One of the most striking features of living organisms, both animals and plants, is the way their physiology and behavior have adapted to follow the fluctuations of daily light and nocturnal darkness. A clock in the brain synchronized to environmental cues generates biological changes that vary over a 24-hour cycle—circadian rhythms (from the Latin words circa and diem, meaning “about” and “a day,” respectively). In this way, the earth’s rotation is reproduced in the dynamics of our neuronal circuits.
The sleep-wakefulness cycle is a typical circadian rhythm. Wakefulness is characterized by sensory activity and movement; during sleep the senses lose touch with their surroundings, and movements subside. This periodic loss of consciousness appears on electroencephalogram (EEG) recordings as a clear signature: deep sleep consists of slow oscillations of high amplitude. Wakefulness, in contrast, is made up of fast, low-amplitude oscillations. Much about sleep remains a mystery, however. Why would an animal shut down basic sensory and motor activity for hours on end, leaving itself a target for predators? This question becomes more acute in aquatic mammals, which need to regulate breathing and body temperature while they sleep.
Remarkably, some animals have solved this problem by developing the ability to sleep with one half their brain while remaining vigilant with the other—a behavior known as unihemispheric slow-wave sleep (USWS). Still others engage in USWS under some circumstances but put both hemispheres to bed when necessary. Marine mammals, bird species and possibly reptiles enter a half-on/half-off state, sometimes keeping one eye open during these intervals. Recently researchers have even discovered a vestigial form of unihemispheric sleep in humans.
Half-slumber provides a fascinating vista into the science of sleep. While studies are carried out on the dormant half, the opposite side can serve as the requisite control for experiments. The ability to thrive with a relative lack of sleep, as dolphins and some birds do, may provide ideas for treating human sleep disorders, which often affect one brain hemisphere more than the other.
Asleep but not Really
The study of unihemispheric sleep started in 1964, when controversial researcher John C. Lilly suggested that dolphins could sleep using one side of the brain after observing that the animals keep only one eye closed during their daily rest. Lilly assumed that when asleep, dolphins could still watch and listen to their surroundings. It would take later experiments to determine what was happening in cetacean brains.
Cetaceans—whales, dolphins and porpoises—are still the subjects of studies on unihemispheric sleep. The animals preserve two physiological features from their ancestors’ life on land: lungs for breathing air and mechanisms for maintaining nearly constant body temperature in water (thermoregulation). Sleeping with half a brain, it seems, has allowed them to retain those features in an aquatic environment.
More recently, Lev Mukhametov of the A. N. Severtsov Institute of Ecology and Evolution at the Russian Academy of Sciences and his colleagues looked more deeply than Lilly did into what was happening in the cetacean brain. Mukhametov and his colleagues studied sleep extensively in bottlenose dolphins. In EEG recordings, the researchers consistently found that one hemisphere of the animals’ brain was in a state of slow-wave sleep, while the other was awake. They rarely observed sleep in both hemispheres (which is called bihemispheric slow-wave sleep, or BSWS), and they recorded no unequivocal signs of the rapid eye movement (REM) sleep associated with dreaming.
During USWS the awake hemisphere of a dolphin’s brain controls swimming and surfacing to breathe. As Lilly surmised from cursory observation, the animal’s one open eye, linked to the contralateral awake hemisphere of the brain, allows a dolphin to monitor for predators and swim in unison with its companions while the other half of the brain rests. In 1999 P. Dawn Goley of the department of biological sciences at Humboldt State University observed—as did Guido Gnone of the Aquarium of Genoa in Italy and his colleagues in 2001—that when dolphins swam in groups, the open eye of a pod member maintained visual contact with others. If a partner shifted to the opposite side, the eye pattern reversed.
Dolphins also confront cold water temperatures that expose them to high heat loss. Keeping one hemisphere of the brain awake during rest allows the animals to stay warm by frequently moving their flippers and tail to swim and hover near the surface while they sleep—observations reported by Praneshri Pillay and Paul R. Manger, both then at the University of the Witwatersrand, Johannesburg.
