Search

Every spring and fall, billions of songbirds fly thousands of miles between their summer breeding grounds in North America and their wintering grounds in the more hospitable climes of southern California, Mexico, and Central and South America. Many aspects of this remarkable voyage remain obscure, especially if, and how, nocturnal migrators get any sleep at night. Field observations indicate that presumably sleep-deprived fliers appear no worse for wear, foraging, navigating, and avoiding predators with aplomb. Results suggest that wild songbirds drastically reduce sleep time during migration.

Besides regulating the amount of light that reaches the retina, fluctuations in pupil size also occur in isoluminant conditions during accommodation, during movement and in relation to cognitive workload, attention and emotion. Recent studies in mammals and birds revealed that the pupils are also highly dynamic in the dark during sleep. However, despite exhibiting similar sleep states (rapid eye movement [REM] and non-REM [NREM] sleep), wake and sleep state-dependent changes in pupil size are opposite between mammals and birds, due in part to differences in the type (striated vs. smooth) and control of the iris muscles. Given the link between pupil dynamics and cognitive processes occurring during wakefulness, sleep-related changes in pupil size might indicate when related processes are occurring during sleep. Moreover, the divergent pupillary behaviour observed between mammals and birds raises the possibility that changes in pupil size in birds are a readout of processes not reflected in the mammalian pupil., (© 2023 The Authors. European Journal of Neuroscience published by Federation of European Neuroscience Societies and John Wiley & Sons Ltd.)

We examined the presence/absence and parcellation of cholinergic neurons in the hypothalami of five birds: a Congo grey parrot (Psittacus erithacus), a Timneh grey parrot (P. timneh), a pied crow (Corvus albus), a common ostrich (Struthio camelus), and an emu (Dromaius novaehollandiae). Using immunohistochemistry to an antibody raised against the enzyme choline acetyltransferase, hypothalamic cholinergic neurons were observed in six distinct clusters in the medial, lateral, and ventral hypothalamus in the parrots and crow, similar to prior observations made in the pigeon. The expression of cholinergic nuclei was most prominent in the Congo grey parrot, both in the medial and lateral hypothalamus. In contrast, no evidence of cholinergic neurons in the hypothalami of either the ostrich or emu was found. It is known that the expression of sleep states in the ostrich is unusual and resembles that observed in the monotremes that also lack hypothalamic cholinergic neurons. It has been proposed that the cholinergic system acts globally to produce and maintain brain states, such as those of arousal and rapid-eye-movement sleep. The hiatus in the cholinergic system of the ostrich, due to the lack of hypothalamic cholinergic neurons, may explain, in part, the unusual expression of sleep states in this species. These comparative anatomical and sleep studies provide supportive evidence for global cholinergic actions and may provide an important framework for our understanding of one broad function of the cholinergic system and possible dysfunctions associated with global cholinergic neural activity., (© 2024 The Authors. The Journal of Comparative Neurology published by Wiley Periodicals LLC.)

Microsleeps, the seconds-long interruptions of wakefulness by eye closure and sleep-related brain activity, are dangerous when driving and might be too short to provide the restorative functions of sleep. If microsleeps do fulfill sleep functions, then animals faced with a continuous need for vigilance might resort to this sleep strategy. We investigated electroencephalographically defined sleep in wild chinstrap penguins, at sea and while nesting in Antarctica, constantly exposed to an egg predator and aggression from other penguins. The penguins nodded off >10,000 times per day, engaging in bouts of bihemispheric and unihemispheric slow-wave sleep lasting on average only 4 seconds, but resulting in the accumulation of >11 hours of sleep for each hemisphere. The investment in microsleeps by successfully breeding penguins suggests that the benefits of sleep can accrue incrementally.

Findings in marine mammals and birds provide opportunities to explore sleep's functions.

Mammalian sleep has been implicated in maintaining a healthy extracellular environment in the brain. During wakefulness, neuronal activity leads to the accumulation of toxic proteins, which the glymphatic system is thought to clear by flushing cerebral spinal fluid (CSF) through the brain. In mice, this process occurs during non-rapid eye movement (NREM) sleep. In humans, ventricular CSF flow has also been shown to increase during NREM sleep, as visualized using functional magnetic resonance imaging (fMRI). The link between sleep and CSF flow has not been studied in birds before. Using fMRI of naturally sleeping pigeons, we show that REM sleep, a paradoxical state with wake-like brain activity, is accompanied by the activation of brain regions involved in processing visual information, including optic flow during flight. We further demonstrate that ventricular CSF flow increases during NREM sleep, relative to wakefulness, but drops sharply during REM sleep. Consequently, functions linked to brain activation during REM sleep might come at the expense of waste clearance during NREM sleep., (© 2023. The Author(s).)

