“The key to the mystery of sleep are the similarities between human sleep and sleep of the cockroaches, flies and plants”

Irene Tobler 2

The suisse investigator Irene Tobler, the biggest world specialist in animal sleep gives an exclusive interview to the iSleep, in which she unveils the sleep mechanisms of several species and answers a lot of curiosities: the animals that sleeps more and less, only with an hemisphere, standing, on top of the trees, with eyes open, that ruminate and sleep at the same time… A big scientific interest in the study of animal sleep is understanding sleep in humans and here the investigator opens a window of hope: “It is necessary to investigate the similarities of sleep of cockroaches, flies and plants to unveil the mysteries of human sleep”.

 

When and how did you begin to be interested in animal sleep?

The topic of my master thesis was visual discrimination in ants. During the day I marked and trained individual ants in an artificial arena to fetch little food tidbits in either of 2 places I had marked with different visual tasks. They learnt readily, but I was soon curious to know whether they came out of their nest at night and “cheat”. I installed a folding bed in the broom closet, set the alarm clock for 2-hourly wakeups and checked on the presence of my colorfully marked ants in the arena during the night hours: only very rarely was an ant out of the nest. I assumed they were sleeping. Little did I know then that my professional life would be dedicated to sleep research

I believe that all mammals sleep. Is that the case of animals in general?

I’m not sure we can generalize what we know from relatively few species to all animals. Recordings have been performed in few animals, considering the large amount of species and especially their diversity. Nature is full of surprises. And who knows, maybe there are species which have adapted not to sleep at all. Sometimes the definition of sleep has to be applied more loosely, for example in dolphins which move all the time and nevertheless sleep.

Which are the species that sleep less? It appears that the giraffe sleeps just a little.

It does appear that especially large herbivores like the giraffe sleep very little. The only study comprising weeks and weeks of 24 h recordings, which I obtained in a zoo in Holland (based on behavior and not on EEG), resulted in 4-5.5 hours per day, including some rare siestas. It is safe to assume that in the wild, where giraffes are exposed to predators, they sleep even less. Possibly there is a lot of compensation with drowsiness or light sleep.


Which is the animal that sleeps the mostg? Is it true that the hedgehog and cockroach sleep a lot?

The longest “sleepers” are bats, sloths, carnivores such as the ferret, and yes, hedgehogs. Again here caution is needed. Most numbers are based on recordings performed in laboratories or outside enclosures. The sloths recorded by telemetry in Panama by the group of Niels Rattenborg obtained 6 h less sleep than the previously 16-17 h recorded in a laboratory.
Cockroaches, which belong to the Class Insects “sleep” for 6 h per 24 h (immobility alone is not “sleep”; the 6 h were derived by combining immobility and body posture with high arousal threshold).
Considering that Chiara Cirelli’s recordings of several 1000 Drosophila mutants show that there are mutants that sleep as little as 3 h and others up to 21 h, we should not generalize from the two cockroach species I recorded.

If you had to assign one key feature to sleep in mammals, which one would it be? What about birds, reptiles and fish?

Enhanced arousal threshold during relative quiescence is a key feature, which in mammals correlates with the appearance of slow waves in the EEG. But even this feature does not apply to all mammals, because as mentioned above for dolphins, quiescence is not always present.
To my knowledge no one has measured arousal thresholds in conjunction with behavior or EEG in birds. The eye opening of a single eye that can be observed in many birds complicates the interpretation of whether they sleep. Therefore, we rely on the EEG correlates to determine whether they sleep. And migration is yet a problem to be solved: can birds sleep during migration?
Behavior in reptiles and fish is temperature dependent; therefore even arousal responses to stimuli must be interpreted with caution.

Can one say that plants sleep?

Perhaps. Since we do not yet know the function(s) of sleep we need to keep an open mind as to how living beings have adapted to optimize their “rest” periods in order to survive. Certainly plants “know” when it is day and when it is night, and this affects their biochemistry and physiology dramatically.

We may say that the sleep needs of animals depend on their metabolism, their size and energy consumption… Is that so?

