User:Eugene M. Izhikevich/Proposed/Sleep in animals
<review>General comment: Since this chapter covers sleep in mammals and not 'animals' I suggest modifying the title accordingly. Why does the recommended reading include papers on avian sleep?</review>
Sleep in mammals (or sleep phylogeny) refers to the variation in the nature and amount of sleep across species. A primary motivation for the study of sleep in various animals is to gain some insight into the function(s) of sleep. What aspects of sleep, if any, are present in all mammals? What aspects of sleep differ between animals? Why are there two kinds of sleep, REM (rapid eye movement) sleep and non-REM sleep?
The amount and nature of sleep is correlated with age, body size and ecological variables, including life in the terrestrial vs. aquatic environment, diet and the safety of the sleeping site. The sleep phylogeny literature suggests that sleep reduces activity to the amount needed for feeding and species reproduction, and maximizes energy conservation, thereby furthering genetic survival. Theories of REM sleep function have suggested that in addition to these functions, this state may have a role in periodic brain activation during sleep, in localized brain and body recuperative processes and in emotional regulation.
Sleep studies in terrestrial mammals
Daily sleep amounts vary substantially throughout the mammalian class. Some animals, such as bats and opossums, sleep for 18-20 h/day ( Figure 1), whereas others, such as the elephant and giraffe, sleep as little as 3-4 h/day. <review>Why are Tobler's studies which are more comprehensive and more recent than Zepelin's original data on sleep in giraffes and elephants not cited here?</review> One might expect that species in each mammalian order would have a similar pattern of sleep because of their defining genetic, behavioral, and anatomical similarities. However, this is not the case. Primates as a group or carnivores as a group or rodents as a group do not have a characteristic sleep duration. Sleep time in these various orders overlaps extensively and any “order related” contribution to sleep duration must be small relative to other factors (Zepelin et al., 2005). Human sleep does not appear to be quantitatively unique in its duration or in the proportion or absolute amount of REM sleep.
Daily sleep amounts are highest in carnivores, lower in omnivores and lowest in herbivores. Sleep time is inversely correlated with body mass in herbivores. This correlation is responsible for a significant overall correlation between body mass and sleep time over all mammals studied to date (Zepelin et al., 2005) (Figure 1). <review>It would be helpful to mention how much of the variance is explained with this correlation, actually it is rather small</review>
Most studies of mammalian sleep have been performed on placental (eutherian) or marsupial mammals. The third subclass of mammals is the monotremes, found in Australia and New Guinea. These egg laying mammals have more genetic and physiological similarities to reptiles and birds than do other mammals and are thought to have more characteristics of the common mammalian ancestor (Grutzner et al., 2004). In contrast to placental mammals, both the echidna and platypus show evidence of brainstem activation during sleep, with the platypus displaying intense rapid eye, limb and bill movements periodically during sleep. However, the low voltage neocortical EEG typically seen in placental and marsupial mammals during REM sleep is not consistently present during sleep in either the echidna or platypus during these motor activities. Instead the neocortical EEG may resemble that of non-REM sleep (Siegel et al., 1996; Siegel et al., 1999). Thus, these “primitive” mammals appear to have a form of REM sleep largely localized to the brainstem.
Sleep in marine mammals
All terrestrial mammals show relatively high voltage low frequency (slow) neocortical electrical brain waves (EEG) bilaterally during the behavioral state that is recognized as non-REM sleep. In contrast, cetaceans (whales and dolphins) almost never have high voltage slow waves in both hemispheres at the same time (Mukhametov et al., 1977; Lyamin et al., 2004). The manatee (Trichechus inunguis, a member of the order Sirenia) also has unihemispheric slow waves (Mukhametov et al., 1992). The eye contralateral to the hemisphere with slow waves is almost always closed while the other eye is almost always open. <review>Depending which paper one refers to, the correlation between eye open/closed states is rather loose. I would mention this and provide a reference</review>. There have been no published reports documenting REM sleep in cetaceans, making them the only studied mammals in which this state has not been observed.
The bottlenose dolphin (Tursiops truncatus), when not floating or resting on the bottom <review>specify bottom of what</review>, generally swims in a single direction (usually counterclockwise) even as the brain hemisphere with slow waves alternates. Some smaller cetacean species are rarely, if ever, immobile, moving and avoiding obstacles 24 h a day from birth until death, even during unihemispheric slow wave activity; these animals may never exhibit the immobility that is used in terrestrial mammals to define the state of sleep (Mukhametov et al., 2002).
