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Behavioral, neurophysiological and evolutionary perspectives on unihemispheric sleep N.C. Rattenborg * , C.J. Amlaner, S.L. Lima Department of Life Sciences, Indiana State University, Terre Haute, IN 47809, USA Received 1 March 2000; revised 31 July 2000; accepted 15 August 2000 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. q 2000 Elsevier Science Ltd. All rights reserved. Keywords: Unihemispheric; Slow-wave sleep; Sleep function; Sleep mechanisms; Sleep regulation; Functional lateralization; Predator detection; Aquatic mammals; Birds; Reptiles 1. Introduction Animals spend their lives in two apparently mutually exclusive states, wakefulness and sleep. Wakefulness enables animals to adaptively interact with their environ- ment, while sleep serves a vital [1], yet unknown func- tion [2]. Sleep necessarily occurs at the expense of wakefulness, yet adaptive waking performance is contin- gent 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 wake- fulness and sleep; one cerebral hemisphere sleeps while the other remains awake, a unique state known as uni- hemispheric sleep. The following review is intended to serve as a compre- hensive synopsis on unihemispheric sleep. While significant reviews exist on unihemispheric sleep in aquatic mammals [4–6], no single source has incorporated the diverse and often obscure literature on unihemispheric sleep in other animals. Moreover, in the past few years a renewed interest in unihemispheric sleep has resulted in several significant findings that warrant discussion within the context of previous work on unihemispheric sleep. In the interest of providing the reader with an exhaustive review of the subject, we have incorporated virtually every study on unihemispheric sleep, including descriptive studies based on small sample sizes. Although conclusions based on such studies are necessarily tentative, their inclusion simul- taneously highlights the breadth and limits of our under- standing of unihemispheric sleep. Finally, throughout the review we present several speculative perspectives on unihemispheric sleep. In doing so, we hope to provide the impetus for developing further research and insight into unihemispheric sleep, and sleep in general. We will discuss unihemispheric sleep at various levels throughout this review. The background, behavioral ecol- ogy and evolutionary history of unihemispheric sleep will be discussed for each taxonomic group in which sleep occurs unihemispherically; aquatic mammals (i.e. Ceta- cea, Pinnipedia and Sirenia), birds, and possibly reptiles. When appropriate, significant parallels and differences between groups will be highlighted. For organizational Neuroscience and Biobehavioral Reviews 24 (2000) 817–842 PERGAMON NEUROSCIENCE AND BIOBEHAVIORAL REVIEWS 0149-7634/00/$ - see front matter q 2000 Elsevier Science Ltd. All rights reserved. PII: S0149-7634(00)00039-7 www.elsevier.com/locate/neubiorev * Corresponding author. Department of Psychiatry, University of Wisconsin Medical School/Madison, 6001 Research Park Blvd., Madison, WI 53719, USA. Tel.: 11-608-263-6115; fax: 11-608-263-0265. E-mail address: [email protected] (N.C. Rattenborg).

Behavioral, neurophysiological and evolutionary perspectives on unihemispheric sleep

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Page 1: Behavioral, neurophysiological and evolutionary perspectives on unihemispheric sleep

Behavioral, neurophysiological and evolutionary perspectives onunihemispheric sleep

N.C. Rattenborg* , C.J. Amlaner, S.L. Lima

Department of Life Sciences, Indiana State University, Terre Haute, IN 47809, USA

Received 1 March 2000; revised 31 July 2000; accepted 15 August 2000

Abstract

Several animals mitigate the fundamental conflict between sleep and wakefulness by engaging in unihemispheric sleep, a unique stateduring which one cerebral hemisphere sleeps while the other remains awake. Among mammals, unihemispheric sleep is restricted to aquaticspecies (Cetaceans, eared seals and manatees). In contrast to mammals, unihemispheric sleep is widespread in birds, and may even occur inreptiles. Unihemispheric sleep allows surfacing to breathe in aquatic mammals and predator detection in birds. Despite the apparent utility inbeing able to sleep unihemispherically, very few mammals sleep in this manner. This is particularly interesting since the reptilian ancestors tomammals may have slept unihemispherically. The relative absence of unihemispheric sleep in mammals suggests that a trade off existsbetween unihemispheric sleep and other adaptive brain functions occurring during sleep or wakefulness. Presumably, the benefits of sleepingunihemispherically only outweigh the costs under extreme circumstances such as sleeping at sea. Ultimately, a greater understanding of thereasons for little unihemispheric sleep in mammals promises to provide insight into the functions of sleep, in general.q 2000 ElsevierScience Ltd. All rights reserved.

Keywords: Unihemispheric; Slow-wave sleep; Sleep function; Sleep mechanisms; Sleep regulation; Functional lateralization; Predator detection; Aquaticmammals; Birds; Reptiles

1. Introduction

Animals spend their lives in two apparently mutuallyexclusive states, wakefulness and sleep. Wakefulnessenables animals to adaptively interact with their environ-ment, while sleep serves a vital [1], yet unknown func-tion [2]. Sleep necessarily occurs at the expense ofwakefulness, yet adaptive waking performance is contin-gent upon sleep [3]. Thus, animals face a situation inwhich sleep and wakefulness are inevitably in conflict.However, several animals have essentially side-steppedthis problem by simultaneously engaging in both wake-fulness and sleep; one cerebral hemisphere sleeps whilethe other remains awake, a unique state known as uni-hemispheric sleep.

The following review is intended to serve as a compre-hensive synopsis on unihemispheric sleep. While significantreviews exist on unihemispheric sleep in aquatic mammals[4–6], no single source has incorporated the diverse and

often obscure literature on unihemispheric sleep in otheranimals. Moreover, in the past few years a renewed interestin unihemispheric sleep has resulted in several significantfindings that warrant discussion within the context ofprevious work on unihemispheric sleep. In the interest ofproviding the reader with an exhaustive review of thesubject, we have incorporated virtually every study onunihemispheric sleep, including descriptive studies basedon small sample sizes. Although conclusions based onsuch studies are necessarily tentative, their inclusion simul-taneously highlights the breadth and limits of our under-standing of unihemispheric sleep. Finally, throughout thereview we present several speculative perspectives onunihemispheric sleep. In doing so, we hope to provide theimpetus for developing further research and insight intounihemispheric sleep, and sleep in general.

We will discuss unihemispheric sleep at various levelsthroughout this review. The background, behavioral ecol-ogy and evolutionary history of unihemispheric sleep willbe discussed for each taxonomic group in which sleepoccurs unihemispherically; aquatic mammals (i.e. Ceta-cea, Pinnipedia and Sirenia), birds, and possibly reptiles.When appropriate, significant parallels and differencesbetween groups will be highlighted. For organizational

Neuroscience and Biobehavioral Reviews 24 (2000) 817–842PERGAMON

NEUROSCIENCE AND

BIOBEHAVIORAL

REVIEWS

0149-7634/00/$ - see front matterq 2000 Elsevier Science Ltd. All rights reserved.PII: S0149-7634(00)00039-7

www.elsevier.com/locate/neubiorev

* Corresponding author. Department of Psychiatry, University ofWisconsin Medical School/Madison, 6001 Research Park Blvd., Madison,WI 53719, USA. Tel.:11-608-263-6115; fax:11-608-263-0265.

E-mail address:[email protected] (N.C. Rattenborg).

Page 2: Behavioral, neurophysiological and evolutionary perspectives on unihemispheric sleep

and historic reasons, much of the review will follow thechronological sequence in which discoveries were made.Following a discussion of each group, we will review thepotential neurophysiological mechanisms involved inunihemispheric sleep, including a discussion regardingwhy only one type of sleep (i.e. slow-wave sleep,SWS) occurs unihemispherically. Although humans donot sleep unihemispherically, several related findingsthat hint at a tendency for unihemispheric sleep inhumans will also be included. Throughout the review,promising areas for future research will be identified,especially those which may yield clues to the functionof sleep. Finally, having demonstrated the adaptiveadvantages of being able to sleep unihemispherically,we will attempt to answer the more difficult, and rarelyasked question: Why do most mammals sleepbihemi-spherically?

2. What is unihemispheric sleep?

A definition of unihemispheric sleep is necessarilycontingent upon a definition of sleep itself. Sleep can bedistinguished from wakefulness using both behavioral andphysiological criteria. Behaviorally, sleep is characterizedas a period of sustained quiescence in a species-specificposture or site, with reduced responsiveness to externalstimulation. However, with sufficient stimulation sleepinganimals rapidly return to wakefulness [7,8]. In mammalsand birds, behavioral sleep is usually associated with twodistinct cyclically alternating physiological sleep states;slow-wave sleep (SWS, also called non-rapid-eye-move-ment sleep, or quiet sleep) and rapid-eye-movement(REM) sleep (also called paradoxical or active sleep).Although changes in several physiological parametersdistinguish SWS and REM sleep from each other and wake-fulness (e.g. muscle tone, eye movements, autonomic func-tion, etc.), changes in electroencephalographic (EEG)activity have received the most attention. During wakeful-ness, the EEG exhibits low-amplitude, high-frequencyactivity reflecting the activated (or desynchronized) stateof the brain. In contrast to wakefulness, SWS is character-ized 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 tostages 3 and 4 of non-REM sleep, whereas in other animalsSWS usually refers to all stages of non-REM sleep). EEGspectral power in the delta band is often defined as slow-wave activity. The amount of slow-wave activity is thoughtto reflect the intensity or depth of SWS [9–12] (but seediscussions 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]. EEGactivity during REM sleep is similar to that observed duringwakefulness. However, REM sleep can be distinguishedfrom wakefulness, in part, by a loss of muscle tone (inter-

mittently interrupted by brief skeletal muscle twitching),rapid-eye-movements, suspended thermoregulation, penileerections and autonomic instability, including irregularheart and respiratory rate.

Although two types of sleep exist, only SWS is knownto occur unihemispherically. The definition of unihemi-spheric SWS (USWS) is usually based almost exclu-sively on EEG activity. Unequivocal USWS occurswhen one hemisphere shows unambiguous waking EEGactivity, while the other shows unambiguous SWS activ-ity. However, alert wakefulness and SWS are states thatfall at the extreme ends of a continuum, characterized bya progression from a low-amplitude, high-frequencyEEG during alert wakefulness to a high-amplitude,low-frequency EEG during SWS. Consequently, asdiscussed below, animals that show unequivocal USWSalso display intermediate states (e.g. SWS in one hemi-sphere and a state intermediate between alert wakeful-ness and SWS in the other). Such states are oftenclassified as an interhemispheric asymmetry in SWS,rather than outright USWS. While such a distinctionmight have merit, interhemispheric asymmetries inSWS and USWS appear to simply reflect differentdegrees of the same phenomenon. Along these lines,pending a functional reason for distinguishing betweenthese states, Mukhametov [5] chose to refer to bothstates as USWS. Similarly, in this review, we will defineUSWS as an alternating interhemispheric asymmetry inSWS, associated with behavioral signs of wakefulness,such as unilateral eye closure (i.e. closure of one eye)and/or swimming. By referring to an interhemisphericasymmetry in SWS as USWS we do not intend to indi-cate that all waking functions remain intact and all sleepfunctions suspended in the “awake” hemisphere.Certainly, it is conceivable that the intermediate levelof low-frequency activity in the “awake” hemisphererepresents a further compromise between sleep andwakefulness; the hemisphere remains awake enough tomeet the ecological demands for wakefulness, while stillobtaining some of the benefits of sleep.

The phenomenon of unihemispheric sleep necessarilychallenges the traditional definitions of sleep. For example,aquatic mammals that swim during USWS are clearly notquiescent. Such violations of the traditional definitions haveled some to question whether USWS should be categorizedas sleep, e.g. [20]. However, this apparent problem lies inthe definition of sleep imposed, rather than the phenomenonof USWS itself. In the case of dolphins, which almost neversleep bihemispherically, to discount the presence of USWSon the basis of definitional problems is equivalent to sayingdolphins do not sleep. Given the ubiquity of sleep in theanimal kingdom [21,22], and the fatal consequences of notsleeping [1], such a conclusion seems unfounded. Conse-quently, as with any biological definition, the definition ofsleep needs to evolve to encompass new discoveries, such asUSWS.

N.C. Rattenborg et al. / Neuroscience and Biobehavioral Reviews 24 (2000) 817–842818

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3. Unihemispheric sleep in aquatic mammals

3.1. Cetaceans: dolphins, porpoises and whales

The order Cetacea is comprised of two suborders ofexclusively aquatic mammals, Odontoceti (dolphins,porpoises and toothed whales) and Mysticeti (filter-feedingbaleen whales) [23] (but see Ref. [24]). Based on fossil[25,26] and molecular [24,27] evidence, the closest livingrelatives to Cetaceans are the even-toed ungulates (Artio-dactyla). Interestingly, within Artiodactyla, Cetaceansappear most closely related to the semi-aquatic hippopota-muses [28]. To date, USWS has been identified in fourspecies from the Cetacean suborder Odontoceti (Table 1),however, the EEG has not yet been recorded from the sub-order Mysticeti (see Lyamin et al. [29] for behavioral obser-vations of sleep in a baleen whale).

