The Journal of Neuroscience, March 5, 2008, 28(10):2659-2666; doi:10.1523/JNEUROSCI.4670-07.2008
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Behavioral/Systems/Cognitive
Competitive and Noncompetitive Odorant Interactions in the Early Neural Coding of Odorant Mixtures
Jean-Pierre Rospars,1
Petr Lansky,2
Michel Chaput,3 and
Patricia Duchamp-Viret3
1Institut National de la Recherche Agronomique, Unité Mixte de Recherche (UMR) 1272, Physiologie de l'Insecte and Unité Mathématiques et Informatique Appliquées, F-78000 Versailles, France, 2Institute of Physiology, Academy of Sciences of the Czech Republic, Videnska 1083, CZ-142 20 Prague 4, Czech Republic, and 3Laboratoire de Neurosciences Sensorielles, Comportement, Cognition, Centre National de la Recherche Scientifique, UMR 5020, Université de Lyon–Lyon 1, F-69366 Lyon Cedex 07, France
Correspondence should be addressed to Dr. Jean-Pierre Rospars, Institut National de la Recherche Agronomique, Unité Mixte de Recherche 1272, Physiologie de l'Insecte, F-78000 Versailles, France. Email: rospars{at}versailles.inra.fr
Most olfactory receptor neurons (ORNs) express a single type of olfactory receptor that is differentially sensitive to a wide variety of odorant molecules. The diversity of possible odorant-receptor interactions raises challenging problems for the coding of complex mixtures of many odorants, which make up the vast majority of real world odors. Pure competition, the simplest kind of interaction, arises when two or more agonists can bind to the main receptor site, which triggers receptor activation, although only one can be bound at a time. Noncompetitive effects may result from various mechanisms, including agonist binding to another site, which modifies the receptor properties at the main binding site. Here, we investigated the electrophysiological responses of rat ORNs in vivo to odorant agonists and their binary mixtures and interpreted them in the framework of a quantitative model of competitive interaction between odorants. We found that this model accounts for all concentration-response curves obtained with single odorants and for about half of those obtained with binary mixtures. In the other half, the shifts of curves along the concentration axis and the changes of maximal responses with respect to model predictions, indicate that noncompetitive interactions occur and can modulate olfactory receptors. We conclude that, because of their high frequency, the noncompetitive interactions play a major role in the neural coding of natural odorant mixtures. This finding implies that the CNS activity caused by mixtures will not be easily analyzed into components, and that mixture responses will be difficult to generalize across concentration.
Key words: sensory coding; olfactory receptor neuron; in vivo; signal transduction; allostery; mixture interaction
Received July 30, 2007;
revised Dec. 17, 2007;
accepted Jan. 20, 2008.
Correspondence should be addressed to Dr. Jean-Pierre Rospars, Institut National de la Recherche Agronomique, Unité Mixte de Recherche 1272, Physiologie de l'Insecte, F-78000 Versailles, France. Email: rospars{at}versailles.inra.fr
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