The Orbitofrontal Cortex Is Required for Learned Modulation of Innate Olfactory Behavior.

Animals have evolved innate responses to cues including social, food, and predator odors. In the natural environment, animals are faced with choices that involve balancing risk and reward where innate significance may be at odds with internal need. The ability to update the value of a cue through learning is essential for navigating changing and uncertain environments. However, the mechanisms involved in this modulation are not well defined in mammals. We have established a new olfactory assay that challenges a thirsty mouse to choose an aversive odor over an attractive odor in foraging for water, thus overriding their innate behavioral response to odor. Innately, mice prefer the attractive odor port over the aversive odor port. However, decreasing the probability of water at the attractive port leads mice to prefer the aversive port, reflecting a learned override of the innate response to the odors. The orbitofrontal cortex (OFC) is a fourth-order olfactory brain area, involved in flexible value association, with behaviorally relevant outputs throughout the limbic system. We performed optogenetic and chemogenetic silencing experiments that demonstrate the OFC is necessary for this learned modulation of innate aversion to odor. Further, we characterized odor evoked c-fos expression in learned and control mice and found significant suppression of activity in the bed nucleus of the stria terminalis, lateral septum, and central and medial amygdala. These findings reveal that the OFC is necessary for the learned override of innate behavior and may signal to limbic structures to modulate innate response to odor.

A Rose by Another Name? Odor Misnaming is Associated with Linguistic Properties.

Naming common odors is a surprisingly difficult task: Odors are frequently misnamed. Little is known about the linguistic properties of odor misnamings. We test whether odor misnamings of old adults carry information about olfactory perception and its connection to lexical-semantic processing. We analyze the olfactory-semantic content of odor source naming failures in a large sample of older adults in Sweden (n = 2479; age 58-100 years). We investigate whether linguistic factors and semantic proximity to the target odor name predict how odors are misnamed, and how these factors relate to overall odor identification performance. We also explore the primary semantic dimensions along which misnamings are distributed. We find that odor misnamings consist of surprisingly many vague and unspecific terms, such as category names (e.g., fruit) or abstract or evaluative terms (e.g., sweet). Odor misnamings are often strongly associated with the correct name, capturing properties such as its category or other abstract features. People are also biased toward misnaming odors with high-frequency terms that are associated with olfaction or gustation. Linguistic properties of odor misnamings and their semantic proximity to the target odor name predict odor identification performance, suggesting that linguistic processing facilitates odor identification. Further, odor misnamings constitute an olfactory-semantic space that is similar to the olfactory vocabulary of English. This space is primarily differentiated along pleasantness, edibility, and concreteness dimensions. Odor naming failures thus contain plenty of information about semantic odor knowledge.

Single-neuron representations of odours in the human brain.

Olfaction is a fundamental sensory modality that guides animal and human behaviour1,2. However, the underlying neural processes of human olfaction are still poorly understood at the fundamental-that is, the single-neuron-level. Here we report recordings of single-neuron activity in the piriform cortex and medial temporal lobe in awake humans performing an odour rating and identification task. We identified odour-modulated neurons within the piriform cortex, amygdala, entorhinal cortex and hippocampus. In each of these regions, neuronal firing accurately encodes odour identity. Notably, repeated odour presentations reduce response firing rates, demonstrating central repetition suppression and habituation. Different medial temporal lobe regions have distinct roles in odour processing, with amygdala neurons encoding subjective odour valence, and hippocampal neurons predicting behavioural odour identification performance. Whereas piriform neurons preferably encode chemical odour identity, hippocampal activity reflects subjective odour perception. Critically, we identify that piriform cortex neurons reliably encode odour-related images, supporting a multimodal role of the human piriform cortex. We also observe marked cross-modal coding of both odours and images, especially in the amygdala and piriform cortex. Moreover, we identify neurons that respond to semantically coherent odour and image information, demonstrating conceptual coding schemes in olfaction. Our results bridge the long-standing gap between animal models and non-invasive human studies and advance our understanding of odour processing in the human brain by identifying neuronal odour-coding principles, regional functional differences and cross-modal integration.

