Monoamine Release during Unihemispheric Sleep and Unihemispheric Waking in the Fur Seal

Lyamin, Oleg I.; Lapierre, Jennifer L.; Kosenko, Peter O.; Kodama, Tohru; Bhagwandin, Adhil; Korneva, Svetlana M.; Peever, John H.; Mukhametov, L. M.; Siegel, Jerome M.

doi:10.5665/sleep.5540

Cited by 37 publications

(18 citation statements)

References 38 publications

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“…As we showed in a prior study [8], the interhemispheric EEG asymmetry during SWS in fur seals is maximally expressed in the range of 1.2–4.0 Hz. It is also present in other frequencies (e.g., 4.0–16.0 Hz) but it is less pronounced.…”

Section: Methodssupporting

confidence: 60%

Eye state asymmetry during aquatic unihemispheric slow wave sleep in northern fur seals (Callorhinus ursinus)

et al. 2019

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Unihemispheric slow wave sleep (USWS) is a unique form of sleep in which one brain hemisphere maintains low voltage electrical activity indicative of waking while the opposite exhibits slow wave electrical activity indicative of sleep. USWS is present in several marine mammals and in some species of birds. One proposed biological function of USWS is to enable the animal to monitor the environment to detect predators or conspecifics. While asymmetrical eye state was often observed during behavioral sleep in birds and marine mammals, electrophysiological (electroencephalogram, EEG) correlates between the asymmetry of eye state and EEG of two cortical hemispheres have not been reliably established. This study examined the association between eye state and EEG activity during aquatic sleep in two subadult northern fur seals ( Callorhinus ursinus) , taking advantage of the simultaneous visibility of both eyes when the seals were in the prone position. We found that during USWS the eye contralateral to the sleeping hemisphere was closed on average 99.4±0.1% of the recording time. The eye contralateral to the waking hemisphere opened briefly for on average 1.9±0.1 sec with a rate of 8.2±1.0 per min. This eye was open on average 24.8±2.5% of the USWS time and it was closed no longer than 3 sec, on average 39.4±5.6% of the time. These data indicate that fur seals sleep in seawater by having intermittent visual monitoring. Our findings document the extent of visual monitoring of both eyes during USWS and support the idea that USWS allows intermittent visual vigilance. Thus, USWS serves two functions in the fur seal, facilitating movement and visual vigilance, which may also be the case in cetaceans.

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Section: Methodssupporting

confidence: 60%

Eye state asymmetry during aquatic unihemispheric slow wave sleep in northern fur seals (Callorhinus ursinus)

et al. 2019

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“…Serotonin, norepinephrine, and histamine release is not lateralized during USWS in fur seals. 132 , 160 However, acetylcholine release is lateralized during USWS 131 of fur seals, being greater in the hemisphere showing low-voltage EEG pattern (quiet waking). 131 Perhaps, the asymmetrical release of acetycholine plays a role in the temporary unihemispheric awakening in fur seals.…”

Section: Unihemispheric Sleep and Neural And Neurochemical Mechanismsmentioning

confidence: 99%

Unihemispheric sleep and asymmetrical sleep: behavioral, neurophysiological, and functional perspectives

Mascetti

2016

NSS

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Sleep is a behavior characterized by a typical body posture, both eyes’ closure, raised sensory threshold, distinctive electrographic signs, and a marked decrease of motor activity. In addition, sleep is a periodically necessary behavior and therefore, in the majority of animals, it involves the whole brain and body. However, certain marine mammals and species of birds show a different sleep behavior, in which one cerebral hemisphere sleeps while the other is awake. In dolphins, eared seals, and manatees, unihemispheric sleep allows them to have the benefits of sleep, breathing, thermoregulation, and vigilance. In birds, antipredation vigilance is the main function of unihemispheric sleep, but in domestic chicks, it is also associated with brain lateralization or dominance in the control of behavior. Compared to bihemispheric sleep, unihemispheric sleep would mean a reduction of the time spent sleeping and of the associated recovery processes. However, the behavior and health of aquatic mammals and birds does not seem at all impaired by the reduction of sleep. The neural mechanisms of unihemispheric sleep are unknown, but assuming that the neural structures involved in sleep in cetaceans, seals, and birds are similar to those of terrestrial mammals, it is suggested that they involve the interaction of structures of the hypothalamus, basal forebrain, and brain stem. The neural mechanisms promoting wakefulness dominate one side of the brain, while those promoting sleep predominates the other side. For cetaceans, unihemispheric sleep is the only way to sleep, while in seals and birds, unihemispheric sleep events are intermingled with bihemispheric and rapid eye movement sleep events. Electroencephalogram hemispheric asymmetries are also reported during bihemispheric sleep, at awakening, and at sleep onset, as well as being associated with a use-dependent process (local sleep).

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“…Northern fur seals (Callorhinus ursinus) show unihemispheric sleep preferentially while sleeping in the water (Lyamin et al, 2017). Acetylcholine release was found to be lateralized and tightly linked to the hemisphere that was awake, while histamine, serotonin, and noradrenaline were found to be synchronously released from both the awake and asleep hemispheres (Lapierre et al, 2013;Lapierre et al, 2007;Lyamin et al, 2016). These findings suggest that acetylcholine is responsible for unihemispheric EEG activation, and future studies modulating the activity of cholinergic neurons would provide causal evidence.…”

Section: Motivational Regulation Of Sleep/wake Statesmentioning

confidence: 79%

Neuronal Mechanisms for Sleep/Wake Regulation and Modulatory Drive

Eban-Rothschild

Appelbaum

Lecea

2017

Neuropsychopharmacol.

190

118

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Humans have been fascinated by sleep for millennia. After almost a century of scientific interrogation, significant progress has been made in understanding the neuronal regulation and functions of sleep. The application of new methods in neuroscience that enable the analysis of genetically defined neuronal circuits with unprecedented specificity and precision has been paramount in this endeavor. In this review, we first discuss electrophysiological and behavioral features of sleep/wake states and the principal neuronal populations involved in their regulation. Next, we describe the main modulatory drives of sleep and wakefulness, including homeostatic, circadian, and motivational processes. Finally, we describe a revised integrative model for sleep/wake regulation.

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Monoamine Release during Unihemispheric Sleep and Unihemispheric Waking in the Fur Seal

Abstract: A commentary on this article appears in this issue on page 491.

Cited by 37 publications

References 38 publications

Eye state asymmetry during aquatic unihemispheric slow wave sleep in northern fur seals (Callorhinus ursinus)

Eye state asymmetry during aquatic unihemispheric slow wave sleep in northern fur seals (Callorhinus ursinus)

Unihemispheric sleep and asymmetrical sleep: behavioral, neurophysiological, and functional perspectives

Neuronal Mechanisms for Sleep/Wake Regulation and Modulatory Drive

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