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Unihemispheric slow-wave sleep (USWS), also termed as asymmetric slow-wave sleep (ASWS), is characterized by having one hemisphere of the brain in a state of slow-wave sleep and the other hemisphere in a state that is anywhere between slow-wave sleep and alert wakefulness. The phenomenon has been observed in a number of terrestrial, aquatic as well as avian species. Unique physiology, including differential release of the neurotransmitter acetylcholine has been linked to the phenomenon. [1] It is hypothesized that there are a range of reasons for species to exhibit USWS, including the ability to sleep in areas of high predation or during long migratory flights. The behavior remains an important research topic because of the information it may provide neuroscientists on the broader mechanisms behind sleep in general.[2]

Northern Fur Seal (Callorhinus ursinus) exhibits unihemispheric slow-wave sleep in aquatic environments.

Definition/Characterization[edit]

The state of unihemispheric slow-wave sleep can be defined as having one hemisphere of the brain in a state of slow-wave sleep and the other hemisphere in a state that is anywhere between slow-wave sleep and alert wakefulness. Where in the continuum between slow-wave sleep and alert wakefulness the “sleeping” hemisphere falls varies between species and circumstances, but having this “interhemisphereic asymmetry”, difference in states between hemispheres, is characterized as unihemispheric slow-wave sleep [3] and is done for several reasons in many different animals.

"Sleep" and Slow-Wave Sleep[edit]

Sleep is generally defined behaviorally and electrophysiologically. Behaviorally, characteristics that define sleep include: inactivity, ability to rapidly return to awake state, elevated arousal threshold (to return to wakefulness), and increase following sleep deprivation. Electrophysiological characteristics can be determined by an electroenceohaigraph (EEG) and can be used to classify sleep into states. Sleep can be split into two major states: REM and SWS. During REM (rapid-eye movement) sleep, muscles are fully relaxed and the EEG of a REM sleeper’s brain shows low-amplitude, high-frequency waves almost identical to those displayed during wakefulness. During SWS (slow-wave sleep), a sleeper’s brain shows high-amplitude, low-frequency “delta” or “theta” waves. Slow-wave sleep refers to the deepest stage of non-REM in humans and all non-REM sleep in all other animals.

USWS’s challenge to this definition[edit]

Unihemispheric slow-wave sleep is defined electrophysiologically, and sleepers in USWS often exhibit characteristics that challenge the typical behavioral characteristics of sleep. Animals sleeping in unihemispheric slow-wave sleep have been shown to stand, swim and even fly - defying the elementary definition of inactivity that accompanies the behavioral characterization of sleep. [4]


Species exhibiting USWS[edit]

Aquatic mammals[edit]

Carnivora[edit]

A major difference between the orders pinnipeds and the cetaceans is that, while the Cetaceans solely sleep in water, pinnipeds are capable of sleeping on either land or water. In addition, pinnipeds that exhibit USWS do so at a higher rate while sleeping in water than on land. Significant research has been done illustrating that the northern fur seal can alternate between BSWS and USWS depending on its location while sleeping. While on land, 69% of all SWS is BSWS; however, when sleep takes place in water, 68% of all SWS is found with interhemispheric EEG asymmetry (USWS). Most likely because of their ability to sleep on land, animals in this order exhibit REM sleep along with USWS. The unihemispheric slow-wave sleep that these animals do exhibit in water is suspected to be because of their need to maintain swimming and respiration during those times, and to monitor predation risks.[1]

Species Found In
Of the order Carnivora, the Pinnipeds have been shown to sleep in USWS. Though no USWS has been observed in true seals, different species in the group Otariidae, eared seals, have been found to exhibit USWS including:

Sirenia[edit]

REM has been found in this order of mammals, even though they remain in water the extent of their time. USWS has been found in one of the species of this order and it is suspected that this group exhibits USWS in a similar form and for similar reasons to the final order of aquatic mammals, Cetaceans, though more study is needed.[6]