3.2. Background of Cetacean unihemispheric sleep

Lilly [30] was the first to suggest that dolphins (Tursiopstruncatus) could sleep unihemispherically:

In regard to lateralization of the sleep pattern, theseanimals sleep with one eye closed at a time. The eyeclosures are 180 degrees out of phase; it is rare to haveboth eyes closed at once … Alternate sides are restedalternatively.

Subsequently, Lilly [31] suggested that dolphins sleepwith one eye open to “assure that the animal is alwaysscanning his environment with at least half of his afferentinputs”. Although Lilly did not record unihemispheric sleepEEG activity, his behavioral results clearly anticipatedfuture observations of such sleep in dolphins.

Recordings from the pilot whale (Globicephala scammoni;actually a type of dolphin) provided the first electrophysiolo-gical evidence for USWS in a Cetacean [32,33]. EEG activitywas recorded from the parieto-occipital region of each hemi-sphere in a single whale. Interhemispheric asymmetry in theEEG, characterized by high-amplitude, low-frequency activ-ity in one hemisphere concurrent with low-amplitude, high-frequency activity in the other hemisphere was observedduring periods classified as “relaxed wakefulness”. Thisasymmetry tended to alternate between hemispheres.Although such sleep was classified as relaxed wakefulnessrather than some form of USWS per se, these results providethe earliest EEG evidence for USWS in a Cetacean.

The recognition and comprehensive characterization ofUSWS in Cetaceans began in earnest in the early 1970swith research from Lev Mukhametov’s laboratory at theSevertsov Institute of Evolutionary Morphology and Ecol-ogy of Animals, USSR (now Russian) Academy ofSciences. Mukhametov, Supin and Polyakova [34] werethe first to recognize the interhemispheric asymmetry duringsleep in Cetaceans as USWS. To date, Mukhametov’s grouphave identified USWS in all three of the Cetacean species

investigated (Table 1); the bottlenose dolphin (Tursiopstruncates) [34,35] (see also Ref. [36]), the common porpoise(Phocoena phocoena) [6], and the Amazonian dolphin (Iniageoffrensis) [37]. Mukhametov and colleagues provideseveral English summaries of their research on sleep inCetaceans and other aquatic mammals [4–6].

In all three species studied, three stages of EEG activitywere identified: (1) wakefulness, characterized by low-ampli-tude, high-frequency activity; (2) an intermediate stagebetween wakefulness and “deep” SWS, characterized bysleep-spindles, theta and delta waves; and (3) “deep” SWScharacterized by delta waves of maximal amplitude. Wakeful-ness and the intermediate stage both occurred bihemispheri-cally and unihemispherically. However, deep SWS onlyoccurred unihemispherically. In bottlenose dolphins, bihemi-spheric wakefulness occupied approximately two thirds of thetime, with the remaining third being comprised mainly ofUSWS (i.e. wakefulness in one hemisphere and the intermedi-ate stage in the other, or wakefulness in one hemisphere anddeep SWS in the other) [6]. Episodes of USWS lasted onaverage 42.5 min (range 3.5–131.5) and tended to alternatebetween hemispheres [35]. Similar patterns were observed inporpoises [6] and in Amazonian dolphins [37]. In bottlenosedolphins, all types of sleep were most likely to occur at nightand during the second half of the day; sleep time was markedlyreduced during the first half of the day and at dusk [35]. Inter-estingly, REM sleep occurs infrequently and/or in a modifiedmanner in Cetaceans. While electrophysiological studieseither report little [33] or no [4,38] signs of REM sleep, severalresearchers have observed behavioral signs of REM sleep,including muscle twitching, REMs and penile erections[29,39–44] (but see Ref. [45]).

In Cetaceans, each hemisphere functions as an inde-pendent unit with respect to sleep. Simultaneous record-ings from the frontal, parietal and occipital cortexrevealed that while deep SWS may start or end asynchro-nously within different regions of a single hemisphere,during stable deep SWS, all regions of the hemisphereshow similar delta activity (Fig. 1) [5,34]. Furthermore,low-frequency activity recorded from thalamic nucleioccurs concurrently with USWS in the ipsilateral cortex[46]. Thus, USWS is a characteristic of both cortical andsubcortical structures. USWS in bottlenose dolphins andporpoises is also reflected in hemispheric corticaltemperature. Brain temperature recordings from the leftand right parietal cortex during USWS revealed interhe-mispheric asymmetries in temperature that paralleledhemispheric EEG activity; temperature was higher inthe awake hemisphere, and lower in the sleeping hemi-sphere [47,48]. This relationship is consistent with otherstudies that found a reduction in brain temperature andmetabolism during SWS (reviewed in Ref. [49]).

Given that each hemisphere can sleep independently, anobvious question arises as to whether one hemisphere sleepsmore than the other. In early reports, it appeared that withinindividual dolphins sleep was more likely to occur in one

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Table 1All studies containing EEG or behavioral signs of unihemispheric sleep. In a few cases, studies which either explicitly report the absence of unihemisphericsleep, or which serve to demonstrate a point regarding unihemispheric sleep (e.g. true seals) are also included (USWS, unihemispheric slow-wave sleep;BSWS, bihemispheric slow-wave sleep; REM, rapid-eye-movement sleep; UEC, unilateral eye closure) (Key: Blank, no data provided;1, present; –, absent;?, data reported insufficient to determine presence or absence; 1, REM not detected, but may be present in small amounts or in a modified form; 2, UEC presentduring sleep, but not necessarily associated with USWS in opposite hemisphere; 3, BSWS only recorded following sleep deprivation; 4, EEG recorded fromonly one hemisphere, or EEG from both hemispheres combined; 5, absence may be due to short observation period; 6, EEG spikes and sharp waves, rather thanslow-wave activity during SWS (observed only in reptiles))

Taxon USWS BSWS REM UEC Note References

MAMMALS

CetaceaOdontoceti: Toothed whales, dolphins and porpoises

Amazonian dolphin (Inia geoffrensis) 1 2 2 1 1, 2 [37,44]Pilot whale (Globicephala scammoni) 1 1 1 3 [32,33]Bottlenose dolphin (Tursiops truncatus) 1 2 2 1 1, 2 [4,34]Pacific white-sided dolphin (Lagenorhynchusobliquidens)

1 [60]

Common porpoise (Phocoena phocoena) 1 2 2 1 [4,6]Mysticeti: Baleen whales

Gray whale (Eschrichtius robustus) 1/? 1 1 [29]

CarnivoraPinnipedia

Otariidae: Eared sealsNorthern fur seal (Callorhinus ursinus) 1 1 1 1 [6,76]Cape fur seal (Arctocephalus pusillus) 1 1 1 1 [75]Stellar’s sea lion (Eumetopias jubatus) 1 1 1 [214]Southern sea lion (Otari bryonia) 1 1 1 [80]

Phocidae: True sealsCaspian seal (Phoca caspia) 2 1 1 [6,81]Harp seal (Pagophilus groenlandicus) 2 1 1 2 [77,82]Elephant seal (Mirounga angustirostris) 2 1 1 [84]Grey seal (Halichoerus grypus) ? ? 1 2 4 [86]

SireniaCaribbean manatee (Trichechus manatus) 2 1 1 5 [95,215]Amazonian manatee (Trichechus inunguis) 1 1 1 [95,96]

BIRDS

Rheiformes: Rheas 2 5 [104]Tinamiformes: Tinamous 2 5 [104]Casuariiformes: Cassowaries and emus 2 5 [104]Sphenisciformes: Penguins

Humboldt penguin (Spheniscus humboldti) 1 [104,107]Podicipediformes: Grebes

Western grebe (Aechmorphorus occidentalis) 1 [104,107]Ciconiformes: Herons, ibises, storks and allies

Chilean flamingo (Phoenicopterus chilensis) 1 [104,107]Anseriformes: Swans, ducks and geese

Canada goose (Branta canadensis) 1 [104,107]White-faced whistling duck (Dendrocygnaviduata)

1 [104,107]

Mallard (Anas platyrhynchos) 1 1 1 1 [113,118,119]1 [216]

North American black duck (Anas rubripes) 1 [104,107]Chiloe wigeon (Anas sibilatrix) 1 [104,107]Cape teal (Anas capensis) 1 [104,107]Mandarin duck (Aix galericulata) 1 [104,107]Ringed teal (Callonetta leucophrys) 1 [104,107]Crested screamer (Chauna torquata) 1 [104,107]

Falconiformes: Diurnal birds of preyCommon kestrel (Falco tinnunculus) 1 [104,107]

Galliformes: Chickenlike birdsCommon turkey (Meleagris gallopavo) 1 [104,107]

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hemisphere; certain dolphins slept more with the left hemi-sphere, while others slept more with the right [4,34,37].However, recordings performed over several non-consecu-tive 24-hour sessions revealed that hemispheric sleep timewas equivalent when averaged across sessions within indi-viduals [35]. Thus, during any given session one hemispheremay sleep more than the other, but when viewed over alonger time scale both hemispheres sleep equal amounts.

As in Lilly’s early behavioral study of bottlenosedolphins, unilateral eye closure was observed in Mukhame-tov’s dolphins. However, a relationship between eye stateand the state of the contralateral hemisphere was notobserved; the hemisphere contralateral to the open eye

was either awake or asleep [4]. Nevertheless, visual stimulipresented to the open eye during USWS elicited behavioraland EEG arousal, even when the contralateral hemispherewas asleep ([50], cited in [4]; see also [44] for behavioralarousal in Amazonian dolphins). This is surprising sinceneuroanatomical and neurophysiological findings suggestthat the hemisphere contralateral to the open eye should beawake. As a result of complete decussation of the optic nervesin dolphins [51,52], only the contralateral visual cortex exhi-bits evoked potentials in response to flashes of light presentedto an eye during wakefulness ([50], cited in [36]). Thus, thefindings from awake dolphins are difficult to reconcile withthose observed during USWS.

N.C. Rattenborg et al. / Neuroscience and Biobehavioral Reviews 24 (2000) 817–842 821

Table 1 (continued)

Taxon USWS BSWS REM UEC Note References

Domestic chicken (Gallus gallus domesticus) 1 1 1 1 [97,98,101]1 1 1 [102]? ? 1 1 4 [217]

Northern bobwhite (Colinus virginianus) 1 1 1 1 [106]Japanese quail (Coturnix japonica) 1 1 1 1 [103]

Gruiformes: Cranes, rails and alliesStanley crane (Anthropoides paradisea) 1 [104,105]

Charadriiformes: Shorebirds, gulls, auks and alliesGlaucous-winged gull (Larus glaucescens) 1 1 1 1 [104,107]Ring-billed gull (Larus delawarensis) 1 [104,107]Pigeon guillemot (Cepphus columba) 1 [104,107]

Columbiformes: Pigeons and dovesNicobar pigeon (Caloenas nicobarica) 1 [104,107]Domestic pigeon (Columba livia) 2 1 1 ? [111]

1 1 1 1 [115]Psittaciformes: Parrots and allies

Orange-fronted conure (Aratinga canicularis) 1 1 1 1 2 [110]Cuculiformes: Cuckoos and alliesStrigiformes: Owl

Barn owl (Tyto alba) 1 [104,107]Snowy owl (Nyctea scandiaca) 1 [104,107]Burrowing owl (Athene cunicularia) 1 [104,107]

Apodiformes: Swifts and hummingbirds 2 5 [104]Coraciiformes: Kingfishers and allies

Rufous-capped motmot (Baryphthengusruficapillus)

1 [104,107]

Passeriformes: Perching birdsBlue jay (Cyanoccitta cristata) 1 [104,107]Brewer’s blackbird (Euphagus cyanocephalus) 1 [104,107]Blackbird (Turdus merula) 1 1 1 ? [112]

REPTILES

Chelonia: Turtles and tortoisesBox turtle (Terrapene carolina) ? ? 2 1 4, 6 [148]Red-footed tortoise (Geochelone carbonaria) 2 1 2 1 6 [149]

Crocodilia: Crocodiles, alligators and caimansCaiman (Caiman sclerops) 1 2 1 [141]Caiman (Caiman latirostris) ? ? 1/? 1 4, 6 [145]

