Melanopsin Regulates Both Sleep-Promoting and Arousal-Promoting Responses to Light

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.

Light-Dependent Regulation of Sleep and Wake States by Prokineticin 2 in Zebrafish

“…Taken together, these results suggest that Prok2 overexpression induces sleep by increasing hypothalamic galn levels. Similar to our findings, a recent study using nocturnal rodents found that sleep induced by green light at night is associated with increased galn expression in the VLPO (Pilorz et al, 2016). These results suggest that the direct effect of light on sleep may act via galn -expressing hypothalamic neurons in both diurnal zebrafish and nocturnal rodents.…”

Intrinsically Photosensitive Retinal Ganglion Cells (ipRGCs) Are Necessary for Light Entrainment of Peripheral Clocks

“…By filtering out blue light, which optimally drives melanopsin phototransduction, light-induced increases in corticosterone and adrenal clock gene expression in rats were prevented (Rahman et al, 2008). Conversely, exposure to blue light in mice increases plasma corticosterone and gene expression in adrenals more efficiently than longer wavelengths of light [53] and the effects of blue light were attenuated in melanopsin knockout mice [53]. These published findings are consistent with the data presented here, in which blocking ipRGC neurotransmission prevented photic entrainment of corticosterone rhythms in mice.…”

Constant Light Desynchronizes Olfactory versus Object and Visuospatial Recognition Memory Performance

“…The method of blood collection and CORT measurement are described in Pilorz et al (2016). Briefly, trunk blood was obtained from the site of decapitation and collected into microcentrifuge tubes containing the anticoagulant ethylenediaminetetraacetic acid (EDTA; Sigma-Aldrich), with 5 μl of EDTA for every 250 μl of blood collected.…”