We know that in cetaceans and other animals, the overall sleep-wake cycle is governed by interactions among multiple brain structures, including the brain stem, the hypothalamus and the basal forebrain. Precisely what regulates unihemispheric sleep remains a mystery, although we have clues. In 2012 David J. Kedziora and his colleagues at the University of Sydney worked out a mathematical model of USWS intended to represent dolphin sleep habits. In it, substructures within the hypothalamus in each hemisphere—the ventrolateral preoptic nuclei—exchange messages to regulate when sleep occurs in each hemisphere. It appears that inhibitory signals transmitted between the two hemispheres could allow one side to go to sleep while the other stays awake. Deep-brain structures, such as the posterior commissures in the brain stem, would also be involved. (The posterior commissures are extremely large in dolphins, giving rise to questions about their role in managing sleep.) The University of Sydney model gives neuroscientists a way to explore the mechanisms of how the brain hands off the delicate task of allocating sleep to one hemisphere or another.
Environmental cues also seem to play a role. Because the sleep-promoting neurons in the hypothalamus are thermosensitive, a rise or fall in brain temperature causes a corresponding fluctuation in the firing rate of these neurons. Indeed, in 1982 Mukhametov and his colleagues found that during USWS dolphins’ brain temperatures decreased in the sleeping hemisphere and remained constant in the awake one.
A Singular Adaptation
Cetaceans evolved from a common terrestrial ancestor with hippopotamuses and other hoofed mammals. The move from a terrestrial to an aquatic environment was gradual and may have included a semiaquatic transition that entailed significant physiological and behavioral adjustments. Consequently, cetaceans’ sleep behavior represents a singular example of adaptation to a new environment that demonstrates a trade-off between the need for sleep and survival.
Other animals make similar compromises. Seals, for example, have adopted various evolutionary solutions to the closely related problem of breathing and sleeping in water and on land. Some families of seals eschew USWS altogether. It has not turned up in earless, or “true,” seals (the family Phocidae), including harp and elephant seals.
Northern fur seals (the family Otariidae), however, demonstrate a different story. In 2017 Oleg I. Lyamin of the A. N. Severtsov Institute of Ecology and Evolution reported that unlike dolphins, which appear to rarely experience BSWS and perhaps never enter REM sleep at all, northern fur seals undergo multiple sleep types, including BSWS, REM and USWS, in both their aquatic and terrestrial lairs. On land, BSWS predominates. In water, the amount of time spent in USWS increases, compared with that on land. REM sleep in water diminishes or even disappears.
When immersed in water and experiencing USWS, fur seals adopt a body posture that allows them to sleep, breathe and track approaching predators: they lie on one side with one flipper in the water and paddle continuously with it while keeping their other three flippers in the air to reduce heat loss. Their nostrils, meanwhile, remain out of the water so the seals can breathe. The brain hemisphere on the opposite side from the moving flipper (and the one open eye) is awake, letting the animals issue motor commands for paddling and retaining postural stability. On land, USWS allows fur seals to watch for predators and coordinate activity with companions, but it does not help with breath control, body temperature or coordination of movement.
Some birds, too, engage in unihemispheric sleep as they balance the need for rest and defensive alertness. (At times, USWS is combined with BSWS and REM.) In 1996 Jadwiga Szymczak, then at Nicolaus Copernicus University in Poland, recorded the presence of slow-wave EEGs in one hemisphere of the European black bird. And in 2001 Niels C. Rattenborg, then at the department of life sciences at Indiana State University, and his colleagues did the same in pigeons. Similarly, in 1999 Rattenborg had found that mallard ducks sleep with only half a brain to watch for threats. Ducks that kept one eye open while stationed at the outside edges of a group showed 150 percent higher levels of USWS than birds located toward the center. The open eyes of the “sentinel” ducks were directed away from the group. Mark A. Elgar, now at the University of Melbourne in Australia, reported in a 1989 study that vigilance decreases when the group grows larger and when an animal moves toward the center of the group.
Migrating birds during nonstop, long-distance flights also rely on differing sleep strategies. In 2016 Rattenborg, now at the Max Planck Institute for Ornithology in Seewiesen, Germany, and his team studied USWS and BSWS in great frigate birds (Fregata minor) during their 10-day sojourns. In a single USWS episode, one hemisphere showed a waking EEG pattern contralateral to the direction of a flight turn, indicating that the open eye on the opposite side was watching where the flock was headed. Also, Thomas Fuchs, then at Bowling Green State University, discovered in 2006 that Swainson’s thrush compensates for the loss of sleep during night flight by increasing total sleep time, taking daytime micro naps and, when perching, closing one eye.