The human olfactory bulb communicates perceived odor valence to the piriform cortex in the gamma band and receives a refined representation back in the beta band.

A core function of the olfactory system is to determine the valence of odors. In humans, central processing of odor valence perception has been shown to take form already within the olfactory bulb (OB), but the neural mechanisms by which this important information is communicated to, and from, the olfactory cortex (piriform cortex, PC) are not known. To assess communication between the 2 nodes, we simultaneously measured odor-dependent neural activity in the OB and PC from human participants while obtaining trial-by-trial valence ratings. By doing so, we could determine when subjective valence information was communicated, what kind of information was transferred, and how the information was transferred (i.e., in which frequency band). Support vector machine (SVM) learning was used on the coherence spectrum and frequency-resolved Granger causality to identify valence-dependent differences in functional and effective connectivity between the OB and PC. We found that the OB communicates subjective odor valence to the PC in the gamma band shortly after odor onset, while the PC subsequently feeds broader valence-related information back to the OB in the beta band. Decoding accuracy was better for negative than positive valence, suggesting a focus on negative valence. Critically, we replicated these findings in an independent data set using additional odors across a larger perceived valence range. Combined, these results demonstrate that the OB and PC communicate levels of subjective odor pleasantness across multiple frequencies, at specific time points, in a direction-dependent pattern in accordance with a two-stage model of odor processing.

Consistent social odor representation across 7 languages: the Social Odor Scale translation and validation.

The Social Odor Scale (SOS) is a 12-item questionnaire initially developed and validated in Italian and German to investigate self-reported awareness of social odors, which are odors emanating from the human body that convey diverse information and evoke various emotional responses. The scale includes a total score and 3 subscales representing social odors in the respective categories: romantic partner, familiar, and strangers. Here, we aimed to (i) replicate the validation of the Italian and German versions of the SOS, (ii) translate and validate the SOS into multiple additional languages (French, English, Dutch, Swedish, Chinese), and (iii) explore whether the factor structure of each translated version aligns with the original versions. Confirmatory Factor Analysis (CFA) supported the scale's structure, yielding a good fit across all languages. Notable differences in SOS mean scores were observed among the different languages: Swedish participants exhibited lower social odor awareness compared to the other groups, whereas Chinese participants reported higher social odor awareness compared to Dutch and Swedish participants. Furthermore, SOS scores correlated with respondents' geographical location, with higher (i.e. northern) latitudes linked to lower social odor awareness. These results corroborate the SOS as a valid and reliable instrument, especially for the SOS total score and the Familiar and Partner factors, emphasizing the influence of individual and geographic factors on social odor awareness.

Object-oriented olfaction: challenges for chemosensation and for chemosensory research.

Many animal species use olfaction to extract information about objects in their environment. Yet, the specific molecular signature that any given object emits varies due to various factors. Here, we detail why such variability makes chemosensory-mediated object recognition such a hard problem, and we propose that a major function of the elaborate chemosensory network is to overcome it. We describe previous work addressing different elements of the problem and outline future research directions that we consider essential for a full understanding of object-oriented olfaction. In particular, we call for extensive representation of olfactory object variability in chemical, behavioral, and electrophysiological analyses. While written with an emphasis on macrosmatic mammalian species, our arguments apply to all organisms that employ chemosensation to navigate complex environments.

Autonomic Responses Associated with Olfactory Preferences of Fragrance Consumers: Skin Conductance, Respiration, and Heart Rate.

