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Sleep is a highly conserved state across the animal kingdom. However, sleep duration, behavior and associated neural activity show great diversity across taxonomic groups, and sometimes even within the same species. Understanding sleep functions depends on understanding when sleep emerged, which of its characteristics have persisted throughout evolution, and what accounts for the similarities and differences in sleep behavior and neurophysiology across different species. Here, we provide an overview of the latest findings in comparative sleep neurophysiology and highlight remarkable examples of sleep flexibility. We discuss the implications that these findings have on the proposed functions of sleep.

For many decades, sleep researchers have sought to determine which species 'have' rapid eye movement (REM) sleep. In doing so, they relied predominantly on a template derived from the expression of REM sleep in the adults of a small number of mammalian species. Here, we argue for a different approach that focuses less on a binary decision about haves and have nots, and more on the diverse expression of REM sleep components over development and across species. By focusing on the components of REM sleep and discouraging continued reliance on a restricted template, we aim to promote a richer and more biologically grounded developmental-comparative approach that spans behavioral, physiological, neural, and ecological domains.

Recent technological advancements allow researchers to measure electrophysiological parameters of animals, such as sleep, in remote locations by using miniature dataloggers. Yet, continuous recording of sleep might be constrained by the memory and battery capacity of the recording devices. These limitations can be alleviated by recording intermittently instead of continuously, distributing the limited recording capacity over a longer period. We assessed how reduced sampling of sleep recordings affected measurement precision of NREM sleep, REM sleep, and Wake. We analysed a dataset on sleep in barnacle geese that we resampled following 12 different recording schemes, with data collected for 1 min per 5 min up to 1 min per 60 min in steps of 5 min. Recording 1 min in 5 min still yielded precise estimates of hourly sleep-wake values (correlations of 0.9) while potentially extending the total recording period by a factor of 5. The correlation strength gradually decreased to 0.5 when recording 1 min per 60 min. For hourly values of Wake and NREM sleep, the correlation strength in winter was higher compared with summer, reflecting more fragmented sleep in summer. Interestingly for hourly values of REM sleep, correlations were unaffected by season. Estimates of total 24 h sleep-wake values were similar for all intermittent recording schedules compared to the continuous recording. These data indicate that there is a large safe range in which researchers can periodically record sleep. Increasing the sample size while maintaining precision can substantially increase the statistical power, and is therefore recommended whenever the total recording time is limited.

Sleep is a behavioral and physiological state that is thought to serve important functions. Many animals go through phases in the annual cycle where sleep time might be limited, for example, during the migration and breeding phases. This leads to the question whether there are seasonal changes in sleep homeostasis. Using electroencephalogram (EEG) data loggers, we measured sleep in summer and winter in 13 barnacle geese (Branta leucopsis) under semi-natural conditions. During both seasons, we examined the homeostatic regulation of sleep by depriving the birds of sleep for 4 and 8 h after sunset. In winter, barnacle geese showed a clear diurnal rhythm in sleep and wakefulness. In summer, this rhythm was less pronounced, with sleep being spread out over the 24-h cycle. On average, the geese slept 1.5 h less per day in summer compared with winter. In both seasons, the amount of NREM sleep was additionally affected by the lunar cycle, with 2 h NREM sleep less during full moon compared to new moon. During summer, the geese responded to 4 and 8 h of sleep deprivation with a compensatory increase in NREM sleep time. In winter, this homeostatic response was absent. Overall, sleep deprivation only resulted in minor changes in the spectral composition of the sleep EEG. In conclusion, barnacle geese display season-dependent homeostatic regulation of sleep. These results demonstrate that sleep homeostasis is not a rigid phenomenon and suggest that some species may tolerate sleep loss under certain conditions or during certain periods of the year., Sleep, 44 (4), ISSN:1550-9109, ISSN:0161-8105

Twice a year, thousands of migratory bird species cover huge distances between their wintering and breeding grounds. Prior to migration, birds become hyperphagic and accumulate large energy reserves (King and Farner 1965; Odum 1960; McWilliams and Karasov 2005). During the crossings of large ecological barriers such as deserts or seas, birds perform multi-hour flights that can lead to depletion of their energy stores and to a generalized physiological stress, forcing them to make stopovers at the first suitable sites found after the barrier to rest and restore energy reserves (Schmaljohann et al. 2007). The physiological condition at arrival, in particular the extent of fat reserves, has a major influence on stopover behavior (Fusani et al. 2009; Goymann et al. 2010) and, time spent at the stopover site depends on the interplay between body condition at arrival (Dierschke and Delingat 2001; Goymann et al. 2010; Cohen et al. 2014; Smith and McWilliams 2014; Dossman et al. 2018) and the speed at which birds can restore their energy reserves (Lindstrom 2003; Gomez et al. 2017). Migration is one of the most intense energy demanding life history stages, during which the highest mortality occurs (Sillett and Holmes 2002; Alerstam et al. 2003). Moreover, it is often associated with drastic physiological and behavioral changes other than the rapid gain and loss of energy stores. Several diurnal species, including a large proportion of passerine birds, become nocturnal migrants (Berthold 1973, 1996; Gwinner 1996). Flying at night and eating to accumulate energy reserves during the day limits the time available to sleep, which may become a constraint during this life history stage. Sleep is essential for all organisms (Shaw et al. 2002) and its deprivation may have dramatic consequences (Karni et al. 1994; Stickgold et al. 2000; Van Dongen et al. 2003), leading in the worst case to death (Rechtschaffen et al. 1983; Rechtschaffen and Bergmann 2002; Shaw et al. 2002). A large part of a bird’s life is spent sleeping (Toates 1980) but the function of this behavior is, in general, poorly understood. Several functions have been hypothesized, such as physiological restoration (Adam 1980; Reimund 1994; Mignot 2008), energy conservation (Berger 1975) and allocation (Schmidt 2014), clearance of metabolic waste products (Xie et al. 2013; Lim et al. 2013; Fultz et al. 2019), or memory consolidation (Maquet 2001; Stickgold et al. 2001). Among these, metabolic clearance has attracted considerable attention (Xie et al. 2013; Zhang et al. 2018). One group of molecules that might require clearance are the so-called reactive oxygen species (ROS) (Reimund 1994), atoms, or molecules with an unpaired electron. Given their chemical nature, these metabolites are highly reactive with biological molecules (i.e., proteins, lipids, and DNA) and can cause serious damage to the organism (Kregel and Zhang 2007; Cooper-Mullin and McWilliams 2016; Skrip and McWilliams 2016). Organisms can build antioxidant capacity (AOX), which can counteract ROS by reducing their reactivity, by upregulating antioxidant enzymes (enzymatic AOX) and by consuming dietary antioxidants (non-enzymatic AOX). According to the “free radical flux theory of sleep,” sleep clears ROS that have accumulated in the brain during wakefulness by reducing neurons’ activity and increasing enzymatic antioxidant mechanisms (Reimund 1994). Some evidence supporting the free radical flux theory has been found in Drosophila, where high ROS concentration in neurons directly triggers sleep (Hill et al. 2020). Moreover, the brain oxidative balance could be influenced by ROS produced in other tissues (e.g., liver, muscles, and red blood cells) and circulating antioxidants transported by the bloodstream. In this perspective, sleep may provide a direct antioxidant benefit to the brain and also play an important role in the maintenance of the oxidative balance in the periphery of the body. If sleep functions as, or allocates energy to, an antioxidant defense for the whole organism, it should be responsive to circulating ROS and thus may influence the oxidative status of the organism. Although endurance migratory flights have been shown to increase ROS production (Costantini et al. 2008; Jenni-Eiermann et al. 2014), whether intense refueling bouts (Lindstrom 2003; Maggini et al. 2015) influence ROS concentration remains debated. Previous studies conducted on mammals showed that a high caloric intake is associated with high oxidative damage (Masoro 2000; Sohal and Weindruch 1996; Weindruch and Sohal 1997). Eikenaar et al. (2016) found that northern wheatears (Oenanthe oenanthe) that were experimentally fasted and refed and thus rapidly refueling did not increase oxidative damage, at least in part because of increased AOX. Skrip et al. (2015) also found that two species of free-living warblers that were fattening in preparation for fall migration increased AOX as they built fat stores; however, oxidative damage was also higher in fatter birds suggesting an inescapable hazard of using primarily fats as fuel. Moreover, sleep restriction experienced during migratory periods (Rattenborg et al. 2004) should reduce ROS clearance and lead to a further increase in circulating ROS levels. According to the hypothesis of an antioxidant function of sleep (Reimund 1994), sleeping during stopovers might help to reduce ROS concentration. A few field observations are in line with this hypothesis. Several European migratory species were reported to show diurnal sleep after crossing ecological barriers such as the Sahara Desert (Jenni-Eiermann et al. 2011) and the Mediterranean (Schwilch et al. 2002). For example, at Saharan stopover sites, migratory birds in good condition sleep during most of the day, despite having sufficient energy reserves to continue migration (Bairlein 1985; Biebach et al. 1986). The proportion of time spent sleeping/active, during both day and night, is strongly dependent on the physiological condition at arrival (Fusani et al. 2009; Ferretti et al. 2019b). Altogether, these studies suggest that migratory warblers, during both fall (Bairlein 1985; Biebach et al. 1986) and spring (Fusani et al. 2009; Ferretti et al. 2019b) migration, profit from stopover sites after crossing large ecological barriers to recover from sleep loss accumulated during non-stop flights. In addition, recent work from our group has shown that the posture adopted during sleep may influence energy conservation (Ferretti et al. 2019b). Birds can sleep in a tucked posture, in which the head is turned backward and tucked in the scapular feathers, or untucked, with the head pulled toward the body facing forward (Amlaner and Ball 1983). Lean migrating garden warblers (Sylvia borin) sleep mainly tucked in to reduce heat loss through the head, and this posture reduces conductance and, therefore, metabolic rate. By contrast, birds with large energy reserves expend more energy while sleeping untucked but react more quickly to threats. Thus, sleep posture preference during migration is the result of a trade-off between energy consumption and anti-predator vigilance (Ferretti et al. 2019b). In the present study, we investigated the relationship between oxidative status, energy stores, food intake, and sleep in two migratory songbird species, the garden warbler and the whitethroat (Sylvia communis), at a Mediterranean stopover site during spring migration. Both species are long-distance migrants that cross similar large ecological barriers, and are abundant at our field site. Based on previous studies (Fusani et al. 2009; Goymann et al. 2010; Eikenaar and Schlafke 2013; Lupi et al. 2016), we expected birds with poor energy reserves to invest more time in energy recovery during the day and to sleep during most of the night with the head tucked. Birds with a large amount of energy reserves, on the contrary, should show a mainly untucked diurnal sleep pattern and higher nocturnal restlessness. Within this scenario, we hypothesized that there is a correlation between the oxidative status and the amount and type of sleep. Birds that land at the stopover site after an endurance flight are likely to have high ROS concentration. If sleep facilitates recovery from increased ROS, we predict that birds with higher levels of ROS will sleep longer, unless these birds also have a high antioxidant capacity. Moreover, birds with a high oxidative unbalance where pro-oxidant exceed antioxidants are expected to display a tucked sleep posture more often, which allows for deeper sleep and probably more efficient recovery from oxidative stress.