Storms can cause widespread seabird stranding and wrecking, 1 , 2 , 3 , 4 , 5 yet little is known about the maximum wind speeds that birds are able to tolerate or the conditions they avoid. We analyzed >300,000 h of tracking data from 18 seabird species, including flapping and soaring fliers, to assess how flight morphology affects wind selectivity, both at fine scales (hourly movement steps) and across the breeding season. We found no general preference or avoidance of particular wind speeds within foraging tracks. This suggests seabird flight morphology is adapted to a "wind niche," with higher wing loading being selected in windier environments. In support of this, wing loading was positively related to the median wind speeds on the breeding grounds, as well as the maximum wind speeds in which birds flew. Yet globally, the highest wind speeds occur in the tropics (in association with tropical cyclones) where birds are morphologically adapted to low median wind speeds. Tropical species must therefore show behavioral responses to extreme winds, including long-range avoidance of wind speeds that can be twice their operable maxima. By contrast, Procellariiformes flew in almost all wind speeds they encountered at a seasonal scale. Despite this, we describe a small number of cases where albatrosses avoided strong winds at close range, including by flying into the eye of the storm. Extreme winds appear to pose context-dependent risks to seabirds, and more information is needed on the factors that determine the hierarchy of risk, given the impact of global change on storm intensity. 6 , 7 ., Competing Interests: Declaration of interests The authors declare no competing interests., (Copyright © 2023 Elsevier Inc. All rights reserved.)

The evolutionary origins of sleep and its sub-states, rapid eye movement (REM) and non-REM (NREM) sleep, found in mammals and birds, remain a mystery. Although the discovery of a single type of sleep in jellyfish suggests that sleep evolved much earlier than previously thought, it is unclear when and why sleep diversified into multiple types of sleep. Intriguingly, multiple types of sleep have recently been found in animals ranging from non-avian reptiles to arthropods to cephalopods. Although there are similarities between these states and those found in mammals and birds, notable differences also exist. The diversity in the way sleep is expressed confounds attempts to trace the evolution of sleep states, but also serves as a rich resource for exploring the functions of sleep., Competing Interests: Declaration of interests No interests are declared., (Copyright © 2022 Elsevier Ltd. All rights reserved.)

Sleep serves many important functions. And yet, emerging studies over the last decade indicate that some species routinely sleep little, or can temporarily restrict their sleep to low levels, seemingly without cost. Taken together, these systems challenge the prevalent view of sleep as an essential state on which waking performance depends. Here, we review diverse case-studies, including elephant matriarchs, post-partum cetaceans, seawater sleeping fur seals, soaring seabirds, birds breeding in the high Arctic, captive cavefish, and sexually aroused fruit flies. We evaluate the likelihood of mechanisms that might allow more sleep than is presently appreciated. But even then, it appears these species are indeed performing well on little sleep. The costs, if any, remain unclear. Either these species have evolved a (yet undescribed) ability to supplant sleep needs, or they endure a (yet undescribed) cost. In both cases, there is urgent need for the study of non-traditional species so we can fully appreciate the extent, causes, and consequences of ecological sleep loss., (© The Author(s) 2022. Published by Oxford University Press on behalf of Sleep Research Society.)

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., (© 2021 The Authors. Journal of Sleep Research published by John Wiley & Sons Ltd on behalf of European Sleep Research Society.)

Mammalian pupils respond to light 1 , 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 sleep 4-7 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., Competing Interests: Declaration of interests The authors declare no competing interests., (Copyright © 2021 Elsevier Inc. All rights reserved.)

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 Research Society 2020. Published by Oxford University Press on behalf of the Sleep Research Society.)

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., Competing Interests: Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper., (Copyright © 2021 The Authors. Published by Elsevier Ltd.. All rights reserved.)