Yes, this is true to some extent for mammals, but in some species more so than in others: herbivorous animals ingest fewer calories, so they need to spend much more time eating, with little time remaining for sleep, while carnivores ingest large amounts of calories in one meal and spend much more time asleep. We have no idea which factors determine “sleep need” in birds, reptiles, fish and invertebrates.

Do all animals show compensatory mechanisms after sleep deprivation?

Years ago, in 1983, I introduced this feature thereby expanding the traditional definition of sleep. So far compensatory mechanisms regulating the amount of sleep and its intensity seem to be present in all mammals that have been recorded after sleep deprivation. The inclusion of the capacity to compensate for “sleep” loss in the definition of sleep led to its investigation in birds, “lower” vertebrates (fish) and especially invertebrates (which I began by studying the response to deprivation of “rest” in cockroaches, easy to breed and well known in circadian rhythm literature, and later in scorpions, even older arthropods than insects).

Animals have a polyphasic sleep. Why?

I assume that only highly evolved mammals have the capacity to maintain wakefulness for as long as 16-18 hours. Even primates can be observed napping once or twice during the day. Most rodents, carnivores and herbivores intersperse long waking bouts with sleep bouts which can last 1-2 hours during their circadian activity phase. Daily sleep-wake “architecture” appears to be much more flexible that it was once assumed. For example, having to work for food rather than obtaining food “ad libitum” or changing waking behaviors by providing cage enrichment (e.g. a running wheel), leads to much longer waking episodes. On the other hand it is believed that also humans were more polyphasic before the light bulb was invented!

You developed extensive sleep studies on several species, including cockroaches. What conclusions did you draw?

Sleep is a fascinating topic. So many animals have developed an impressive diversity of behaviors in order to obtain their daily sleep! But sleep function remains a mystery. Studying sleep in different species, rather than focusing on a few laboratory “models” can tell us much more about the diversity of sleep. Finding similar features in sleep between humans, cockroaches and flies (and maybe plants?) may be the key to unlock the mystery of sleep!

Are there species whose sleep is undeniably more difficult to study? For example, sleep in snails, frogs…?

Yes, animals that live in the water, like fish, newts and coelenterates can be observed and manipulated, but their neuronal activity is more difficult to record.
How birds sleep during the thousands of miles of migration remains a mystery. New technologies are being developed which make more species accessible for sleep recordings.

I believe that in the water sea lions sleep with only a half hemisphere and with both hemispheres when on land. Is that so? Why?

You refer to “deep” sleep. In contrast to dolphins, and the beluga whale sea lions and fur seals do have the capacity to obtain “deep” sleep, characterized by large amplitude slow waves, simultaneously in both hemispheres. It is interesting that the amount of unihemispheric sleep was shown by Oleg Lyamin to diminish when fur seals sleep on land compared to the amount recorded while they sleep in water. This led to the assumption that it is maintaining their nose above water to enable breathing which keeps one hemisphere awake. Unihemispheric sleep may be a “compromise” and global bihemispheric sleep is always preferable (perhaps more “efficient”?). Animals seem to choose to sleep bilaterally when possible, even when they are equipped with the capacity to sleep with only one half of the brain at a time.

Dolphins continue to swim while sleeping with only one hemisphere. What process is involved here?

The processes are still unknown. Possibly connectivity between the hemispheres or laterality in subcortical “sleep-promoting” and “wake-promoting” systems is involved. The corpus callosum, which is the main commissure connecting the two hemispheres is considerably smaller in cetaceans, as compared to other species. This may enable unihemispheric sleep. Less is known about the role of deep brain structures. Evidence suggests that in seals the release of some wake-promoting neurotransmitters is also lateralized. The ability to sleep with one hemisphere at a time is a remarkable adaptation, and took a long time to evolve since it entails major reorganization of brain systems. But it certainly helped these species to become very successful, conquering the aquatic environment as mammals equipped with lungs.

Are there many animals sleeping with only half the brain? Is that why many do it with one eye open or is it a whole different process?

