Behavioral separation of liking and wanting in response to olfactory and visual food cues.

In real-world settings, food rewards are processed in parallel across several sensory modalities, but paradigms that compare contributions of different modalities are lacking. While odor perception in particular is frequently implicated in appetite regulation, the mechanisms by which food odors differentially evoke experiences of wanting and liking remain poorly understood. This study addressed this gap by dissociating liking from wanting responses for olfactory stimuli, and establishing commonalities and differences relative to the visual modality. In two separate experiments, participants (n1 = 37, n2 = 43) rated content-matched batteries of odors and pictures, respectively, for their ability to elicit pleasure (liking) and desire to eat (wanting). A third experiment (n3 = 39) utilized a combined olfactory-visual paradigm to test the separation of these dimensions in a multisensory context. Our results show that participants differentiated clearly and reliably between liking and wanting for both odors and pictures, as demonstrated by a high difference score between the two in non-food (high liking, low wanting), but not in food (both high) or disgusting stimuli (both low), and high within-session retest reliability. Higher variability for olfactory relative to visual assessments was observed and likely reflects well-established difficulties with odor object identification. Taken together, our study demonstrates that olfactory stimuli can be used in experimental settings to evoke separable experiences of liking and wanting for food and non-food stimuli. Manipulating these components independently across sensory modalities in experimental studies could generate novel insights into how olfactory and visual cues differentially contribute to anticipatory and consummatory food reward processing, in healthy and disordered eating.

Odor-Taste Interactions in Food Perception: Exposure Protocol Shows No Effects of Associative Learning.

Repeated exposure can change the perceptual and hedonic features of flavor. Associative learning during which a flavor's odor component is affected by co-exposure with taste is thought to be central in this process. However, changes can also arise due to exposure to the odor in itself. The aim of this study was to dissociate effects of associative learning from effects of exposure without taste by repeatedly presenting one odor together with sucrose and a second odor alone. Sixty individuals attended two testing sessions separated by a 5-day Exposure Phase during which the stimuli were presented as flavorants in chewing gums that were chewed three times daily. Ratings of odor sweetness, odor pleasantness, odor intensity enhancement by taste, and odor referral to the mouth were collected at both sessions. Consistent with the notion that food preferences are modulated by exposure, odor pleasantness increased between the sessions independently of whether the odor (basil or orange flower) had been presented with or without sucrose. However, we found no evidence of associative learning in any of the tasks. In addition, exploratory equivalence tests suggested that these effects were either absent or insignificant in magnitude. Taken together, our results suggest that the hypothesized effects of associative learning are either smaller than previously thought or highly dependent on the experimental setting. Future studies are needed to evaluate the relative support for these explanations and, if experimental conditions can be identified that reliably produce such effects, to identify factors that regulate the formation of new odor-taste associations.

Temporolimbic cortical volume is associated with semantic odor memory performance in aging.

Olfactory function, and specifically semantic olfactory memory (i.e., odor identification), has frequently been shown to predict cognitive functioning across multiple domains in old age. This observation suggests that olfactory function can serve as a marker for the integrity of temporolimbic cortical networks, but a clear delineation of this association is still missing. To address this issue, the present study employed voxel-based morphometry in a region of interest-based design to determine the extent to which gray matter volumes of core olfactory and memory areas are associated with olfactory memory performance in an aging population free from neurodegenerative disease. We further aimed to determine potential overlap in structural anatomical correlates, and differences in association strength, for semantic and episodic olfactory memory. Structural magnetic resonance imaging (MRI), episodic and semantic odor memory and episodic and semantic verbal memory data were collected in 422 participants from the Swedish National Study on Aging and Care in Kungsholmen (SNAC-K), all aged â€‹≥ â€‹60 years. Controlling for age and education, semantic, but not episodic, olfactory memory was positively related to gray matter volume in a cluster extending from the anterior hippocampus and amygdala into the posterior piriform cortex. The observed associations remained even when verbal memory performance was controlled for, supporting a link between the olfactory memory domain and cortical volume over and above more generalized memory abilities. As such, our data provide evidence for distinct functional-structural associations for semantic odor memory, supporting the idea of temporolimbic integrity as a neurobiological substrate linking olfactory function to cognitive health in old age.

