Light at night increases body mass by shifting the time of food intake

Abstract

The global increase in the prevalence of obesity and metabolic disorders coincides with the increase of exposure to light at night (LAN) and shift work. Circadian regulation of energy homeostasis is controlled by an endogenous biological clock that is synchronized by light information. To promote optimal adaptive functioning, the circadian clock prepares individuals for predictable events such as food availability and sleep, and disruption of clock function causes circadian and metabolic disturbances. To determine whether a causal relationship exists between nighttime light exposure and obesity, we examined the effects of LAN on body mass in male mice. Mice housed in either bright (LL) or dim (DM) LAN have significantly increased body mass and reduced glucose tolerance compared with mice in a standard (LD) light/dark cycle, despite equivalent levels of caloric intake and total daily activity output. Furthermore, the timing of food consumption by DM and LL mice differs from that in LD mice. Nocturnal rodents typically eat substantially more food at night; however, DM mice consume 55.5% of their food during the light phase, as compared with 36.5% in LD mice. Restricting food consumption to the active phase in DM mice prevents body mass gain. These results suggest that low levels of light at night disrupt the timing of food intake and other metabolic signals, leading to excess weight gain. These data are relevant to the coincidence between increasing use of light at night and obesity in humans.

Fig. 1.

Body mass, fat pad mass, and glucose tolerance were altered in mice exposed to bright or dim light at night. (A) Weekly body mass for mice throughout the study (*P ≤ 0.05 when LD differs from both LL and DM groups; ^&P ≤ 0.05 between all groups). Mice exposed to light at night had elevated body mass beginning 1 wk after placement in experimental light conditions and continuing throughout the remainder of the study. (B) Body mass gain and epididymal fat pad mass differed among groups at the conclusion of the study, suggesting increases in body mass may be caused by changes in body fat composition. (C) Mice exposed to either DM or LL had reduced glucose tolerance, and DM and LL mice failed to recover blood glucose as rapidly as LD mice (*P ≤ 0.05 when LD differs from both LL and DM groups; ⁺P ≤ 0.05 when glucose level is higher in the DM group than in the LD group). (D) Body mass at the time of the GTT correlated positively with final blood glucose levels.

Fig. 2.

Representative activity records from mice held in (A) LD, (B) DM, and (C) LL conditions. Home cage locomotor activity was measured by intersecting infrared beams and is shown in a double-plotted actogram. Mice in LL conditions became arrhythmic, but mice in DM conditions maintained rhythmicity. (D) All mice had equivalent total 24-h activity (P > 0.05).

Fig. 3.

(A) Serum corticosterone concentrations were reduced in LL mice but not in DM mice at the two time points measured, suggesting that glucocorticoids did not mediate the changes in body mass (*P ≤ 0.05 from LL and DM). (B) Mice exposed to LL and DM conditions ate more food during the light phase than during the dark phase, behavior that is atypical in nocturnal animals (*P ≤ 0.05). (C and D) Body mass (C) and blood glucose levels (D) are associated with percentage of daytime food consumption. (C) Percentage of food consumed during the day correlated with final blood glucose levels obtained in the GTT. (D) Body mass at the conclusion of the study correlated positively with percentage of daytime food intake.

Fig. 4.

Body mass gain and epididymal fat pad mass differed among groups at the conclusion of the study. (A) Total body mass gain and (B) epididymal fat pad mass (#P ≤ 0.05 when group differs from LD; ^†P ≤ 0.05 when FD differs from both FA and FL). Timed feeding during the dark in mice exposed to LAN prevented increased weight gain and elevated epididymal fat pad mass. (C) Serum corticosterone concentrations are altered by timed feeding. Feeding mice during the dark resulted in increased corticosterone concentrations at Zeitgeber time (ZT) 16, irrespective of light condition (*P ≤ 0.05 when FD differs from FA and FL).