Rapid eye movement (REM) sleep is a paradoxical state of wake-like brain activity occurring after non-REM (NREM) sleep in mammals and birds. In mammals, brain cooling during NREM sleep is followed by warming during REM sleep, potentially preparing the brain to perform adaptively upon awakening. If brain warming is the primary function of REM sleep, then it should occur in other animals with similar states. We measured cortical temperature in pigeons and bearded dragons, lizards that exhibit NREM-like sleep and REM-like sleep with brain activity resembling wakefulness. In pigeons, cortical temperature decreased during NREM sleep and increased during REM sleep. However, brain temperature did not increase when dragons switched from NREM-like to REM-like sleep. Our findings indicate that brain warming is not a universal outcome of sleep states characterized by wake-like activity, challenging the hypothesis that their primary function is to warm the brain in preparation for wakefulness., Competing Interests: The authors declare no competing interests., (© 2020 The Authors.)

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., (© 2020 The Authors. European Journal of Neuroscience published by Federation of European Neuroscience Societies and John Wiley & Sons Ltd.)

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 Research Society 2019. Published by Oxford University Press on behalf of the Sleep Research Society.)

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., Competing Interests: Declaration of Interests The authors declare no competing interests., (Copyright © 2020 Elsevier Inc. All rights reserved.)

Little is known about how songbirds modulate sleep during migratory periods. Due to the alternation of nocturnal endurance flights and diurnal refueling stopovers, sleep is likely to be a major constraint for many migratory passerine species. Sleep may help to increase the endogenous antioxidant capacity that counteracts free radicals produced during endurance flight and reduces energy expenditure. Here, we investigated the relationship between sleep behavior, food intake, and two markers of physiological condition-the amount of energy reserves and oxidative status-in two migratory songbird species, the garden warbler ( Sylvia borin ) and the whitethroat ( Sylvia communis ). In garden warblers, birds with high energy stores were more prone to sleep during the day, while this condition-dependent sleep pattern was not present in whitethroats. In both species, birds with low energy stores were more likely to sleep with their head tucked in the feathers during nocturnal sleep. Moreover, we found a positive correlation between food intake and the extent of energy reserves in garden warblers, but not in whitethroats. Finally, we did not find significant correlations between oxidative status and sleep, or oxidative status and energy stores. Despite our study was not comparative, it suggests that different species might use different strategies to manage their energy during stopover and, additionally, it raises the possibility that migrants have evolved physiological adaptations to deal with oxidative damage produced during migration., (© The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology.)

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., (Copyright © 2019 Elsevier Ltd. All rights reserved.)

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., (Copyright © 2019 The Author(s). Published by Elsevier Ltd.. All rights reserved.)

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., (Copyright © 2019 Elsevier Ltd. All rights reserved.)

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.

Birds exhibit two types of sleep that are in many respects similar to mammalian rapid eye movement (REM) and non-REM (NREM) sleep. As in mammals, several aspects of avian sleep can occur in a local manner within the brain. Electrophysiological evidence of NREM sleep occurring more deeply in one hemisphere, or only in one hemisphere - the latter being a phenomenon most pronounced in dolphins - was actually first described in birds. Such asymmetric or unihemispheric NREM sleep occurs with one eye open, enabling birds to visually monitor their environment for predators. Frigatebirds primarily engage in this form of sleep in flight, perhaps to avoid collisions with other birds. In addition to interhemispheric differences in NREM sleep intensity, the intensity of NREM sleep is homeostatically regulated in a local, use-depended manner within each hemisphere. Furthermore, the intensity and temporo-spatial distribution of NREM sleep-related slow waves varies across layers of the avian hyperpallium - a primary visual area - with the slow waves occurring first in, and propagating through and outward from, thalamic input layers. Slow waves also have the greatest amplitude in these layers. Although most research has focused on NREM sleep, there are also local aspects to avian REM sleep. REM sleep-related reductions in skeletal muscle tone appear largely restricted to muscles involved in maintaining head posture. Other local aspects of sleep manifest as a mixture of features of NREM and REM sleep occurring simultaneously in different parts of the neuroaxis. Like monotreme mammals, ostriches often exhibit brainstem-mediated features of REM sleep (muscle atonia and REMs) while the hyperpallium shows EEG slow waves typical of NREM sleep. Finally, although mice show slow waves in thalamic input layers of primary sensory cortices during REM sleep, this is not the case in the hyperpallium of pigeons, suggesting that this phenomenon is not a universal feature of REM sleep. Collectively, the local aspects of sleep described in birds and mammals reveal that wakefulness, NREM sleep, and REM sleep are not always discrete states.