Sqamata: Lizards and snakesChameleon (Chameleo jacksoni) ? ? 2 1 4, 6 [143]Chameleon (Chameleo melleri) ? ? 2 1 4, 6 [143]Black iguana (Ctenosaura pectinata) ? ? 2 1 4, 6 [144]Green iguana (Iguana iguana) ? ? 2 1 4, 6 [146]

? ? 2 1 4, 6 [145]Western fence lizard (Sceloporus occidentalis) 1 [153]

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In the three dolphin species studied, USWS was behavio-rally indistinguishable from periods of quiet wakefulness, awaking state during which the animal is not actively inter-acting with its surroundings. During both quiet wakefulnessand USWS, bottlenose and Amazonian dolphins swimslowly or hover at the water’s surface [5,37]. When hover-ing at the surface, only fin movements required to maintain astable posture were observed. During periods of USWS withconstant slow swimming, dolphins may take a breath of airat the surface without awakening the sleeping hemisphere.In a behavioral study, Flanigan also observed slow swim-ming and hovering at the surface during apparent sleep inbottlenose [39] and Pacific white-sided (Lagenorhynchusobliquidens) [53] dolphins. However, in addition to hover-ing at the surface, McCormick [54] observed periods ofresting on the tank bottom with one or both eyes open inbottlenose dolphins. Periods of resting on the bottom wereperiodically interrupted by surfacing to breathe (see also[30]). Porpoises (Phocoena phocoena) differ from dolphinsin that they swim continuously without ever hovering at thesurface [6,45]. Constant swimming during apparent sleephas also been reported in the Dall porpoise (Phocoenoidesdalli) (see [54]), Indus dolphin (Platanista indi) [55], andBeluga whale (Delphinapterus leucas) [56,57]. In additionto slow swimming, Lyamin et al. [41] observed lying on thebottom in Beluga whales. Interestingly, lying on the bottomwas only observed in the whale that was well adapted tocaptivity. Finally, having observed slow swimming duringsleep in the Pacific white-sided dolphin, bottlenose dolphinand Beluga whale, but not in their predator, the killer whale(Orcinus orca) [40], Flanigan [53] suggested that swimmingduring sleep facilitates a rapid transition from sleep toescape behavior if a threat arises.

3.3. Function of unihemispheric sleep in Cetaceans

The presence of swimming during USWS in Cetaceans

suggests that USWS functions primarily to maintain themotor activity required for surfacing to breathe [6]. Indeed,as mentioned above, surfacing to breathe occurs duringUSWS. Consistent with this idea, respiration ceases duringpentobarbitol-induced bihemispheric slow-wave sleep(BSWS), and breathing during diazepam-induced BSWSonly occurs during brief returns to USWS [6,58] (see alsoRef. [54]). Apparently, the complex movements andreflexes required for Cetacean respiration are incompatiblewith BSWS. Mukhametov suggests that this may also explainthe absence or modified nature of REM sleep in Cetaceans,since the lossof muscle tone typical of mammalian REM sleepmay interfere with the motions required for breathing in Ceta-ceans [4,38,42]. However, it remains unclear as to whydolphins do not simply hold their breath during brief periodsof BSWS, as observed in some seals (see below). One possi-bility is that by sleeping unihemispherically Cetaceans areable to sleep (albeit with one hemisphere at a time) forextended periods without frequent interruptions to breathe[5]. Finally, USWS might allow sleep, surfacing to breatheand migration to occur concurrently in Cetaceans [59].

USWS in Cetaceans may also serve additional functionsunrelated to swimming and breathing. The fact that dolphinsfrequently keep one eye open and responsive during USWSsuggests that dolphins use USWS to visually monitor theirenvironment, as suggested by Lilly [31]. Indeed, in a recentbehavioral study of a group of four captive Pacific white-sided dolphins, Goley [60] found that dolphins use unilateraleye closure in a functional manner. At night the dolphinsceased vocalizing, formed a tight group, and swam slowly ina counterclockwise direction (see also Ref. [61]). Goleypredicted that the dolphins at either edge of the groupwould keep the open eye directed away from the group, asif watching for approaching predators. However, in directcontrast to this prediction, the dolphins actually kept theopen eye directed towards the center of the group, whilethe eye facing away from the group remained closed.

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Fig. 1. EEG recorded from the parieto-occipital cortex (A) of a bottlenose dolphin during unihemispheric slow-wave sleep with either the left (B) or right (C)hemisphere asleep. Note the high-amplitude, low-frequency EEG activity in the sleeping hemisphere and the low-amplitude, high-frequency EEG activity inthe awake hemisphere. Reprinted from Brain Research, Vol 134, Mukhametov, L.M., Supin, A.Y., Polyakova, I.G., Interhemispheric asymmetry of theelectroencephalographic sleep patterns in dolphins, 581–584, 1977, with permission from Elsevier Science.

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Furthermore, when the dolphins changed their positionwithin the group, eye state changed accordingly. For exam-ple, when a dolphin switched from the right side to the leftside of the group, it switched from having only the right eyeclosed to having only the left eye closed. Since eye stateswitches occurred approximately on an hourly basis, a dura-tion similar to that observed for bouts of hemispheric sleep[35], Goley concluded that position and eye state changesmay allow each hemisphere a turn to sleep. Given thesefindings, the lack of a correlation between which eye isopen and which hemisphere is asleep reported by Mukha-metov [4] remains enigmatic (see above). Finally, althoughthese findings suggest that dolphins use unilateral eyeclosure to maintain visual contact with their group, unilat-eral eye closure may also serve a predator detection func-tion. Since the group was vertically staggered as it swam,Goley notes that dolphins may be able to visually monitortheir surroundings by scanning past their schoolmates.Certainly, as with many biological processes, unilateraleye closure and USWS are likely to serve several non-mutually exclusive functions in Cetaceans.

3.4. Regulation of unihemispheric sleep in Cetaceans

The discovery of USWS in Cetaceans provided a uniqueopportunity to address several key issues regarding the regu-lation of SWS in mammals. Previous studies from variousterrestrial species have shown an increase in SWS time and/or intensity (reflected in increased slow-wave activity) follow-ing sleep deprivation (reviewed in Refs. [62–64]; but seediscussions in Refs. [13–17]) suggesting that the brain home-ostatically compensates for lost sleep. However, prior to thediscovery of USWS it was unclear whether SWS was regu-lated as a whole brain phenomenon or locally within differentregions of the brain. Following the discovery of USWS inCetaceans, it became apparent that SWS might be homeosta-tically regulated independently within each hemisphere.

Unihemispheric sleep deprivation in bottlenose dolphinsrevealed SWS was in fact regulated unihemispherically[4,65]. Unihemispheric sleep deprivation was achieved byawakening the dolphin whenever the targeted hemispherefell asleep; the non-deprived hemisphere was allowed tosleep as long as the deprived hemisphere remained awake.The first sign of independent hemispheric sleep regulationwas an increase in the frequency of attempts to fall asleepmade by the deprived hemisphere as the deprivation proce-dure progressed. Moreover, following unihemispheric sleepdeprivation, SWS time (SWS intensity was not reported)increased primarily in the deprived hemisphere; the non-deprived hemisphere did not compensate for sleep lost inthe deprived hemisphere. The unihemispheric sleep reboundwas greatest immediately following deprivation, a featuretypical of SWS rebounds in mammals (reviewed inRefs. [62–64]), and the normal tendency for sleep to alter-nate between hemispheres was accentuated during recovery.

The results from unihemispheric sleep deprivation in

dolphins have several implications for understanding theregulation of SWS. First, these results convincingly demon-strate that the rebounds in SWS observed following sleepdeprivation in previous studies are the result of lost sleep,rather than a non-specific variable (e.g. stress, enforcedactivity, etc.) associated with the deprivation procedure. Ifthe rebound in SWS had resulted from stress induced by thedeprivation procedure, then both hemispheres should haveshown an increase in SWS in response to unihemisphericsleep deprivation. Second, the presence of unihemisphericsleep regulation appears to contradict theories of sleep regu-lation based on diffuse sleep factors circulating in the bloodor cerebrospinal fluid ([5,65]; reviewed in Refs. [66,67]; seealso Ref. [68]). If SWS were primarily regulated by diffusesleep factors, then deprivation of one hemisphere shouldhave caused an increase in SWS in the non-deprived hemi-sphere during deprivation, as well as an increase in SWS inboth hemispheres following deprivation. Instead, the resultssuggest that sleep factors accumulate and influence SWSindependently within each hemisphere. Although the needfor sleep may accumulate independently within each hemi-sphere, the acquisition of such sleep must involve the reci-procal coordination of both hemispheres since SWS almostnever occurs simultaneously in both hemispheres, evenfollowing bihemispheric sleep deprivation [34,65].

In addition to enhancing our understanding of SWS regu-lation, the results from unihemispheric sleep deprivationalso provide significant clues to the function of sleep. Atthe most fundamental level, the results clearly indicate thatsleep serves a primary function for the brain, rather than thebody. Indeed swimming during USWS in Cetaceans showsthat the body does not necessarily rest during sleep. By nomeans does this indicate that sleep serves no function for thebody; certainly sleep may be necessary for the brain (orhemisphere) to effectively regulate several bodily functionssuch as thermoregulation, immune system integrity andtissue restoration (see [2,69]). The presence of unihemi-spheric SWS regulation, and USWS itself, also raises thequestion as to what is the smallest component of the centralnervous system that requires sleep. Indeed, the discovery ofUSWS regulation has influenced current functional sleeptheories which propose that sleep may be regulated locallywithin small portions of each hemisphere ([70–72]; forevidence of local sleep see [73,74]).

3.5. Pinnipedia: eared and true seals

The apparent link between USWS and an aquatic lifestyleled to the exploration of sleep in another group of aquaticmammals, the pinnipeds. The order pinnipedia is comprisedof three families: Otariidae (eared seals: sea lions and furseals), Phocidae (true seals) and Odobenidae (walrus;Odobenus rosmarus). Pinnipeds are particularly interestingsince, unlike Cetaceans, they sleep in the water and on land.Electrophysiological sleep states have been investigated inseveral species of eared and true seals (Table 1), but the

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walrus has not been studied. In brief, USWS allows earedseals to sleep and breathe regularly at the water’s surface,whereas true seals hold their breath under water while bothhemispheres sleep simultaneously.

3.6. Unihemispheric sleep in eared seals

USWS has been observed in all four species of eared sealsinvestigated (Table 1). However, unlike Cetaceans, earedseals also exhibit BSWS and unequivocal REM sleep(Fig. 2). USWS in eared seals consists primarily of an inter-hemispheric asymmetry in SWS; one hemisphere displaysdeep SWS, while the other exhibits an intermediate stage[75,76]. As in Cetaceans, USWS is a feature of the entirehemisphere [6,76], although the interhemispheric asymme-try in SWS is most pronounced in the occipital and parietalregions (O.I. Lyamin, personal communication). Episodesof SWS usually start with several minutes of USWS,followed by a transition to BSWS [5]. The amount ofSWS composed of USWS increases with age, but even furseals as young as two weeks old display small amounts ofUSWS ([78, cited in [77], [6]). A decrease in REM sleep,similar to that observed in terrestrial mammals (reviewed inRef. [18]), also occurs with increasing age.

Eared seals provide a unique opportunity to test thehypothesis that USWS is linked to sleeping and breathing

in water, since they sleep in water and on land, and displayboth USWS and BSWS [6,76]. Consequently, if USWS islinked to sleeping and breathing in water, the proportion ofSWS composed of USWS should increase when sleep inwater is compared to that on land. This prediction is basedon the assumption that USWS is a less efficient means ofmeeting a daily hemispheric sleep quota, and thereforeshould only be utilized when BSWS is less feasible (e.g.in the water). In the four fur seals studied, the proportion ofSWS composed of USWS did in fact increase from 41.6%on land to 66.9% in water [6,76]. Along these lines, USWSalso increases in young seals when they make the transitionfrom sleeping on land to sleeping in water [78].

The link between USWS and breathing in water is alsosupported by the observation that fur seals assume a uniqueposture when sleeping unihemispherically in water. Adultand young [78] fur seals lay on their side with three flippersin the air, while the front flipper in the water constantlypaddles (Fig. 3). This posture keeps the nostrils above thewater’s surface, thus allowing concurrent sleep and breath-ing. Sleeping with three flippers out of the water may alsominimize heat loss through the flippers [6]. While in thisposture, the hemisphere contralateral to the moving flippertends to be more awake (desynchronized) than the otherhemisphere. Although tactile sensory input from the movingflipper or vibrissae in the water may keep the contralateral

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Fig. 2. Electrophysiologic recordings of the cape fur seal during different states: (1) wakefulness; (2) REM sleep; unihemispheric slow-wave sleepwith eitherthe left (3) or right (4) hemisphere asleep; and (5) bihemispheric slow-wave sleep. The EEG was recorded from the left and right fronto-occipital (LFOandRFO) and fronto-parietal (LFP and RFP) cortex. EMG, neck electromyogram; ECG, electrocardiogram; EOG, electrooculogram. Reprinted fromNeuroscience Letters, Vol 143, Lyamin OI, Chetyrbok, I.S., Unilateral EEG activation during sleep in the cape fur seal,Arctocephalus pusillus, 263-266,1992, with permission from Elsevier Science.