<review>I suggest including 2-3 sentences on sleep in Pinnipeds, to make a chapter on sleep in marine mammals more complete</review>
Postpartum sleep behavior in cetaceans
Further evidence for the unique properties of “sleep” in cetaceans are the phenomena of a near absence of sleep behavior in neonates and a postpartum reduction of sleep behavior in their mothers (Lyamin et al., 2005). All terrestrial mammals have minimal activity and maximal total sleep and REM sleep amounts at birth, with sleep gradually decreasing and activity gradually increasing to adult levels as the animals grow to maturity (Carskadon and Dement, 2005). <review>Why cite C and D here, if the sentence refers to animal sleep?</review> This is not the pattern in cetaceans. Killer whales (Orcinus orca) and dolphins have minimal amounts of sleep behavior (i.e., immobility or eye closure) at birth, with sleep behavior slowly increasing to adult levels over a period of months. This minimal amount of sleep behavior occurs during the period of most rapid growth of body and brain for the newborn, during a period of bonding to the mother and learning how to nurse, find food, avoid predators and swim efficiently. The continuous activity of cetaceans has adaptive value in allowing the neonate, which is much less insulated by body fat than the adults, to thermoregulate in cold ocean water. The suppression of sleep behavior also allows the neonate to swim with and be protected by its mother during development. As the animal gains mass and blubber and approaches adult size, adult-like “sleep” or rest behavior, including periods of immobility, emerges. Both mother and calf go without substantial amounts of immobility and without substantial amounts of the eye closure linked to unihemispheric slow waves during the postpartum period. Keeping rats awake for comparable periods is lethal.<review>Omit this last sentence: cause of death is unknown, many unspecific factors contributed to the death of the rats. In addition, the dolphin data do not include EEG whereas Rechtschaffen's data are based on polygraphic recordings, so a comparison of the two data sets is misleading</review> Neither cetacean mother nor calf show any rebound increase in the amount of sleep behavior following this period. <review>Were these animals observed for a sufficiently long time to warrant this statement? It should be specified whether the animals were observed during day and night</review>
<review>The original paper in Nature elicited two replies. I suggest more caution in generalizing here, since Scholarpedia is dedicated to a large readership which will be unaware of the problems</review>
Neocortical activity and sleep
Although neocortical EEG changes are the most easily observed electrical correlate of non-REM sleep, as they are recordable from scalp electrodes in humans and from electrodes placed on the surface of the cortex in other animals, sleep produces large changes in the rates and patterns of neuronal activity in nearly all brain regions. Cortical EEG phenomena are controlled by and reflect activity in thalamic, hypothalamic and brainstem reticular regions. The cellular activity changes underlying the changes in neocortical EEG include calcium fluxes into and hyperpolarization of neocortical and thalamic neurons that are synchronized in large populations, producing high voltage brain waves (Steriade, 2005; Huber et al., 2004). But neocortical size does not correlate positively with sleep amount. Both total brain weight and encephalization correlate poorly and negatively with total non-REM and REM sleep amounts (Zepelin et al., 2005). The elephant, which has the largest neocortex of any terrestrial mammal, has one of the smallest sleep amounts. Conversely, the rat and the platypus, which have smooth cortices with small total neocortical volumes, have extremely large amounts of non-REM and REM sleep, with the platypus having more REM sleep than any other animal studied to date (Siegel et al., 1999).
Although neocortical size does not appear to be a major determinant of either nonREM or REM sleep amounts, recent work <review>the first paper investigating this regional use-dependent aspect was from Kattler in 1994, therefore hardly recent</review> has indicated that neocortical activity during sleep may be altered by prior waking activity. Some such changes dissipate with continued waking, (Krueger et al., 1999 <review>this paper is a theoretical approach well worth citing, but neither Krueger nor Obal performed experiments to support the statement they are being cited for</review>;Huber et al., 2004; Vyazovskiy et al., 2004) suggesting that localized recuperative processes may occur during either waking or sleep in systems projecting to, or within, the neocortex.
