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Taufique, S.K.T.; Prabhat, A. Artificial Light at Night and Associated Neuronal Changes. Encyclopedia. Available online: https://encyclopedia.pub/entry/19712 (accessed on 24 July 2024).
Taufique SKT, Prabhat A. Artificial Light at Night and Associated Neuronal Changes. Encyclopedia. Available at: https://encyclopedia.pub/entry/19712. Accessed July 24, 2024.
Taufique, S K Tahajjul, Abhilash Prabhat. "Artificial Light at Night and Associated Neuronal Changes" Encyclopedia, https://encyclopedia.pub/entry/19712 (accessed July 24, 2024).
Taufique, S.K.T., & Prabhat, A. (2022, February 21). Artificial Light at Night and Associated Neuronal Changes. In Encyclopedia. https://encyclopedia.pub/entry/19712
Taufique, S K Tahajjul and Abhilash Prabhat. "Artificial Light at Night and Associated Neuronal Changes." Encyclopedia. Web. 21 February, 2022.
Artificial Light at Night and Associated Neuronal Changes
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This entry is adapted from the peer-reviewed paper 10.3390/birds3010003

Artificial light at night (ALAN) has changed the pattern of the natural day-night environment. In recent times, a good amount of focus has been put on the research related with changes in night illumination due to rapid urbanization. It has shown to affect circadian rhythms that regulate almost all physiological processes in animals including sleep and cognition. In the early 2010s, most behavioural and molecular studies of light at night were focused on nocturnal rodents. However, until recently, songbirds have taken the front seat, as most are diurnal and show higher cognitive behaviour like mammalian model systems. Artificial light at night (ALAN) affects circadian rhythms and physiology in songbirds. Most of the studies, both in wild and captive birds, have shown negative consequences of ALAN on daily timing, sleep, physiology and higher brain functions.

artificial light at night birds behaviour brain function cognition epigenetics melatonin sleep circadian rhythm brain health

1. Introduction

The usage of artificial electrical lightning has led to an increase in artificial light at night (ALAN), and now, ALAN covers more than 80% of the world’s inhabited areas [1], which has become a global concern and has recently been asserted as a source of environmental pollution by the American Medical Association. During the last decade, the consequences of ALAN in an ecological aspect, in particular, its effects on avian species, have received great interest [2]. ALAN exposure disrupts the clock-regulated daily patterns of physiology and behaviour and suppresses nocturnal melatonin production [3][4]. Like most organisms, birds have evolved to keep time with the 24 h environmental light-dark cycle, which is regulated by the endogenous circadian clock(s). Daily timings and temporal niches are important for fitness and survival. ALAN exposures have been reported to be associated with serious ecological and health consequences, such as disruption of immune, metabolic, reproductive, and cognitive functions in both birds and mammals [5][6].
The presence of ALAN is a disturbance of the natural habitat, with bright intensity of light close to the light source and low intensity of light at greater distances at night-time, and evidence shows comparable effects of both no-night environment (24 h constant light, LL) and dLAN (dim light at night) in laboratory and field experiments. There is accumulating evidence that exposure to ALAN regulates and suppresses daily rhythm of activity, melatonin level, and sleep in birds. The circadian clock in congruence with melatonin and sleep regulate avian cognitive performance. Many studies in wild birds have shown the adverse effects of ALAN on several territorial behaviours, including reproduction, singing, migration, and sleep [7][8][9][10][11]. However, field studies have suggested ALAN increases foraging opportunities in Domestic Pigeon (Columba livia domestica) by promoting nocturnal activity and feeding [12] and night foraging in Southern Lapwing (Vanellus chilensis) [13]. It is also reported that ALAN allows the Northern Mockingbird (Mimus polyglottos) to feed nestlings after dark [14]. Thus, ALAN changes the circadian phase of the feeding behaviour along with the increase in nocturnal activity. Further, ALAN increases foraging opportunities in nocturnal predatory birds, such as European Nightjars (Caprimulgus europaeus) and Burrowing Owl (Athene cunicularia), by increasing the abundance of the prey near the light source [15][16]. Thus, modifying the nest-site selection might increase vulnerability for the highly specialized birds [13]. Additionally, several laboratory studies have demonstrated the negative effects of ALAN (LL and dLAN) on learning, memory, mood, and exploration [17][18][19]. Although there is limited research on this topic, most of the insights on the adverse effects of ALAN on cognitive functions are from behavioural studies. Nevertheless, these results raise an intriguing question about the molecular underpinning of the ALAN-induced negative consequences on brain functions. Despite clear evidence of potential consequences, how the environmental light signal is translated and induces long-term consequences to remain unclear. In this review, I have first outlined the consequences of the ALAN circadian system and sleep, then mainly focused on the effects of ALAN on brain functions and known underlying mechanisms. Thereafter, I have highlighted the possible involvement of melatonin and epigenetic modifications in ALAN-induced responses. The overarching mechanism(s) are general and apply to many different species; however, here, the researchers focused on bird species and discussed the importance of the avian system for a better understanding of the subject.

