Portal de Periódicos da CAPES

Niels C. Rattenborg

2018; Elsevier BV; Volume: 28; Issue: 24 Linguagem: Inglês

10.1016/j.cub.2018.10.029

1879-0445

Niels C. Rattenborg,

Sleep and Wakefulness Research

Niels Rattenborg received his Bachelor of Arts in Psychology from Washington University (St. Louis) in 1986. After a stint in the healthcare industry, he obtained his PhD from the Department of Life Sciences at Indiana State University (Terre Haute) in 1999 and then completed a postdoc in the Department of Psychiatry at the University of Wisconsin (Madison) in 2005. In the same year, Rattenborg moved with his family to the Max Planck Institute for Ornithology (MPIO) in Seewiesen to establish an independent research group focused on avian sleep. In 2017, he received the Outstanding Scientific Achievement Award from the Sleep Research Society for demonstrating that birds can sleep in flight. Rattenborg aims to gain insight into the evolution and functions of sleep through the study of birds. How did you become a sleep scientist? My father was a professor of Anesthesiology at the University of Chicago, but I did not intentionally get involved in sleep research to follow in his footsteps. After completing high school, he helped me to get a summer job in the Department of Neurology with neurologist Jean-Paul Spire. There, I learned to run electroencephalogram (EEG) diagnostic tests on patients with various neurological disorders. As they often fell asleep during these tests, I was also introduced to the fascinating changes in brain activity that occur when we drift off to sleep. As sleep medicine was an emerging field that relied on similar technology, I started to run sleep studies during summer breaks from college. After graduating, I accepted a full-time position as a technician in a sleep clinic in St. Louis with Kristyna Hartse. Ironically, Kristyna had investigated the evolution of sleep through the study of reptiles during her PhD at the University of Chicago and later switched from academia to the growing field of sleep medicine. During the endless night shifts spent monitoring snoring patients and desperately trying to stay awake, I became increasingly interested in the basic neurobiology and physiology behind those squiggly lines that inked across the paper being spat out by the two-meter-tall polysomnograph. Digging through text books shortened the night for me and also revealed how little was known about sleep. Unfortunately, after moving to another clinic, I was promoted to lab manager. Although this was a well-paid and important job that contributed to helping people sleep better, the management aspects of the position pulled me away from exploring the basic science of sleep. Finally, 10 years after completing college, I decided to leave the healthcare industry to start a PhD. As I had an interest in birds and evolution dating back to grade school and high school, respectively, I decided to investigate the evolution of sleep through the study of birds. Twenty-plus years later, snoring has been replaced by the sounds of seabirds on an island in the Galápagos, and polysomnographs are small enough for frigatebirds to wear them as hats while flying non-stop over the Pacific Ocean for weeks at a time. Despite having traveled far from the sleep clinic, I strongly believe that determining if and how birds sleep when faced with ecological demands that require sustained wakefulness can influence our understanding of human sleep. My time spent working in sleep clinics certainly broadened my perspectives on sleep in ways that continue to influence my research. However, a 10-year gap in an academic record would normally cause search committees to question a candidate’s commitment. Luck with experiments that actually worked and inspired editors at influential journals certainly enabled me to bridge this gap. Although things could have easily gone south academically, attempting to migrate from industry to academia at this ‘late’ stage was not as risky for me as it might seem. Unlike students who follow the unwavering path straight to graduate school, I had an obvious safety net; if being an academic did not work out, I could always return to work in a sleep clinic. Indeed, as my postdoc was ending, I was very close to accepting an offer to resume work with James Walsh in the clinic I had left years earlier. Then, out of the blue, I received an email from the Max Planck Institute offering me a dream job. What’s your favorite experiment? The first experiment from my dissertation is my favorite. It was known that, in addition to sleeping in the conventional way with both eyes closed and both cerebral hemispheres asleep, birds sometimes sleep with one eye open and the opposite hemisphere awake. However, it was unknown whether birds could switch on this unihemispheric sleep when needed to watch for predators. My mentors (Charles Amlaner and Steven Lima) and I considered several ways to test this hypothesis, but in the end the ducks that I was studying provided