Species Found In
The second order of aquatic mammals, sirenia include three species of manatees. Experiments have only exhibited USWS in the Amazonian manatee (trichechus inunguis).[5]

Cetaceans[edit]

The final order of aquatic mammals has been shown to exhibit USWS the most. Of the Cetaceans, Odontoceti (dolphins, porpoises and toothed whales) have been found to sleep unihemispherically. In the other order of Cetaceans, Mysticeti (whales), has not displayed unihemispheric slow-wave sleep. [3] Their use of USWS is characterized by factors such as heat, predation and maintaining swimming.[7] These species do not sleep in REM, or sleep in a modified form of REM. This is theoretically because they must maintain swimming during all times of their day and, being mammals, need to also maintain respiration during these times. [7][6]

Species Found In
Of all the cetacean species, USWS has been found to be exhibited in the following species:

Birds[edit]

Many species of birds have been found to demonstrate USWS. This is quite unlike mammals, where it is relatively uncommon, only occurring in aquatic mammals. These species vary widely, from songbirds and birds of prey to domestic birds. Those not yet studied tend to exhibit unilateral eye closure characteristic of unihemispheric sleep.[8] Many studies have been done on these groups of birds and how their use of USWS is characterized by factors such as heat, learning, behavior/imprinting, predation, flight and migration.[8]

Species Found In
Multiple species of birds have been found to exhibit USWS including:

Reptiles and Amphibians[edit]

Not much study has been done on Reptiles and Amphibians, but several species have been shown to use USWS. This use of USWS is mostly governed by the risk of predation present during observation.[9] Studies of the Desert Iguana (Dipsosaurus dorsalis) showed that the species does sleep unihemispherically and that the amount of unihemispheric slow-wave sleep is varied depending on the environmental threats perceived by the lizard.[9] Western fence lizards (Sceloporus occidentalis) have also been shown to use asynchronous eye closure - suggesting unihemispheric slow-wave sleep. This study also indicated that the amount of asymmetric eye closure in the fence lizard was related to predator detection. [10]

Species Found In

Fish and Insects[edit]

It is difficult to study Fish and Insect sleep for several reasons including their lack of eyelids, their size and their need to be in water (fish). For these reasons, not much study has been done on species in these groups to demonstrate their use of USWS but it is likely that they also exhibit the function. [5] Species to note in their behavior towards sleep include sharks and pelagic fish. Interesting work has also begun with the fruit fly regarding sleep.[7]


Reasons for USWS[edit]

Experiments with unihemispheric slow-wave sleep demonstrate that it is a mechanism used only in certain circumstances or environments. The implementation of USWS, then, has reasons behind it. The reasons for sleeping in unihemispheric slow-wave sleep have been hypothesized to vary from being in a high-risk predator environment, to needing to maintain respiration. Unihemispheric sleep has been shown to aid in the visual vigilance of the environment, the preservation of movement, and in Cetaceans, the controlling of the respiratory system.[11]

Sleeping Under Risk of Predation[edit]

Most species of birds are able to detect approaching predators during unihemispheric slow-wave sleep. It has been found that the usage of USWS of certain species of birds increases as the risk of predation increases.[2] A study of mallard ducks corroborated this idea by lining the birds up and motoring amounts of USWS in relation to level of (perceived) predation threat. The "group edge effect" describes the phenomenon in which birds roosting at the edge of the flock are more alert and often scanning for predators. These birds are more at risk than the birds in the center of the flock and are required to be on the lookout. In the study, birds more at risk showed a 150% increase in unihemispheric slow-wave sleep and were more likely to keep the eye directed away from the group open. The same study showed a rapid response to threatening visual stimuli shown to the open eye. [4] In another study with nesting mallard ducks it was again found that vigilance (unihemispheric slow-wave sleep) increased with increasing risks of predation. Increased vegetation obscuring the nest from viewing the surrounding environment/predators stimulated increased sleep unihemispherically, and during times when visibility was higher (daylight) USWS also was increased. These results also support the idea that unihemispheric slow-wave sleep is used to balance predator vigilance and the need for sleep. [12] [13]