Prefrontal Control Over Occipital Responses to Crossmodal Overlap Varies Across the Congruency Spectrum.

While matched crossmodal information is known to facilitate object recognition, it is unclear how our perceptual systems encode the more gradual congruency variations that occur in our natural environment. Combining visual objects with odor mixtures to create a gradual increase in semantic object overlap, we demonstrate high behavioral acuity to linear variations of olfactory-visual overlap in a healthy adult population. This effect was paralleled by a linear increase in cortical activation at the intersection of occipital fusiform and lingual gyri, indicating linear encoding of crossmodal semantic overlap in visual object recognition networks. Effective connectivity analyses revealed that this integration of olfactory and visual information was achieved by direct information exchange between olfactory and visual areas. In addition, a parallel pathway through the superior frontal gyrus was increasingly recruited towards the most ambiguous stimuli. These findings demonstrate that cortical structures involved in object formation are inherently crossmodal and encode sensory overlap in a linear manner. The results further demonstrate that prefrontal control of these processes is likely required for ambiguous stimulus combinations, a fact of high ecological relevance that may be inappropriately captured by common task designs juxtaposing congruency and incongruency.

The intraparietal sulcus governs multisensory integration of audiovisual information based on task difficulty.

Object recognition benefits maximally from multimodal sensory input when stimulus presentation is noisy, or degraded. Whether this advantage can be attributed specifically to the extent of overlap in object-related information, or rather, to object-unspecific enhancement due to the mere presence of additional sensory stimulation, remains unclear. Further, the cortical processing differences driving increased multisensory integration (MSI) for degraded compared with clear information remain poorly understood. Here, two consecutive studies first compared behavioral benefits of audio-visual overlap of object-related information, relative to conditions where one channel carried information and the other carried noise. A hierarchical drift diffusion model indicated performance enhancement when auditory and visual object-related information was simultaneously present for degraded stimuli. A subsequent fMRI study revealed visual dominance on a behavioral and neural level for clear stimuli, while degraded stimulus processing was mainly characterized by activation of a frontoparietal multisensory network, including IPS. Connectivity analyses indicated that integration of degraded object-related information relied on IPS input, whereas clear stimuli were integrated through direct information exchange between visual and auditory sensory cortices. These results indicate that the inverse effectiveness observed for identification of degraded relative to clear objects in behavior and brain activation might be facilitated by selective recruitment of an executive cortical network which uses IPS as a relay mediating crossmodal sensory information exchange.

Multisensory flavor perception: The relationship between congruency, pleasantness, and odor referral to the mouth.

Our hedonic response to a food is determined by its flavor, an inherently multisensory experience that extends beyond the mere addition of its odor and taste. While congruency is known to be important for multisensory processes in general, little is known about its specific role in flavor processing. The aim of the present study was to delineate the effects of odor-taste congruency on two central aspects of flavor: odor referral (or mislocalization) to the mouth, and pleasantness. We further aimed to test whether an eventual effect on pleasantness was mediated by odor referral. Aqueous solutions containing odors and tastes were prepared to create food-like stimuli with varying degrees of congruency, ranging from maximally incongruent to maximally congruent in nine steps. Thirty participants reported where they perceived the odors, and how much they liked the solutions. Congruency had a positive linear effect both on odor referral to the oral cavity and on pleasantness. However, the effect of congruency on pleasantness was not mediated by odor referral. These results indicate that as an odor-taste mixture approximates a mental representation of a familiar food, its components are increasingly merged into one perceptual object sensed in the mouth. In parallel, the mixture is evaluated as increasingly pleasant, which promotes consumption of familiar foods that have been determined through experience to be non-toxic. While the modulatory role of congruency on pleasantness and odor referral was confirmed, our results also indicate that these effects arise through distinct perceptual mechanisms.

Phantom Smells: Prevalence and Correlates in a Population-Based Sample of Older Adults.

