Verbal cues modulate hedonic perception of odors in 5-year-old children as well as in adults

The judgment of pleasantness/unpleasantness is the prominent reaction to the olfactory world. In human adults, the hedonic valence of odor perception is affected by various factors, among which is an individual's lexical knowledge about smells. The present study examined whether such top-down effects of lexical knowledge on hedonic judgment of olfactory input are similar in children (5-6 years) and adults (20-25 years). In both groups, the lexical knowledge was found to influence the perception of the least emotional (or most neutral) odors: the pleasantness of the smells of banana and mint was enhanced when participants were given the corresponding odor label before olfactory sensation. These results lend support to the notion that, during childhood, smells are not only encoded perceptually but that verbal encoding also steers contextual effects that may be prominent factors in the early memorization and categorization of odors.     

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.     

Ghrelin, leptin and adiponectin as possible predictors of the hedonic value of odors

Several lines of evidence point to a close relationship between the hormones of energy homeostasis and the olfactory system. Examples are the localization of leptin and adiponectin receptors in the olfactory system or increased activation of brain regions related to the palatability and the hedonic value of food in response to food pictures after application of ghrelin. In this preliminary study, we tested in 31 subjects (17 male and 14 female) if and to what extent the peripheral blood concentrations of "satiety" hormones, such as leptin, adiponectin, and ghrelin (acyl and total), are correlated with the self-ratings of odor pleasantness and with the objective olfactory and gustatory ability. The hedonic values of some odors were found to be differently rated between donors depending on gender and body weight. The concentrations of leptin, adiponectin and total ghrelin were significantly associated with the hedonic value of pepper black oil, but failed to show significant correlations for 5 other odors tested. Except for a significant association between leptin and odor identification, hormone concentrations were not linked to the abilities of smell and taste. Peripheral adipokines and gut hormones may alter the perception and pleasantness of specific odors, presumably either directly through their receptors in the olfactory system or indirectly through central interfaces between the regulation systems of olfaction, appetite control, memory and motivation.     

Molecular and cellular basis of human olfaction

The human olfactory systems recognize and discriminate a large number of different odorant molecules. The detection of chemically distinct odorants begins with the binding of an odorant ligand to a specific receptor protein in the ciliary membrane of olfactory neurons. To address the problem of olfactory perception at a molecular level, we have cloned, functionally expressed, and characterized some of the human olfactory receptors from chromosome 17. Our results show that a receptor protein is capable of recognizing the particular chemical substructure of an odor molecule and, therefore, is able to respond only to odorants that have a defined molecular structure. These findings represent the beginning of the molecular understanding of odorant recognition in humans. In the future, this knowledge could be used for the design of synthetic ideal receptors for specific odors (biosensors), or the perfect odor molecule for a given receptor.     

Measures of human olfactory perception during pregnancy

Although considerable anecdotal evidence suggests that pregnancy affects olfactory sensitivity, scientific evidence is limited and inconclusive. Whereas hedonic ratings are affected by pregnancy, odor identification is not. The aim of the current study was to examine odor perception in women across pregnancy and in the postpartum period. One hundred nonsmoking women who were pregnant, postpartum, or had never been pregnant were tested on the University of Pennsylvania Smell Identification Test (UPSIT). Intensity ratings and scratch patterns were collected as potential indicators of sensitivity, and participants rated the odors' pleasantness. Participants also rated their own sense of smell. Mean UPSIT scores did not differ significantly across groups indicating no difference in odor identification. Trends in planned comparisons suggested that in the first trimester, odors were rated as more intense and less pleasant. In the first trimester, women scratched the odor strips significantly fewer times. Consistent with previous reports, 90% of pregnant women reported that specific odors smelled less pleasant and 60% reported that some odors smelled more pleasant. Although nearly two-thirds of pregnant women rated their olfactory sensitivity to be enhanced during pregnancy and overall pregnant women's self-rated olfactory sensitivity was higher than controls', self-ratings were not correlated with UPSIT scores nor odor intensity ratings. These results suggest that these and previous findings may reflect the fact that the effect of pregnancy on olfaction is small and inconsistent.     