Studies working with Desert Iguanas exposed to a predator of the reptile showed reduction in amount of bihemispheric sleep and increase in amount of asymmetrical or “asynchronous” eye closure (AEC). Further, the eye open during sleep most frequently was directed towards the predator - supporting the theory of USWS as an anit-predation device. [9] A similar study of Western fence lizards showed a large reduction in bihemispheric sleep (both eyes closed) and increase in AEC and USWS in response to a predator in the terrarium (as opposed to no change in those lizards exposed to a novel moving stimulus). The open eye during AEC similarly tended to be oriented towards the nearby threat. [10]

Learning, Behavior and Imprinting[edit]

The influence on unihemispheric sleep after periods of learning, behavior and imprinting has been shown in several studies, especially with relation to work with the domestic chick. In one study, chicks reared in pairs showed a bias for more right unihemispheric slow-wave sleep (right hemisphere sleeps) during the second week with their fellows, while those separated from socialization showed no or the opposite bias. This suggests that this difference in amounts of unihemispheric slow-wave sleep in a certain hemisphere is related to social learning tasks. Further this research suggests that the lateralization of the brain that results in differential usage also results in differential need for sleep in that hemisphere. [14] Another similar study related imprinting learning in domestic chicks to differential amounts of USWS (often referred to as monocular/unihemispheric sleep “Mo–Un sleep” when studying chicks). These chicks were allowed to imprint on an object before it was either removed or switched. Unihemispheric slow-wave sleep increased in amount for those who had their imprinting object removed, with no changes in control or switching groups. No bias between hemispheres in amount of USWS was found for control groups or before removal/changes in imprinting object, but significant increase in left-hemisphere sleep occurred after changes or removal. This suggests that secondary imprinting learning (occurring in the left hemisphere) was triggered by a change or removal of the imprinting object and that unihemispheric slow-wave sleep increases in proportion to the lateralized use (possibly because of increased consolidation in that hemisphere). [15]

A following study suggested the same, calling USWS a kind of “local” sleep to recover/consolidate from increased use of that hemisphere in learning tasks. Chicks were exposed to two color-based tasks and a spatial task. Controls of the color tasks (exposed but did not have to learn task) showed slight bias for more right-hemisphere sleep and controls for the spatial task showed no bias. Those that did learn the tasks showed significant increase in/bias for left-unihemispheric slow-wave sleep in the color based tasks and right-USWS in the spatial task – suggesting unihemispheric slow-wave sleep is triggered by lateralized use. [16] This result was replicated exactly when domestic chicks learned a spatial feeding task. Controls showed no bias while the spatial learning task group showed a significant increase in right-hemisphere sleep; again corroborating the idea that amount increase in the hemisphere’s USWS is related to dominance of the right hemisphere during spatial learning trials. [17]

Surfacing for Air and Maintaining Swimming[edit]

Unihemispheric slow-wave sleep seems to allow the simultaneous sleeping and surfacing to breathe of aquatic mammals including both dolphins and seals. Bottlenose dolphins are one specific species of cetaceans that have been proven experimentally to use USWS in order to maintain both swimming patterns and the surfacing for air while sleeping.[18]

Five swimming patterns were observed by Shpak et al. in the Commerson's Dolphin. From this, it was proposed that USWS occurs in these species during the states of “circular swimming” and “quiet chaotic” swimming (at the bottom of a tank), during which other characteristics of sleep were found including muscle jerks and erection in males. [7] Three similar types of swimming behavior during USWS were observed by Sekiguchi in his bottlenose dolphins: "bottom-rest" immobile near the bottom of the tank, "surface-rest" immobile floating at the water surface, and "swim-rest" again observing circle-swimming near the bottom in a repeated path. Sekiguchi observed further behavioral characteristics of sleep with these behaviors – decreased breath frequency and asymmetric eye closure. Trips to the surface for respiration were observed during these swim-sleep periods during which sleep appeared to continue (one eye stayed closed).[6]

