Johan Poncelet

Humans and mice express similar olfactory preferences.

In humans, the pleasantness of odors is a major contributor to social relationships and food intake. Smells evoke attraction and repulsion responses, reflecting the hedonic value of the odorant. While olfactory preferences are known to be strongly modulated by experience and learning, it has been recently suggested that, in humans, the pleasantness of odors may be partly explained by the physicochemical properties of the odorant molecules themselves. If odor hedonic value is indeed predetermined by odorant structure, then it could be hypothesized that other species will show similar odor preferences to humans. Combining behavioral and psychophysical approaches, we here show that odorants rated as pleasant by humans were also those which, behaviorally, mice investigated longer and human subjects sniffed longer, thereby revealing for the first time a component of olfactory hedonic perception conserved across species. Consistent with this, we further show that odor pleasantness rating in humans and investigation time in mice were both correlated with the physicochemical properties of the molecules, suggesting that olfactory preferences are indeed partly engraved in the physicochemical structure of the odorant. That odor preferences are shared between mammal species and are guided by physicochemical features of odorant stimuli strengthens the view that odor preference is partially predetermined. These findings open up new perspectives for the study of the neural mechanisms of hedonic perception.

Dissociated Representations of Pleasant and Unpleasant Olfacto-Trigeminal Mixtures: An fMRI Study

How the pleasantness of chemosensory stimuli such as odorants or intranasal trigeminal compounds is processed in the human brain has been the focus of considerable recent interest. Yet, so far, only the unimodal form of this hedonic processing has been explored, and not its bimodal form during crossmodal integration of olfactory and trigeminal stimuli. The main purpose of the present study was to investigate this question. To this end, functional magnetic resonance imaging (fMRI) was used in an experiment comparing brain activation related to a pleasant and a relatively unpleasant olfacto-trigeminal mixture, and to their individual components (CO2 alone, Orange alone, Rose alone). Results revealed first common neural activity patterns in response to both mixtures in a number of regions: notably the superior temporal gyrus and the caudate nucleus. Common activations were also observed in the insula, although the pleasant mixture activated the right insula whereas the unpleasant mixture activated the left insula. However, specific activations were observed in anterior cingulate gyrus and the ventral tegmental area only during the perception of the pleasant mixture. These findings emphasized for the firs time the involvement of the latter structures in processing of pleasantness during crossmodal integration of chemosensory stimuli.

Improved smell pleasantness after odor-taste associative learning in humans

Whereas some aspects of olfactory hedonism in humans are present from birth, others form during development and throughout adulthood. Although it is generally agreed that such hedonic representations emerge by associative learning, it is not yet clear which learning parameters are prominent. The present study investigated the influence of number of trials on odor preference acquisition in human adults. Forty-eight subjects randomly assigned to three groups were tested in three sessions. In the first session, subjects ranked eight food odors from most pleasant to most unpleasant. The second session consisted in an associative learning, the two most neutral odors were randomly associated with a drink: one odor with water (CS-) and the other odor with a pleasant sweet solution (CS+). In the third session subjects ranked the eight food odors again. In group A, CS+ was paired three times with the US, and in group B only once; in group C, CS+ was paired only once with the US but with a total duration identical to that in group A. Results showed that CS+ was ranked as significantly more pleasant after learning in group A (p<.05), but not in groups B and C (p>.05). In conclusion, the study showed that a neutral smell can acquire positive emotional features after being paired with a pleasant taste, and that this learning depends on the number of associations between smell and taste.

Semantic Knowledge Influences Prewired Hedonic Responses to Odors

Background Odor hedonic perception relies on decoding the physicochemical properties of odorant molecules and can be influenced in humans by semantic knowledge. The effect of semantic knowledge on such prewired hedonic processing over the life span has remained unclear. Methodology/Principal Findings The present study measured hedonic response to odors in different age groups (children, teenagers, young adults, and seniors) and found that children and seniors, two age groups characterized by either low level of (children) or weak access to (seniors) odor semantic knowledge, processed odor hedonics more on the basis of their physicochemical properties. In contrast, in teenagers and young adults, who show better levels of semantic odor representation, the role of physicochemical properties was less marked. Conclusions/Significance These findings demonstrate for the first time that the biological determinants that make an odor pleasant or unpleasant are more powerful at either end of the life span.

Perceptual and Sensorimotor Differences between “Good” and “Poor” Olfactory Mental Imagers

Like odor perception, odor imagery is characterized by wide variability between individuals. The present two‐part study sought to assess whether this inter‐individual variability is underlain by behavioral differences in actual odor perception. In study 1, subjects judged the intensity, pleasantness, familiarity and edibility of 3 odorants. Participants were split into two olfactory imagery groups (“good” versus “poor” olfactory imagers) according to their scores on an imagery questionnaire. Results showed that good olfactory imagers judged all odors as more familiar and more edible than did poor olfactory imagers. Study 2 sought to determine whether these effects derived from a particular strategy of reenacting olfactomotor responses to smells on the part of good olfactory imagers, by recording their sniffs during odor perception. Results revealed that good olfactory imagers sniffed all odors longer and, again, judged these same odors as more edible and familiar. This supports the hypothesis of more complete odor processing and better access to odor semantics in good olfactory imagers.