Sleep may be adaptive because it conserves energy and suppresses behavior across portions of the circadian cycle, just as hibernation does across certain seasons (O'Hara et al., 1999). Large herbivores may have evolved reduced sleep amounts because they are more vulnerable to predators than small herbivores (Lima et al., 2005). <review>It is difficult to reconcile this last sentence with the low amount of sleep of elephants which are hardly vulnerable during their sleep</review> A second hypothesis is that these grazing animals may need to spend more time awake in order to eat, because of the low caloric density of their food. <review>The animals in the wild (giraffes/elephants) do not walk around at night and graze, their feeding is pretty much restricted to times when there is still light. Also, giraffes spend hours ruminating while elephants do not.</review> A complimentary hypothesis is that small herbivores and other mammals may need to maximize sleep amounts in order to conserve energy, because their relatively high surface area to body mass ratio makes it costly to maintain their body temperature, but retreating to a warm, protected nest may minimize this cost. A striking feature of sleep in animals with small daily sleep amounts, such as many herbivores, is that sleep depth, as judged by sensory response threshold <review>reference?</review>, appears to be less than that in animals requiring more sleep; i.e., animals with reduced sleep amounts do not appear to “make up” for reduced sleep by sleeping more “deeply.” <review>Waking threshold determined by stimulation after sleep deprivation has not been strictly investigated:. The sentence is misleading because what is needed here are studies recording the EEG and evaluating whether there is an EEG marker for sleep intensity in herbivores as there is for many other mammals.</review>
Energy conservation may be particularly important in newborns. Their high surface area to body mass ratio and need for rapid growth makes the energy conservation achieved by sleep highly adaptive. Furthermore, animals that are immature at birth benefit from the sleep-induced reduction in exposure to danger. When body size increases and sensory-motor systems mature, young animals derive greater benefits from waking activities, seek food and can begin to defend themselves, consistent with the developmental decrease in sleep time.
Body mass, metabolism and sleep control
One of the best established relations in mammalian biology is the inverse relationship between body mass and mass specific metabolic rate. Small animals have high metabolic rates; large animals have low metabolic rates. Brain metabolic rate is correlated with body metabolic rate (Turner et al., 2005). Elevated metabolism is linked to a number of biochemical changes, several of which have been linked to sleep control.
Sleep time may be related to defense against oxidative stress. A high metabolic rate results in the generation of high levels of reactive oxygen species by mitochondria. This reactive oxygen species generation has been linked to normal aging. Sleep deprivation in the rat is accompanied by indications of increased oxidative stress and evidence of membrane disruption in the hippocampus, subcortical brain regions and peripheral tissues (Eiland et al., 2002; Ramanathan et al., 2002; Everson et al., 2005) There appear to be no such changes in the neocortex (Gopalakrishnan et al., 2004; Ramanathan et al., 2002) Higher brain metabolic rates may require longer periods of sleep to interrupt reactive oxygen species induced damage to brain cells, facilitate the synthesis and activities of molecules that protect brain cells from oxidative stress, allow sufficient time for the repair or replacement of essential cellular components in neurons and glia (Zimmerman et al., 2004), and deal with other biochemical consequences of waking metabolic activity.
<review> In my view this entire chapter on metabolism is generalizing findings obtained mainly in the rat to “sleep in animals”. It would be necessary to specify at several places which species is being referred to. In addition it should be clear to the reader that this chapter refers to studies in laboratories in a very artificial environment. Little or nothing is known about metabolic demands and the effects on sleep and sleep patterns in animals in the wild. </review>
One may hypothesize that the “ratio” of the energy conservation benefit of sleep to the waking metabolic activity-derived need for sleep for brain recuperation varies across species. Carnivores and omnivores, which tend to have more sleep than predicted on the basis of body mass, may make more use of the energy conservation aspects of sleep, since their generally safe sleep places (Allison and Cicchetti, 1976) and abilities to eat meals with high caloric density may make continuous activity unnecessary. In such a situation, genetic fitness might best be served by energy conservation, which would reduce the need for hunting, aid nurturing of the young, speed development and generally aid in reproductive success.
Protein synthesis in the brain is increased during slow wave sleep (Nakanishi et al., 1997). New neurons are generated in adult animals in the olfactory bulb, the subventricular zone lining the lateral ventricles, and in the subgranular cell layer of the dentate gyrus of the hippocampus, in a process that produces functional neurons in 3-4 weeks. It has been shown that this neurogenesis is facilitated by exercise and blocked by stress. Short term (2-3 day) total sleep deprivation, even when done controlling for other forms of stress, also blocks subsequent neurogenesis in the dentate gyrus (Guzman-Marin et al., 2003). Thus, sleep may have a general role in allowing or facilitating neurogenesis.
