The role of taste and oral somatosensation in olfactory localization

Although there is only one set of olfactory receptors, odours are experienced as smells when sniffing things (e.g., sniffing a wine's bouquet) and as flavours when the olfactory stimulus is present in the mouth (e.g., drinking wine). How this location binding—external versus internal environment—is achieved is poorly understood. Experiment 1 employed a new procedure to study localization, which was then used to explore whether localization is primarily dependent upon simultaneous oral somatosensation. Experiment 2, using solutions of varying viscosity, and Experiment 3, using oral movement of varying vigour, revealed that sniffed odours are not localized to the mouth by somatosensation alone. Instead, Experiment 4 demonstrated that a tastant needs to be present and that increasing tastant concentration generates increasing oral localization. Experiment 5 found that this reliance upon gustation reflects the previously observed “confusion” that people show for taste and smell stimuli in the mouth. We suggest that this “confusion” reflects the gustatory system's superior ability to suppress olfactory attention, thus assisting flavour binding.     

The smell of cooperativeness: Do human body odours advertise cooperative behaviours?

Several physical features influence the perception of how cooperative a potential partner is. While previous work focused on face and voice, it remains unknown whether body odours influence judgements of cooperativeness and if odour-based judgements are accurate. Here, we first collected axillary odours of cooperative and uncooperative male donors through a public good game and used them as olfactory stimuli in a series of tasks examining whether and how they influence cooperative decision-making in an incentivized economic game and ratings of cooperativeness. Our results show that having access to the donor's body odours provided a strategic advantage to women during economic decisions (but not to men): with age, women were more likely to cooperate with cooperative men and to avoid interacting with uncooperative men. Ratings of cooperativeness were nonetheless unrelated to the donors’ actual cooperativeness. Finally, while men with masculine and intense body odours were judged less cooperative, we found no evidence that donors’ actual cooperativeness was associated with less masculine or less intense body odour. Overall, our findings suggest that, as faces and voices, body odours influence perceived cooperativeness and might be used accurately and in a non-aware manner as olfactory cues of cooperativeness, at least by women.     

The discrimination of dog odours by humans

The domestic dog is able to identify both individual conspecifics, i.e. other dogs, and individual interspecifics, e.g. humans, by smell. Whilst humans can recognise individual members of their own species using olfactory information, it is unknown whether they can identify members of any other species in this manner. We examined the ability of humans to identify individual dogs by smell. Twenty-six dog owners were required to smell two blankets, one impregnated with the odour of their own dog, the other impregnated with the odour of an unfamiliar dog. Participants were required to indicate which of the odours smelt the strongest, which smelt the most pleasant, and which of the odours belonged to their own dog. Most of the participants (88.5%) were able to recognise the odour of their own dog. They showed no significant bias, however, in responding which of the odours they thought smelt the strongest or most pleasant. The results indicate that dogs produce odours that are individually distinctive to their owners, and highlight the fact that humans can recognise members of another species using olfactory cues--an ability presumably acquired without conscious effort.     

Smelling objects

Objects are central to perception and our interactions with the world. We perceive the world as parsed into discrete entities that instantiate particular properties, and these items capture our attention and shape how we interact with the environment. Recently there has been some debate about whether the sense of smell allows us to perceive odours as discrete objects, with some suggesting that olfaction is aspatial and doesn’t allow for object-individuation. This paper offers two empirically tractable criteria for assessing whether particular objects are exhibited in perceptual experience—(1) susceptibility to figure-ground segregation and (2) perceptual constancies—and argues that these criteria are fulfilled by olfactory perception, and thus there are olfactory objects. I argue that there are, in fact, two different ways that olfaction allows for figure-ground segregation. First, I look at various Gestalt grouping principles, which are thought to govern when features are perceived as grouped into structured wholes, segregated from everything around them. I argue that these principles apply to olfactory experience, providing evidence of non-spatial figure-ground segregation. Second, I defend the contentious idea that a spatial variety of figure-ground segregation can also occur in olfaction. To see this, however, we need to look to empirical evidence showing that tactile stimulation and bodily movements play a crucial role in olfactory phenomenology. Finally, I draw on empirical evidence and olfactory phenomenology to argue that there are perceptual constancies in olfactory experience, allowing us to perceive odours as coherent objects that survive shifts in our perspectives on the world.

