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

Abstract

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).

Integrity of Corpus Callosum Is Essential for the Cross-Hemispheric Propagation of Sleep Slow Waves: A High-Density EEG Study in Split-Brain Patients

“…However, since the cortical distribution of slow-wave origins was not systematically and significantly affected by the resection of the CC, the observed asymmetry could be entirely explained by the reduced cross-hemispheric slow-wave propagation. This observation is in line with previous evidence suggesting that the lack or resection of inter-hemispheric connections is not sufficient for the manifestation of unihemispheric sleep ( Berlucchi, 1966 ; Montplaisir et al, 1990 ; Nielsen et al, 1993 ), as naturally seen in some animal species, such as birds and cetaceans ( Rattenborg et al, 2000 ; Mascetti, 2016 ). On the other hand, the absence (as in birds) or small size (as in cetaceans; Tarpley and Ridgway, 1994 ) of the CC may prevent the cross-hemispheric spreading of sleep slow waves, and thus represent one fundamental prerequisite for unihemispheric sleep.…”

Local aspects of sleep and wakefulness

“…Similar unihemispheric sleep patterns have been observed in several species of whales, manatees, some seals as well as several birds [6,7]. Although unihemispheric sleep does not occur in humans, a recent study has shown that during the first night in a laboratory environment, the left hemisphere displays less SWA and is more reactive to external stimuli compared to the right hemisphere, potentially acting as a ‘night watch’ to monitor unfamiliar surroundings [8 • ].…”

Does the mind wander when the brain takes a break? Local sleep in wakefulness, attentional lapses and mind-wandering

“…Such regional aspects of sleep activity had already been observed in certain animal species (e.g. dolphins who can enter unihemispheric sleep, sleeping in one brain hemisphere at a time) (Mascetti, Gian Gastone, 2016;Rattenborg et al, 2019) and in sleep pathologies (Castelnovo et al, 2016;Dodet et al, 2015;Riedner et al, 2016;Terzaghi et al, 2009). However, in the past few years, local sleep involving changes in sleep depth within NREM sleep has been robustly observed in individuals without sleep disorders (Huber et al, 2004;Nir et al, 2011).…”