Interactions of odorants with olfactory receptors and receptor neurons match the perceptual dynamics observed for woody and fruity odorant mixtures

European Journal of Neuroscience

Volumn 35, Issue 3-4, 2012, Pages 584-597

  Chaput, M A ^a   El Mountassir, F ^b   Atanasova, B ^b   Thomas Danguin, T ^b   Le Bon, A M ^b   Perrut, A ^c   Ferry, B ^a   Duchamp Viret, P ^a  

^a UNIVERSITÉ DE LYON   (France)

^b UNIVERSITÉ DE BOURGOGNE   (France)

^c UNIVERSITÉ LYON 1   (France)

Author keywords

Human; Odour mixture; Olfactory receptor neurons; Olfactory receptors; Rat

Indexed keywords

CELL RECEPTOR; ISOPENTYL ACETATE; LACTONE; 2 METHYL 3 OCTALACTONE; LACTONE DERIVATIVE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CELL INTERACTION; CELL STRAIN HEK293; CONCENTRATION RESPONSE; CONTROLLED STUDY; HUMAN; HUMAN CELL; IN VIVO STUDY; MALE; MOLECULAR IMAGING; NERVE CELL STIMULATION; NONHUMAN; OLFACTOMETRY; OLFACTORY DISCRIMINATION; OLFACTORY RECEPTOR; PERCEPTIVE DISCRIMINATION; PRIORITY JOURNAL; PSYCHOPHYSICS; RAT; RED WINE; SENSORY NERVE CELL; SENSORY SYSTEM ELECTROPHYSIOLOGY; ADULT; ANIMAL TISSUE; FEMALE; HUMAN EXPERIMENT; NORMAL HUMAN; ODOR; OLFACTORY EPITHELIUM; OLFACTORY SYSTEM;

ACTION POTENTIALS; ANIMALS; CALCIUM; CELL LINE, TRANSFORMED; DOSE-RESPONSE RELATIONSHIP, DRUG; FRUIT; GENE EXPRESSION REGULATION; HUMANS; INDIVIDUALITY; MALE; ODORS; OLFACTORY PERCEPTION; OLFACTORY RECEPTOR NEURONS; PSYCHOPHYSICS; RATS; RATS, WISTAR; RECEPTORS, ODORANT; SMELL; STIMULATION, CHEMICAL; TRANSFECTION; WOOD;

EID: 84857036921     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2011.07976.x     Document Type: Article

References (74)

