Mieke J.I. Martens

Differences between liking and wanting signals in the human brain and relations with cognitive dietary restraint and body mass index

BACKGROUND Eating behavior is determined, to a significant extent, by the rewarding value of food (ie, liking and wanting). OBJECTIVE We determined brain regions involved in liking and wanting and related brain signaling to body mass index (BMI; in kg/m(2)) and dietary restraint. DESIGN Fifteen normal-weight female subjects [mean ± SEM age: 21.5 ± 0.4 y; BMI: 22.2 ± 0.2] completed a food-choice paradigm by using visually displayed food items during functional magnetic resonance imaging scans. Two scans were made as follows: one scan was made in a fasted condition, and one scan was made in a satiated condition. The paradigm discriminated between liking and wanting, and subjects were offered items rated highly for wanting immediately after each scan. Imaging contrasts for high and low liking and wanting were made, and data for regions of interest were extracted. Activation related to liking and wanting, respectively, was determined. Outcomes were correlated to cognitive dietary restraint and BMI. RESULTS Dietary restraint predicted liking task-related signaling (TRS) in the amygdala, striatum, thalamus, and cingulate cortex (r = -0.5 ± 0.03, P < 0.00001). In the nucleus accumbens, the premeal liking and wanting TRS and premeal to postmeal liking TRS changes correlated positively with dietary restraint [bilateral average r = 0.6 ± 0.02, P < 0.04 (Bonferroni corrected)]. BMI and hunger predicted wanting TRS in the hypothalamus and striatum (P < 0.05). Postmeal liking TRS in the striatum, anterior insula, and cingulate cortex and wanting TRS in the striatum predicted the energy intake (liking: r = -0.3 ± 0.05, P < 0.0001; wanting: r = -0.3 ± 0.03, P < 0.00001). CONCLUSIONS Successful dietary restraint was supported by liking TRS from premeal to postmeal in the nucleus accumbens. Reward-related signaling was inversely related to BMI and energy intake, indicating reward deficiency.

Increased sensitivity to food cues in the fasted state and decreased inhibitory control in the satiated state in the overweight

BACKGROUND Flexibility of food reward-related brain signaling (FRS) between food and nonfood stimuli may differ between overweight and normal-weight subjects and depend on a fasted or satiated state. OBJECTIVE The objective was to assess this flexibility in response to visual food and nonfood cues. DESIGN Twenty normal-weight [mean ± SEM BMI (in kg/m(2)) = 22.7 ± 0.2; mean ± SEM age = 22.4 ± 0.4 y] and 20 overweight (BMI = 28.1 ± 0.3; age = 24.0 ± 0.7 y) participants completed 2 fMRI scans. Subjects arrived in a fasted state and consumed a breakfast consisting of 20% of subject-specific energy requirements between 2 successive scans. A block paradigm and a food > nonfood contrast was used to determine FRS. RESULTS An overall stimulus × condition × subject group effect was observed in the anterior cingulate cortex (ACC) (P < 0.006, F((1,38)) = 9.12) and right putamen (P < 0.006, F((1,38)) = 9.27). In all participants, FRS decreased from the fasted to the satiated state in the cingulate (P < 0.005, t((39)) = 3.15) and right prefrontal cortex (PFC) (P < 0.006, t((39)) = 3.00). In the fasted state, they showed FRS in the PFC (P < 0.004, t((39)) = 3.17), left insula (P < 0.009, t((39)) = 2.95), right insula (P < 0.005, t((39)) = 3.12), cingulate cortex (P < 0.004, t((39)) = 3.21), and thalamus (P < 0.006, t((39)) = 2.96). In the satiated state, FRS was limited to the left insula (P < 0.005, t((39)) = 3.21), right insula (P < 0.006, t((39)) = 3.04), and cingulate cortex (P < 0.005, t((39)) = 3.15). Regarding subject group, in the fasted state, FRS in the ACC was more pronounced in overweight than in normal-weight subjects (P < 0.005, F((1,38)) = 9.71), whereas in the satiated state, FRS was less pronounced in overweight than in normal-weight subjects in the ACC (P < 0.006, F((1,38)) = 9.18) and PFC (P < 0.006, F((1,38)) = 8.86), which suggests lower inhibitory control in the overweight. CONCLUSION FRS was higher in the overweight in the satiated state; however, when sufficiently satiated, the overweight showed decreased inhibitory control signalling, which facilitates overeating. This trial was registered in the Dutch clinical trial register as NTR2174.