Studies of a captive pod of Pacific white-sided dolphins displayed that dolphins slept in USWS and chose to keep the eye open that was directed towards the swimming group rather than leaving open the eye facing the surrounding ocean. This was shown to be consistent with position within the group, as the selected open eye changed when the group rearranged positions. [7][19] A similar eye closure pattern was observed in the bottlenose dolphin, where the eye closed tended to be that facing the interior of a circular path during restful circle-swims. These results support the idea that USWS is used to maintain swimming and to maintain group contact/navigate during these sleep-swims. [6]These findings regarding unihemispheric slow-wave sleep being used to maintain swimming were repeated in studying the white whale. [20]

Thermoregulation[edit]

Brain temperature has been shown to drop when a sleeping EEG is exhibited in one or both hemispheres. This decrease in temperature has been linked to a method to thermoregulate and conserve energy while maintaining the vigilance of USWS. This thermoregulation during USWS has been demonstrated in dolphins and is believed to be conserved among species exhibiting USWS.[21] Experiments administering Diazepam to dolphins to induce USWS also showed a possible connection between the induction of unihemispheric slow-wave sleep and reduction in blood flow and metabolism in the sleeping hemisphere. [22] Another study of Cetaceans suggested that the maintenance of swimming helps to further regulate body temperature in the cold ocean environment. The study showed a strong correlation between heat-generating tail beats and circumstances in which more heat could be lost, suggesting that the need for thermoregulation is related to the need to maintain motion during sleep in cetaceans. [23]

Maintaining Flight and Migration[edit]

It has been shown that there are seasonal and temperature differences in amounts of sleep and times of waking in free-living songbirds. [24] When migrating, birds may undergo unihemispheric slow-wave sleep in order to simultaneously sleep while visually navigating flight.[8] Though EEG measurements have not been able to be conducted during flight, studies of birds such as the common swift, which never lands to rest, suggest that flight and unihemispheric slow-wave sleep are compatible. Like the maintenance of swimming in aquatic mammals, the use of USWS allows for the monitoring of direction and environment using the eye contra-lateral (opposite) to the awake hemisphere (left open during unihemispheric slow-wave sleep). This suggests another purpose for unihemispheric slow-wave sleep: balancing sleep and flight during times when great flights must occur, such as during migration. [8]

Physiology[edit]

In most animals, slow-wave sleep (SWS) is characterized by high amplitude, low frequency electroencephalography (EEG) readings. In USWS, only one hemisphere of the brain exhibits a sleep EEG while the other hemisphere exhibits an EEG typical of wakefulness, but there are other significant physiological aspects of USWS too. [5]

Eye opening[edit]

In domestic chicks and other species of birds exhibiting USWS, one eye remained open contra-lateral to the "awake" hemisphere, while the closed eye was shown to be contra-lateral (on the opposite side of the head) to the hemisphere engaging in slow-wave sleep.[25] This has also been shown to be the favored behavior of white whale and many Cetaceans, although inconsistencies have arisen directly relating the sleeping hemisphere and open eye. The open eye has been shown to be responsive to stimuli and it is predicted that this feature of USWS aids in predator detection, and maintaining flight, swimming and group contact. [11]

Trade-off[edit]

The study of unihemispheric slow-wave sleep also suggests that there is a trade-off in the use of USWS, and in the need for sleep itself. Under less stressful circumstances (i.e. sleeping out of water, low predation risk, not migration season, etc.), across the board it has been shown that Bihemispheric sleep, if possible, is chosen above USWS. This demonstrates that the quality or sleep unihemispherically is less preferable than that of BSWS or REM. The exchange for safety versus sleep itself is also demonstrated by the existence of USWS: Unihemispheric sleep serves as a compromise between the two. [9][26][3][4]

Short-Term Plasticity[edit]