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hemisphere awake, it seems more likely that the wakingstate permits movement to occur since the flipper does notmove during USWS on land [6]. Interestingly, as soon as thefur seal enters REM sleep, flipper movement stops and thehead sinks under water [79]. This may account for the loweramount of REM sleep when sleep in water is compared tothat on land [6,79]. Cape fur seals (Arctocephalus pusillus)also exhibit USWS when sleeping on land (the EEG has notbeen recorded in water) and assume the same posture as thenorthern fur seal when sleeping in the water [75].

USWS has also been recorded in the two species of sealions investigated, the Stellar’s (Eumetopias jubatus) ([214,cited in [75]) and southern sea lions (Otari bryonia) [80].However, sleep in water has been investigated only in theStellar’s sea lion. Rather than lying on their side at thesurface, as in fur seals, Stellar’s sea lions swim continuouslyduring USWS, a pattern similar to dolphins. Thus, USWS insea lions is not associated with the posture shown in Fig. 3for fur seals, but does appear to be linked with motor activ-ity required for surfacing to breathe.

USWS may also serve non-respiratory functions, such aspredator detection, since it also occurs on land. Consistentwith a predator detection function, USWS appears to beassociated with unilateral eye closure in fur seals sleepingon land [75]. Unlike the situation in dolphins, but like that inbirds (see below), the hemisphere contralateral to the openeye is more awake (desynchronized) than the other hemi-sphere in both northern and cape fur seals. Furthermore, onland cape fur seals usually sleep with the open eye facingaway from the substrate, suggesting that fur seals use USWS

to monitor the environment for predators or conspecifics.Assuming that the association between unilateral eyeclosure and USWS holds when sleeping in water, thisstate may also allow fur seals to visually detect predators,such as sharks and killer whales, approaching from below.In summary, as suggested for Cetaceans, USWS may servemultiple, non-mutually exclusive functions in eared seals.

3.7. No unihemispheric sleep in true seals

Ironically, the absence of USWS in true seals providedanother unique opportunity to investigate the evolution ofUSWS in aquatic mammals. Sleep has been studied in fourspecies of seals in the family Phocidae (Table 1). However,the EEG was recorded from both hemispheres in only threespecies; Caspian seals (Phoca caspia) [4,81], young harpseals (Pagophilus groenlandicus) [77,82,83] and youngelephant seals (Mirounga angustirostris) [84,85]. Duringsleep on land and in the water, all three species displayBSWS and REM sleep, but not USWS. The seals usuallyremain motionless during sleep on land and in the water.During sleep on land or at the water’s surface, breathingmay occur without arousal from sleep. Elephant seals float-ing near the surface may also raise their head above thesurface to breathe without awakening from SWS [84].However, when sleeping under water, seals hold their breathand periodically awaken to return to the surface to breathe.Although sleep in grey seals (Halichoerus grypus) wasrecorded from only one hemisphere, this species also remainsessentially motionless and shows long respiratory pauses

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Fig. 3. Posture assumed by northern fur seals during unihemispheric slow-wave sleep in water. In this example, the fur seal is lying on its left side while the leftflipper (connected to the awake (right) hemisphere) constantly paddles. This posture allows the fur seal to keep its nostrils above the water’s surface, while theleft hemisphere sleeps. When the fur seal switches to lying on its right side, the left hemisphere remains awake while the right hemisphere sleeps. Reprintedwith permission of Grass-Telefactor, An Astro-Med, Inc. Product Group.

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during sleep under water [86]. Since true seals tend to inhabitthe polar regions [87], breath holding during BSWS may belinked to the need to sleep while submerged under the polar icefields [75,82]. The presence of long respiratory pauses and theabsence of motion during BSWS under water in true seals lendsupport to the hypothesis that USWS and the accompanyingmotor activity allows eared seals to sleep and breathe concur-rently inwater. When the results fromboth families ofseals arecompared it becomes clear that each strategy is a solution tothe same problem, sleeping and breathing in an aquatic envir-onment; true seals sacrifice breathing to maintain sleep, andeared seals sacrifice sleep in one hemisphere to maintainbreathing.

3.8. Evolution of sleep and breathing in pinnipedia

The interpretation of the evolutionary sequence leading totwo distinct forms of sleeping and breathing in water is heav-ily dependent upon our current understanding of pinnipedevolution. Although earlier work suggested an independentorigin for true seals and eared seals plus walruses, with trueseals evolving from musteloidea (weasel- or otter-like) ances-tors, and eared seals and walruses evolving from ursoidea(bear-like) ancestors, recent fossil [88] and molecular [89–91] evidence indicates that both groups evolved from acommon semi-aquatic ancestor, most closely related to muste-loidea [90]. This raises the question as to whether sleeping inwater evolved before or after the two groups diverged. Ifsleeping in water evolved after divergence, then breath hold-ing during BSWS in true seals and USWS in eared seals prob-ably evolved as independent solutions to the same problem.However, if sleeping in water evolved prior to divergence,then sleep in one of the families was secondarily modified;depending upon the ancestral form of sleep, USWS was eitherlost by true seals or acquired by eared seals.

3.9. Sirenia: manatees

The link between USWS and the aquatic environment ledto the investigation of sleep in the final group of aquaticmammals, the Sirenia. The order Sirenia includes threespecies of manatees and one dugong that appear to beclosely related to elephants and hyraxes [92–94]. Sireniaare exclusively aquatic, inhabiting shallow waters. Onlytwo studies have investigated sleep in Sirenia (Table 1).The first recorded sleep in a single Caribbean manatee(Trichechus manatus), but failed to detect USWS ([215,cited in [95]). However, the authors caution that the shortrecording period (only two nights) may have limited theirability to detect USWS. The second study investigated sleepin a two-year-old female Amazonian manatee (Trichechusinunguis) [95,96]. In addition to the typical features ofmammalian REM sleep and SWS, this manatee alsodisplayed USWS. SWS occupied 27% of the recordingtime (REM sleep only 1%) with approximately 25% ofSWS occurring unihemispherically. In contrast to dolphinsand eared seals, USWS was not associated with the main-

tenance of motor activity required for respiration; the mana-tee remained motionless at the bottom of the pool during allstages of sleep. In both species of manatee, each respiratoryact was associated with a brief, bilateral arousal from eitherSWS or REM sleep, a pattern similar to that recorded in trueseals sleeping under water. In this respect, the presence ofUSWS in manatees is inconsistent with the hypothesis thatUSWS evolved in aquatic mammals only to facilitatebreathing during sleep. USWS in manatees may thereforeserve other functions such as predator detection.

4. Unihemispheric sleep in birds

4.1. Background of avian unihemispheric sleep

And smale fowles … slepen al the night with open ye¨Chaucer (1386).

In the prologue to Chaucer’s,The Canterbury Tales, birdsare observed sleeping with an open eye. Nearly 600 yearslater, scientists revealed that this observation was not just atale. Spooner [97] was the first to demonstrate an associationbetween unilateral eye closure and USWS in birds. DuringEEG studies of young chickens (Gallus gallus domesticus),Spooner observed periods of unilateral eye closure asso-ciated with an interhemispheric EEG asymmetry; the hemi-sphere contralateral to the open eye showed activity typicalof wakefulness, while the other showed activity typical ofSWS. Unilateral eye closure and EEG asymmetry occurredin association with periods of bilateral eye closure andBSWS. Visual stimuli presented to the open eye producedrapid behavioral and EEG arousal, indicating that thecontralateral hemisphere was functionally awake. Althoughnot explicitly identified as USWS, Spooner’s observationsprovide the earliest EEG evidence for USWS in birds or anyanimal.

Subsequent studies also found an association betweenunilateral eye closure and USWS in chickens and othergalliformes. In a developmental EEG study, Peters, Vonder-ahe and Schmid [98] observed that sleeping three-week-oldchickens responded to a mild stimulus (e.g. a faint sound orgentle blow of air) by opening only the eye closest to thestimulus source, a response associated with desynchroniza-tion (or awakening) of only the contralateral hemisphere.Peters et al. were the first to fully recognize the implicationsof these findings in young chickens, noting that their result“raises a theoretical question as to whether this particularchick is asleep or awake”. Subsequently, Ookawa alsoobserved an association between unilateral eye closureand USWS in young chickens ([99]; see also Ref. [100]for interhemispheric EEG asymmetry in chicken embryos),adult chickens ([101]; see also Ref. [102]) and adult japa-nese quail (Coturnix coturnix japonica) [103] (Table 1).Furthermore, as in dolphins and fur seals, surface andsubcortical recordings from chickens revealed that USWS

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was apparently a characteristic of the entire hemisphere[101].

Despite these early studies, avian USWS went largelyunnoticed by sleep researchers until its rediscovery in theglaucous-winged gull (Larus glaucescens). Ball et al.[104,105] investigated the physiology of gulls sleeping inthe laboratory and their sleep behavior in the wild. As inchickens and quail, USWS in gulls was also associatedwith unilateral eye closure. Ball et al. [104] also measuredthe metabolic rate occurring during various behavioral andEEG states. Since metabolic rate is usually lower duringSWS when compared to wakefulness [49], the metabolicrate during USWS should be intermediate between BSWSand wakefulness. However, the metabolic rate duringUSWS was similar to that occurring during BSWS, withboth being lower than wakefulness. In this respect, birds inUSWS are ‘metabolically asleep’ with one hemisphereawake. Future studies employing recordings of corticaltemperature, an indirect measure of brain metabolism[49], may reveal an interhemispheric asymmetry in corticaltemperature similar to that observed in dolphins duringUSWS.

In wild gulls, bouts of unilateral eye closure usuallyoccurred in close temporal proximity with periods of bilat-eral eye closure [105]. Episodes of unilateral and bilateraleye closure lasted 3–4 s; such short sleep bouts are typicalof birds that sleep in the open [106]. Unilateral eye closure,and presumably USWS, comprised 17% of total sleep timebased on eye closure. Closure of the right eye was as likelyas closure of the left, indicating no population bias for onehemisphere to sleep more than the other. However, the eyethat was closed was influenced by environmental conditionssuch as the direction of the sun or wind. In general, the eyefacing adverse conditions remained closed more often thanthe other. Although this may indicate a protective functionfor unilateral eye closure independent of USWS, it seemsmore likely that closure of the eye towards adverse condi-tions simply reflects an optimal choice for which eye tosleep with under the prevailing conditions.

Given the association between unilateral eye closure andUSWS reported in several studies, Ball et al. [104,107] usedeye state to determine the prevalence of USWS in birds. Asurvey of birds sleeping in a zoological park revealedunilateral eye closure, and presumably USWS, in speciesfrom diverse taxonomic groups (Table 1). Unilateral eyeclosure occurred in 29 species from 13 orders, includingsocial and solitary, terrestrial and aquatic, diurnal andnocturnal, and in species with lateral and frontally facingeyes. Unilateral eye closure was not detected in Cuculi-formes (cuckoos), Apodiformes (swifts and hummingbirds),and the flightless ratites; Tinamiformes (tinamous), Rhei-formes (rheas) and Casuariiformes (cassowaries and emus).However, Ball et al. [104] caution that further observationsare needed to confirm the absence of unilateral eye closurein these groups. These behavioral results suggest thatUSWS is widespread in birds, and raise the question as to

whether their theropod dinosaur ancestors [108,109] alsoslept unihemispherically.

Despite the prevalence of unilateral eye closure and itsassociation with USWS in birds, a few studies have failed todetect this pattern. Ayala-Guerrero et al. [110] reportedperiods of interhemispheric asymmetry in high-amplitudeslow-waves during SWS in parakeets (Aratinga canicu-laris), but apparently these periods were not associatedwith unilateral eye closure. Tobler and Borbe´ly [111]were unable to detect unilateral eye closure in pigeons(Columba livia), due to the difficulty of observing botheyes simultaneously, and no signs of USWS were observedin the EEG. Szymczak et al. [112] recorded episodes ofUSWS from the ectostriatum (most other studies haverecorded the EEG from the hyperstriatum accessorium, orvisual Wulst) of the European Blackbird (Turdus merula),but were also unable to observe both eyes simultaneously.Although the eye facing the camera was almost alwaysclosed during USWS, the authors did not report whetherthe hemisphere closest to the camera was almost alwaysawake, as would be expected if the eye facing away fromthe camera were open.