Assessing the olfactory preferences of consumers is an important aspect of fragrance product development and marketing. With the advancement of wearable device technologies, physiological signals hold great potential for evaluating olfactory preferences. However, there is currently a lack of relevant studies and specific explanatory procedures for preference assessment methods that are based on physiological signals. In response to this gap, a synchronous data acquisition system was established using the ErgoLAB multi-channel physiology instrument and olfactory experience tester. Thirty-three participants were recruited for the olfactory preference experiments, and three types of autonomic response data (skin conductance, respiration, and heart rate) were collected. The results of both individual and overall analyses indicated that olfactory preferences can lead to changes in skin conductance (SC), respiration (RESP), and heart rate (HR). The trends of change in both RESP and HR showed significant differences (with the HR being more easily distinguishable), while the SC did not exhibit significant differences across different olfactory perception preferences. Additionally, gender differences did not result in significant variations. Therefore, HR is more suitable for evaluating olfactory perception preferences, followed by RESP, while SC shows the least effect. Moreover, a logistic regression model with a high accuracy (84.1%) in predicting olfactory perception preferences was developed using the changes in the RESP and HR features. This study has significant implications for advancing the assessment of consumer olfactory preferences.

Olfaction modulates cortical arousal independent of perceived odor intensity and pleasantness.

Throughout history, various odors have been harnessed to invigorate or relax the mind. The mechanisms underlying odors' diverse arousal effects remain poorly understood. We conducted five experiments (184 participants) to investigate this issue, using pupillometry, electroencephalography, and the attentional blink paradigm, which exemplifies the limit in attentional capacity. Results demonstrated that exposure to citral, compared to vanillin, enlarged pupil size, reduced resting-state alpha oscillations and alpha network efficiency, augmented beta-gamma oscillations, and enhanced the coordination between parietal alpha and frontal beta-gamma activities. In parallel, it attenuated the attentional blink effect. These effects were observed despite citral and vanillin being comparable in perceived odor intensity, pleasantness, and nasal pungency, and were unlikely driven by semantic biases. Our findings reveal that odors differentially alter the small-worldness of brain network architecture, and thereby brain state and arousal. Furthermore, they establish arousal as a unique dimension in olfactory space, distinct from intensity and pleasantness.

Olfactory performance and odor liking are negatively associated with food neophobia in children aged between 3 and 9 years.

BACKGROUND: Child food neophobia, i.e., rejection or avoidance of novel foods at a young age, is a prevalent nutrition problem that affects the quality of children's diet and impedes the development of healthy food preferences. Sensory sensitivity can relate to the degree of food neophobia, but previous studies rarely focused on the olfactory component of this problem in children. OBJECTIVE: We aimed to thoroughly examine the relationship between various aspects of olfactory sensitivity and food neophobia in children. METHODS: 246 children aged between three and nine years took part in a food neophobia assessment as well as in a comprehensive, psychophysical olfactory testing. RESULTS: We found that certain smell perception aspects such as lower odor liking, poorer odor identification ability as well as lower sensitivity to an unknown non-food odor all significantly predicted higher food neophobia in children. Among individual characteristics of either a child or a caregiver, only the child's age significantly and positively predicted food neophobia. The exploratory model looking into the role of family environment factors predicting self-reported food neophobia in children revealed that food neophobia was associated with lower control given to a child in this child's feeding process, as well as with a more frequent use of food as a reward in feeding. CONCLUSIONS: We suggest that suppressed olfactory perception and performance can play a unique role in child nutritional difficulties. The study inspires further considerations of olfaction-engaging interventions to counteract food-neophobia in children.

Anterior Olfactory Cortices Differentially Transform Bottom-Up Odor Signals to Produce Inverse Top-Down Outputs.

Odor information arrives first in the main olfactory bulb and is then broadcasted to the olfactory cortices and striatum. Downstream regions have unique cellular and connectivity architectures that may generate different coding patterns to the same odors. To reveal region-specific response features, tuning and decoding of single-unit populations, we recorded responses to the same odors under the same conditions across regions, namely, the main olfactory bulb (MOB), the anterior olfactory nucleus (AON), the anterior piriform cortex (aPC), and the olfactory tubercle of the ventral striatum (OT), of awake male mice. We focused on chemically closely related aldehydes that still create distinct percepts. The MOB had the highest decoding accuracy for aldehydes and was the only region encoding chemical similarity. The MOB had the highest fraction of inhibited responses and narrowly tuned odor-excited responses in terms of timing and odor selectivity. Downstream, the interconnected AON and aPC differed in their response patterns to the same stimuli. While odor-excited responses dominated the AON, the aPC had a comparably high fraction of odor-inhibited responses. Both cortices share a main output target that is the MOB. This prompted us to test if the two regions convey also different net outputs. Aldehydes activated AON terminals in the MOB as a bulk signal but inhibited those from the aPC. The differential cortical projection responses generalized to complex odors. In summary, olfactory regions reveal specialized features in their encoding with AON and aPC differing in their local computations, thereby generating inverse net centrifugal and intercortical outputs.

