The effects of high-intensity exercise on neural responses to images of food

Daniel R Crabtree, Edward S Chambers, Robert M Hardwick, Andrew K Blannin

Research output: Contribution to journalArticle

31 Citations (Scopus)

Abstract

BACKGROUND: Acute bouts of high-intensity exercise modulate peripheral appetite regulating hormones to transiently suppress hunger. However, the effects of physical activity on central appetite regulation have yet to be fully investigated.

OBJECTIVE: We used functional magnetic resonance imaging (fMRI) to compare neural responses to visual food stimuli after intense exercise and rest.

DESIGN: Fifteen lean healthy men [mean ± SD age: 22.5 ± 3.1 y; mean ± SD body mass index (in kg/m(2)): 24.2 ± 2.4] completed two 60-min trials-exercise (EX; running at ∼70% maximum aerobic capacity) and a resting control trial (REST)-in a counterbalanced order. After each trial, an fMRI assessment was completed in which images of high- and low-calorie foods were viewed.

RESULTS: EX significantly suppressed subjective appetite responses while increasing thirst and core-body temperature. Furthermore, EX significantly suppressed ghrelin concentrations and significantly enhanced peptide YY release. Neural responses to images of high-calorie foods significantly increased dorsolateral prefrontal cortex activation and suppressed orbitofrontal cortex (OFC) and hippocampus activation after EX compared with REST. After EX, low-calorie food images increased insula and putamen activation and reduced OFC activation compared with REST. Furthermore, left pallidum activity was significantly elevated after EX when low-calorie images were viewed and was suppressed when high-calorie images were viewed, and these responses correlated significantly with thirst.

CONCLUSIONS: Exercise increases neural responses in reward-related regions of the brain in response to images of low-calorie foods and suppresses activation during the viewing of high-calorie foods. These central responses are associated with exercise-induced changes in peripheral signals related to appetite-regulation and hydration status. This trial was registered at www.clinicaltrials.gov as NCT01926431.

Original languageEnglish
Pages (from-to)258-267
Number of pages10
JournalThe American Journal of Clinical Nutrition
Volume99
Issue number2
Early online date4 Dec 2013
DOIs
Publication statusPublished - Feb 2014

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Exercise
Food
Prefrontal Cortex
Appetite Regulation
Thirst
Ghrelin
Magnetic Resonance Imaging
Peptide YY
Globus Pallidus
Hunger
Putamen
Appetite
Body Temperature
Reward
Running
Hippocampus
Body Mass Index
Brain

Keywords

  • Adolescent
  • Adult
  • Appetite
  • Appetite Regulation
  • Body Mass Index
  • Choice Behavior
  • Cross-Over Studies
  • Energy Intake
  • Exercise
  • Female
  • Food
  • Food Preferences
  • Humans
  • Image Processing, Computer-Assisted
  • Magnetic Resonance Imaging
  • Male
  • Photic Stimulation
  • Prefrontal Cortex
  • Reward
  • Young Adult

Cite this

The effects of high-intensity exercise on neural responses to images of food. / Crabtree, Daniel R; Chambers, Edward S; Hardwick, Robert M; Blannin, Andrew K.

In: The American Journal of Clinical Nutrition, Vol. 99, No. 2, 02.2014, p. 258-267.

Research output: Contribution to journalArticle

Crabtree, Daniel R ; Chambers, Edward S ; Hardwick, Robert M ; Blannin, Andrew K. / The effects of high-intensity exercise on neural responses to images of food. In: The American Journal of Clinical Nutrition. 2014 ; Vol. 99, No. 2. pp. 258-267.
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abstract = "BACKGROUND: Acute bouts of high-intensity exercise modulate peripheral appetite regulating hormones to transiently suppress hunger. However, the effects of physical activity on central appetite regulation have yet to be fully investigated.OBJECTIVE: We used functional magnetic resonance imaging (fMRI) to compare neural responses to visual food stimuli after intense exercise and rest.DESIGN: Fifteen lean healthy men [mean ± SD age: 22.5 ± 3.1 y; mean ± SD body mass index (in kg/m(2)): 24.2 ± 2.4] completed two 60-min trials-exercise (EX; running at ∼70{\%} maximum aerobic capacity) and a resting control trial (REST)-in a counterbalanced order. After each trial, an fMRI assessment was completed in which images of high- and low-calorie foods were viewed.RESULTS: EX significantly suppressed subjective appetite responses while increasing thirst and core-body temperature. Furthermore, EX significantly suppressed ghrelin concentrations and significantly enhanced peptide YY release. Neural responses to images of high-calorie foods significantly increased dorsolateral prefrontal cortex activation and suppressed orbitofrontal cortex (OFC) and hippocampus activation after EX compared with REST. After EX, low-calorie food images increased insula and putamen activation and reduced OFC activation compared with REST. Furthermore, left pallidum activity was significantly elevated after EX when low-calorie images were viewed and was suppressed when high-calorie images were viewed, and these responses correlated significantly with thirst.CONCLUSIONS: Exercise increases neural responses in reward-related regions of the brain in response to images of low-calorie foods and suppresses activation during the viewing of high-calorie foods. These central responses are associated with exercise-induced changes in peripheral signals related to appetite-regulation and hydration status. This trial was registered at www.clinicaltrials.gov as NCT01926431.",
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author = "Crabtree, {Daniel R} and Chambers, {Edward S} and Hardwick, {Robert M} and Blannin, {Andrew K}",
note = "We thank Stuart Derbyshire for granting us the fMRI scanning time required to conduct this study. We also thank Nina Salman for conducting the fMRI scanning and Charnjit Sindu for providing assistance with the fMRI data analysis. Finally, we thank the volunteers for participating in this study. The authors’ responsibilities were as follows—DRC: contributed to the research design, conducted the data collection, analyzed the data, wrote the manuscript, and had primary responsibility for the final content; ESC: conceived the study, contributed to the research design, contributed to the data collection, provided essential materials, provided data analysis assistance, and wrote the manuscript; RMH: provided essential materials, contributed to the data analysis, and helped write the manuscript; and AKB: supervised the project, contributed to the research design, conducted the data collection, provided essential materials, provided data, assisted with the analysis, and wrote the manuscript. There were no conflicts of interest reported.",
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AU - Crabtree, Daniel R