Most of our knowledge about the regulation and function of sleep is based on studies in a restricted number of mammalian species, particularly nocturnal rodents. Hence, there is still much to learn from comparative studies in other species. Birds are interesting because they appear to share key aspects of sleep with mammals, including the presence of two different forms of sleep, i.e. non-rapid eye movement (NREM) and rapid eye movement (REM) sleep. We examined sleep architecture and sleep homeostasis in the European starling, using miniature dataloggers for electroencephalogram (EEG) recordings. Under controlled laboratory conditions with a 12:12 h light–dark cycle, the birds displayed a pronounced daily rhythm in sleep and wakefulness with most sleep occurring during the dark phase. Sleep mainly consisted of NREM sleep. In fact, the amount of REM sleep added up to only 1~2% of total sleep time. Animals were subjected to 4 or 8 h sleep deprivation to assess sleep homeostatic responses. Sleep deprivation induced changes in subsequent NREM sleep EEG spectral qualities for several hours, with increased spectral power from 1.17 Hz up to at least 25 Hz. In contrast, power below 1.17 Hz was decreased after sleep deprivation. Sleep deprivation also resulted in a small compensatory increase in NREM sleep time the next day. Changes in EEG spectral power and sleep time were largely similar after 4 and 8 h sleep deprivation. REM sleep was not noticeably compensated after sleep deprivation. In conclusion, starlings display signs of NREM sleep homeostasis but the results do not support the notion of important REM sleep functions., Sleep, 43 (6), ISSN:1550-9109, ISSN:0161-8105

Sleep is considered to be of crucial importance for performance and health, yet much of what we know about sleep is based on studies in a few mammalian model species under strictly controlled laboratory conditions. Data on sleep in different species under more natural conditions may yield new insights in the regulation and functions of sleep. We therefore performed a study with miniature electroencephalogram (EEG) data loggers in starlings under semi-natural conditions, group housed in a large outdoor enclosure with natural temperature and light. The birds showed a striking 5-h difference in the daily amount of non-rapid-eye-movement (NREM) sleep between winter and summer. This variation in the amount of NREM sleep was best explained by night length. Most sleep occurred during the night, but when summer nights became short, the animals displayed mid-day naps. The decay of NREM sleep spectral power in the slow-wave range (1.1-4.3 Hz) was steeper in the short nights than in the longer nights, which suggests that birds in summer have higher sleep pressure. Additionally, sleep was affected by moon phase, with 2 h of NREM sleep less during full moon. The starlings displayed very little rapid-eye-movement (REM) sleep, adding up to 1.3% of total sleep time. In conclusion, this study demonstrates a pronounced phenotypical flexibility in sleep in starlings under semi-natural conditions and shows that environmental factors have a major impact on the organization of sleep and wakefulness.

Summary REM sleep is a paradoxical state accompanied by suspended thermoregulation that is preferentially expressed under optimal ambient temperatures. Komagata and colleagues now demonstrate that activity in hypothalamic melanin concentrating hormone neurons is essential for the temperature-dependent modulation of REM sleep.

Mammalian pupils respond to light1,2 and dilate with arousal, attention, cognitive workload, and emotions,3 thus reflecting the state of the brain. Pupil size also varies during sleep, constricting during deep non-REM sleep4-7 and dilating slightly during REM sleep.4-6 Anecdotal reports suggest that, unlike mammals, birds constrict their pupils during aroused states, such as courtship and aggression,8-10 raising the possibility that pupillary behavior also differs between mammals and birds during sleep. Here, we measured pupil size in awake pigeons and used their translucent eyelid to investigate sleep-state-dependent changes in pupil size. Male pigeons constricted their pupils during courtship and other male-female interactions but not while engaging in other waking behaviors. Unlike mouse pupils, the pigeons' pupils were dilated during non-REM sleep, while over 1,000 bursts of constriction and relaxation, which we call rapid iris movements (RIMs), occurred primarily during REM sleep. Consistent with the avian iris being composed largely of striated muscles,11-15 rather than smooth muscles, as in mammals, pharmacological experiments revealed that RIMs are mediated by nicotinic cholinergic receptors in the iris muscles. Despite receiving input from a parasympathetic nucleus, but consistent with its striated nature, the avian iris sphincter muscle behaves like skeletal muscles controlled by the somatic nervous system, constricting during courtship displays, relaxing during non-REM sleep, and twitching during REM sleep. We speculate that during wakefulness, pupillary constrictions are involved in social communication, whereas RIMs occurring during REM sleep might maintain the efficacy of this motor system and/or reflect the processing of associated memories.

