A mammal and bird's-eye-view of the pupil during sleep and wakefulness.

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.

A comparison of continuous and intermittent EEG recordings in geese: How much data are needed to reliably estimate sleep-wake patterns?

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.

Divergent neuronal activity patterns in the avian hippocampus and nidopallium.

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.

The low-down on sleeping down low: pigeons shift to lighter forms of sleep when sleeping near the ground.

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.

Sleep-Related Electrophysiology and Behavior of Tinamous (Eudromia elegans): Tinamous Do Not Sleep Like Ostriches.

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.

Plumes of neuronal activity propagate in three dimensions through the nuclear avian brain.

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.

Apparent absence of hypothalamic cholinergic neurons in the common ostrich and emu: Implications for global brain states during sleep.

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.

Linking melanism to brain development: expression of a melanism-related gene in barn owl feather follicles covaries with sleep ontogeny.

BACKGROUND: 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 reaching pleiotropic effects. The mechanisms linking these traits remain poorly understood, and the potential involvement of developmental processes occurring in the brain early in life has not been investigated. We examined the ontogeny of rapid eye movement (REM) sleep, a state involved in brain development, in a wild population of barn owls (Tyto alba) exhibiting inter-individual variation in melanism and covarying traits. In addition to sleep, we measured melanistic feather spots and the expression of a gene in the feather follicles implicated in melanism (PCSK2). RESULTS: As in mammals, REM sleep declined with age across a period of brain development in owlets. In addition, inter-individual variation in REM sleep around this developmental trajectory was predicted by variation in PCSK2 expression in the feather follicles, with individuals expressing higher levels exhibiting a more precocial pattern characterized by less REM sleep. Finally, PCSK2 expression was positively correlated with feather spotting. CONCLUSIONS: We demonstrate that the pace of brain development, as reflected in age-related changes in REM sleep, covaries with the peripheral activation of the melanocortin system. Given its role in brain development, variation in nestling REM sleep may lead to variation in adult brain organization, and thereby contribute to the behavioral and physiological differences observed between adults expressing different degrees of melanism.

Diverse sleep strategies at sea.

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

The evolution and diversification of sleep.

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.

Wide-spread brain activation and reduced CSF flow during avian REM sleep.

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.

Seabird morphology determines operational wind speeds, tolerable maxima, and responses to extremes.

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.

The missing cost of ecological sleep loss.

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.

Local sleep homeostasis in the avian brain: convergence of sleep function in mammals and birds?

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.

Pupillary behavior during wakefulness, non-REM sleep, and REM sleep in birds is opposite that of mammals.

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.

Cloud cover amplifies the sleep-suppressing effect of artificial light at night in geese.

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.

Seasonal variation in sleep homeostasis in migratory geese: a rebound of NREM sleep following sleep deprivation in summer but not in winter.

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.

Half-awake to the risk of predation.

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.

Comparative Perspectives that Challenge Brain Warming as the Primary Function of REM Sleep.

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.