Unihemispheric slow wave sleep and the state of the eyes in a white whale

doi:10.1016/S0166-4328(01)00346-1

Behavioural Brain Research

Volume 129, Issues 1–2, 1 February 2002, Pages 125-129

https://doi.org/10.1016/S0166-4328(01)00346-1 Get rights and content

Abstract

We recorded electroencephalogram (EEG) and simultaneously documented the state of both eyelids during sleep and wakefulness in a sub-adult male white whale over a 4-day-period. We showed that the white whale was the fifth species of Cetaceans, which exhibits unihemispheric slow wave sleep. We found that the eye contralateral to the sleeping hemisphere in this whale was usually closed (right eye, 52% of the total sleep time in the contralateral hemisphere; left eye, 40%) or in an intermediate state (31 and 46%, respectively) while the ipsilateral eye was typically open (89 and 80%). Episodes of bilateral eye closure in this whale occupied less than 2% of the observation time and were usually recorded during waking (49% of the bilateral eye closure time) or low amplitude sleep (48%) and rarely in high amplitude sleep (3%). In spite of the evident overall relationship between the sleeping hemisphere and eye state, EEG and eye position in this whale could be independent over short time periods (less than 1 min). Therefore, eye state alone may not accurately reflect sleep state in Cetaceans. Our data support the idea that unihemispheric sleep allows Cetaceans to monitor the environment.

Section snippets

Acknowledgements

The study was supported by Utrish Dolphinarium Ltd. and the Medical Research Service of the Veterans Administration, USPHS grant NS32819. The authors thank E. Rozanova for veterinary support and two anonymous reviewers whose comments improved the final version of the manuscript.

References (17)

O.I. Lyamin et al.
Unilateral EEG activation during sleep in the cape fur seal, Arctocephalus pusillus
Neurosci. Lett.
(1992)
L.M. Mukhametov
Unihemispheric slow-wave sleep in the Amazonian dolphin, Inia geoffrensis
Neurosci. Lett.
(1987)
L.M. Mukhametov et al.
Interhemispheric asymmetry of the electroencephalographic sleep patterns in dolphins
Brain Res.
(1977)
N.C. Rattenborg et al.
Facultative control of avian unihemispheric sleep under the risk of predation
Behav. Brain Res.
(1999)
N.C. Rattenborg et al.
Behavioral, neurological and evolutionary perspectives on unihemispheric sleep
Neurosci. Biobehav. Rev.
(2000)
Castellini MA. Sleep in aquatic mammals. In: Carley D, Radulovacki M, editors. Animal Models of Sleep Related Breathing...
P.G. Goley
Behavioral aspects of sleep in pacific white-sided dolphins (Lagenorhynchus obliquidens, Gill 1866)
Mar. Mamm. Sci.
(1999)
J.C. Lilly
Animals in aquatic environments: adaptation of mammals to the ocean

There are more references available in the full text version of this article.

Cited by (80)