It is also notable that USWS has been demonstrated to be a controllable factor, whether consciously or unconsciously. [26] It has been shown that along with the use of USWS only in certain environments, sleepers in USWS can demonstrate short term plasticity in using it. Studies have found that if an animal being exposed to a stimulus (i.e. fake predator) is exposed without consequence for a period of time, the animal will desensitize to the stimulus and accordingly sleep less in USWS and more in bihemispheric sleep. A study of Desert Iguanas safely exposed to a nearby sidewinder snake (a predator of the reptile) found the iguanas to plastically change their amount of bihemispheric sleep, varying the total down by 50% in exchange for increased USWS. Unharmed after a period of time in this setup, iguanas eventually desensitized to the danger and once again decreased USWS. [9] This finding has been repeated for pigeons. [12]

Role of acetylcholine[edit]

Due to the origin of USWS in the brain, neurotransmitters are believed to be involved in its regulation. The neurotransmitter acetylcholine has been linked to hemispheric activation in northern fur seals. Acetylcholine is released in nearly the same low amounts per hemisphere in bilateral slow-wave sleep (BSWS). However, in USWS, the maximal release of the neurotransmitter acetylcholine is just found in the hemisphere exhibiting an EEG trace resembling wakefulness. The hemisphere exhibiting SWS is marked by minimal release of acetylcholine. This model of acetylcholine release has been further discovered in additional species such as the bottlenose dolphin.[1]

Anatomical variations found in species exhibiting USWS[edit]

Smaller corpus callosum[edit]

USWS requires hemispheric separation to isolate the cerebral hemispheres enough to ensure that the one can engage in SWS while the other is awake. The corpus callosum is the anatomical structure in the mammalian brain which allows for interhemispheric communication (communication in the brain between hemispheres). Cetaceans have been observed to have a smaller corpus callosum when compared to other mammals. Similarly birds lack a corpus callosum altogether and have only few means of interhemispheric connections. Other evidence contradicts this potential role; sagital separations of the corpus callosum in other animals have been found to result in strictly bihemispheric (BSWS) sleep. As a result it seems this anatomical difference, though well correlated, may not directly explain the existence of USWS.[5]

Noradrenergic diffuse modulatory system variations[edit]

A promising method of identifying the neuroanatomical structures responsible for USWS is continuing comparisons of brains that exhibit USWS with those that do not. Some studies have shown induced USWS in non-USWS-exhibiting animals as a result of sagital cross-sections of brain regions, including the lower brain stem, while leaving the corpus callosum intact. Other comparisons found that mammals exhibiting USWS have a larger posterior commissure and increased decussation of nerve fibers from the locus coeruleus in the brain stem. This is consistent with the fact that one form for neuromodulation, the noradrenergic diffuse modulatory system present in the locus coeruleus, is involved in regulating arousal, attention, and sleep-wake cycles.[5]

Complete crossing of the optic nerve[edit]

Complete crossing of the nerves at the optic chiasm in birds has also stimulated research. Complete decussation of the optic tract has been studied as a method of ensuring that the open eye only activates the hemisphere on the same side as the eye. Some evidence indicates that this alone is not enough, as blindness would theoretically prevent USWS if visual stimuli was the sole player in triggering USWS. However, USWS was still exhibited in blinded birds despite the absence of visual input.[5]

Future research[edit]

Recent studies have illustrated that the white-crowned sparrow, as well as other passerines, have the capability of sleeping most significantly during the migratory season while in flight. However, the sleep patterns in this study were observed during migratory restlessness in captivity and might not be analogous to those of free-flying birds. To truly determine if birds can sleep in flight, recordings of brain activity must take place during flight instead of after landing. A method of recording brain activity in pigeons during flight has recently proven promising in that it could obtain an EEG of each hemisphere even if only for short periods of time. Coupled with simulated windtunnels in a controlled setting, these new methods of measuring brain activity could clarify the truth behind whether or not birds sleep during flight.[8]
Additionally, based on research elucidating the role of acetylcholine in control of USWS, additional neurotransmitters are being researched to understand their roles in the asymmetric sleep model. [1]

References[edit]