Rapid eye movement (REM) sleep amount is positively correlated with total sleep amount and negatively correlated with body weight. However, if one statistically controls for body weight or brain weight, REM sleep amount is most strongly correlated with immaturity at birth (Zepelin et al., 2005). Altricial animals, those that are immature at birth, tend to have more REM sleep than animals that are mature at birth, or precocial. This tendency is marked in the neonatal period. But perhaps more remarkable is that altricial mammals continue to have more REM sleep as adults. The platypus has eight hours of REM sleep per day as an adult. The platypus neonate cannot thermoregulate, locomote, acquire food or defend itself at birth and lives attached to its mother. The ferret, likewise, is immature at birth and the adult has over six hours of REM sleep per day. In contrast, the guinea pig has only one hour of REM sleep per day as an adult (Jouvet-Mounier et al., 1970). The guinea pig is born with teeth, claws, fur and eyes open; it thermoregulates at birth, locomotes within an hour of birth and eats solid food within a day of birth. Similarly, the sheep and giraffe are relatively mature at birth and have little REM sleep (less than one hr/day) at maturity (Zepelin et al., 2005). The extremely high levels of REM sleep seen at birth, followed by a slow decrease to adult levels in altricial terrestrial animals, must be an important clue to its function. This time course, combined with the observation that neuronal activity levels are high in REM sleep, led to the hypothesis that this sleep state is involved in the development of the brain.
Dolphins, which can be continuously mobile while having unihemispheric slow waves must have continuous brainstem activity to control this movement, since the brainstem is the final path for motor control. This contrasts with the situation in land mammals, all of which have bilateral slow waves and immobility during sleep and greatly reduced brainstem activity. The absence or reduction of REM sleep in marine mammals displaying unihemispheric slow waves supports the hypothesis that the stimulation of brainstem activating systems is an important function of REM sleep. Similarly, the manifestation of REM sleep in monotremes as a largely brainstem state, without marked neocortical activation, suggests that REM sleep may have evolved as a state of brainstem activation, with cortical stimulation functions added later in evolution. The cold-induced increase in REM sleep amount in the isolated brainstem, the increased REM sleep amount at the minimum of the circadian brain and body temperature cycles and the increase in the temperatures of brain regions during REM sleep (Baker et al., 2005; Wehr, 1992) are consistent with this brainstem activation hypothesis.
Allison T, Cicchetti DV (1976) Sleep in mammals: Ecological and constitutional correlates. Science 194:732-734.
Baker FC, Angara C, Szymusiak R, McGinty D (2005) Persistence of sleep-temperature coupling after suprachiasmatic nuclei lesions in rats. Am J Physiol Regul Integr Comp Physiol ..
Carskadon MA, Dement WC (2005) Normal human sleep. In: Principles and Practice of Sleep Medicine (Kryger MH, Roth T, Dement WC, eds), pp 13-23. Philadelphia: W.B. Saunders.
Eiland MM, Ramanathan L, Gulyani S, Gilliland M, Bergmann BM, Rechtschaffen A, Siegel JM (2002) Increases in amino-cupric-silver staining of the supraoptic nucleus after sleep deprivation. Brain Res 945:1-8.
Everson CA, Laatsch CD, Hogg N (2005) Antioxidant defense responses to sleep loss and sleep recovery. Am J Physiol Regul Integr Comp Physiol 288:R374-R383.
Gopalakrishnan A, Ji LL, Cirelli C (2004) Sleep deprivation and cellular responses to oxidative stress. Sleep 27:27-35.
Grutzner F, Rens W, Tsend-Ayush E, El-Mogharbel N, O'Brien PC, Jones RC, Ferguson-Smith MA, Marshall GJ (2004) In the platypus a meiotic chain of ten sex chromosomes shares genes with the bird Z and mammal X chromosomes. Nature 432:913-917.
Guzman-Marin R, Suntsova N, Stewart DR, Gong H, Szymusiak R, McGinty D (2003) Sleep deprivation reduces proliferation of cells in the dentate gyrus of the hippocampus in rats. J Physiol 549:563-571.
Huber R, Ghilardi MF, Massimini M, Tononi G (2004) Local sleep and learning. Nature 430:78-81.
Jouvet-Mounier D, Astic L, Lacote D (1970) Ontogenesis of the states of sleep in rat, cat, and guinea pig during the first postnatal month. Dev Psychobiol 2:216-239.
Krueger JM, Obal FJ, Fang J (1999) Why we sleep: a theoretical view of sleep function. Sleep Med Rev 3:119-129.
Lima SL, Rattenborg NC, Lesku JA, Amlaner CJ (2005) Sleeping under the risk of predation. Anim Behav 70:723-736.
Lyamin O, Pryaslova J, Lance V, Siegel J (2005) Animal behaviour: continuous activity in cetaceans after birth. Nature 435:1177.