Temporal variation in physical activity is mainly determined by the day–night cycle. While this may be true for diurnal species whose vision at night is often poor, the situation might be more complex in nocturnal animals as many such species can see both in the dark and in the daylight. We examined in Barn Owl (Tyto alba) nestlings whether temporal variation of behavioural activities and sleep is shaped by parental feeding visits occurring during the first part of the night and the extent to which they also occur during daylight hours. We measured several behaviours in 280 individuals from 90 broods recorded in 4 years. Parental feeding visits progressively declined in frequency from the beginning to the end of the night, and a number of offspring behaviours followed the same pattern of activity (feeding, vocalization and self-preening). Surprisingly, nestlings were awake not only at sunset, but also at sunrise. Several behaviours (locomotion, wing flapping and sibling interactions, such as pecking and allopreening among nestlings) showed peaks of activity at sunset and sunrise, suggesting that they were performed for other reasons than to interact with parents. Allopreening was performed more often during the day than at night. We conclude that although adult Barn Owls are nocturnal, nestlings display a complex temporal pattern of activity that is governed not only by feeding but also by other unknown factors.

The functions of slow wave sleep (SWS) and rapid eye movement (REM) sleep, distinct sleep substates present in both mammals and birds, remain unresolved. One approach to gaining insight into their function is to trace the evolution of these states through examining sleep in as many taxonomic groups as possible. The mammalian and avian clades are each composed of two extant groups, i.e., the monotremes (echidna and platypus) and therian (marsupial and eutherian [or placental]) mammals, and Palaeognaths (cassowaries, emus, kiwi, ostriches, rheas, and tinamous) and Neognaths (all other birds) among birds. Previous electrophysiological studies of monotremes and ostriches have identified a unique “mixed” sleep state combining features of SWS and REM sleep unlike the well-delineated sleep states observed in all therian mammals and Neognath birds. In the platypus this state is characterized by periods of REM sleep-related myoclonic twitching, relaxed skeletal musculature, and rapid eye movements, occurring in conjunction with SWS-related slow waves in the forebrain electroencephalogram (EEG). A similar mixed state was also observed in ostriches; although in addition to occurring during periods with EEG slow waves, reduced muscle tone and rapid eye movements also occurred in conjunction with EEG activation, a pattern typical of REM sleep in Neognath birds. Collectively, these studies suggested that REM sleep occurring exclusively as an integrated state with forebrain activation might have evolved independently in the therian and Neognath lineages. To test this hypothesis, we examined sleep in the elegant crested tinamou (Eudromia elegans), a small Palaeognath bird that more closely resembles Neognath birds in size and their ability to fly. A 24-h period was scored for sleep state based on electrophysiology and behavior. Unlike ostriches, but like all of the Neognath birds examined, all indicators of REM sleep usually occurred in conjunction with forebrain activation in tinamous. The absence of a mixed REM sleep state in tinamous calls into question the idea that this state is primitive among Palaeognath birds and therefore birds in general.

Coordinated activity in different sets of widely-projecting neurochemical systems characterize waking (W) and sleep (S). How and when this coordination is achieved during development is not known. We used embryos and newborns of a precocial bird species (chickens) to assess developmental activation in different neurochemical systems using cFos expression, which has been extensively employed to examine cellular activation during S and W in adult mammals. Similarly to adult mammals, newborn awake chicks showed significantly higher cFos expression in W-active hypocretin/orexin (H/O), serotonergic Dorsal Raphe, noradrenergic Locus Coeruleus and cholinergic Laterodorsal and Pedunculopontine Tegmental (Ch-LDT/PT) neurons when compared to sleeping chicks. cFos expression was significantly correlated both between these systems, and with the amount of W. S-active melanin-concentrating hormone (MCH) neurons showed very low cFos expression with no difference between sleeping and awake chicks, possibly due to the very short duration of S episodes. In embryonic chicks, cFos expression was low or absent across all five systems at embryonic day (E) 12. Unexpectedly, a strong activation was seen at E16 in H/O neurons. The highest activation of Ch-LDT/PT (also S-active) and MCH neurons was seen at E20. These data suggest that maturation of arousal systems is achieved soon after hatching, while S-control networks are active in late chick embryos.

Virtually all land mammals and birds have two sleep states: slow-wave sleep (SWS) and rapid eye movement (REM) sleep [1, 2]. After deprivation of REM sleep by repeated awakenings, mammals increase REM sleep time [3], supporting the idea that REM sleep is homeostatically regulated. Some evidence suggests that periods of REM sleep deprivation for a week or more cause physiological dysfunction and eventual death [4, 5]. However, separating the effects of REM sleep loss from the stress of repeated awakening is difficult [2, 6]. The northern fur seal (Callorhinus ursinus) is a semiaquatic mammal [7]. It can sleep on land and in seawater. The fur seal is unique in showing both the bilateral SWS seen in most mammals and the asymmetric sleep previously reported in cetaceans [8]. Here we show that when the fur seal stays in seawater, where it spends most of its life [7], it goes without or greatly reduces REM sleep for days or weeks. After this nearly complete elimination of REM, it displays minimal or no REM rebound upon returning to baseline conditions. Our data are consistent with the hypothesis that REM sleep may serve to reverse the reduced brain temperature and metabolism effects of bilateral nonREM sleep, a state that is greatly reduced when the fur seal is in the seawater, rather than REM sleep being directly homeostatically regulated. This can explain the absence of REM sleep in the dolphin and other cetaceans and its increasing proportion as the end of the sleep period approaches in humans and other mammals.

International audience; Sleep is a universal and complex state and it is widely agreed that this state is present in every animal species. However, the evolutionary origins of sleep remain ignored or misunderstood, which has led researchers to study, in various species, this common behaviour of all living organisms. Sleep is commonly studied at various levels under laboratory conditions, using tethered devices which record electroencephalographic or electromyographic readings. These artificial settings tend to induce stress, reduce animal freedom and prevent the use of sleeping shelters. In this paper, we present a novel, implantable instrumentation for a complete characterization of sleep under natural conditions suitable for a wide range of animal species, even for animals as small as pigeons or mice. Several configurations of this system are possible to enable the measurement of up to 16 electrophysiology channels, 3 temperature channels as well as 3-axes accelerometry. With an embedded flash memory card for the storage of data collected, the system can be used as a datalogger for the recording of signals in the field.

Sleep-related brain activity occurring during non-rapid eye-movement (NREM) sleep is proposed to play a role in processing information acquired during wakefulness. During mammalian NREM sleep, the transfer of information from the hippocampus to the neocortex is thought to be mediated by neocortical slow-waves and their interaction with thalamocortical spindles and hippocampal sharp-wave ripples (SWRs). In birds, brain regions composed of pallial neurons homologous to neocortical (pallial) neurons also generate slow-waves during NREM sleep, but little is known about sleep-related activity in the hippocampus and its possible relationship to activity in other pallial regions. We recorded local field potentials (LFP) and analogue multiunit activity (AMUA) using a 64-channel silicon multi-electrode probe simultaneously inserted into the hippocampus and medial part of the nidopallium (i.e., caudal medial nidopallium; NCM) or separately into the caudolateral nidopallium (NCL) of adult female zebra finches (Taeniopygia guttata) anesthetized with isoflurane, an anesthetic known to induce NREM sleep-like slow-waves. We show that slow-waves in NCM and NCL propagate as waves of neuronal activity. In contrast, the hippocampus does not show slow-waves, nor sharp-wave ripples, but instead displays localized gamma activity. In conclusion, neuronal activity in the avian hippocampus differs from that described in mammals during NREM sleep, suggesting that hippocampal memories are processed differently during sleep in birds and mammals.