2. Artificial Light at Night—Circadian Misalignment and Sleep Disruption

In birds, separate independent circadian oscillators are present in the hypothalamus, retina, and pineal gland, which interact with each other and the periodic environment (e.g., light-dark cycle) to produce timing at the functional level [20]. The environmental light cue is detected by the photoreceptors present in the retinas, pineal gland, and deep brain photoreceptors [20]. Thus, activation of these photoreceptors can alter the expression of clock genes and nocturnal melatonin levels. Exposure to night-time light disrupts the circadian system and desynchronizes the associated behavioural rhythms in both wild and captive birds. In Eurasian Blackbird (Turdus merula) and Great Tits (Parus major), LAN induced activity in the dark phase and nocturnal restlessness was observed [21][22]. Interestingly, the effects of ALAN on activity behaviour are intensity and wavelength-dependent in Great Tits [11]. Similarly, no-night environment (constant light; LL) and dLAN exposure induced arrhythmicity in the activity and rest pattern and night-time restlessness in captive Zebra Finches (Taeniopygia guttata) and House Crows (Corvus splendens) [17][18][19]. The presence of an ALAN environment has been shown to alter the daily singing behaviour in free-living songbirds (European Robin (Erithacus rubecula), Common Blackbird, Song Thrush (Turdus philomelos), Great Tits, Blue tits (Cyanistes caeruleus), Common Chaffinch (Fringilla coelebs), and American Robins (Turdus migratorius)), and similarly in captive songbirds (Zebra Finch) [8][19][23]. ALAN also changes the migratory stopover behaviours of various nocturnal migratory birds [8][9] and negatively affects survival and fitness in birds. Further, it also disrupts the daily rhythms in hormonal secretion, in particular, the release of melatonin [18][19], which plays an important regulatory role in many physiological processes including body mass, metabolism, immunity, and sleep [24].
The temporal organization of daily behaviours is governed by the molecular clock, which functions in a closed transcriptional-translational negative feedback loop and is formed by a set of clock genes [20]. Clock (Circadian locomotor output cycles kaput) and Bmal1 (Brain and muscle Arnt-like protein-1) form the positive limb, and Per (Period) and Cry (Cryptochrome) genes form the negative limb of the molecular clock. Recent evidence suggests that ALAN-induced behavioural and physiological changes are associated with disruption of circadian clock gene expression in birds [25][26]. Zebra Finches born under an LL environment in the laboratory showed differential effects with loss of rhythmicity in the activity and singing behaviour in 30% in males and activity behaviour in 30% females. However, the overall song quality declined [27]. Additionally, there was the loss of rhythmic expression of clock genes in the hypothalamus and song nuclei under LL [27]. Similarly, female Zebra Finches born under LL showed a loss of rhythmic expression of clock genes in the hypothalamus and peripheral tissues [28]. Further, dLAN affects the expression of Bmal1 in the brain, liver, spleen, and blood tissues in Great Tits, along with alteration in metabolic and immune genes [25]. dLAN reduced the peak amplitude of the Per2 gene rhythm, but not Bmal1, in the hypothalamus of zebra finches. Additionally, dLAN exposure abolished the rhythm in the expression of clock and cry1 genes [26]. Further, ALAN impairs metabolism and alters metabolic gene (Sirtuin1; Sirt1, Glucose 6-phosphatase; G6pc and Forkhead box protein O1; Foxo1) expression in Zebra Finches [29][30]. Another study demonstrated the effects on the diurnal pattern of gene expression of pro-inflammatory (Interleukin-1β; Il-1β, Interleukin-6; Il-6) and anti-inflammatory (Il-10) genes in the brain of Zebra Finches [31]. It has also been suggested that the urban environment (exposure to ALAN) changes the phase or amplitude of the gene expression rhythm in the hypothalamus, retina, and pineal gland of Eurasian Tree Sparrow (Passer montanus) [32].
A critical circadian clock-dependent effect of ALAN might be associated with sleep defects in birds [10][11][18][26][33]. Growing evidence demonstrates that ALAN can influence the total amount, timing and structure of sleep in many bird species e.g., Domestic Pigeons (Columba livia domestica), Great Tits, Corvids, and Zebra Finches. Great Tits spent a significant amount of time awake inside their nest box during night-time in the presence of dLAN compared to the conspecifics in the dark nights [10]. dLAN also increased nocturnal vigilance in Indian Peafowl (Pavo cristatus) to avoid predators and thus faced a trade-off between vigilance and sleep [33]. Additionally, there was a decrease in resting period and an increase in sleep deprivation in House Crows exposed to LL and dLAN [17][18]. Some evidence suggests these changes in sleep behaviour are associated with reduced oxalate, a biomarker of sleep debt, as shown in Great Tits and Zebra Finches [11][26]. In Zebra Finches, ALAN has also been shown to alter the expression of genes associated with sleep [26]. With advancements in technology, recent electroencephalogram (EEG)-based sleep studies have now provided further insights into the effects of ALAN on sleep in birds. Studies have demonstrated that, when exposed to urban intensities of ALAN, sleep in captive Domestic Pigeons and Australian Magpies (Cracticus tibicen tyrannica) was reduced with slow-wave activity during non-REM sleep and showed more fragmentation with a lower fraction of REM sleep (out of total sleep) compared to dark night [34]. Together, these results provide behavioural, genomics, and electrophysiological evidence of disrupting effects of ALAN on circadian rhythms, nocturnal melatonin levels, and sleep behaviour. However, it is difficult to pinpoint the causal link between the consequences and ALAN-induced disruption of temporal organization. With several studies suggesting melatonin suppression, pineal melatonin has been proposed to be a possible link mediating the environmental light cues to the brain [3][4][5][24].

