Unihemispheric slow-wave sleep
Encyclopedia
Unihemispheric slow-wave sleep (USWS), also termed asymmetric slow-wave sleep (ASWS), is characterized by slow-wave activity in one hemisphere of the brain while a low voltage EEG, characteristic of wakefulness, is present in the other. The phenomenon has been observed in a number of terrestrial and aquatic as well as avian species. Unique physiology, including differential release of the neurotransmitter acetylcholine has been linked to the phenomenon. USWS offers a number of benefits, including the ability to rest in areas of high predation or during long migratory flights. The behavior remains an important research topic because USWS is possibly the first animal behavior which uses different regions of the brain to simultaneously control sleep and wakefulness.
) when in safe conditions, but will increase the usage of USWS if the environment has a potential to become dangerous. It is more beneficial to sleep using both hemispheres; however, the positives of unihemispheric slow-wave sleep prevail over its negatives under extreme conditions. While in unihemispheric slow-wave sleep, birds will sleep with one open eye towards the direction from which predators are more likely to approach. When birds do this in a flock, this is called the "group edge effect".
The "group edge effect" describes the phenomenon in which birds positioned 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 for both their own safety and the safety of the flock as a whole. These birds will spend more time in unihemispheric slow-wave sleep than the birds towards the center. Since USWS allows for the one eye to still be open, the cerebral hemisphere that undergoes slow-wave sleep varies depending on the position of the bird relative to the rest of the flock. If the bird's left side is facing outward, the left hemisphere will be in slow-wave sleep; if the bird's right side is facing outward, the right hemisphere will be in slow-wave sleep. This is because the eyes are contra-lateral to the left and right hemispheres of the cerebral cortex
. The open eye of the bird is always directed towards the outside of the group, in the direction predators could potentially attack from.
(EEG) readings. This is also known as desynchronized state of the brain, or deep sleep. In USWS, only one hemisphere exhibits the deep sleep EEG while the other hemisphere exhibits an EEG typical of wakefulness with a low amplitude and high frequency. There also exist instances in which hemispheres are in transitional stages of sleep, but they have not been the subject of study due to their ambiguous nature. USWS represents the first known behavior in which one part of the brain controls sleep while another part controls wakefulness.
has been linked to hemispheric activation in northern fur seals. Acetylcholine is released in nearly the same amounts per hemisphere in bilateral slow-wave sleep. However, in USWS, the maximal release of the cortical acetylcholine neurotransmitter is lateralized to 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.
has been demonstrated in dolphins and is believed to be conserved among species exhibiting USWS.
is the anatomical structure in the mammalian brain which allows for interhemispheric communication. 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 transsections of the corpus callosum have been found to result in strictly bihemispheric sleep. As a result it seems this anatomical difference, though well correlated, does not directly explain the existence of USWS.
and increased decussation
of ascending fibers from the locus coeruleus in the brainstem. 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.
in birds has also stimulated research. Complete decussation of the optic tract has been seen as a method of ensuring the open eye strictly activates the ipsilateral hemisphere. Some evidence indicates that this alone is not enough as blindness would theoretically prevent USWS if retinal nerve stimuli was the sole player. However, USWS was still exhibited in blinded birds despite the absence of visual input.
, 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. Free-flying birds might be able to spend some time sleeping while in non-migratory flight as well when in unobstructed sky as opposed to in controlled captive conditions. 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 but for relatively short periods of time. Coupled with simulated windtunnels in a controlled setting, these new methods of measuring brain activity could elucidate the truth behind whether or not birds sleep during flight.
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.
Cetaceans
- Of all the cetacean species, USWS has been found to be exhibited in the following four species:
- Bottlenose dolphinBottlenose DolphinBottlenose dolphins, the genus Tursiops, are the most common and well-known members of the family Delphinidae, the family of oceanic dolphins. Recent molecular studies show the genus contains two species, the common bottlenose dolphin and the Indo-Pacific bottlenose dolphin , instead of one...
(tursiops truncates) - PorpoisePorpoisePorpoises are small cetaceans of the family Phocoenidae; they are related to whales and dolphins. They are distinct from dolphins, although the word "porpoise" has been used to refer to any small dolphin, especially by sailors and fishermen...