1. Araneda, R.C., Kini, A.D. & Firestein, S. (2000) The molecular receptive range of an odorant receptor. Nat. Neurosci., 3, 1248-1255.
2. Araneda, R.C., Peterlin, Z., Zhang, X., Chesler, A. & Firestein, S. (2004) A pharmacological profile of the aldehyde receptor repertoire in rat olfactory epithelium. J. Physiol., 555, 743-756.
3. Arctander, S. (1969) Perfume and flavor chemicals. Monclair, NJ, USA, Steffen Arctander.
4. Atanasova, B., Thomas-Danguin, T., Langlois, D., Nicklaus, S. & Etiévant, P. (2004) Perceptual interactions between fruity and woody notes of wine. Flavour Frag. J., 19, 476-482.
5. Atanasova, B., Thomas-Danguin, T., Chabanet, C., Langlois, D., Nicklaus, S. & Etievant, P. (2005) Perceptual interactions in odour mixtures: odour quality in binary mixtures of woody and fruity wine odorants. Chem. Senses, 30, 209-217.
6. Baker, R.A. (1964) Response parameters including synergism-antagonism in aqueous odor measurement. Ann. NY Acad. Sci., 116, 495-503.
7. Bargmann, C.I. (1997) Olfactory receptors, vomeronasal receptors, and the organization of olfactory information. Cell, 90, 585-587.
8. Bell, G.A., Laing, D.G. & Panhuber, H. (1987) Odour mixture suppression: evidence for a peripheral mechanism in human and rat. Brain Res., 426, 8-18.
9. Berglund, B. & Olsson, M.J. (1993) Odor-intensity interaction in binary mixtures. J. Exp. Psychol. Hum. Percept. Perform., 19, 302-314.
10. Bieri, S., Monastyrskaia, K. & Schilling, B. (2004) Olfactory receptor neuron profiling using sandalwood odorants. Chem. Senses, 29, 483-487.
11. Boyle, J.A., Djordjevic, J., Olsson, M.J., Lundstrom, J.N. & Jones-Gotman, M. (2009) The human brain distinguishes between single odorants and binary mixtures. Cereb. Cortex, 19, 66-71.
12. Breer, H. & Boekhoff, I. (1991) Odorants of the Same Odor Class Activate Different 2nd Messenger Pathways. Chem. Senses, 16, 19-29.
13. Brodin, M., Laska, M. & Olsson, M.J. (2009) Odor interaction between Bourgeonal and its antagonist undecanal. Chem. Senses, 34, 625-630.
14. Buck, L. & Axel, R. (1991) A novel multigene family may encode odorant receptors - a molecular basis for odor recognition. Cell, 65, 175-187.
15. Cabanis, J.C., Cabanis, M.T., Cheynier, V. & Teissedre, P.L. (1998) Tables de composition. In Flanzy, C. (Ed), OEnologie-Fondements Scientifiques et Technologiques. Lavoisier, Paris, pp. 315-336.
16. Cain, W.S. & Drexler, M. (1974) Scope and evaluation of odor counteraction and masking. Ann. NY Acad. Sci., 237, 427-439.
17. Cerdán, T.G., Rodríguez Mozaz, S. & Ancín Azpilicueta, C. (2002) Volatile composition of aged wine in used barrels of French oak and of American oak. Food Res. Int., 35, 603-610.
18. Chess, A., Simon, I., Cedar, H. & Axel, R. (1994) Allelic inactivation regulates olfactory receptor gene expression. Cell, 78, 823-834.
19. Cometto-Muniz, J.E., Cain, W.S. & Abraham, M.H. (2003) Dose-addition of individual odorants in the odor detection of binary mixtures. Behav. Brain Res., 138, 95-105.
20. Daniel, P.C., Burgess, M.F. & Derby, C.D. (1996) Responses of olfactory receptor neurons in the spiny lobster to binary mixtures are predictable using a noncompetitive model that incorporates excitatory and inhibitory transduction pathways. J. Comp. Physiol. [A], 178, 523-536.
21. Duchamp, A., Revial, M.F., Holley, A. & Mac Leod, P. (1974) Odor discrimination by frog olfactory receptors. Chem. Senses, 1, 213-233.
22. Duchamp-Viret, P., Chaput, M.A. & Duchamp, A. (1999) Odor response properties of rat olfactory receptor neurons. Science, 284, 2171-2174.
23. Duchamp-Viret, P., Duchamp, A. & Chaput, M. (1993) GABAergic control of odor-induced activity in the frog olfactory bulb-Electrophysiological study with picrotoxin and bicuculline. Neuroscience, 53, 111-120.
24. Duchamp-Viret, P., Duchamp, A. & Chaput, M.A. (2000) Peripheral odor coding in the rat and frog: quality and intensity specification. J. Neurosci., 20, 2383-2390.
25. Duchamp-Viret, P., Duchamp, A. & Chaput, M.A. (2003) A Single olfactory sensory neurons simultaneously integrate the components of an odor mixture. Eur. J. Neurosci., 18, 2690-2696.