So far only dolphins, sea lions and a sea cow have been shown to sleep with one hemisphere at a time. This EEG pattern correlates quite often, but not always, with contralateral eye-closure. Whether the very short epochs of unilateral eye closure and corresponding change in EEG activity in birds is comparable to unihemispheric sleep, which can last from minutes up to several hours is still an open question. On the other hand, it is likely that some lateralization during sleep is present in many species. Most functions in animals are lateralized to some extent. For example, most of us humans and also rats are left-handed or right-handed. There is some evidence (also from my laboratory) that laterality during waking behaviors correlate with interhemispheric asymmetry during sleep.

Cows and deer sleep standing up, I believe. Is that common to many other animals? What is the explanation?

Yes, I have described this also in elephants and giraffes and observed it during my activity recordings in sheep and mountain goats. Standing sleep is known also for horses and donkeys. There are some claims that even humans can sleep while marching when they are very tired!
It is fair to assume that sleep occurring in animals while standing is not very deep. This idea could be experimentally verified by measuring their arousal threshold. Animals only lie down to sleep when they are undisturbed and very tired. Also, lying down to sleep helps thermoregulation; it allows curling up and saving energy.

Birds and many other animals do not fall from trees while sleeping. Why?

The anatomy of bird legs and feet is so that when they stretch their legs their fingers relax. When they relax, lower their bodies and bend their legs, their fingers grip the branch they are standing on. Sloths hang on branches by their extremely powerful claws. Also bats sleep upside down while hanging by their claws from a tree branch or smallest crevice in caves. As in birds, their feet have evolved to be clamped when all muscles are relaxed. When bats relax, their weight pulls down the tendons to the talons which clench closed.

Koalas and raccoons sleep while crouching between well-chosen tree branches. Young monkeys cling to their mothers and can sleep while holding on to them. This is another very interesting adaptation, since young animals need much more sleep than adults.

It appears that cows can ruminate while sleeping. How can this mechanism be explained?

The EEG of cows was recorded years ago by Yves Ruckebusch, a French veterinarian. He described the simultaneous occurrence of rumination and nonREM sleep. Recent work from colleagues in Cambridge has shown that also sheep sleep while ruminating, but they obtain only nonREM sleep, no REM sleep is possible while simultaneously ruminating.

I do not know the mechanism, but it is possible that some lower brain regions are to some extent “awake” and enable these automatic movements without disturbing sleep. After all, we do not stop breathing during sleep, although breathing is to some extent under central control.

A prehistoric curiosity: what would the dinosaurs’ sleep look like?

I doubt I would dare measure arousal thresholds in Tyrannosaurus Rex, Triceratops or Allosaurus even if available! My guess is that their sleep would be similar to that of modern reptiles. Perhaps Archeopterix would already show signs of REM sleep. It would be interesting to look at the DNA of dinosaurs and identify common genes involved in sleep and wake regulation between them and modern animals. The molecules, involved in sleep regulation, such as certain peptides, are preserved across evolution and may well have been playing the same role millions of years ago.

What is the most bizarre sleep habit you have observed among the animals you have studied?

Watching elephants going to sleep only meters away from the bay of hay I sat on for several nights (the elephants were chained). I loved to see them touching each other with their tusks, establishing body contact with the ones asleep. Only in film have I seen sea otters sleep holding hands in order not to drift apart while floating in the ocean on their backs.

Some animals sleep in various positions. What is the strangest position you have ever observed?

Images of sleeping dogs and cats are most popular on the internet because there is practically no position they cannot assume while sleeping. Bears will sleep in the most hilarious postures, especially the young ones; check on them in the internet!

There is this famous video of a Bizkit dog having a very restless sleep. Why are movements in animals so common during sleep?

The behavior of the Bizkit is not normal, but unfortunately looks very funny. The movements we observe in animals during normal sleep occur, as in humans, during REM sleep. In animals they comprise leg and tail movements, twitches of the ears and whiskers and rapid eye movements.

Dolphins are the only mammals that have no REM sleep. Why?

I don’t know. Maybe they would drown during REM sleep due to the accompanying muscle atonia.

Animals have more REM sleep than humans. Why?