Loss of olfactory function is common in old age, but evidence regarding qualitative olfactory dysfunction in the general older population is scarce. The current study investigates the prevalence and correlates of phantom smell experiences (phantosmia) in a population-based study (Swedish National Study on Aging and Care in Kungsholmen [SNAC-K]) of Swedish adults (n = 2569) aged between 60 and 90 years. Phantosmia was assessed through a standardized interview and defined as reporting having experienced an odor percept in the absence of any stimuli in the surrounding environment that could emit the odor. The relationships between phantosmia and demographic, genetic, health-related, and behavioral variables were analyzed with hierarchical logistic regression analyses. The overall prevalence of phantom smells was 4.9%, and was associated with female gender, carrying the met allele of the BDNF gene, higher vascular risk burden, and reporting distorted smell sensations (parosmia). Olfactory dysfunction was, however, not related to phantosmia. The most frequently reported phantom smell was smoky/burnt. A novel finding was that some individuals reported phantom smells with an autobiographical connotation. The results from this study indicate that the prevalence of phantosmia in the general older population is not negligible and that some factors that are beneficial for preserved olfactory function, such as female gender and the BDNF met allele, are also associated with the occurrence of phantom smells.

Superadditive opercular activation to food flavor is mediated by enhanced temporal and limbic coupling.

Food perception is characterized by a transition from initially separate sensations of the olfactory and gustatory properties of the object toward their combined sensory experience during consumption. The holistic flavor experience, which occurs as the smell and taste merge, extends beyond the mere addition of the two chemosensory modalities, being usually perceived as more object-like, intense and rewarding. To explore the cortical mechanisms which give rise to olfactory-gustatory binding during natural food consumption, brain activation during consumption of a pleasant familiar beverage was contrasted with presentation of its taste and orthonasal smell alone. Convergent activation to all presentation modes was observed in executive and chemosensory association areas. Flavor, but not orthonasal smell or taste alone, stimulated the frontal operculum, supporting previous accounts of its central role in the formation of the flavor percept. A functional dissociation was observed in the insula: the anterior portion was characterized by sensory convergence, while mid-dorsal sections activated exclusively to the combined flavor stimulus. psycho-physiological interaction analyses demonstrated increased neural coupling between the frontal operculum and the anterior insula during flavor presentation. Connectivity was also increased with the lateral entorhinal cortex, a relay to memory networks and central node for contextual modulation of olfactory processing. These findings suggest a central role of the insular cortex in the transition from mere detection of chemosensory convergence to a superadditive flavor representation. The increased connections between the frontal operculum and medial temporal memory structures during combined olfactory-gustatory stimulation point to a potential mechanism underlying the acquisition and modification of flavor preferences.

Neural responses to dynamic multimodal stimuli and pathology-specific impairments of social cognition in schizophrenia and depression.

BACKGROUND: Individuals with schizophrenia and people with depression both show abnormal behavioural and neural responses when perceiving and responding to emotional stimuli, but pathology-specific differences and commonalities remain mostly unclear. AIMS: To directly compare empathic responses to dynamic multimodal emotional stimuli in a group with schizophrenia and a group with depression, and to investigate their neural correlates using functional magnetic resonance imaging (fMRI). METHOD: The schizophrenia group (n = 20), the depression group (n = 24) and a control group (n = 24) were presented with portrait-shot video clips expressing emotion through three possible communication channels: facial expression, prosody and content. Participants rated their own and the actor's emotional state as an index of empathy. RESULTS: Although no group differences were found in empathy ratings, characteristic differences emerged in the fMRI activation patterns. The schizophrenia group demonstrated aberrant activation patterns during the neutral speech content condition in regions implicated in multimodal integration and formation of semantic constructs. Those in the depression group were most affected during conditions with trimodal emotional and trimodal neutral stimuli, in key regions of the mentalising network. CONCLUSIONS: Our findings reveal characteristic differences in patients with schizophrenia compared with those with depression in their cortical responses to dynamic affective stimuli. These differences indicate that impairments in responding to emotional stimuli may be caused by pathology-specific problems in social cognition.

Orbitofrontal cortex and olfactory bulb volume predict distinct aspects of olfactory performance in healthy subjects.

