Dim light in the evening causes coordinated realignment of circadian rhythms, sleep, and short-term memory

Shu K E Tam,Stuart N Peirson,David M Bannerman,Selma Tir,Angus S Fisk,Laurence A Brown,Vladyslav V Vyazovskiy,Russell G Foster,Vincent Van Der Vinne,Tatiana S Wilson,Mary E Harrington,Carina A Pothecary

doi:10.1073/pnas.2101591118

Shu K E Tam, Stuart N Peirson + Show 10 more

Open Access

https://doi.org/10.1073/pnas.2101591118

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Abstract

Light provides the primary signal for entraining circadian rhythms to the day/night cycle. In addition to rods and cones, the retina contains a small population of photosensitive retinal ganglion cells (pRGCs) expressing the photopigment melanopsin (OPN4). Concerns have been raised that exposure to dim artificial lighting in the evening (DLE) may perturb circadian rhythms and sleep patterns, and OPN4 is presumed to mediate these effects. Here, we examine the effects of 4-h, 20-lux DLE on circadian physiology and behavior in mice and the role of OPN4 in these responses. We show that 2 wk of DLE induces a phase delay of ∼2 to 3 h in mice, comparable to that reported in humans. DLE-induced phase shifts are unaffected in Opn4-/- mice, indicating that rods and cones are capable of driving these responses in the absence of melanopsin. DLE delays molecular clock rhythms in the heart, liver, adrenal gland, and dorsal hippocampus. It also reverses short-term recognition memory performance, which is associated with changes in preceding sleep history. In addition, DLE modifies patterns of hypothalamic and cortical cFos signals, a molecular correlate of recent neuronal activity. Together, our data show that DLE causes coordinated realignment of circadian rhythms, sleep patterns, and short-term memory process in mice. These effects are particularly relevant as DLE conditions-due to artificial light exposure-are experienced by the majority of the populace on a daily basis.

Highlights

Light provides the primary signal for entraining circadian rhythms to the day/night cycle
Locomotor Activity Rhythms Are Phase Delayed under dim artificial lighting in the evening (DLE)
Under constant darkness (DD), activity rhythms in mice with prior exposure to DLE free ran at later clock times than mice with prior exposure to light/dark cycle (LD) (n = 8 Albumin-Cre;DbpKI/+ mice per group as described in Molecular Rhythms Are Delayed under DLE), with an overall phase difference of ∼4 h [main effects of Prior Lighting: F(1, 14) = 6.77, P = 0.021; F(1, 14) = 6.30, P = 0.025; and F(1, 14) = 6.20, P = 0.026, for onsets, midpoints, and offsets, respectively]

Summary

Introduction

Light provides the primary signal for entraining circadian rhythms to the day/night cycle. DLE delays molecular clock rhythms in the heart, liver, adrenal gland, and dorsal hippocampus It reverses short-term recognition memory performance, which is associated with changes in preceding sleep history. Our data show that DLE causes coordinated realignment of circadian rhythms, sleep patterns, and short-term memory process in mice. Studies on the photoreceptors mediating circadian entrainment led to the identification of a distinct photoreceptor system consisting of a subset of photosensitive retinal ganglion cells (pRGCs) expressing the photopigment melanopsin (OPN4) [6, 7] These cells have a peak sensitivity at ∼480 nm [8, 9], differing from the classical visual system, which in humans is most sensitive to light at ∼555 nm, corresponding to the red and green cones of the fovea [10]. How does the mammalian brain adapt to changes in daylength? In humans, exposure to long-day photoperiods delays melatonin onset but advances melatonin offset, compressing the internal

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