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Sleep and the Adolescent Brain
Journal Pre-proof Sleep and the Adolescent Brain Chiara EG Fontanellaz-Castiglione, Andjela Markovic, Leila Tarokh
PII:
S2468-8673(20)30014-6
DOI:
https://doi.org/10.1016/j.cophys.2020.01.008
Reference:
COPHYS 280
To appear in:
Current Opinion in Physiology
Please cite this article as: Fontanellaz-Castiglione CE, Markovic A, Tarokh L, Sleep and the Adolescent Brain, Current Opinion in Physiology (2020), doi: https://doi.org/10.1016/j.cophys.2020.01.008
This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2019 Published by Elsevier.
Sleep and the Adolescent Brain Chiara E. G. Fontanellaz-Castiglione1, Andjela Markovic1, and Leila Tarokh1* [email protected] (1)
University Hospital of Child and Adolescent Psychiatry and Psychotherapy, University of Bern, Bern, Switzerland
*
Corresponding author: Leila Tarokh, PhD, University Hospital of Child and Adolescent Psychiatry and Psychotherapy, University of Bern, Bolligenstrasse 111, Haus A, 3000 Bern
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Abstract Adolescence is a period of significant brain maturation, and cognitive and emotional development. Interacting and reflecting with these processes is sleep. In this review we synthesize the current and emerging literature on the role of adolescent sleep in brain maturation. On the one hand, studies in animals and humans suggest that sleep actively supports neurodevelopment during the adolescent period, although mechanisms have yet to be elucidated. On the other hand, over the last decade the value of sleep as a time to measure brain activity and study the brain maturational process has been appreciated. The transition from childhood to adolescence also heralds changes to sleep behavior, with sleep duration shortening across the adolescent period. This decline has important implications for adolescent cognitive and mental health, although the long-term consequences on adolescent brain maturation remain unknown.
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Keywords: Sleep, Adolescence, Brain, Plasticity
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Introduction Sleep is vital to our wellbeing, although its functions have not yet been fully understood. Given that humans spend a third of the day sleeping, writing in 1971, Allan Rechtschaffen astutely observed, “If sleep doesn’t serve an absolutely vital function, it is the greatest mistake evolution ever made” (1). Sleep duration is longest during development in animals and humans, suggesting that sleep may play an even more integral function during maturation. While the role(s) of sleep during development remains elusive, one hypothesis is that in addition to the daily neuronal maintenance that sleep performs in the adult brain, during development sleep actively supports brain maturation (2) (3, 4). Therefore, an adequate amount of sleep may be especially central during periods of rapid brain maturation. This review synthesizes the literature about the role of sleep in adolescent brain development and provides a summary of changes to sleep physiology during adolescence (for a definition of adolescence, see Box 1). Finally, the changes to sleep physiology are discussed within the behavioral context of adolescent sleep and implications for adolescent well-being are discussed. Sleep: Does it have a unique role regarding the developing adolescent brain? The evidence is now overwhelming that sleep need does not change across adolescent development. A series of elegant studies allowing ample time in bed showed that given the opportunity, human adolescents will sleep an average of 9.3 hours (5, 6). Interestingly, studies in adolescent mice show a similar pattern of stable sleep duration across the adolescent period (P19 to P111), suggesting that the biological processes that sleep
supports during this developmental phase may be preserved across species (7). One such process may be brain plasticity, which is supported by sleep and is higher during development than other life phases (reviewed in (8)). Another may be the active shaping of brain networks through synaptic pruning. Both humans and mice undergo a period of synaptic pruning following puberty (see Box 1 for details), the purpose of which is the trimming back of weak synaptic connections, while highly used connections are strengthened resulting in an increase in the efficiency of network processing (9). A study using two-photon microscopy to study cortical spines in adolescent mice (between ages P23 and P44), found a net decline in spines across several hours (6-8 hours) of sleep, suggesting that sleep may play an active role in synaptic pruning during this developmental phase (10).