(phocoena phocoena) - Amazon river dolphin (inia geoffrensis)
- Pilot whalePilot whalePilot whales are cetaceans belonging to the genus Globicephala. There are two extant species, the long-finned pilot whale and the short-finned pilot whale . The two are not readily distinguished at sea and analysis of the skulls is the best way to tell the difference between them...
(globicephala scammoni) - Beluga whale (delphinapterus leucus)
- Bottlenose dolphin
Pinnipeds
- A major difference between the 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. Though no USWS has been observed in true seals, four different species eared seals have been found to exhibit USWS including:
- Northern fur sealNorthern Fur SealThe Northern fur seal is an eared seal found along the north Pacific Ocean, the Bering Sea and the Sea of Okhotsk. It is the largest member of the fur seal subfamily and the only species in the genus Callorhinus.-Physical description:Northern fur seals have extreme sexual dimorphism, with males...
(Callorhinus ursinus)
-
- 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 present bilaterally; however, when sleep takes place in water, 68% of all SWS is found with interhemispheric EEG asymmetry, indicating USWS.
- Steller sea lion (Eumetopias jubatus)
- Southern sea lion (Otari bryonia)
Sirenia
- The final order of aquatic mammals, sireniaSireniaSirenia is an order of fully aquatic, herbivorous mammals that inhabit swamps, rivers, estuaries, marine wetlands, and coastal marine waters. Four species are living, in two families and genera. These are the dugong and manatees...
, include three species of manatees. Experiments have only exhibited USWS in the Amazonian manateeAmazonian ManateeThe Amazonian Manatee is a species of manatee that lives in the freshwater habitats of the Amazon basin. They are found in Brazil, Peru, Colombia, Ecuador, Guyana and Venezuela. Amazonian manatees are aquatic animals of the Sirenia order and are also known as "seacows". Their colour is grey but...
(trichechus inunguis).
Birds
- The common swiftCommon SwiftThe Common Swift is a small bird, superficially similar to the Barn Swallow or House Martin. It is, however, completely unrelated to those passerine species, since swifts are in the separate order Apodiformes...
(apus apus) was the best candidate for research aimed at determining whether or not birds exhibiting USWS can sleep in flight. The selection of the common swift as a model stemmed from observations elucidating the fact that the common swift left its nest at night, only returning in the early morning. Still, evidence for USWS is strictly circumstantial and based on the notion that if swifts must sleep to survive, they must do so via aerial roosting as little other time is spent sleeping in a nest.
- Multiple other species of birds have also been found to exhibit USWS including:
- White-crowned sparrowWhite-crowned SparrowThe White-crowned Sparrow is a medium-sized sparrow native to North America.- Description :Adults are long and have black and white stripes on their head, a grey face, brown streaked upper parts and a long tail. The wings are brown with bars and the underparts are grey. Their bill is pink or yellow...
(zonotrichia leucophrys gambelii) - MallardMallardThe Mallard , or Wild Duck , is a dabbling duck which breeds throughout the temperate and subtropical Americas, Europe, Asia, and North Africa, and has been introduced to New Zealand and Australia....
(Anas platyrhynchos). - Domestic chicken (Gallus gallus domesticus),
- Northern bobwhite (Colinus virginianus),
- Japanese quailJapanese QuailThe Japanese Quail, also known as Coturnix Quail, Coturnix japonica, is a species of Old World Quail found in East Asia. They are a migratory species, breeding in Manchuria, southeastern Siberia, northern Japan, and the Korean Peninsula, and wintering in the south of Japan and southern China. They...
(Coturnix japonica) - Glaucous-winged GullGlaucous-winged GullThe Glaucous-winged Gull, Larus glaucescens, is a large, white-headed gull residing from the western coast of Alaska to the coast of Washington. It also breeds on the northwest coast of Alaska. During non-breeding seasons they can be found along the coast of California...
(Larus glaucescens) - Orange-fronted parakeetOrange-fronted ParakeetThe Orange-fronted Parakeet or Orange-fronted Conure , also known as the Half-moon Conure, is a medium-sized parrot which is a resident from western Mexico to Costa Rica.-Taxonomy:There are three subspecies:...