3. Adverse Effects on Cognitive Functions

Circadian disruption and ALAN are implicated in impaired cognition and mood disorders. Many studies have shown the negative effects of LL and dLAN on both cognitive performances and depression in birds [17][18][19]. Studies on House Crows have provided evidence of declined visuospatial learning and memory in presence of LL. The crows were caught in the wild and exposed to LL for 10–14 days in captivity [17]. Thereafter, behavioural rhythms were recorded, and crows were tested for learning and memory tasks. Crows showed impaired spatial and pattern-association learning when exposed to LL, compared to dark nights [17]. At the brain level, there was decreased neuronal activity in the hippocampus (HP) and caudal nidopallium (NC). Further, there was alteration in the midbrain (substantia nigra; SN and ventral tegmental area; VTA) dopaminergic system, as shown by decreased numbers and activity of tyrosine hydroxylase (TH) immunoreactive cells in LL [17]. An LL-induced decrease in TH-positive dopamine neurons has been also shown in rats and implicated in mental disorders [35]. Additionally, an LL-induced decrease in neurogenesis and dendritic complexity of the newborn neurons in the hippocampus and caudal nidopallium has also been shown in House Crows [36]. Similarly, a behavioural experiment on aviary-bred Zebra Finches exposed to LL demonstrated it had detrimental effects on activity and signing rhythms [19][27][28]. In addition, LL induced a decline in advanced brain functions such as learning and personality traits in Zebra Finches (Taeniopygia guttata) in adults, and in future generations as well [19]. Similarly, a recent study also suggested dLAN negatively affects cognitive performance (novel object exploration and learning and memory) in Zebra Finches [37].
Another study demonstrated that House Crows exposed to dLAN showed depressive-like responses, such as reduced eating and grooming, and increased feather-picking and self-mutilation associated with sleep deprivation [18]. Feather-picking and self-mutilation in birds can be considered analogous to trichotillomania (hair-pulling behaviour) in humans and is associated with a depression-like negative state [37][38]. In these crows, dLAN induces changes in hippocampal Bdnf, Il-1β, Tnfr1, and Nr4a2 expression, and importantly, dLAN affected the histone H3 acetylation at the brain-derived neurotrophic factor (Bdnf) gene and repressed Bdnf mRNA expression. dLAN also modulates the expression of the histone deacetylase-4 (Hdac4) gene in the hippocampus. dLAN reduces neurogenesis in the hippocampus, and it has been suggested that BDNF is involved in decreased hippocampal neurogenesis and the development of depressive-like responses [39]. In contrast to House Crows, Zebra Finches exposed to dLAN showed decreased neuronal density and therefore a compensatory increase in neurogenesis in the hippocampus [40][41].