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More indirect evidence collected in humans also suggests that sleep actively contributes to shaping teenagers’ brains. For example, a correlation between shorter total time in bed on weekdays, as well as later bedtime on weekends with reduced grey matter volumes in frontal, anterior cingulate, precuneus cortex regions (11), hippocampal volume (12) and white matter integrity (13) has been found. Although, other factors such as genes, may explain the correlation between sleep duration and brain volume, these studies provide some evidence that sleep may shape the human brain during development.
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NREM Sleep Neurophysiology During Adolescence In addition to guiding brain maturation, sleep is often seen as a window to the developing brain, offering the opportunity to examine brain structure and function. Two oscillations during non-rapid eye movement (NREM) sleep have been the primary focus of investigation: slow waves and spindles. Slow waves are oscillations of low frequency (< 5 Hz) and high amplitude generated by both the neocortex and the thalamus (14). Sleep spindles, on the other hand, are waxing and waning oscillations in the frequency range between 11 and 16 Hz generated through thalamocortical loops (15).
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Across adolescence, sleep physiology as reflected in the sleep EEG undergoes dramatic changes. A rapid reduction in SWA of approximately 40% takes place (16-20) with the steepest decline around the age of 12.5 years for girls and 13.5 years for boys (18). This decline has been linked to the aforementioned synaptic pruning processes whereby fewer synapses result in less synchronized synaptic activity – the substrate of EEG amplitude (21). Therefore, the higher amount of SWA in the pre-pubertal brain may be due to greater number, more highly connected, and synchronous synapses in the immature brain. In addition to the reduction in SWA, the topographic distribution of SWA changes as reflected by a shift of the region exhibiting maximal SWA from posterior to anterior sites (22). A similar postero-anterior trajectory has been observed for cortical maturation (e.g., (23)) further suggesting that the adolescent decline in SWA may be a marker of brain maturation. This notion is supported by significant correlations between SWA and cortical gray matter volume as measured by means of magnetic resonance imaging (MRI) (24, 25). We note that the association between cortical gray matter volume and sleep EEG power has been found to also be significant for other NREM sleep EEG frequency bands (24), suggesting that synaptic pruning, which in turn results in reduced cortical grey matter volume, is reflected across frequency bands. To wit, a decline in the duration and amplitude of sleep spindles is also observed during adolescent development (26-28). Beyond simply reflecting a decline in cortical volume, the changes to SWA and spindles may also have implications for sleep itself. With regards to SWA, the synaptic homeostasis hypothesis (SHY) posits that slow waves achieve sleep dependent
recuperation through synaptic downscaling (29). According to this hypothesis, by the end of the waking day, synaptic strength in many neural circuits undergoes an increase due to continuous learning. Synaptic renormalization is needed to regulate net energy consumption via down-regulation of synaptic strength. Thus within a developmental context, SHY would posit that during adolescence, a period when the number of synapses is on the decline, less SWA is required to achieve the same amount of sleep dependent recuperation. Therefore the decline in SWA across adolescence may not just reflect a decline in synapses, but also be due to the diminished need for sleep recuperation as a result of less synaptic activity during the day.
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A further implication of the decline in SWA during adolescence is that sleep becomes lighter, since SWA is a marker of sleep depth. Indeed, with the onset of adolescence individuals report greater difficulty falling and staying asleep. Objective PSG data confirm this (30, 31). While increased sleep onset latency in humans has been attributed to a number of environmental and psychological factors (e.g., increases in anxiety), interestingly sleep latency also increases across adolescence in mice (P19 to P111), suggesting that the decline in sleep pressure due to the reduced number of synapses, may in part account for increased sleep onset latency (7). Similarly, sleep spindles have been proposed to serve a sleep protective function (32, 33) and the developmental decline of these oscillations may in part explain the increase in arousals or wake after sleep onset observed both in mice (7) and humans (34).
