Biological constraints on configural odour mixture perception.

Comparative olfaction Elemental perception Invertebrates Odour object Odour-guided behaviour Vertebrates

Journal

The Journal of experimental biology
ISSN: 1477-9145
Titre abrégé: J Exp Biol
Pays: England
ID NLM: 0243705

Informations de publication

Date de publication:
15 03 2022
Historique:
entrez: 14 3 2022
pubmed: 15 3 2022
medline: 3 5 2022
Statut: ppublish

Résumé

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.

Identifiants

pubmed: 35285471
pii: 274695
doi: 10.1242/jeb.242274
pmc: PMC8996812
pii:
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : CNRS
Organisme : Agence Nationale de la Recherche
ID : ANR-2010-JCJC-1410-1
Organisme : Agence Nationale de la Recherche
Organisme : FEDER
Organisme : NIA NIH HHS
ID : R01 AG037693
Pays : United States

Informations de copyright

© 2022. Published by The Company of Biologists Ltd.

Déclaration de conflit d'intérêts

Competing interests The authors declare no competing or financial interests.

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Auteurs

Gérard Coureaud (G)

Centre de Recherche en Neurosciences de Lyon, Team Sensory Neuroethology (ENES), CNRS/INSERM/UCBL1/UJM, 69500 Lyon, France.

Thierry Thomas-Danguin (T)

Centre des Sciences du Goût et de l'Alimentation, Team Flavor, Food Oral Processing and Perception, INRAE, CNRS, Institut Agro Dijon, Université Bourgogne Franche-Comté, 21000 Dijon, France.

Jean-Christophe Sandoz (JC)

Evolution, Genomes, Behavior and Ecology, CNRS, Université Paris-Saclay, IRD, 91190 Gif-sur-Yvette, France.

Donald A Wilson (DA)

Department of Child & Adolescent Psychiatry, New York University Langone School of Medicine and Nathan S. Kline Institute for Psychiatric Research, New York, NY 10016, USA.

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