Summary Each spring and fall, millions of normally diurnal birds switch to migrating at night. Most of these are small songbirds (passerine) migrating long distances that need to alternate their migratory flights with refueling stopovers [ 1 , 2 ], which can account for up to 80% of the total migratory period [ 3 ]. After a long nocturnal flight, these birds face the contrasting needs to recover sleep and refill depleted energy stores, all while vulnerable to predation [ 4 , 5 ]. Here, we investigated how garden warblers at a Mediterranean stopover site modulate their sleep behavior in relation to their metabolic state. At night, garden warblers in poor metabolic condition sleep more and exhibit less migratory restlessness than birds in good condition do. In addition, rather than sleeping with their head facing forward, birds in poor condition prefer to sleep with their head turned and tucked in their feathers. We further show that sleep with the head tucked is associated with lower respiratory and metabolic rates and reduced heat loss mediated by hiding the head—the body part with the highest heat dissipation—under the feathers. However, the benefit of conserving energy while sleeping with the head tucked was countered by reduced anti-predator vigilance. Birds presented with a sound simulating the approach of a predator responded more slowly when the head was tucked than when it was untucked. Consequently, our study demonstrates that through changing their sleep position and intensity, migrating songbirds can negotiate a previously unknown trade-off between sleep-mediated energy conservation and anti-predatory vigilance.

In modern society the night sky is lit up not only by the moon but also by artificial light devices. Both of these light sources can have a major impact on wildlife physiology and behaviour. For example, a number of bird species were found to sleep several hours less under full moon compared to new moon and a similar sleep-suppressing effect has been reported for artificial light at night (ALAN). Cloud cover at night can modulate the light levels perceived by wildlife, yet, in opposite directions for ALAN and moon. While clouds will block moon light, it may reflect and amplify ALAN levels and increases the night glow in urbanized areas. As a consequence, cloud cover may also modulate the sleep-suppressing effects of moon and ALAN in different directions. In this study we therefore measured sleep in barnacle geese (Branta leucopsis) under semi-natural conditions in relation to moon phase, ALAN and cloud cover. Our analysis shows that, during new moon nights stronger cloud cover was indeed associated with increased ALAN levels at our study site. In contrast, light levels during full moon nights were fairly constant, presumably because of moonlight on clear nights or because of reflected artificial light on cloudy nights. Importantly, cloud cover caused an estimated 24.8% reduction in the amount of night-time NREM sleep from nights with medium to full cloud cover, particularly during new moon when sleep was unaffected by moon light. In conclusion, our findings suggest that cloud cover can, in a rather dramatic way, amplify the immediate effects of ALAN on wildlife. Sleep appears to be highly sensitive to ALAN and may therefore be a good indicator of its biological effects., Environmental Pollution, 273, ISSN:0269-7491, ISSN:1878-2450, ISSN:1873-6424

International audience; Background: Sleep is an inactive state of reduced environmental awareness shared by all animals. When compared to wakefulness, sleep behavior is associated with changes in physiology and brain activity. The nature of these changes varies considerably across species, and therefore is a rich resource for gaining insight into the evolution and functions of sleep. A major obstacle to capitalizing on this resource is the lack of a small device capable of recording multiple biological parameters for extended periods of time both in the laboratory and the field.New method: ONEIROS is a new tool designed for conducting sleep research on small, freely moving animals. The miniature, standalone system is capable of recording up to 26 electrophysiological signals (electroencephalogram, electromyogram, electrooculogram, electrocardiogram), metabolic (3 temperature channels) and behavior via an accelerometer for several days. In addition, the device is equipped with a vibrating motor which can be used to assess arousal thresholds and to disrupt sleep. The system is available in telemetric or data-logger configuration useable in the field.Results: To demonstrate the efficacy of this tool, we simultaneously recorded for the first time, electroencephalogram, hippocampal local field potential, electromyogram, electrooculogram, brain, body and ambient temperature, and 3D accelerometry. We also deprived rats of paradoxical sleep by triggering the vibrating motor after online recognition of the state. Finally, by successfully recording a pigeon in an 8 m3 aviary in a social context with the device in the logger configuration, we demonstrate the feasibility of using the device in the field.

Birds have overcome the problem of sleeping in risky situations by developing the ability to sleep with one eye open and one hemisphere of the brain awake. Such unihemispheric slow-wave sleep is in direct contrast to the typical situation in which sleep and wakefulness are mutually exclusive states of the whole brain. We have found that birds can detect approaching predators during unihemispheric slow-wave sleep, and that they can increase their use of unihemispheric sleep as the risk of predation increases. We believe this is the first evidence for an animal behaviourally controlling sleep and wakefulness simultaneously in different regions of the brain.

Despite being a prominent aspect of animal life, sleep and its functions remain poorly understood. As with any biological process, the functions of sleep can only be fully understood when examined in the ecological context in which they evolved. Owing to technological constraints, until recently, sleep has primarily been examined in the artificial laboratory environment. However, new tools are enabling researchers to study sleep behaviour and neurophysiology in the wild. Here, we summarize the various methods that have enabled sleep researchers to go wild, their strengths and weaknesses, and the discoveries resulting from these first steps outside the laboratory. The initial studies to ‘go wild’ have revealed a wealth of interindividual variation in sleep, and shown that sleep duration is not even fixed within an individual, but instead varies in response to an assortment of ecological demands. Determining the costs and benefits of this inter- and intraindividual variation in sleep may reveal clues to the functions of sleep. Perhaps the greatest surprise from these initial studies is that the reduction in neurobehavioural performance resulting from sleep loss demonstrated in the laboratory is not an obligatory outcome of reduced sleep in the wild.This article is part of the themed issue ‘Wild clocks: integrating chronobiology and ecology to understand timekeeping in free-living animals’.

The possession of a rhythm is usually described as an important adaptation to regular changing environmental conditions such as the light-dark cycle. However, recent studies have suggested plasticity in the expression of a rhythm depending on life history and environmental factors. Barn owl ( Tyto alba) nestlings show variations in behavior and physiology in relation to the size of black feather spots, a trait associated with many behavioral and physiological phenotypes including the circadian expression of corticosterone and the regulation of body mass. This raises the possibility that individual spottiness could be associated with rhythmicity in sleep-wakefulness. Owlets showed ultradian rhythms in sleep-wakefulness, with a period length of 4.5 to 4.9 h. The period length of wakefulness and non-REM sleep was shorter in heavily compared to lightly spotted female nestlings, whereas in males, the opposite result was found. Furthermore, male and female nestlings displaying small black spots showed strong rhythmicity levels in wakefulness and REM sleep. This might be an advantage in a stable environment with predictable periodic changes in light, temperature, or social interactions. Heavily spotted nestlings displayed weak rhythms in wakefulness and REM sleep, which might enable them to be more flexible in reactions to unexpected events such as predation or might be a mechanism to save energy. These findings are consistent with previous findings showing that large-spotted nestlings switch more frequently between wakefulness and sleep, resulting in higher levels of vigilance compared to small-spotted conspecifics. Thus, nestlings with larger black feather spots might differently handle the trade-off between wakefulness and sleep, attention, and social interactions compared to nestlings with smaller black spots.

Wakefulness enables animals to interface adaptively with the environment. Paradoxically, in insects to humans, the efficacy of wakefulness depends on daily sleep, a mysterious, usually quiescent state of reduced environmental awareness. However, several birds fly non-stop for days, weeks or months without landing, questioning whether and how they sleep. It is commonly assumed that such birds sleep with one cerebral hemisphere at a time (i.e. unihemispherically) and with only the corresponding eye closed, as observed in swimming dolphins. However, the discovery that birds on land can perform adaptively despite sleeping very little raised the possibility that birds forgo sleep during long flights. In the first study to measure the brain state of birds during long flights, great frigatebirds (Fregata minor) slept, but only during soaring and gliding flight. Although sleep was more unihemispheric in flight than on land, sleep also occurred with both brain hemispheres, indicating that having at least one hemisphere awake is not required to maintain the aerodynamic control of flight. Nonetheless, soaring frigatebirds appeared to use unihemispheric sleep to watch where they were going while circling in rising air currents. Despite being able to engage in all types of sleep in flight, the birds only slept for 0.7 h d−1during flights lasting up to 10 days. By contrast, once back on land they slept 12.8 h d−1. This suggests that the ecological demands for attention usually exceeded that afforded by sleeping unihemispherically. The ability to interface adaptively with the environment despite sleeping very little challenges commonly held views regarding sleep, and therefore serves as a powerful system for examining the functions of sleep and the consequences of its loss.

