Niels Rattenborg

Max Planck Institute for Ornithology - Seewiesen · Avian Sleep Group

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...

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,...

Oceanic mesoscale systems are characterized by inherent variability. Climatic change adds entropy to this system, making it a highly variable environment in which marine species live. Being at the higher levels of the food chain, predators maximize their performance through plastic foraging strategies. Individual variability within a population and...

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...

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 sle...

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 costs. Taken together, these systems challenge the prevalent view of sleep as an essential state on which waking performance depends. Here,...

Understanding the characteristics of a species’s distribution represents a challenge in marine environments because movement patterns and foraging areas are restricted by highly dynamic spatiotemporal variations in environmental conditions. In response to this heterogeneous context, marine predators such as seabirds need to maximize their foraging...

Understanding the characteristics of a species’s distribution represents a challenge in marine environments because movement patterns and foraging areas are restricted by highly dynamic spatiotemporal variations in environmental conditions. In response to this heterogeneous context, marine predators such as seabirds need to maximize their foraging...

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 implicated in Alzheimer’s disease. The glymphatic system is thought to clear these proteins by flushing cerebral spinal fluid (CSF) through the brain. In mice, this pr...

Flying seabirds are adapted for windy environments 1,2 . Despite this, storms can cause widespread strandings and wrecks, demonstrating that these seabirds are not always able to avoid or compensate for extreme conditions 3,4,5,6,7 . The maximum wind speeds that birds can operate in should vary with morphology and flight style ⁸ , but this has been...

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 intermitte...

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 dur...

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 be...

Birds share many traits in common with mammals, including homeothermy and large brains capable of performing complex cognitive processes. Interestingly, birds also exhibit two sleep states in many, but not all, respects similar to mammalian NREM and REM sleep. Recent EEG-based studies of birds in the wild revealed novel adaptations such as the abil...

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) d...

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,...

Synopsis 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 prod...

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 th...

Sleep’s role in memory consolidation is widely accepted. However, the role of the different sleep states and accompanying neurophysiological activity is still actively debated. Most theories of sleep-related memory consolidation are based on studies in a few mammalian species. Recent evidence from research in birds, which exhibit sleep states that...

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 thalamocorti...

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 hav...

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...

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 evol...

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 fa...

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.

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 labora...

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 bei...

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...

Progression of suppression durations at the different isoflurane levels: (A) Mean suppression duration (black dot, standard error bars in grey) becomes longer with increasing anesthesia level. (B) Normalized suppression duration per isoflurane level (colored circles) and per bird (different graphs). Duration of suppression episodes was stable withi...

Video (slowed down 25x) of the image sequence shown in Figure 7B. Slow-wave propagation pattern under 1.5% isoflurane anesthesia.

High temporal resolution (2 ms) plots of propagating slow-waves during low (1.5%) and high (3.0%) isoflurane anesthesia depicted in Figure 7B (frame 320–380) and Figure 7C (frame 650–670), respectively. Similar to NREM sleep, the local field potential (LFP) activity under anesthesia generally initiates along the diagonal of the recording plane, cor...

Slow-wave trajectories and propagation direction during higher isoflurane levels: (A) Wave trajectories along the 2D-plane of the recording array (N = 50 or less random waves; plus signs depict electrode sites) under 2.0, 2.5, and 3.0% isoflurane anesthesia, which are comparable to the trajectory plots depicted in Figure 8A. (B) Net wave propagatio...

Video (slowed down 25x) of the image sequence shown in Figure 7A. Slow-wave propagation pattern during natural NREM sleep.

Video (slowed down 25x) of the image sequence shown in Figure 7C. Slow-wave propagation pattern under 3.0% isoflurane anesthesia.

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, SomnivoreTM, for automated wake–sleep stage classification. We designed an algorithm that extracts features from v...

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, unde...

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...

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 incre...

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 functi...

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.

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...

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...

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 phys...

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 ea...

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 tempora...

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 s...

