Abstract
Consumption of high-fat diet acutely alters the daily rhythm of eating behavior and circadian organization (the phase relationship between oscillators in central and peripheral tissues) in mice. Voluntary wheel-running activity counteracts the obesogenic effects of high-fat diet and also modulates circadian rhythms in mice. In this study, we sought to determine whether voluntary wheel-running activity could prevent the proximate effects of high-fat diet consumption on circadian organization and behavioral rhythms in mice. Mice were housed with locked or freely rotating running wheels and fed chow or high-fat diet for 1 week and rhythms of locomotor activity, eating behavior, and molecular timekeeping (PERIOD2::LUCIFERASE luminescence rhythms) in ex vivo tissues were measured. Wheel-running activity delayed the phase of the liver rhythm by 4 h in both chow- and high-fat diet-fed mice. The delayed liver phase was specific to wheel-running activity since an enriched environment without the running wheel did not alter the phase of the liver rhythm. In addition, wheel-running activity modulated the effect of high-fat diet consumption on the daily rhythm of eating behavior. While high-fat diet consumption caused eating events to be more evenly dispersed across the 24 h-day in both locked-wheel and wheel-running mice, the effect of high-fat diet was much less pronounced in wheel-running mice. Together these data demonstrate that wheel-running activity is a salient factor that modulates liver phase and eating behavior rhythms in both chow- and high-fat-diet fed mice. Wheel-running activity in mice is both a source of exercise and a self-motivating, rewarding behavior. Understanding the putative reward-related mechanisms whereby wheel-running activity alters circadian rhythms could have implications for human obesity since palatable food and exercise may modulate similar reward circuits.
Highlights
Circadian rhythms of physiology and behavior have endogenous ∼24-h periods that synchronize to environmental cycles of light/dark and food availability (Takahashi et al, 2001)
Voluntary wheel-running activity prevents the obesogenic effects of high-fat diet in mice (Krawczewski Carhuatanta et al, 2011)
We previously showed that after one week of HFD consumption, mice experienced a 10% increase in body mass, the phase of their liver clock was advanced by 5 h, and their eating behavior rhythm was less robust (Pendergast et al, 2013)
Summary
Circadian rhythms of physiology and behavior have endogenous ∼24-h periods that synchronize to environmental cycles of light/dark and food availability (Takahashi et al, 2001). Changes in environmental cycles of light/dark and timing of food intake, such as occurs with transmeridian air travel or rotating shift-work, induces internal desynchronization of circadian clocks so that physiological and behavioral rhythms are no longer optimally tuned to environmental conditions (Yamazaki et al, 2000). We recently investigated the proximate effects of high-fat diet consumption on daily rhythms of behavior and on the phase relationship between tissue oscillators in mice (i.e., circadian organization). We measured the phases of the circadian gene fusion protein reporter rhythms [PERIOD2::LUCIFERASE (PER2::LUC)] in explanted tissues and found that most tissue clocks, including the SCN, arcuate nucleus of the hypothalamus, and white adipose tissue, are resistant to the acute effects of high-fat diet consumption (Pendergast et al, 2013). In addition to the alteration of the liver rhythm, the daily rhythm of eating behavior is immediately altered by high-fat diet as eating events become uniformly distributed across the day and night
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