The unified theory of sleep: Eukaryotes endosymbiotic relationship with mitochondria and REM the push-back response for awakening
2023, Neurobiology of Sleep and Circadian Rhythms
The Unified Theory suggests that sleep is a process that developed in eukaryotic animals from a relationship with an endosymbiotic bacterium. Over evolutionary time the bacterium evolved into the modern mitochondrion that continues to exert an effect on sleep patterns, e.g. the bacterium Wolbachia establishes an endosymbiotic relationship with Drosophila and many other species of insects and is able to change the host's behaviour by making it sleep. The hypothesis is supported by other host-parasite relationships, e.g., Trypanosoma brucei which causes day-time sleepiness and night-time insomnia in humans and cattle. For eukaryotes such as Monocercomonoids that don't contain mitochondria we find no evidence of them sleeping.
Mitochondria produce the neurotransmitter gamma aminobutyric acid (GABA), and ornithine a precursor of the neurotransmitter GABA, together with substances such as 3,4dihydroxy phenylalanine (DOPA) a precursor for the neurotransmitter dopamine: These substances have been shown to affect the sleep/wake cycles in animals such as Drosophilia and Hydra.
Eukaryote animals have traded the very positive side of having mitochondria providing aerobic respiration for them with the negative side of having to sleep. NREM (Quiet sleep) is the process endosymbionts have imposed upon their host eukaryotes and REM (Active sleep) is the push-back adaptation of eukaryotes with brains, returning to wakefulness.
The functions of sleep
2023, Encyclopedia of Sleep and Circadian Rhythms: Volume 1-6, Second Edition
The function or functions of sleep are not known, but it is likely they are principally for the brain. Physiology of organs apart from the nervous system is very similar in quiet wake and sleep, but the activity of the brain is very different between sleep and wake and extremely different between the two sleep states. Critically the brain must be taken off-line to accomplish sleep functions putting the individual at great risk. Several hypotheses of sleep function are being investigated and are discussed in this review. They include restoration of cerebral energy reserves, neuroplasticity and synaptic downscaling, memory consolidation, and glymphatic clearance of metabolic wastes. Rest states are virtually ubiquitous among animals, but we don't know if they or any of their functions are homologous with mammalian and avian sleep. Evolution may have added species specific functions to rest or sleep states, for example hibernation as an extension of ubiquitous mammalian sleep. So, there may be primitive/common functions of rest/sleep and derived functions. A critical question to ask of any hypothetical sleep function is why the brain has to be taken off-line to accomplish that function. Putative sleep functions described by different hypotheses may be synergistic and linked. The functions of NREM and REM sleep are most likely different, but could be related and interdependent in a homeostatic relationship.
Sleep in aquatic species
2023, Encyclopedia of Sleep and Circadian Rhythms: Volume 1-6, Second Edition
Fully aquatic cetaceans can sleep while in motion with only one eye closed at a time. They display a unique form of sleep called unihemispheric slow-wave sleep and show no apparent indications of rapid eye movement (REM). Semiaquatic mammals can sleep both on land and in water and display two different sleep patterns. Sleep in the first group (true seals and walrus) is largely not different from that seen in terrestrial mammals, except for long apneas displayed both on land and in water. Sleep in others (e.g., fur seals) is similar to the sleep of terrestrial mammals while on land and to the sleep of cetaceans while in water.
Cyclic alternation of quiet and active sleep states in the octopus
2021, iScience
Previous observations suggest the existence of ‘Active sleep’ in cephalopods. To investigate in detail the behavioral structure of cephalopod sleep, we video-recorded four adult specimens of Octopus insularis and quantified their distinct states and transitions. Changes in skin color and texture and movements of eyes and mantle were assessed using automated image processing tools, and arousal threshold was measured using sensory stimulation. Two distinct states unresponsive to stimulation occurred in tandem. The first was a ‘Quiet sleep’ state with uniformly pale skin, closed pupils, and long episode durations (median 415.2 s). The second was an ‘Active sleep’ state with dynamic skin patterns of color and texture, rapid eye movements, and short episode durations (median 40.8 s). ‘Active sleep’ was periodic (60% of recurrences between 26 and 39 min) and occurred mostly after ‘Quiet sleep’ (82% of transitions). These results suggest that cephalopods have an ultradian sleep cycle analogous to that of amniotes.
Sleep in Aquatic Mammals
2019, Handbook of Behavioral Neuroscience
Citation Excerpt :
The remaining time was occupied by episodes of both hemispheres displaying either (1) different forms of EEG synchronization (high-voltage EEG of maximal amplitude in one hemisphere and low-voltage EEG in the other) or (2) low-voltage EEG in both hemispheres; these states represent asymmetrical SWS (ASWS, 4%–15% of the total SWS time in different animals) or low-voltage bilateral SWS (BSWS, 7%–22%), respectively. High-voltage BSWS was never recorded in studied cetaceans under normal conditions (Lyamin, Manger, et al., 2008; Mukhametov, 1987; Mukhametov et al., 1997; Mukhametov & Polyakova, 1981), except for instances of several seconds of BSWS in a beluga (< 0.2% of TST; Lyamin, Mukhametov, Siegel, et al., 2002). In bottlenose dolphins, uninterrupted episodes of USWS lasted 4–132 min (on average 42 + 2 min), and the number of episodes ranged between 2 and 12 per day (5 + 1; Mukhametov et al., 1997, Lyamin, Mukhametov, & Siegel, 2004).
The sleep of aquatic mammals is different from sleep in terrestrial mammals. These differences are determined by physical properties of the aquatic and terrestrial environments. Dolphins and porpoises (cetaceans) have only one sleeplike state, called unihemispheric slow-wave sleep (USWS). It has been suggested that USWS allows vigilance and motion and facilitates breathing controlled by the waking hemisphere. Semiaquatic pinnipeds can sleep both on land and in water. The pattern of sleep in fur seals and sea lions (Otariidae) is similar to that in terrestrial mammals when they are on land but similar to the sleep in cetaceans when they are in water. Sleep in “true seals” (Phocidae) and in the walruses (the only representative of the Odobenidae family) is similar to that in terrestrial mammals both on land and in water, with the exception of long apneas, which allow them to sleep in water at depth and survive predation and harsh freezing conditions.
Silent porpoise: potential sleeping behaviour identified in wild harbour porpoises
2017, Animal Behaviour
All animals sleep and it is essential for maintaining optimal brain function. However, cetaceans engage in the unusual practice of unihemispherical sleep, where only half of their brain sleeps at a time, due to their constant need for movement and breathing. Most studies of sleep in cetaceans have occurred in captivity. However, tagging devices have now developed to the point where the data collected from wild animals can be assessed against published criteria for defining sleep behaviourally. Seven acoustic and behavioural data loggers were deployed on harbour porpoises, Phocoena phocoena, in Danish waters between May 2010 and August 2011 and stayed on the animals between 53 and 72 h, recording 1884 to 2755 valid dives per animal. Parabolic dives with significantly reduced bioacoustic activity and a stereotyped behavioural pattern were identified as potential sleeping periods. The recordings for nearly half of the parabolic dives were found to contain no vocalization (echolocation clicks), significantly more than other dive types. Of the remaining parabolic dives, the click rate was, when normalized to their individual means, also significantly lower than detected in other dive types. Additionally, parabolic dives were shallow compared to all other dive types, and found to have a stereotypic low-energy profile. They were also found to contain fewer rolls and incorporate a lower vertical descent rate than most other dive types. If the data are representative, harbour porpoises spend a small, but meaningful amount of their diving time engaged in parabolic dives and thus potentially sleeping. All animals have a fundamental need for undisturbed sleep. These quiet periods thus need to be considered in studies of anthropogenic effects, but also those employing passive acoustic monitoring techniques, as well as in efforts to reduce incidental bycatch in fisheries, given the associated periods of reduced environmental awareness.