Human perception of Parkinson's disease body odor in comparison to the volatile organic compounds of Parkinson's disease.

INTRODUCTION: Patients with Parkinson's Disease (PD) have a distinctive body odor, which was first described by a patient's wife as musky and strong. Later analysis of sebum of patients with PD revealed four volatile organic compounds (VOC) (perillic aldehyde, hippuric acid, eicosane, octadecanal), that differed from healthy subjects, and the patient's wife confirmed that three of them smelled like patients with PD. However, it is unclear whether other people can also perceive this PD body odor and whether it can be artificially recreated. Hence, we aimed to systematically assess whether young women can perceive the PD body odor and whether they can discriminate between the PD body odor and the "artificial PD odor" composed of the four VOCs mentioned above. METHODS: T-shirts were collected from 19 people with idiopathic PD and 15 age- and gender-matched healthy participants to represent the PD body odor and the healthy body odor, respectively. The four VOCs were diluted in 1,2-propanediol to prepare the artificial PD body odor. Body odors were rated by 26 young women. RESULTS: PD body odor was perceived as more musty, strong, smelly, and unpleasant compared to healthy and artificial PD body odor. Furthermore, around 80 % of women were able to discriminate PD body odor from artificial PD body odor. CONCLUSION: Overall, this study confirmed a distinctive body odor quality of patients with PD, which can be perceived by young women. However, the four VOCs, composing the artificial PD body odor, were insufficient to reproduce the body odor from PD patients.

The relationship between social odour awareness and emotional contagion susceptibility in females.

Previous research has shown a strong link between our sense of smell and emotion. More recently, the importance we attach to olfaction has been found to relate to our susceptibility to 'catch' the emotions of others. We explore this further by examining the relation between a newly developed measure of olfaction (social odour scale, SOS), which measures awareness of social odours, and emotional contagion susceptibility in female participants. The study therefore aimed to test the strength of this relationship and also help validate the English language version of the SOS. Female (n = 148) participants completed an online study that measured odour awareness [SOS; important of odour questionnaire, IOQ] and emotional contagion (EC). We found that the English version of the SOS yielded high reliability and supported the previous factor structure of the scale; additionally, we demonstrated a strong association between the SOS and IOQ which provides criterion validity for its usage. The study also revealed that whilst both the SOS and IOQ were positively associated with EC, the SOS was the more accurate predictor. These findings provide further validation for the use of the SOS and suggest that our subjective awareness of olfaction, especially concerning 'social odours' is an accurate predictor of emotional contagion.

Altered functional connectivity of primary olfactory cortex-hippocampus-frontal cortex in subjective cognitive decline during odor stimulation.