the answer. While watching two ducks sleeping side by side, I noticed that they kept the eye facing each other closed and the eye facing away open. Guided by this observation, we literally put our ducks in a row and rotated their position in the flock across nights to systematically test their ability to resort to unihemispheric sleep. When compared with ducks that were safely flanked by other birds, those relegated to an end of the row increased the proportion of sleep that they spent with one eye open and showed a strong preference for directing the open eye away from the other birds, as if looking out for predators. Presumably, the ducks perceived less risk from the side that was flanked by other ducks when it was compared with the side that was exposed to the rest of the world. Aside from the basic discovery, I like this experiment because it underscores the insight that can be gained from simply spending time observing animals. It also underscores the importance of considering an animal’s ecological context when studying sleep, as well as other aspects of neurobiology. Finally, when this paper was published, I told reporters that, “if birds can do it, humans might be able to do it in some form or another.” At the time, this probably sounded like a farfetched idea from a graduate student who was overly eager to please reporters who were pushing for a direct connection from basic science to humans. Nonetheless, a recent study (Curr. Biol. (2016) 26, 1190–1194) showed that people sleep less deeply with parts of the left hemisphere on the first night in an unfamiliar environment, possibly to keep an ear out for bumps in the night. As such, the study on ducks serves as a strong example of how basic research, seemingly without any utility, can inform our understanding of humans. Why have you taken sleep research into the wild? Historically, sleep research focused on traditional lab animals individually housed under highly controlled conditions with all their needs provided ad libitum. Obviously, this approach has yielded important insights into sleep, and my group’s work on the neurophysiology of sleep in pigeons remains lab-based. However, sleep research on captive animals has undoubtedly missed complex interrelationships between sleep and the ecological context experienced in the wild that might provide novel clues to the functions of sleep. In some cases, captivity might also introduce artificial challenges for which the animal has no adaptive response, and this in turn may impact how they sleep. Although comparative sleep researchers voiced this concern and the need for sleep studies in the wild as early as the 1970s, their research remained confined to the lab due to the absence of tools for recording the changes in EEG and electromyogram activity that define sleep and its sub-states — rapid eye movement (REM) and non-REM sleep — in mammals and birds. Consequently, attempts were made to relate inter-specific differences in sleep duration recorded in captivity to ecological conditions experienced in the wild; the assumption (or hope) was that the time spent sleeping reflects an inflexible, species-specific biological need, shaped by evolution, that should be expressed in the same way regardless of where an animal sleeps. Although this is probably true to some degree, early attempts to investigate the impact of ecological conditions on sleep (albeit in captivity) revealed flexibility in sleep. My ‘ecological’ (lab-based) dissertation research on unihemispheric sleep in ducks and postdoc study of seasonal changes in sleep in migratory songbirds (conducted with Ruth Benca, Martin Wikelski, and others) also demonstrated that sleep is far more flexible than traditionally thought. Given this flexibility, it is also conceivable that animals sleep differently in captivity than they do in the wild. This is particularly problematic when attempting to interpret the functional implications of relationships between certain traits and sleep duration measured in captivity, especially if these traits also predict how a species’ sleep responds to captivity. For instance, do prey species sleep less because natural selection has favored a lower need for sleep or are they simply more likely to lose sleep over being held captive than predatory species? Obviously, early comparative sleep researchers did their best with the available technology. Nonetheless, I think that many of these old questions need to be revisited in the wild. Fortunately, not long after starting my lab at the MPIO, I heard that Alexei Vyssotski and Hans-Peter Lipp, from both the University of Zurich and the Swiss Federal Institute of Technology (ETH), had developed a small device for recording brain activity in free-flying homing pigeons. This tool allowed us to escape the confines of the lab and investigate sleep for the first time in the real-world ecological context in which it evolved. Importantly, our initial forays into the wild revealed that sloths are not so slothful, sleeping only 9–10 