A review of behavioral, neurophysiological and evolutionary perspectives on unihemispheric sleep in mammals, birds, reptiles, amphibians and fish 1 Charles J. Amlaner, Niels C. Rattenborg, and Steven L. Lima Department of Life Sciences, Indiana State University, Terre Haute, IN 47809, USA 1 Abstracted from Rattenborg, Amlaner and Lima, 2000, Neuroscience and Biobehavioural Reviews 24:817-842 Abstract: 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. Introduction: Animals spend their lives in two apparently mutually exclusive states, wakefulness and sleep. Wakefulness enables animals to adaptively interact with their environment, while sleep serves a vital [1], yet unknown function [2]. Sleep necessarily occurs at the expense of wakefulness, yet adaptive waking performance is contingent upon sleep [3]. Thus, animals face a situation in which sleep and wakefulness are inevitably in conflict. However, several animals have essentially side-stepped this problem by simultaneously engaging in both wakefulness and sleep; one cerebral hemisphere sleeps while the other remains awake, a unique state known as unihemispheric sleep. What is unihemispheric sleep? A definition of unihemispheric sleep is necessarily contingent upon a definition of sleep itself. Sleep can be distinguished from wakefulness using both behavioral and physiological criteria. Behaviorally, sleep is characterized as a period of sustained quiescence in a species-specific posture or site, with reduced responsiveness to external stimulation. However, with sufficient stimulation sleeping animals rapidly return to wakefulness [7, 8]. In mammals and birds, behavioral sleep is usually associated with two distinct cyclically alternating physiological sleep states; slow-wave sleep (SWS, also called non-rapid-eye-movement sleep, or quiet sleep) and rapid-eye-movement (REM) sleep (also called paradoxical or active sleep). Although changes in several physiological parameters distinguish SWS and REM sleep from each other and wakefulness (e.g. muscle tone, eye movements, autonomic function, etc.), changes in electroencephalographic (EEG) activity have received the most attention. During wakefulness, the EEG exhibits low-amplitude, high-frequency activity reflecting the activated (or desynchronized) state of the brain. In contrast to wakefulness, SWS is characterized by high-amplitude, low-frequency (or synchronized) EEG activity, often referred to as delta (<4 Hz) or theta (4–8 Hz) activity. (Note: In humans, SWS only refers to stages 3 and 4 of non-REM sleep, whereas in other animals SWS usually refers to all stages of non-REM sleep). EEG spectral power in the delta band is often defined as slow wave activity. The amount of slow-wave activity is thought to reflect the intensity or depth of SWS [9–12] (but see discussions in Refs. [13–17]). In mammals, but not birds, sleep-spindles, brief bursts of high-frequency activity (e.g. 12–16 Hz in primates) also occur during SWS [18, 19]. EEG activity during REM sleep is similar to that observed during wakefulness. However, REM sleep can be distinguished from wakefulness, in part, by a loss of muscle tone (intermittently interrupted by brief skeletal muscle twitching), rapid-eye- movements, suspended thermoregulation, penile erections and autonomic instability, including irregular heart and respiratory rate. Although two types of sleep exist, only SWS is known to occur unihemispherically. The definition of unihemispheric SWS (USWS) is usually based almost exclusively on EEG activity. Unequivocal USWS occurs when one hemisphere shows unambiguous waking EEG activity, while the other shows unambiguous SWS activity. However, alert wakefulness and SWS are states that fall at the extreme ends of a continuum, characterized by a progression from a low-amplitude, high-frequency EEG during alert wakefulness to a high-amplitude, low-frequency EEG during SWS. Consequently, as discussed below, animals that show unequivocal USWS also display intermediate states (e.g. SWS in one hemisphere and a state intermediate between alert wakefulness and SWS in the other). Such states are often classified as an interhemispheric asymmetry in SWS, rather than outright USWS. While such a