Biological constraints on configural odour mixture perception

Abstract

Animals, including humans, detect odours and use this information to behave efficiently in the environment. Frequently, odours consist of complex mixtures of odorants rather than single odorants, and mixtures are often perceived as configural wholes, i.e. as odour objects (e.g. food, partners). The biological rules governing this 'configural perception' (as opposed to the elemental perception of mixtures through their components) remain weakly understood. Here, we first review examples of configural mixture processing in diverse species involving species-specific biological signals. Then, we present the original hypothesis that at least certain mixtures can be processed configurally across species. Indeed, experiments conducted in human adults, newborn rabbits and, more recently, in rodents and honeybees show that these species process some mixtures in a remarkably similar fashion. Strikingly, a mixture AB (A, ethyl isobutyrate; B, ethyl maltol) induces configural processing in humans, who perceive a mixture odour quality (pineapple) distinct from the component qualities (A, strawberry; B, caramel). The same mixture is weakly configurally processed in rabbit neonates, which perceive a particular odour for the mixture in addition to the component odours. Mice and honeybees also perceive the AB mixture configurally, as they respond differently to the mixture compared with its components. Based on these results and others, including neurophysiological approaches, we propose that certain mixtures are convergently perceived across various species of vertebrates/invertebrates, possibly as a result of a similar anatomical organization of their olfactory systems and the common necessity to simplify the environment's chemical complexity in order to display adaptive behaviours.

Keywords: Comparative olfaction; Elemental perception; Invertebrates; Odour object; Odour-guided behaviour; Vertebrates.

Fig. 1.

Demonstration of configural perception of the AB mixture in four different species. In humans: (A) mean pineappleness of the AB mixture compared with its components; (B) replication including the CD mixture (ethyl caproate+furaneol); (C) mean pineappleness of AB in participants pre-exposed to AB (group G1), A and B separately (G2), a control mixture (G3), or the components of the control mixture (G4). In rabbits: (D,E,F) proportions of rabbit pups responding orally to odorants A, B or C and to the AB, A′B′ or AC mixtures 24 h after the learning of AB (D), A (E) or A then B (F); (G) responses 48 h after the learning of AB then re-exposure to A and B followed by NaCl or anisomycin (AN) injection. MP, mammary pheromone. In mice: (H) freezing of mice exposed to the conditioned stimulus (CS)+ odorant A, the elemental mixture A′B′, the configural mixture AB, and the CS– odorant vanillin (Van); (I) hierarchical cluster analysis of mouse single-unit ensembles recorded in the anterior piriform cortex (aPC) after exposure to A, B, the AB mixture or the A′B′ mixture (similar results were observed in rats, not shown). In honeybees: (J,K) proboscis extension responses (PER) in a protocol in which bees received rewarded presentations of mixture components (A/B, or hexanol/nonanol H/N) but non-rewarded presentations of the mixture (AB or HN); (L) comparison of differentiation scores (sum of responses to the rewarded elements minus those to the mixture over the whole procedure) for the AB and HN mixtures, and the control AC, BC and EF mixtures. *P<0.05, **P<0.01, ***P<0.001.