Sanne Boesveldt

Identification of human gustatory cortex by activation likelihood estimation

Over the last two decades, neuroimaging methods have identified a variety of taste‐responsive brain regions. Their precise location, however, remains in dispute. For example, taste stimulation activates areas throughout the insula and overlying operculum, but identification of subregions has been inconsistent. Furthermore, literature reviews and summaries of gustatory brain activations tend to reiterate rather than resolve this ambiguity. Here, we used a new meta‐analytic method [activation likelihood estimation (ALE)] to obtain a probability map of the location of gustatory brain activation across 15 studies. The map of activation likelihood values can also serve as a source of independent coordinates for future region‐of‐interest analyses. We observed significant cortical activation probabilities in: bilateral anterior insula and overlying frontal operculum, bilateral mid dorsal insula and overlying Rolandic operculum, and bilateral posterior insula/parietal operculum/postcentral gyrus, left lateral orbitofrontal cortex (OFC), right medial OFC, pregenual anterior cingulate cortex (prACC) and right mediodorsal thalamus. This analysis confirms the involvement of multiple cortical areas within insula and overlying operculum in gustatory processing and provides a functional “taste map” which can be used as an inclusive mask in the data analyses of future studies. In light of this new analysis, we discuss human central processing of gustatory stimuli and identify topics where increased research effort is warranted. Hum Brain Mapp, 2011.

Gustatory and olfactory dysfunction in older adults: a national probability study

BACKGROUND Olfactory and gustatory functions have not been well characterized in older adults in the US. Consequently, their relationships to sociodemographic characteristics, as well as physical and mental health, were studied in a large national probability sample using brief validated tests of chemosensory function. METHODS A five-odour identification test and taste-impregnated strips of filter paper (sweet, sour, bitter, and salty) assessed the ability to identify chemosensory stimuli. RESULTS Severe gustatory dysfunction was more prevalent than severe olfactory dysfunction. Age, education and sex were independently associated with performance on both the olfactory and gustatory identification tasks. Higher scores were associated with female sex, higher level of education, and lower age. Odour identification scores exhibited a positive, albeit weak, correlation with BMI, and food-related odours were better identified than non-food odours. In addition, odour identification performance was also negatively associated with depressive symptoms. CONCLUSIONS These data demonstrate a high prevalence of severe gustatory and, to a somewhat lesser extent, olfactory dysfunction in a population-based sample and demonstrate that even brief tests are capable of detecting correlations between both chemical senses and relevant health measures outside a clinical setting.

Signal-to-noise ratio of chemosensory event-related potentials

OBJECTIVE We investigated the influence of the number of stimuli on signal-to-noise (S/N) ratio of CSERP. METHODS CSERP from 20 normosmic subjects were obtained in response to stimulation with two olfactory (H(2)S and PEA) and a trigeminal (CO(2)) stimulant. For each of these odors, 160 stimuli were delivered into the right nostril (duration 200ms, mean ISI 30s) using a constant-flow, air-dilution olfactometer. For each EEG recording site (Fz, Cz, Pz, C3, C4), peak-to-peak amplitude N1P2 and noise amplitude levels were determined. Subsequently, S/N ratios were calculated. RESULTS The S/N ratios for olfactory ERP generally improved for H(2)S and PEA. For responses to PEA, S/N ratios increased significantly up to 80 averages (S/N ratio=5.6). The number of stimuli for an optimal S/N ratio for trigeminal ERP was slightly lower, i.e. 60 averages (S/N ratio=7.9). CONCLUSIONS S/N N1P2 ratios in olfactory and trigeminal ERP significantly improve with an increasing number of responses averaged under these experimental conditions. This is mainly due to a reduction of noise level. Applying more stimuli has little additional effect on S/N ratio due to a concomitant decrease in signal amplitude. SIGNIFICANCE An optimal S/N ratio is essential when recording CSERP in neurodegenerative disorders, where responses may be of low amplitude, and for medico-legal purposes.

