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. 2017 Feb 6;27(3):423-430.
doi: 10.1016/j.cub.2016.12.009. Epub 2017 Jan 19.

Increases in Physical Activity Result in Diminishing Increments in Daily Energy Expenditure in Mice

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Free PMC article

Increases in Physical Activity Result in Diminishing Increments in Daily Energy Expenditure in Mice

Timothy J O'Neal et al. Curr Biol. .
Free PMC article

Abstract

Exercise is a common component of weight loss strategies, yet exercise programs are associated with surprisingly small changes in body weight [1-4]. This may be due in part to compensatory adaptations, in which calories expended during exercise are counteracted by decreases in other aspects of energy expenditure [1, 5-10]. Here we examined the relationship between a rodent model of voluntary exercise- wheel running- and total daily energy expenditure. Use of a running wheel for 3 to 7 days increased daily energy expenditure, resulting in a caloric deficit of ∼1 kcal/day; however, total daily energy expenditure remained stable after the first week of wheel access, despite further increases in wheel use. We hypothesized that compensatory mechanisms accounted for the lack of increase in daily energy expenditure after the first week. Supporting this idea, we observed a decrease in off-wheel ambulation when mice were using the wheels, indicating behavioral compensation. Finally, we asked whether individual variation in wheel use within a group of mice would be associated with different levels of daily energy expenditure. Despite a large variation in wheel running, we did not observe a significant relationship between the amount of daily wheel running and total daily energy expenditure or energy intake across mice. Together, our experiments support a model in which the transition from sedentary to light activity is associated with an increase in daily energy expenditure, but further increases in physical activity produce diminishingly small increments in daily energy expenditure.

Keywords: behavioral compensation; energy expenditure; metabolism; obesity; physical activity; running wheel; voluntary exercise; weight loss; wheel running.

Figures

Figure 1
Figure 1. Short-term wheel running alters energy balance
(A) Experimental design: mice (n = 15) were housed in indirect calorimetry chambers for a baseline phase (3 days; locked wheel) followed by a wheel access phase (3 days; unlocked wheel), and measures were collected throughout in 13 min bins. (B) Mice with regular use of running wheels (5645 ± 1485 wheel turns per day) were included in analyses (n = 10). (C) Energy expenditure (blue, left y-axis) and wheel running (orange, right y-axis) over the baseline and wheel access phases. (D) Total energy expenditure significantly increased by ~5% during the wheel access phase (p = 0.03). (E) Body weight was unchanged over the course of the baseline and wheel access phases (p = 0.10). (F) Respiratory exchange ratio (VCO2:VO2) was slightly but significantly decreased during the wheel access phase (p = 0.003). (G) Daily food intake decreased by ~10% during the wheel access phase (p = 0.005). Data shown as mean ± SEM or mean with individual mice; paired ttest or repeated-measures ANOVA followed by Fisher’s LSD post-hoc; *p < 0.05, **p < 0.01. Raw data for this figure presented in Supplemental tables online.
Figure 2
Figure 2. Changes in energy balance due to wheel running do not persist over time
(A) Experimental design: mice (n = 7) were housed in home cages for a baseline phase (7 days) followed by a wheel access phase (21 days). (B) Energy expenditure (blue, left y-axis) and wheel running (orange, right y-axis) over the baseline and wheel access phases. (C) Wheel running significantly and continually increased throughout the wheel access phase (p = 0.002). (D) Energy expenditure increased upon initial wheel access (p = 0.0096) but did not significantly change over the course of the wheel access phase (p = 0.60). (E) By the end of the wheel access phase, daily food intake was significantly greater than during the baseline phase (p = 0.003). (F) Initial wheel access caused a significant energetic deficit (p = 0.02) that waned over the following weeks of wheel access despite sustained wheel use. (G) Body mass decreased across the experiment (p < 0.0001), which was attributed to a change in fat mass. (H–I) Modeled (H) energy expenditure and (I) respiratory exchange ratio as functions of time. See also Figure S1. Data shown as mean ± SEM (shaded region) or mean with individual mice; paired t-test or repeated-measures ANOVA followed by Bonferroni’s or Fisher’s LSD post-hoc; *p < 0.05; **p < 0.01, ***p < 0.001. Raw data for this figure presented in Supplemental tables online.
Figure 3
Figure 3. Wheel running was associated with an increase in off-wheel physical inactivity
(A) Experimental design: mice (n = 8) were housed in behavioral chambers with ceiling-mounted cameras for a baseline phase (7 days) followed by a wheel phase (21 days). (B) Wheel running increased during the wheel access phase (p = 0.006). (C–D) Neither energy expenditure (p = 0.28) nor daily food intake (p = 0.46) significantly changed as a result of wheel access or use. (E) Body mass did not change significantly across this experiment. (F) Initial wheel access resulted in negative energy balance that reversed over three additional weeks of wheel access (p = 0.002). (G) Representative activity paths from the baseline (top) and wheel access (bottom) phases. During the wheel phase, off-wheel ambulation (green, left y-axis) significantly decreased (p < 0.0001) while wheel running (orange, right y-axis) significantly increased (p = 0.006) over time. Data shown as mean ± SEM; repeated-measures ANOVA followed by Bonferroni’s post-hoc; **p < 0.01, ***p < 0.001. Raw data for this figure presented in Supplemental tables online.
Figure 4
Figure 4. Natural variation in wheel running does not correlate with energy intake or expenditure
(A) Mice (n = 41) had substantial variance in daily wheel running activity. (B–C) Neither energy expenditure nor daily food intake significantly correlated with wheel use. (D–E) Both total body mass and fat mass formed significant inverse relationships with wheel use. (F). Lean mass was not significantly correlated with wheel use. Data shown as mean ± SEM or as individual mice; linear or non-linear regressions. Raw data for this figure presented in Supplemental tables online.

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