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Typical sleep postures of sea otters sleeping in the water. (A) During quiet sleep (QS), sea otters float on their back with their head and limbs held out of the water. (B and C) During the transition from QS to active sleep (AS) a loss of muscle tone causes the head and limbs to drop and the otter to roll over. (D) During AS the otter floats on its belly with the nostrils below the surface. Reprinted with permission from Lyamin, O.I., Oleksenko, A.I., 2000. Behavioral sleep in captive sea otters. Aquat. Mamm. 26, 132–136, Copyright 2000, courtesy of Kathleen M. Dudzinski.
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Sleep is ubiquitous throughout the animal kingdom. Nonetheless, we still do not have a firm grasp on its functions. Whatever its functions, we should expect them to vary in accord with the diverse morphologies, physiologies, ecologies, and life histories of different species and taxonomic groups. Moreover, one apparently universal feature of sleep—...
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... mammals also experience reduced muscle tone during AS, even though it can interfere with breathing ( Lyamin et al., 2008). Although sea otters (Enhydra lutris) can float on their back with their head held out of the water during QS, during apparent AS their muscles relax and the head falls below the surface ( Fig. 6; Lyamin and Oleksenko, 2000). Similarly, fur seals (family Otariidae) can keep their nostrils above the surface by floating on their side while paddling one flipper during unihemispheric or asymmetric QS. However, during AS, paddling stops and their head sinks below the surface. As a result, fur seals greatly reduce the time spent in ...
Citations
... Might sleep also contribute to the developmental plasticity that enables the functional integration of brain and body? Indeed, for decades, researchers addressed similar developmental questions by noting that early postnatal life is the time when animals-vertebrates and invertebrates alikesleep the most (Blumberg and Rattenborg, 2017;Kayser and Biron, 2016). For example, in humans and rats, rapid eye movement (REM) and non-REM sleep (or active and quiet sleep, respectively) exhibit distinct developmental profiles, with REM sleep being more prevalent in early life than non-REM sleep (Jouvet-Mounier et al., 1970;Roffwarg et al., 1966) (Figure 1). ...
A defining feature of early infancy is the immense neural plasticity that enables animals to develop a brain that is functionally integrated with a growing body. Early infancy is also defined as a period dominated by sleep. Here, we describe three conceptual frameworks that vary in terms of whether and how they incorporate sleep as a factor in the activity-dependent development of sensory and sensorimotor systems. The most widely accepted framework is exemplified by the visual system where retinal waves seemingly occur independent of sleep-wake states. An alternative framework is exemplified by the sensorimotor system where sensory feedback from sleep-specific movements activates the brain. We prefer a third framework that encompasses the first two but also captures the diverse ways in which sleep modulates activity-dependent development throughout the nervous system. Appreciation of the third framework will spur progress toward a more comprehensive and cohesive understanding of both typical and atypical neurodevelopment.
... We have reviewed ten recent reports (since 2016) dealing with the evolution of sleep. Eight out of them (Miyazaki et al., 2017;Blumberg & Rattenborg, 2017;Joiner, 2016;Ungurean et al., 2019;Anafi et al., 2019;Kashiwagi and Hayashi, 2020;Blumberg and Rattenborg, 2017) accepted the presence of behavioral sleep in poikilothermic vertebrates and invertebrates. Regarding the remainder, one was eclectic, simply demanding for non-homeothermic animals the same rigorous methods used for ascertaining sleep in mammals and, vice-versa, applying to mammals the molecular techniques developed in invertebrates (Hartse, 2017). ...
... We have reviewed ten recent reports (since 2016) dealing with the evolution of sleep. Eight out of them (Miyazaki et al., 2017;Blumberg & Rattenborg, 2017;Joiner, 2016;Ungurean et al., 2019;Anafi et al., 2019;Kashiwagi and Hayashi, 2020;Blumberg and Rattenborg, 2017) accepted the presence of behavioral sleep in poikilothermic vertebrates and invertebrates. Regarding the remainder, one was eclectic, simply demanding for non-homeothermic animals the same rigorous methods used for ascertaining sleep in mammals and, vice-versa, applying to mammals the molecular techniques developed in invertebrates (Hartse, 2017). ...
... Instead, we should seek to understand infant sleep on its own terms (Blumberg and Seelke, 2010). Ultimately, any complete resolution to the mysteries of sleep will have to account for its early expression and transformation across the lifespan as well as its expression in a diversity of species (Blumberg and Rattenborg, 2017;. ...