Several factors may account for the discrepancies in thereporting of avian USWS. Perhaps the simplest explanationis that USWS is genuinely lacking in some species.However, a more probable explanation involves the natureof the avian EEG. When compared to mammals, the magni-tude of change in EEG amplitude and frequency from wake-fulness to SWS is relatively small in birds (reviewed inRefs. [106,111]). This is due, in part, to low-frequencyactivity occurring during wakefulness. Given the smalldifferences in EEG activity between wakefulness andSWS, assessments based on visual scoring of the EEGmay fail to detect all but the most extreme levels of inter-hemispheric asymmetry. Furthermore, subtle levels of inter-hemispheric asymmetry associated with unilateral eyeclosure may only become apparent when the state of botheyes is monitored closely.

In the first objective assessment of avian USWS, we useddigital period amplitude analysis (PAA) of the EEG inmallard ducks (Anas platyrhynchos) to characterize theassociation between unilateral eye closure and USWS[113]. PAA is a time domain algorithm which uses zerovoltage crosses, first derivatives and integrated wave ampli-tudes to quantify the amplitude, or power (mV2), of differentfrequencies in the EEG [114]. In this study, episodes of eacheye state were paired up with the PAA results from thecorresponding EEG. As expected, on average, low-frequency power (1–6 Hz) [106] in the hemisphere contral-ateral to the closed eye was greater than that in the hemi-sphere contralateral to the open eye, indicating USWS(Fig. 4). However, low-frequency power in the hemispherecontralateral to the open eye was still greater than thatoccurring during wakefulness with both eyes open. Sincethe open eye and contralateral hemisphere were capable ofresponding rapidly to a threatening visual stimulus, this

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intermediate level of power was interpreted as indicating aquiet waking state, intermediate between a fully alert stateand SWS. Thus, while these results objectively confirm thatunilateral eye closure is associated with USWS in mallards,they also reveal the subtle nature of this effect, a finding thatmay explain some of the discrepancies in the reporting ofUSWS mentioned above. Indeed, we recently completed aPAA analysis of sleep in pigeons (Columba livia), whichrevealed an association between unilateral eye closure andUSWS similar to that observed in mallards [115]. Futureanalyses of the avian EEG using similar objective techni-ques (e.g. PAA or fast Fourier transform power spectralanalysis) (reviewed in Refs. [116,117]) may reveal similareffects in additional species.

4.2. Function of avian unihemispheric sleep

Relatively few studies have addressed the function ofUSWS in birds. Given that birds keep one eye open duringUSWS, the most intuitive explanation is that birds useUSWS to monitor their environment for predators whilestill obtaining some of the benefits of sleep. Rattenborg etal. [118,119] explicitly tested the predator detection hypoth-esis by manipulating the level of risk perceived by sleepingbirds. Since the risk of predation varies considerably overtime and space [120], it was reasoned that birds shouldpossess an ability to facultatively control whether theysleep unihemispherically or bihemispherically. This expec-tation is based upon the assumption that USWS is a lessefficient means of meeting daily hemispheric sleep require-

ments when compared to sleeping with both hemispheressimultaneously. Consequently, when sleeping under lowrisk a bird should sleep with both hemispheres simulta-neously, thereby maximizing the amount of sleep obtainedper hemisphere per unit of time. However, under high risk abird should increase the proportion of sleep that is unihemi-spheric, thereby mitigating to some extent the conflictbetween sleep and vigilance. Finally, since threats oftenarise from a specific direction, birds should chose to orientthe open eye during USWS in the direction of a potentialthreat.

Birds are in fact capable of facultatively controlling whenthey sleep unihemispherically in response to changes inpredation risk. When compared to mallard ducks sleepingsafely in the center of a group, those positioned at the edgeof a group (a position which animals perceive as dangerous)[121,122] showed a 150% increase in USWS and a strongpreference for directing the open eye away from the centerof the group [118,119]. Thus, birds not only have the capa-city to facultatively control when they sleep unihemispheri-cally, but they utilize this ability in a manner that reducesthe conflict between sleep and predator detection. Whilebirds may also use USWS to visually monitor theirsurroundings for things other than predators (e.g. conspeci-fics, food availability, changes in the weather, etc.), predatordetection is likely to be the most important given the conse-quences of failing to detect an approaching predator.

Avian USWS may also serve functions unrelated to moni-toring the environment. Circumstantial evidence suggeststhat some birds may sleep while flying, and it has beensuggested that such sleep occurs unihemispherically[59,70,123]; but see [124]. For example, since the Europeanswift (Apus apus) spends the night in flight, they may obtainsome sleep while flying (reviewed in Ref. [125]). Similarly,the wideawake tern (Sterna fuscata) spends months at seaand quickly becomes waterlogged if it lands on the water’ssurface, leading Ashmole [126] to suggest that they “gettheir rest on the wing”. Many birds that sleep at night duringmost of the year abruptly shift to flying long distances atnight during migration. Whether such birds forgo sleepduring migration, shift to sleeping during the day, or sleepwhile flying is unknown. The only direct, yet anecdotal,evidence for unihemispheric sleep during flight is our obser-vation of glaucous-winged gulls closing one eye whileflying to their roost (C.J.A., personal observation). Giventhe association between unilateral eye closure and USWSpreviously demonstrated in this species [104,105], thesegulls were probably sleeping unihemispherically whileflying.

Sleep during flight may not be as remarkable as it firstseems. For instance, birds may simply engage in brief boutsof sleep while gliding. However, sleep during poweredflight may also be possible, since stereotypical locomotormovements, such as walking or flapping are controlled byspinal reflexes. In fact, flight can occur in birds with bothhemispheres disconnected from the spinal cord [106],

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Fig. 4. The relationship between eye state and EEG power for the left (opencircles) and right (filled circles) hemispheres in the mallard. The four eyestates are both left and right eye open (LO/RO), both left and right eyeclosed (LC/RC), left eye closed and right eye open (LC/RO), and left eyeopen and right eye closed (LO/RC). For each individual mallard (N� 6)EEG power was standardized as a percent of the average power observedduring bihemispheric slow-wave sleep, averaged across all frequency binsfor each bird’s hemisphere. Episodes of REM sleep were excluded from theLC/RC data. Reported values are means^S.E. Greater low-frequencypower in the hemisphere contralateral to the closed eye during unilateraleye closure indicates USWS, see Rattenborg et al. [113,119] for furtherdetails.

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suggesting the possibility of bihemispheric sleep duringflight. Although flight may be possible during bihemisphericsleep, USWS may well be needed to navigate and managethe finer adjustments necessary for flight. Indeed, birdsflying in flocks may utilize USWS to monitor their positionrelative to the rest of the flock in a manner similar to thatobserved in Pacific white-sided dolphins sleeping whileswimming in a group (see above).

4.3. Unihemispheric sleep and functional lateralization inthe avian brain

One area of avian sleep research that promises to yieldsignificant clues to the function of sleep is the potentialrelationship between USWS and functional lateralizationin the avian brain. Several studies from diverse species ofbirds have revealed that each hemisphere is specialized toperform certain cognitive functions (reviewed in Refs.[127,128]). Given that SWS may be related to some aspectof brain functioning during wakefulness, relationshipsbetween hemispheric sleep and functional lateralizationmay provide insight into the causal factors for sleep.Since young chickens display functional lateralization(reviewed in Refs. [123,129]) and USWS, this speciesprovides a unique opportunity to investigate the potentialrelationship between waking brain function and sleep.

Two behavioral studies have explored the relationshipbetween functional lateralization and USWS in chickens.In both studies, eye state was used as an indirect measureof brain state. First, Rogers and Chaffey ([130], cited in[123]) recorded eye states in small groups of 1–17 dayold male chickens. Time spent in both bilateral and unilat-eral eye closure showed consistent changes with age. First,due largely to the decline in bilateral eye closure, theproportion of eye closure that was unilateral increasedwith age. Second, during week two, chickens closed theleft eye more frequently than the right. An examination ofthe pattern of eye state transitions provided a clue to thepossible function of this bias. During the second week, tran-sitions from wakefulness to USWS occurred equally withclosure of the left or right eye. However, transitions frombilateral eye closure to unilateral eye closure usuallyinvolved opening the right eye. Rogers [123] suggests thatthis preference for opening the right eye, presumably tomonitor the environment, is related to the fact that the lefthemisphere is sensitive to major changes in the environ-ment, whereas the right hemisphere is sensitive to changesin detail [131]. Thus, chickens may preferentially open theright eye to check for major changes in the environment,such as the approach of a predator or the location of conspe-cifics. However, whether this eye preference reflects anadaptive behavioral decision or a greater need for sleep inthe right hemisphere at this age remains unclear.

Recently, Mascetti et al. [132] demonstrated shifts in eyepreferences during USWS associated with changes in thechicken’s rearing conditions. Eye state was recorded from

female chickens during the first two weeks of life. Chickenswere raised either with an imprinting object (plastic ball) orin isolation. As in the previous study, bilateral eye closuredecreased and unilateral eye closure increased with age.Furthermore, a significant bias for closure of the left eyewas also observed during the second week under both rear-ing conditions. However, during the first week, only chick-ens raised without an imprinting object showed a bias forclosure of the left eye; chickens raised with an imprintingobject showed no bias for closing one eye more than theother during the first week. Mascetti et al. tentativelysuggest that in chickens raised with an imprinting object,the need to consolidate imprinting memories, a processthought to occur in the left hemisphere [133], may lead tomore sleep in the left hemisphere and an increase in righteye closure, thereby reducing the bias for left eye closureobserved in the absence of an imprinting object (the initialbias for left eye closure remains unexplained). However,following imprinting in chickens, Solodkin et al. [134]observed an increase in REM sleep, but not SWS (USWSwas not addressed in this study). Since REM sleep occursbihemispherically (see below) with both eyes closed, theshift in unilateral eye closure reported by Mascetti et al.does not appear to be related to REM sleep. Nevertheless,since several studies also implicate SWS in memory proces-sing [135–138], Mascetti et al.’s findings may still reflect anincrease in left hemisphere SWS due to unihemisphericmemory processing.

Young chickens also showed shifts in lateralized eye useduring USWS in response to changes in the environment.Mascetti et al. observed an increase in right eye closurefollowing changes in the visual characteristics of theimprinting object. Since fully awake young chickens selec-tively use the left eye and right hemisphere to view novelobjects [131,139], Mascetti et al. suggested that the increasein right eye closure reflects an increase in the use of the lefteye in response to novelty in the environment (i.e. changingthe characteristics of the imprinting object). In this respect,USWS is not simply an epiphenomenon of each hemisphererequiring different amounts of sleep, but may also reflectadaptive decisions regarding eye use. According to thishypothesis, we would expect that by changing the charac-teristics of the chicken’s environment it should be possibleto elicit use of either the left or right eye during USWS. Forexample, changing the characteristics of a cue whichprovides the chicken with meaningful information (impend-ing danger, food availability, etc.) should affect which eye ituses during unilateral eye closure; cues requiring the specia-lizations of the right hemisphere should be viewed with theleft eye, whereas those requiring the specializations of theleft hemisphere should be viewed with the right eye.However, the extent to which a bird utilizes the preferredhemisphere should be limited by that hemispheres need forsleep. Presumably, the less preferred hemisphere will even-tually take over while the preferred hemisphere sleeps.Ultimately, given the presence of functional lateralization

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in the avian brain, the eye a bird chooses to use duringUSWS is likely to influence the manner in which thewhole bird responds to its environment [59].

The behavioral results from young chickens demonstratea unique and largely unexplored opportunity to relatewaking brain function to sleep. Future studies may clarifywhether the age-related shifts in eye preference duringUSWS indicate a greater need for sleep in one hemisphereand/or an adaptive utilization of hemispheric specializationsduring USWS. Presumably, these factors are interrelatedsince extended use of the preferred hemisphere may leadto a greater sleep debt in that hemisphere.

5. Unihemispheric sleep in other vertebrates?

5.1. Reptiles

Despite displaying unequivocal behavioral signs of sleep,several conflicting electrophysiological correlates of beha-vioral sleep have been reported in reptiles (reviewed in Ref.[140]). Most studies report an association between beha-vioral sleep and intermittent high-amplitude, spikes andsharp waves in the EEG. However, a few studies report anassociation between behavioral sleep and high-amplitude,low-frequency activity, e.g. [141]. Complicating mattersfurther are studies that failed to detect any changes in theEEG during behavioral sleep, e.g. [142]. Although somecontroversy persists, Hartse [140] argues convincingly thathigh-amplitude, spikes and sharp waves define a reptiliansleep state homologous with mammalian and presumablyavian SWS.

