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

Authors

  • M. A. Chaput,

    1. UMR 5292, Centre de recherche en neurosciences de Lyon, Université de Lyon, CNRS, INSERM, 50 avenue Tony Garnier, F-69366 Lyon, France
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  • F. El Mountassir,

    1. Centre des Sciences du Goût et de l’Alimentation, UMR6265 CNRS, UMR1324 INRA, Université de Bourgogne, Agrosup Dijon, F-21000 Dijon, France
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  • B. Atanasova,

    1. Centre des Sciences du Goût et de l’Alimentation, UMR6265 CNRS, UMR1324 INRA, Université de Bourgogne, Agrosup Dijon, F-21000 Dijon, France
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  • T. Thomas-Danguin,

    1. Centre des Sciences du Goût et de l’Alimentation, UMR6265 CNRS, UMR1324 INRA, Université de Bourgogne, Agrosup Dijon, F-21000 Dijon, France
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  • A. M. Le Bon,

    1. Centre des Sciences du Goût et de l’Alimentation, UMR6265 CNRS, UMR1324 INRA, Université de Bourgogne, Agrosup Dijon, F-21000 Dijon, France
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  • A. Perrut,

    1. Département Mathématiques, Institut Camille Jordan, Université de Lyon 1, 21 Avenue Claude Bernard, T-69622 Villeurbanne, France
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  • B. Ferry,

    1. UMR 5292, Centre de recherche en neurosciences de Lyon, Université de Lyon, CNRS, INSERM, 50 avenue Tony Garnier, F-69366 Lyon, France
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  • P. Duchamp-Viret

    1. UMR 5292, Centre de recherche en neurosciences de Lyon, Université de Lyon, CNRS, INSERM, 50 avenue Tony Garnier, F-69366 Lyon, France
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M. A. Chaput, as above.
E-mail: chaput@olfac.univ-lyon1.f

Abstract

The present study aimed to create a direct bridge between observations on peripheral and central responses to odorant mixtures and their components. Three experiments were performed using mixtures of fruity (isoamyl acetate; ISO) and woody (whiskey lactone; WL) odorants known to contribute to some of the major notes in Burgundy red wine. These experiments consisted of (i) calcium imaging of human embryonic kidney cells (HEK293T) transfected with olfactory receptors (ORs); (ii) single-unit electrophysiological recordings from olfactory receptor neurons (ORNs) and analyses of electro-olfactogram (EOG) responses in the rat nose in vivo; and (iii) psychophysical measurements of the perceived intensity of the mixtures as rated by human subjects. The calcium imaging and electrophysiological results revealed that ISO and WL can act simultaneously on single ORs or ORNs and confirm that receptor responses to mixtures are not the result of a simple sum of the effects of the individual mixture compounds. The addition of WL to ISO principally suppressed the ORN activation induced by ISO alone and was found to enhance this activation in a subset of cases. In the human studies, the addition of high concentrations of WL to ISO decreased the perceived intensity of the ISO. In contrast, the addition of low concentrations of WL enhanced the perceived intensity of the fruity note (ISO) in this mixture, as it enhanced EOG responses in ORNs. Thus, both OR and ORN responses to ISO + WL mixtures faithfully reflected perceptual response changes, so the odour mixture information is set up after the peripheral stage of the olfactory system.

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