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Acute stress and food-related reward activation in the brain during food choice during eating in the absence of hunger

International Journal of Obesity volume 34, pages 172–181 (2010)Cite this article

Abstract

Background:

Stress results in eating in the absence of hunger, possibly related to food reward perception.

Hypothesis:

Stress decreases food reward perception.

Aim:

Determine the effect of acute stress on food choice and food choice reward-related brain activity.

Subjects:

Nine females (BMI=21.5±2.2 kg/m2, age=24.3±3.5 years).

Procedure:

Fasted subjects came twice to randomly complete either a rest or stress condition. Per session, two functional MRI scans were made, wherein the subjects chose the subsequent meal (food images). The rewarding value of the food was measured as liking and wanting. Food characteristics (for example, crispiness, fullness of taste and so on), energy intake, amount of each macronutrient chosen, plasma cortisol and Visual Analog Scale (VAS) hunger and satiety were measured.

Results:

Fasted state was confirmed by high hunger (80±5 mm VAS). Breakfast energy intake (3±1 MJ) and liking were similar in all conditions. Wanting was lower postprandially (Δ=−0.3 items/category, P<0.01). Breakfast decreased hunger (−42 mm VAS, P<0.01). Postprandially, energy intake (−1.1 MJ), protein intake (−14.7 g) and carbohydrate intake (−32.7 g all P<0.05) were lower. Fat intake was not different (−7.3, P=0.4). Putamen activity was not lower postprandially. Cortisol levels were increased in the stress condition (Area under the curve of cortisol: ΔAUC=+2.2 × 104 nmol min−1 l−1, P<0.05). Satiety was lower after breakfast (−8 mm VAS, P<0.01). Postprandial energy intake, protein intake and carbohydrate intake were relatively higher compared with the rest condition, resulting from more choice for crispiness and fullness of taste (P<0.05). Brain activation was reduced in reward areas: amygdala, hippocampus and cingulate cortex (AUC=−13.33, −1.34, −2.56% blood oxygen level dependent (BOLD) s for choosing breakfast and AUC=−9.31, −1.25, −2.34%BOLD s<0.05 for choosing the second meal). Putamen activation was decreased postprandially (AUC=−1.2%BOLD s, P<0.05).

Conclusion:

Reward signaling and reward sensitivity were significantly lower under stress, coinciding with increased energy intake from food choice for more crispiness and fullness of taste. The changes in putamen activation may reflect specifically decreased reward prediction sensitivity.

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Acknowledgements

We gratefully acknowledge S Verhoef for help with the practical work, P Schoffelen for his contribution regarding the technical realization of the scan paradigm and the synchronization with the scanner, S Gijsen for essential help and input concerning the fMRI scanner and A Heinecke for his extensive support for the analyses with BrainVoyager. Furthermore, we thank M Hulsbosch, W Sluismans and J Sulon for analyzing the serum and plasma hormone samples.

Author information

Authors and Affiliations

  1. Department of Human Biology, Maastricht University, Maastricht, The Netherlands

    J M Born, S G T Lemmens, F Rutters, A G Nieuwenhuizen & M S Westerterp-Plantenga

  2. Top Institute Food and Nutrition, Wageningen, The Netherlands

    J M Born, S G T Lemmens & A G Nieuwenhuizen

  3. Department of Cognitive Neuroscience, Maastricht University, Maastricht, The Netherlands

    E Formisano & R Goebel

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  1. J M Born
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Correspondence to J M Born.

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Author contribution

JMB conducted the experiment, including fMRI, developed the fMRI data analysis, analyzed the data and wrote the manuscript. SGTL conducted the experiment, assisted with fMRI and reviewed the manuscript and developed the liking and wanting paradigm. FR advised on the fMRI paradigm and reviewed the manuscript. AGN advised on the setup of the experiment concerning the acute stress paradigm and reviewed the manuscript. EF and RG advised on the setup of the fMRI paradigm, data analysis and reviewed the manuscript. MSWP conceived the experiment and developed the liking and wanting paradigm reviewed the manuscript.

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Born, J., Lemmens, S., Rutters, F. et al. Acute stress and food-related reward activation in the brain during food choice during eating in the absence of hunger. Int J Obes 34, 172–181 (2010). https://doi.org/10.1038/ijo.2009.221

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