Purpose of review

I review the current status of the hypothesis that sleep is critically involved in memory consolidation and conclude that there are major methodological problems with the studies used to support this hypothesis.

Recent findings

Memory consolidation is similar in quiet waking and sleep (Humiston GB, Tucker MA, Summer T, Wamsley EJ. Sci Rep 18;9(1):19345, 2019), and suppression of REM sleep for long periods is compatible with learning and highly adaptive behavior (Lyamin OI, Korneva SM, Obukhova ED, Mukhametov LM, Siegel JM. Dokl Biol Sci 463:211-4, 2015; Lyamin OI, Kosenko PO, Korneva SM, Vyssotski AL, Mukhametov LM, Siegel JM. Current Biology 28(12):2000-5, 2018); despite their considerable abilities to navigate and remember, African elephants have very small amount of sleep, and learning interference effects have not been adequately controlled for in studies purporting to show sleep-dependent memory consolidation (Sosic-Vasic Z, Hille K, Kroner J, Spitzer M, Kornmeier J. Frontiers in psychology 9:82, 2018; Yonelinas AP, Ranganath C, Ekstrom AD, Wiltgen BJ. Nat Rev Neurosci 20(6):364-75, 2019).

Summary

Memory consolidation clearly occurs in both sleep and waking. Whether, and the extent to which, consolidation might differ in these two states has not been conclusively determined.

Why do we sleep? The sleep patterns and mechanisms that occur throughout development may give us a clue.

Prospective epidemiological studies in industrial societies indicate that 7 h of sleep per night in people aged 18 years or older is optimum, with higher and lower amounts of sleep predicting a shorter lifespan. Humans living a hunter-gatherer lifestyle (eg, tribal groups) sleep for 6-8 h per night, with the longest sleep durations in winter. The prevalence of insomnia in hunter-gatherer populations is low (around 2%) compared with the prevalence of insomnia in industrial societies (around 10-30%). Sleep deprivation studies, which are done to gain insights into sleep function, are often confounded by the effects of stress. Consideration of the duration of spontaneous daily sleep across species of mammals, which ranges from 2 h to 20 h, can provide important insights into sleep function without the stress of deprivation. Sleep duration is not related to brain size or cognitive ability. Rather, sleep duration across species is associated with their ecological niche and feeding requirements, indicating a role for wake-sleep balance in food acquisition and energy conservation. Brain temperature drops from waking levels during non-rapid eye movement (non-REM) sleep and rises during REM sleep. Average daily REM sleep time of homeotherm orders is negatively correlated with average body and brain temperature, with the largest amount of REM sleep in egg laying (monotreme) mammals, moderate amounts in pouched (marsupial) mammals, lower amounts in placental mammals, and the lowest amounts in birds. REM sleep might, therefore, have a key role in the regulation of temperature and metabolism of the brain during sleep and in the facilitation of alert awakening.

Sleep can be seen as an environmentally determined, adaptive behavior.

Female hypocretin knockout (Hcrt KO) mice have increased body weight despite decreased food intake compared to wild type (WT) mice. In order to understand the nature of the increased body weight, we carried out a detailed study of Hcrt KO and WT, male, and female mice. Female KO mice showed consistently higher body weight than WT mice, from 4 to 20 months (20-60%). Fat, muscle, and free fluid levels were all significantly higher in adult (7-9 months) as well as old (18-20 months) female KO mice compared to age-matched WT mice. Old male KO mice showed significantly higher fat content (150%) compared to age-matched WT mice, but no significant change in body weight. Respiratory quotient (-19%) and metabolic rates (-14%) were significantly lower in KO mice compared to WT mice, regardless of gender or age. Female KO mice had significantly higher serum leptin levels (191%) than WT mice at 18-20 months, but no difference between male mice were observed. Conversely, insulin resistance was significantly higher in both male (73%) and female (93%) KO mice compared to age- and sex-matched WT mice. We conclude that absence of the Hcrt peptide has gender-specific effects. In contrast, Hcrt-ataxin mice and human narcoleptics, with loss of the whole Hcrt cell, show weight gain in both sexes.

We previously showed that total sleep deprivation increased antioxidant responses in several rat brain regions. We also reported that chronic hypoxia enhanced antioxidant responses and increased oxidative stress in rat cerebellum and pons, relative to normoxic conditions. In the current study, we examined the interaction between these two parameters (sleep and hypoxia). We exposed rats to total sleep deprivation under sustained hypoxia (SDSH) and compared changes in antioxidant responses and oxidative stress markers in the neocortex, hippocampus, brainstem, and cerebellum to those in control animals left undisturbed under either sustained hypoxia (UCSH) or normoxia (UCN). We measured changes in total nitrite levels as an indicator of nitric oxide (NO) production, superoxide dismutase (SOD) activity and total glutathione (GSHt) levels as markers of antioxidant responses, and levels of thiobarbituric acid-reactive substances (TBARS) and protein carbonyls as signs of lipid and protein oxidation products, respectively. We found that acute (6h) SDSH increased NO production in the hippocampus and increased GSHt levels in the neocortex, brainstem, and cerebellum while decreasing hippocampal lipid oxidation. Additionally, we observed increased hexokinase activity in the neocortex of SDSH rats compared to UCSH rats, suggesting that elevated glucose metabolism may be one potential source of the enhanced free radicals produced in this brain region. We conclude that short-term insomnia under hypoxia may serve as an adaptive response to prevent oxidative stress.

Optogenetic stimulation of the locus coeruleus noradrenergic neurons can increase wakefulness, and high-frequency stimulation decreases noradrenaline levels and produces loss of muscle tone similar to that seen in cataplexy.

The presence of dreams in human sleep, especially in REM sleep, and the detection of physiologically similar states in mammals has led many to ponder whether animals experience similar sleep mentation. Recent advances in our understanding of the anatomical and physiological correlates of sleep stages, and thus dreaming, allow a better understanding of the possibility of dream mentation in nonhuman mammals. Here, we explore the potential for dream mentation, in both non-REM and REM sleep across mammals. If we take a hard-stance, that dream mentation only occurs during REM sleep, we conclude that it is unlikely that monotremes, cetaceans, and otariid seals while at sea, have the potential to experience dream mentation. Atypical REM sleep in other species, such as African elephants and Arabian oryx, may alter their potential to experience REM dream mentation. Alternatively, evidence that dream mentation occurs during both non-REM and REM sleep, indicates that all mammals have the potential to experience dream mentation. This non-REM dream mentation may be different in the species where non-REM is atypical, such as during unihemispheric sleep in aquatic mammals (cetaceans, sirens, and Otariid seals). In both scenarios, the cetaceans are the least likely mammalian group to experience vivid dream mentation due to the morphophysiological independence of their cerebral hemispheres. The application of techniques revealing dream mentation in humans to other mammals, specifically those that exhibit unusual sleep states, may lead to advances in our understanding of the neural underpinnings of dreams and conscious experiences.

A new study presents evidence of sex-related sleep reduction in males of two marsupial mice species but not in females. The growing experimental data suggest that seasonal sleep reduction, linked to migrations and reproductive periods, is common among animals.