Integration of homeostatic signaling and food reward processing in the human brain
Joe J. Simon, Anne Wetzel, Maria Hamze Sinno, Mandy Skunde, Martin Bendszus, Hubert Preissl, Paul Enck, Wolfgang Herzog, Hans-Christoph Friederich
Joe J. Simon, Anne Wetzel, Maria Hamze Sinno, Mandy Skunde, Martin Bendszus, Hubert Preissl, Paul Enck, Wolfgang Herzog, Hans-Christoph Friederich
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Clinical Research and Public Health Neuroscience

Integration of homeostatic signaling and food reward processing in the human brain

Abstract

BACKGROUND. Food intake is guided by homeostatic needs and by the reward value of food, yet the exact relation between the two remains unclear. The aim of this study was to investigate the influence of different metabolic states and hormonal satiety signaling on responses in neural reward networks. METHODS. Twenty-three healthy participants underwent functional magnetic resonance imaging while performing a task distinguishing between the anticipation and the receipt of either food- or monetary-related reward. Every participant was scanned twice in a counterbalanced fashion, both during a fasted state (after 24 hours fasting) and satiety. A functional connectivity analysis was performed to investigate the influence of satiety signaling on activation in neural reward networks. Blood samples were collected to assess hormonal satiety signaling. RESULTS. Fasting was associated with sensitization of the striatal reward system to the anticipation of food reward irrespective of reward magnitude. Furthermore, during satiety, individual ghrelin levels were associated with increased neural processing during the expectation of food-related reward. CONCLUSIONS. Our findings show that physiological hunger stimulates food consumption by specifically increasing neural processing during the expectation (i.e., incentive salience) but not the receipt of food-related reward. In addition, these findings suggest that ghrelin signaling influences hedonic-driven food intake by increasing neural reactivity during the expectation of food-related reward. These results provide insights into the neurobiological underpinnings of motivational processing and hedonic evaluation of food reward. TRIAL REGISTRATION. ClinicalTrials.gov NCT03081585. FUNDING. This work was supported by the German Competence Network on Obesity, which is funded by the German Federal Ministry of Education and Research (FKZ 01GI1122E).

Authors

Joe J. Simon, Anne Wetzel, Maria Hamze Sinno, Mandy Skunde, Martin Bendszus, Hubert Preissl, Paul Enck, Wolfgang Herzog, Hans-Christoph Friederich

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Figure 3

Neural activation during monetary reward processing.

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Neural activation during monetary reward processing. (A) During the expe...
(A) During the expectation of monetary-related reward, percentage signal change extracted from the right and left ventral striatum was influenced by reward level (F(1,21) = 21.47, P < 0.001, F(1,21) = 28.06, P < 0.001, n = 22, respectively) but not by satiety state (all P values > 0.47, n = 23). We observed no interaction between reward level and satiety state (all P values > 0.47, n = 23). (B) During the receipt of food-related reward, percentage signal change extracted from the right and left orbitofrontal cortex was neither influenced by reward level nor by satiety state (all P values > 0.09, n = 23). Activity in the medial orbitofrontal cortex was influence by reward level (F(1,21) = 12.36, P < 0.001, n = 23) but not by satiety state (P = 0.81, n = 23). We observed an interaction effect between reward level and satiety state in the medial orbitofrontal cortex (F(2,42) = 4.26, P = 0.021, n = 23) but the right or left orbitofrontal cortex (all P values > 0.34, n = 23). Repeated-measures ANOVAs were used for the statistical analysis. In box-and-whisker plots, horizontal bars indicate the medians, boxes indicate 25th to 75th percentiles, and whiskers indicate 10th and 90th percentiles.