Recent research on crows also demonstrated the negative impact of LL and dLAN on brain architecture. LL and dLAN decreased neuronal soma size and glial numbers in the hippocampus and lateral caudal nidopallium [42]. Neuronal soma size and glia-neuron ratios are important for optimal brain functions [42][43][44]. In humans, reductions in soma size and glial density have been implicated to be associated with reduced cognitive abilities related to depressive mental pathologies [45][46]. Altogether, in addition to behavioural changes, ALAN influences the brain at both structural and functional levels in bird brains, like the results from studies on rodents. For instance, rats exposed to LL showed impaired hippocampal-dependent spatial learning with accompanying changes in long-term depression in hippocampal neurons [47] and decreased neurogenesis [48].
Sleep deprivation is associated with memory deficits, compromised attention and decision-making, and mood disorders in rodents [49][50][51]. In birds, ALAN-induced sleep deficits and cognitive dysfunctions are shown in House Crows and Zebra Finches. In contrast, Peafowl and Great Tits exposed to ALAN showed sleep disruption but unimpaired cognitive performances [33][52]. Few studies on nocturnal mice showed ALAN-induced depressive behaviour but without any effects on sleep after ALAN exposure [51][53]. However, the depth of the relationship between sleep and cognitive functions is unclear and warrants further research. Nonetheless, as noted earlier, the ALAN effects on brain functions could also be mediated through the hormonal pathway. Melatonin functions as a critical molecule in the regulation of brain function either directly or indirectly by altering the circadian rhythm and sleep. Thus, it is pertinent to understand the direct involvement of melatonin in the regulation of neuronal plasticity.
Table 1. Summary of the results from recent studies in different avian species highlighting the effects of light at night on behavioural phenotypes and the molecular correlates.
Species Light
Environment		 Affected Behavioural Phenotype Molecular
Correlates		 Study
American Robins (Turdus migratorius) ALAN - Advances the morning chorus into the night   Miller [23]
European Robin (Erithacus rubecula)
Eurasian Blackbird (Turdus merula)
Song Thrush (Turdus philomelos)
Great Tits (Parus major)
Blue Tits (Cyanistes caeruleus)
Common Chaffinch (Fringilla coelebs)		 dLAN - Alters the phenology of dawn and dusk singing (Earlier in the year than before)   Da Silva et al. [8]
Blackbirds dLAN (~0.3 lux) - Early onset of activity and night restlessness   Dominoni and Partecke [22]
Blackbirds dLAN (~0.3 lux) - Increase in pre-dawn activity  Decreased nocturnal melatonin levels Dominoni et al. [54]
Blackbirds dLAN (~0.3 lux) - Advances seasonal testicular growth.   Dominoni et al. [55]
Great Tits dLAN (~ 1.6 lux) - Sleep deficits   Raap et al. [10]
Great Tits Different doses of dLAN (~0.05, 0.15, 0.5, 1.5 or 5 lux) - Dose-dependent increase in nocturnal activity dose Dose-dependent reduction in nocturnal melatonin levels deJong et al. [23]
Great Tits dLAN (~8 lux) of different wavelength - Increase in nocturnal activity
- Sleep deficits		 Decreased plasma oxalic acid
Reduced telomere length (cellular ageing)		 Ouyang et al. [11]
Great Tits dLAN (~0.1, 0.5, 1.5 and 5 lux) - Advanced wake-up time Shift in Bmal1 expression
Shift in metabolite expressions
Desynchronization of metabolic and immune genes		 Dominoni et al. [25]
Blue Tits
(Cyanistes caeruleus)		 dLAN (2 lux)   Affects feather glucocorticoid levels Dominoni et al. [56]
Indian Peafowl (Pavo cristatus) dLAN (~0.75 lux) - Increased nocturnal vigilance