26. Duchamp-Viret, P., Duchamp, A. & Vigouroux, M. (1989) Amplifying role of convergence in olfactory system. A comparative study of receptor cell and second order neuron sensitivities. J. Neurophysiol., 61, 1085-1094.
27. Gesteland, R.C. (1959) Comments on microelectrodes. Proc. Inst. Radio Eng., 47, 1856-1862.
28. Godfrey, P.A., Malnic, B. & Buck, L.B. (2004) The mouse olfactory receptor gene family. Proc. Natl. Acad. Sci. USA, 101, 2156-2161.
29. Grabenhorst, F., Rolls, E.T., Margot, C., da Silva, M.A. & Velazco, M.I. (2007) How pleasant and unpleasant stimuli combine in different brain regions: odor mixtures. J. Neurosci., 27, 13532-13540.
30. Grosmaitre, X., Fuss, S.H., Lee, A.C., Adipietro, K.A., Matsunami, H., Mombaerts, P. & Ma, M. (2009) SR1, a mouse odorant receptor with an unusually broad response profile. J. Neurosci., 29, 14545-14552.
31. Grossman, K.J., Mallik, A.K., Ross, J., Kay, L.M. & Issa, N.P. (2008) Glomerular activation patterns and the perception of odor mixtures. Eur. J. Neurosci., 27, 2676-2685.
32. Ishii, A., Roudnitzky, N., Beno, N., Bensafi, M., Hummel, T., Rouby, C. & Thomas-Danguin, T. (2008) Synergy and masking in odor mixtures: an electrophysiological study of orthonasal vs. retronasal perception. Chem. Senses, 33, 553-561.
33. Jobson, J.D. (1991) Applied Multivariate Data Analysis: Volume 1: Regression and Experimental Design (Springer Texts in Statistics), 621 pp.
34. Jones, F.N. & Woskow, M.H. (1964) On the intensity of odor mixtures. Ann. NY Acad. Sci., 116, 484-494.
35. Kajiya, K., Inaki, K., Tanaka, M., Haga, T., Kataoka, H. & Touhara, K. (2001) Molecular bases of odor discrimination: reconstitution of olfactory receptors that recognize overlapping sets of odorants. J. Neurosci., 21, 6018-6025.
36. Kay, L.M., Lowry, C.A. & Jacobs, H.A. (2003) Receptor contributions to configural and elemental odor mixture perception. Behav. Neurosci., 117, 1108-1114.
37. Kurahashi, T., Lowe, G. & Gold, G.H. (1994) Suppression of odorant responses by odorants in olfactory receptor cells. Science, 265, 118-120.
38. Laing, D.G. & Glemarec, A. (1992) Selective attention and the perceptual analysis of odor mixtures. Physiol. Behav., 52, 1047-1053.
39. Laing, D.G. & Jinks, A.L. (2001) Psychophysical analysis of complex odor mixtures. CHIMIA, 55, 413-420.
40. Laing, D.G. & Willcox, M.E. (1987) An investigation of the mechanisms of odor suppression using physical and dichorhinic mixtures. Behav. Brain Res., 26, 79-87.
41. Lin, D.Y., Shea, S.D. & Katz, L.C. (2006) Representation of natural stimuli in the rodent main olfactory bulb. Neuron, 50, 937-949.
42. Malnic, B., Hirono, J., Sato, T. & Buck, L.B. (1999) Combinatorial receptor codes for odors. Cell, 96, 713-723.
43. Matarazzo, V., Clot-Faybesse, O., Marcet, B., Guiraudie-Capraz, G., Atanasova, B., Devauchelle, G., Cerutti, M., Etievant, P. & Ronin, C. (2005) Functional characterization of two human olfactory receptors expressed in the baculovirus Sf9 insect cell system. Chem. Senses, 30, 195-207.
44. Mc Clintock, T.S. & Ache, B.W. (1989) Hyperpolarizing Receptor Potentials in Lobster Olfactory Receptor Cells - Implications for Transduction and Mixture Suppression. Chem. Senses, 14, 637-647.
45. Michel, W.C. & Ache, B.W. (1992) Cyclic nucleotides mediate an odor-evoked potassium conductance in lobster olfactory receptor cells. J. Neurosci., 12, 3979-3984.
46. Michel, W.C. & Ache, B.W. (1994) Oor-evoked inhibition in primary olfactory receptor neurons. Chem. Senses, 19, 11-24.
47. Michel, W.C., McClintock, T.S. & Ache, B.W. (1991) Inhibition of lobster olfactory receptor cells by an odor-activated potassium conductance. J. Neurophysiol., 65, 446-453.
48. Miyazawa, T., Gallagher, M., Preti, G. & Wise, P.M. (2008) Synergistic mixture interactions in detection of perithreshold odors by humans. Chem. Senses, 33, 363-369.
49. Moio, L., Schlich, P., Issanchou, S., Etiévant, P. & Feuillat, M. (1993) Description de la typicité arômatique de vins de Bourgogne issus du cépage Chardonnay. J. int. Sciences de la vie et du vin, 27, 179-189.
50. Noe, J. & Breer, H. (1998) Functional and molecular characterization of individual olfactory neurons. J. Neurochem., 71, 2286-2293.
51. Oka, Y., Omura, M., Kataoka, H. & Touhara, K. (2004) Olfactory receptor antagonism between odorants. EMBO J., 23, 120-126.