J. Gasparini, N.C. Rattenborg et A. Roulin ont contribué de manière équivalente à cette publication.; Poor environmental conditions experienced during early development can have negative long-term consequences on fitness. Animals can compensate for negative developmental effects through phenotypic plasticity by diverting resources from non-vital to vital traits such as spatial memory to enhance foraging efficiency. We tested in young feral pigeons (Columba livia) how diets of different nutritional value during development affect the capacity to retrieve food hidden in a spatially complex environment, a process we refer to as `spatial memory'. Parents were fed with either high-or low-quality food from egg laying until young fledged, after which all young pigeons received the same high-quality diet until memory performance was tested at 6 months of age. The pigeons were trained to learn a food location out of 18 possible locations in one session, and then their memory of this location was tested 24 h later. Birds reared with the low-quality diet made fewer errors in the memory test. These results demonstrate that food quality during development has long-lasting effects on memory, with a moderate nutritional deficit improving spatial memory performance in a foraging context. It might be that under poor feeding conditions resources are redirected from non-vital to vital traits, or pigeons raised with low-quality food might be better in using environmental cues such as the position of the sun to find where food was hidden.

Insight into the functions of sleep in humans can be gained through studying sleep in animals. In contrast to model-based approaches which emphasize similarities between sleep in humans and animals amenable to experimental manipulation, comparative-based approaches give equal emphasis to the similarities and differences in sleep across the animal kingdom, and thereby aim to reveal overarching principles not readily apparent using other approaches. Avian sleep serves as a prime example. Birds independently evolved rapid eye movement (REM) and non-REM sleep, states that are in many, but, importantly, not all respects comparable to those in mammals. When compared to the sleep traits specific to one group, those shared by mammals and birds are more likely to be involved in fundamental functions. In this review, we summarize recent advances in our understanding of avian sleep, and the implications that such comparative work has for understanding sleep in mammals, including ourselves.

Journal of Comparative Physiology A, 199 (3), ISSN:0340-7594, ISSN:1432-1351

Many birds fly non-stop for days or longer, but do they sleep in flight and if so, how? It is commonly assumed that flying birds maintain environmental awareness and aerodynamic control by sleeping with only one eye closed and one cerebral hemisphere at a time. However, sleep has never been demonstrated in flying birds. Here, using electroencephalogram recordings of great frigatebirds (Fregata minor) flying over the ocean for up to 10 days, we show that they can sleep with either one hemisphere at a time or both hemispheres simultaneously. Also unexpectedly, frigatebirds sleep for only 0.69 h d−1 (7.4% of the time spent sleeping on land), indicating that ecological demands for attention usually exceed the attention afforded by sleeping unihemispherically. In addition to establishing that birds can sleep in flight, our results challenge the view that they sustain prolonged flights by obtaining normal amounts of sleep on the wing., Nature Communications, 7, ISSN:2041-1723

Externally mounted transmitters or loggers may adversely affect migration performance for reasons other than the effects of added mass. The added frontal area of a payload box increases drag, and if the box triggers separation of the boundary layer over the posterior body, the drag coefficient could also be increased, possibly by a large amount. Any such effects would lead directly to a decreased migration range and reduced energy reserves on completion of migration. We measured the body drag coefficients of Rose-coloured Starlings in the Seewiesen wind tunnel by the wingbeat-frequency method. The speed at which the wingbeat frequency passed through a minimum was taken to be an estimate of the minimum-power speed (V mp), from which the body drag coefficient was calculated in turn. Dummy transmitter boxes were mounted on the bird’s back by attaching them with Velcro to a side-loop harness pad. The pad alone projected 6 mm above the bird’s back, and increased the drag coefficient by nearly 50%, as compared to the “clean” configuration with no harness. Adding boxes (square-ended or streamlined) produced no further significant increase in the drag coefficient, but the addition of a sloping antenna increased it to nearly twice the clean value. These increases are attributed to separation of the boundary layer over the posterior upper body, triggered by the payload. We then ran computer simulations of a particular Barnacle Goose, for which detailed information was available from an earlier satellite-tracking project, to see how its migration range and reserves on arrival would be affected if its transmitter installation also caused flow separation and affected the body drag coefficient in a similar way. By representing the range calculation in terms of energy height, we separated the effect of the transmitter’s mass, which reduces the fat fraction (and hence also energy height) at departure, from that of flow separation, which steepens the energy gradient. The effect of the mass is small, and increases only slightly with increasing distance, whereas a steeper energy gradient not only reduces the range but also reduces the reserves remaining on arrival, to an extent that increases with migration distance. Energy height is related to the fat fraction rather than the fat mass, and is therefore preferable to energy as such, for expressing reserves in birds of different sizes.

The transition from wakefulness to sleep is marked by pronounced changes in brain activity. The brain rhythms that characterize the two main types of mammalian sleep, slow-wave sleep (SWS) and rapid eye movement (REM) sleep, are thought to be involved in the functions of sleep. In particular, recent theories suggest that the synchronous slow-oscillation of neocortical neuronal membrane potentials, the defining feature of SWS, is involved in processing information acquired during wakefulness. According to the Standard Model of memory consolidation, during wakefulness the hippocampus receives input from neocortical regions involved in the initial encoding of an experience and binds this information into a coherent memory trace that is then transferred to the neocortex during SWS where it is stored and integrated within preexisting memory traces. Evidence suggests that this process selectively involves direct connections from the hippocampus to the prefrontal cortex (PFC), a multimodal, high-order association region implicated in coordinating the storage and recall of remote memories in the neocortex. The slow-oscillation is thought to orchestrate the transfer of information from the hippocampus by temporally coupling hippocampal sharp-wave/ripples (SWRs) and thalamocortical spindles. SWRs are synchronous bursts of hippocampal activity, during which waking neuronal firing patterns are reactivated in the hippocampus and neocortex in a coordinated manner. Thalamocortical spindles are brief 7–14 Hz oscillations that may facilitate the encoding of information reactivated during SWRs. By temporally coupling the readout of information from the hippocampus with conditions conducive to encoding in the neocortex, the slow-oscillation is thought to mediate the transfer of information from the hippocampus to the neocortex. Although several lines of evidence are consistent with this function for mammalian SWS, it is unclear whether SWS serves a similar function in birds, the only taxonomic group other than mammals to exhibit SWS and REM sleep. Based on our review of research on avian sleep, neuroanatomy, and memory, although involved in some forms of memory consolidation, avian sleep does not appear to be involved in transferring hippocampal memories to other brain regions. Despite exhibiting the slow-oscillation, SWRs and spindles have not been found in birds. Moreover, although birds independently evolved a brain region – the caudolateral nidopallium (NCL) – involved in performing high-order cognitive functions similar to those performed by the PFC, direct connections between the NCL and hippocampus have not been found in birds, and evidence for the transfer of information from the hippocampus to the NCL or other extra-hippocampal regions is lacking. Although based on the absence of evidence for various traits, collectively, these findings suggest that unlike mammalian SWS, avian SWS may not be involved in transferring memories from the hippocampus. Furthermore, it suggests that the slow-oscillation, the defining feature of mammalian and avian SWS, may serve a more general function independent of that related to coordinating the transfer of information from the hippocampus to the PFC in mammals. Given that SWS is homeostatically regulated (a process intimately related to the slow-oscillation) in mammals and birds, functional hypotheses linked to this process may apply to both taxonomic groups.