Subjective cognitive decline (SCD) is a high-risk population in the preclinical stage of Alzheimer's disease (AD), and olfactory dysfunction is a risk factor for dementia progression. The present study aimed to explore the patterns of functional connectivity (FC) changes in the olfactory neural circuits during olfactory stimulation in SCD subjects. A total of 56 SCD subjects and 56 normal controls (NCs) were included. All subjects were assessed with a cognitive scale, an olfactory behavior test, and olfactory task-based functional magnetic resonance imaging scanning. The FC differences in olfactory neural circuits between the two groups were analyzed by the generalized psychophysiological interaction. Additionally, we calculated and compared the activation of brain regions within the olfactory neural circuits during odor stimulation, the volumetric differences in brain regions showing FC differences between groups, and the correlations between neuroimaging indicators and olfactory behavioral and cognitive scale scores. During odor stimulation, the FC between the bilateral primary olfactory cortex (bPOC) and the right hippocampus in the SCD group was significantly reduced; while the FC between the right hippocampus and the right frontal cortex was significantly increased in the SCD group. The bPOC of all subjects showed significant activation, but no significant difference in activation between groups was found. No significant differences were observed in the volume of the brain regions within the olfactory neural circuits or in olfactory behavior between groups. The volume of the bPOC and right frontal cortex was significantly positively correlated with olfactory identification, and the volume of the right frontal cortex and right hippocampus was significantly correlated with cognitive functions. Furthermore, a significant correlation between the activation of bPOC and the olfactory threshold was found in the whole cohort. These results suggested that while the structure of the olfactory neural circuits and olfactory behavior in SCD subjects remained stable, there were significant changes observed in the FC of the olfactory neural circuits (specifically, the POC-hippocampus-frontal cortex neural circuits) during odor stimulation. These findings highlight the potential of FC alterations as sensitive imaging markers for identifying high-risk individuals in the early stage of AD.

Effects of Emotional Olfactory Stimuli on Modulating Angry Driving Based on an EEG Connectivity Study.

Effectively regulating anger driving has become critical in ensuring road safety. The existing research lacks a feasible exploration of anger-driving regulation. This paper delves into the effect and neural mechanisms of emotional olfactory stimuli (EOS) on regulating anger driving based on EEG. First, this study designed an angry driving regulation experiment based on EOS to record EEG signals. Second, brain activation patterns under various EOS conditions are explored by analyzing functional brain networks (FBNs). Additionally, the paper analyzes dynamic alterations in anger-related characteristics to explore the intensity and persistence of regulating anger driving under different EOS. Finally, the paper studies the frequency energy of EEG changes under EOS through time-frequency analysis. The results indicate that EOS can effectively regulate a driver's anger emotions, especially with the banana odor showing superior effects. Under banana odor stimulus, synchronization between the parietal and temporal lobes significantly decreased. Notably, the regulatory effect of banana odor is optimal and exhibits sustained efficacy. The regulatory effect of banana odor on anger emotions is persistent. Furthermore, the impact of banana odor significantly reduces the distribution of high-energy activation states in the parietal lobe region. Our findings provide new insights into the dynamic characterization of functional connectivity during anger-driving regulation and demonstrate the potential of using EOS as a reliable tool for regulating angry driving.

The Context Matters: Women's Experiences of Their Partner's Odor in Intimate and Sexual Encounters.

Research shows that male body odor plays an important role in women's mate choice and that olfactory abilities are associated with women's sexual functioning. What remains unclear is what types of partner's odor actually shape women's experience during intimate activities. This study therefore explored women's experience associated with the partner's various odors and investigated how they affect women's intimate and sexual encounters. We performed semi-structured individual interviews with 20 single women and 20 women in a long-term relationship. Thematic analysis revealed four key natural odor types of the partner: body odor, sweat, genital odor, and semen odor. Further, we have identified three main types of fragrance odor (cologne, shower gel, and laundry agents) and investigated their perception in both intimate (hugging, kissing, cuddling, lying side by side) and sexual (intercourse, oral sex, ejaculation) contexts. Both partner's natural odor and fragrance affected women's emotional state (ranging from pleasant to unpleasant) and behavioral response (ranging from approach to avoidance of partner). Women's odor perception was frequently context-dependent, so that even mostly negatively perceived odors (e.g., semen, genital odor) were often accepted as part of sexual encounter. Finally, women's perception was negatively modified by partner's specific sweat (after workday, workout, or when the partner is ill) during intimate encounters. Our results highlight the complexity and interindividual variability of partner's odor perception.

Emotion perception through the nose: how olfactory emotional cues modulate the perception of neutral facial expressions in affective disorders.

