Increased colonic propionate reduces anticipatory reward responses in the human striatum to high-energy foods

Byrne, C. S. et al. (2016) Increased colonic propionate reduces anticipatory reward responses in the human striatum to high-energy foods. American Journal of Clinical Nutrition, 104(1), pp. 5-14. (doi: 10.3945/ajcn.115.126706) (PMID:27169834) (PMCID:PMC4919527)

Abstract

Background: Short-chain fatty acids (SCFAs), metabolites produced through the microbial fermentation of nondigestible dietary components, have key roles in energy homeostasis. Animal research suggests that colon-derived SCFAs modulate feeding behavior via central mechanisms. In humans, increased colonic production of the SCFA propionate acutely reduces energy intake. However, evidence of an effect of colonic propionate on the human brain or reward-based eating behavior is currently unavailable. Objectives: We investigated the effect of increased colonic propionate production on brain anticipatory reward responses during food picture evaluation. We hypothesized that elevated colonic propionate would reduce both reward responses and ad libitum energy intake via stimulation of anorexigenic gut hormone secretion. Design: In a randomized crossover design, 20 healthy nonobese men completed a functional magnetic resonance imaging (fMRI) food picture evaluation task after consumption of control inulin or inulin-propionate ester, a unique dietary compound that selectively augments colonic propionate production. The blood oxygen level–dependent (BOLD) signal was measured in a priori brain regions involved in reward processing, including the caudate, nucleus accumbens, amygdala, anterior insula, and orbitofrontal cortex (n = 18 had analyzable fMRI data). Results: Increasing colonic propionate production reduced BOLD signal during food picture evaluation in the caudate and nucleus accumbens. In the caudate, the reduction in BOLD signal was driven specifically by a lowering of the response to high-energy food. These central effects were partnered with a decrease in subjective appeal of high-energy food pictures and reduced energy intake during an ad libitum meal. These observations were not related to changes in blood peptide YY (PYY), glucagon-like peptide 1 (GLP-1), glucose, or insulin concentrations. Conclusion: Our results suggest that colonic propionate production may play an important role in attenuating reward-based eating behavior via striatal pathways, independent of changes in plasma PYY and GLP-1. This trial was registered at clinicaltrials.gov as NCT00750438.

• Item Type: Articles
• Additional Information: The Section of Endocrinology and Investigative Medicine is funded by grants from the Medical Research Council (MRC), Biotechnology and Biological Sciences Research Council (BBSRC), and NIHR, an Integrative Mammalian Biology Capacity Building Award, and an FP7-HEALTH-2009- 241592 EuroCHIP grant, and is supported by the NIHR Biomedical Research Centre Funding Scheme. GSF holds an NIHR Senior Investigator Award, CSB and APG are funded by the United Kingdom MRC, and ESC is funded by the BBSRC.
• Status: Published
• Refereed: Yes
• Glasgow Author(s) Enlighten ID: Preston, Professor Tom and Morrison, Professor Douglas
• Authors: Byrne, C. S., Chambers, E. S., Alhabeeb, H., Chhina, N., Morrison, D. J., Preston, T., Tedford, C., Fitzpatrick, J., Irani, C., Busza, A., Garcia-Perez, I., Fountana, S., Holmes, E., Goldstone, A. P., and Frost, G. S.
• College/School: College of Science and Engineering > Scottish Universities Environmental Research Centre
• Journal Name: American Journal of Clinical Nutrition
• Publisher: American Society for Nutrition
• ISSN: 0002-9165
• ISSN (Online): 1938-3207
• Published Online: 11 May 2016
• Copyright Holders: Copyright © 2016 The Authors
• First Published: First published in American Journal of Clinical Nutrition 104(1): 5-14
• Publisher Policy: Reproduced under a Creative Commons License