Slow breathing and emotions associated with odor-induced autobiographical memories

An important feature of olfactory perception is its dependence on respiratory activity. By inspiration, olfactory information ascends directly to olfactory-related limbic structures. Therefore, every breath with odor molecules activates these limbic areas associated with emotional experience and memory retrieval. We tested whether odors associated with autobiographical memories can trigger pleasant emotional experiences and whether respiration changes during stimulation with these odors. During presentation of odors related to autobiographical memories and control odors, we measured minute ventilation, tidal volume, respiratory frequency, O2 consumption, and end tidal CO2 concentration. Findings showed that autobiographical memory retrieval was associated with increasing tidal volume and decreasing respiratory frequency more than during presentation of control odors. Subjective feelings such as emotional arousal during retrieval of the memory, arousal level of the memory itself, or pleasantness and familiarity toward the odor evoked by autobiographical memory were more specific emotional responses compared with those related to control odors. In addition, high trait anxiety subjects responded with a stronger feeling of being taken back in time and had high arousal levels with tidal volume increases. We discussed assumptions regarding how deep and slow breathing is related to pleasantness and comfortableness of an autobiographical memory.     

Hemispheric lateralization in the processing of odor pleasantness versus odor names

It is well established that for most people linguistic processing is primarily a left hemisphere activity, whereas recent evidence has shown that basic odor perception is more lateralized to the right hemisphere. Importantly, under certain conditions, emotional responding also shows right hemisphere laterality. Hedonic (pleasantness) assessments constitute basic level emotional responses. Given that olfaction is predominantly ipsilateral in function, it was hypothesized that odor pleasantness evaluations may be accentuated by right nostril perception and that odor naming would be superior with left nostril perception. To test this prediction we presented eight familiar neutral-mildly pleasant odors for subjects to sniff through the left and right nostrils. Subjects smelled each odor twice (once through each nostril) at two different sessions, separated by 1 week. At each session subjects provided pleasantness, arousal and naming responses to each odorant. Results revealed that odors were rated as more pleasant when sniffed through the right nostril and named more correctly when sniffed through the left. No effects for arousal were obtained. These findings are consistent with previously demonstrated neural laterality in the processing of olfaction, emotion and language, and suggest that a local and functional convergence may exist between olfaction and emotional processing.     

Emotional processing of odors: evidence for a nonlinear relation between pleasantness and familiarity evaluations

Pleasantness, familiarity, and intensity are 3 interdependent dimensions commonly used to describe the perceived qualities of an odor. In particular, many empirical studies have demonstrated a positive correlation between familiarity and pleasantness. However, on the basis of both theoretical and methodological perspectives, we questioned the validity of such a relation for malodors. We report 2 studies based on subjective judgments of a large sample of odorants (Experiment 1) associated with autonomic recordings (Experiment 2). Multivariate exploratory analysis performed on the data splits the whole odorant set into 2 subsets composed, respectively, of unpleasant and pleasant odorants. Subsequent correlation analyses have shown that the relation between pleasantness and familiarity is specific for the pleasant odors in the 2 experiments. Moreover, autonomic activity was more important in response to malodors than to pleasant odors and was significantly correlated with unpleasantness ratings in the subset of unpleasant odors. These 2 studies argue in favor of a functional dissociation in the relations between both subjective and autonomic responses to odors as a function of pleasantness and indicate that researchers in the olfactory domain should consider the relations between pleasantness and familiarity as more complex than linear.     