Humans and other mammals never sleep more than when they are young. In comparison with adults, newborns sleep in short bouts distributed evenly across the day and night. Gradually, over the first few postnatal months, infant sleep bouts consolidate into longer and longer bouts that increasingly occur more often at night. These basic developmental increases in sleep consolidation and circadian rhythmicity are typical of mammals, whether they occur prenatally (in precocial species like sheep) or postnatally (in altricial species like rats). Another feature of sleep development is that some of the components that characterize it in adults, such as the cortical delta waves of quiet (or non-REM) sleep, are initially absent in early development. Close inspection reveals that cycles of sleep and wake are expressed initially as relatively rapid fluctuations of low and high muscle tone, respectively, coupled with behaviors that are indicative of active (or REM) sleep or wake. It is upon this basic foundation that the increasingly complex features of active and quiet sleep develop. At the neural level, brainstem mechanisms alone are initially sufficient to support basic sleep-wake cycling; forebrain mechanisms are gradually integrated into the system to support such processes as bout consolidation, circadian rhythmicity, and sleep rebound after periods of sleep deprivation. Although we do not yet fully understand why infants sleep as much as they do, recent work is shedding new light on this mystery by focusing on early development as a time of increased brain plasticity.
... Sleep is a mysterious state of reduced environmental awareness found in animals ranging from jellyfish to humans (Joiner, 2016;Libourel and Herrel, 2016;Blumberg and Rattenborg, 2017;Nath et al., 2017;Anafi et al., 2019;Iglesias et al., 2019;Kelly et al., 2019). Sleep in mammals is composed of two states, non-rapid eye movement (NREM) sleep and REM sleep, typically distinguished from one another and wakefulness by changes in brain and muscle activity. ...
Rapid eye movement (REM) sleep is a paradoxical state of wake-like brain activity occurring after non-REM (NREM) sleep in mammals and birds. In mammals, brain cooling during NREM sleep is followed by warming during REM sleep, potentially preparing the brain to perform adaptively upon awakening. If brain warming is the primary function of REM sleep, then it should occur in other animals with similar states. We measured cortical temperature in pigeons and bearded dragons, lizards that exhibit NREM-like sleep and REM-like sleep with brain activity resembling wakefulness. In pigeons, cortical temperature decreased during NREM sleep and increased during REM sleep. However, brain temperature did not increase when dragons switched from NREM-like to REM-like sleep. Our findings indicate that brain warming is not a universal outcome of sleep states characterized by wake-like activity, challenging the hypothesis that their primary function is to warm the brain in preparation for wakefulness.
... Songbirds provide a unique opportunity to study the relationship between dopaminergic system and sleep-wake regulation. Birds exhibit sleep structures similar to mammals (Blumberg and Rattenborg, 2017) and mammalian-like sleep features (such as slow-wave sleep, intermediate sleep, and REM sleep) have been demonstrated in zebra finches (Low et al., 2008). In addition, the midbrain dopaminergic system has been relatively well-characterized in zebra finches. ...
Sleep-wake behaviors are important for survival and highly conserved among animal species. A growing body of evidence indicates that the midbrain dopaminergic system is associated with sleep-wake regulation in mammals. Songbirds exhibit mammalian-like sleep structures, and neurons in the midbrain ventral tegmental area (VTA) and substantia nigra pars compacta (SNc) possess physiological properties similar to those in mammals. However, it remains uncertain whether the neurons in the songbird VTA/SNc are associated with sleep-wake regulation. Here, we show that VTA/SNc neurons in zebra finches exhibit arousal state-dependent alterations in spontaneous neural activity. By recording extracellular single-unit activity from anesthetized or freely behaving zebra finches, we found that VTA/SNc neurons exhibited increased firing rates during wakefulness, and the same population of neurons displayed reduced firing rates during anesthesia and slow-wave sleep. These results suggest that the songbird VTA/SNc is associated with the regulation of sleep and wakefulness along with other arousal regulatory systems. These findings raise the possibility that fundamental neural mechanisms of sleep-wake behaviors are evolutionarily conserved between birds and mammals.
... We have reviewed ten recent reports (since 2016) dealing with the evolution of sleep. Eight out of them (Miyazaki et al., 2017;Blumberg & Rattenborg, 2017;Joiner, 2016;Ungurean et al., 2019;Anafi et al., 2019;Kashiwagi and Hayashi, 2020;Blumberg and Rattenborg, 2017) accepted the presence of behavioral sleep in poikilothermic vertebrates and invertebrates. Regarding the remainder, one was eclectic, simply demanding for non-homeothermic animals the same rigorous methods used for ascertaining sleep in mammals and, vice-versa, applying to mammals the molecular techniques developed in invertebrates (Hartse, 2017). ...
... We have reviewed ten recent reports (since 2016) dealing with the evolution of sleep. Eight out of them (Miyazaki et al., 2017;Blumberg & Rattenborg, 2017;Joiner, 2016;Ungurean et al., 2019;Anafi et al., 2019;Kashiwagi and Hayashi, 2020;Blumberg and Rattenborg, 2017) accepted the presence of behavioral sleep in poikilothermic vertebrates and invertebrates. Regarding the remainder, one was eclectic, simply demanding for non-homeothermic animals the same rigorous methods used for ascertaining sleep in mammals and, vice-versa, applying to mammals the molecular techniques developed in invertebrates (Hartse, 2017). ...