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Concurrent with changes in the amplitude of oscillatory activity during adolescence an increase in brain connectivity occurs during adolescence. During this period an increase in NREM sleep EEG coherence (35), a measure of brain connectivity based on the consistency of phase relationship between two signals (21), is seen. This increase has been associated with functional reorganization (36) and increased myelination (37) in adolescence – processes leading to more efficient and dynamic interactions between brain regions. Furthermore, the adolescent increase in NREM sleep EEG sigma coherence (associated with spindle coherence) is significantly correlated with improvement in cognitive performance (38), suggesting that increases in coherence are of functional significance.
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Further indication of brain rewiring may be the observed linear increase in spindle frequency (39, 40). Although the mechanism resulting in the increase in spindle frequency is unclear, one hypothesis is that the decrease of slow wave sleep across adolescence results in a decline in thalamic hyperpolarization (40). Since spindle frequency is inversely related to the duration and degree of thalamocortical hyperpolarization (41), the adolescent decline in slow wave sleep results in an increase in spindle frequency. An alternate hypothesis is that the increase in spindle frequency reflects increased efficiency and strength of existing brain circuits through axonal myelination (42). To summarize, both slow waves and sleep spindles undergo declines in amplitude across adolescent development, while sleep spindles increase in frequency and density (43), and decrease in duration (43). While, the decline in spindle amplitude and increase in spindle frequency likely reflects changes in cortical grey and white matter volume respectively, the mechanism(s) underlying the changes to spindle duration and density are less clear. Furthermore, whether slow waves and spindles serve differing functions during adolescent development as compared to adulthood is unclear due to the scarcity of studies comparing the role of these oscillations in adults to adolescents (44).
Despite these changes, some sleep EEG features (for example, the morphology of the power spectra (45) and fast spindle duration (46)) demonstrate trait-like behavior, suggesting a potentially strong genetic contribution. Indeed, recent research has provided evidence for genetic determination of sleep EEG power (47) and topography (48) in adolescence. These studies find that over posterior regions, 80-90% of the observed variance in SWA and sigma power is explained by genetic factors, while over anterior regions the majority of variance is explained by environmental factors (47). These findings indicate a regional variation in genetic contribution to sleep EEG power and imply that the factors shaping the sleep EEG depend on frequency and, thus, might reflect differential mechanisms of brain function.
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REM Sleep During Adolescence: Because the emphasis of recent research has been on the oscillations of NREM sleep, less is known about the role of REM sleep in adolescent development. What is known is that some of the adolescent changes to NREM sleep, such as the decline in power (26, 27) (49) and increase in coherence (35), are mirrored in REM sleep. The state independence of these changes suggests the maturation of brain anatomy summarized above underlie this decline.
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Most of the research to date has focused on changes to REM sleep architecture across the adolescent period. Under sleep-satiated conditions (i.e., sufficient sleep prior to PSG measurement), the duration of REM sleep does not change across the adolescent period (26, 27). On the other hand, a recent study has shown that when sleep duration is experimentally truncated, the reduction in REM sleep duration is proportionally greater than NREM sleep (50). In this study, a decrease of both NREM and REM sleep upon reducing sleep duration from 10 to 7 hours in 10- to 14-year-olds was observed, however, the reduction in REM sleep was proportionally greater than that of NREM sleep suggesting that under sleep deprived condition NREM sleep may have biological priority (50). Further evidence of this is the first REM sleep episode may be “skipped” (27, 51) in some adolescents, likely due to high NREM sleep pressure at this age. To summarize, there is a significant knowledge gap in our understanding of the role of REM sleep in adolescent development. Given the importance of REM sleep in infant brain maturation (2), understanding the function of REM sleep in adolescence is of the utmost importance.
