Developmental changes in elemental and configural perception of odor mixtures in young rabbits.

Development can change the way organisms represent their environment and affect their behavior. In vision, complex stimuli are treated as the sum of their elements (elemental perception) in children or as a whole (configural perception) in adults. However, the influence of development in elemental/configural perception has never been tested in olfaction. Here we explored this issue in young rabbits, which are known to perceive during the neonatal period certain binary odor mixtures elementally and others weak configurally. Using conditioning and behavioral testing procedures, we set out six experiments evaluating the putative evolution of their odor perception between birth and weaning. Results highlighted that between postnatal days 2 and 9 the perception of an initially weak configural mixture became robust configural while that of two elemental mixtures did not. Additional switches from elemental to configural perception were observed at postnatal day 24. The use of a chemically more complex senary mixture resulted also in a shift from weak to robust configural perception between postnatal days 2 and 9. Thus, the perception of certain odor mixtures may rapidly evolve toward a more holistic mode in young rabbits, which may help simplifying their representation of the environment once out of the nest.

Feel, smell and see in an egg: emergence of perception and learning in an immature invertebrate, the cuttlefish embryo.

It is now well established that prenatal sensory experience affects development itself and has long-term consequences in terms of postnatal behavior. This study focused on the functionality of the sensory system in cuttlefish in ovo. Embryos of stage 23, 25 and 30 received a tactile, chemical or visual stimulus. An increase of mantle contraction rhythm was taken to indicate a behavioral response to the stimulus. We clearly demonstrated that tactile and chemical systems are functional from stage 23, whereas the visual system is functional only from stage 25. At stage 25 and 30, embryos were also exposed to a repeated light stimulus. Stage 30 embryos were capable of habituation, showing a progressive decrease in contractions across stimulations. This process was not due to fatigue as we observed response recovery after a dishabituation tactile stimulus. This study is the first to show that cuttlefish embryos behaviorally respond to stimuli of different modalities and that the visual system is the last to become functional during embryonic development, as in vertebrate embryos. It also provides new evidence that the memory system develops in ovo in cuttlefish.

Configural processing of odor mixture: does the learning of elements prevent the perception of configuration in the newborn rabbit?

Although elemental perception of odor mixtures allows us to perceive the component odor qualities, configural perception leads to the emergence of a new odor percept. The 6-odorant Red Cordial (RC) mixture is weak configurally perceived in newborn rabbits, meaning that pups respond to the odorants after conditioning to the mixture but cannot generalize to the mixture after conditioning to a single odorant. They need to know more than 50% of the elements to respond to the mixture. This suggests that their responsiveness to RC depends on the familiar vs. unfamiliar bits of information that they perceive in it. To go further, we tested the complementary hypothesis that after learning 4 or 5 odorants, the configural perception disappears, allowing pure elemental perception of the whole mixture. In Exp. 1, repeated conditionings to RC decreased the pups' responsiveness to the odorants, i.e., facilitated RC configural perception. In Exp. 2, pups were first conditioned to a sub-mixture of 4 or 5 RC elements and then repeatedly conditioned to RC to determine whether early elemental learning reduced the facilitation of RC configural perception. As pups weakly responded to the RC mixture components, the early conditioning did not prevent this facilitation. In Exp. 3, after daily conditioning to the sub-mixture and then to the whole mixture, the configural perception of RC remained unaffected. The present results confirm that rabbit pups respond to the configural RC mixture according to the perceived ratio of familiar/unfamiliar cues and highlight that the perception of the RC configuration resists the previous acquisition of elements that compose the mixture.

Newborn rabbit perception of 6-odorant mixtures depends on configural processing and number of familiar elements.

Perception of odors, i.e. usually of mixtures of odorants, is elemental (the odorants' odor qualities are perceived in the mixture) or configural (the odor quality of the mixture differs from the one of each odorant). In human adults, the Red Cordial (RC) mixture is a configurally-processed, 6-odorant mixture. It evokes a red cordial odor quality while none of the elements carries that odor. Interestingly, in newborn rabbits, the same RC mixture is weak configurally perceived: the newborns behaviorally respond to all the elements after conditioning to the whole mixture, but not to the mixture after conditioning to a single element. Thus, they perceive in the RC mixture both the odor quality of the RC configuration and the quality of each element. Here, we aimed to determine whether this perception is modulated by quantitative (number of elements) and/or qualitative bits of information (nature of elements) previously learned by the animals. Newborns were conditioned to RC sub-mixtures of different complexity and composition before behavioral testing to RC. Pups generalized their sucking-related response to RC after learning at least 4 odorants. In contrast, after conditioning to sub-mixtures of another 6-odorant mixture, the elementally perceived MV mixture, pups responded to MV after learning one or two odorants. The different generalization to RC and MV mixtures after learning some of their elements is discussed according to three hypotheses: i) the configural perception of RC sub-mixtures, ii) the ratio of familiar/unfamiliar individual information elementally and configurally perceived, iii) the perception of RC becoming purely elemental. The results allow the first hypothesis to be dismissed, while further experiments are required to distinguish between the remaining two.

The perception of odor objects in everyday life: a review on the processing of odor mixtures.

Smelling monomolecular odors hardly ever occurs in everyday life, and the daily functioning of the sense of smell relies primarily on the processing of complex mixtures of volatiles that are present in the environment (e.g., emanating from food or conspecifics). Such processing allows for the instantaneous recognition and categorization of smells and also for the discrimination of odors among others to extract relevant information and to adapt efficiently in different contexts. The neurophysiological mechanisms underpinning this highly efficient analysis of complex mixtures of odorants is beginning to be unraveled and support the idea that olfaction, as vision and audition, relies on odor-objects encoding. This configural processing of odor mixtures, which is empirically subject to important applications in our societies (e.g., the art of perfumers, flavorists, and wine makers), has been scientifically studied only during the last decades. This processing depends on many individual factors, among which are the developmental stage, lifestyle, physiological and mood state, and cognitive skills; this processing also presents striking similarities between species. The present review gathers the recent findings, as observed in animals, healthy subjects, and/or individuals with affective disorders, supporting the perception of complex odor stimuli as odor objects. It also discusses peripheral to central processing, and cognitive and behavioral significance. Finally, this review highlights that the study of odor mixtures is an original window allowing for the investigation of daily olfaction and emphasizes the need for knowledge about the underlying biological processes, which appear to be crucial for our representation and adaptation to the chemical environment.

Cerebral correlates of visual lateralization in Sepia.

The common cuttlefish, Sepia officinalis (cephalopod mollusc) has recently become a relevant model for studying the setting-up of brain asymmetry among invertebrates. As the animals age from 3 to 30 days post hatching, they progressively develop a left-turning bias resulting from an eye-use preference. The aim of this study is to investigate whether anatomical (vertical, peduncle, inferior buccal, and optic lobes) or neurochemical (monoamines in optic lobes) brain asymmetries are present in the cuttlefish brain at 3 or at 30 post hatching days; and whether these correlate with side-turning preferences. We here find brain and behavioral asymmetry only at 30 post hatching days. Cuttlefish displayed a significant population bias towards a larger right peduncle lobe, and higher monoamine concentration in the left optic lobe (i.e. serotonin, dopamine and noradrenaline). None of these brain asymmetries were correlated to the studied side-turning bias. However, we found individual variation in the magnitude of the vertical and optic lobes asymmetry. A striking correlation was found with the behavioral results: the larger the right optic lobe and the right part of the vertical lobe, the stronger the bias to turn leftwards. To our knowledge, this is the first study to demonstrate a relationship at the individual level between brain and behavioral asymmetries in invertebrates.