Sleep in unnatural times: illuminated night negatively affects sleep and associated hypothalamic gene expressions in diurnal zebra finches

Abstract

We investigated the effects of exposure at ecologically relevant levels of dim light at night (dLAN) on sleep and the 24 h hypothalamic expression pattern of genes involved in the circadian timing ( per2, bmal1 , reverb-β , cry1 , ror-α , clock ) and sleep regulatory pathways (cytokines: tlr4 , tnf - α , il-1β , nos ; Ca 2+ -dependent pathway: camk2 , sik3 , nr3a ; cholinergic receptor, achm3 ) in diurnal female zebra finches. Birds were exposed to 12 h light (150 lux) coupled with 12 h of absolute darkness or of 5 lux dim light for three weeks. dLAN fragmented the nocturnal sleep in reduced bouts, and caused sleep loss as evidenced by reduced plasma oxalate levels. Under dLAN, the 24 h rhythm of per2 , but not bmal1 or reverb-β , showed a reduced amplitude and altered peak expression time; however, clock , ror-α and cry1 expressions showed an abolition of the 24 h rhythm. Decreased tlr4 , il-1β and nos , and the lack of diurnal difference in achm3 messenger RNA levels suggested an attenuated inhibition of the arousal system (hence, awake state promotion) under dLAN. Similarly, changes in camk2 , sik3 and nr3a expressions suggested dLAN-effects on Ca 2+ -dependent sleep-inducing pathways. These results demonstrate dLAN-induced negative effects on sleep and associated hypothalamic molecular pathways, and provide insights into health risks of illuminated night exposures to diurnal animals.

Artificial light at night leads to circadian disruption in a songbird: integrated evidence from behavioural, genomic and metabolomic data

“…Sampled within a day after being brought into captivity, urban birds showed clear advances in the circadian system, including, as in our birds, in hypothalamic BMAL1. Other experimental studies have also confirmed effects of ALAN on avian rhythms in brain and other tissues (16,17). In our study, only some of the investigated regulatory genes aligned with the ALANdependent advances of rhythms in behavior and BMAL1.…”

“…In free-living and captive organisms, altered daily and annual activity has been widely reported, and experimental illumination has confirmed causal effects of ALAN (11,12). Still, it is largely unclear whether the circadian system, its multiple components, and the physiological pathways it coordinates, remain synchronized with activity patterns (13)(14)(15)(16)(17)(18). ALAN has also been shown to induce physiological changes, including in endocrine, immune and metabolic pathways (15,19,20).…”

Light, Sleep and Performance in Diurnal Birds

“…Numerous studies also found that when exposed to artificial light at night, birds show increased activity [ 44 , 55 , 66 , 67 , 68 , 69 , 70 , 71 , 72 , 73 ], delayed chirping behavior [ 74 ], increased vigilance [ 75 ] and reduced sleep behavior at night [ 43 , 76 , 77 , 78 , 79 ], but see [ 80 , 81 ]. There is some evidence that these changes in behavior are associated with reduced circulating oxalate [ 66 , 79 ], a biomarker of sleep debt in rats and humans [ 82 ]. However, other studies found an increase [ 83 ] or no change [ 84 ] in oxalate under artificial light at night, raising the possibility that the level of oxalate does not reflect prior sleep/wake history in birds [ 84 ].…”

“…However, other studies found an increase [ 83 ] or no change [ 84 ] in oxalate under artificial light at night, raising the possibility that the level of oxalate does not reflect prior sleep/wake history in birds [ 84 ]. In captive zebra finches ( Taeniopygia guttata ), artificial light at night has also been found to alter expression of genes involved in sleep regulation [ 79 ]. Together, these studies provide accumulating evidence for disruptive effects of artificial lighting on avian sleep.…”

“…The peak in non-REM sleep intensity also appeared delayed, which further suggests some physiological disruption of sleep regulation. Other research demonstrates that urban intensities of light at night (0.03 to 8 lux) can suppress circulating melatonin concentrations [ 55 , 68 , 72 , 89 ] and alter expression of clock genes [ 79 ], suggesting that circadian pathways could mediate some of the effects of artificial light at night on sleep. Together, these findings suggest that artificial light can influence sleep both directly and indirectly, and that the importance of various pathways might vary depending on the species or context.…”