All animals in which sleep has been studied express signs of sleep-like behaviour, suggesting that sleep must have some fundamental functions that are sustained by natural selection. Those functions, however, are still not clear. Here, we examine the ecological relevance of sleep from the perspective of behavioural trade-offs that might affect fitness. Specifically, we highlight the advantage of using food-caching animals as a system in which a conflict might occur between engaging in sleep for memory/learning and hypothermia/torpor to conserve energy. We briefly review the evidence for the importance of sleep for memory, the importance of memory for food-caching animals and the conflicts that might occur between sleep and energy conservation in these animals. We suggest that the food-caching paradigm represents a naturalistic and experimentally practical system that provides the opportunity for a new direction in sleep research that will expand our understanding of sleep, especially within the context of ecological and evolutionary processes.

The comparative methods of evolutionary biology are a useful tool for investigating the functions of sleep. These techniques can help determine whether experimental results, derived from a single or few species, apply broadly across a specified group of animals. In this way, comparative analysis is a powerful complement to experimentation. The variation in the time mammalian species spend asleep has been most amenable for use with this approach, given the large number of mammals for which sleep data exist. Here, it is assumed that interspecific variation in the time spent asleep reflects underlying differences in the need for sleep. If true, then significant predictors of sleep times should provide insight into the function of sleep. Many such analyses have sought the evolutionary determinants of mammalian sleep by relating the time spent in the two basic states of sleep, rapid eye movement (REM) and non-REM sleep, to constitutive variables thought to be functionally related to sleep. However, the early analyses had several methodological problems, and recent re-analyses have overturned some widely accepted relationships, such as the idea that species with higher metabolic rates engage in more sleep. These more recent studies also provide evolutionarily broad support for a neurophysiological role for REM sleep. Furthermore, results from comparative analyses suggest that animals are particularly vulnerable to predation during REM sleep, a finding that lends further support to the notion that REM sleep must serve an important function. Here, we review the methodology and results of quantitative comparative studies of sleep. We highlight important developments in our understanding of the evolutionary determinants of sleep and emphasize relationships that address prevailing hypotheses for the functions of sleep. Lastly, we outline a possible future for comparative analyses, focusing on work in non-mammalian groups, the use of more physiologically meaningful variables, and electrophysiological sleep studies conducted in the wild.

Birds are the only taxonomic group other than mammals that exhibit high-amplitude slow-waves in the electroencephalogram (EEG) during sleep. This defining feature of slow-wave sleep (SWS) apparently evolved independently in mammals and birds, as reptiles do not exhibit similar EEG activity during sleep. In mammals, the level of slow-wave activity (SWA) (low-frequency spectral power density) during SWS increases and decreases as a function of prior time spent awake and asleep, respectively, and therefore reflects homeostatically regulated sleep processes potentially tied to the function of SWS. Although birds also exhibit SWS, previous sleep deprivation studies in birds did not detect a compensatory increase in SWS-related SWA during recovery, as observed in similarly sleep-deprived mammals. This suggested that, unlike mammalian SWS, avian SWS is not homeostatically regulated, and therefore might serve a different function. However, we recently demonstrated that SWA during SWS increases in pigeons following short-term sleep deprivation. Herein we summarize research on avian sleep homeostasis, and cast our evidence for this phenomenon within the context of theories for the function of SWS in mammals. We propose that the convergent evolution of homeostatically regulated SWS in mammals and birds was directly linked to the convergent evolution of large, heavily interconnected brains capable of performing complex cognitive processes in each group. Specifically, as has been proposed for mammals, the interconnectivity that forms the basis of complex cognition in birds may also instantiate slow, synchronous network oscillations during SWS that in turn maintain interconnectivity and cognition at an optimal level.

Summary Birds provide a unique opportunity to evaluate current theories for the function of sleep. Like mammalian sleep, avian sleep is composed of two states, slow-wave sleep (SWS) and rapid eye-movement (REM) sleep that apparently evolved independently in mammals and birds. Despite this resemblance, however, it has been unclear whether avian SWS shows a compensatory response to sleep loss (i.e., homeostatic regulation), a fundamental aspect of mammalian sleep potentially linked to the function of SWS. Here, we prevented pigeons (Columba livia) from taking their normal naps during the last 8 h of the day. Although time spent in SWS did not change significantly following short-term sleep deprivation, electroencephalogram (EEG) slow-wave activity (SWA; i.e., 0.78–2.34 Hz power density) during SWS increased significantly during the first 3 h of the recovery night when compared with the undisturbed night, and progressively declined thereafter in a manner comparable to that observed in similarly sleep-deprived mammals. SWA was also elevated during REM sleep on the recovery night, a response that might reflect increased SWS pressure and the concomitant ‘spill-over’ of SWS-related EEG activity into short episodes of REM sleep. As in rodents, power density during SWS also increased in higher frequencies (9–25 Hz) in response to short-term sleep deprivation. Finally, time spent in REM sleep increased following sleep deprivation. The mammalian-like increase in EEG spectral power density across both low and high frequencies, and the increase in time spent in REM sleep following sleep deprivation suggest that some aspects of avian and mammalian sleep are regulated in a similar manner.

A well-defined sleep deprivation (SD) syndrome has been observed in studies with rats under conditions of severe sleep loss on the Disk-Over-Water (DOW) apparatus. Observation of the sleep deprivation syndrome across taxa would assist in the elucidation of the function of sleep. In the present study, the effects of total sleep deprivation were assessed in pigeons, a biologically relevant choice given that birds are the only non-mammalian taxon known to exhibit unequivocal rapid-eye-movement (REM) sleep and non-REM (NREM) sleep. Pigeons were deprived of sleep for 24-29 days on the DOW by rotating the disk and requiring them to walk whenever sleep was initiated. Control (C) birds were also housed on the DOW and required to walk only when the deprived (D) birds were required to walk due to sleep initiation. NREM and REM sleep amounts were reduced from baseline during the deprivation for both D and C birds, although D birds obtained less NREM sleep than controls. Across the deprivation, D birds had their total sleep reduced by 54% of baseline (scored in 4 s epochs), whereas previous studies in rats on the DOW reported total sleep reduction of as much as 91% (scored in 30 s epochs). Pigeons proved to be more resistant to sleep deprivation by the DOW method and were much more difficult to deprive over the course of the experiment. Overall, the pigeons showed recovery sleep patterns similar to those seen in rats; i.e., rebound sleep during recovery was disproportionately composed of REM sleep. They did not, however, show the obvious external physical signs of the SD syndrome nor the large metabolic and thermoregulatory changes associated with the syndrome. The DOW method was thus effective in producing sleep loss in the pigeon, but was not as effective as it is in rats. The absence of the full SD syndrome is discussed in the context of limitations of the DOW apparatus and the possibility of species-specific adaptations that birds may possess to withstand or adapt to conditions of limited sleep opportunity.

Sleep appears to effect some sort of neural maintenance, but a complete theory of the function of sleep must address why such maintenance requires a behavioural shutdown (or unconsciousness) that leaves an animal vulnerable to predators. We present a simple, strategic model to determine the degree of sleep that minimizes the risk of predation. We assume that the brain is composed of neural units that can, in theory, ‘sleep’ independently of each other, and that a given neural unit must go offline for maintenance/sleep. We also assume that the probability of detecting an attack depends on the fraction of neural units that are awake. We found that having all neural units offline simultaneously (i.e. shutdown sleep) is often the safest way to perform neural maintenance, even though partial sleep makes predators more detectable. This counterintuitive result reflects the assumptions that, in a state of partial sleep, (1) neural maintenance takes longer to complete and (2) predator detection is less effective than suggested by the proportion of neural units online. Partial sleep is a possible outcome when the risk of attack increases as more neural units are taken offline. Minimal sleep (with only one or a few units offline) is a possible outcome when the attack rate while awake is substantially higher than when asleep. Partial sleep of a sort is known to occur in some animals, but there is no apparent evidence for the idea of minimal sleep.