52. Olson, K.S. & Derby, C.D. (1995) Inhibition of taurine and 5'AMP olfactory receptor sites of the spiny lobster Panulirus argus by odorant compounds and mixtures. J. Comp. Physiol. [A], 176, 527-540.
53. Peterlin, Z., Li, Y., Sun, G., Shah, R., Firestein, S. & Ryan, K. (2008) The importance of odorant conformation to the binding and activation of a representative olfactory receptor. Chem. Biol., 15, 1317-1327.
54. Pet'ka, J., Etiévant, P. & Callement, G. (2000) Suitability of different plastic materials for head or nose spaces short term storage. Analysis, 28, 330-335.
55. Reisert, J. & Restrepo, D. (2009) Molecular tuning of odorant receptors and its implication for odor signal processing. Chem. Senses, 34, 535-545.
56. Rospars, J.P., Lansky, P., Chaput, M. & Duchamp-Viret, P. (2008) Competitive and noncompetitive odorant interactions in the early neural coding of odorant mixtures. J. Neurosci., 28, 2659-2666.
57. Rouby, C. & Holley, A. (1995) Temporal competition between odorants: effect of different time intervals on the perception of monorhinic and dichorhinic binary mixtures. Perception, 24, 1083-1097.
58. Sanz, G., Schlegel, C., Pernollet, J.C. & Briand, L. (2005) Comparison of odorant specificity of two human olfactory receptors from different phylogenetic classes and evidence for antagonism. Chem. Senses, 30, 69-80.
59. Serizawa, S., Ishii, T., Nakatani, H., Tsuboi, A., Nagawa, F., Asano, M., Sudo, K., Sakagami, J., Sakano, H., Ijiri, T., Matsuda, Y., Suzuki, M., Yamamori, T., Iwakura, Y. & Sakano, H. (2000) Mutually exclusive expression of odorant receptor transgenes. Nat. Neurosci., 3, 687-693.
60. Serizawa, S., Miyamichi, K. & Sakano, H. (2004) One neuron-one receptor rule in the mouse olfactory system. Trends Genet., 20, 648-653.
61. Sokolic, L., Laing, D.G. & McGregor, I.S. (2007) Asymmetric suppression of components in binary aldehyde mixtures: behavioral studies in the laboratory rat. Chem. Senses, 32, 191-199.
62. Spehr, M., Wetzel, C.H., Hatt, H. & Ache, B.W. (2002) 3-phosphoinositides modulate cyclic nucleotide signaling in olfactory receptor neurons. Neuron, 33, 731-739.
63. Spehr, M., Schwane, K., Heilmann, S., Gisselmann, G., Hummel, T. & Hatt, H. (2004) Dual capacity of a human olfactory receptor. Curr. Biol., 14, R832-R833.
64. Spillman, P.J. (1997) Oakwood contribution to wine aroma. Thesis: horticulture, Viticulture and Oenology. J Agric Food Chem, University of Adelaïde, pp. 1-367.
65. Takeuchi, H., Ishida, H., Hikichi, S. & Kurahashi, T. (2009) Mechanism of olfactory masking in the sensory cilia. J. Gen. Physiol., 133, 583-601.
66. Thomas-Danguin, T., Ishii, A., Etiévant, P. & Antanasova, B. (2009) Le bouquet du vin: résultat d'une intégration sensorielle différente au nez et en bouche. Revue des oenologues et des techniques vitivinicoles et onologiques, 132, 53-55.
67. Ukhanov, K., Corey, E.A., Brunert, D., Klasen, K. & Ache, B.W. (2010) Inhibitory odorant signaling in Mammalian olfactory receptor neurons. J. Neurophysiol., 103, 1114-1122.
68. Vigouroux, M., Viret, P. & Duchamp, A. (1988) A wide concentration range olfactometer for delivery of short reproducible odor pulses. J. Neurosci. Methods, 24, 57-63.
69. Wiltrout, C., Dogra, S. & Linster, C. (2003) Configurational and nonconfigurational interactions between odorants in binary mixtures. Behav. Neurosci., 117, 236-245.
70. Wise, P.M., Miyazawa, T., Gallagher, M. & Preti, G. (2007) Human odor detection of homologous carboxylic acids and their binary mixtures. Chem. Senses, 32, 475-482.
71. Yamada, H. & Nakatani, K. (2001) Odorant-induced hyperpolarization and suppression of cAMP-activated current in newt olfactory receptor neurons. Chem. Senses, 26, 25-34.
72. Young, J.M., Friedman, C., Williams, E.M., Ross, J.A., Tonnes-Priddy, L. & Trask, B.J. (2002) Different evolutionary processes shaped the mouse and human olfactory receptor gene families. Hum. Mol. Genet., 11, 535-546.
73. Zhao, H. & Firestein, S. (1999) Vertebrate odorant receptors. Cell. Mol. Life Sci., 56, 647-659.
74. Zhao, H. Q., Ivic, L., Otaki, J. M., Hashimoto, M., Mikoshiba, K. & Firestein, S. (1998) Functional expression of a mammalian odorant receptor. Science, 279, 237-242.