google Scholar
  73. Y. Makino, M. Yasuike, Y. Naka, H. Miura, and M. Yano, “Principal characteristics in odor recognition naturally emerge from spatiotemporal coding,” Neuroscience Research, vol. 61, supplement, p. S249, 2008. View at Google Scholar
  74. Y. Makino, M. Yasuike, Y. Naka, H. Miura, and M. Yano, “A computational algorithm for odor representation using a spatiotemporal sequence,” Society for Neuroscience Abstract, vol. 362, p. 15, 2008. View at Google Scholar
  75. K. MacLeod and G. Laurent, “Distinct mechanisms for synchronization and temporal patterning of odor-encoding neural assemblies,” Science, vol. 274, no. 5289, pp. 976–979, 1996. View at Publisher · View at Google Scholar · View at Scopus
  76. M. Stopfer, S. Bhagavan, B. H. Smith, and G. Laurent, “Impaired odour discrimination on desynchronization of odour-encoding neural assemblies,” Nature, vol. 390, no. 6655, pp. 70–74, 1997. View at Publisher · View at Google Scholar · View at Scopus
  77. J. S. de Belle and M. Heisenberg, “Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies,” Science, vol. 263, no. 5147, pp. 692–695, 1994. View at Google Scholar · View at Scopus
  78. J. B. Connolly, I. J. H. Roberts, J. D. Armstrong et al., “Associative learning disrupted by impaired Gs signaling in Drosophila mushroom bodies,” Science, vol. 274, no. 5295, pp. 2104–2107, 1996. View at Google Scholar · View at Scopus
  79. J. Dubnau, L. Grady, T. Kitamoto, and T. Tully, “Disruption of neurotransmission in Drosophila mushroom body blocks retrieval but not acquisition of memory,” Nature, vol. 411, no. 6836, pp. 476–480, 2001. View at Publisher · View at Google Scholar · View at Scopus
  80. R. Gillette and W. J. Davis, “The role of the metacerebral giant neuron in the feeding behavior of Pleurobranchaea,” Journal of Comparative Physiology A, vol. 116, no. 2, pp. 129–159, 1977. View at Publisher · View at Google Scholar · View at Scopus
  81. K. R. Weiss and I. Kupfermann, “Homology of the giant serotonergic neurons (metacerebral cells) in Aplysia and pulmonate molluscs,” Brain Research, vol. 117, no. 1, pp. 33–49, 1976. View at Publisher · View at Google Scholar · View at Scopus
  82. M. S. Livingstone, R. M. Harris-Warrick, and E. A. Kravitz, “Serotonin and octopamine produce opposite postures in lobsters,” Science, vol. 208, no. 4439, pp. 76–79, 1980. View at Google Scholar · View at Scopus
  83. C. M. Lent and M. H. Dickinson, “Serotonin integrates the feeding behavior of the medicinal leech,” Journal of Comparative Physiology A, vol. 154, no. 4, pp. 457–471, 1984. View at Publisher · View at Google Scholar · View at Scopus
  84. G. Bicker and R. Menzel, “Chemical codes for the control of behaviour in arthropods,” Nature, vol. 337, no. 6202, pp. 33–39, 1989. View at Google Scholar · View at Scopus
  85. E. A. Kravitz, “Serotonin and aggression: insights gained from a lobster model system and speculations on the role of amine neurons in a complex behavior,” Journal of Comparative Physiology A, vol. 186, no. 3, pp. 221–238, 2000. View at Google Scholar · View at Scopus
  86. K. M. Crisp and K. A. Mesce, “To swim or not to swim: regional effects of serotonin, octopamine and amine mixtures in the medicinal leech,” Journal of Comparative Physiology A, vol. 189, no. 6, pp. 461–470, 2003. View at Publisher · View at Google Scholar · View at Scopus
  87. S. Watanabe, S. Kawahara, and Y. Kirino, “Glutamate induces CI and K+ currents in the olfactory interneurons of a terrestrial slug,” Journal of Comparative Physiology A, vol. 184, no. 6, pp. 553–562, 1999. View at Publisher · View at Google Scholar · View at Scopus