Affected by smells? Environmental chemical responsivity predicts odor perception

Strong negative reactions, physical symptoms, and behavioral disruptions due to environmental odors are common in the adult population. We investigated relationships among such environmental chemosensory responsivity (CR), personality traits, affective states, and odor perception. Study 1 showed that CR and neuroticism were positively correlated in a sample of young adults (n = 101), suggesting that persons high in neuroticism respond more negatively to environmental odors. Study 2 explored the relationships among CR, noise responsivity (NR), neuroticism, and odor perception (i.e., pleasantness and intensity) in a subset of participants (n = 40). High CR was associated with high NR. Regression analyses indicated that high CR predicted higher odor intensity ratings and low olfactory threshold (high sensitivity) predicted lower pleasantness ratings. However, neuroticism was not directly associated with odor ratings or thresholds. Overall, the results suggest that CR and odor thresholds predict perceptual ratings of odors and that high CR is associated with nonchemosensory affective traits.     

Auditory-olfactory integration: congruent or pleasant sounds amplify odor pleasantness

Even though we often perceive odors while hearing auditory stimuli, surprisingly little is known about auditory-olfactory integration. This study aimed to investigate the influence of auditory cues on ratings of odor intensity and/or pleasantness, with a focus on 2 factors: "congruency" (Experiment 1) and the "halo/horns effect" of auditory pleasantness (Experiment 2). First, in Experiment 1, participants were presented with congruent, incongruent, or neutral sounds before and during the presentation of odor. Participants rated the odors as being more pleasant while listening to a congruent sound than while listening to an incongruent sound. In Experiment 2, participants received pleasant or unpleasant sounds before and during the presentation of either a pleasant or unpleasant odor. The hedonic valence of the sounds transferred to the odors, irrespective of the hedonic tone of the odor itself. The more the participants liked the preceding sound, the more pleasant the subsequent odor became. In contrast, the ratings of odor intensity appeared to be little or not at all influenced by the congruency or hedonic valence of the auditory cue. In conclusion, the present study for the first time provides an empirical demonstration that auditory cues can modulate odor pleasantness.     

The major histocompatibility complex and the chemosensory signalling of individuality in humans

The chemosensory identity of mice and rats is determined partly by polymorphic genes of the major histocompatibility complex (MHC). In inbred strains of mice, as well as in seminatural populations, MHC‐associated mating preferences selectively influence reproductive success, thus serving to promote heterozygocity in the MHC. In order to determine whether MHC‐associated chemosignals are present in humans, two studies were conducted. In a first study, olfactory identification of MHC‐associated chemosignals was conducted on 12 trained rats' responses to the urine odors of humans. In a second study, MHC‐associated olfactory cues in humans were analyzed by means of gas chromatography. The results indicate that the urine odors of humans are associated with the MHC and demonstrate that the profile of volatile components in the urine odors shows some association with the MHC. Furthermore, results show that a profile of some specific components, as well as a few ubiquitous volatiles, constitutes MHC‐associated odor signals in humans. This revised version was published online in July 2006 with corrections to the Cover Date.     

Hedonic taste in Drosophila revealed by olfactory receptors expressed in taste neurons

Taste and olfaction are each tuned to a unique set of chemicals in the outside world, and their corresponding sensory spaces are mapped in different areas in the brain. This dichotomy matches categories of receptors detecting molecules either in the gaseous or in the liquid phase in terrestrial animals. However, in Drosophila olfactory and gustatory neurons express receptors which belong to the same family of 7-transmembrane domain proteins. Striking overlaps exist in their sequence structure and in their expression pattern, suggesting that there might be some functional commonalities between them. In this work, we tested the assumption that Drosophila olfactory receptor proteins are compatible with taste neurons by ectopically expressing an olfactory receptor (OR22a and OR83b) for which ligands are known. Using electrophysiological recordings, we show that the transformed taste neurons are excited by odor ligands as by their cognate tastants. The wiring of these neurons to the brain seems unchanged and no additional connections to the antennal lobe were detected. The odor ligands detected by the olfactory receptor acquire a new hedonic value, inducing appetitive or aversive behaviors depending on the categories of taste neurons in which they are expressed i.e. sugar- or bitter-sensing cells expressing either Gr5a or Gr66a receptors. Taste neurons expressing ectopic olfactory receptors can sense odors at close range either in the aerial phase or by contact, in a lipophilic phase. The responses of the transformed taste neurons to the odorant are similar to those obtained with tastants. The hedonic value attributed to tastants is directly linked to the taste neurons in which their receptors are expressed.     