AU - Chambers, Edward S

AU - Hardwick, Robert M

AU - Blannin, Andrew K

N1 - We thank Stuart Derbyshire for granting us the fMRI scanning time required to conduct this study. We also thank Nina Salman for conducting the fMRI scanning and Charnjit Sindu for providing assistance with the fMRI data analysis. Finally, we thank the volunteers for participating in this study. The authors’ responsibilities were as follows—DRC: contributed to the research design, conducted the data collection, analyzed the data, wrote the manuscript, and had primary responsibility for the final content; ESC: conceived the study, contributed to the research design, contributed to the data collection, provided essential materials, provided data analysis assistance, and wrote the manuscript; RMH: provided essential materials, contributed to the data analysis, and helped write the manuscript; and AKB: supervised the project, contributed to the research design, conducted the data collection, provided essential materials, provided data, assisted with the analysis, and wrote the manuscript. There were no conflicts of interest reported.

PY - 2014/2

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N2 - BACKGROUND: Acute bouts of high-intensity exercise modulate peripheral appetite regulating hormones to transiently suppress hunger. However, the effects of physical activity on central appetite regulation have yet to be fully investigated.OBJECTIVE: We used functional magnetic resonance imaging (fMRI) to compare neural responses to visual food stimuli after intense exercise and rest.DESIGN: Fifteen lean healthy men [mean ± SD age: 22.5 ± 3.1 y; mean ± SD body mass index (in kg/m(2)): 24.2 ± 2.4] completed two 60-min trials-exercise (EX; running at ∼70% maximum aerobic capacity) and a resting control trial (REST)-in a counterbalanced order. After each trial, an fMRI assessment was completed in which images of high- and low-calorie foods were viewed.RESULTS: EX significantly suppressed subjective appetite responses while increasing thirst and core-body temperature. Furthermore, EX significantly suppressed ghrelin concentrations and significantly enhanced peptide YY release. Neural responses to images of high-calorie foods significantly increased dorsolateral prefrontal cortex activation and suppressed orbitofrontal cortex (OFC) and hippocampus activation after EX compared with REST. After EX, low-calorie food images increased insula and putamen activation and reduced OFC activation compared with REST. Furthermore, left pallidum activity was significantly elevated after EX when low-calorie images were viewed and was suppressed when high-calorie images were viewed, and these responses correlated significantly with thirst.CONCLUSIONS: Exercise increases neural responses in reward-related regions of the brain in response to images of low-calorie foods and suppresses activation during the viewing of high-calorie foods. These central responses are associated with exercise-induced changes in peripheral signals related to appetite-regulation and hydration status. This trial was registered at www.clinicaltrials.gov as NCT01926431.

AB - BACKGROUND: Acute bouts of high-intensity exercise modulate peripheral appetite regulating hormones to transiently suppress hunger. However, the effects of physical activity on central appetite regulation have yet to be fully investigated.OBJECTIVE: We used functional magnetic resonance imaging (fMRI) to compare neural responses to visual food stimuli after intense exercise and rest.DESIGN: Fifteen lean healthy men [mean ± SD age: 22.5 ± 3.1 y; mean ± SD body mass index (in kg/m(2)): 24.2 ± 2.4] completed two 60-min trials-exercise (EX; running at ∼70% maximum aerobic capacity) and a resting control trial (REST)-in a counterbalanced order. After each trial, an fMRI assessment was completed in which images of high- and low-calorie foods were viewed.RESULTS: EX significantly suppressed subjective appetite responses while increasing thirst and core-body temperature. Furthermore, EX significantly suppressed ghrelin concentrations and significantly enhanced peptide YY release. Neural responses to images of high-calorie foods significantly increased dorsolateral prefrontal cortex activation and suppressed orbitofrontal cortex (OFC) and hippocampus activation after EX compared with REST. After EX, low-calorie food images increased insula and putamen activation and reduced OFC activation compared with REST. Furthermore, left pallidum activity was significantly elevated after EX when low-calorie images were viewed and was suppressed when high-calorie images were viewed, and these responses correlated significantly with thirst.CONCLUSIONS: Exercise increases neural responses in reward-related regions of the brain in response to images of low-calorie foods and suppresses activation during the viewing of high-calorie foods. These central responses are associated with exercise-induced changes in peripheral signals related to appetite-regulation and hydration status. This trial was registered at www.clinicaltrials.gov as NCT01926431.

KW - Adolescent

KW - Adult

KW - Appetite

KW - Appetite Regulation

KW - Body Mass Index

KW - Choice Behavior

KW - Cross-Over Studies

KW - Energy Intake

KW - Exercise

KW - Female

KW - Food

KW - Food Preferences

KW - Humans

KW - Image Processing, Computer-Assisted

KW - Magnetic Resonance Imaging

KW - Male

KW - Photic Stimulation

KW - Prefrontal Cortex

KW - Reward

KW - Young Adult

U2 - 10.3945/ajcn.113.071381

DO - 10.3945/ajcn.113.071381

M3 - Article

VL - 99

SP - 258

EP - 267

JO - The American Journal of Clinical Nutrition

JF - The American Journal of Clinical Nutrition

SN - 0002-9165

IS - 2

ER -