Hedonic and sensory characteristics of odors conditioned by pairing with tastants in humans

Animals readily acquire positive odor-taste hedonic associations, but evidence for this in humans remains weak and was explored further. Retronasal pairing of odors with sucrose or salty stimuli (Experiment 1) increased the rated sweetness of sucrose-paired odors without altering liking, although changes in odor pleasantness correlated with sucrose liking. Experience of odors with sucrose or quinine by sweet likers (Experiment 2) found increased pleasantness and sweetness for sucrose-paired odors, whereas quinine-paired odors became less liked and more bitter. Odor-sucrose pairings in sweet likers and dislikers (Experiment 3) found increased sweetness in both groups but increased odor liking only in likers. These data suggest that evaluative and sensory learning are dissociable and that evaluative changes are sensitive to individual differences in sweet liking.     

Resistance to extinction of conditioned odor perceptions: evaluative conditioning is not unique

A tasteless odor will smell sweeter after being sampled by mouth with sucrose and will smell sourer after being sampled with citric acid. This tasty-smell effect was found in experiments that compared odor-taste and color-taste pairings. Using odors and colors with minimal taste (Experiment 1), the authors found that repeated experience of odor-taste mixtures produced conditioned changes in odor qualities that were unaffected by intermixed color-taste trials (Experiment 2). An extinction procedure, consisting of postconditioning presentations of the odor in water, had no detectable effect on the changed perception of an odor (Experiments 3 and 4). In contrast, this procedure altered judgments about the expected taste of colored solutions. Evaluative conditioning (conditioned changes in liking) is claimed to be resistant to extinction. However, these results suggest that resistance to extinction in odors is related to the way they are encoded rather than to their hedonic properties.     

Olfactory categorization: A developmental study

This study examined the ability of children to classify fruit and flower odors. We asked four groups of children (4-11years of age) and a group of adults to identify, categorize, and evaluate the edibility, liking, and typicality of 12 fruit and flower odors. Results showed an increase in interindividual agreement with age for the taxonomic (fruit/flower) and function-based (edible/nonedible) categories but not for the hedonic component. So, it seems that this hedonic component is not the explicit basis for this increase in interindividual agreement when categorizing an odor as a fruit/flower odor or as being edible or nonedible. An age-related trend was also observed on the typicality scores: The youngest group of children did not show a typicality gradient, but all of the other groups did. Blackcurrant and lemon were rated as the most typical fruit odors, whereas raspberry and peach were rated as the least typical. For flower odorants, results were not as clear, yet it seems that for all groups lavender was considered as quite typical.     

The effect of verbal context on olfactory perception

Three experiments were conducted to examine how verbal context and sensory stimulation interact to influence odor hedonic perception. Eight common odors were presented in their natural and synthetic forms, and verbal labels designating name and source (natural, synthetic) information were either explicitly given, self-generated, falsely provided, or not provided. Results revealed that verbal information about source influenced hedonic ratings whether or not the odorant itself was also present. When odorants were presented without verbal labels, olfactory evaluations were based in sensation. Name and source information contributed different levels of meaning and influence to perceptual evaluations. The findings are discussed with reference to an experiential-collocation model for odor-label interactions and a dual-coding hypothesis for olfactory perception.     

The influence of verbal labeling on the perception of odors: evidence for olfactory illusions?

Using the definition that an illusion is observed when a stimulus is invariant but context alters its perception, we examined whether verbal context could produce olfactory illusions. To test this effect, we chose five odors with minimally fixed sources and that could be interpreted with various hedonic connotations. The odors were violet leaf, patchouli, pine oil, menthol, and a 1:1 mixture of isovaleric and butyric acids. Subjects individually sniffed each odor at two different sessions separated by one week. At each session an odor was given a different verbal label (either positive or negative) and subjects rated the odors on several hedonic scales and provided perceptual and interpretative responses to them. Results showed that the perception of an odor could be significantly influenced by the label provided for it. We propose that the cases where verbal labels inverted odor perception are the first empirical demonstrations of olfactory illusions.     