Just noticeable differences in component concentrations modify the odor quality of a blending mixture

The odors we perceive are mainly the result of mixtures of odorants that, however, are commonly perceived as single undivided entities; nevertheless, the processes involved remain poorly explored. It has been recently reported that perceptual blending based on configural olfactory processing can cause odorant mixtures to give rise to an emergent odor not present in the components. The present study examined whether specific component proportions are required to elicit an emergent odor. Starting from the composition of a ternary target mixture in which an emergent pineapple odor was perceived, 4 concentration levels of each component were chosen to elicit just noticeable differences (JNDs). Each combination of levels was used to design sample mixtures. Fifteen subjects evaluated the intensity, typicality, and pleasantness of each sample mixture against the target mixture in a paired-comparison protocol. Statistical modeling showed that a variation of less than 1 JND in one of the components was sufficient to induce a significant decrease in pineapple odor typicality in the ternary mixture. This finding confirms previous findings on perceptual blending in simple odorant mixtures and underscores the human ability to discriminate between odor percepts induced by mixtures including very similar odorant proportions.     

Odor representations in the rat olfactory bulb change smoothly with morphing stimuli

Many species of mammals are very good at categorizing odors. One model for how this is achieved involves the formation of "attractor" states in the olfactory processing pathway, which converge to stable representations for the odor. We analyzed the responses of rat olfactory bulb mitral/tufted (M/T) cells using stimuli "morphing" from one odor to another through intermediate mixtures. We then developed a phenomenological model for the representation of odors and mixtures by M/T cells and show that >80% of odorant responses to different concentrations and mixtures can be expressed in terms of smoothly summing responses to air and the two pure odorants. Furthermore, the model successfully predicts M/T cell responses to odor mixtures when respiration dependence is eliminated. Thus, odor mixtures are represented in the bulb through summation of components, rather than distinct attractor states. We suggest that our olfactory coding model captures many aspects of single and mixed odor representation in M/T cells.     

Perceptual blending in odor mixtures depends on the nature of odorants and human olfactory expertise

Our olfactory system is confronted with complex mixtures of odorants, often recognized as single entities due to odor blending (e.g., coffee). In contrast, we are also able to discriminate odors from complex mixtures (e.g., off-odors). Therefore, the olfactory system is able to engage either configural or elemental processes when confronted with mixtures. However, the rules that govern the involvement of these processes during odor perception remain poorly understood. In our first experiment, we examined whether simple odorant mixtures (binary/ternary) could elicit configural perception. Twenty untrained subjects were asked to evaluate the odor typicality of mixtures and their constituents. The results revealed a significant increase in odor typicality in some but not all mixtures as compared with the single components, which suggest that perceptual odor blending can occur only in specific mixtures (configural processing). In our second experiment, we tested the hypothesis that general olfactory expertise can improve elemental perception of mixtures. Thirty-two trained subjects evaluated the odor typicality of the stimuli presented during the first experiment, and their responses were compared with those obtained from the untrained panelists. The results support the idea that general training with odors increases the elemental perception of binary and ternary blending mixtures.     

