December 27, 2017

„Mum, how do dolphins sleep?“: Sleep throughout the animal kingdom

Have you ever wondered whether your dog sleeps like you – and yaps because he is probably dreaming about the mailman? Do all animals need sleep as much as we do? And how on Earth do they continue swimming or even flying during sleep?

Smart because of Mattresses?
First of all, we should define what we are talking about: Sleep can be characterized in many ways, but without electroencephalography with wild animals, we should focus on the behavioral definition: Sleep is when the animal exhibits a rapidly reversible state of immobility and reduced responsiveness to external stimuli. Furthermore, an increased drive for sleep (rebound effect) is expected after sleep deprivation [1].
Lets start with our closest relatives: Great apes exhibit monophasic sleep (like humans and unlike the majority of other mammals), meaning that they concentrate their sleep in one period per day. Theories claim the reason for this is that they are (like us) capable of building a comfortable and safe sleeping platform - allowing them to sleep more safely and therefore more deeply. Maybe our cognitive abilities just came from very comfy beds [2]?

Apes build comfy beds
 
But there are other intelligent animals that definitely have no mattress to sleep on. Many dolphins are able to rest one half of their brain while the other one controls breathing, for which marine mammals have to come to the surface. This phenomenon, which some of us would love to do during boring seminars, is called uni-hemispheric slow-waves (USW). It enables dolphins, whales and also many birds to rest one hemisphere at a time with the contralateral eye closed, changing to the other one after about two hours [1]. Brain waves similar to slow-wave sleep and REM sleep in humans have been recorded in flying frigate birds which migrate for several months at a time [3]. Remarkably, when in REM sleep, these birds as well as some other mammals like the sperm whale also show bi-hemispheric sleep. However, this behaviour can only be found on the ground – or in the case of sperm whales while floating vertically in the ocean, holding their breath for a long time [4]. A strategy like this would never work in many sharks, since they need constant flow through their gills to be able to breathe. Some seem to solve this problem by doing “yo-yo diving“: First they swim to the surface to then glide downwards, giving themselves a short period of rest [5].

Different Animals sleep differently
The sleeping behaviour of terrestrial animals can also be very different from ours: Does anyone sleep while standing - No?! Horses and other bigger herbivores often do, with help of their stay apparatus, which consists of ligaments and tendons that lock into place. Still, many of them need to lie down for REM sleep as it comes with strong muscle atonia. Due to this, horses, giraffes and also elephants actually end up having much less sleep than we are used to, getting away with just 2-4 hours per day [6]. Many short naps seem to be more beneficial for these animals, since it enables them to spend more time alert when predators are around.
Who wouldn’t like to be capable of skipping 5-6 hours sleep per day in order to prepare the next lab meeting? New-born orcas outperform us a lot when it comes to little sleep: They stay awake for one full month after birth, and only rest while pressing their body against their mother. Compared to this, big brown bats and hairy armadillos lead a pretty relaxed life, sleeping for roughly 20 hours per day [6]. 
Image Source: http://bit.ly/2B1GiM7
So far we were mostly talking about sleep similar to human non-REM. But do animals also dream? Of course, no one can ask a cat whether it was recently dreaming of mice. Anyway, many mammals, birds and even reptiles show physiological patterns with consistent with REM sleep. Dragonflies have 350 REM cycles per day, each of them lasting 80s [7] and the platypus spends approximately 5.8-8 h/day in REM [8]. REM sleep is sometimes seen as a key feature during evolution of the amniote – the common ancestor of mammals, birds and reptiles that lived more than 300 million years ago [7]. However, octopus also seem to have REM like sleep patterns that go along with changing colours and twitching of their arms [9].
Yet, the animal kingdom consists of more than vertebrates. What about insects, nematodes and porifera (sponges)? While for porifera there is no evidence of sleeping behavior, the fruitfly D. melanogaster has not only been shown to have sleep-like resting patterns but also exhibit cognitive impairment upon sleep depriviation [1]. A fatigue period (lethargus) before moulting in C. elegans suggests that sleep is somehow connected to development and related to neuronal changes [10].

What's the Purpose behind Sleep...?
Of course most sleep studies focused on very few animals from each taxa so far. For instance, just 50 out of 60000 vertebrate species have been tested for all sleep criteria so far and not all of them were found to meet all of the criteria. Nevertheless sleep-like behavior seems to be present in various animals. Can we assume that all these animals sleep for the same reason - and if so what is the reason?
Over years, several theories on the function of sleep have been developed. The original idea that sleep is mainly necessary to conserve energy seems quite unlikely nowadays since it decreases metabolism by very little amounts (5-10%), whereas hibernation saves a lot more energy [11]. Another very prominent idea is that sleep is important for learning and memory consolidation (see article of page 6). Even though there is evidence for a role of sleep in memory, it is still disputed what this role exactly is – ranging from memory deletion during REM sleep to maturation of memory circuits [12]. Recently, sleep has been linked with a restorative function in the central nervous system, leading to a clearance of free radicals and other metabolic waste that accumulates during wakefulness [13]. While many of these processes definitely occur during sleep, they don’t explain the great variation in sleep needs and patterns throughout the animal kingdom. 

Do all animals sleep for the same reason?

Trying to address this, some researchers now regard sleep as a state of adaptive inactivity, optimizing the timing of behavior according to prey/food availability and threats in the environment. In this scenario, continuous wakefulness implies the greatest energy demands but maximizes niche exploitation. This can explain why giraffes sleep so little (they have a very low-caloric diet and a high threat of predators). For bats that feed specifically on insects being active between dusk and initial hours of darkness, on the other hand, a longer period of time awake would be highly maladaptive since it increases their risk of becoming prey [14].

... we don't fully know (yet)!
Exploring sleeping behavior of other animals can, therefore, help to clarify its function in humans. While sleep deprivation in humans and rodents so far suggests that sleep influences cognition, emotion, immunity and memory, the function of sleep can still be substantially different when looking at all animals that exhibit sleep-like resting behavior. We should all be aware that, as put by Michel Jouvet, a famous sleep researcher who just passed away, "it’s not enough to use the brain of your experimental animal, it’s also necessary to use your own”. 

Annika Reinhold, MSc Student MedNeuro

References:
[1] Siegel, 2008, Trends in Neurosciences
[2] Shumaker et al., 2014, American Journal of Physical Anthropology
[3] Rattenborg et al., 2016, Nature Communications
[4] Miller et al., 2008, Current Biology
[7] Shein-Idelson et al., 2016, Science
[8] Siegel et al., 1999, Neuroscience
[10] Sing et al., 2013, Sleep
[11] Assefa et al., 2015, AIMS Neuroscience
[12] Diekelmann & Born, 2010, Nature Reviews Neuroscience
[13] Xie et al., 2013, Science
[14] Siegel, 2009, Nature Reviews Neuroscience



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