- Sleep loss		   Yorzinski et al. [33]
European Nightjars (Caprimulgus europaeus) dLAN - Increased foraging opportunity
- Changes in habitat selection		   Sierro and Erhardt [15]
Burrowing Owl (Athene cunicularia) dLAN - Increased foraging opportunity
- Nest habitat selection near a light source		   Rodríguez et al. [16]
House Crow (Corvus splendens) LL (~150 lux) - Activity rhythm disruption
-Learning and memory deficits		 Reduced neuronal activity in HP and NC
Decreased expression of Tyrosine hydroxylase in the mid-brain		 Taufique and Kumar [17]
House Crow LL (~150 lux) - Learning and memory deficits Decreased neurogenesis and dendritic complexity in HP and NC Taufique et al. [36]
House Crow dLAN (~6 lux) - Increase in nocturnal activity
- Sleep deprivation
- Depressive-like behaviour		 Decreased expression of Bdnf, Il1β, Tnfr1, Nr4a2 in HP
Increased Hdac4 expression and histone H3 acetylation of Bdnf gene in HP
Decreased neurogenesis in HP
Decreased levels of nocturnal melatonin		 Taufique et al. [18]
* Behavioural phenotypes were rescued by elimination of dLAN
House Crow LL (~150 lux) and dLAN (~6 lux)   Decreased neuronal soma size
Reduced glia–neuron ratio		 Taufique et al. [42]
Zebra Finch
(Taeniopygia guttata)		 LL (~5 lux) - Disturbed activity rhythm
- Learning deficits		   Jha and Kumar [19]
Zebra Finch (male) LL (~150 lux) - Disrupted activity and singing behaviour (30% of individuals)
- Decline in song quality, reduced amplitude and song production		 Loss of rhythm in the expression of clock genes in hypothalamus Prabhat et al. [27]
Zebra Finch (female) LL (~150 lux) - Fattening, weight gain, and lipid accumulation in the liver Loss of rhythm in the expression of clock genes in hypothalamus and peripheral tissues Prabhat et al. [28]
Zebra Finch LL (~400 lux) and dLAN (~3 lux) - Loss of melatonin and corticosterone diurnal pattern
Altered diurnal pattern of cytokines in the brain		 Mishra et al. [31]
Zebra Finch dLAN (~5 lux) - Induced night-time feeding and perch-hopping
- Sleep deprivation
- Learning and memory deficits
- Increased neophobia		   Prabhat et al. [37]
Zebra Finch dLAN (~5 lux) - Sleep deficits Decreased plasma oxalate levels
Decreased Tlr4, Il-b, Nos gene expression, and attenuated Achm3 mRNA levels
Changes in gene expression of Ca2+ dependent sleep-inducing pathway		 Batra et al. [26]
Zebra Finch dLAN (~5 lux) - Increased night-time activity
- Nocturnal feeding
- Body fattening and weight gain		 Increased levels of plasma glucose
Decreased levels of thyroxine and triglycerides
Altered metabolic genes expression (Sirt1, G6pc, and Foxo1)		 Batra et al. [29]
Zebra Finch LL (~150 lux) and dLAN (~5 lux) - Body fattening and weight gain
- Hepatic lipid accumulation		 Changes in gut microbiome with a decline in Lactobacillus richness Malik et al. [30]
* Phenotype was rescued by Lactobacillus supplement
Zebra Finch dLAN   Increased neuronal recruitment reduced neuronal density in the hippocampus
Decreased nocturnal melatonin levels		 Moaraf et al. [40][41]
Domestic Pigeons (Columba livia domestica) and Australian Magpies (Cracticus tibicen tyrannica) dLAN (~9.6 and 18.89) - reduced sleep duration and fragmentation
- slow-wave activity during non-REM sleep
- reduced REM sleep		   Aulsebrook et al. [34]