Acquired hedonic and sensory characteristics of odours: Influence of sweet liker and propylthiouracil taster status

Repeated pairings of novel food-related odours with sweet tastes can result in enduring changes in sweetness of the odour alone, but have less consistent effects on odour liking. Variation in ability to taste propylthiouracil (PROP) might account for this, since PROP supertasters (ST) have been reported both to experience stronger sweetness intensity and to be more likely to dislike sweetness than do PROP nontasters (NT). Alternatively, individual differences in liking for sweetness may transfer to sweet-paired odours independently of PROP sensitivity. To explore this, evaluations of sucrose, saccharin, and PROP solutions were used to classify 92 volunteers as either sweet likers or dislikers and as PROP ST, NT, or medium tasters (MT). Changes in pleasantness of odours that had been paired with the taste of saccharin increased in sweet likers but decreased in dislikers. Odour sweetness increased regardless of PROP taster or sweet liker status. PROP ST rated saccharin as more bitter than did other taster groups and also showed greater increases in acquired bitterness of the saccharin-paired odour. Overall, these data suggest that individual differences in evaluation of saccharin reliably predict subsequent changes in evaluation of saccharin-paired odours, with hedonic changes corresponding with liking for sweet tastes and sensory changes reflecting differences in sensory quality between PROP taster groups.     

Similarity in the qualities of individual odors among kin and species in Turkish (Mesocricetus brandti) and golden (Mesocricetus auratus) hamsters.

In this investigation, the authors used habituation techniques to explore similarities and differences in the qualities of individual odors from hamsters. In Experiment 1, male Turkish hamsters (Mesocricetus brandti) treated flank-gland odors of 2 males from 1 litter as similar compared with the odor of a male from another litter, whether the odor donors were familiar or unfamiliar. At the same time, the Turkish hamsters discriminated between the subtle differences in the individual odors of their familiar brothers. In Experiment 2, male Turkish and golden hamsters (Mesocricetus auratus) treated the flank-gland odors of 2 unfamiliar, unrelated conspecifics as similar compared with the flank odor of a heterospecific individual. The results suggest that similarities in individual odors are related to genetic similarity of the odor donors. These similarities could provide a basis for different types of social recognition, including kin and species recognition.     

Smelling what was there: Acquired olfactory percepts are resistant to further modification

Repeated exposure to a mixture of two odors can increase their perceived similarity to each other when presented separately. Experiment 1 failed to detect any reduction of this effect by an interference treatment consisting of separate exposures to the odors after they had first been presented as a mixture. Exposure to a mixture also results in participants mistakenly rating this mixture and its elements as having occurred with equal frequency (i.e., confusing the mixture and its elements). The interference treatment did not affect this either, whereas it did change judgments about the frequency of a color–odor mixture and its elements. The greater resistance to interference of odor–odor learning compared to color–odor learning may result from configural encoding of odor–odor mixtures. Experiment 2 found that separate exposures to two odors not previously mixed decreased their perceived similarity. This result was inconsistent with the possibility that the interference treatment in Experiment 1 had tended to increase the similarity of the two odors, for example, by a process of sensory adaptation. Rather it suggested a process akin to acquired distinctiveness.     

Age-related changes in children's hedonic response to male body odor

Male sweat smells disgusting to many adults, but it is unclear whether children find it so. In Experiment 1A, children (mean age = 8.7 years) and adolescents (M=16.6 years) smelled male sweat and other odors, rated each for liking, and attempted their identification. Only female adolescents disliked male sweat and could identify it. Experiment 1B, using the same procedure, obtained this gender difference in adults (M=26.7 years). In Experiment 2, children (M=8.1 years) and adolescents (M=16.6 years) were cued about the identity of the same odors. Irrespective of gender, adolescents disliked male sweat more than did children. In sum, dislike for the odor of male sweat may be an acquired social response that is based on odor identification.     

