Abstract
Light plays a critical role in the regulation of numerous aspects of physiology and behaviour, including the entrainment of circadian rhythms and the regulation of sleep. These responses involve melanopsin (OPN4)-expressing photosensitive retinal ganglion cells (pRGCs) in addition to rods and cones. Nocturnal light exposure in rodents has been shown to result in rapid sleep induction, in which melanopsin plays a key role. However, studies have also shown that light exposure can result in elevated corticosterone, a response that is not compatible with sleep. To investigate these contradictory findings and to dissect the relative contribution of pRGCs and rods/cones, we assessed the effects of light of different wavelengths on behaviourally defined sleep. Here, we show that blue light (470 nm) causes behavioural arousal, elevating corticosterone and delaying sleep onset. By contrast, green light (530 nm) produces rapid sleep induction. Compared to wildtype mice, these responses are altered in melanopsin-deficient mice (Opn4-/-), resulting in enhanced sleep in response to blue light but delayed sleep induction in response to green or white light. We go on to show that blue light evokes higher Fos induction in the SCN compared to the sleep-promoting ventrolateral preoptic area (VLPO), whereas green light produced greater responses in the VLPO. Collectively, our data demonstrates that nocturnal light exposure can have either an arousal- or sleep-promoting effect, and that these responses are melanopsin-mediated via different neural pathways with different spectral sensitivities. These findings raise important questions relating to how artificial light may alter behaviour in both the work and domestic setting.
Highlights
In addition to its familiar visual function the mammalian retina mediates a broad range of non-image forming responses to light, including the entrainment of circadian rhythms [1], regulation of pineal melatonin synthesis [2], pupillary light constriction [3] and the regulation of sleep [4,5,6]
Light exerts profound effects on our physiology and behaviour, setting our biological clocks to the correct time and regulating when we are asleep and we are awake. The photoreceptors mediating these responses include the rods and cones involved in vision, as well as a PLOS Biology | DOI:10.1371/journal.pbio
We found that blue light was aversive, delaying sleep onset and increasing glucocorticoid levels
Summary
In addition to its familiar visual function the mammalian retina mediates a broad range of non-image forming responses to light, including the entrainment of circadian rhythms [1], regulation of pineal melatonin synthesis [2], pupillary light constriction [3] and the regulation of sleep [4,5,6]. Research on these responses led to the identification of a novel retinal photoreceptor, consisting of a subset of photosensitive retinal ganglion cells (pRGCs) expressing the photopigment melanopsin (OPN4) [7,8]. Recent studies have shown that visual responses may be modulated by irradiance information detected by melanopsin, for example, in light adaptation [18]
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