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Sleep behavior during adolescence and its impact on daily life Despite the stable “need” for sleep across adolescence and the importance of sleep in adolescent brain development, most adolescents do not obtain an adequate amount of sleep (reviewed in (52)). This sleep deficit is largely due to an interaction of biological systems with environmental factors, which push and pull in opposite directions. The circadian system pushes adolescents towards later bedtimes while the decline in homeostatic sleep pressure described above allows for adolescents to stay up later than their younger counterparts (reviewed in (53)). Environmental factors pushing sleep later include newly gained bedtime autonomy (e.g., (53, 54)), homework (e.g., (55)) the use of electronic devices (e.g. cellphone, internet) (e.g., (54, 56, 57)) and social media use (57). Pulling rise times towards the early morning hours is school start time, which does not change across the adolescent period (58) (59). This push and pull leads to chronic sleep deprivation in adolescents and to tired teenagers (52). Newer experimental and observational studies in adolescents have reported that multiple nights of sleep restriction, typical during adolescence, have a negative effect on various cognitive functions as well as mood (reviewed in (52)). For example, insufficient sleep has a negative impact on various complex mental processes and cognitive abilities as executive function (Lo, Ong, Leong, Gooley, & Chee, 2016), cognitive flexibility (Tee, Gan,
Tan, & Chin, 2018), processing speed (Cohen-Zion, Shabi, Levy, Glasner, & Wiener, 2016; Lim, Lo, & Chee, 2017) working memory (Lo et al., 2016; Tee et al., 2018).and mental health (Bei, Manber, Allen, Trinder, & Wiley, 2017; Brand et al., 2019). Although the consequences of insufficient sleep in adolescents mirror those observed in adults, it is unclear whether they are more pronounced in adolescents as compared to adults. This knowledge gap is due to the dearth of studies measuring the same cognitive constructs in adults and adolescents. Furthermore, the long-term consequences of short sleep, which may have a stronger impact on the developing brain are unknown and should be addressed by future research.
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Conclusion Taken together, evidence is emerging that sleep actively supports brain development through the shaping of synaptic connections. Whether sleep also plays a role in establishing network connectivity has not yet been studied. Although preliminary evidence suggests changes in network connectivity across the course of a night of sleep in young children (60), whether such changes have long-term implication is unknown. What is clear, however, is that sleep supports manifold biological functions, many of them critical to healthy development.
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Acknowledgements The authors would like to acknowledge the following source of funding: Interfaculty Research Cooperation grant “Decoding Sleep: From Neurons to Health & Mind” from the University of Bern (to LT).
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Box 1: What and when is adolescence? In humans, adolescence is understood to be the stage of development that begins with the onset of physical maturation (puberty) and ends with gaining adult autonomy (e.g. driving license, independent living, financial self-responsibility, etc.) (61). However, the boundaries of adolescence are blurry and it is not a single event that signals its beginning or end. Nonetheless, based on these guidelines, the world health organization (WHO) defines human adolescence as the second decade of life (ages 10 to 19 years). In mice, adolescence typically encompasses the period from weaning (≈ P21) to sexual maturity (P37-48). In both humans and mice, adolescence is characterized by behavioral and biological hallmarks that make this period unique. Behaviorally, adolescence is accompanied by increased risktaking, novelty-seeking and peer-directed social interaction in both species. Biologically, a period of rapid synaptic pruning is seen, wherein the number of synaptic connections undergoes marked decline. Generally speaking in both species this pruning commences around the time of puberty and continues to the end of the adolescent period defined above. We note, however, nuances in this process, with certain brain regions beginning and ending the synaptic pruning phase at different times (e.g., (23)). For a thorough review of the brain and behavioral changes occurring in human and rodent adolescence see (62).
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PII:
S2468-8673(20)30014-6
DOI:
https://doi.org/10.1016/j.cophys.2020.01.008
Reference:
COPHYS 280
To appear in:
Current Opinion in Physiology
Please cite this article as: Fontanellaz-Castiglione CE, Markovic A, Tarokh L, Sleep and the Adolescent Brain, Current Opinion in Physiology (2020), doi: https://doi.org/10.1016/j.cophys.2020.01.008
This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2019 Published by Elsevier.