Long-lasting memory for an odor acquired at the mother's breast

Whether neonatal odor memory can persist into toddlerhood and influence behaviors that tap processes related to cognition (attention and exploration), motivation (choice and consumption), and emotion (hedonic processing) remains under-researched. Using a quasi-experimental longitudinal design, we examined whether an odor experienced at the mother's breast can be retained at 7 and 21 months. The prescribed prophylactic use of a camomile-scented balm defined two groups: infants exposed (CaE) or never exposed (CaNE) to camomile odor. At 7 months, exploratory responses to three similar objects differing in odor (including camomile) were analyzed. At 21 months, three tasks were used to assess toddlers' (i) facial responses; (ii) exploratory responses to three similar, but differently odorized objects; and (iii) choices between two bottles carrying different odors. CaE infants displayed preferential responses for camomile odor at both ages in every task. In contrast, CaNE infants behaved either randomly or more negatively to camomile odor. This study indicates that early odor memories acquired during breastfeeding can be reactivated and influence behavioral processes until at least toddlerhood.     

Influence du contexte sémantique sur la performance d'identification d'odeurs

Our olfactory knowledge is mainly implicit and the last step for cognitive processing of odors — naming — is not always performed. To facilitate naming, odor identification by forced choice between alternatives is used. However, presenting names induces semantic priming. To assess which level of spontaneous odor processing is influenced by semantic context, we compared three priming conditions. Our results indicate that the identification process is based mainly on the rejection of semantic categories that are most remote from the target, and firstly of those with a different hedonic valence. The analysis of identification errors supports the hypothesis that odor naming rests more on global semantic discriminations than on what is called lexical access in other sensory modes.     

Scopolamine enhances generalization between odor representations in rat olfactory cortex

Acetylcholine (ACh) has a critical, modulatory role in plasticity in many sensory systems. In the rat olfactory system, both behavioral and physiological data indicate that ACh may be required for normal odor memory and synaptic plasticity. Based on these data, neural network models have hypothesized that ACh muscarinic receptors reduce interference between learned cortical representations of odors within the piriform cortex. In this study, odor receptive fields of rat anterior piriform cortex (aPCX) single-units for alkane odors were mapped before and after either a systemic injection of the muscarinic receptor antagonist scopolamine (0.5 mg/kg) or aPCX surface application of 500 μM scopolamine (or saline/ACSF controls). Cross-habituation between alkanes differing by two to four carbons was then examined following a 50-sec habituating stimulus. The results demonstrate that neither aPCX spontaneous activity nor odor-evoked activity (receptive field) was affected by scopolamine, but that cross-habituation in aPCX neurons was enhanced significantly by either systemic or cortical scopolamine. These results indicate that scopolamine selectively enhances generalization between odor representations in aPCX in a simple memory task. Given that ACh primarily affects intracortical association fibers in the aPCX, the results support a role for the association system in odor memory and discrimination and indicate an important ACh modulatory control over this basic sensory process.     

The role of the dorsal CA1 and ventral CA1 in memory for the temporal order of a sequence of odors

Memory for the temporal order of a sequence of odors was assessed in male rats. A sequence of five odors mixed in sand was presented in digging cups one at a time to each rat in a sequence that varied on each trial. A reward was buried in each cup. Following the fifth odor, two of the previous five odors were presented simultaneously and the rat needed to choose the odor that occurred earliest in the sequence to receive a reward. Temporal separations of 1, 2, or 3 were used which represented the number of odors that occurred between the two odors in the sequence. Once pre-operative criterion was reached, rats received a control, dorsal CA1 (dCA1), or ventral CA1 (vCA1) lesion and were retested on the task. On post-operative trials, only the vCA1 group was impaired relative to both control and dCA1 groups. All groups of rats could discriminate between the odors. The data suggest that the vCA1, but not dorsal CA1, is involved in separating sensory events (odors) in time so that one odor can be remembered separate from another odor.     