While recent studies suggest an important role of higher order olfactory brain areas for basic olfactory performance, the extent to which cortical and peripheral neural markers account for separate portions of the variability in olfactory perceptual acuity is still unclear. We addressed this question by correlating voxel-based morphometry data from 90 healthy adults with olfactory performance measures. Supplementing this approach with region of interest (ROI) analyses of functionally defined olfactory cortical regions and olfactory bulb volume, we sought to disentangle the relative contribution of central and peripheral areas to behavioral variability. Whole-brain analyses revealed a significant positive correlation of gray matter volume and olfactory function scores in the right orbital sulcus. This effect was confirmed by the ROI analyses, which further indicated a significant association of the olfactory score with olfactory bulb volume. Moreover, a functional dissociation was observed, with central and peripheral mechanisms explaining different aspects of the observed behavioral variance in the olfactory subscores. In line with previous clinical studies, these data thus suggest an important role of regional gray matter volume in the right orbitofrontal cortex and olfactory bulb volume for olfactory performance in healthy individuals.

Statistical localization of human olfactory cortex.

Functional neuroimaging methods have been used extensively during the last decades to explore the neural substrates of olfactory processing. While a general consensus on the functional anatomy of olfactory cortex is beginning to emerge, the mechanisms behind the functions of individual processing nodes still remain debated. Further, it remains unclear to which extent divergent findings result from differences in methodological approaches. Using Activation Likelihood Estimation (ALE), the aim of the present study was to statistically combine all published data on functional neuroimaging of olfaction to provide a probability map reflecting the state of the field to date. Additionally, we grouped studies according to various methodological approaches to investigate whether these systematically affected the reported findings. A total of 45 studies (69 contrasts, 594 foci) met our inclusion criteria. Significant ALE peaks for odor against baseline were observed in areas commonly labeled as primary and secondary olfactory cortex, such as the piriform and orbitofrontal cortex, amygdala, anterior insula, and ventral putamen. In addition, differences were observed in the extent to which different methods were able to induce activation in these different nodes of the olfactory network.

Opposing amygdala and ventral striatum connectivity during emotion identification.

Lesion and electrophysiological studies in animals provide evidence of opposing functions for subcortical nuclei such as the amygdala and ventral striatum, but the implications of these findings for emotion identification in humans remain poorly described. Here we report a high-resolution fMRI study in a sample of 39 healthy subjects who performed a well-characterized emotion identification task. As expected, the amygdala responded to THREAT (angry or fearful) faces more than NON-THREAT (sad or happy) faces. A functional connectivity analysis of the time series from an anatomically defined amygdala seed revealed a strong anticorrelation between the amygdala and the ventral striatum/ventral pallidum, consistent with an opposing role for these regions in during emotion identification. A second functional connectivity analysis (psychophysiological interaction) investigating relative connectivity on THREAT vs. NON-THREAT trials demonstrated that the amygdala had increased connectivity with the orbitofrontal cortex during THREAT trials, whereas the ventral striatum demonstrated increased connectivity with the posterior hippocampus on NON-THREAT trials. These results indicate that activity in the amygdala and ventral striatum may be inversely related, and that both regions may provide opposing affective bias signals during emotion identification.

Trimodal processing of complex stimuli in inferior parietal cortex is modality-independent.

In humans, multisensory mechanisms facilitate object processing through integration of sensory signals that match in their temporal and spatial occurrence as well as their meaning. The generalizability of such integration processes across different sensory modalities is, however, to date not well understood. As such, it remains unknown whether there are cerebral areas that process object-related signals independently of the specific senses from which they arise, and whether these areas show different response profiles depending on the number of sensory channels that carry information. To address these questions, we presented participants with dynamic stimuli that simultaneously emitted object-related sensory information via one, two, or three channels (sight, sound, smell) in the MR scanner. By comparing neural activation patterns between various integration processes differing in type and number of stimulated senses, we showed that the left inferior frontal gyrus and areas within the left inferior parietal cortex were engaged independently of the number and type of sensory input streams. Activation in these areas was enhanced during bimodal stimulation, compared to the sum of unimodal activations, and increased even further during trimodal stimulation. Taken together, our findings demonstrate that activation of the inferior parietal cortex during processing and integration of meaningful multisensory stimuli is both modality-independent and modulated by the number of available sensory modalities. This suggests that the processing demand placed on the parietal cortex increases with the number of sensory input streams carrying meaningful information, likely due to the increasing complexity of such stimuli.