     

Olfactory cues are more effective than visual cues in experimentally triggering autobiographical memories

Folk wisdom often refers to odours as potent triggers for autobiographical memory, akin to the Proust phenomenon that describes Proust’s sudden recollection of a childhood memory when tasting a madeleine dipped into tea. Despite an increasing number of empirical studies on the effects of odours on cognition, conclusive evidence is still missing. We set out to examine the effectiveness of childhood and non-childhood odours as retrieval cues for autobiographical memories in a lab experiment. A total of 170 participants were presented with pilot-tested retrieval cues (either odours or images) to recall childhood memories and were then asked to rate the vividness, detail, and emotional intensity of these memories. Results showed that participants indeed reported richer memories when presented with childhood-related odours than childhood-related images or childhood-unrelated odours or images. An exploratory analysis of memory content with Linguistic Inquiry and Word Count did not reveal differences in affective content. The findings of this study support the notion that odours are particularly potent in eliciting rich memories and open up numerous avenues for further exploration.     

Item-specific proactive interference in olfactory working memory

We examine item-specific olfactory proactive interference (PI) effects and undertake comparisons with verbal and non-verbal visual stimuli. Using a sequential recent-probes task, we show no evidence for PI with hard-to-name odours (Experiment 1). However, verbalisable odours do exhibit PI effects (Experiment 2). These findings occur despite above chance performance and similar serial position functions across both tasks. Experiments 3 and 4 apply words and faces, respectively, to our modified procedure, and show that methodological differences cannot explain the null finding in Experiment 1. The extent to which odours exhibit analogous PI effects to that of other modalities is, we argue, contingent on the characteristics of the odours employed.     

Embryonic olfactory learning in frogs.

We examined the effect of embryonic olfactory experiences on behaviour after hatching in two species of anuran amphibians, Rana temporaria and Rana sylvatica. Odorants (orange and citral) injected into the egg were "learned" by the embryo and subsequently preferred by tadpoles after hatching. The observed preferences were specific to the odours experienced prior to hatching, and tadpoles discriminated between the odour experienced as embryos and a novel odour. The acquired preference was maintained after metamorphosis for those individuals that exhibited a preference as tadpoles. Preferences of tadpoles were also influenced "naturally" by odours present in the water surrounding the developing embryos. The experimentally induced olfactory preferences did not appear to influence the exhibition of sibling recognition abilities. The study represents the first demonstration of "embryonic" learning in amphibians, and the functions and importance of early olfactory learning for amphibians are discussed.     

Embryonic olfactory learning in frogs

We examined the effect of embryonic olfactory experiences on behaviour after hatching in two species of anuran amphibians, Rana temporaria and Rana sylvatica. Odorants (orange and citral) injected into the egg were “learned” by the embryo and subsequently preferred by tadpoles after hatching. The observed preferences were specific to the odours experienced prior to hatching, and tadpoles discriminated between the odour experienced as embryos and a novel odour. The acquired preference was maintained after metamorphosis for those individuals that exhibited a preference as tadpoles. Preferences of tadpoles were also influenced “naturally” by odours present in the water surrounding the developing embryos. The experimentally induced olfactory preferences did not appear to influence the exhibition of sibling recognition abilities. The study represents the first demonstration of “embryonic” learning in amphibians, and the functions and importance of early olfactory learning for amphibians are discussed.     

Olfactory awareness is positively associated to odour memory

We investigated the relationship between olfactory awareness and olfactory proficiency as determined by a set of standardised olfactory tasks. Olfactory awareness was indexed by scores in questionnaires focusing on odour interest, imagery ability, and prevalence of olfactory dreams. Nineteen subjects with high and 20 subjects with low odour awareness were presented with a set of standardised olfactory tasks: odour threshold, episodic odour recognition, and odour identification. The results showed that individuals with high odour awareness excelled in odour memory and identified more odours as compared with the low awareness group. Interestingly, odour naming ability exerted no influence on odour memory. Furthermore, high odour awareness was not related to a more sensitive olfactory sensory system as determined by olfactory threshold measurements.     

Are olfactory images sensory in nature?

We investigated the features of olfactory mental images by comparing odour images with perceptual and semantic representations. Participants who were assigned to three groups made similarity judgments about 17 common odours by smelling odours, imagining odours, or on the basis of the meaning of odour source names. In the smelling group, every pair of odours was compared. In the imagining group, imagined odours were compared twice, both before and after associative learning of the odour/name combinations. In the meaning group, the odour source names were compared in terms of general word meanings. Nonmetric multidimensional scaling analysis was applied to each group of similarity data and three-dimensional sensory, mental, and semantic spaces were composed. 17 elements in the mental and semantic spaces were superimposed onto the sensory space by Procrustes rotation. We found that the averaged distances of the 17 elements between the sensory and the mental spaces (either before or after learning) were smaller than those between the sensory and semantic spaces. We suggest that odour images have sensory features, especially after associative learning between perceived odours and their names.     

