High-fat diet acutely affects circadian organisation and eating behavior

Abstract

The organisation of timing in mammalian circadian clocks optimally coordinates behavior and physiology with daily environmental cycles. Chronic consumption of a high-fat diet alters circadian rhythms, but the acute effects on circadian organisation are unknown. To investigate the proximate effects of a high-fat diet on circadian physiology, we examined the phase relationship between central and peripheral clocks in mice fed a high-fat diet for 1 week. By 7 days, the phase of the liver rhythm was markedly advanced (by 5 h), whereas rhythms in other tissues were not affected. In addition, immediately upon consumption of a high-fat diet, the daily rhythm of eating behavior was altered. As the tissue rhythm of the suprachiasmatic nucleus was not affected by 1 week of high-fat diet consumption, the brain nuclei mediating the effect of a high-fat diet on eating behavior are likely to be downstream of the suprachiasmatic nucleus.

Fig. 1

Body weight of mice fed a high-fat diet (HFD) for 1 week. Male heterozygous PER2::LUC mice were single-housed at 7 weeks old and provided with chow ad libitum until 8 weeks old. At 8 weeks old, mice were provided with fresh chow (gray symbols and dotted gray lines; n=7) or a HFD (black symbols and solid black lines; n=7). Body weights, measured at 7, 8, and 9 weeks old, from all individual mice are shown.

Fig. 2

A high-fat diet (HFD) alters the pattern of locomotor activity. Representative double-plotted actograms (5-min bins) of male heterozygous PER2::LUC mice maintained in a 12-h light/12-h dark cycle (light and dark indicated by black and white bars, respectively, above actograms). General activity was continuously monitored with passive infrared sensors. All mice were provided with chow ad libitum for the first week. After 1 week, chow was replaced with either fresh chow (A) or a HFD (B). The times when food was replaced are indicated by asterisks on the left halves of the actograms. The arrows indicate when the mice were removed from the light-tight boxes for tissue culture. The actograms shown are typical examples from a total of chow (n=7, HFD: n=7 mice).

Fig. 3

Effects of a high-fat diet (HFD) on tissue bioluminescence rhythms. Bioluminescence (x-axis: counts/s) recorded from tissue explants prepared from male heterozygous PER2::LUC mice fed either chow (A, C, E, G, I, K, M and O) or a HFD (45% kcal from fat; B, D, F, H, J, L, N and P) for 1 week. The lighting condition of the previous light/dark cycle is indicated for the first day; open bars are light and black bars are dark. WAT, white adipose tissue.

Fig. 4

A high-fat diet (HFD) alters circadian organization. Male heterozygous PER2::LUC mice were fed either chow (gray circles) or HFD (black circles) for 1 week. The mean (±SD) phases were determined from the peaks of PER2::LUC expression during the interval between 12 and 36 h in culture and were plotted relative to the time of last lights on where 24 h is lights on and 36 h is lights off (black and white bar at top). The sample size is shown (number of rhythmic tissues/number of tissues tested). Tissues were taken from the mice shown in Fig. 1, except the aorta, which was collected from only half of the mice. *p=0.02; ***p=0.001. WAT, white adipose tissue.

Fig. 5

The eating behavior rhythm is altered by a high-fat diet (HFD). Single-plotted actograms (1-min bins; maximum 1 count/bin; x-axis: time in h; y-axis: days) of eating events (A, E, I and M) and locomotor activity (C, G, K and O) from male wild-type mice maintained in a 12-h light/12-h dark cycle (light and dark indicated by black and white bars, respectively, above actograms). Eating behavior (scored from video collected by infrared camera) and general activity (monitored with passive infrared sensors) were simultaneously collected from the same mouse. On day 0, the mouse was singly housed and provided with chow ad libitum. On day 3, chow was replaced with a HFD (~2.5 h before lights off, indicated by asterisks on the actograms). Circular histograms (plotted in 2.5° bins) show the distribution of eating events (B, F, J and N; scale: inner circle, 0; middle circle, 4.5; outer circle, 9) and activity events (D, H, L and P; scale: inner circle, 0; middle circle, 6.5; outer circle, 13) for each mouse during chow (left panels, day 2 of actogram) and a HFD (right panels, day 4 of actogram) consumption relative to the time of day (where ZT0 is lights on and ZT12 is lights off). The mean vectors are reported in