To date, no electrophysiological study has reportedunihemispheric sleep in a reptile. However, most of thereptilian sleep studies predate widespread knowledge ofthis phenomenon, and many only employed a single EEGrecording that combined the electrical activity from bothhemispheres. Nevertheless, the apparent prevalence ofunilateral eye closure during behavioral sleep in reptilessuggests that sleep, in some form, may occur unihemispheri-cally. Unilateral eye closure during behavioral sleep hasbeen reported in species from each of the three orders ofreptiles in which sleep has been investigated: Squamata(lizards and snakes), Crocodilia (crocodiles, alligators andcaimans) and Chelonia (turtles and tortoises) (Table 1). Thetwo species in the remaining living order of reptiles,Rhynchocephalia (tuataras), have not been studied.

In the four species of Squamata investigated, only beha-vioral signs of unihemispheric sleep were detected. Tauberet al. [143] recorded sleep behavior and EEG activity fromtwo species of chameleons (Chameleo jacksoniand C.melleri). Unilateral eye closure was observed during beha-vioral sleep while in a prone posture. However, the authorsdid not report whether the EEG that recorded the combinedactivity from both hemispheres ofC.melleri showedchanges associated with unilateral eye closure. Flanigan

[144] also observed unilateral eye closure at the start andtermination of behavioral quiescence in black (Ctenosaurapectinata) and green (Iguana iguana) iguanid lizards (seealso Refs. [145,146]). Interestingly, there appeared to be abias for opening one eye more than the other. The ‘favored’eye tended to be the last to close at the onset of behavioralsleep and the first to open towards the termination of sleep.This pattern was accentuated during sleep deprivation withthe iguanas attempting to close the favored eye morefrequently. Periodic opening of one or both eyes reducedthe occurrence of spikes and sharp waves in black iguanas.However, since the EEG recorded the combined activity ofboth hemispheres it was not possible to determine whetherthis affect resulted from awakening in one or both hemi-spheres.

Two studies provide behavioral evidence for unihemi-spheric sleep in Crocodilia. Warner and Huggins [141]recorded the EEG from each hemisphere separately inyoung caimans (Caiman sclerops). Unlike other studies onthe same species which reported an association betweenbehavioral sleep and spikes and sharp waves, e.g. [147],Warner and Huggins found an association between beha-vioral sleep and high-amplitude, low-frequency activity(see discussion in Ref. [140]). However, they did not reportwhether unilateral eye closure had an affect on EEG activ-ity. Unilateral eye closure was also observed in anotherspecies of caiman (C. latirostris), but no EEG evidencefor unihemispheric sleep was reported [145].

Unilateral eye closure has been reported in two species ofturtles. In the box turtle (Terrapene carolina) unilateral eyeclosure, particularly of one specific eye, was observedusually at the onset of behavioral sleep [148]. However,after induced arousal, unilateral eye closure was alsoobserved for up to 4–12 h following resumption of beha-vioral sleep. As in iguanas [144], periodic opening of one orboth eyes reduced the occurrence of spikes and sharp wavesin the EEG, which recorded the combined activity of bothhemispheres. Flanigan [149] also recorded sleep behaviorand EEG activity from the red-footed tortoise (Geochelonecarbonaria). However, unlike the previous study on turtles,the EEG was recorded from each hemisphere separately.Unilateral eye closure occurred at the onset of behavioralsleep, especially during respiratory acts. Furthermore, as inthe box turtle, periodic opening of one specific eye oftenpersisted for several hours after induced arousal. EEGspikes and sharp waves occurred bilaterally and unilaterally,suggesting that sleep, in some form, may occur unihemi-spherically. However, the brief opening of one eye wasassociated with a reduction in the incidence of large ampli-tude spikes and sharp waves inboth hemispheres. In thisrespect, unilateral eye closure appears to be associated witha bihemispheric awakening or lightening of sleep, ratherthan unihemispheric sleep. However, the actual data uponwhich these conclusions are based were not reported. Giventhe significant implications that such findings may have forunderstanding the evolution of unihemispheric sleep,

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further studies utilizing objective methods for quantifyingEEG activity (e.g. PAA or fast Fourier transform powerspectral analysis) (reviewed in Refs. [116,117]; see alsoRefs. [150,151]) are clearly needed for reptiles.

Recently, Mathews and Amlaner [152,153] attempted toclarify whether reptilian unilateral eye closure showsgreater affinity with wakefulness or sleep. Sleep behaviorwas studied in the western fence lizard (Sceloporus occi-dentalis). Based on the results from earlier sleep studies inreptiles, it was reasoned that if unilateral eye closure reflectsa sleeping state, then it should occur primarily while in aprone sleeping posture during the dark phase of the photo-period and arousal latencies should be longer during unilat-eral eye closure when compared to both eyes open. On allmeasures, unilateral eye closure showed greater affinity withwakefulness than sleep. Unilateral eye closure occurredmore often during the light phase while the lizards assumedelevated postures, previously ascribed to wakefulness.Furthermore, arousal latencies in response to visual stimulipresented to the open eye during unilateral eye closure werenot elevated when compared to both eyes open. While theseresults argue against unilateral eye closure reflecting a sleepstate, the functional basis of unilateral eye closure in reptilesremains unclear. This is particularly problematic since byclosing one eye, reptiles reduce their ability to visuallydetect passing prey or approaching predators.

One possible non-sleep related function for unilateral eyeclosure is the prevention of evaporative water loss throughthe eyes. By closing one eye at a time, reptiles may be ableto reduce water loss, while still being able to visually moni-tor a portion of their surroundings. However, Kavanau [70]suggests that if prevention of water loss was the only func-tion for eye closure, then the eyelids should be transparent,as in snakes and some lizards, rather than opaque asobserved in most reptiles. Transparent eyelids wouldallow visual processing to persist while the eyeremained moist. Instead of preventing water loss, Kava-nau suggests that as the need for sleep evolved, opaqueeyelids became necessary to occlude the stream ofvisual information that would otherwise interfere withproposed sleep processes involved in maintaining adap-tive neural circuitry. Given that eye closure occursunilaterally, this line of reasoning suggests that sleep,in some form, may occur unihemispherically in reptiles.

To complicate matters, Mathews and Amlaner [152,153]suggest that short arousal latencies may not necessarily indi-cate an absence of USWS. Certainly, the results from visualtests performed on birds and dolphins during USWS (seeabove) challenge the assumption that USWS should impairarousal latencies; despite having one hemisphere asleep,birds and dolphins respond rapidly to visual stimulipresented to the open eye. Thus, arousal latencies to visualstimulation may not effectively differentiate wakefulnessfrom USWS. Indeed, elevated arousal latencies wouldseem to defeat the apparent purpose of keeping one eyeopen. However, the extent of visual processing during

USWS still needs to be determined. It is conceivable thatvisual processing during USWS is restricted to the detectionof gross changes in the environment, while finer levels ofprocessing are in fact impaired.

Another approach to determining whether unilateral eyeclosure reflects USWS as per avian unilateral eye closure isto compare the circumstances under which reptiles and birdsuse unilateral eye closure. If reptilian unilateral eye closureis a precursor to avian USWS then reptiles should use unilat-eral eye closure in a manner similar to that observed inbirds. As reviewed above, birds use unilateral eye closureand USWS to monitor their environment for approachingpredators. Similarly, Tauber et al. [143] suggested thatunilateral eye closure served a ‘sentinel’ function in chame-leons. Certainly, the observation that unilateral eye closurepersisted after induced arousal in the box turtle [148] andred-footed tortoise [149] is consistent with a predator detec-tion function if the turtles perceived the experimenter to be athreat. Along these lines, it would be interesting to knowwhether the turtles’ open eye faced the direction from whichthe experimenter approached. Finally, Mathews and Amla-ner’s [153] finding that unilateral eye closure in the westernfence lizard occurs primarily in the light phase while in anelevated posture, a pattern similar to that observed in youngchickens [132], is also consistent with a predator detectionfunction. Mathews et al. [154] recently tested the predatordetection hypothesis directly, and showed that unilateral eyeclosure increased following exposure to a predator. Further-more, the lizards showed a preference for directing the openeye toward the last known location of the predator. Both ofthese responses are very similar to those observed inmallards sleeping under low and high risk [118,119].

Another parallel between reptiles and birds is the poten-tial link between a preference for closing one eye more thanthe other and functional lateralization in the brain. Asmentioned above, an eye preference was observed inblack and green iguanas [144], box turtles [148], and red-footed tortoises [149]. This preference is particularly inter-esting since, as in birds, recent studies have found hemi-spheric specializations in reptiles (reviewed in Refs.[128,155]). Moreover, a preference for opening one specificeye following a disturbance (i.e. induced arousal), is similarto the response observed in chickens following changes intheir imprinting object [132]. However, in the reptilestudies, the authors did not report whether it was alwaysthe left or the right eye that remained open. Consequently,it is unclear whether an eye closure bias exists in reptiles.

5.2. Amphibians

The prevalence of behavioral signs of unihemisphericsleep in reptiles suggests that their amphibian ancestorsslept in a similar manner. Relatively few studies have inves-tigated sleep in amphibians (reviewed in Ref. [140]), andnone of these provide adequate information to assess thepresence or absence of EEG signs of unihemispheric

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sleep. Moreover, as in reptiles some studies report EEGcorrelates of behavioral sleep, while others failed to detectany sleep-related changes in the EEG. Unilateral eye closurehas only been reported in the bull frog (Rana catesbiana)[156]. However, it only occurred briefly during respiratoryacts, and did not appear to be associated with behavioralsleep. The other studies in amphibians neither report thepresence nor absence of unilateral eye closure. Thus, addi-tional studies aimed at detecting unilateral eye closure, andpotential neurophysiological correlates, during behavioralsleep would be informative.

5.3. Fish

The few studies of sleep in fish provide no evidence forunihemispheric sleep. Only two studies have investigatedthe EEG in fish (reviewed in Ref. [140]). In the tench(Tinca tinca), the EEG remained unchanged during wake-fulness and behavioral sleep [157]. Conversely, in thecatfish (Ictalurus nebulosus), the transition from wakeful-ness to sleep was characterized by an increase in low-frequency activity and spikes [158]. However, since theEEG apparently recorded the combined activity of bothhemispheres, no evidence for unihemispheric sleep wasprovided. Although several studies have reported behavioralsleep in fish (reviewed in Ref. [140]), the absence of eyeclosure in most fish necessarily precludes behavioral signsof unihemispheric sleep, such as unilateral eye closure.Along these lines, Kavanau [124] argues against thepresence of unihemispheric sleep in constantly swimmingfish based, in part, on the absence of unilateral eye closure.Despite the absence of unilateral eye closure, sleep in someform may nevertheless occur unihemispherically in fish.

6. Neurophysiological mechanisms of unihemisphericsleep

The neuroanatomical structures and neurophysiologicalprocesses responsible for USWS remain largely unknown.An understanding of the potential mechanisms behindUSWS is contingent upon an understanding of sleepmechanisms in general. Since only SWS occurs unihemi-spherically, we will focus on those mechanisms involved inthe alternation between SWS and wakefulness. Althoughvirtually all of the research into sleep mechanisms is derivedfrom mammals, several of these mechanisms probably alsoapply to birds (reviewed in Refs. [106,159,160]).

The alternation between wakefulness and SWS involvesthe integration of influences from several components of thecentral nervous system (reviewed in Ref. [161]). Certaincomponents actively promote wakefulness, whereas othersactively promote SWS. The components involved in wake-fulness include the reticular formation, locus coeruleus,posterior hypothalamus, subthalamus and basal forebrain.The reticular formation consists of a network of neuraltissue in the central region of the brainstem that spans

from the medulla to the thalamus and hypothalamus. Thereticular formation receives collateral input from variousascending sensory pathways, and projects via two mainroutes, dorsally to the thalamus, and ventrally to the poster-ior hypothalamus, subthalamus, and basal forebrain. Projec-tions from these regions cause activation throughout thecortex. Although cortical activation is influenced by sensoryinput indirectly via the reticular formation, and to a lesserextent via sensory pathways, sleep does not simply arisefrom the absence of sensory input. In addition to beinginfluenced by the reticular formation, the posterior hypotha-lamus, subthalamus and basal forebrain are capable of acti-vating the cortex without input from the reticular formation.Consequently, wakefulness arises from both sensory inputand wakefulness promoting neurons. Conversely, SWSarises from a combination of reduced sensory input viathe reticular formation and increased activity in sleeppromoting neurons in the medulla, preoptic area, anteriorhypothalamus, and basal forebrain.