Propagating slow-waves in electroencephalogram (EEG) or local field potential (LFP) recordings occur during non-rapid eye-movement (NREM) sleep in both mammals and birds. Moreover, in both, input from the thalamus is thought to contribute to the genesis of NREM sleep slow-waves. Interestingly, the general features of slow-waves are also found under isoflurane anesthesia. However, it is unclear to what extent these slow-waves reflect the same processes as those giving rise to NREM sleep slow-waves. Similar slow-wave spatio-temporal properties during NREM sleep and isoflurane anesthesia would suggest that both types of slow-waves are based on related processes. We used a 32-channel silicon probe connected to a transmitter to make intra-cortical recordings of the visual hyperpallium in naturally sleeping and isoflurane anesthetized pigeons ( Columba livia ) using a within-bird design. Under anesthesia, the amplitude of LFP slow-waves was higher when compared to NREM sleep. Spectral power density across all frequencies (1.5-100 Hz) was also elevated. In addition, slow-wave coherence between electrode sites was higher under anesthesia, indicating higher synchrony when compared to NREM sleep. Nonetheless, the spatial distribution of slow-waves under anesthesia was more comparable to NREM sleep than to wake or REM sleep. Similar to NREM sleep, slow-wave propagation under anesthesia mainly occurred in the thalamic input layers of the hyperpallium, regions which also showed the greatest slow-wave power during both recording conditions. This suggests that the thalamus could be involved in the genesis of slow-waves under both conditions. Taken together, although slow-waves under isoflurane anesthesia are stronger, they share spatio-temporal activity characteristics with slow-waves during NREM sleep.

Manual scoring of polysomnography data is labor-intensive and time-consuming, and most existing software does not account for subjective differences and user variability. Therefore, we evaluated a supervised machine learning algorithm, Somnivore TM , for automated wake-sleep stage classification. We designed an algorithm that extracts features from various input channels, following a brief session of manual scoring, and provides automated wake-sleep stage classification for each recording. For algorithm validation, polysomnography data was obtained from independent laboratories, and include normal, cognitively-impaired, and alcohol-treated human subjects (total n = 52), narcoleptic mice and drug-treated rats (total n = 56), and pigeons ( n = 5). Training and testing sets for validation were previously scored manually by 1-2 trained sleep technologists from each laboratory. F -measure was used to assess precision and sensitivity for statistical analysis of classifier output and human scorer agreement. The algorithm gave high concordance with manual visual scoring across all human data (wake 0.91 ± 0.01; N1 0.57 ± 0.01; N2 0.81 ± 0.01; N3 0.86 ± 0.01; REM 0.87 ± 0.01), which was comparable to manual inter-scorer agreement on all stages. Similarly, high concordance was observed across all rodent (wake 0.95 ± 0.01; NREM 0.94 ± 0.01; REM 0.91 ± 0.01) and pigeon (wake 0.96 ± 0.006; NREM 0.97 ± 0.01; REM 0.86 ± 0.02) data. Effects of classifier learning from single signal inputs, simple stage reclassification, automated removal of transition epochs, and training set size were also examined. In summary, we have developed a polysomnography analysis program for automated sleep-stage classification of data from diverse species. Somnivore enables flexible, accurate, and high-throughput analysis of experimental and clinical sleep studies.

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 m 3 aviary in a social context with the device in the logger configuration, we demonstrate the feasibility of using the device in the field., (Copyright © 2018 Elsevier B.V. All rights reserved.)