Human protein status modulates brain reward responses to food cues

BACKGROUND Protein is indispensable in the human diet, and its intake appears tightly regulated. The role of sensory attributes of foods in protein intake regulation is far from clear. OBJECTIVE We investigated the effect of human protein status on neural responses to different food cues with the use of functional magnetic resonance imaging (fMRI). The food cues varied by taste category (sweet compared with savory) and protein content (low compared with high). In addition, food preferences and intakes were measured. DESIGN We used a randomized crossover design whereby 23 healthy women [mean ± SD age: 22 ± 2 y; mean ± SD body mass index (in kg/m(2)): 22.5 ± 1.8] followed two 16-d fully controlled dietary interventions involving consumption of either a low-protein diet (0.6 g protein · kg body weight(-1) · d(-1), ~7% of energy derived from protein, approximately half the normal protein intake) or a high-protein diet (2.2 g protein · kg body weight(-1) · d(-1), ~25% of energy, approximately twice the normal intake). On the last day of the interventions, blood oxygen level-dependent (BOLD) responses to odor and visual food cues were measured by using fMRI. The 2 interventions were followed by a 1-d ad libitum phase, during which a large array of food items was available and preference and intake were measured. RESULTS When exposed to food cues (relative to the control condition), the BOLD response was higher in reward-related areas (orbitofrontal cortex, striatum) in a low-protein state than in a high-protein state. Specifically, BOLD was higher in the inferior orbitofrontal cortex in response to savory food cues. In contrast, the protein content of the food cues did not modulate the BOLD response. A low protein state also increased preferences for savory food cues and increased protein intake in the ad libitum phase as compared with a high-protein state. CONCLUSIONS Protein status modulates brain responses in reward regions to savory food cues. These novel findings suggest that dietary protein status affects taste category preferences, which could play an important role in the regulation of protein intake in humans. This trial was registered at www.trialregister.nl/trialreg/admin/rctview.asp?TC=3288 as NTR3288.

Dynamics of autonomic nervous system responses and facial expressions to odors

Why we like or dislike certain products may be better captured by physiological and behavioral measures of the autonomic nervous system (ANS) than by conscious or classical sensory tests. Responses to pleasant and unpleasant food odors presented in varying concentrations were assessed continuously using facial expressions and responses of the ANS. Results of 26 young and healthy female participants showed that the unpleasant fish odor triggered higher heart rates and skin conductance responses, lower skin temperature, fewer neutral facial expressions and more disgusted and angry expressions (p < 0.05). Neutral facial expressions differentiated between odors within 100 ms, after the start of the odor presentation followed by expressions of disgust (180 ms), anger (500 ms), surprised (580 ms), sadness (820 ms), scared (1020 ms), and happy (1780 ms) (all p-values < 0.05). Heart rate differentiated between odors after 400 ms, whereas skin conductance responses differentiated between odors after 3920 ms. At shorter intervals (between 520 and 1000 ms and between 2690 and 3880 ms) skin temperature for fish was higher than that for orange, but became considerable lower after 5440 ms. This temporal unfolding of emotions in reactions to odors, as seen in facial expressions and physiological measurements supports sequential appraisal theories.

Cross-cultural color-odor associations

Colors and odors are associated; for instance, people typically match the smell of strawberries to the color pink or red. These associations are forms of crossmodal correspondences. Recently, there has been discussion about the extent to which these correspondences arise for structural reasons (i.e., an inherent mapping between color and odor), statistical reasons (i.e., covariance in experience), and/or semantically-mediated reasons (i.e., stemming from language). The present study probed this question by testing color-odor correspondences in 6 different cultural groups (Dutch, Netherlands-residing-Chinese, German, Malay, Malaysian-Chinese, and US residents), using the same set of 14 odors and asking participants to make congruent and incongruent color choices for each odor. We found consistent patterns in color choices for each odor within each culture, showing that participants were making non-random color-odor matches. We used representational dissimilarity analysis to probe for variations in the patterns of color-odor associations across cultures; we found that US and German participants had the most similar patterns of associations, followed by German and Malay participants. The largest group differences were between Malay and Netherlands-resident Chinese participants and between Dutch and Malaysian-Chinese participants. We conclude that culture plays a role in color-odor crossmodal associations, which likely arise, at least in part, through experience.

Odors: appetizing or satiating? Development of appetite during odor exposure over time.