What about US?
Humans do not engage in classic USWS, but they occasionally experience something reminiscent of it. Masako Tamaki and her group at Brown University made EEG recordings when people spent the night in an unfamiliar environment. In a 2016 publication by Tamaki, the EEGs showed slow waves indicative of deep sleep in the right hemisphere and shallow slow-wave activity in the left hemisphere, a sign of more alertness. The left hemisphere, moreover, was more easily aroused than its opposite half. This asymmetry, referred to as the first-night effect, disappears by the second night but seems to preserve vigilance in an unfamiliar place. It is reminiscent of mothers who retain a low awakening threshold to cries or other noises they identify as coming from their babies.
We may feel the sleep debt after the first night away from home. But other animals that sleep with one side of the brain all the time seem to be well adapted to their routines. Those that immerse themselves in USWS spend less time sleeping, compared with those that engage in BSWS or REM sleep.
Even so, their ability to swim, fly, eat or socialize with companions remains undiminished. Dolphins spend almost two thirds of their day awake and the rest of the time in USWS, trading off sleep time between the two hemispheres. Brain and body recovery, however, does not appear to be affected, despite the absence of REM sleep.
In 1997 Mukhametov and his colleagues reported that dolphins in sleep studies always appeared to be in good health. In captivity, where scientists could observe the animals closely, dolphins learned and memorized complex tasks. Frigate birds sharply reduced total sleep while flying but maintained a high level of attention and efficient flight performance during their extended journeys.
Some animals seem to cope by sharing the half-sleep burden. Mallard ducks that act as flock sentinels by keeping one eye open lose sleep but without impaired behavior. The birds later pass off their lookout roles to a companion on another day. Unihemispheric sleep continues to fascinate the research community because it illustrates the diverse evolutionary strategies that have emerged to allow animals to get their rest every day.
The interest generated in USWS from field experiments has even made it into a laboratory tool for exploring the role of sleep in helping to shape development of the brain just after birth. In 1999 my group in the department of general psychology at the University of Padova in Italy found that just-born chickens (Gallus gallus) experienced significantly more left-hemisphere sleep during the first week after hatching. The chicks favored that hemisphere in those early days to learn about stimuli—patterns and colors—that must be processed for the first time by their new brain: sleep appeared to play a role in organizing what they had just learned.
Right-hemisphere sleep increased in the chicks as activity such as spatial analysis and the processing of new events prevailed on that side in the second week. When we trained chicks in a color-discrimination task, they subsequently registered more left USWS (with their right eye closed and their left hemisphere asleep) because that hemisphere was dominant in learning about colors. Chicks used the left eye for a spatial-learning task that required them to select one of four containers in a particular corner of their enclosure. They had to pick the container with a hole on top that contained a food treat. When they were done, chicks showed more right USWS (with their left eye closed and their right hemisphere sleeping) to rest the side of the brain that specializes in this type of task.
The most active hemisphere—whether engaged in USWS or BSWS—spent relatively more time sleeping to allow for recovery. Meanwhile the open eye on the side of the nondominant hemisphere took over to watch for predators and to stay apprised of the environment. In fact, moving a dark object over the cage during USWS caused chicks to wake immediately, startle and emit distress calls. Vigilance remained intact, but it did not detract from sleep as a time to sort out the intense sensory experiences of the birds’ first days in a new world.
Ultimately studying animals that sleep with half a brain could aid us in understanding the continuing biological enigma of sleep—and perhaps even sleep problems in humans. Apnea and other disorders sometimes have effects more in one hemisphere than the other. This work may help answer how a species balances the benefits of rest with a need to protect itself against a hungry predator. Sleeping with one side of the brain is a brilliant answer to this dilemma, enabling an animal to experience conscious and unconscious states all at once. Research on unihemispheric sleep resonates through the millennia with a frequently quoted passage from Heraclitus’ Fragments:“Even a soul submerged in sleep is hard at work and helps make something of the world.”