Niels C. Rattenborg

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.

Sleeping under the risk of predation.

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

Migratory sleeplessness in the white-crowned sparrow (Zonotrichia leucophrys gambelii)

Twice a year, normally diurnal songbirds engage in long-distance nocturnal migrations between their wintering and breeding grounds. If and how songbirds sleep during these periods of increased activity has remained a mystery. We used a combination of electrophysiological recording and neurobehavioral testing to characterize seasonal changes in sleep and cognition in captive white-crowned sparrows (Zonotrichia leucophrys gambelii) across nonmigratory and migratory seasons. Compared to sparrows in a nonmigratory state, migratory sparrows spent approximately two-thirds less time sleeping. Despite reducing sleep during migration, accuracy and responding on a repeated-acquisition task remained at a high level in sparrows in a migratory state. This resistance to sleep loss during the prolonged migratory season is in direct contrast to the decline in accuracy and responding observed following as little as one night of experimenter-induced sleep restriction in the same birds during the nonmigratory season. Our results suggest that despite being adversely affected by sleep loss during the nonmigratory season, songbirds exhibit an unprecedented capacity to reduce sleep during migration for long periods of time without associated deficits in cognitive function. Understanding the mechanisms that mediate migratory sleeplessness may provide insights into the etiology of changes in sleep and behavior in seasonal mood disorders, as well as into the functions of sleep itself.

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.

Sleeping outside the box: electroencephalographic measures of sleep in sloths inhabiting a rainforest

The functions of sleep remain an unresolved question in biology. One approach to revealing sleeps purpose is to identify traits that explain why some species sleep more than others. Recent comparative studies of sleep have identified relationships between various physiological, neuroanatomical and ecological traits, and the time mammals spend in rapid eye movement (REM) and non-REM sleep. However, owing to technological constraints, these studies were based exclusively on animals in captivity. Consequently, it is unclear to what extent the unnatural laboratory environment affected time spent sleeping, and thereby the identification and interpretation of informative clues to the functions of sleep. We performed the first electroencephalogram (EEG) recordings of sleep on unrestricted animals in the wild using a recently developed miniaturized EEG recorder, and found that brown-throated three-toed sloths (Bradypus variegatus) inhabiting the canopy of a tropical rainforest only sleep 9.63 h d−1, over 6 h less than previously reported in captivity. Although the influence of factors such as the age of the animals studied cannot be ruled out, our results suggest that sleep in the wild may be markedly different from that in captivity. Additional studies of various species are thus needed to determine whether the relationships between sleep duration and various traits identified in captivity are fundamentally different in the wild. Our initial study of sloths demonstrates the feasibility of this endeavour, and thereby opens the door to comparative studies of sleep occurring within the ecological context within which it evolved.

Adaptive Sleep Loss in Polygynous Pectoral Sandpipers

You Snooze, You Lose Sleep serves restorative and memory functions, but it does not always operate analogously across species. Deferral of sleep may be possible when selection strongly favors the awake. Lesku et al. (p. 1654; see the Perspective by Siegel) show that sleep may be deferred without cost or impairment in pectoral sandpipers. These birds breed collectively in the high Arctic, and male competition is intense. Competing for, and displaying to, females are both physically and cognitively demanding, yet birds who slept the least showed no decrease in their ability to perform these activities. Indeed, those males who slept the least obtained the most matings and sired the most offspring. Male pectoral sandpipers go without sleep for days in order to mate as often as possible in the high Arctic. The functions of sleep remain elusive. Extensive evidence suggests that sleep performs restorative processes that sustain waking brain performance. An alternative view proposes that sleep simply enforces adaptive inactivity to conserve energy when activity is unproductive. Under this hypothesis, animals may evolve the ability to dispense with sleep when ecological demands favor wakefulness. Here, we show that male pectoral sandpipers (Calidris melanotos), a polygynous Arctic breeding shorebird, are able to maintain high neurobehavioral performance despite greatly reducing their time spent sleeping during a 3-week period of intense male-male competition for access to fertile females. Males that slept the least sired the most offspring. Our results challenge the view that decreased performance is an inescapable outcome of sleep loss.

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 groups 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.

Avian sleep homeostasis: Convergent evolution of complex brains, cognition and sleep functions in mammals and birds

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

Increased EEG spectral power density during sleep following short‐term sleep deprivation in pigeons (Columba livia): evidence for avian sleep homeostasis

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

Evolution of slow-wave sleep and palliopallial connectivity in mammals and birds: a hypothesis.

Mammals and birds are the only animals that exhibit rapid eye-movement (REM) sleep and slow-wave sleep (SWS). Whereas the electroencephalogram (EEG) during REM sleep resembles the low-amplitude, high-frequency EEG of wakefulness, the EEG during SWS displays high-amplitude, slow-waves (1-4Hz). The absence of similar slow-waves (SWs) in sleeping reptiles suggests that the neuroanatomical and neurophysiological traits necessary for the genesis of SWs evolved independently in the mammalian and avian ancestors. Advances in our understanding of comparative neuroanatomy and the genesis of mammalian SWs suggest that the absence of SWs in reptiles is due to limited connectivity within the pallium, the dorsal portion of the telencephalon that includes the mammalian neocortex, reptilian dorsal cortex and avian Wulst (hyperpallium), as well as the dorsal ventricular ridge in birds and reptiles and the mammalian claustrum and pallial amygdala. In mammals, the slow oscillation (<1Hz) of cortical neurons acts through reciprocal corticothalamic loops and corticocortical connections to synchronize the 1-4Hz activity of thalamocortical neurons in a manner sufficient to generate SWs detectable in the EEG. Given the role that corticocortical (or palliopallial) connections play in the genesis of SWs in mammals, the degree of palliopallial connectivity might explain why birds show SWs and reptiles do not. Indeed, whereas the mammalian neocortex and avian pallium show extensive palliopallial connectivity, the reptilian pallium exhibits limited intrapallial connections. I thus propose that the evolution of SWs is linked to the independent evolution of extensive palliopallial connectivity in mammals and birds. As suggested by experiments functionally linking SWs to performance enhancements, the palliopallial connections that give rise to SWs might also depend on SWs to maintain their efficacy.