(Aratinga canicularis) - Common Blackbird (Turdus merula)
- White-crowned sparrow
Benefits
Many species of birds and marine mammals have advantages due to the capability to undergo unihemispheric slow-wave sleep including, but not limited to an increased chance of the evasion of potential predators and ability to sleep during migration. Unihemispheric sleep aids in the visual vigilance of the environment, the preservation of movement, and in cetaceans, the controlling of the respiratory system.Adaptation to high-risk predation
Most species of birds are able to detect approaching predators during unihemispheric slow-wave sleep. During flight, birds maintain visual vigilance while sleeping using USWS by keeping one eye open. The utilization of unihemispheric slow-wave sleep by avian species is directly proportional to the risk of predation. In other words, the usage of USWS of certain species of birds increases as the risk of predation increases.Survival of the fittest adaptation
The evolution of both cetaceans and birds may have involved some mechanisms in order to help increase the chance of avoiding predators. Certain species, especially species of birds, that acquired the ability to perform unihemispheric slow-wave sleep had an advantage and were more likely to escape their potential predators over certain species that lacked the ability.Regulation based on surroundings
Birds can sleep more efficiently by sleeping with both hemispheres simultaneously (bi-hemispheric slow wave sleepSlow-wave sleep
Slow-wave sleep , often referred to as deep sleep, consists of stages 3 and 4 of non-rapid eye movement sleep, according to the Rechtschaffen & Kales standard of 1968. As of 2008, the American Academy of Sleep Medicine has discontinued the use of stage 4, such that the previous stages 3 and 4 now...
) when in safe conditions, but will increase the usage of USWS if the environment has a potential to become dangerous. It is more beneficial to sleep using both hemispheres; however, the positives of unihemispheric slow-wave sleep prevail over its negatives under extreme conditions. While in unihemispheric slow-wave sleep, birds will sleep with one open eye towards the direction from which predators are more likely to approach. When birds do this in a flock, this is called the "group edge effect".
The "group edge effect" describes the phenomenon in which birds positioned 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 for both their own safety and the safety of the flock as a whole. These birds will spend more time in unihemispheric slow-wave sleep than the birds towards the center. Since USWS allows for the one eye to still be open, the cerebral hemisphere that undergoes slow-wave sleep varies depending on the position of the bird relative to the rest of the flock. If the bird's left side is facing outward, the left hemisphere will be in slow-wave sleep; if the bird's right side is facing outward, the right hemisphere will be in slow-wave sleep. This is because the eyes are contra-lateral to the left and right hemispheres of the cerebral cortex
Cerebral cortex
The cerebral cortex is a sheet of neural tissue that is outermost to the cerebrum of the mammalian brain. It plays a key role in memory, attention, perceptual awareness, thought, language, and consciousness. It is constituted of up to six horizontal layers, each of which has a different...
. The open eye of the bird is always directed towards the outside of the group, in the direction predators could potentially attack from.
Surfacing for air while sleeping in marine mammals
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 over the course of five days.Ability to rest during long flights
When migrating, birds may undergo unihemispheric slow-wave sleep in order to simultaneously sleep while visually navigating flight.Physiology
In most animals, slow-wave sleep (SWS) is characterized by high amplitude, low frequency electroencephalographyElectroencephalography
Electroencephalography is the recording of electrical activity along the scalp. EEG measures voltage fluctuations resulting from ionic current flows within the neurons of the brain...
(EEG) readings. This is also known as desynchronized state of the brain, or deep sleep. In USWS, only one hemisphere exhibits the deep sleep EEG while the other hemisphere exhibits an EEG typical of wakefulness with a low amplitude and high frequency. There also exist instances in which hemispheres are in transitional stages of sleep, but they have not been the subject of study due to their ambiguous nature. USWS represents the first known behavior in which one part of the brain controls sleep while another part controls wakefulness.