Processing of disgusted faces is facilitated by odor primes: a functional MRI study.

Facilitation of emotional face recognition is an established phenomenon for audiovisual crossmodal stimulation, but not for other sensory modalities. The present study used a crossmodal priming task to identify brain systems controlling olfactory-visual interactions during emotion processing. BOLD fMRI was acquired for 44 healthy subjects during an emotional face discrimination task preceded by an emotionally valenced odorant. Behavioral performance showed that recognition of disgusted faces was improved by the presentation of an olfactory stimulus irrespective of its emotional valence. No such facilitation was seen for other facial expressions. The neuroimaging data showed a selective default network responsivity to emotional faces which was modulated by odor condition. Among disgust faces, hypoactivations during trials preceded by odorants indicated the presence of priming effects. Consistent with studies investigating the brain systems associated with audiovisual emotional integration, activity modulations in clusters in fusiform gyrus, middle frontal and middle cingulate gyrus corresponded to the observed behavioral facilitation. Our study further shows modulation of signal in the anterior insula during trials combining negatively valenced odor and disgusted faces, suggesting a modality-specific mechanism for integration of the disgust response and olfaction. These results indicate the presence of a central network with modality-specific and -unspecific components modulating emotional face recognition.

Multisensory integration of emotionally valenced olfactory-visual information in patients with schizophrenia and healthy controls.

BACKGROUND: Patients with schizophrenia frequently have deficits in social cognition, and difficulties in the discrimination of emotional facial expressions have been discussed as an important contributing factor. We investigated whether this impairment is aggravated by difficulties relating the observed facial expression to contextual information, as is often provided by emotionally valenced crossmodal stimulation. METHODS: We investigated the effects of odorant primes on the accuracy and speed of emotional face recognition. Healthy controls and patients with schizophrenia were exposed to 2-second odorant stimuli: vanillin (pleasant), ambient air (neutral) and hydrogen sulfide (unpleasant). The odours were followed by an emotional face recognition task, in which participants determined if a face showed happiness, disgust or neutral affect. RESULTS: Controls showed improved performance in the categorization of disgusted faces after all types of odour stimulation irrespective of the emotional valence. However, in controls, the response time for happy faces was slower after presentation of any odour. Schizophrenia patients showed an attenuated effect of olfactory priming on disgust recognition, which resulted in the increased performance differences between the groups. This effect was particularly strong for the unpleasant odour. LIMITATIONS: The study design did not allow us to fully differentiate between the effects of perceived odour intensity and valence. A possible contribution of cognitive deficits on the observed effects should be investigated in future studies. CONCLUSION: Our results provide novel evidence for a special connection between the presentation of odorant cues and the accuracy of recognition of disgusted faces in healthy controls. This recognition advantage is disturbed in patients with schizophrenia and appears to contribute to the observed deficit in emotional face recognition.

A Prospective Study on Risk Factors for Olfactory Dysfunction in Aging.

BACKGROUND: Olfactory dysfunction (OD) refers to a reduced or absent ability to smell. OD negatively impacts health and quality of life and its prevalence increases with advancing age. Since OD may be an early marker of dementia and impending death, more knowledge regarding risk factors of OD in aging is warranted. The objective was therefore to explore longitudinally which demographic, genetic, clinical, lifestyle, and cognitive factors predict the development of OD. METHODS: The study included participants aged 60-90 years from the Swedish National Study on Aging and Care in Kungsholmen (SNAC-K), who did not have OD at baseline and were reassessed with an odor identification task at a 6-year follow-up (n = 1,004). Risk factors of OD were assessed with multivariable logistic regression analyses. RESULTS: The percentage of incident OD cases was 14.2% over 6 years in the total sample and this number increased monotonically with age. Increasing age, carrying the ε4 allele of the APOE gene, atrial fibrillation, cerebrovascular disease, and current smoking were found to be risk factors for the development of OD, whereas better olfactory identification and verbal episodic memory proficiency at baseline were identified as protective factors. CONCLUSIONS: In addition to nonmodifiable factors (age and genetic risk), several modifiable risk factors of OD were identified. This suggests that it might be possible to reduce OD incidence through the management of vascular risk factors and maintenance of a healthy lifestyle.