Sleep is ubiquitous throughout the animal kingdom. Nonetheless, we still do not have a firm grasp on its functions. Whatever its functions, we should expect them to vary in accord with the diverse morphologies, physiologies, ecologies, and life histories of different species and taxonomic groups. Moreover, one apparently universal feature of sleep—...

Poor environmental conditions experienced during early development can have negative long-term consequences on fitness. Animals can compensate 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 (Col...

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 expr...

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 electroencephalo...

Supplementary Figures 1-19, Supplementary Table 1, Supplementary Discussion and Supplementary References

Three-dimensional flight trajectory showing the timing of sleep and high-altitude ascents. GPS data points collected every 5 min were used to plot the geographic coordinate and altitude relative to sea level at night (18:00 - 06:00). The movie focuses on one bird. Vertical lines connect the coordinate to the corresponding altitude for each GPS data...

High temporal resolution flight trajectory of a frigatebird showing circular and straight flight modes. The movie shows the flight trajectory from Fig. 1d.

Three-dimensional flight trajectory showing the timing of sleep. GPS data points collected every 5 min were used to plot the geographic coordinate and altitude relative to sea level at night (18:00 - 06:00). The movie focuses on one bird (same as in Fig. 2 and 3c). Vertical lines connect the coordinate to the corresponding altitude for each GPS dat...

Dropping behavior in a flying frigatebird. The movie shows a juvenile magnificent frigatebird (Fregata magnificens) momentarily dropping when it pulls its left wing in to preen the flight feathers. This behavior was also observed in great frigatebirds (Fregata minor) (N.C.R. pers. observ.). Movie by G.D'O.

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, whi...

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 k...

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 anima...

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 predatio...

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 uniqu...

This article was originally published in the Encyclopedia of Sleep published by Elsevier, and the attached copy is provided by Elsevier for the author's benefit and for the benefit of the author's institution, for non-commercial research and educational use including without limitation use in instruction at your institution, sending it to specific...

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 simi...

Intra-specific variation in melanocyte pigmentation, common in the animal kingdom, has caught the eye of naturalists and biologists for centuries. In vertebrates, dark, eumelanin pigmentation is often genetically determined and associated with various behavioral and physiological traits, suggesting that the genes involved in melanism have far reach...

Insight into the function of sleep may be gained by studying animals in the ecological context in which sleep evolved. Until recently, technological constraints prevented electroencephalogram (EEG) studies of animals sleeping in the wild. However, the recent development of a small recorder (Neurologger 2) that animals can carry on their head permit...

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 bi...

Imaging 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.

In most animals, sleep is considered a global brain and behavioral state. However, recent intracortical recordings have shown that aspects of non-rapid eye movement (NREM) sleep and wakefulness can occur simultaneously in different parts of the cortex in mammals, including humans. Paradoxically, however, NREM sleep still manifests as a global behav...

The three 2-dimensional plots that constitute the 3-dimensional Figure 3 in the main article. (reprinted here in the bottom left corner). These plots illustrate the distinctiveness of wakefulness (green), slow wave sleep (SWS, blue) and rapid eye movement (REM) sleep (red) based on differences in eye movements (measured via electrooculogram, EOG),...

Video showing the behavioral correlates of slow wave sleep (SWS) and rapid eye movement (REM) sleep in the ostrich. SWS is characterized by open eyes and a vertically-held head; REM sleep is characterized by bilateral eye closure and a drooping head. (MP4)

Supporting Material. (PDF)

(A–H) Electroencephalogram (EEG) of the left and right hyperpallia, electrooculogram (EOG) of the left and right eye, the three axes (heave, sway and surge) of the head-mounted accelerometer (ACC), and electromyogram (EMG) of the nuchal muscle showing slow wave sleep (SWS, blue bar), rapid eye movement (REM) sleep (red bar) and wakefulness (green b...

Mammals and birds engage in two distinct states of sleep, slow wave sleep (SWS) and rapid eye movement (REM) sleep. SWS is characterized by slow, high amplitude brain waves, while REM sleep is characterized by fast, low amplitude waves, known as activation, occurring with rapid eye movements and reduced muscle tone. However, monotremes (platypuses...

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 t...