Lyamin OI, Mukhametov LM, Siegel JM (2004) Relationship between sleep and eye state in Cetaceans and Pinnipeds. Arch Ital Biol 142:557-568.
Mukhametov LM, Lyamin OI, Chetyrbok IS, Vassilyev AA, Diaz RP (1992) Sleep in an Amazonian manatee, Trichechus inunguis. Experientia 48:417-419.
Mukhametov LM, Lyamin OI, Shpak OV, Manger P, Siegel JM (2002) Swimming styles and their relationship to rest and activity states in captive Commerson's dolphins. Proceedings of the 14th Biennial Conference on the Biology of Marine Mammals, Vancouver, Nov 27-Dec 3152.
Mukhametov LM, Supin AY, Polyakova IG (1977) Interhemispheric asymmetry of the electroencephalographic sleep patterns in dolphins. Brain Res 134:581-584.
Nakanishi H, Sun Y, Nakamura RK, Mori K, Ito M, Suda S, Namba H, Storch FI, Dang TP, Mendelson W, Mishkin M, Kennedy C, Gillin JC, Smith CB, Sokoloff L (1997) Positive correlations between cerebral protein synthesis rates and deep sleep in Macaca mulatta. Eur J Neurosci 9:271-279.
O'Hara BF, Watson FL, Srere HK, Kumar H, Wiler SW, Welch SK, Bitting L, Heller HC, Kilduff TS (1999) Gene expression in the brain across the hibernation cycle. J Neurosci 19:3781-3790.
Ramanathan L, Gulyani S, Nienhuis R, Siegel JM (2002) Sleep deprivation decreases superoxide dismutase activity in rat hippocampus and brainstem. Neuroreport 13:1387-1390.
Siegel JM, Manger P, Nienhuis R, Fahringer HM, Pettigrew J (1996) The echidna Tachyglossus aculeatus combines REM and non-REM aspects in a single sleep state: implications for the evolution of sleep. J Neuroscience 16:3500-3506.
Siegel JM, Manger PR, Nienhuis R, Fahringer HM, Shalita T, Pettigrew JD (1999) Sleep in the platypus. Neuroscience 91:391-400.
Steriade M (2005) Brain electrical activity and sensory processing during waking and sleep. In: Principles and Practice of Sleep Medicine (Kryger MH, Roth T, Dement WC, eds), pp 101-119. Philadelphia: Elsevier Saunders.
Turner N, Else PL, Hulbert AJ, Rana T, Couture P (2005) An allometric comparison of microsomal membrane lipid composition and sodium pump molecular activity in the brain of mammals and birds. The acyl composition of mammalian phospholipids: an allometric analysis. J Exp Biol 208:371-381.
Vyazovskiy VV, Welker E, Fritschy JM, Tobler I (2004) Regional pattern of metabolic activation is reflected in the sleep EEG after sleep deprivation combined with unilateral whisker stimulation in mice. Eur J Neurosci 20:1363-1370.
Wehr TA (1992) A brain-warming function for REM sleep. Neurosci Biobehav Rev 16:379-397.
Zepelin H, Siegel JM, Tobler I (2005) Mammalian sleep. In: Principles and Practice of Sleep Medicine (Kryger MH, Roth T, Dement WC, eds), pp 91-100. Philadelphia: Elsevier Saunders.
Zimmerman JE, Mackiewicz M, Galante RJ, Zhang L, Cater J, Zoh C, Rizzo W, Pack AI (2004) Glycogen in the brain of Drosophila melanogaster: diurnal rhythm and the effect of rest deprivation. J Neurochem 88:32-40.
Amlaner CJ, Ball NJ (1994) Avian sleep. In: Principles and Practice of Sleep Medicine (Kryger MH, Roth T, Dement WC, eds), pp 81-94. Philadelphia: W.B. Saunders Company.
Rattenborg NC, Lima SL, Amlaner CJ (1999) Facultative control of avian unihemispheric sleep under the risk of predation. Behav Brain Res 105:163-172.
Siegel JM (2005) Clues to the functions of mammalian sleep. Nature 437:1264-1271.
Tobler I (2005) Phylogeny of sleep regulation. In: Principles and Practice of Sleep Medicine (Kryger MH, Roth T, Dement WC, eds), pp 77-90. Philadelphia: Elsevier Saunders.
Zepelin H, Siegel JM, Tobler I (2005) Mammalian sleep. In: Principles and Practice of Sleep Medicine (Kryger MH, Roth T, Dement WC, eds), pp 91-100. Philadelphia: Elsevier Saunders.