Sleeping with one hemisphere at a time would appear torequire a degree of hemispheric separation. In mammals, thecorpus callosum is the main route of interhemisphericcommunication. Although the corpus callosum is notdirectly involved in controlling SWS, extensive interhemi-spheric communication may prevent the development ofsleep in only one hemisphere at a time. Accordingly,when compared to other mammals, Cetaceans have anunusually small corpus callosum [162]. For example,despite having cerebral hemispheres five times larger thanhumans, the corpus callosum of killer whales is the samesize as in humans [36]. Similarly, birds lack a corpus callo-sum, and only have small interhemispheric commissures[163]. While these findings seem to support a role for thecorpus callosum in USWS, other lines of evidence argueagainst such a role. Although the degree of interhemisphericEEG coherence (a measure of synchrony between homolo-gous portions of each hemisphere) may be reduced follow-ing sagittal transsection of the corpus callosum [164–166],or in humans lacking a corpus callosum [167,168], sleep isinvariably bihemispheric under these conditions. Thus,while the corpus callosum seems to be involved in interhe-mispheric synchronization of EEG activity during sleep, itdoes not contribute to the genesis of BSWS. Consequently,the small interhemispheric connections observed in animalswith USWS do not appear to account for USWS.

Having ruled out interhemispheric connections, USWSmust arise from the functional independence of subcorticalstructures. The results from early lesion studies providesome clues to the potential mechanisms responsible forUSWS. In cats, SWS developed asynchronously in eachhemisphere only following sagittal transsection of thelower brainstem [165,169]. This pattern was observedeven when the interhemispheric commissures, includingthe corpus callosum, were left intact. These findings suggestthat USWS may arise from the separation or ‘uncoupling’ ofsleep regions in the lower brainstem. However, the functional

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independence of such sleep regions alone does not account forthe highly coordinated USWS in animals like dolphins.Mukhametov [4] suggests that USWS in dolphins arisesfrom “the functional independenceand(authors’ italics) reci-procal interrelation of the two halves of some synchronizing ordesynchronizing system in the lower brainstem”. Transition-ing between USWS and BSWS in eared seals and birds alsoappears to be a coordinated process, since, as previouslymentioned, these animals are apparently capable of control-ling when they sleep unihemispherically.

One promising approach to identifying the neuroanatomicalstructures involved in coordinating USWS would be tocompare the brains of animals with USWS to those lackingUSWS. Anatomical differences in regions involved in thecontrol of sleep and wakefulness may yield clues to USWS.For instance, when compared to mammals lacking USWS, theposterior commissure of mammals with USWS was larger andshowed greater decussation of the ascending fibers from thelocus coeruleus in the brainstem (P. Manger, personal commu-nication). This difference was most profound in dolphins, thegroup of animals in which USWS is most well developed.These findings are promising since the noradrenergic neuronsof the locus coeruleus are known to be involved in maintainingvigilance and cortical activation [170] (reviewed inRef. [161]). Interestingly, elephants also showed this modifi-cation in the posterior commissure. Given this finding, andrecent evidence that suggests that manatees and elephantsshare a common aquatic ancestor [92], elephants may alsosleep unihemispherically.

In birds, the association between unilateral eye closureand USWS has greatly influenced discussions of avianUSWS control. In particular, several authors relate USWSto the fact that the optic nerves decussate completely at theoptic chiasma in birds [97,98]. For example, Spooner [97]attributed USWS in young chickens to “complete decussa-tion of the optic tract and almost complete anatomicalseparation of the anterior reticular formation neurons bythe third ventricle (p. 75)”. Accordingly, this has led tothe suggestion that avian USWS results from unilateralvisual input which activates the contralateral hemisphere(either directly via the visual pathways or indirectly viathe reticular formation), rather than the active involvementof sleep and wakefulness promoting regions, as suggestedfor dolphins [6]. While unilateral visual input may contri-bute to USWS, several lines of evidence indicate that USWSarises from the active control of sleep and wakefulnessseparately in each hemisphere. First, complete decussationat the optic chiasma is only the first step in the avian visualsystem. The avian visual system includes two main path-ways, the thalamofugal pathway and the tecotofugal path-way, which are thought to be homologous with themammalian geniculostriate and colliculothalamocorticalpathways, respectively [171]. In birds with laterally posi-tioned eyes, the thalamofugal pathway conveys visualinformation primarily to the visual Wulst (i.e. hyperstriatumaccessorium) of the contralateral cerebral hemisphere

[172–175]. Since most avian sleep studies have recordedthe EEG from the Wulst, this projection pathway appearsto be consistent with the proposition that avian USWS arisesfrom unilateral visual input. However, USWS is alsorecorded from the ectostriatum [101,112], a portion of thecerebral hemisphere that receives bilateral visual input fromthe tectofugal pathway [172]. Consequently, if USWS wassimply the result of unilateral visual processing, then onlythe Wulst contralateral to the closed eye should show SWS,while the ectostriatum of both hemispheres should showwaking activity. However, since one entire hemisphere,including the ectostriatum is involved in USWS, visualinput alone does not appear to account for avian USWS.

Other lines of evidence also argue against a primary rolefor unilateral visual input in maintaining USWS. In anattempt to determine whether USWS was strictly a resultof unilateral visual input, Ookawa studied sleep in unilater-ally [176] and bilaterally [177] blinded chickens. If USWSwas a result of unilateral visual input, then blinded chickensshould no longer exhibit USWS. However, despite theabsence of visual input, USWS was still observed in theblinded birds. Similarly, USWS was also observed in gullsduring complete darkness [104]. While these studies suggestthat USWS is endogenously controlled, Ookawa [177] notesthat USWS may also occur in response to unilateral auditoryinput, as observed in young chickens [98]. Although unilat-eral sensory input may awaken one hemisphere or keep onehemisphere from falling asleep, the observation that transi-tions from BSWS to USWS occur in the apparent absence ofexternal stimuli in young chickens [123] and mallard ducks[119], indicates that USWS is endogenously controlledunder certain circumstances. Moreover, as shown inmallards, such transitions are performed in a precise andadaptive manner, with the eye facing a threat being morelikely to open. From this line of evidence, it is clear thatinstead of being a passive result of unilateral visual input,avian USWS is an endogenously controlled adaptive state ofreadiness during which visual processing can occur.

Finally, a discussion of the potential mechanismsinvolved in avian USWS control would be incomplete with-out considering the role of melatonin. In birds andmammals, melatonin is released from the pineal glandduring the dark phase of the photoperiod. In pigeons,constant light suppresses circadian rhythms in circulatingmelatonin [178] and sleep [179], whereas infusions ofphysiological levels of melatonin restore sleep duringconstant light [180,181]. Thus, in contrast to mammals inwhich melatonin appears to induce species-specific noctur-nal behavior (i.e. sleep in diurnal mammals and wakefulnessin nocturnal mammals) [182], melatonin has a direct sleepinducing effect in pigeons (Note: melatonin is probably notthe only factor controlling sleep in birds, since many birdsare aphasic, engaging in sleep and wakefulness throughoutthe photoperiod; [106,183]). Despite melatonin’s somno-genic effect in pigeons, we have recently recorded unilateraleye closure and USWS in pigeons during the dark phase of

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the photoperiod [115]. Interestingly, Berger’s group did notaddress the issue of unilateral eye closure or USWS in thestudies mentioned above. This apparent discrepancy may beattributable, in part, to the difficulty in viewing both eyessimultaneously and the subtle level of interhemisphericasymmetry in low-frequency activity associated with unilat-eral eye closure in birds (see discussion above). Neverthe-less, our results may be compatible with the sleep inducingeffects of melatonin if certain neural mechanisms enablebirds to selectively activate one hemisphere during sleep,thereby overriding the effects of melatonin. Interestingly,these results suggest that while diffuse sleep factors (mela-tonin in this case) can exert global sleep-inducing effects,other mechanisms may competitively regulate wakefulnessat a local level within the brain (see Ref. [68]).

7. Unihemispheric REM sleep?

Sleep in mammals and birds is composed of two distinctstates, SWS and REM sleep, yet only SWS is known tooccur unihemispherically. This raises the question as towhy unihemispheric REM sleep has not been observed.Actually, the issue of unihemispheric REM sleep encom-passes two questions: (1) why does REM sleep not occurunihemispherically with SWS in the other hemisphere; and(2) why does REM sleep not occur unihemispherically withwakefulness in the other hemisphere. Noting the similarityin EEG activity occurring during wakefulness and REMsleep, a few early studies entertained the idea that the“awake” hemisphere during USWS might actually be inREM sleep, rather than wakefulness. However, given theabsence of other signs of REM sleep, it was concludedthat the hemisphere was in fact awake [34,47,177]. Indeed,a combination of SWS in one hemisphere and REM sleep inthe other would seem to defeat the likely function of unihe-mispheric sleep: obtaining the simultaneous benefits ofwakefulness and sleep.

The reasons for the absence of strictly unihemisphericREM sleep (REM sleep in one hemisphere and wakefulnessin the other) are less clear. Two potentially interrelatedexplanations may account for the absence of unihemisphericREM sleep. REM sleep in one hemisphere may interferewith waking functions, or wakefulness in one hemispheremay interfere with REM sleep functions. Regarding theformer, Horne [184] suggests that since some form ofmentation (i.e. ‘dreaming’) probably occurs in animalsduring REM sleep [185], animals may be unable to adap-tively reconcile the different forms of mentation occurringin each hemisphere during unihemispheric REM sleep.Moreover, it is interesting to note that while cats with asagittal transsection of the interhemispheric commissuresand brainstem were able to simultaneously display REMsleep in one hemisphere and SWS in the other, REMsleep in one hemisphere and wakefulness in the other wasnever observed [165]. In reference to interfering with REM

sleep, it is conceivable that some of the proposed functionsfor REM sleep, such as memory processing [137,186,187],require that both hemispheres be in a state of REM sleep.Alternatively, the loss of muscle tone associated with REMsleep may simply counteract potential benefits gained frombeing able to engage in unihemispheric REM sleep. Finally,since long bouts of REM sleep may be incompatible withrespiration in aquatic mammals [42] and predator detectionin birds, an inability to develop unihemispheric REM sleepmay have led to the reduction or modification of REM sleepin both aquatic mammals [42] and birds [106]. As a result,these animals may have developed other means of compen-sating for less REM sleep [42,188] (see also Ref. [189]).

8. Human unihemispheric sleep?

Humans are not known to sleep unihemispherically. Evenfollowing transsection of the corpus callosum, or in humanslacking a callosum, sleep is invariably bihemispheric. Yet,certain studies, which have found interhemispheric asym-metries during BSWS in humans, seem to warrant discus-sion within the context of USWS. First, in a study ofinterhemispheric EEG asymmetry, Armitage et al. [190]found greater asymmetry in theta and delta activity duringSWS (i.e. human stage 4 sleep) when compared to stage 2 orREM sleep (see also Ref. [191]). Moreover, the direction(left . right, or right. left) of this asymmetry tended toalternate between hemispheres, a pattern which Armitageet al. related to the alternation of USWS in aquaticmammals and birds. Interestingly, auditory evoked poten-tials elicited during sleep also show greater absolute inter-hemispheric asymmetry during SWS when compared tostage 2 or REM sleep [192]. This later finding is particularlyrelevant with respect to USWS, since it indicates that at anygiven time one hemisphere maintains greater auditorycontact with the environment. Armitage et al. [190] attrib-uted these EEG asymmetries to an ultradian rhythm in hemi-spheric synchronicity (see also Ref. [193]) which may beinfluenced by factors that determine hemispheric sleep debt,such as task performance during prior wakefulness.

Recent findings suggest that waking performance can, infact, influence subsequent SWS unihemispherically. Kattleret al. [73] addressed several fundamental questions regard-ing SWS regulation by selectively stimulating one portionof the brain during wakefulness. Previous studies had shownan increase in SWS time and/or intensity (reflected in slow-wave activity) in response to increased time spent awake(reviewed in Ref. [62]), however, it has been unclearwhether time awake alone produces this effect, or whetherthe type of activity occurring during wakefulness also has anaffect. Furthermore, recent theoretical models of SWS regu-lation suggested that SWS might be regulated locally inresponse to brain use [71,72,194,195]. To test whetherwaking activity has a local influence on SWS, Kattler et al.[73] increased the amount of waking activity occurring in

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one portion of the brain by vibrating one hand. Previouspositron emission tomography studies demonstrated thatthis type of stimulation primarily activates the somatosen-sory cortex of the contralateral hemisphere [196–198]. Aspredicted, following stimulation, slow-wave activity duringSWS increased only in the contralateral somatosensorycortex. The fact that this effect was restricted to the brainregion stimulated during prior wakefulness demonstratesthat slow-wave activity during SWS can be influenced bylocal brain use. Thus, even in animals lacking USWS, thepropensity for sleep can be influenced at the hemispheric, oreven more local, level.