Influence of Consumption of a High-Protein vs. High-Carbohydrate Meal on the Physiological Cortisol and Psychological Mood Response in Men and Women

Consumption of meals with different macronutrient contents, especially high in carbohydrates, may influence the stress-induced physiological and psychological response. The objective of this study was to investigate effects of consumption of a high-protein vs. high-carbohydrate meal on the physiological cortisol response and psychological mood response. Subjects (n = 38, 19m/19f, age = 25±9 yrs, BMI = 25.0±3.3 kg/m2) came to the university four times, fasted, for either condition: rest-protein, stress-protein, rest-carbohydrate, stress-carbohydrate (randomized cross-over design). Stress was induced by means of a psychological computer-test. The test-meal was either a high-protein meal (En% P/C/F 65/5/30) or a high-carbohydrate meal (En% P/C/F 6/64/30), both meals were matched for energy density (4 kJ/g) and daily energy requirements (30%). Per test-session salivary cortisol levels, appetite profile, mood state and level of anxiety were measured. High hunger, low satiety (81±16, 12±15 mmVAS) confirmed the fasted state. The stress condition was confirmed by increased feelings of depression, tension, anger, anxiety (AUC stress vs. rest p<0.02). Consumption of the high-protein vs. high-carbohydrate meal did not affect feelings of depression, tension, anger, anxiety. Cortisol levels did not differ between the four test-sessions in men and women (AUC nmol·min/L p>0.1). Consumption of the test-meals increased cortisol levels in men in all conditions (p<0.01), and in women in the rest-protein and stress-protein condition (p<0.03). Men showed higher cortisol levels than women (AUC nmol·min/L p<0.0001). Consumption of meals with different macronutrient contents, i.e. high-protein vs. high-carbohydrate, does not influence the physiological and psychological response differentially. Men show a higher meal-induced salivary cortisol response compared with women.

A solid high-protein meal evokes stronger hunger suppression than a liquefied high-protein meal.

Hunger is a potential problem for compliance with an energy‐restricted diet. Relatively high‐protein meal‐replacement products have been shown to diminish this problem; they are available as liquid and solid meals, yet their physical state can affect hunger suppression. The objective was to investigate the differences in appetite profile and physiological parameters after consumption of a single‐macronutrient, subject‐specific, high‐protein meal in liquefied vs. solid form, controlled for energy density, weight, and volume. Ten male subjects (age: 21.1 ± 3.9 years; BMI: 22.4 ± 1.2 kg/m2) were offered lunch subject‐specifically as 15% of daily energy requirement (DER), consisting of solid (steamed chicken breast + 750 ml water) or liquefied protein (steamed chicken breast blended in 500 ml water + 250 ml water). Appetite profiles, insulin, glucose, and ghrelin were measured over 3 h. Comparing the solid vs. liquefied condition, oral exposure time did not differ between conditions (19.2 ± 0.4 and 18.8 ± 0.6 min, respectively; P = 0.13). Area under the curve (AUC) effects were observed for thirst; statistically significant condition × time interactions and statistically significant differences at several time points were observed for desire to eat (condition × time P < 0.05; 31 ± 6 mm vs. 53 ± 8 mm; P < 0.04 at 115 min) and thirst (condition × time P < 0.01; 27 ± 8 mm vs. 41 ± 8 mm; P < 0.05 at 30 min and 23 ± 6 mm vs. 41 ± 8 mm; P < 0.02 at 70 min) to be lower, while hunger suppression (79 ± 3 mm and 52 ± 10 mm; P < 0.03 at 20 min and 61 ± 7 mm and 44 ± 8 mm; P < 0.03 at 115 min) was higher in the solid condition. Glucose, insulin, and ghrelin concentration curves were similar for both conditions. In conclusion, solid protein evokes a stronger suppression of hunger and desire to eat than liquefied protein.