Sleep and the Adolescent Brain Chiara E. G. Fontanellaz-Castiglione1, Andjela Markovic1, and Leila Tarokh1* [email protected] (1)
University Hospital of Child and Adolescent Psychiatry and Psychotherapy, University of Bern, Bern, Switzerland
*
Corresponding author: Leila Tarokh, PhD, University Hospital of Child and Adolescent Psychiatry and Psychotherapy, University of Bern, Bolligenstrasse 111, Haus A, 3000 Bern
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Abstract Adolescence is a period of significant brain maturation, and cognitive and emotional development. Interacting and reflecting with these processes is sleep. In this review we synthesize the current and emerging literature on the role of adolescent sleep in brain maturation. On the one hand, studies in animals and humans suggest that sleep actively supports neurodevelopment during the adolescent period, although mechanisms have yet to be elucidated. On the other hand, over the last decade the value of sleep as a time to measure brain activity and study the brain maturational process has been appreciated. The transition from childhood to adolescence also heralds changes to sleep behavior, with sleep duration shortening across the adolescent period. This decline has important implications for adolescent cognitive and mental health, although the long-term consequences on adolescent brain maturation remain unknown.
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Keywords: Sleep, Adolescence, Brain, Plasticity
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Introduction Sleep is vital to our wellbeing, although its functions have not yet been fully understood. Given that humans spend a third of the day sleeping, writing in 1971, Allan Rechtschaffen astutely observed, “If sleep doesn’t serve an absolutely vital function, it is the greatest mistake evolution ever made” (1). Sleep duration is longest during development in animals and humans, suggesting that sleep may play an even more integral function during maturation. While the role(s) of sleep during development remains elusive, one hypothesis is that in addition to the daily neuronal maintenance that sleep performs in the adult brain, during development sleep actively supports brain maturation (2) (3, 4). Therefore, an adequate amount of sleep may be especially central during periods of rapid brain maturation. This review synthesizes the literature about the role of sleep in adolescent brain development and provides a summary of changes to sleep physiology during adolescence (for a definition of adolescence, see Box 1). Finally, the changes to sleep physiology are discussed within the behavioral context of adolescent sleep and implications for adolescent well-being are discussed. Sleep: Does it have a unique role regarding the developing adolescent brain? The evidence is now overwhelming that sleep need does not change across adolescent development. A series of elegant studies allowing ample time in bed showed that given the opportunity, human adolescents will sleep an average of 9.3 hours (5, 6). Interestingly, studies in adolescent mice show a similar pattern of stable sleep duration across the adolescent period (P19 to P111), suggesting that the biological processes that sleep
supports during this developmental phase may be preserved across species (7). One such process may be brain plasticity, which is supported by sleep and is higher during development than other life phases (reviewed in (8)). Another may be the active shaping of brain networks through synaptic pruning. Both humans and mice undergo a period of synaptic pruning following puberty (see Box 1 for details), the purpose of which is the trimming back of weak synaptic connections, while highly used connections are strengthened resulting in an increase in the efficiency of network processing (9). A study using two-photon microscopy to study cortical spines in adolescent mice (between ages P23 and P44), found a net decline in spines across several hours (6-8 hours) of sleep, suggesting that sleep may play an active role in synaptic pruning during this developmental phase (10).
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More indirect evidence collected in humans also suggests that sleep actively contributes to shaping teenagers’ brains. For example, a correlation between shorter total time in bed on weekdays, as well as later bedtime on weekends with reduced grey matter volumes in frontal, anterior cingulate, precuneus cortex regions (11), hippocampal volume (12) and white matter integrity (13) has been found. Although, other factors such as genes, may explain the correlation between sleep duration and brain volume, these studies provide some evidence that sleep may shape the human brain during development.