Background:Exposure to palatable food odors influences appetite responses, either promoting or inhibiting food intake. Possibly, food odors are appetizing after a short exposure (of circa 1–3 min), but become satiating over time (circa 10–20 min).Objective:To investigate the effect of odor exposure on general appetite and sensory-specific appetite (SSA) over time.Design:In a cross-over study, 21 unrestrained women (age: 18–45 years; BMI: 18.5–25 kg m−2) were exposed for 20 min to eight different odor types: five food odors, two nonfood odors and no-odor. All odors were distributed in a test room at suprathreshold levels. General appetite, SSA and salivation were measured over time.Results:All food odors significantly increased general appetite and SSA, compared with the no-odor condition. The nonfood odors decreased general appetite. All effects did not change over time during odor exposure. Savory odors increased the appetite for savory foods, but decreased appetite for sweet foods, and vice versa after exposure to sweet odors. Neither food odors nor nonfood odors affected salivation.Conclusions:Palatable food odors were appetizing during and after odor exposure and did not become satiating over a 20-min period. Food odors had a large impact on SSA and a small impact on general appetite. Moreover, exposure to food odors increased the appetite for congruent foods, but decreased the appetite for incongruent foods. It may be hypothesized that, once the body is prepared for intake of a certain food with a particular macronutrient composition, it is unfavorable to consume foods that are very different from the cued food.

Food preference and intake in response to ambient odours in overweight and normal-weight females

In our food abundant environment, food cues play an important role in the regulation of energy intake. Odours can be considered as external cues that can signal energy content in the anticipatory phase of eating. This study aims to determine whether exposure to olfactory cues associated with energy dense foods leads to increased food intake and greater preference for energy-dense foods. In addition, we assessed whether BMI and hunger state modulated this effect. Twenty-five overweight (mean BMI: 31.3 kg/m(2), S.E.: 0.6) and 25 normal-weight (mean BMI: 21.9 kg/m(2), S.E.: 0.4) females, matched on age and restraint score, participated. In 6 separate sessions they were exposed to odours of three different categories (signalling non-food, high-energy food and low-energy food) in two motivational states (hungry and satiated). After 10 min of exposure food preference was assessed with a computerized two-item forced choice task and after 20 min a Bogus Taste Test was used to determine energy intake (kcal and g). In a hungry state, the participants ate more (p<.001) and preferred high-energy products significantly more often (p<.001) when compared to the satiated state. A trend finding for the interaction between hunger and BMI suggested that the food preference of overweight participants was less affected by their internal state (p=.068). Neither energy intake (kcal: p=.553; g: p=.683) nor food preference (p=.280) was influenced by ambient exposure to odours signalling different categories. Future studies need to explore whether food odours can indeed induce overeating. More insight is needed regarding the possible influence of context (e.g. short exposure duration, large variety of food) and personality traits (e.g. restraint, impulsive) on odour-induced overeating.

Detecting Fat Content of Food from a Distance: Olfactory-Based Fat Discrimination in Humans

The desire to consume high volumes of fat is thought to originate from an evolutionary pressure to hoard calories, and fat is among the few energy sources that we can store over a longer time period. From an ecological perspective, however, it would be beneficial to detect fat from a distance, before ingesting it. Previous results indicate that humans detect high concentrations of fatty acids by their odor. More important though, would be the ability to detect fat content in real food products. In a series of three sequential experiments, using study populations from different cultures, we demonstrated that individuals are able to reliably detect fat content of food via odors alone. Over all three experiments, results clearly demonstrated that humans were able to detect minute differences between milk samples with varying grades of fat, even when embedded within a milk odor. Moreover, we found no relation between this performance and either BMI or dairy consumption, thereby suggesting that this is not a learned ability or dependent on nutritional traits. We argue that our findings that humans can detect the fat content of food via odors may open up new and innovative future paths towards a general reduction in our fat intake, and future studies should focus on determining the components in milk responsible for this effect.

Food odours direct specific appetite

Olfactory food cues were found to increase appetite for products similar in taste. We aimed to replicate this phenomenon for taste (sweet/savoury), determine whether it extends to energy density (high/low) as well, and uncover whether this effect is modulated by hunger state. Twenty-nine healthy-weight females smelled four odours differing in the energy density and taste they signalled, one non-food odour, and one odourless solution (control), in random order, for three minutes each. Appetite for 15 food products was rated in the following two minutes. Mixed model analyses revealed that exposure to an odour signalling a specific taste (respectively sweet, savoury) led to a greater appetite for congruent food products (sweet/savoury) compared to incongruent food products (savoury p < 0.001; sweet p < 0.001) or neutral food products (p = 0.02; p = 0.003). A similar pattern was present for the energy-density category (respectively high-energy dense, low-energy dense) signalled by the odours (low-energy products p < 0.001; high-energy products p = 0.008). Hunger state did not have a significant impact on sensory-specific appetite. These results suggest that exposure to food odours increases appetite for congruent products, in terms of both taste and energy density, irrespective of hunger state. We speculate that food odours steer towards intake of products with a congruent macronutrient composition.