  1. ^ a b c d Lapierre, Jennifer L.; Kosenko, Peter O.; Lyamin, Oleg I.; Kodama, Tohru; Mukhametov, Lev M.; Siegel, Jerome M. (2007). "Cortical Acetylcholine Release Is Lateralized during Asymmetrical Slow-Wave Sleep in Northern Fur Seals". The Journal of Neuroscience. 27 (44): 11999–12006. doi:10.1523/JNEUROSCI.2968-07.2007. PMID 17978041.
  2. ^ a b Rattenborg, Niels C.; Lima, Steven L.; Amlaner, Charles J. (1999). "Half-awake to the risk of predation". Nature. 397: 397–398. doi:10.1038/17037.
  3. ^ a b c Rattenborg, N.C.; Amlaner, C.J.; Lima, S.L. (2000). "Behavioral, Evolutionary Perspectives on Unihemispheric Slow-Wave Sleep". Neuroscience and Biobehavioral Reviews. 24: 817–842. {{cite journal}}: Cite has empty unknown parameter: |1= (help)
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  6. ^ a b c d Sekiguchi, Yuske; et al. (2003). "Resting behaviors of captive bottlenose dolphins (Tursiops truncatus)". Physiology & Behavior. 79: 643–653. {{cite journal}}: Cite has empty unknown parameter: |1= (help); Explicit use of et al. in: |last2= (help)
  7. ^ a b c d e O. V., Shpak; et al. (2009). "States of Rest and Activity in the Commerson's Dolphin 'Cephalorhynchus commersonii'". Journal of Evolutionary Biochemistry and Physiology. 45: 111–119. {{cite journal}}: Cite has empty unknown parameter: |1= (help); Explicit use of et al. in: |last2= (help)
  8. ^ a b c d e f Rattenborg, Niels C. (2006). "Do birds sleep in flight?". Naturwissenschaften. 93: 413–425. {{cite journal}}: Cite has empty unknown parameter: |1= (help)
  9. ^ a b c d e f Revell, Timothy K.; Hayes, William K. (2009). "Desert Iguanas (Dipsosaurus dorsalis) Sleep Less When in Close Proximity to a Rattlesnake Predator (Crotalus cerastes)". Journal of Herpetology. 43: 29–37. {{cite journal}}: Cite has empty unknown parameter: |1= (help)
  10. ^ a b c Mathews, Christian G.; Lesku, John A.; Lima, Steven L. (2006). "Asynchronous Eye Closure as an Anti-Predator Behavior in the Western Fence Lizard (Sceloporus occidentalis)". Ethology. 112: 286–292. {{cite journal}}: Cite has empty unknown parameter: |1= (help)
  11. ^ a b Lyamin, O.I.; Mukhametov, L.M.; Siegel, J.M. last4=Nazarenko; Polyakova, I.G.; Shpak, O.V. (2002). "Unihemispheric slow wave sleep and the state of the eyes in a white whale". Behavior Brain Research. 129 (1–2): 125–129. doi:10.1016/S0166-4328(01)00346-1. PMID 11809503. {{cite journal}}: |first4= missing |last4= (help); Missing pipe in: |first3= (help)CS1 maint: numeric names: authors list (link) Cite error: The named reference "White Whale" was defined multiple times with different content (see the help page).
  12. ^ a b Javurkova, Veronika; Horkat, David; Kreisinger, Jakub (2011). "Factors Affecting Sleep/vigilance Behaviour in Incubating Mallards". Ethology. 117: 345–355. {{cite journal}}: Cite has empty unknown parameter: |1= (help)
  13. ^ Walter, Timothy J.; Marar, Uma (2007). "Sleeping With One Eye Open" (PDF). Capitol Sleep Medicine Newsletter. pp. 3621–3628.
  14. ^ Bobbo, Daniela; Vallortigara, Giorgio (2006). "Effects of social interaction on monocular/unihemispheric sleep in male and female domestic chicks". Biological Psychology. 73: 213–219. {{cite journal}}: Cite has empty unknown parameter: |1= (help)