4. Melatonin Induced Modulation of Neuroplasticity

The pineal gland hormone melatonin (N-acetyl-methoxy tryptamine) is produced and secreted under the dark phase (also known as ‘hormone of darkness) and is involved in many bodily functions [57][58]. Melatonin synthesized by the pineal gland is released into the third ventricle, from where it is diffused to different regions of the brain and relays environmental light-dark information. Melatonin mediates its functions through signalling pathways coupled to its receptor MT1 and MT2 [58][59]. The mechanism(s) of modulation of neuroplastic changes by melatonin in the hippocampus involves the activation of hippocampal expression of melatonin receptors. Melatonin induces hippocampal cell proliferation [60] and increases neuronal survival [61] in the hippocampus, which is associated with the activation of MT1 and MT2 receptors [62]. In addition, melatonin is also involved in the regulation of cognitive performances. Melatonin attenuates memory and cognitive deficits due to sleep deprivation in rats [63][64]. Sleep deprivation decreases BDNF and CaMKII expression in the hippocampus, whereas melatonin prevents these changes and improves cognitive abilities [64]. Melatonin receptors are involved in the modulation of mood behaviour. Genetic deletion of MT2 but not MT1 receptor induces depressive- and anxiety-like behaviours in mice [59].
Although both nocturnal and diurnal species produce melatonin during the dark phase, laboratory strains of mice (C57bl/6) lack detectable melatonin rhythms completely. Studies performed on mice (undetectable melatonin rhythms) versus Siberian Hamsters and House Crows (robust melatonin rhythm) have reported similar effects of ALAN on mood [15][32][33]. Melatonin production is sensitive to light and ALAN of even very low-intensity exposures, which also suppresses melatonin production in diurnal animals such as birds, fishes, and humans [15][19][55][56][57][58][59][60][61][62][63][64][65][66][67]. Additionally, it is important to mention that light plays a different role in diurnal and nocturnal animals; thus, the effect of ALAN might be different concerning the temporal organization of daily behaviours and melatonin rhythms. Further, exogenous melatonin also promotes dendritic maturation and axonogenesis in the hippocampus of mice [60]. Light at night conditions has been shown to suppress melatonin and affect neurogenesis in diurnal birds [15][28][39][40]. Plasma melatonin levels have also been shown to be lower in Tree Sparrows from urban environments, compared to rural birds. The results demonstrated that expression of Aanat, Mel1 and Mel2 genes in the pineal is disrupted in urban-dwelling Tree Sparrows [28]. Thus, it is proposed that melatonin suppression by ALAN is not the only mechanism but may be an important effecter molecule in ALAN-induced effects on neuroplasticity and cognition in diurnal animals, including humans.

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S K Tahajjul Taufique
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Abhilash Prabhat
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