Memory of single odorant or odorant mixture in the newborn rabbit: Time-course, mechanisms and functions – MEMOLAP

The ethological approach (G. Coureaud/T. Thomas-Danguin) enabled to promote, by conditioning, the acquisition of single odorants or mixtures of odorants in newborn rabbits and to determine through behavioural testing their ability to distinctively respond to, and thus discriminate, these information over a shorter or longer period. In addition, by measuring the weight of neonates before and after the daily nursing, we assessed whether the exposure to a learned odorant or a mixture of odorants scented on the abdomen of the mother facilitated nipple location and milk intake.
The pharmacological approach (G. Ferreira) allowed to selectively disrupt the memory of some odours learned in mixture and to evaluate whether newborns remembered differently odorants which constitute a mixture from the whole mixture itself.
Finally, the neurobiological approach (F. Datiche) allowed imaging the brain activation and analyzing the activity in situations of neonatal exposure to an odorant, to ascertain how it changes before/after learning, and whether and how it differs according to the perception of the odorant alone or in mixture with a second odorant.

Three main results emerge from this project: 1) the perception of certain odour mixtures as “objects” and not mere assembly of components. This is demonstrated here even early in life and in absence of learning; 2) the distinct memory of the mixture vs. its components after learning the “mixture object”; 3) the specific brain processing of the mixture object vs. its odorants, and the plasticity of this processing after learning. This work paves the way for new national and international collaborations on the topic of odour mixture perception, and brings interesting data to industry and public health.

During this project we met researchers from other laboratories (one in France and one in the USA) with whom collaborations have been started and are currently fundraising. These collaborations will allow to accentuate the knowledge of processes highlighted here in the rabbit, and to expand our investigation to other species, including humans. Indeed, every organism is confronted to odours in mixtures. Thus, in animals from different species, we suspect that common perceptual and neurosensory processes allow to treat certain mixtures as odor objects. In this domain, obtaining better knowledges paves the way to economic issues (e.g. characterization of the typical bouquet allowing the identification and recognition of a food or perfume by consumers) and public health (reduction of risk compounds - salt, sugar - without modifying the olfactory appreciation of food, detection of a contaminant in a chemically complex environment).

This project resulted in the publication of seven scientific papers in renowned international journals, one additional manuscript is currently in the process of peer review and one other is in preparation. Furthermore, 24 communications in international (14) or national (10) conferences were made. One article and 3 actions were also designed for the general public. Finally, a scientific conference was organized with more than 200 people (French researchers and students, foreign guests) interested in animal behavior.

In mammals, maternal odour signals affect significantly and sometimes primarily the feeding behaviour of the newborn since they contribute to the localization and oral seizing of the nipples. However, their neonatal perception in the highly complex natural environment remains weakly known. A vital need for the newborn is indeed to extract information from the environmental complexity. He can achieve it while answering in a predisposed way to certain odour molecules (pheromones) and/or while learning new odorants that quickly acquire a biological value through the action of reinforcing agents. But one can wonder how the newborn perceives, incorporates, memorizes and associates together these molecules within the mixtures of odorants that surround it, and at which moment and how a simplification of the surrounding chemical complexity relies on the attribution of the value of signal to a mixture as a whole more than to some of its components.

In an original way, the present project aims to determine in 8 Experiments how olfactory cues impact the feeding behaviour of young mammals during the first postnatal days according to their complexity, i.e. when cues are single odorants perceived out of mixture (Task 1 - Exp. 1 to 4) or the same odorants perceived in mixture (Task 2 - Exp. 5 to 8). In parallel of behavioural investigations, we will study the memory and cerebral reorganization induced by the learning of these simple/complex odour stimuli (Tasks 1+2). To that goal, the European rabbit constitutes a particularly relevant model system. Indeed, newborn rabbits a) display a stereotyped sucking behaviour in response to maternal odours; b) the signals emitted by the mother are pheromones (the Mammary Pheromone; MP) or perinatally learned stimuli; c) the MP promotes in pups the extremely rapid learning of a novel odorant/mixture of odorants that becomes then an efficient releaser of sucking behaviour and may thus influences the milk intake during nursing; d) some identified odour mixtures have been demonstrated to be perceived by newborn rabbits in an elemental (perception of the odours of each component of the mixture) or configural way (perception of an odour specific to the mixture); e) methods for ethological, chemical, neurobiological (c-fos cerebral imaging) and neuropharmacological (use of agents that induce selective amnesia of consolidated information) investigations related to the learning, perception and behavioural responses of rabbit pups to these odorants/odour mixtures exist and are already used by the young researchers involved in the present programme.

In a scientific and social context currently concerned by questions related to the development of feeding behaviour and food preferences, we propose here an unprecedented multidisciplinary research project aiming to better understand the bond established by the organism with food from early in life, and the cerebral, cognitive and behavioural mechanisms engaged in the perception/memorization of the more or less complex flavour of food substrates, which governs their acceptance. This program should lead to important theoretical issues related to the coding, perception, discrimination, retention and behavioural outcomes of the learning of single odorants or odour mixtures referred to food. It is of direct interest for our own species since the mixtures used here in rabbit pups are known to be perceived in a similar way (elemental or configural) by human adults. Finally, the results should trigger attention of the industrial and public health domains.