Odour-imagery ability is linked to food craving, intake, and adiposity change in humans.

It is well-known that food-cue reactivity (FCR) is positively associated with body mass index (BMI)1 and weight change2, but the mechanisms underlying these relationships are incompletely understood. One prominent theory of craving posits that the elaboration of a desired substance through sensory imagery intensifies cravings, thereby promoting consumption3. Olfaction is integral to food perception, yet the ability to imagine odours varies widely4. Here we test in a basic observational study whether this large variation in olfactory imagery drives FCR strength to promote adiposity in 45 adults (23 male). We define odour-imagery ability as the extent to which imagining an odour interferes with the detection of a weak incongruent odour (the 'interference effect'5). As predicted in our preregistration, the interference effect correlates with the neural decoding of imagined, but not real, odours. These perceptual and neural measures of odour imagery are in turn associated with FCR, defined by the rated craving intensity of liked foods and cue-potentiated intake. Finally, odour imagery exerts positive indirect effects on changes in BMI and body-fat percentage over one year via its influences on FCR. These findings establish odour imagery as a driver of FCR that in turn confers risk for weight gain.

Odor imagery but not perception drives risk for food cue reactivity and increased adiposity.

Mental imagery has been proposed to play a critical role in the amplification of cravings. Here we tested whether olfactory imagery drives food cue reactivity strength to promote adiposity in 45 healthy individuals. We measured odor perception, odor imagery ability, and food cue reactivity using self-report, perceptual testing, and neuroimaging. Adiposity was assessed at baseline and one year later. Brain responses to real and imagined odors were analyzed with univariate and multivariate decoding methods to identify pattern-based olfactory codes. We found that the accuracy of decoding imagined, but not real, odor quality correlated with a perceptual measure of odor imagery ability and with greater adiposity changes. This latter relationship was mediated by cue-potentiated craving and intake. Collectively, these findings establish odor imagery ability as a risk factor for weight gain and more specifically as a mechanism by which exposure to food cues promotes craving and overeating.

Olfactory decoding is positively associated with ad libitum food intake in sated humans.

The role of olfaction in eating behavior and body weight regulation is controversial. Here we reanalyzed data from a previous functional magnetic resonance imaging study to test whether central olfactory coding is associated with hunger/satiety state, food intake, and change in body weight over one year in healthy human adults. Since odor quality and category are coded across distributed neural patterns that are not discernible with traditional univariate analyses, we used multi-voxel pattern analyses to decode patterns of brain activation to food versus nonfood odors. We found that decoding accuracies in the piriform cortex and amygdala were greater in the sated compared to hungry state. Sated decoding accuracies in these and other regions were also associated with post-scan ad libitum food intake, but not with weight change. These findings demonstrate that the fidelity of olfactory decoding is influenced by meal consumption and is associated with immediate food intake, but not longer-term body weight regulation.

Fat and Carbohydrate Interact to Potentiate Food Reward in Healthy Weight but Not in Overweight or Obesity.

Prior work suggests that actual, but not estimated, energy density drives the reinforcing value of food and that energy from fat and carbohydrate can interact to potentiate reward. Here we sought to replicate these findings in an American sample and to determine if the effects are influenced by body mass index (BMI). Thirty participants with healthy weight (HW; BMI 21.92 ± 1.77; M ± SD) and 30 participants with overweight/obesity (OW/OB; BMI 29.42 ± 4.44) rated pictures of common American snacks in 120-kcal portions for liking, familiarity, frequency of consumption, expected satiety, healthiness, energy content, energy density, and price. Participants then completed an auction task where they bid for the opportunity to consume each food. Snacks contained either primarily carbohydrate, primarily fat, or roughly equal portions of fat and carbohydrate (combo). Replicating prior work, we found that participants with HW bid the most for combo foods in linear mixed model analyses. This effect was not observed among individuals with OW/OB. Additionally, in contrast with previous reports, our linear regression analyses revealed a negative relationship between the actual energy density of the snacks and bid amount that was mediated by food price. Our findings support altered macronutrient reinforcement in obesity and highlight potential influences of the food environment on the regulation of food reward.