Several mammalian-based theories propose that the varying patterns of neuronal activity occurring in wakefulness and sleep reflect different modes of information processing. Neocortical slow-waves, hippocampal sharp-wave ripples, and thalamocortical spindles occurring during mammalian non-rapid eye-movement (NREM) sleep are proposed to play a role in systems-level memory consolidation. Birds show similar NREM and REM (rapid eye-movement) sleep stages to mammals; however, it is unclear whether all neurophysiological rhythms implicated in mammalian memory consolidation are also present. Moreover, it is unknown whether the propagation of slow-waves described in the mammalian neocortex occurs in the avian "cortex" during natural NREM sleep. We used a 32-channel silicon probe connected to a transmitter to make intracerebral recordings of the visual hyperpallium and thalamus in naturally sleeping pigeons (Columba livia). As in the mammalian neocortex, slow-waves during NREM sleep propagated through the hyperpallium. Propagation primarily occurred in the thalamic input layers of the hyperpallium, regions that also showed the greatest slow-wave activity (SWA). Spindles were not detected in both the visual hyperpallium, including regions receiving thalamic input, and thalamus, using a recording method that readily detects spindles in mammals. Interestingly, during REM sleep fast gamma bursts in the hyperpallium (when present) were restricted to the thalamic input layers. In addition, unlike mice, the decrease in SWA from NREM to REM sleep was the greatest in these layers. Taken together, these variant and invariant neurophysiological aspects of avian and mammalian sleep suggest that there may be associated mechanistic and functional similarities and differences between avian and mammalian sleep.

Both mammals and birds exhibit two sleep states, slow wave sleep (SWS) and rapid eye movement (REM) sleep. Studying certain aspects of sleep-related electrophysiology in freely behaving animals can present numerous methodological constraints, particularly when even fine body movements interfere with electrophysiological signals. Interestingly, under light general anesthesia, mammals and birds also exhibit slow waves similar to those observed during natural SWS. For these reasons, slow waves occurring under general anesthesia are commonly used in the investigation of sleep-related neurophysiology. However, how spectral properties of slow waves induced by anesthesia correspond to those occurring during natural SWS in birds has yet to be investigated systematically. In this study, we systematically analyzed spectral properties of electroencephalographic (EEG) patterns of pigeons ( Columba livia ) occurring under two commonly used anesthetics, isoflurane and urethane. These data were compared with EEG patterns during natural sleep. Slow waves occurring during spontaneous SWS, and those induced with isoflurane and urethane all showed greatest absolute power in the slowest frequencies (<3 Hz). Isoflurane and urethane-induced slow waves had near-identical power spectra, and both had higher mean power than that observed during SWS for all frequencies examined (0-25 Hz). Interestingly, burst suppression EEG activity observed under deeper planes of isoflurane anesthesia could occur bihemispherically or unihemispherically. Electrophysiological patterns while under isoflurane and urethane share phenomenological and spectral similarities to those occurring during SWS, notably the generation of high amplitude, slow waves, and peak low-frequency power. These results build upon other studies which suggest that some anesthetics exert their effects by acting on natural sleep pathways. As such, anesthesia-induced slow waves appear to provide an acceptable model for researchers interested in investigating sleep-related slow waves utilizing electrophysiological methods not suitable for use in freely behaving birds.

Sleep in birds is composed of two distinct sub-states, remarkably similar to mammalian slow-wave sleep (SWS) and rapid eye movement (REM) sleep. However, it is unclear whether all aspects of mammalian sleep are present in birds. We examined whether birds suppress REM sleep in response to changes in sleeping conditions that presumably evoke an increase in perceived predation risk, as observed previously in rodents. Although pigeons sometimes sleep on the ground, they prefer to sleep on elevated perches at night, probably to avoid nocturnal mammalian ground predators. Few studies to date have investigated how roosting sites affect sleep architecture. We compared sleep in captive pigeons on days with and without access to high perches. On the first (baseline) day, low and high perches were available; on the second day, the high perches were removed; and on the third (recovery) day, the high perches were returned. The total time spent sleeping did not vary significantly between conditions; however, the time spent in REM sleep declined on the low-perch night and increased above baseline when the pigeons slept on the high perch during the recovery night. Although the amount of SWS did not vary significantly between conditions, SWS intensity was lower on the low-perch night, particularly early in the night. The similarity of these responses between birds and mammals suggests that REM sleep is influenced by at least some ecological factors in a similar manner in both groups of animals., Competing Interests: Competing interestsThe authors declare no competing or financial interests., (© 2018. Published by The Company of Biologists Ltd.)