Humans can decode emotional states from the body odors of the conspecifics and this type of emotional communication is particularly relevant in conditions in which social interactions are impaired, as in depression and social anxiety. The present study aimed to explore how body odors collected in happiness and fearful conditions modulate the subjective ratings, the psychophysiological response and the neural processing of neutral faces in individuals with depressive symptoms, social anxiety symptoms, and healthy controls (N = 22 per group). To this aim, electrocardiogram (ECG) and HD-EEG were recorded continuously. Heart Rate Variability (HRV) was extracted from the ECG as a measure of vagal tone, event-related potentials (ERPs) and event-related spectral perturbations (ERPSs) were extracted from the EEG. The results revealed that the HRV increased during the fear and happiness body odors conditions compared to clean air, but no group differences emerged. For ERPs data, repeated measure ANOVA did not show any significant effects. However, the ERPSs analyses revealed a late increase in delta power and a reduced beta power both at an early and a late stage of stimulus processing in response to the neutral faces presented with the emotional body odors, regardless of the presence of depressive or social anxiety symptoms. The current research offers new insights, demonstrating that emotional chemosignals serve as potent environmental cues. This represents a substantial advancement in comprehending the impact of emotional chemosignals in both individuals with and without affective disorders.

Tropospheric ozone effect on olfactory perception and olfactory bulb dopaminergic interneuron excitability.

Ozone (O3) forms in the Earth's atmosphere, both naturally and by reactions of man-made air pollutants. Deleterious effects of O3 have been found in the respiratory system. Here, we examine whether O3 alters olfactory behavior and cellular properties in the olfactory system. For this purpose, mice were exposed to O3 at a concentration found in highly polluted city air [0.8 ppm], and the behavior elicited by social and non-social odors in habituation/dishabituation tests was assessed. In addition, the electrical responses of dopaminergic olfactory bulb (OB) neurons were also evaluated. O3 differentially compromises olfactory perception to odors: it reduces responses to social and non-social odors in Swiss Webster mice, while this effect was observed in C57BL/6 J mice only for some non-social odors. Additionally, O3 reduced the rate of spontaneous spike firing in periglomerular dopaminergic cells (PG-DA) of the OB. Because this effect could reflect changes in excitability and/or synaptic inputs, the ability of O3 to alter PG-DA spontaneous activity was also tested together with cell membrane resistance, membrane potential, rheobase and chronaxie. Taken together, our data suggest the ability of O3 to affect olfactory perception.

Competitive (but not cooperative) body odors bias the discrimination of action intentions towards cooperation.

Odors help us to interpret the environment, including the nature of social interactions. But, whether and how they influence the ability to discriminate the intentional states embedded in actions is unclear. In two experiments, we asked two independent groups of participants to discriminate motor intentions from videos showing one agent performing a reach-to-grasp movement with another agent with a cooperative or a competitive intent, and the same movement performed alone at either natural- or fast-speed, as controls. Task-irrelevant odor primes preceded each video presentation. Experiment 1 (N = 19) included masked cooperative and competitive body odors (human sweat collected while the donors were engaged in cooperative and competitive activities), whereas Experiment 2 (N = 20) included a common odor (cedarwood oil) and no odor (clean air) as primes. In an odor-primed, two-alternative forced choice task, participants discriminated the intention underlying the observed action. The results indicated that the odor exposure modulated the discrimination speed across different intentions, but only when the action intentions were hard to discriminate (cooperative vs. individual natural-speed, and competitive vs. individual fast-speed). Contrary to our hypothesis, a direct odor-action intention compatibility effect was not found. Instead, we propose a negative arousal compatibility-like effect to explain our results. Discrimination of high arousing action intentions (i.e., competitive) took longer when primed by high arousing odors (common odor and competitive body odor) than by low arousing odors (cooperative body odor and no odor). Discrimination of low arousing action intentions (i.e., cooperative) took longer when primed by low arousing odors than by high arousing odors. All in all, competitive (but not cooperative) body odors bias the discrimination of action intentions towards cooperation.