Development of MacroPics: A novel food picture set to dissociate the effects of carbohydrate and fat on eating behaviors.

Emerging evidence suggests that fat and carbohydrate interact to potentiate the reward value of food (DiFeliceantonio et al., 2018). The primary goal of the current study was to develop a novel picture set to facilitate research into the effects of macronutrient composition on food choice and eating behavior. Toward this aim, we developed "MacroPics." In Experiment 1, we photographed 120-kcal portions of 60 snack foods falling into one of the three macronutrient categories: (1) mostly carbohydrate, (2) mostly fat, or (3) a combination of fat and carbohydrate. Sixty-one participants rated the images for liking, familiarity, frequency of consumption, healthiness, estimated energy content (in kcal), and expected satiation. A subset of these images consisting of 36 items was then selected in an iterative process to minimize differences in ratings between the macronutrient categories while simultaneously ensuring similar within-category variability on a number of food characteristics (e.g., energy density, portion size, retail price) and visual properties (e.g., color, complexity, visual area). In Experiment 2, an independent sample of 67 participants rated the pictures of the final 36-item MacroPics. Both experiments reveal similar participant ratings across categories for item liking, familiarity, frequency, healthiness, and estimated energy content. Protein content was higher in the fat compared to the carbohydrate and combination categories, leading to higher ratings of estimated satiety and energy density for fatty foods. Item and macronutrient category characteristics of the final MacroPics set are reported.

No evidence for an association between obesity and milkshake liking.

BACKGROUND: Prevailing models of obesity posit that hedonic signals override homeostatic mechanisms to promote overeating in today's food environment. What researchers mean by "hedonic" varies considerably, but most frequently refers to an aggregate of appetitive events including incentive salience, motivation, reinforcement, and perceived pleasantness. Here we define hedonic as orosensory pleasure experienced during eating and set out to test whether there is a relationship between adiposity and the perceived pleasure of a palatable and energy-dense milkshake. METHODS: The perceived liking, wanting, and intensity of two palatable and energy-dense milkshakes were assessed using the Labeled Hedonic Scale (1), visual analog scale (VAS), and Generalized Labeled Magnitude Scale (2) in 110 individuals ranging in body mass index (BMI) from 19.3 to 52.1 kg/m2. Waist circumference, waist-hip ratio, and percent body fat were also measured. Importantly, unlike the majority of prior studies, we attempted to standardize internal state by instructing participants to arrive to the laboratory neither hungry nor full and at least 1-h fasted. Data were analyzed with general linear and linear mixed effects models (GLMs). Hunger ratings were also examined prior to hedonic measurement and included as covariates in our analyses. RESULTS: We identified a significant association between ratings of hunger and milkshake liking and wanting. By contrast, we found no evidence for a relationship between any measure of adiposity and ratings of milkshake liking, wanting, or intensity. CONCLUSIONS: We conclude that adiposity is not associated with the pleasure experienced during consumption of our energy-dense and palatable milkshakes. Our results provide further evidence against the hypothesis that heightened hedonic signals drive weight gain.

Identification of a brain fingerprint for overweight and obesity.

The brain plays a central role in the pathophysiology of overweight and obesity. Connectome-based Predictive Modeling (CPM) is a newly developed, data-driven approach that exploits whole-brain functional connectivity to predict a behavior or trait that varies across individuals. We used CPM to determine whether brain "fingerprints" evoked during milkshake consumption could be isolated for common measures of adiposity in 67 adults with overweight and obesity. We found that CPM captures more variance in waist circumference than either percent body fat or BMI, the most frequently used measures to assess brain correlates of obesity. In a post-hoc analysis, we were also able to derive a largely separable functional connectivity network predicting fasting blood insulin. These findings suggest that, in individuals with overweight and obesity, brain network patterns may be more tightly coupled to waist circumference than BMI or percent body fat and that adiposity and glucose tolerance are associated with distinct maps, pointing to dissociable central pathophysiological phenotypes for obesity and diabetes.