Linking Light Exposure and Subsequent Sleep: A Field Polysomnography Study in Humans

Emma J Wams, Tom Woelders, Irene Marring, Laura van Rosmalen, Domien G M Beersma, Marijke C M Gordijn, Roelof A Hut, Emma J Wams, Tom Woelders, Irene Marring, Laura van Rosmalen, Domien G M Beersma, Marijke C M Gordijn, Roelof A Hut

Abstract

Study objectives: To determine the effect of light exposure on subsequent sleep characteristics under ambulatory field conditions.

Methods: Twenty healthy participants were fitted with ambulatory polysomnography (PSG) and wrist-actigraphs to assess light exposure, rest-activity, sleep quality, timing, and architecture. Laboratory salivary dim-light melatonin onset was analyzed to determine endogenous circadian phase.

Results: Later circadian clock phase was associated with lower intensity (R2 = 0.34, χ2(1) = 7.19, p < .01), later light exposure (quadratic, controlling for daylength, R2 = 0.47, χ2(3) = 32.38, p < .0001), and to later sleep timing (R2 = 0.71, χ2(1) = 20.39, p < .0001). Those with later first exposure to more than 10 lux of light had more awakenings during subsequent sleep (controlled for daylength, R2 = 0.36, χ2(2) = 8.66, p < .05). Those with later light exposure subsequently had a shorter latency to first rapid eye movement (REM) sleep episode (R2 = 0.21, χ2(1) = 5.77, p < .05). Those with less light exposure subsequently had a higher percentage of REM sleep (R2 = 0.43, χ2(2) = 13.90, p < .001) in a clock phase modulated manner. Slow-wave sleep accumulation was observed to be larger after preceding exposure to high maximal intensity and early first light exposure (p < .05).

Conclusions: The quality and architecture of sleep is associated with preceding light exposure. We propose that light exposure timing and intensity do not only modulate circadian-driven aspects of sleep but also homeostatic sleep pressure. These novel ambulatory PSG findings are the first to highlight the direct relationship between light and subsequent sleep, combining knowledge of homeostatic and circadian regulation of sleep by light. Upon confirmation by interventional studies, this hypothesis could change current understanding of sleep regulation and its relationship to prior light exposure.

Clinical trial details: This study was not a clinical trial. The study was ethically approved and nationally registered (NL48468.042.14).

Keywords: actigraphy; chronobiology; circadian rhythms; scoring; sleep/wake mechanisms.

© Sleep Research Society 2017. Published by Oxford University Press [on behalf of the Sleep Research Society].

Figures

Figure 1
Figure 1
Study design representation. Timeline shows the two assessment periods (rest–activity; and PSG). Light measurements are shown in yellow with subsequent rest periods (blue) and sleep periods (green). The first half of the timeline indicates a week of rest–activity measurements with light and subsequent sleep comparisons indicated by the red arrows. All daily comparisons of light and subsequent sleep were included in the analyses controlling for subject. After this rest–activity measurement period, a salivary melatonin collection was conducted to determine subject’s DLMO (grey). Following this, there was a period of no assessments lasting at least 1 week dependent on the subject’s randomization of a Wednesday or Saturday first PSG assessment night (dashed lines). The two PSG recordings are shown in green and each was compared with the preceding light exposure (indicated by blue arrows).
Figure 2
Figure 2
Example of original activity and light data trace. Data were obtained from an intermediate chronotype participant with a DLMO of 19.5 hours. Top panel: Log transformed light intensity data (black lines indicate intensity per minute bin) with harmonic regression sine function (dashed line) plotted for the first week. Bottom panel: black lines indicate activity counts per minute, divided by 1000.
Figure 3
Figure 3
Relationships between dim-light melatonin onset, light exposure, and sleep timing. (A) Higher maximal fitted light intensity exposure was related to earlier DLMO timing. (B) In a curvi-linear fashion, later DLMO was generally related to later time of first exposure to >10 lux when accounting for differences in daylength (model prediction: black line, standard error of mixed model: grey range). (C) Later DLMO timing was related to later sleep onset.
Figure 4
Figure 4
Light exposure and its relationship to subsequent sleep disturbances. (A) Later first exposure to more than 10 lux was related to increased sleep disturbance (number of awakenings per hour), when controlling for daylength (model prediction: black line, standard error of mixed model: grey range). (B) Higher maximal light intensities during the day were followed by more sleep disturbances (number of awakenings per hour TST) within DLMO timing groups (DLMO) timing (red: DLMO > 21 hours, orange: 19 hours ≤ DLMO ≤ 21 hours, green: DLMO

Figure 5

Light exposure and subsequent sleep…

Figure 5

Light exposure and subsequent sleep architecture. (A) Shorter latencies to first REM sleep…

Figure 5
Light exposure and subsequent sleep architecture. (A) Shorter latencies to first REM sleep episode were associated with preceding later timing to first exposure to more than 10 lux (black circles indicate average values of two PSG recordings and of the same 2 days of light recordings and dashed line indicates model fit) and (B) later preceding timing of maximal light exposure. (C) A lower percentage of REM sleep was associated with higher preceding maximal light intensities (model prediction: black line, standard error of mixed model: grey range). This relationship was modulated by DLMO timing, though all DLMO timing categories showed the same relationship (red: DLMO > 21 hours, orange: 19 hours ≤ DLMO ≤ 21 hours, green: DLMO

Figure 6

Sleep stage accumulation related to…

Figure 6

Sleep stage accumulation related to preceding maximal light exposure intensity. (A) SWS accumulation…

Figure 6
Sleep stage accumulation related to preceding maximal light exposure intensity. (A) SWS accumulation was higher throughout the sleep period in individuals previously exposed to higher maximal light intensities (p < .05). (B) REM sleep accumulation was lower in individuals previously exposed to higher maximal light intensities (p < .05). (C) Wake accumulation was significantly lower at the beginning of the sleep period in individuals previously exposed to higher maximal light intensities (p < .05). In all graphs, line at top indicates a significant difference between groups at that time percentage of total sleep, p < .05.