Mammals and birds are the only animals that exhibit high-amplitude slow-waves (SWs) in the electroencephalogram during sleep. The SWs that characterize slow-wave sleep (SWS) in mammals and birds reflect the large-scale synchronization of slow neuronal activity. In mammals, this synchronization is dependent upon the high degree of interconnectivity within the neocortex, a cytoarchitectonic trait also found in the avian hyperpallium, but not the reptilian dorsal cortex. Consequently, I recently proposed that the presence of SWs in sleeping mammals and birds, and their absence in sleeping reptiles, is attributable to the greater degree of interconnectivity within the neocortex and hyperpallium when compared to the dorsal cortex [N.C. Rattenborg, Evolution of slow-wave sleep and palliopallial connectivity in mammals and birds: A hypothesis, Brain Res. Bull. 69 (2006) 20-29]. Rial et al. (this issue) challenge this hypothesis by noting that high-amplitude SWs occur in awake reptiles. Based largely on this observation, they suggest that SWS in homeotherms evolved from reptilian wakefulness. SWs in awake reptiles do not seem to reflect neural processes comparable to those that generate sleep-related SWs in homeotherms, however. Moreover, the proposed conversion of reptilian wakefulness into SWS is untenable from behavioral, mechanistic and functional perspectives. A more parsimonious explanation is that the precursor state to SWS in homeotherms was a state comparable to reptilian sleep, rather than wakefulness, with the primary difference being that the reptilian dorsal cortex lacks the interconnectivity necessary to generate sleep-related SWs in the electroencephalogram.

Every studied animal engages in sleep, and many animals spend much of their lives in this vulnerable behavioural state. We believe that an explicit description of this vulnerability will provide many insights into both the function and architecture (or organization) of sleep. Early studies of sleep recognized this idea, but it has been largely overlooked during the last 20 years. We critically evaluate early models that suggested that the function of sleep is antipredator in nature, and outline a new model in which we argue that whole-brain or ‘blackout’ sleep may be the safest way to sleep given a functionally interconnected brain. Early comparative work also suggested that the predatory environment is an important determinant of sleep architecture. For example, species that sleep in risky environments spend less time in the relatively vulnerable states of sleep. Recent experimental work suggests that mammals and birds shift to relatively vigilant (lighter) states of sleep in response to an increase in perceived risk; these results mirror the influence of stress on sleep in humans and rats. We also outline a conceptual model of sleep architecture in which dynamic changes in sleep states reflect a trade-off between the benefits of reducing a sleep debt and the cost of predation. Overall, many aspects of plasticity in sleep related to predation risk require further study, as do the ways in which sleeping animals monitor predatory threats. More work outside of the dominant mammalian paradigm in sleep is also needed. An ecologically based view of sleeping under the risk of predation will provide an important complement to the traditional physiological and neurological approaches to studying sleep and its functions.

In addition to entraining circadian rhythms, light has acute effects on sleep and wakefulness in mammals. To determine whether light and darkness have similar effects in birds, the only non-mammalian group that displays sleep patterns comparable to mammals, we examined the effects of lighting changes on sleep and wakefulness in the pigeon. We quantified sleep behavior (i.e., bilateral or unilateral eye closure) in pigeons maintained under a 12:12 LD cycle, and immediately following a change from a 12:12 to a 3:3 LD cycle. During both LD cycles, sleep was most prevalent during dark periods. During the 3:3 LD cycle, darkness had the greatest sleep promoting effect during the hours corresponding to the subjective night of the preceding 12:12 LD cycle, whereas light suppressed sleep across circadian phases. As previously suggested, the light-induced decrease in sleep in the subjective night might be partly mediated by the suppression of melatonin by light. Although the sleep promoting effect of darkness was modulated by the circadian rhythm, sleep in darkness occurred during all circadian phases, suggesting that darkness per se may play a direct role in inducing sleep. In addition to the effects of lighting on behavioral state, we observed an overall bias toward more right eye closure under all lighting conditions, possibly reflecting a response to the novel testing environment.

SummaryImaging of the chicken embryo in the egg has revealed that the entire brain can be switched on for the first time earlier than expected by exposure to maternal vocalizations.

Study objectives Interspecific variation in sleep measured in captivity correlates with various physiological and environmental factors, including estimates of predation risk in the wild. However, it remains unclear whether prior comparative studies have been confounded by the captive recording environment. Herein we examine the effect of predation pressure on sleep in sloths living in the wild. Design Comparison of two closely related sloth species, one exposed to predation and one free from predation. Setting Panamanian mainland rainforest (predators present) and island mangrove (predators absent). Participants Mainland (Bradypus variegatus, five males and four females) and island (Bradypus pygmaeus, six males) sloths. Interventions None. Measurements and results Electroencephalographic (EEG) and electromyographic (EMG) activity was recorded using a miniature data logger. Although both species spent between 9 and 10 h per day sleeping, the mainland sloths showed a preference for sleeping at night, whereas island sloths showed no preference for sleeping during the day or night. Standardized EEG activity during nonrapid eye movement (NREM) sleep showed lower low-frequency power, and increased spindle and higher frequency power in island sloths when compared to mainland sloths. Conclusions In sloths sleeping in the wild, predation pressure influenced the timing of sleep, but not the amount of time spent asleep. The preference for sleeping at night in mainland sloths may be a strategy to avoid detection by nocturnal cats. The pronounced differences in the NREM sleep EEG spectrum remain unexplained, but might be related to genetic or environmental factors.

Understanding the function of variation in sleep requires studies in the natural ecological conditions in which sleep evolved. Sleep has an impact on individual performance and hence may integrate the costs and benefits of investing in processes that are sensitive to sleep, such as immunity or coping with stress. Because dark and pale melanic animals differentially regulate energy homeostasis, immunity and stress hormone levels, the amount and/or organization of sleep may covary with melanin-based colour. We show here that wild, cross-fostered nestling barn owls (Tyto alba) born from mothers displaying more black spots had shorter non-REM (rapid eye movement) sleep bouts, a shorter latency until the occurrence of REM sleep after a bout of wakefulness and more wakefulness bouts. In male nestlings, the same sleep traits also correlated with their own level of spotting. Because heavily spotted male nestlings and the offspring of heavily spotted biological mothers switched sleep-wakefulness states more frequently, we propose the hypothesis that they could be also behaviourally more vigilant. Accordingly, nestlings from mothers displaying many black spots looked more often towards the nest entrance where their parents bring food and towards their sibling against whom they compete. Owlets from heavily spotted mothers might invest more in vigilance, thereby possibly increasing associated costs due to sleep fragmentation. We conclude that different strategies of the regulation of brain activity have evolved and are correlated with melanin-based coloration.

Aquatic mammals (i.e., Cetaceans, eared seals and manatees) and birds show interhemispheric asymmetries (IA) in slow-wave sleep-related electroencephalographic (EEG) activity, suggesting that the depth of sleep differs between hemispheres. In birds, an association between unilateral eye closure and IA has been reported in five species from three orders (i.e., Galliformes, Charadriiformes, and Anseriformes). Moreover, unilateral eye closure has been observed during behaviorally defined sleep in 29 species from 13 avian orders, suggesting that birds in general display IA during sleep. Despite the apparent prevalence of unilateral eye closure and IA in birds, previous work did not detect IA in the pigeon, thereby challenging the conclusion that this is a general feature of birds. Using digital period amplitude analysis, an objective method for quantifying EEG power (a measure of wave amplitude) across different frequencies, we demonstrate that pigeons do, in fact, display an association between unilateral eye closure and IA. For a given hemisphere, standardized 2–4 Hz EEG power was greater when the contralateral eye was closed when compared to open. We also found that pigeons used the open eye during IA to monitor their environment. In addition, individual pigeons showed a bias for keeping one eye open more than the other. The direction (left vs. right) of this bias differed across birds, and appeared to be influenced by the structure of the surrounding environment. Finally, with the addition of pigeons (order Columbiformes), IA associated with unilateral eye closure has been recorded in four avian orders, suggesting that this form of sleep is widespread in birds.

