Perceptual and processing differences between physical and dichorhinic odor mixtures
Introduction
Most odors that we encounter in our daily life are comprised of hundreds of individually smelling components. For instance, the smell of a rose can be comprised of more than 200 components (although not necessarily perceived as more complex than the rose-smelling single component phenyl ethyl alcohol; Keller and Vosshall, 2004). How, then, are the components of a natural odor combined into a more or less unitary percept? Most studies indicate that odors do not combine additively, that is, neural or perceptual responses to mixtures are not linear sums of responses to components. Instead, the intensity of responses is typically less than would be expected from simple additivity (Ferreira, 2012). Moreover, individual components in the mixture percept can be more or less suppressed and the overall mixture quality can vary in how well individual components can be perceived (Jinks and Laing, 2001, Sinding et al., 2013). These interactions can take place at the peripheral or various central levels of the olfactory sensory pathway (Cruz and Lowe, 2013). The focus of the current study was to investigate what effect these interactions could have on binary odor mixtures when controlling for the route of stimulation (monorhinic or dichorhinic).
Odorant interaction has been observed in the periphery, for instance through competition, where one agonist competes for the same receptor site with another agonist or antagonist. Noncompetitive, e.g. allosteric interaction has also been observed. That is, the main binding site is then activated by an agonist whereas occupation at a second site modifies the binding or activation properties of the agonist at the main site (Rospars, 2013). Whereas studies on fruit fly favor competitive interaction (Münch et al., 2013), studies on rat clearly indicate the occurrence of noncompetitive interactions. A study of several binary mixtures (Rospars et al., 2008) indicated that about half of the mixtures could be described by a syntopic interaction model that is based on competitive interaction, and the other half implied noncompetitive interaction. The authors argued that this noncompetitive modulation added a new combinatorial dimension of olfactory coding that may contribute to the emergence of new perceptual qualities different from each component.
Although interaction is indicated at the periphery (Chaput et al., 2012), more central processing may also be a part in forming the mixture percept (Rouby and Holley, 1995, Boyle et al., 2009, Zhou and Chen, 2009). Boyle et al. (2009) showed that the lateral part of the orbitofrontal cortex seems to respond to the impurity of a mixture in a graded fashion, and the anterior part seems to act more like an on–off detector for odor mixtures. Psychophysically, the difference between peripheral and central processing can be investigated by utilizing the fact that the human nose is comprised of two nasal chambers, divided by a septum, each leading up to an olfactory epithelium. The olfactory receptors neurons in the epithelium of each side project information to its ipsilateral olfactory bulb. The projections from the olfactory bulb to the primary olfactory cortex, via the lateral olfactory tract are primarily ipsilateral (Price, 1990, Shipley and Reyes, 1991, Lascano et al., 2010). However, there are also contralateral connections via the anterior commissure, the corpus callosum, and the hippocampal commissure (Shipley and Ennis, 1996, Doty et al., 1997). Overall, the olfactory system seems to mainly project information ipsilaterally to the side of stimulation (Gottfried, 2006). By comparing the effects of presenting a mixture of two substances in the same nostril (physical mixture) in comparison to presenting the same two odorants simultaneously into separate nostrils (dichorhinic mixture) the specific contribution of interactions at the receptor site can be estimated. A few such studies have been performed. Laing and Willcox (1987) found that the suppression of the individual componentś qualities that is typically observed as a result of mixing was generally larger for physical than for dichorhinic mixtures. In line with these results, Cain (1975) reported that individual components were suppressed more in physical mixtures and that the overall intensity of dichorhinic mixtures tended to be higher than that of physical mixtures. Cain nevertheless concluded that the interaction of physical and dichorhinic mixtures was “similar”. Rouby and Holley (1995) pursued temporal aspects of mixture interaction. They presented mixture components with some or no delay between components and found – overall – a higher suppression of individual components’ qualities in dichorhinic compared to physical mixtures. Taken together, dichorhinic mixtures are more intense than physical, although individual components have been shown to be both more and less suppressed in dichorhinic mixtures.
With behavioral and electro-physiological techniques, the current study investigated the effects of peripheral processing by comparing physical and dichorhinic mixtures, thus utilizing that via dichorhinic presentation of mixture components, the peripheral interaction can be bypassed making the resulting percept dependent on central processes. The aim was threefold: (1) to study the change of overall intensity observed for dichorhinic mixtures; (2) to investigate whether such release from overall change of mixture intensity, based on bypassing the peripheral site of interaction, would affect the quality, and (3) to test whether the perception of physical and dichorhinic mixtures was paralleled by according changes in early and late measures of olfactory event-related potentials (OERP). Early components of the OERP are believed to reflect more sensory aspects of the stimulus processing, such as stimulus intensity and quality, whereas later components are associated with more cognitive aspects, such as the familiarity or salience of the stimulus (Hummel and Kobal, 2001).
Section snippets
Participants
Twenty-four healthy volunteers, 12 men and 12 women, between the ages of 18 and 35 years participated in the study [mean (M) = 23.9, standard deviation (SD) = 3.6]. All participants were right-handed and non-smokers. Handedness was assessed using a translated version of the Edinburgh Inventory (Oldfield, 1971), participants scoring equal or less than +9 were excluded from the study. Using the “Sniffin’ Sticks” threshold test (Hummel et al., 1997), all participants were screened for threshold
Perception
The route of delivery altered the perceived intensity (Fig. 1a). When presented dichorinally, mixtures were rated as more intense than when presented monorhinally (Dichorhinic mixtures: M = 36.4, SD = 18.8; Physical mixtures: M = 32.4, SD = 18.5); t(19) = −2.23, p = .038).
Both mixtures exhibited a nominal dominance of A (eugenol) over B (l-carvone); for physical mixtures this dominance was significant (odor A: M = 57.1%, SD = 13.9; one-sample t-test against 50%; t(19) = 2.26, p = .036), but not for dichorhinic
Discussion
The current study set out to test early processing of binary odor mixtures. In line with Cain (1975) the results indicated that dichorhinic mixtures are more intense than physical mixtures. In other words, a binary mixture stimulus, distributed over two sensory epithelia (i.e., odorant A to one epithelium and B to the other) was perceived as more intense than the same two components presented to one side. Moreover, the perceived quality had a tendency to shift between mixture types. In parallel
Conclusion
Peripheral interaction between mixture components is analyzed by bypassing the first site of possible interaction, the receptor surface. This approach revealed changes in basic aspects of perception that were corroborated, for the first time, by electrophysiological measurements.
Acknowledgments
Thanks to Johan Lundström for comments on a previous version of this manuscript. Funded by the Swedish Research Council (421 2005-1779; 421 2012-1225) to M.J.O., by Stiftelsen Lars Hiertas Minne to M.S. and by a grant from the Deutsche Forschungsgemeinschaft to T.H. (DFG HU 441/10-1).
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