Figure 7

Subsequent sleep stage accumulation related…

Figure 7

Subsequent sleep stage accumulation related to timing of first exposure to more than…

Figure 7
Subsequent sleep stage accumulation related to timing of first exposure to more than 10 lux. (A) SWS accumulation was higher in individuals that previously had earlier first exposure to > 10 lux (p < .05). (B) REM sleep accumulation was lower in individuals that previously had earlier first exposure to >10 lux (p < .05). (C) Wake accumulation was significantly lower throughout the sleep period in individuals that previously had earlier first exposure to >10 lux (p < .05). In all graphs, line at top indicates a significant difference between groups at that time percentage of total sleep, p < .05.
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    1. Daan S, Hut RA. Circadian Clock, Program, Oscillator, Pacemaker, Synchroniser? In: Honma K, Honma S, eds. Circadian Clocks. Hokkaido University Press; 2016:21–32.
    1. Berson DM, Dunn FA, Takao M. Phototransduction by retinal ganglion cells that set the circadian clock. Science. 2002; 295(5557): 1070–1073. - PubMed
    1. Khalsa SB, Jewett ME, Cajochen C, Czeisler CA. A phase response curve to single bright light pulses in human subjects. J Physiol. 2003; 549(Pt 3): 945–952. - PMC - PubMed
    1. Gooley JJ, Rajaratnam SM, Brainard GC, Kronauer RE, Czeisler CA, Lockley SW. Spectral responses of the human circadian system depend on the irradiance and duration of exposure to light. Sci Transl Med. 2010; 2(31): 31ra33. - PMC - PubMed
    1. Schmidt TM, Chen SK, Hattar S. Intrinsically photosensitive retinal ganglion cells: many subtypes, diverse functions. Trends Neurosci. 2011; 34(11): 572–580. - PMC - PubMed
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Figure 5
Figure 5
Light exposure and subsequent sleep architecture. (A) Shorter latencies to first REM sleep episode were associated with preceding later timing to first exposure to more than 10 lux (black circles indicate average values of two PSG recordings and of the same 2 days of light recordings and dashed line indicates model fit) and (B) later preceding timing of maximal light exposure. (C) A lower percentage of REM sleep was associated with higher preceding maximal light intensities (model prediction: black line, standard error of mixed model: grey range). This relationship was modulated by DLMO timing, though all DLMO timing categories showed the same relationship (red: DLMO > 21 hours, orange: 19 hours ≤ DLMO ≤ 21 hours, green: DLMO

Figure 6

Sleep stage accumulation related to…

Figure 6

Sleep stage accumulation related to preceding maximal light exposure intensity. (A) SWS accumulation…

Figure 6
Sleep stage accumulation related to preceding maximal light exposure intensity. (A) SWS accumulation was higher throughout the sleep period in individuals previously exposed to higher maximal light intensities (p < .05). (B) REM sleep accumulation was lower in individuals previously exposed to higher maximal light intensities (p < .05). (C) Wake accumulation was significantly lower at the beginning of the sleep period in individuals previously exposed to higher maximal light intensities (p < .05). In all graphs, line at top indicates a significant difference between groups at that time percentage of total sleep, p < .05.

Figure 7

Subsequent sleep stage accumulation related…

Figure 7

Subsequent sleep stage accumulation related to timing of first exposure to more than…

Figure 7
Subsequent sleep stage accumulation related to timing of first exposure to more than 10 lux. (A) SWS accumulation was higher in individuals that previously had earlier first exposure to > 10 lux (p < .05). (B) REM sleep accumulation was lower in individuals that previously had earlier first exposure to >10 lux (p < .05). (C) Wake accumulation was significantly lower throughout the sleep period in individuals that previously had earlier first exposure to >10 lux (p < .05). In all graphs, line at top indicates a significant difference between groups at that time percentage of total sleep, p < .05.
All figures (7)
Figure 6
Figure 6
Sleep stage accumulation related to preceding maximal light exposure intensity. (A) SWS accumulation was higher throughout the sleep period in individuals previously exposed to higher maximal light intensities (p < .05). (B) REM sleep accumulation was lower in individuals previously exposed to higher maximal light intensities (p < .05). (C) Wake accumulation was significantly lower at the beginning of the sleep period in individuals previously exposed to higher maximal light intensities (p < .05). In all graphs, line at top indicates a significant difference between groups at that time percentage of total sleep, p < .05.
Figure 7
Figure 7
Subsequent sleep stage accumulation related to timing of first exposure to more than 10 lux. (A) SWS accumulation was higher in individuals that previously had earlier first exposure to > 10 lux (p < .05). (B) REM sleep accumulation was lower in individuals that previously had earlier first exposure to >10 lux (p < .05). (C) Wake accumulation was significantly lower throughout the sleep period in individuals that previously had earlier first exposure to >10 lux (p < .05). In all graphs, line at top indicates a significant difference between groups at that time percentage of total sleep, p < .05.

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