Nesting chinstrap penguins accrue large quantities of sleep through seconds-long microsleeps.

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.

The effect of food quality during growth on spatial memory consolidation in adult pigeons.

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.

Sleep and vigilance linked to melanism in wild barn owls.

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.

Evaluation of two minimally invasive techniques for electroencephalogram recording in wild or freely behaving animals.

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 permitted the first recordings of sleep in nature. To facilitate sleep studies in the field and to improve the welfare of experimental animals, herein, we test the feasibility of using minimally invasive surface and subcutaneous electrodes to record the EEG in barn owls. The EEG and behaviour of four adult owls in captivity and of four chicks in a nest box in the field were recorded. We scored a 24-h period for each adult bird for wakefulness, slow-wave sleep (SWS), and rapid-eye movement (REM) sleep using 4 s epochs. Although the quality and stability of the EEG signals recorded via subcutaneous electrodes were higher when compared to surface electrodes, the owls' state was readily identifiable using either electrode type. On average, the four adult owls spent 13.28 h awake, 9.64 h in SWS, and 1.05 h in REM sleep. We demonstrate that minimally invasive methods can be used to measure EEG-defined wakefulness, SWS, and REM sleep in owls and probably other animals.

A bird-brain view of episodic memory.

In humans, the hippocampus plays a critical role in the formation of episodic memories. Although non-human animals are unable to report whether they also re-experience past events, at least some birds and mammals exhibit 'episodic-like' memory characterized by an ability to recall what happened where and when. In mammals, the hippocampus interacts closely with virtually the entire neocortex to form episodic-like memories. The hippocampus receives highly processed information from high-order association areas, and thereby the rest of the neocortex. Distinct neurophysiological hippocampal rhythms (theta and sharp-wave ripples) coordinate activity between the hippocampus and high-order association areas during the encoding and retrieval of information contributing to episodic-like memories. Although recent studies have demonstrated that food hoarding birds are able to remember what food they hid where and when, neuroanatomical and neurophysiological studies suggest that there may be a fundamental difference between episodic-like memory in birds and mammals. In contrast to the mammalian hippocampus, the avian hippocampus only receives visual and olfactory input; most high-order association areas in the avian brain involved in performing functions similar to those performed by neocortical association areas do not project to the hippocampus or structures providing it with direct input. Consistent with this neuroanatomical difference, mammalian-like rhythms involved in communicating between the hippocampus and neocortical high-order association areas have not been found in birds. Collectively, this suggests that information contributing to episodic-like memory is more limited and processed in a different manner in birds when compared to mammals.

Unilateral eye closure and interhemispheric EEG asymmetry during sleep in the pigeon (Columba livia).

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

Behavioral, neurophysiological and evolutionary perspectives on unihemispheric sleep.

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

Facultative control of avian unihemispheric sleep under the risk of predation.

Birds and aquatic mammals are the only taxonomic groups known to exhibit unihemispheric slow-wave sleep (USWS). In aquatic mammals, USWS permits sleep and breathing to occur concurrently in water. However, the function of avian USWS has been unclear. Our study is based on the premise that avian USWS serves a predator detection function, since the eye contralateral to the awake hemisphere remains open during USWS. If USWS functions as a form of predator detection, then birds should be able to control both the proportion of slow-wave sleep composed of USWS and the orientation of the open eye in response to changes in predation risk. To test these predictions we recorded eye state and the EEG of mallard ducks (Anas platyrhynchos) sleeping in groups of four birds arranged in a row. Birds at the ends of the row were more exposed than those in the central positions, who were flanked on both sides by other birds, and thus should perceive a greater risk of predation. Consistent with a predator detection function, when compared to birds in the group's center, birds at the exposed ends of the row showed a 150% increase in USWS and a preference for directing the open eye away from the group, the direction from which a predator is most likely to approach. Furthermore, during USWS mallards responded rapidly to threatening visual stimuli presented to the open eye. This ability to facultatively control sleep and wakefulness simultaneously in different regions of the brain probably involves the neuroanatomical interhemispheric separation responsible for independent hemispheric functioning during wakefulness in birds.