Mode of Consumption Plays a Role in Alleviating Hunger and Thirst

While studying the effect of structure on satiety, effects of mode of consumption, additional water to drink, and thirst have been neglected. The objective was to assess effects of structure, mode of consumption of food, and additional drinking of water on fullness and thirst. In study 1, 20 subjects (BMI 22.5 ± 0.5 kg/m2; age 21.4 ± 3 years) underwent consumption conditions; SEW: solids to eat + 750 ml water to drink; LEW: liquefied soup to eat including 500 ml water + 250 ml water separately to drink; LDW: the same as LEW but served as drinks; SE, LE, and LD: the same as previous but without water to drink. In study 2, a subset of subjects underwent consumption conditions: solid carbohydrate, solid protein, solid fat: the same as SEW, but for each macronutrient separately; liquefied carbohydrate, liquefied protein, liquefied fat: the same as LEW, but for each macronutrient separately. Appetite, insulin concentration, glucose concentration, and ghrelin concentration were measured. Eating, independent of structure, suppressed desire to eat more than drinking (P < 0.01). Drinking water separately vs. water consumption in the food suppressed thirst more (P < 0.001). Regarding protein, satiety was higher in the solid vs. liquefied condition, while blood parameters were not significantly different. Only after drinking a meal most subjects (80%) wanted to consume more of the same meal, in order to alleviate hunger (63%) or quench thirst (37%). We conclude that mode of consumption plays a role in alleviating hunger and thirst. Subjects required further consumption after drinking the meal, motivated by hunger or thirst, showing that drinking a meal causes confusion that may imply a risk of overconsumption.

Protein v. carbohydrate intake differentially affects liking- and wanting-related brain signalling

Extreme macronutrient intakes possibly lead to different brain signalling. The aim of the present study was to determine the effects of ingesting high-protein v. high-carbohydrate food on liking and wanting task-related brain signalling (TRS) and subsequent macronutrient intake. A total of thirty female subjects (21.6 (SD 2.2) years, BMI 25.0 (SD 3.7) kg/m²) completed four functional MRI scans: two fasted and two satiated on two different days. During the scans, subjects rated all food items for liking and wanting, thereby choosing the subsequent meal. The results show that high-protein (PROT) v. high-carbohydrate (CARB) conditions were generated using protein or carbohydrate drinks at the first meal. Energy intake and hunger were recorded. PROT (protein: 53.7 (SD 2.1) percentage of energy (En%); carbohydrate: 6.4 (SD 1.3) En%) and CARB conditions (protein: 11.8 (SD 0.6) En%; carbohydrate: 70.0 (SD 2.4) En%) were achieved during the first meal, while the second meals were not different between the conditions. Hunger, energy intake, and behavioural liking and wanting ratings were decreased after the first meal (P< 0.001). Comparing the first with the second meal, the macronutrient content changed: carbohydrate -26.9 En% in the CARB condition, protein -37.8 En% in the PROT condition. After the first meal in the CARB condition, wanting TRS was increased in the hypothalamus. After the first meal in the PROT condition, liking TRS was decreased in the putamen (P< 0.05). The change in energy intake from the first to the second meal was inversely related to the change in liking TRS in the striatum and hypothalamus in the CARB condition and positively related in the PROT condition (P< 0.05). In conclusion, wanting and liking TRS were affected differentially with a change in carbohydrate or protein intake, underscoring subsequent energy intake and shift in macronutrient composition.

