Aerobic exercise modulates anticipatory reward processing via the μ-opioid receptor system

Abstract

Physical exercise modulates food reward and helps control body weight. The endogenous µ-opioid receptor (MOR) system is involved in rewarding aspects of both food and physical exercise, yet interaction between endogenous opioid release following exercise and anticipatory food reward remains unresolved. Here we tested whether exercise-induced opioid release correlates with increased anticipatory reward processing in humans. We scanned 24 healthy lean men after rest and after a 1 h session of aerobic exercise with positron emission tomography (PET) using MOR-selective radioligand [¹¹ C]carfentanil. After both PET scans, the subjects underwent a functional magnetic resonance imaging (fMRI) experiment where they viewed pictures of palatable versus nonpalatable foods to trigger anticipatory food reward responses. Exercise-induced changes in MOR binding in key regions of reward circuit (amygdala, thalamus, ventral and dorsal striatum, and orbitofrontal and cingulate cortices) were used to predict the changes in anticipatory reward responses in fMRI. Exercise-induced changes in MOR binding correlated negatively with the exercise-induced changes in neural anticipatory food reward responses in orbitofrontal and cingulate cortices, insula, ventral striatum, amygdala, and thalamus: higher exercise-induced opioid release predicted higher brain responses to palatable versus nonpalatable foods. We conclude that MOR activation following exercise may contribute to the considerable interindividual variation in food craving and consumption after exercise, which might promote compensatory eating and compromise weight control.

Keywords: brain imaging; food reward; opioid release; physical exercise.

Figure 1

Timeline for experimental sessions. Subjects underwent two PET and fMRI scans on separate days: after rest and after exercise. The order of the scans was counterbalanced across subjects. Affective and perceptual responses were measured at the beginning of each session and after the scans and additionally during and after exercise. Changes in BP_ND (exercise minus rest) measured with PET were used to predict changes in BOLD (exercise minus rest) measured with fMRI. RPE, rating of perceived exertion; PANAS, positive and negative affect schedule; VAS, visual analogue scale; PSQ, perceived stress questionnaire [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 2

Experimental design for fMRI. Participants viewed alternating 15.75 s epochs with palatable foods, nonpalatable foods, or cars. Each block contained 6 stimuli from one category, intermixed with fixation crosses [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 3

(a) Brain regions where BOLD‐fMRI responses were larger (orange) and smaller (blue) when viewing foods versus cars. (b) Brain regions where BOLD‐fMRI responses were larger (orange) and smaller (blue) when viewing palatable versus nonpalatable foods. The data are thresholded at p < .01, FDR corrected at cluster level [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 4

Exercise‐induced reduction in fullness (a) and increase in prospective food consumption (b) as well as higher mean rating of perceived exertion during exercise (c) and increased positive affect after exercise (d) predicted higher responses to palatable versus nonpalatable foods in exercise compared with rest (p < .05, FDR corrected). The scatterplots show least‐square regression lines with 95% confidence intervals and are shown for visual purposes only, statistical inference is based on the full‐volume SPM analysis

Figure 5

Higher self‐reported physical activity minutes per week (a) and higher maximal oxygen uptake (b) predicted lower responses to foods versus cars in exercise compared with rest (p < .05, FDR corrected). The scatterplots show least‐square regression lines with 95% confidence intervals and are shown for visual purposes only, statistical inference is based on the full‐volume SPM analysis

Figure 6

Cumulative maps showing the number of ROIs (out of 10) whose [¹¹C]carfentanil BP_ND was correlated (p < .05, FDR corrected) with BOLD responses to (a) palatable versus nonpalatable foods between exercise and rest conditions and to (b) foods versus cars between exercise and rest conditions [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 7

Brain regions where exercise‐induced change in thalamic MOR availability is associated with the difference in BOLD‐fMRI responses to palatable versus nonpalatable foods between exercise and rest conditions (a), and where exercise‐induced change in MOR availability in dorsal caudate is associated with the difference in BOLD‐fMRI responses to palatable versus nonpalatable foods between exercise and rest conditions (b). The scatterplots show least‐square regression lines with 95% confidence intervals and are shown for visual purposes only, statistical inference is based on the full‐volume SPM analysis [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 8

Whole‐brain exploratory analysis revealed that exercise‐induced change in MOR binding correlated negatively with increased hunger (a) and prospective food consumption (b) and positively with decreased fullness (c) and satiety (d). Negative change in BP_ND is consistent with increased endogenous opioid release. The scatterplots show least‐square regression lines with 95% confidence intervals and are shown for visual purposes only, statistical inference is based on the full‐volume SPM analysis