Phenomenological differences between familiar and unfamiliar odours

Unfamiliar odours are harder to discriminate than familiar odours. We explored the phenomenal basis of this difference. In experiments la and 1b, participants profiled odour quality for two sets of familiar and unfamiliar odours. In both cases unfamiliar odours were redolent of more odour qualities than familiar stimuli. In experiment 2, participants received (i) a set of familiar and unfamiliar odours and learnt their names, and (ii) a further set of familiar and unfamiliar odours to which they were exposed. Participants then profiled these stimuli as well as a further unexposed set of familiar and unfamiliar odours. Exposure, but not naming, led to a significantly smaller difference between the familiar and unfamiliar stimuli, in terms of their redolence to other odours, when compared to unexposed control stimuli. Unfamiliar exposed odours were also judged as less redolent than unexposed unfamiliar odours. These observations are consistent with a mnemonic basis for odour-quality perception.     

Synaptic adaptation and odor-background segmentation

Habituation is a form of non-associative memory that plays an important role in filtering stable or redundant inputs. The present study examines the contribution of habituation and cortical adaptation to odor-background segmentation. Segmentation of target odorants from background odorants is a fundamental computational requirement for the olfactory system. Recent electrophysiological data have shown that odor specific adaptation in piriform cortex neurons, mediated at least partially by synaptic adaptation between the olfactory bulb outputs and piriform cortex pyramidal cells, may provide an ideal mechanism for odor-background segmentation. This rapid synaptic adaptation acts as a filter to enhance cortical responsiveness to changing stimuli, while reducing responsiveness to static, potentially background stimuli. Using previously developed computational models of the olfactory system, we here show how synaptic adaptation at the olfactory bulb input to the piriform cortex, as demonstrated electrophysiologically, creates odor specific adaptation. We show how this known feature of olfactory cortical processing can contribute to adaptation to a background odor and to odor-background segmentation. We then show in a behavioral experiment that the odor-background segmentation is perceptually important and functions at the same time-scale as the synaptic adaptation observed between the olfactory bulb and cortex.     

Olfactory hedonic context affects both self-report and behavioural indices of palatability

Prior exposure to either a pleasant or unpleasant context may affect later hedonic judgments of a common target stimulus. We explored whether this effect translates into behaviour in the chemical senses. In experiment 1 participants experienced either a pleasant or unpleasant set of odours or pictures, followed by an unfamiliar odour. After self-report hedonic evaluations of the odour, participants were allowed to drink it in solution, followed by a further evaluation of its flavour. Participants reported liking the odour less after smelling pleasant odours and drank less of it too, relative to the unpleasant context. There was no differential context effect for emotive pictures. Experiment 2 replicated these effects, but also included a no-context control. This revealed that the consumption effect was localised to the pleasant olfactory context, whilst contextual effects for liking ratings were primarily localised to the unpleasant olfactory context. In conclusion, hedonic context affects both self-report and behaviour, but not in the same way.     

The nonclassical mereology of olfactory experiences

Synthese - While there is a growing philosophical interest in analysing olfactory experiences, the mereological structure of odours considered in respect of how they are perceptually experienced...     

Odour memory and odour hedonics in children

The characteristics of olfactory memory during development were investigated and the hypothesis that the pleasantness of smells may be affected by previous associations with pleasant or unpleasant objects or events was tested. This type of emotional memory was compared in the immediate and long-term recognition of olfactory stimuli. Children from three different age groups (mean ages: 6 years 6 months; 8 years 9 months; and 10 years 5 months) were subdivided into two groups. One group was presented with six different odours, each with a slide depicting a pleasant picture. The other group was presented with the odours accompanied by unpleasant pictures. Immediately after stimulus presentation the subjects underwent a recognition test. One month later the subjects underwent a second recognition test, at the end of which they were required to give an evaluation of the pleasantness of each odour on a nine-point scale. At no age level did the pictures matched to the odours affect the recognition score. Olfactory memory varied with age, chiefly because memory decay increased with age, perhaps because of greater proactive interference. With increasing age more rapid decay was set against better immediate recognition. The hypothesis that the hedonic characteristics of odours are partially learned and are affected by events experienced in other modalities was supported.     

Sex differences in human olfaction: Between evidence and enigma

The sex of individuals plays an important part in determining their olfactory abilities, with females generally being superior to males. The present review examines the way in which sex differences influence sensitivity, identification, familiarity, and recognition of odours. It also examines whether sex differences are more pronounced with some odours than others, and how sex differences are affected by the manner of testing. Two different explanations for the superiority of females over males in olfaction are evaluated.     