In addition to being sensitive to prior waking perfor-mance, changes in the level of interhemispheric EEG asym-metry are also correlated with mental disorders. SeveralEEG parameters distinguish patients with major depressivedisorders (MDD) from healthy controls [199–201]. Ofparticular relevance to unihemispheric sleep is the findingthat interhemispheric EEG coherence (a measure of inde-pendence of EEG activity in the two hemispheres) is rela-tively low in MDD patients.

Recently, Sinton et al. [202] have also identified a similarphenomenon in rats. When compared to rats sleeping inpairs, rats sleeping alone show lower interhemisphericcoherence. Sinton et al. suggest that lower coherence inrats is related to the stress of isolation. Stress may alsoaccount for the similar results in humans with MDD[200]. Although stress may mediate lower interhemisphericcoherence in isolated rats, this effect may still reflect anadaptive response. As previously mentioned, in healthyhumans, one cerebral hemisphere may be more responsivethan the other to auditory input during SWS. Along theselines, lower interhemispheric coherence may allow isolatedrats to maintain greater auditory contact with the surround-ing environment. As a result, rats sleeping alone may bebetter equipped to detect approaching predators. Thishypothesis can be readily tested by comparing auditoryarousal thresholds during SWS between isolated and pairedrats. Similar analyses of interhemispheric coherence andarousal thresholds in healthy humans sleeping under lowand high stress conditions would also be of particular inter-est, since stress induced insomnia may arise, in part, fromhypersensitivity to environmental stimuli.

It is tempting to speculate that the potential link betweenstress and lower interhemispheric coherence in terrestrialmammals is evolutionarily homologous to USWS in birdsand possibly reptiles. However, reduced interhemisphericcoherence is not the only change noted in the EEG ofisolated rats and MDD patients. Isolated rats and MDDpatients also show lowerintrahemispheric coherence, afinding not known to occur in animals with USWS. More-over, MDD patients also show greater beta (16–32 Hz),theta and delta activity in the right hemisphere duringREM sleep, greater beta in the right hemisphere duringSWS (reviewed in Ref. [200]), as well as stable asymmetriesin waking prefrontal alpha (8–13 Hz) activity (reviewed in

Refs. [203,204]). Thus MDD appears to be associated with ageneral dysregulation of brain activity at various levels.Furthermore, unlike rats given a partner, this dysregulationdoes not disappear during remission in MDD patients[201,204]. Consequently, while stress may mediate bothUSWS (at least in birds) and lower interhemispheric coher-ence in terrestrial mammals, it remains unclear whetherthese effects are homologous. A greater understanding ofthe mechanisms behind both USWS and EEG dysregulationin MDD may clarify whether these states are in some wayrelated.

9. Why do most mammals sleepbihemispherically?

Given the utility of sleeping unihemispherically, it issurprising that most mammals sleepbihemispherically.Sleep has been investigated in several of the major groupsof mammals [18,21,205,206], yet only aquatic mammals areknown to sleep unihemispherically. The restricted occur-rence of USWS in mammals becomes even more intriguingif the reptilian ancestors to mammals slept unihemispheri-cally. Although the results from modern reptiles clearlyremain equivocal with respect to USWS, and there arelimitations inherent in drawing conclusions about ancientreptiles from studies on modern reptiles [207], the preva-lence of unilateral eye closure in modern reptiles suggeststhat the reptilian ancestors to mammals and birds may haveslept unihemispherically. Assuming that the reptilian ances-tors did sleep unihemispherically, or exhibited a precursorstate, then why did only mammals lose the capacity to sleepunihemispherically? A clue may lie in the early stages ofmammalian evolution. Early mammals were small, noctur-nal, shrew-like insectivores [208,209] that presumably sleptduring the day, hidden safely in their burrows to avoidpredation from diurnally active reptiles. Presumably, as aresult of being protected in their burrows, there was no needfor unihemispheric sleep. In fact, sleeping unihemispheri-cally may have been selected against since it would be a lessefficient means of sleeping. By the time the descendants ofearly mammals radiated back into diurnal niches, they mayhave lost the capacity to sleep unihemispherically.

Sleeping exclusively bihemispherically may have alsobeen favored if this form of sleep is somehow superior tothe bihemishperic sleep exhibited by animals capable ofunihemispheric sleep. For example, BSWS in animalscapable of USWS may be fundamentally different fromBSWS in animals that do not sleep unihemispherically. Inthe former, the two hemispheres may be viewed as sleepingindependently, but at the same time, whereas in the later, thehemispheres may be sleeping as a coordinated or integratedwhole. Along these lines, sleep may play a role in integrat-ing the functions of different brain regions. Thus, BSWS interrestrial mammals may be superior to the BSWS inanimals with USWS because it allows integration withinand between hemispheres, rather than just within a

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particular hemisphere. Assuming that the proposed or otherunspecified benefits of sleeping exclusively bihemispheri-cally are incompatible with an ability to sleep unihemi-spherically, it may have been beneficial for earlymammals to forgo unihemispheric sleep, in particular ifthey had a lower need for maintaining vigilance duringsleep as suggested above.

Regardless of whether mammals lost the ability to sleepunihemispherically, or never had the capacity in the firstplace, the limited occurrence of USWS in mammalssuggests that the evolution of USWS is constrained bycosts associated with sleeping unihemispherically. Forexample, the neuroanatomical reorganization required forUSWS may be incompatible with the proposed benefits ofsleeping exclusively bihemispherically, or other adaptivefunctions of the central nervous system occurring duringeither sleep or wakefulness. Such functions may be relatedto the significant changes in brain organization that occurredwhen early mammals invaded nocturnal niches [210].Consequently, only under certain circumstances, such assleeping at sea, may the benefits of USWS outweigh thecosts. Although the specifics of such a tradeoff remainobscure, this scenario needs to be considered when attempt-ing to explain the limited occurrence of USWS in mammals.Ultimately, a greater understanding of the mechanismsinvolved in USWSmight reveal whether such a tradeoff exists.

Finally, the near absence of USWS in mammals mayresult from a more simple explanation; sleeping unihemi-spherically is not the only solution to the conflict betweenwakefulness and sleep. Indeed, other solutions may beeasier to develop. For example, some animals such asruminants compromise between sleep and wakefulness byengaging in extended periods of drowsiness [211], an inter-mediate state between SWS and wakefulness. Presumably,by engaging in drowsiness animals maintain some degree ofawareness while simultaneously obtaining some of thebenefits of sleep. Since all mammals engage in drowsinessduring the transition from wakefulness to sleep, the evolu-tion of this strategy would simply involve the elaboration ofan existing state, rather than a reorganization of the nervoussystem. Behavioral adaptations may also mitigate theconflict between sleep and wakefulness. For example, bysleeping in safe locations or in large groups many animalsreduce the risk of predation during sleep. In this respect, theneed to sleep may have had a profound influence on theevolution of habitat selection and sociality in animals[212,213].

10. Conclusions

(1) A largely unexplored area in behavioral ecology is theinherent conflict between sleep and wakefulness. Wakeful-ness is clearly an adaptive state that allows animals to inter-act with their environment, yet its efficacy is contingentupon sleep, a vulnerable state of reduced responsiveness.

The evolution of unihemispheric sleep exemplifies thispoint and serves as a unique solution to the problem.Although mammals and birds exhibit two types of sleep(i.e. SWS and REM sleep), only SWS occurs unihemi-spherically. Since alert wakefulness and deep SWS fall atthe extreme ends of a continuum, animals that displayunequivocal USWS also show intermediate states; onehemisphere may sleep deeply, while the other is in a statebetween full alertness and SWS. Such interhemisphericasymmetries in SWS reflect different degrees of unihemi-spheric sleep, and appear to have the same functional basisas unequivocal USWS.

(2) Among mammals, USWS has only been observed inthree aquatic orders (i.e. Cetacea, Pinnipedia and Sirenia). InCetaceans, virtually all of their sleep is USWS, whereaseared seals and manatees also display bihemispheric SWS(BSWS) and REM sleep. In Cetaceans and eared seals,USWS allows surfacing to breathe and sleep to occur simul-taneously in an aquatic environment. Despite sharing acommon aquatic ancestor with eared seals, true seals arenot known to sleep unihemispherically. Instead, true sealshold their breath while sleeping bihemispherically underwater, a strategy that may have arisen in conjunction withbreath holding under the polar ice fields. The function ofUSWS in Sirenia remains unclear since they do not useUSWS for surfacing to breathe. Therefore, USWS in Sireniais likely to serve other functions such as threat detection.Indeed, USWS may also serve a predator detection functionin Cetaceans and eared seals, since they keep one eye openduring USWS.

(3) In contrast to mammals, USWS appears to be wide-spread among birds. Birds also exhibit both BSWS andREM sleep. An association between USWS and unilateraleye closure suggests that USWS serves a predator detectionfunction in birds. Indeed, birds are capable of facultativelycontrolling when they sleep unihemispherically verses bihe-mispherically in a manner consistent with such a function.Birds may also use USWS to monitor other aspects oftheir environment, and circumstantial evidence suggeststhat birds may actually sleep unihemispherically duringextended flights.

(4) The few studies of sleep in fish and amphibians failedto detect either behavioral or electrophysiological evidencefor unihemispheric sleep. Several studies have investigatedsleep in modern reptiles, however, the results are equivocalwith respect to USWS, and sleep in general, since the elec-trophysiological correlates of mammalian and avian SWSare not consistently present in reptiles. However, thepresence of unilateral eye closure during behavioral sleepsuggests that sleep, in some form, may occur unihemispheri-cally in reptiles. Moreover, the use of unilateral eye openingfor predator detection in both reptiles and birds suggests thatavian unilateral eye closure, and possibly USWS, evolvedfrom reptilian unilateral eye closure.

(5) There is a tendency to view USWS as a highlyspecialized form of sleep which evolved from bihemispheric

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sleep. Certainly, the observation that only highly specializedaquatic mammals display USWS supports this view.However, the apparent prevalence of USWS in birds and thepossible existence of USWS in modern reptiles suggest thatUSWS is in fact the ancestral form of sleep. Even if closure ofone eye is not associated with unihemispheric sleep in reptiles,this behavioral state may have served as a precursor forUSWS. Ultimately, a final conclusion on the early stages ofUSWS evolution awaits future studies aimed at identifyingpotential neurophysiological correlates of unilateral eyeclosure in reptiles.

(6) The reasons for the relative absence of USWS inmammals remain obscure. The mammalian brain does notappear to be fundamentally constrained in its ability todevelop USWS since this state has apparently arisen on atleast three separate occasions in mammals (i.e. Cetacea,Pinnipedia and Sirenia). Even terrestrial mammals such asrats and humans exhibit slight interhemispheric asymme-tries in EEG activity during BSWS, which may indicate apropensity for unihemispheric sleep. Alternatively, thelimited occurrence of USWS suggests that there are costsassociated with sleeping unihemispherically. Specifically,the reorganization of the central nervous system requiredfor USWS may interfere with other adaptive brain func-tions, such as integrating the functions of both hemispheres.Consequently, the benefits of USWS may outweigh thecosts only under extreme circumstances, such as sleepingat sea. The relative absence of USWS may also reflect thefact that other solutions to the conflict between sleep andwakefulness are easier to develop. For example, manymammals engage in extended periods of drowsiness, anintermediate state that may serve as a compromise betweensleep and wakefulness. Ultimately, a greater understandingof the reasons for little USWS in mammals promises toprovide insight into the functions of sleep in general.

(7) Although very little is known about the precise neuro-physiological mechanisms involved in USWS, the controlof USWS in aquatic mammals and birds appears to involvethe coordination of functionally independent sleep andwakefulness regions, possibly located in the brainstem. Agreater understanding of the mechanisms responsible forUSWS promises to yield further insight into the mechan-isms behind SWS in general.

(8) The discovery and investigation of USWS hassignificantly influenced our overall understanding ofsleep. In particular, the finding that SWS is homeosta-tically regulated independently within each hemispherein dolphins demonstrates that sleep serves a primaryfunction for the brain. However, the specific aspectsof wakefulness that cause and/or are dependent uponsleep remain unclear. The discovery of consistent shiftsin hemispheric sleep time associated with functionallateralization in the developing avian brain provides apromising paradigm in which to address these questions.Clearly, the manner in which animals reconcile thefundamental conflict between sleep and wakefulness

has and will continue to serve as a powerful tool forunraveling the functional reasons behind sleep.

Acknowledgements

We would like to thank the following people for theirvaluable comments on earlier drafts of this manuscript:Ruth Benca, Oleg Lyamin, Paul Manger, Chris Mathewsand Chris Sinton. We also thank Oleg Lyamin, Paul Mangerand Chris Sinton for their willingness to share several piecesof unpublished data that greatly enhanced the manuscript.Finally we thank the reviewers for their helpful comments.

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