Cross-modal integration of emotions in the chemical senses

Although the brain structures involved in integrating odorant and trigeminal stimuli are well-documented, there is still a need to clarify (1) how emotional response is represented in the human brain during cross-modal interaction between odors and trigeminal stimuli, and (2) whether the degree of congruency between the two types of stimuli influences these emotional responses and their neural processing. These questions were explored combining psychophysics, event-related potentials (ERP) and fMRI in the same group of 17 subjects under a “congruent condition” (intranasal carbon dioxide mixed with the smell of orange, a combination found in soda drinks, for example), and an “incongruent condition” (intranasal carbon dioxide mixed with the smell of rose, a combination not encountered in everyday life). Responses to the 3 constituent stimuli (carbon dioxide, orange, and rose) were also measured. Hedonic and intensity ratings were collected for all stimulations. The congruent bimodal stimulus was rated as more pleasant than the incongruent. This behavioral effect was associated with enhanced neural activity in the hippocampus and anterior cingulate gyrus, indicating that these brain areas mediate reactivation of pleasant and congruent olfactory-trigeminal associations.

Repeated exposure to odors induces affective habituation of perception and sniffing.

Olfactory perception, and especially hedonic evaluation of odors, is highly flexible, but some mechanisms involved in this flexibility remain to be elucidated. In the present study we aimed at better understanding how repeated exposure to odors can affect their pleasantness. We tested the hypothesis of an affective habituation to the stimuli, namely a decrease of emotional intensity over repetitions. More specifically, we tested whether this effect is subject to inter-individual variability and whether it can also be observed at the olfactomotor level. Twenty-six participants took part in the experiment during which they had to smell two odorants, anise and chocolate, presented 20 times each. On each trial, sniff duration and volume were recorded and paired with ratings of odor pleasantness and intensity. For each smell, we distinguished between “likers” and “dislikers,” namely individuals giving positive and negative initial hedonic evaluations. Results showed a significant decrease in pleasantness with time when the odor was initially pleasant (“likers”), while unpleasantness remained stable or slightly decreased when the odor was initially unpleasant (“dislikers”). This deviation toward neutrality was interpreted as affective habituation. This effect was all the more robust as it was observed for both odors and corroborated by sniffing, an objective measurement of odor pleasantness. Affective habituation to odors can be interpreted as an adaptive response to stimuli that prove over time to be devoid of positive or negative outcome on the organism. This study contributes to a better understanding of how olfactory preferences are shaped through exposure, depending on the individuals own initial perception of the odor.

Olfactory and Gustatory Mental Imagery: Modulation by Sensory Experience and Comparison to Auditory Mental Imagery

Olfactory and gustatory mental images are defined as short-term memory representations of olfactory or gustatory events that give rise to the experience of “smelling with the mind’s nose” or “tasting with the mind’s tongue.” This chapter reviews converging evidence supporting the view that, as with visual mental images, odor and taste mental images preserve some aspects of olfactory and gustatory percepts. The variability that affects both types of imagery is also considered in an experiment comparing the effect of experience on chemosensory mental imagery and auditory mental imagery.

The Presentation of Olfactory–Trigeminal Mixed Stimuli Increases the Response to Subsequent Olfactory Stimuli

The aim of this study was to evaluate the effect of (1) the addition of trigeminal stimuli to an olfactory stimulus and (2) the congruence in the odorous mixture after repeated odor presentation. Twenty-five normosmic volunteers were enrolled and presented stimulation blocks, consisting of three habituation stimuli (H) (orange odor), one dishabituation (DH) (control condition, orange odor; congruent condition, orange odor + CO2; incongruent condition, orange odor + l-isopulegol), and one dishabituated stimulus (D) (orange odor). Olfactory event-related potentials were analyzed. Response amplitudes differed significantly in the incongruent condition (N1P2 between H3 and D; peak to peak N1P2 at electrode positions Cz, Fz, and Pz; response amplitudes between H3 and DH). The addition of CO2 modified the perception of orange odor, pronouncing a fruity note, whereas the addition of l-isopulegol as a DH pronounced the l-isopulegol note. This study provides evidence that incongruent trigeminal-olfactory stimulants increase the response to subsequent olfactory stimulus.

Expertise shapes domain‐specific functional cerebral asymmetry during mental imagery: the case of culinary arts and music

Mental imagery in experts has been documented in visual arts, music and dance. Here, we examined this issue in an understudied art domain, namely, culinary arts. Previous research investigating mental imagery in experts has reported either a stronger involvement of the right hemisphere or bilateral brain activation. The first aim of our study was to examine whether culinary arts also recruit such a hemispheric pattern specifically during odor mental imagery. In a second aim, we investigated whether expertise effects observed in a given sensory domain transfer to another modality. We combined psychophysics and neurophysiology to study mental imagery in cooks, musicians and controls. We collected response times and event‐related potentials (ERP) while participants mentally compared the odor of fruits, the timbre of musical instruments and the size of fruits, musical instruments and manufactured objects. Cooks were faster in imagining fruit odors, and musicians were faster in imagining the timbre of musical instruments. These differences were not observed in control participants. This expertise effect was reflected in the ERP late positive complex (LPC): only experts showed symmetric bilateral activation, specifically when cooks imagined odors and when musicians imagined timbres. In contrast, the LPC was significantly greater in the left hemisphere than in the right hemisphere for non‐expert participants in all conditions. These findings suggest that sensory expertise does not involve transfer of mental imagery ability across modalities and highlight for the first time that olfactory expertise in cooks induces a balance of activations between hemispheres as does musical expertise in musicians.