Mood induction with olfactory stimuli reveals differential affective responses in males and females.

Olfactory perception is characterized by interpersonal variability. Although gender has been identified as a potential influencing factor, currently little is known about its effect on perceived hedonicity of individual odorants. This study assessed gender differences in emotional appraisal of 3 odorants (eugenol, vanillin, and hydrogen sulfide [H(2)S]), presented to 25 healthy subjects (13 males, 12 females) in a blocked design. Standardized scales rating valence and judgments of emotional experience were used for stimulus evaluation. Results indicate ambiguous pleasantness ratings for eugenol as well as stronger responses to vanillin odorant in female subjects; furthermore, in emotional experience ratings, the effect of eugenol was found to be gender dependent, evoking more positive and less negative emotions in female subjects than in males. The gender dependence of the mood response to eugenol necessitates reconsideration of this odorant as a reliable gender independent olfactory stimulus for studies on olfaction and emotion.

Multisensory Enhancement of Odor Object Processing in Primary Olfactory Cortex.

Identification of an object based on its odor alone is inherently difficult, but becomes easier when other senses provide supporting cues. This suggests that crossmodal sensory input facilitates neural processing of olfactory object information; however, direct evidence is still lacking. Here, we tested the effect of multisensory stimulation on information processing in the human posterior piriform cortex (PPC), a region linked to olfactory object encoding. Participants were exposed to familiar objects in the form of uni-, bi-, and trimodal combinations of odors, videos, and sounds. We hypothesized that the PPC would respond to non-olfactory object information, and that activity would increase linearly with the number of senses providing relevant object information. As predicted, visual object information activated the PPC and activity increased linearly with the number of relevant sensory channels. The crossmodal response pattern thus indicates that the PPC does not exclusively respond to olfactory information, but also to crossmodal object information important for olfactory processing. The continuous activity increase suggests that the PPC further acts as a multisensory binding site where pertinent input from multiple senses results in an increased neural response to the odor object. This potentially represents a neural mechanism for the well-known behavioral improvement present in odor object recognition during concurrent crossmodal sensory stimulation.

Impaired olfaction is associated with cognitive decline and neurodegeneration in the brain.

OBJECTIVE: We aimed to examine whether impaired olfaction is associated with cognitive decline and indicators of neurodegeneration in the brain of dementia-free older adults. METHODS: Within the Rush Memory and Aging Project, 380 dementia-free participants (mean age = 78 years) were followed for up to 15 years, and underwent MRI scans. Olfactory function was assessed using the Brief Smell Identification Test (B-SIT) at baseline, and categorized as anosmia (B-SIT <6), hyposmia (B-SIT 6-10 in men and 6-10.25 in women), and normal (B-SIT 10.25-12 in men and 10.5-12 in women). Cognitive function was annually assessed with a battery of 21 tests, from which composite scores were derived. Structural total and regional brain volumes were estimated. Data were analyzed using linear regression and mixed-effects models. RESULTS: At study entry, 138 (36.3%) had normal olfactory function, 213 (56.1%) had hyposmia, and 29 (7.6%) had anosmia. In multiadjusted mixed-effects models, hyposmia (ß = -0.03, 95% confidence interval [CI] -0.05 to -0.02) and anosmia (ß = -0.13, 95% CI -0.16 to -0.09) were associated with faster rate of cognitive decline compared to normal olfaction. On MRI, impaired olfaction (hyposmia or anosmia) was related to smaller volumes of the hippocampus (ß = -0.19, 95% CI -0.33 to -0.05), and in the entorhinal (ß = -0.16, 95% CI -0.24 to -0.08), fusiform (ß = -0.45, 95% CI -0.78 to -0.14), and middle temporal (ß = -0.38, 95% CI -0.72 to -0.01) cortices. CONCLUSION: Impaired olfaction predicts faster cognitive decline and might indicate neurodegeneration in the brain among dementia-free older adults.