  15. ^ Bobbo, Daniela; Vallortigara, Giorgio; Mascetti, Gian Gastone (2006). "The effects of early post-hatching changes of imprinting object on the pattern of monocular/unihemispheric sleep of domestic chicks". Behavioural Brain Research. 170: 23–28. {{cite journal}}: Cite has empty unknown parameter: |1= (help)
  16. ^ Mascetti, Gian Gastone; Vallortigara, Giorgio; Bobbo, Daniela (2007). "Monocular-unihemispheric sleep and visual discrimination learning in the domestic chick". Experimental Brain Research. 176: 70–84. {{cite journal}}: Cite has empty unknown parameter: |1= (help)
  17. ^ Nelini, Cristian; Bobbo, Daniela; Mascetti, Gian G. (2010). "Local sleep: a spatial learning task enhances sleep in the right hemisphere of domestic chicks (Gallus gallus)". Experimental Brain Research. 205: 195–204. {{cite journal}}: Cite has empty unknown parameter: |1= (help)
  18. ^ Ridgway, Sam; Carder, Don; Finneran, James; Keogh, Mandy; Kamolnick, Tricia; Todd, Mark; Goldblatt, Allen (2006). "Dolphin Continuous Auditory Vigilance for Five Days". The Journal of Experimental Biology. 209 (18): 3621–3628. doi:10.1242/jeb.02405. PMID 16943502.
  19. ^ GOLEY, PATRICIA (1999). "BEHAVIORAL ASPECTS OF SLEEP IN PACIFIC WHITE-SIDED DOLPHINS (LAGENORHYNCHUS OBLIQUIDENS, GILL 1865)". MARINE MAMMAL SCIENCE. 15: 1054–1064. {{cite journal}}: Cite has empty unknown parameters: |1= and |2= (help)
  20. ^ Lyamin, O.I.; et al. (2003). "Unihemispheric slow wave sleep and the state of the eyes in a white whale". Behavioural Brain Research. 129: 125–129. {{cite journal}}: Cite has empty unknown parameters: |1= and |2= (help); Explicit use of et al. in: |last2= (help)
  21. ^ McGinty, Dennis; Szymusiak, Ronald (1990). "Keeping cool: a hypothesis about the mechanisms and functions of slow-wave sleep". Trends in Neuroscience. 13 (12): 480–487. doi:10.1016/0166-2236(90)90081-K.
  22. ^ Ridgway, Sam; et al. (2006). "Functional imaging of dolphin brain metabolism and blood flow". The Journal of Experimental Biology. 209: 2902–2910. {{cite journal}}: Cite has empty unknown parameter: |1= (help); Explicit use of et al. in: |last2= (help)
  23. ^ PILLAY, PRANESHRI; MANGER, PAUL R . (2004). "Testing thermogenesis as the basis for the evolution of cetacean sleep phenomenology". Journal of Sleep Research. 13: 353–358. {{cite journal}}: Cite has empty unknown parameter: |1= (help)
  24. ^ Steinmeyer, Corinna; Schielzeth, Holger; Mueller, Jakob C. (2010). "Variation in sleep behaviour in free-living blue tits, Cyanistes caeruleus: effects of sex, age and environment". Animal Behaviour. 80: 853–864. {{cite journal}}: Cite has empty unknown parameter: |1= (help)
  25. ^ Mascetti, Gian G.; Rugger, Marina; Vallortigara, Giorgio; Bobbo, Daniela (2006). "Monocular-unihemispheric sleep and visual discrimination learning in the domestic chick". Experimental Brain Research. 176 (1): 70–84. doi:10.1007/s00221-006-0595-3.
  26. ^ a b Phillips, Andrew J. K.; Robinson, Peter A.; Kedziora, David J. (2010). "Mammalian Sleep Dynamics: How Diverse Features Arise from a Common Physiological Framework". PLoS Computational Biology. 6: 1–9. {{cite journal}}: Cite has empty unknown parameter: |1= (help)


Category:Sleep physiology Category:Unsolved problems in neuroscience Category:Vision

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