Entrainment of the human circadian clock to the natural light-dark cycle

Abstract

The electric light is one of the most important human inventions. Sleep and other daily rhythms in physiology and behavior, however, evolved in the natural light-dark cycle [1], and electrical lighting is thought to have disrupted these rhythms. Yet how much the age of electrical lighting has altered the human circadian clock is unknown. Here we show that electrical lighting and the constructed environment is associated with reduced exposure to sunlight during the day, increased light exposure after sunset, and a delayed timing of the circadian clock as compared to a summer natural 14 hr 40 min:9 hr 20 min light-dark cycle camping. Furthermore, we find that after exposure to only natural light, the internal circadian clock synchronizes to solar time such that the beginning of the internal biological night occurs at sunset and the end of the internal biological night occurs before wake time just after sunrise. In addition, we find that later chronotypes show larger circadian advances when exposed to only natural light, making the timing of their internal clocks in relation to the light-dark cycle more similar to earlier chronotypes. These findings have important implications for understanding how modern light exposure patterns contribute to late sleep schedules and may disrupt sleep and circadian clocks.

Figure 1. Experimental protocol from one participant

Data represent recordings from the Actiwatch-L recorder with activity denoted by black ticks and light exposure above ~1000 lux threshold denoted in yellow. Data are double plotted, with successive days plotted both next to and beneath each other and clock hour is indicated on the abscissa. Light-dark cycle (open and closed bars) on the top abscissa denotes approximate sunrise and sunset times. Sleep episodes are characterized by low activity levels. Exposure to electrical and natural lighting and sleep timing while the participant continued to live in their work-home-social constructed environment are shown on days 1–7. The initial assessment of internal circadian phase occurred on days 8–9 in the laboratory denoted by blue shading. After one night of sleep at home, exposure to the natural light-dark cycle while camping and associated sleep times occurred on days 10–16. On the last day of camping (day 16) subjects were driven directly to the laboratory for follow-up assessment of internal circadian phase on days 16–17. Conditions were sequential so that that sunrise and sunset times would be as similar as possible between conditions.

Figure 2. Light exposure

Average light exposure (lux) plotted on a log scale during the week of exposure to electrical lighting in the constructed environment and exposure to the natural light-dark cycle while camping. Data are double plotted so that light levels across midnight (24h local clock time) can be more easily observed. For reference, one lux is equivalent to the light exposure received by the eye when gazing at a candle 1m away, moonlight is ~0.1 lux, typical indoor lighting is ~200 lux, sunrise or sunset is ~10,000 lux and looking at a bright blue midday sky is >100,000 lux.

Figure 3. Circadian and sleep timing

Timing of the average melatonin onset (black upward triangles), melatonin midpoint (red squares), and melatonin offset (blue downward triangles) after a week of exposure to electrical lighting in the constructed environment versus exposure to the natural light-dark cycle while camping. Average sunrise and sunset times are provided for the ~two week study. Average sunrise time occurred 11 minutes later and sunset 4 minutes earlier during the week of camping as compared to the week of electrical lighting. Sleep start and wake times are presented as average times during each week. Error bars represent ± standard deviations. We did not observe a change in the duration of the melatonin rhythm defined by the time between melatonin onset and offset (p=0.66, two tailed). Exposure to longer dark episodes, as occur naturally at latitudes away from the equator during winter are likely necessary to expand the duration of the melatonin rhythm[17,18]. Larger differences in circadian timing during exposures to the electrical lighting-constructed environment versus natural light than that observed in our midsummer study may also be expected during winter.

Figure 4. Association between chronotype and circadian timing and the change in circadian timing

Chronotypes derived from the Morningness-Eveningness Questionnaire (MEQ)[27] and the Munich Chronotype Questionnaire (MCTQ)[28,29] were significantly correlated (r=−0.96, p<0.001, two-tailed). Associations between chronotype scores and circadian phase were similar regardless of the chronotype measure used, therefore we present data from the MCTQ using the timing of midsleep on free days corrected (MSFsc)[28]. After exposure to electrical lighting,. we found a strong association between chronotype and the timing of the DLMO_25% (Panel A; r=0.83, p=0.01, two-tailed). After exposure to natural light however, no significant association between chronotype and circadian timing was observed (Panel B; r=0.42, p=0.28, two-tailed) likely due to a reduction in variance of the clock hour of the DLMO_25% in the stronger zeitgeber of the natural light-dark cycle. Chronotype was significantly correlated with the change in DLMO_25%, (Panel C; r=0.75, p=0.031, two-tailed) such that participants with later chronotypes, denoted by later clock times of the MSFsc, showed larger advances in the timing of their DLMO_25%. On average, for every hour of MSFsc chronotype under electrical lighting conditions, DLMO_25% moved 0.83 hours earlier after exposure to natural light. Symbols represent individual subjects and positive values indicate advances in the DLMO_25% in hours. The solid line represents a linear fit of the data and the dashed line represents sunset.