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

Claire S Byrne, Edward S Chambers, Habeeb Alhabeeb, Navpreet Chhina, Douglas J Morrison, Tom Preston, Catriona Tedford, Julie Fizpatrick, Cherag Irani, Albert Busza, Isabel Garcia-Perez, Sofia Fountana, Elaine Holmes, Anthony P Goldstone, Gary S Frost

Research output: Contribution to journalArticle

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.
Original languageEnglish
JournalThe American Journal of Clinical Nutrition
Early online date11 May 2016
DOIs
Publication statusE-pub ahead of print - 11 May 2016

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Propionates
Reward
Food
Volatile Fatty Acids
Feeding Behavior
Energy Intake
Peptide YY
Glucagon-Like Peptide 1
Inulin
Caudate Nucleus
Nucleus Accumbens
Oxygen
Brain
Magnetic Resonance Imaging
Corpus Striatum
Amygdala
Prefrontal Cortex
Cross-Over Studies
Fermentation
Meals

Cite this

Byrne, Claire S ; Chambers, Edward S ; Alhabeeb, Habeeb ; Chhina, Navpreet ; Morrison, Douglas J ; Preston, Tom ; Tedford, Catriona ; Fizpatrick, Julie ; Irani, Cherag ; Busza, Albert ; Garcia-Perez, Isabel ; Fountana, Sofia ; Holmes, Elaine ; Goldstone, Anthony P ; Frost, Gary S. / Increased colonic propionate reduces anticipatory reward responses in the human striatum to high-energy foods. In: The American Journal of Clinical Nutrition. 2016.
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title = "Increased colonic propionate reduces anticipatory reward responses in the human striatum to high-energy foods",
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.",
author = "Byrne, {Claire S} and Chambers, {Edward S} and Habeeb Alhabeeb and Navpreet Chhina and Morrison, {Douglas J} and Tom Preston and Catriona Tedford and Julie Fizpatrick and Cherag Irani and Albert Busza and Isabel Garcia-Perez and Sofia Fountana and Elaine Holmes and Goldstone, {Anthony P} and Frost, {Gary S}",
year = "2016",
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Byrne, CS, Chambers, ES, Alhabeeb, H, Chhina, N, Morrison, DJ, Preston, T, Tedford, C, Fizpatrick, J, Irani, C, Busza, A, Garcia-Perez, I, Fountana, S, Holmes, E, Goldstone, AP & Frost, GS 2016, 'Increased colonic propionate reduces anticipatory reward responses in the human striatum to high-energy foods' The American Journal of Clinical Nutrition. https://doi.org/10.3945/ajcn.115.126706

Increased colonic propionate reduces anticipatory reward responses in the human striatum to high-energy foods. / Byrne, Claire S; Chambers, Edward S; Alhabeeb, Habeeb; Chhina, Navpreet; Morrison, Douglas J; Preston, Tom; Tedford, Catriona; Fizpatrick, Julie; Irani, Cherag; Busza, Albert; Garcia-Perez, Isabel; Fountana, Sofia; Holmes, Elaine; Goldstone, Anthony P; Frost, Gary S.

In: The American Journal of Clinical Nutrition, 11.05.2016.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Increased colonic propionate reduces anticipatory reward responses in the human striatum to high-energy foods

AU - Byrne, Claire S

AU - Chambers, Edward S

AU - Alhabeeb, Habeeb

AU - Chhina, Navpreet

AU - Morrison, Douglas J

AU - Preston, Tom

AU - Tedford, Catriona

AU - Fizpatrick, Julie

AU - Irani, Cherag

AU - Busza, Albert

AU - Garcia-Perez, Isabel

AU - Fountana, Sofia

AU - Holmes, Elaine

AU - Goldstone, Anthony P

AU - Frost, Gary S

PY - 2016/5/11

Y1 - 2016/5/11

N2 - 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.

AB - 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.

U2 - 10.3945/ajcn.115.126706

DO - 10.3945/ajcn.115.126706

M3 - Article

JO - The American Journal of Clinical Nutrition

JF - The American Journal of Clinical Nutrition

SN - 0909-9859

ER -