View all citing articles on Scopus

View full text

Article preview

Behavioural Brain Research

Abstract

Section snippets

Acknowledgements

References (17)

Unilateral EEG activation during sleep in the cape fur seal, Arctocephalus pusillus

Neurosci. Lett.

Unihemispheric slow-wave sleep in the Amazonian dolphin, Inia geoffrensis

Neurosci. Lett.

Interhemispheric asymmetry of the electroencephalographic sleep patterns in dolphins

Brain Res.

Facultative control of avian unihemispheric sleep under the risk of predation

Behav. Brain Res.

Behavioral, neurological and evolutionary perspectives on unihemispheric sleep

Neurosci. Biobehav. Rev.

Behavioral aspects of sleep in pacific white-sided dolphins (Lagenorhynchus obliquidens, Gill 1866)

Mar. Mamm. Sci.

Animals in aquatic environments: adaptation of mammals to the ocean

Cited by (80)

The unified theory of sleep: Eukaryotes endosymbiotic relationship with mitochondria and REM the push-back response for awakening

The functions of sleep

Sleep in aquatic species

Cyclic alternation of quiet and active sleep states in the octopus

Sleep in Aquatic Mammals

Silent porpoise: potential sleeping behaviour identified in wild harbour porpoises

Research reportUnihemispheric slow wave sleep and the state of the eyes in a white whale

Abstract

Section snippets

Acknowledgements

Neurosci. Lett.

Neurosci. Lett.

Brain Res.

Behav. Brain Res.

Neurosci. Biobehav. Rev.

Behavioral aspects of sleep in pacific white-sided dolphins (Lagenorhynchus obliquidens, Gill 1866)

Mar. Mamm. Sci.

Animals in aquatic environments: adaptation of mammals to the ocean

Research report
Unihemispheric slow wave sleep and the state of the eyes in a white whale