Recognition memory for social and non-social odors: differential effects of neurotoxic lesions to the hippocampus and perirhinal cortex

The contributions of the hippocampus (HC) and perirhinal cortex (PER) to recognition memory are currently topics of debate in neuroscience. Here we used a rapidly-learned (seconds) spontaneous novel odor recognition paradigm to assess the effects of pre-training N-methyl-D-aspartate lesions to the HC or PER on odor recognition memory. We tested memory for both social and non-social odor stimuli. Social odors were acquired from conspecifics, while non-social odors were household spices. Conspecific odor stimuli are ethologically-relevant and have a high degree of overlapping features compared to non-social household spices. Various retention intervals (5 min, 20 min, 1h, 24h, or 48 h) were used between study and test phases, each with a unique odor pair, to assess changes in novelty preference over time. Consistent with findings in other paradigms, modalities, and species, we found that HC lesions yielded no significant recognition memory deficits. In contrast, PER lesions caused significant deficits for social odor recognition memory at long retention intervals, demonstrating a critical role for PER in long-term memory for social odors. PER lesions had no effect on memory for non-social odors. The results are consistent with a general role for PER in long-term recognition memory for stimuli that have a high degree of overlapping features, which must be distinguished by conjunctive representations.     

Interactions between conditioned and unconditioned flavor preferences

Five experiments investigated how rats' conditioned preferences or aversions for aqueous odors paired with sucrose or salt are affected by their unconditioned response to those tastes. Rats preferred an odor paired with 30% sucrose over an odor paired with 5% sucrose when both were presented in 5% sucrose, but they showed no preference or, if thirsty, showed the reverse preference, when the odors were presented in 30% sucrose. These changes in conditioned preference corresponded to changes in the rats' unconditioned preference for the accompanying sucrose solution. Rats' conditioned aversions for odors paired with salt showed a similar dependence on their reaction to the accompanying salt solution. The results were interpreted as showing that conditioned and unconditioned flavor preferences combine additively, as if mediated by the same sensory representation.     

The Sound of Smell: Associating Odor Valence With Disgust Sounds

Olfaction has recently been highlighted as a sense poorly connected with language. Odor is difficult to verbalize, and it has few qualities that afford mimicry by vision or sound. At the same time, emotion is thought to be the most salient dimension of an odor, and it could therefore be an olfactory dimension more easily communicated. We investigated whether sounds imitative of an innate disgust response can be associated with unpleasant odors. In two experiments, participants were asked to make a forced choice between a pseudoword including a disgust sound and a neutral pseudoword, for pleasant and unpleasant odors. Overall, participants chose more disgust pseudowords than neutral pseudowords for unpleasant odors, but this was not the case for pleasant odors. This effect was not driven by a general association between unpleasant sounds and unpleasant odors, but specifically the sounds [x/χ] and [f], thought to reflect physical responses to disgusting odors, as seen in the Polish fu! or the English ugh!. In line with growing evidence that language can encode odor, we provide the first experimental evidence for an association between the sound of a word and odor valence.     

Role of verbal encoding in shortand long-term odor recognition

The role of verbal encoding in odor recognition memory was investigated using odors of low familiarity to subjects before the experiment began. The experimental procedure included two phases—odor learning (first phase) and odor memory testing (second phase)—separated by a delay of 7 days. Five experimental conditions were established: three conditions of odor learning with names (labeling conditions), one condition of odor learning without names (sensory familiarization), and one condition of no learning prior to testing (control conditions). The labeling conditions differed from each other regarding label characteristics. The names were those of odor sources (veridical names), those personally generated by subjects (generated names), or those derived from the chemical names of the odorants (chemical names). Subjects were required to learn 20 fixed associations between odors (targets or distractors) and 20 names during two daily sessions. The learning sessions included two identification tests and ended by a verbal memory test in which subjects recalled odor names. The odor memory test was split into two parts separated by a retention interval of either 20 min (short-term memory) or 24 h (long-term memory). Data showed that olfactory recognition memory was enhanced in subjects who associated veridical or generated names to odors during the learning session. Chemical names were not appropriate to facilitate odor recognition. Similarly, the level of odor identification was higher for veridical and generated names than for chemical names, though the level of verbal memory for chemical names was substantial. Recognition response latencies were systematically longer for a target odor implying a positive response than for a distractor odor implying a negative response. Together, these data suggest that odor recognition and identification are sensitive to the semantic content of labels associated with odors. Odor memory was adversively influenced by time, but this influence was less pronounced when the names were endowed with a rich semantic content.