Circadian Entrainment to the Natural Light-Dark Cycle across Seasons and the Weekend

Abstract

Reduced exposure to daytime sunlight and increased exposure to electrical lighting at night leads to late circadian and sleep timing [1-3]. We have previously shown that exposure to a natural summer 14 hr 40 min:9 hr 20 min light-dark cycle entrains the human circadian clock to solar time, such that the internal biological night begins near sunset and ends near sunrise [1]. Here we show that the beginning of the biological night and sleep occur earlier after a week's exposure to a natural winter 9 hr 20 min:14 hr 40 min light-dark cycle as compared to the modern electrical lighting environment. Further, we find that the human circadian clock is sensitive to seasonal changes in the natural light-dark cycle, showing an expansion of the biological night in winter compared to summer, akin to that seen in non-humans [4-8]. We also show that circadian and sleep timing occur earlier after spending a weekend camping in a summer 14 hr 39 min:9 hr 21 min natural light-dark cycle compared to a typical weekend in the modern environment. Weekend exposure to natural light was sufficient to achieve ∼69% of the shift in circadian timing we previously reported after a week's exposure to natural light [1]. These findings provide evidence that the human circadian clock adapts to seasonal changes in the natural light-dark cycle and is timed later in the modern environment in both winter and summer. Further, we demonstrate that earlier circadian timing can be rapidly achieved through natural light exposure during a weekend spent camping.

Keywords: advance; circadian phase; delay; non-visual; photoperiod; physiology; scotophase; spectral; spectrum; wavelength.

Figure 1. Winter Light Exposure

Average white light exposure and light of different wavelengths during the week of exposure to (A and B) electrical and natural lighting in the modern environment and exposure to (A and C) only natural light during the week spent camping. Exposure to longer wavelength red light of campfires can be seen in (C). Data are represented as mean on a log scale and are double plotted so light levels can be seen across midnight (24 hr local time). See also Figure S1A and Table S1.

Figure 2. Winter Circadian and Sleep Timing

Average timing of melatonin onset (black upward triangles), midpoint (red squares), and offset (blue downward triangles) following one week exposure to electrical and natural lighting in the modern environment versus following one week exposure to only natural light while camping. Average sunrise and sunset times for the ~2 week study are denoted by vertical black lines. Average sleep start and end times are indicated by the black bar for each week. Clock time = local time. Data are represented as mean ± SD. See also Figures S1–S3.

Figure 3. Melatonin Circadian Phase During Summer and Winter Relative to Solar Darkness

Average timing of melatonin onset (black upward triangles), midpoint (red squares), and offset (blue downward triangles) following ~one week exposure to electrical and natural lighting in the modern environment or only natural light after camping during summer versus winter. The summer data shown are from our previous study [1]. Clock time = standard time. Timing of solar darkness (scotophase) is represented by black bars. Data are represented as mean ± SD.

Figure 4. Summer Circadian and Sleep Timing - Weekend

Average timing of melatonin onset (black upward triangles), midpoint (red squares), and offset (blue downward triangles) after two weekdays exposure to electrical and natural lighting in the modern environment and following two weekend days exposure to electrical and natural light in the modern environment or two weekend days exposure to natural light while camping. Average sunrise and sunset times for the study are denoted by vertical black lines. Average sleep start and end times are indicated by the black bar for each weekday and weekend part of the study. Clock time = local time. Data are represented as mean ± SD. See also Figures S1–S4 and Table S2.