Rapid encoding and perception of novel odors in the rat

To gain insight into which parameters of neural activity are important in shaping the perception of odors, we combined a behavioral measure of odor perception with optical imaging of odor representations at the level of receptor neuron input to the rat olfactory bulb. Instead of the typical test of an animal's ability to discriminate two familiar odorants by exhibiting an operant response, we used a spontaneously expressed response to a novel odorant—exploratory sniffing—as a measure of odor perception. This assay allowed us to measure the speed with which rats perform spontaneous odor discriminations. With this paradigm, rats discriminated and began responding to a novel odorant in as little as 140 ms. This time is comparable to that measured in earlier studies using operant behavioral readouts after extensive training. In a subset of these trials, we simultaneously imaged receptor neuron input to the dorsal olfactory bulb with near-millisecond temporal resolution as the animal sampled and then responded to the novel odorant. The imaging data revealed that the bulk of the discrimination time can be attributed to the peripheral events underlying odorant detection: receptor input arrives at the olfactory bulb 100–150 ms after inhalation begins, leaving only 50–100 ms for central processing and response initiation. In most trials, odor discrimination had occurred even before the initial barrage of receptor neuron firing had ceased and before spatial maps of activity across glomeruli had fully developed. These results suggest a coding strategy in which the earliest-activated glomeruli play a major role in the initial perception of odor quality, and place constraints on coding and processing schemes based on simple changes in spike rate.     

Use of ultrasonic vocalizations to assess olfactory detection in mouse pups treated with 3-methylindole

Altricial mammals use olfaction long before the olfactory bulb has reached its anatomically mature state. Indeed, while audition and vision are still not functional, the olfactory system of newborn animals can clearly process distinct odorant molecules. Although several previous studies have emphasized the important role that olfaction plays in early critical functions, it has been difficult to develop a sensitive and reliable test to precisely quantify olfactory ability in pups. One difficulty in determining early sensory capabilities is the rather limited behavioral repertory of neonates. The present study examines the use of ultrasonic vocalizations emitted by isolated rodent pups as a potential index of odor detection in newborn mice. As early as postnatal day 2, mice reliably decrease their emission of ultrasonic calls in response to odor exposure to the bedding of adult male mice but not in response to clean bedding odors or to non-social odorant molecules. A toxin known to damage the olfactory epithelium in adult, the 3-methylindole, impairs the ultrasonic call responses triggered by exposure to male bedding, thus confirming the efficiency of this olfactotoxin on mice pups. The administration of 3-methylindole severely reduced the life expectancy of the majority of subjects. This result is discussed according to the critical role of olfaction in nipple-seeking behavior in mouse pups.     

Improvement of aroma in transgenic potato as a consequence of impairing tuber browning

Sensory analysis studies are critical in the development of quality enhanced crops, and may be an important component in the public acceptance of genetically modified foods. It has recently been established that odor preferences are shared between humans and mice, suggesting that odor exploration behavior in mice may be used to predict the effect of odors in humans. We have previously found that mice fed diets supplemented with engineered nonbrowning potatoes (-PPO) consumed more potato than mice fed diets supplemented with wild-type potatoes (WT). This prompted us to explore a possible role of potato odor in mice preference for nonbrowning potatoes. Taking advantage of two well established neuroscience paradigms, the "open field test" and the "nose-poking preference test", we performed experiments where mice exploration behavior was monitored in preference assays on the basis of olfaction alone. No obvious preference was observed towards -PPO or WT lines when fresh potato samples were tested. However, when oxidized samples were tested, mice consistently investigated -PPO potatoes more times and for longer periods than WT potatoes. Congruently, humans discriminated WT from -PPO samples with a considerably better performance when oxidized samples were tested than when fresh samples were tested in blind olfactory experiments. Notably, even though participants ranked all samples with an intermediate level of pleasantness, there was a general consensus that the -PPO samples had a more intense odor and also evoked the sense-impression of a familiar vegetable more often than the WT samples. Taken together, these findings suggest that our previous observations might be influenced, at least in part, by differential odors that are accentuated among the lines once oxidative deterioration takes place. Additionally, our results suggest that nonbrowning potatoes, in addition to their extended shelf life, maintain their odor quality for longer periods of time than WT potatoes. To our knowledge this is the first report on the use of an animal model applied to the sensory analysis of a transgenic crop.