The Nocturnal Bottleneck explains how mammals evolved from their reptilian ancestors after inverting the chronotype, form diurnal to nocturnal. Pre-mammals traded-off the excellent visual system of their ancestors for improvements in audition and in olfactory telencephalon, needed for efficient orientation in the dark. This was how the mammalian nocturnal telencephalic wakefulness was born. However, the modified visual system of those pre-mammals became sensitive to the dangerous diurnal light and the exposure would involve a high risk of blindness and death. Therefore, pre-mammals had to remain immobile with closed eyes hidden in lightproof burrows during light time. This was the birth of the mammalian sleep. Typical reptiles distribute their wake time cycling between Basking Behavior, to attain the preferred body temperature, and poikilothermic Goal Directed Behavior, to perform life sustaining tasks. These cycles persisted during the new mammalian sleep. However, as the behavioral output had to be blocked during light time, the paralyzed reptilian Basking Behavior and Goal Directed Behavior cycles became the NREM and REM cycles, respectively. This was how NREM and REM cycles remained incorporated within the mammalian sleep. After the Cretaceous-Paleogene extinction, the environmental pressure for nocturnal life was softened, allowing high variability in chronotype and sleeping patterns. This permitted some mammalian groups, e.g., primates, to begin the quest for diurnal wake.Concluding, sleep constituted an additional bottleneck in the mammalian evolution. The reduced population of pre-mammals that was able to develop sleep during light time, including NREM and REM, became full mammals and survived; the remainder perished.
... Sleep occurs in all investigated animal species, suggesting that it evolved early and serves an important purpose (Blumberg & Rattenborg, 2017;Nath et al., 2017). In mammals, the shift from wakefulness to sleep is associated with distinct changes in neuronal activity in the neocortex. ...
Sleep‐related brain activity occurring during non‐rapid eye‐movement (NREM) sleep is proposed to play a role in processing information acquired during wakefulness. During mammalian NREM sleep, the transfer of information from the hippocampus to the neocortex is thought to be mediated by neocortical slow‐waves and their interaction with thalamocortical spindles and hippocampal sharp‐wave ripples (SWRs). In birds, brain regions composed of pallial neurons homologous to neocortical (pallial) neurons, also generate slow‐waves during NREM sleep, but little is known about sleep‐related activity in the hippocampus and its possible relationship to activity in other pallial regions. We recorded local field potentials (LFP) and analogue multi‐unit activity (AMUA) using a 64‐channel silicon multi‐electrode probe simultaneously inserted into the hippocampus and medial part of the nidopallium (i.e. caudal medial nidopallium; NCM) or separately into the caudolateral nidopallium (NCL) of adult female zebra finches (Taeniopygia guttata) anesthetized with isoflurane, an anaesthetic known to induce NREM sleep‐like slow‐waves. We show that slow‐waves in NCM and NCL propagate as waves of neuronal activity. In contrast, the hippocampus does not show slow‐waves, nor sharp‐wave ripples, but instead displays localized gamma activity. In conclusion, neuronal activity in the avian hippocampus differs from that described in mammals during NREM sleep, suggesting that hippocampal memories are processed differently during sleep in birds and mammals.
... The first type occurs when infants are awake and comprises large (i.e., high-amplitude), continuous, or sustained movements of the limbs, such as stretching, kicking, and yawning. The second type of movement occurs during active sleep, which is most prevalent early in development [11][12][13], and comprises discrete, brief, and jerky movements of the limbs, digits, face, eyes, and, in rodents and many other mammals, whiskers and tail ( Figure 1A). These movements are called myoclonic twitches. ...
Amputees who wish to rid themselves of a phantom limb must weaken the neural representation of the absent limb. Conversely, amputees who wish to replace a lost limb must assimilate a neuroprosthetic with the existing neural representation. Whether we wish to remove a phantom limb or assimilate a synthetic one, we will benefit from knowing more about the developmental process that enables embodiment. A potentially critical contributor to that process is the spontaneous activity - in the form of limb twitches - that occurs exclusively and abundantly during active (REM) sleep, a particularly prominent state in early development. The sensorimotor circuits activated by twitching limbs, and the developmental context in which activation occurs, could provide a roadmap for creating neuroprosthetics that feel as if they are part of the body.
Mammals evolved from small-sized reptiles that developed endothermic metabolism.
This allowed filling the nocturnal niche. They traded-off visual acuity for sensitivity but became
defenseless against the dangerous daylight. To avoid such danger, they rested with closed eyes in
lightproof burrows during light-time. This was the birth of the mammalian sleep, the main finding of
this report. Improved audition and olfaction counterweighed the visual impairments and facilitated
the cortical development. This process is called “The Nocturnal Evolutionary Bottleneck”. Premammals
were nocturnal until the Cretacic-Paleogene extinction of dinosaurs. Some early mammals
returned to diurnal activity, and this allowed the high variability in sleeping patterns observed today.
The traits of Waking Idleness are almost identical to those of behavioral sleep, including homeostatic
regulation. This is another important finding of this report. In summary, behavioral sleep seems to be
an upgrade ofWaking Idleness Indeed, the trait that never fails to show is quiescence. We conclude
that the main function of sleep consists in guaranteeing it during a part of the daily cycle.
