Downregulation of sensory information during sleep

By Iulia-Teodora Vermesan 

Across the animal kingdom, there are several behavioural characteristics that help define sleep. These include a reversible state of immobility with increased arousal thresholds (which distinguishes sleep from coma or hibernation), as well as protected place preference and following specific rituals before sleeping. Circadian regulation ensures following a 24-hour rhythm — provided there are constant conditions — which is associated with a higher risk of “sleep rebound” (Allada & Siegel, 2008). The purpose of sleep can be and still is widely debated, but starting from the previously mentioned characteristics, animals do sleep. 

During normal sleep, there are oscillatory events which fluctuate between quiet and more active periods. These allow sleep arousals to occur and are associated with short bursts of reactivation of organs. These allow the animal to change their body positions and in case of perception of harmful events, to become fully awake (Klasser, Almoznino & Fortuna, 2018).

During wakefulness, cholinergic and monoaminergic neurons in the lateral hypothalamus discharge their neurotransmitters to promote cortical arousal. On the other hand, during sleep, neurons of the ventrolateral preoptic nucleus (VLPO) signal via γ-aminobutyric acid (GABA) and galanin by inhibiting the monoaminergic arousal system. The mechanism of regulating the effects of these neurons is described as a bistable “flip-flop”: monoaminergic neurons firing intensively during wakefulness inhibits the VLPO neurons, and the reverse blocks the discharge of monoamine nuclei during sleep. It is worth noting that if either side of the bistable system is affected in any way, both sleep and wakefulness are affected. Orexin neurons in the hypothalamus sustain the activity of wake-promoting neurons and stabilize the switch between the sleep-wake system (Schwartz and Roth, 2008). 

While sleep is associated with specific synchronized oscillations between the brain hemispheres, EEG studies show that some birds and marine animals undergo unilateral hemispheric sleep, which is connected to a protective mechanism due to the increased vulnerability during sleep. Unihemispheric sleep is associated with asymmetric eye closure as well as wave patterns of mixed amplitudes and frequencies and lack of rapid eye movement sleep (REM). For example, in dolphins, during wakefulness a typical bilateral EEG pattern is observed, while the remaining period involves slow wave sleep (SWS) alternating between hemispheres. Another phenotype of this pattern of sleep is the closure of the eye contralateral to the sleeping hemisphere as well as higher arousal thresholds in the hemisphere contralateral to the one performing SWS. Overall, unihemispheric slow wave sleep (USWS) allows continuous monitoring of the environment for predators. It is noteworthy that although to a lesser extent, this sleep pattern is also observed when animals are studied in laboratory, artificial environments. In their natural habitats, where animals are exposed to increased risk, they are more vigilant to external stimuli (Mascetti 2016). 

It is reasonable to think that in USWS the wake-promoting mechanism prevails on one side of the brain, while inducing sleep would prevail on the other side. Discharge of noradrenergic neurons in mammals is associated with wakefulness and to some extent in SWS, but their activity is completely abolished during REM sleep. In cetaceans, the need to swim continuously emphasizes the importance of controlling the muscle tone, continuous discharge of noradrenaline is expected since maintenance of the muscle tone is permanently vital for them — asleep or not. Along with the lack of REM sleep, noradrenaline production and increased glial cells help cetaceans overcome continuous breathing and swimming during sleep. While not much is known about the neuronal groups controlling the sleep in cetaceans, the hemispheric independence might be reinforced by the anatomical links between the two hemispheres. That is, by looking at the commissural systems of the central nervous system and how these differ in animals performing USWS versus bihemispheric slow wave sleep (BSWS). By looking at the anterior commissure, the corpus callosum and the posterior commissure, it is noticeable that all are reduced in comparison to the total brain size in cetaceans. This might be correlated to a lower density of neurons connecting the hemispheres, thus contributing to hemisphere independence (Lyamin et al., 2008). Vyazovskiy et al. showed that reduced or absent corpus callosum in cats produces similar findings to EEG studies in cetaceans. This suggests that synchronization between the hemispheres in sleep and waking is mediated to a large extent by the connections established between the hemispheres. 

A similar phenomenon has been observed in humans; that is the “first night effect” (FNE). Rather than a sleep disturbance, FNE is a surveillance system manifested in one hemisphere being more vigilant than the other. This phenomenon is often experienced when we sleep in a novel environment. Prolonged sleep-onset latency, reduced arousal thresholds, decreased delta activity which is associated with SWS are the usual phenotypes of FNE (Tamaki & Sasaki, 2019). Some degree of unihemispheric sleep is observed: the right hemisphere follows normal SWS, while the left one is partially alert.

In bihemispheric sleep, the dynamics between sleep and wakefulness are characterized by both high and low degrees of synchronization. Switching between sleep stages is on one hand a stochastic process, but it is regulated by the circuitry forming the bistable flip-flop switches (Ramlow et al., 2019). In animals associated with USWS, it might be enough to start desynchronizing the stages of the hemispheres once: since the connections between them are greatly reduced, the regulatory mechanisms could exert a greatly reduced impact. This could also be a mechanism of adaptability to the needs of the animal, specifically conferring increased vigilance during vulnerable times by structural interhemispheric separation. In humans, symmetry breaking triggered by sleeping in a stressful environment could explain why hemispheres engage in different dynamical states leading to one being in an alert state, while the other is sleeping.

References:

Allada, R. & Siegel, J.M. (2008) Unearthing the phylogenetic roots of sleep. Current biology: CB. [Online] 18 (15), R670–R679. Available from: doi:10.1016/j.cub.2008.06.033.

Klasser, G.D., Almoznino, G. & Fortuna, G. (2018) Sleep and Orofacial Pain. Dental Clinics of North America. [Online] 62 (4), 629–656. Available from: doi:10.1016/j.cden.2018.06.005.

Lyamin, O.I., Manger, P.R., Ridgway, S.H., Mukhametov, L.M., et al. (2008) Cetacean sleep: an unusual form of mammalian sleep. Neuroscience and Biobehavioral Reviews. [Online] 32 (8), 1451–1484. Available from: doi:10.1016/j.neubiorev.2008.05.023.

Mascetti, G.G. (2016) Unihemispheric sleep and asymmetrical sleep: behavioral, neurophysiological, and functional perspectives. Nature and Science of Sleep. [Online] 8, 221–238. Available from: doi:10.2147/NSS.S71970.

Ramlow, L., Sawicki, J., Zakharova, A., Hlinka, J., et al. (2019) Partial synchronization in empirical brain networks as a model for unihemispheric sleep. EPL (Europhysics Letters). [Online] 126 (5), 50007. Available from: doi:10.1209/0295-5075/126/50007.

Schwartz, J.R.L. & Roth, T. (2008) Neurophysiology of Sleep and Wakefulness: Basic Science and Clinical Implications. Current Neuropharmacology. [Online] 6 (4), 367–378. Available from: doi:10.2174/157015908787386050.

Tamaki, M. & Sasaki, Y. (2019) Surveillance During REM Sleep for the First-Night Effect. Frontiers in Neuroscience. [Online] 13, 1161. Available from: doi:10.3389/fnins.2019.01161.

Vyazovskiy, V., Achermann, P., Borbély, A.A. & Tobler, I. (2004) Interhemispheric coherence of the sleep electroencephalogram in mice with congenital callosal dysgenesis. Neuroscience. [Online] 124 (2), 481–488. Available from: doi:10.1016/j.neuroscience.2003.12.018.

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