Study Objectives: The changes in electroencephalogram (EEG) activity that characterize sleep and its sub-states-slow-wave sleep (SWS) and rapid eye movement (REM) sleep-are similar in mammals and birds. SWS is characterized by EEG slow waves resulting from the synchronous alternation of neuronal membrane potentials between hyperpolarized down-states with neuronal quiescence and depolarized up-states associated with action potentials. By contrast, studies of non-avian reptiles report the presence of high-voltage sharp waves (HShW) during sleep. How HShW relate to EEG phenomena occurring during mammalian and avian sleep is unclear. We investigated the spatiotemporal patterns of electrophysiological phenomena in Nile crocodiles (Crocodylus niloticus) anesthetized with isoflurane to determine whether they share similar spatiotemporal patterns to mammalian and avian slow waves., Methods: Recordings of anesthetized crocodiles were made using 64-channel penetrating arrays with electrodes arranged in an 8 × 8 equally spaced grid. The arrays were placed in the dorsal ventricular ridge (DVR), a region implicated in the genesis of HShW. Various aspects of the spatiotemporal distribution of recorded signals were investigated., Results: Recorded signals revealed the presence of HShW resembling those reported in earlier studies of naturally sleeping reptiles. HShW propagated in complex and variable patterns across the DVR., Conclusions: We demonstrate that HShW within the DVR propagate in complex patterns similar to those observed for avian slow waves recorded from homologous brain regions. Consequently, sleep with HShW may represent an ancestral form of SWS, characterized by up-states occurring less often and for a shorter duration than in mammals and birds.

Northern fur seals forego large amounts of rapid eye movement (REM) sleep when sleeping in water, but remain healthy and do not recover this loss once back on land, challenging current theories for the function of REM sleep., (Copyright © 2018 Elsevier Ltd. All rights reserved.)

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'., (© 2017 The Author(s).)

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.

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., (© 2017. Published by The Company of Biologists Ltd.)

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 -1 during 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.

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., (© 2017 S. Karger AG, Basel.)

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., (Copyright © 2016 IBRO. Published by Elsevier Ltd. All rights reserved.)

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.

Here, we propose an original approach to explain one of the great unresolved questions in animal biology: what is the function of sleep? Existing ecological and neurological approaches to this question have become roadblocks to an answer. Ecologists typically treat sleep as a simple behavior, instead of a heterogeneous neurophysiological state, while neuroscientists generally fail to appreciate the critical insights offered by the consideration of ecology and evolutionary history. Redressing these shortfalls requires cross-disciplinary integration. By bringing together aspects of behavioral ecology, evolution, and conservation with neurophysiology, we can achieve a more comprehensive understanding of sleep, including its implications for adaptive waking behavior and fitness., (Copyright © 2016 Elsevier Ltd. All rights reserved.)

Brain rhythms occurring during sleep are implicated in processing information acquired during wakefulness, but this phenomenon has almost exclusively been studied in mammals. In this review we discuss the potential value of utilizing birds to elucidate the functions and underlying mechanisms of such brain rhythms. Birds are of particular interest from a comparative perspective because even though neurons in the avian brain homologous to mammalian neocortical neurons are arranged in a nuclear, rather than a laminar manner, the avian brain generates mammalian-like sleep-states and associated brain rhythms. Nonetheless, until recently, this nuclear organization also posed technical challenges, as the standard surface EEG recording methods used to study the neocortex provide only a superficial view of the sleeping avian brain. The recent development of high-density multielectrode recording methods now provides access to sleep-related brain activity occurring deep in the avian brain. Finally, we discuss how intracerebral electrical imaging based on this technique can be used to elucidate the systems-level processing of hippocampal-dependent and imprinting memories in birds., (Copyright © 2014 Elsevier Ltd. All rights reserved.)

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., (© 2014 The Authors. Journal of Evolutionary Biology © 2014 European Society For Evolutionary Biology.)

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.

Background: In mammals, the slow-oscillations of neuronal membrane potentials (reflected in the electroencephalogram as high-amplitude, slow-waves), which occur during non-rapid eye movement sleep and anesthesia, propagate across the neocortex largely as two-dimensional traveling waves. However, it remains unknown if the traveling nature of slow-waves is unique to the laminar cytoarchitecture and associated computational properties of the neocortex., Results: We demonstrate that local field potential slow-waves and correlated multiunit activity propagate as complex three-dimensional plumes of neuronal activity through the avian brain, owing to its non-laminar, nuclear neuronal cytoarchitecture., Conclusions: The traveling nature of slow-waves is not dependent upon the laminar organization of the neocortex, and is unlikely to subserve functions unique to this pattern of neuronal organization. Finally, the three-dimensional geometry of propagating plumes may reflect computational properties not found in mammals that contributed to the evolution of nuclear neuronal organization and complex cognition in birds.