Not true, it depends largely on the species. Some have little REM sleep (horses, giraffes, rabbits or guinea pigs) and others quite a lot. The record is held by carnivores, and among carnivores, the ferret. There are theories about the function of REM sleep, but little knowledge on why some species have more than others. It is well established that young animals have more REM sleep than adults. This led to the theory that REM sleep may be important for development. However, this still does not explain why there is REM sleep in adults. It is curious that many animals enter REM sleep more frequently during their sleep periods. Mice, for example, can have 50 or even more REM sleep episodes during 24 h, each of them lasting not more than 1-3 min. This amount altogether adds up to an amount similar to humans, who have only 4-6 REM episodes per night, but each of them  lasts 20 min or even longer.

What decisive contributions did the research and study of animal sleep bring into the study of human sleep?

There are two main aspects driving sleep research in animals. One is comparing many different species in order to foster our understanding of the manifestation and functions of sleep. The other is the use of animals as models to understand sleep physiology, its molecular mechanisms, and the genetics of sleep. I cannot imagine sleep research in humans without the contributions from animals.

What are the major challenges for the future in the study of animal sleep, which have implications for human sleep?

We struggle to find good, appropriate animal models to study sleep mechanisms and pathologies afflicting humans. This problem is not unique for sleep but applies also to many neurological and psychiatric disorders, which have diverse causes and very complex mechanisms. Sleep is also very complex. Unless we understand it better, it will be difficult to develop good animal models. On the other hand, I am convinced that the mechanisms leading to normal sleep are best explored in animals. Humans and animals share striking similarities in sleep mechanisms and this opens unique opportunities.

You were born in Zurich, Switzerland, but your parents emigrated to South America when you were four. What is the reason for this shift?

My parents were quite adventurous. After the war they wished to emigrate to a novel environment. The choice could have been Australia, but coincidence drove them to Peru. Before leaving they took Spanish classes which they intensified during the long transatlantic boat trip to Peru.

How was it like to live in Peru and Chile? What memories do you have from that time?

My memories are probably not different from those of other emigrants. There is always the mixture of belonging and not quite belonging, but this did not affect me as a child. Chile has a long history of immigrants, so my place in school and society was not really influenced by my being Swiss. It was more difficult to return to Switzerland, a country I had no memories of, and leaving all my friends behind.

You returned to Switzerland to study at the age of 18. What led to this return?

This was not my decision; I tagged along with my parents, but appreciated the possibility to enter university in Switzerland.

You not only study sleep in animals but you truly like them as well – to discover them, to watch them and to photograph them. Which picture was harder to take?

You describe me quite accurately! Animals don’t move around when they sleep. So photographing animals sleeping is not such a challenge. But to catch adult giraffes sleeping, because they are so sensitive to people’s presence at night was only possible with dark sensitive infra-red cameras. The young giraffes I could easily photograph because they take frequent naps during the day even in outside enclosures.

A typical anecdote is my first viewing of a sleeping sea lion floating at the bottom of the aquarium in Valencia. While I was trying to capture the sleeping animal on a photo I was glued to the glass oblivious of my surroundings until I had to be complimented out of the building upon closing time. Many day-active animals begin sleeping when zoos close.

Can you tell us a funny story related to your sleep?

There is nothing special about my sleep. As a child I was often caught sleep-walking and typically had no recollection of this when awake the next day.

Do you frequently dream about animals? Can you tell us one of those dreams?

Rarely (dreams about animals are more common in children, I remember having dreamt of animals as a child, but I do not remember the content).

You were president of ESRS between 2000 and 2004. How would you describe that experience?

It was challenging to be president, but I had a wonderful time. Since I had been treasurer for many years before the presidency and had attended all ESRS congresses since my entry into sleep research (this was in 1975), I knew so many colleagues personally or by name, and had made many friends. This was very helpful in obtaining support for the innovations I wanted to implement to give ESRS a new impetus. I am particularly pleased that the National Sleep Societies could be incorporated within the ESRS and still maintain and pursue their national interests. During my presidency we were successful in establishing European courses in basic and clinical sleep research. These courses were later funded by the European Union (Marie Curie training courses) helping to establish a large network of young scientists interested in sleep.

Despite having held prominent positions, do you think that being a woman has been a disadvantage in you scientist’s career?

In many ways yes, but I never dwelled on such problems.

 

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