Several animals mitigate the fundamental conflict between sleep and wakefulness by engaging in unihemispheric sleep, a unique state during which one cerebral hemisphere sleeps while the other remains awake. Among mammals, unihemispheric sleep is restricted to aquatic species (Cetaceans, eared seals and manatees). In contrast to mammals, unihemispheric sleep is widespread in birds, and may even occur in reptiles. Unihemispheric sleep allows surfacing to breathe in aquatic mammals and predator detection in birds. Despite the apparent utility in being able to sleep unihemispherically, very few mammals sleep in this manner. This is particularly interesting since the reptilian ancestors to mammals may have slept unihemispherically. The relative absence of unihemispheric sleep in mammals suggests that a trade off exists between unihemispheric sleep and other adaptive brain functions occurring during sleep or wakefulness. Presumably, the benefits of sleeping unihemispherically only outweigh the costs under extreme circumstances such as sleeping at sea. Ultimately, a greater understanding of the reasons for little unihemispheric sleep in mammals promises to provide insight into the functions of sleep, in general.

In their review in PNAS, Allen and Fortin use a comparative neuroanatomical approach to gain insight into the evolution of episodic memory (1). The authors suggest that, as in humans, episodic-like memory in nonhuman mammals depends on a system consisting of the hippocampus, parahippocampal region, and prefrontal cortex (PFC), and, in birds, a similar system consisting of the hippocampus, area parahippocampalis, and nidopallium caudolaterale (NCL), the avian analog of the PFC. Although we agree that the behavioral evidence for episodic-like memory in birds is compelling, in contrast to Allen and Fortin, our interpretation of the available neuroanatomical evidence indicates that key components of this system are missing in birds. In mammals, the PFC is thought to assess the relevance of episodic memories recalled from the hippocampus via its connections with the hippocampus, parahippocampal region, and other higher association areas reactivated during recall and to, then, orchestrate behavior accordingly through projections to motor areas (1). Like the PFC, the NCL is reciprocally connected to higher association and motor output regions and appears to perform executive functions (2). However, of the laboratories (at least four) that have addressed this question, none has detected connections between the NCL and the area parahippocampalis or hippocampus (3) (reviewed in ref. 4). This may be related to the fact that the PFC and NCL are analogous structures that evolved independently and develop from different parts of the pallium; in mammals, the PFC develops from the dorsal pallium, whereas in birds the NCL and the rest of the dorsal ventricular ridge (DVR) develop from the lateral and ventral pallium (5). Interestingly, in birds, rather than developing into a higher-order multimodal association area, such as the PFC, the dorsal pallium develops into the hyperpallium, a structure composed of primary visual and somatosensory/motor subregions (5). Nonetheless, consistent with its developmental homology with mammalian dorsal pallial derivatives, the hyperpallium shares PFC-like connections to the hippocampus, area parahippocampalis, and motor output regions (5) and, as suggested by Bingman and coworkers, may bridge the apparent gap between the hippocampus and NCL by conveying spatial (visual and olfactory) information via known projections to the NCL (3). The NCL could then integrate this information with that received from other association regions in the DVR and, thereby, orchestrate adaptive behaviors. Although this pathway may provide a route for integrating information processed by the hippocampus, hyperpallium, and DVR, additional differences exist between birds and mammals that likely influence the nature of episodic-like memory in the two groups. Unlike mammals, wherein highly processed information from virtually the entire neocortex converges in the hippocampus, enabling it to serve as a node for rapidly encoding experiences and initiating their recall, the avian hippocampus only receives olfactory and visual input and is not privy to much of the information processed by association regions in the DVR (nidopallium and mesopallium), in addition to the NCL (4). Given these fundamental differences in neuroanatomy, to the extent that episodic-like memory depends on information reaching the hippocampus, such memories may be qualitatively different between birds and mammals.

The function of sleep remains elusive. Here, we illustrate the unique usefulness of the study of avian sleep for identifying the purpose of sleep in mammals, including humans. Birds are the only nonmammalian taxonomic group to engage in rapid-eye movement (REM) sleep and non-REM sleep. The fundamental function of these states is one that is present in both groups, and must therefore relate to a feature of sleep present in mammals and birds alike. Such features include ‘cortical’ activation during REM sleep and the slow oscillation underlying non-REM sleep. Using this bird's perspective on the sleeping brain, we contrast two prominent hypotheses for the function of non-REM sleep.

You Snooze, You Lose Sleep serves restorative and memory functions, but it does not always operate analogously across species. Deferral of sleep may be possible when selection strongly favors the awake. Lesku et al. (p. 1654 ; see the Perspective by Siegel ) show that sleep may be deferred without cost or impairment in pectoral sandpipers. These birds breed collectively in the high Arctic, and male competition is intense. Competing for, and displaying to, females are both physically and cognitively demanding, yet birds who slept the least showed no decrease in their ability to perform these activities. Indeed, those males who slept the least obtained the most matings and sired the most offspring.

Summary In most mammals, sleep is composed of two distinct states, rapid eye movement (REM) sleep and slow-wave sleep (SWS). The differentiated nature of mammalian sleep suggests that each state performs a different function, or perhaps different, but complementary components of a unified function. Despite extensive research, the function(s) provided by sleep and its respective sub-states remains the subject of debate (Cirelli and Tononi, 2008; Mignot, 2008; Siegel, 2009; Stickgold and Walker, 2007). One approach to unraveling the function of each sleep state is to trace its evolution. Through identifying the type(s) of animals in which each state evolved, we may reveal biological traits that coevolved with a particular sleep state. Cases of convergent evolution may be particularly informative because they provide the opportunity to isolate traits shared by only those animals that evolved a particular sleep state. The independent coevolution of certain sleep states and traits may be functionally linked. Conversely, the subsequent coevolutionary loss of a particular sleep state and certain traits may also reveal traits that benefit from a particular sleep state. Moreover, assuming that sleep serves an important function, determining how such animals compensate for the loss of a particular sleep state may yield clues to its purpose. Finally, another approach is to identify biological traits that account for the variation in time spent in, and presumably need for, each state. Traits that influence the allocation of time to a particular state may suggest a function for that state. The following chapter summarizes insights into the function of REM sleep gleaned from these comparative approaches.

The function of the brain activity that defines slow wave sleep (SWS) and rapid eye movement (REM) sleep in mammals is unknown. During SWS, the level of electroencephalogram slow wave activity (SWA or 0.5–4.5 Hz power density) increases and decreases as a function of prior time spent awake and asleep, respectively. Such dynamics occur in response to waking brain use, as SWA increases locally in brain regions used more extensively during prior wakefulness. Thus, SWA is thought to reflect homeostatically regulated processes potentially tied to maintaining optimal brain functioning. Interestingly, birds also engage in SWS and REM sleep, a similarity that arose via convergent evolution, as sleeping reptiles and amphibians do not show similar brain activity. Although birds deprived of sleep show global increases in SWA during subsequent sleep, it is unclear whether avian sleep is likewise regulated locally. Here, we provide, to our knowledge, the first electrophysiological evidence for local sleep homeostasis in the avian brain. After staying awake watching David Attenborough's The Life of Birds with only one eye, SWA and the slope of slow waves (a purported marker of synaptic strength) increased only in the hyperpallium—a primary visual processing region—neurologically connected to the stimulated eye. Asymmetries were specific to the hyperpallium, as the non-visual mesopallium showed a symmetric increase in SWA and wave slope. Thus, hypotheses for the function of mammalian SWS that rely on local sleep homeostasis may apply also to birds.