Different importance of the volatile and non-volatile fractions of an olfactory signature for individual social recognition in rats versus mice and short-term versus long-term memory

When tested in the olfactory cued social recognition/discrimination test, rats and mice differ in their retention of a recognition memory for a previously encountered conspecific juvenile: Rats are able to recognize a given juvenile for approximately 45 min only whereas mice show not only short-term, but also long-term recognition memory (≥ 24 h). Here we modified the social recognition/social discrimination procedure to investigate the neurobiological mechanism(s) underlying the species differences. We presented a conspecific juvenile repeatedly to the experimental subjects and monitored the investigation duration as a measure for recognition. Presentation of only the volatile fraction of the juvenile olfactory signature was sufficient for both short- and long-term recognition in mice but not rats. Applying additional volatile, mono-molecular odours to the "to be recognized" juveniles failed to affect short-term memory in both species, but interfered with long-term recognition in mice. Finally immunocytochemical analysis of c-Fos as a marker for cellular activation, revealed that juvenile exposure stimulated areas involved in the processing of olfactory signals in both the main and the accessory olfactory bulb in mice. In rats, we measured an increased c-Fos synthesis almost exclusively in cells of the accessory olfactory bulb. Our data suggest that the species difference in the retention of social recognition memory is based on differences in the processing of the volatile versus non-volatile fraction of the individuals' olfactory signature. The non-volatile fraction is sufficient for retaining a short-term social memory only. Long-term social memory - as observed in mice - requires a processing of both the volatile and non-volatile fractions of the olfactory signature.     

Odor memory: Review and analysis

We critically review the cognitive literature on olfactory memory and identify the similarities and differences between odor memory and visual-verbal memory. We then analyze this literature using criteria from a multiple memory systems approach to determine whether olfactory memory can be considered to be a separate memory system. We conclude that olfactory memory has a variety of important distinguishing characteristics, but that more data are needed to confer this distinction. We suggest methods for the study of olfactory memory that should make a resolution on the separate memory system hypothesis possible while simultaneously advancing a synthetic understanding of olfaction and cognition.     

Peak shift in honey bee olfactory learning

If animals are trained with two similar stimuli such that one is rewarding (S+) and one punishing (S?), then following training animals show a greatest preference not for the S+, but for a novel stimulus that is slightly more different from the S? than the S+ is. This peak shift phenomenon has been widely reported for vertebrates and has recently been demonstrated for bumblebees and honey bees. To explore the nature of peak shift in invertebrates further, here we examined the properties of peak shift in honey bees trained in a free-flight olfactory learning assay. Hexanal and heptanol were mixed in different ratios to create a continuum of odour stimuli. Bees were trained to artificial flowers such that one odour mixture was rewarded with 2 molar sucrose (S+), and one punished with distasteful quinine (S?). After training, bees were given a non-rewarded preference test with five different mixtures of hexanal and heptanol. Following training bees’ maximal preference was for an odour mixture slightly more distinct from the S? than the trained S+. This effect was not seen if bees were initially trained with two distinct odours, replicating the classic features of peak shift reported for vertebrates. We propose a conceptual model of how peak shift might occur in honey bees. We argue that peak shift does not require any higher level of processing than the known olfactory learning circuitry of the bee brain and suggest that peak shift is a very general feature of discrimination learning.     

Can but don’t: olfactory discrimination between own and alien offspring in the domestic cat

Mammalian maternal care usually comes at a large energetic cost. To maximize their fitness, mothers should preferentially care for their own offspring. However, the majority of studies of mother–offspring recognition have focused on herd- or colony-living species and there is little information on maternal discrimination in more solitary-living species. Olfaction has been found to play a major role in mother–offspring recognition across various taxa. Therefore, our aim was to study this in a species evolved from a solitary-living ancestor, the domestic cat. We asked whether cat mothers distinguish between their own and alien offspring when providing maternal care, and whether cat mothers use olfactory cues in the offspring discrimination process. Results of Experiment 1 showed that cat mothers do not discriminate between own and alien young when retrieving them to the nest. They treated own and alien young similarly with respect to latency and order of retrieval. However, the results of Experiments 2 and 3, where we used an olfactory habituation-discrimination technique, showed that mothers were able to distinguish between the odours of their own and alien kittens. We discuss what ecological and/or behavioural factors might influence a mother’s decision when faced with discriminating between own and alien young, and why mothers might not discriminate between them when they are able to do so. Our findings support the view that maternal care alone should not be used as a measure of offspring recognition, and equal maternal care of own and alien young should not be immediately interpreted as an inability to discriminate between them.