hours per day — over 6 hours less than previously reported in captivity. In addition, we have found that the time birds spend sleeping in the wild is vastly more flexible than predicted by traditional, restorative theories for the function of sleep. Overall, I think that it is an exciting time for comparative sleep research, as well as comparative neuroscience in general. Multiple devices are currently being used to investigate various aspects of neurobiology in a diverse array of species in the wild. Undoubtedly, this approach will reveal overarching principles that are currently obscured by the traditional focus on just a few species living in captivity. What are the big challenges in sleep research? Most research indicates that sleep is an essential part of daily life. When we lose sleep, our ability to interact adaptively with the environment becomes compromised. This ranges from lapses in attention while listening to a lecture to falling asleep while driving a car. Sleepiness is even implicated in large disasters, such as the Challenger space shuttle explosion, the Exxon Valdez oil spill, and the nuclear power plant accidents at Three Mile Island and Chernobyl. Decreased waking performance is not unique to humans; even dancing bees lose a step after losing sleep. Impairment arises when the homeostatic pressure to recoup lost sleep causes parts of the brain to fall asleep. In addition, the wear and tear of prolonged wakefulness might impair neuronal performance. Surprisingly, our recent studies on pectoral sandpipers and great frigatebirds suggest that reduced performance is not an evolutionarily inescapable outcome of sleep loss. In collaboration with Bart Kempenaers (MPIO), John Lesku (a PhD student in my lab), and many others, we found that polygynous male pectoral sandpipers that sleep the least are the most successful at siring young, a difficult task that entails out-competing other males for a territory and successfully courting choosy females who decide whether to put all their eggs in a particular male’s (genetic) basket. Although it is possible that this short-sleep strategy incurs long-term costs, higher paternity suggests that sleep loss did not have the immediate and cumulative adverse impact on waking performance that is typically observed in other animals. Similarly, in collaboration with a large team, including Alexei Vyssotski and Martin Wikelski (MPIO), my postdoc, Bryson Voirin, and I recently found that, even though female great frigatebirds can sleep in flight, and usually do so unihemispherically like the ducks, they actually sleep less than an hour per day during week-long foraging trips that are spent entirely on the wing. Reconciling this dichotomy between the wealth of evidence demonstrating decrements in performance resulting from sleep loss, on the one hand, and the ability of some birds to forgo amounts of daily sleep that would render us incapable of safely driving a car, on the other, is an exciting challenge for the sleep research field. Increased motivation, mediated by the release of the wake-promoting neurotransmitter dopamine and/or neuropeptide hypocretin, might sustain adaptive waking performance by keeping the homeostatic pressure for sleep at bay. However, if simply putting the brakes on the homeostat is all that is needed to keep adaptive wakefulness going, this would suggest that neuronal wear and tear caused by wakefulness has no impact on performance. Although this might be correct, it is also possible that unknown resources are summoned to repair wear and tear on the go and thereby prolong periods of adaptive wakefulness. My own personal experience questions whether the ability to perform adaptively on little sleep is simply a function of motivation. While driving to a site in Panama to study frigatebirds, I was caught out on the road late at night by myself. I had planned to make the long drive through this beautiful country during the day, but I got delayed by an auto accident (not my fault) in Panama City and later by a speed trap manned by a friendly police officer who escorted me to an ATM when I failed to produce the appropriate toll. While I was not aware of the speed limit, being a sleep scientist I was acutely aware of the dangers of driving well past my bedtime. However, I did not feel safe sleeping alongside the road. So, I pressed on, desperately trying to stay awake, wishing I was a duck. When I woke up driving on the wrong side of the road, I decided that stopping to sleep was the safer option. Clearly, being motivated to stay awake by the dangers of falling asleep at the wheel was insufficient. Consequently, I suspect that motivation alone does not explain how frigatebirds stay awake throughout most of the monotonous nighttime hours spent gliding over the ocean. Ultimately, determining how some birds are able to perform adaptively on little sleep might inspire a new understanding of sleep’s functions, as well as novel approaches to mitigate the consequences of insufficient sleep in humans.