Satiating Capacity and Post-Prandial Relationships between Appetite Parameters and Gut-Peptide Concentrations with Solid and Liquefied Carbohydrate

Background Differences in satiating capacity of liquid and solid meals are unclear. Objective Investigating appetite parameters, physiological measurements and within-subject relationships after consumption of a single macronutrient, subject-specific carbohydrate meal in liquefied versus solid form, controlled for energy density, weight and volume. Design In a cross-over design, ten male subjects (age = 21.1±3.9 y, BMI = 22.4±1.2 kg/m2) consumed a solid (CS, whole peaches +750 ml water) and liquefied carbohydrate (CL, peach blended in 500 ml water +250 ml water) lunch. Appetite profiles, insulin-, glucose- and ghrelin concentrations were measured over three hours. Post-prandial relationships between appetite and blood parameters were calculated using subject-specific regression analyses. Results Fullness ratings were higher in the CL (85±5 mm) compared to the CS condition (73±8 mm) at 20 min (p<0.03). Glucose concentrations peaked 20 to 30 min after the start of the lunch in the CL condition, and 30 to 40 min after start of the CS condition. Correspondingly, insulin concentrations were peaked at 20–30 min in the CL condition, and at 30–40 min in the CS condition. AUC or condition x time interactions were not different comparing the CL and the CS condition. Insulin was significantly higher in the CS compared to the CL condition 40 min after the start of the lunch (p<0.05). Fullness scores were significantly related to insulin concentrations but not to glucose concentrations; desire to eat scores were significantly associated with ghrelin concentrations in both, the CL and the CS condition. The relationship between fullness scores and glucose concentrations was not statistically significant. Conclusion Liquefied and solid carbohydrate meals do not differ in satiating capacity, supported by appetite profile and relevant blood parameters. Postprandially, fullness and desire to eat were associated with respectively insulin and ghrelin concentrations.

The Hypothalamic-Pituitary-Adrenal Axis, Obesity, and Chronic Stress Exposure: Foods and HPA Axis

The prevalence of overweight and obesity has increased worldwide to epidemic proportions. Dysregulation of the hypothalamic–pituitary–adrenal (HPA) axis and chronic stress exposure are hypothesized to contribute to obesity development. In this review, we discuss the potential role of the HPA axis for energy balance regulation, with particular attention to energy intake. We present evidence from human and animal studies that highlight the bidirectional relationship between HPA axis functioning and energy intake. Of particular interest is the association between dysregulation of the HPA axis and altered homeostatic and non-homeostatic food intake regulation. Lastly, we discuss a model depicting a role for a hyperactive HPA axis in overeating and the development of obesity, suggesting chronic stress as a major risk factor for excessive weight gain and (visceral) obesity.

High HPA-axis activation disrupts the link between liking and wanting with liking and wanting related brain signaling

BACKGROUND Eating behavior changes under stress, i.e. during high HPA-axis activation. AIM Assessment of effects of high versus low HPA-axis activation on liking and wanting related brain signaling in relevant regions. METHODS 15 female subjects (21.5±0.4 years, BMI=22.2±0.4) completed fMRI scans on 2 days, in a fasted as well as a satiated condition on each day. The days were sorted by HPA-axis activation, resulting in two sufficiently separated HPA-axis states which were statistically confirmed (p<.05). During scans, subjects rated liking and wanting for food images; wanting indicated food choice for the subsequent meal. Energy-intake, hunger and fullness were additionally recorded. RESULTS Hunger changed significantly over the meal (p<.001). Energy intake was lower during the second meal (p<.001). Behavioral wanting was lower after breakfast (p<.01), behavioral liking did not change. During low HPA-activation, liking task related signaling (TRS) pre-meal in the anterior insula predicted behavioral liking, wanting TRS in the anterior insula, nucleus accumbens and thalamus predicted behavioral wanting. During high HPA-activation, these relationships were not present pre-meal, but post-meal behavioral liking was predicted in the nucleus accumbens and wanting in the caudate. CONCLUSION High HPA-axis activation disrupted and redirected the connection of behavioral liking/wanting with the specifically associated brain signaling in relevant regions.