Role of acetylcholine
Due to the origin of USWS in the brain, neurotransmitters are believed to be involved in its regulation. The neurotransmitter acetylcholineAcetylcholine
The chemical compound acetylcholine is a neurotransmitter in both the peripheral nervous system and central nervous system in many organisms including humans...
has been linked to hemispheric activation in northern fur seals. Acetylcholine is released in nearly the same amounts per hemisphere in bilateral slow-wave sleep. However, in USWS, the maximal release of the cortical acetylcholine neurotransmitter is lateralized to 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.
Eye opening
In domestic chicks and other species of birds exhibiting USWS, one eye remained open contra-lateral to the "awake" hemisphere. The closed eye was shown to be contra-lateral to the hemisphere engaging in slow-wave sleep. Learning tasks, such as those including predator recognition, demonstrated the open eye could be preferential. This has also been shown to be the favored behavior of white whale, although inconsistencies have arisen directly relating the sleeping hemisphere and open eye. Keeping one eye open aids birds in engaging in USWS while mid-flight as well helping them observe predators in their vicinity.Thermoregulation
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. The thermoregulationThermoregulation
Thermoregulation is the ability of an organism to keep its body temperature within certain boundaries, even when the surrounding temperature is very different...
has been demonstrated in dolphins and is believed to be conserved among species exhibiting USWS.
Smaller corpus callosum
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 callosumCorpus callosum
The corpus callosum , also known as the colossal commissure, is a wide, flat bundle of neural fibers beneath the cortex in the eutherian brain at the longitudinal fissure. It connects the left and right cerebral hemispheres and facilitates interhemispheric communication...
is the anatomical structure in the mammalian brain which allows for interhemispheric communication. 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 transsections of the corpus callosum have been found to result in strictly bihemispheric sleep. As a result it seems this anatomical difference, though well correlated, does not directly explain the existence of USWS.
Noradrenergic diffuse modulatory system variations
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 asynchronous SWS in non-USWS-exhibiting animals as a result of sagital transsections of subcortical regions, including the lower brain stem, while leaving the corpus callosum intact. Other comparisons found that mammals exhibiting USWS have a larger posterior commissureCommissure
A commissure is the place where two things are joined. The term is used especially in the fields of anatomy and biology.In anatomy, commissure refers to a bundle of nerve fibers that cross the midline at their level of origin or entry .* The most common usage of the term refers to the brain's...
and increased decussation
Decussation
Decussation is used in biological contexts to describe a crossing.Examples include:* In the brain, where nerve fibers obliquely cross from one lateral part to the other, that is to say they cross at a level other than their origin...
of ascending fibers from the locus coeruleus in the brainstem. This is consistent with the fact that one form for neuromodulation
Neuromodulation
In Neuromodulation several classes of neurotransmitters regulate diverse populations of central nervous system neurons...
, the noradrenergic diffuse modulatory system present in the locus coeruleus, is involved in regulating arousal, attention, and sleep-wake cycles.
Complete crossing of the optic nerve
Complete crossing of the nerves at the optic chiasmOptic chiasm
The optic chiasm or optic chiasma is the part of the brain where the optic nerves partially cross...
in birds has also stimulated research. Complete decussation of the optic tract has been seen as a method of ensuring the open eye strictly activates the ipsilateral hemisphere. Some evidence indicates that this alone is not enough as blindness would theoretically prevent USWS if retinal nerve stimuli was the sole player. However, USWS was still exhibited in blinded birds despite the absence of visual input.
Future research
Recent studies have illustrated that the white-crowned sparrowWhite-crowned Sparrow
The White-crowned Sparrow is a medium-sized sparrow native to North America.- Description :Adults are long and have black and white stripes on their head, a grey face, brown streaked upper parts and a long tail. The wings are brown with bars and the underparts are grey. Their bill is pink or yellow...
, 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. Free-flying birds might be able to spend some time sleeping while in non-migratory flight as well when in unobstructed sky as opposed to in controlled captive conditions. 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
EEG
EEG commonly refers to electroencephalography, a measurement of the electrical activity of the brain.EEG may also refer to:* Emperor Entertainment Group, a Hong Kong-based entertainment company...
of each hemisphere but for relatively short periods of time. Coupled with simulated windtunnels in a controlled setting, these new methods of measuring brain activity could elucidate the truth behind whether or not birds sleep during flight.
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.