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NREM Sleep Neurophysiology During Adolescence In addition to guiding brain maturation, sleep is often seen as a window to the developing brain, offering the opportunity to examine brain structure and function. Two oscillations during non-rapid eye movement (NREM) sleep have been the primary focus of investigation: slow waves and spindles. Slow waves are oscillations of low frequency (< 5 Hz) and high amplitude generated by both the neocortex and the thalamus (14). Sleep spindles, on the other hand, are waxing and waning oscillations in the frequency range between 11 and 16 Hz generated through thalamocortical loops (15).
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Across adolescence, sleep physiology as reflected in the sleep EEG undergoes dramatic changes. A rapid reduction in SWA of approximately 40% takes place (16-20) with the steepest decline around the age of 12.5 years for girls and 13.5 years for boys (18). This decline has been linked to the aforementioned synaptic pruning processes whereby fewer synapses result in less synchronized synaptic activity – the substrate of EEG amplitude (21). Therefore, the higher amount of SWA in the pre-pubertal brain may be due to greater number, more highly connected, and synchronous synapses in the immature brain. In addition to the reduction in SWA, the topographic distribution of SWA changes as reflected by a shift of the region exhibiting maximal SWA from posterior to anterior sites (22). A similar postero-anterior trajectory has been observed for cortical maturation (e.g., (23)) further suggesting that the adolescent decline in SWA may be a marker of brain maturation. This notion is supported by significant correlations between SWA and cortical gray matter volume as measured by means of magnetic resonance imaging (MRI) (24, 25). We note that the association between cortical gray matter volume and sleep EEG power has been found to also be significant for other NREM sleep EEG frequency bands (24), suggesting that synaptic pruning, which in turn results in reduced cortical grey matter volume, is reflected across frequency bands. To wit, a decline in the duration and amplitude of sleep spindles is also observed during adolescent development (26-28). Beyond simply reflecting a decline in cortical volume, the changes to SWA and spindles may also have implications for sleep itself. With regards to SWA, the synaptic homeostasis hypothesis (SHY) posits that slow waves achieve sleep dependent
recuperation through synaptic downscaling (29). According to this hypothesis, by the end of the waking day, synaptic strength in many neural circuits undergoes an increase due to continuous learning. Synaptic renormalization is needed to regulate net energy consumption via down-regulation of synaptic strength. Thus within a developmental context, SHY would posit that during adolescence, a period when the number of synapses is on the decline, less SWA is required to achieve the same amount of sleep dependent recuperation. Therefore the decline in SWA across adolescence may not just reflect a decline in synapses, but also be due to the diminished need for sleep recuperation as a result of less synaptic activity during the day.
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A further implication of the decline in SWA during adolescence is that sleep becomes lighter, since SWA is a marker of sleep depth. Indeed, with the onset of adolescence individuals report greater difficulty falling and staying asleep. Objective PSG data confirm this (30, 31). While increased sleep onset latency in humans has been attributed to a number of environmental and psychological factors (e.g., increases in anxiety), interestingly sleep latency also increases across adolescence in mice (P19 to P111), suggesting that the decline in sleep pressure due to the reduced number of synapses, may in part account for increased sleep onset latency (7). Similarly, sleep spindles have been proposed to serve a sleep protective function (32, 33) and the developmental decline of these oscillations may in part explain the increase in arousals or wake after sleep onset observed both in mice (7) and humans (34).
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Concurrent with changes in the amplitude of oscillatory activity during adolescence an increase in brain connectivity occurs during adolescence. During this period an increase in NREM sleep EEG coherence (35), a measure of brain connectivity based on the consistency of phase relationship between two signals (21), is seen. This increase has been associated with functional reorganization (36) and increased myelination (37) in adolescence – processes leading to more efficient and dynamic interactions between brain regions. Furthermore, the adolescent increase in NREM sleep EEG sigma coherence (associated with spindle coherence) is significantly correlated with improvement in cognitive performance (38), suggesting that increases in coherence are of functional significance.
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Further indication of brain rewiring may be the observed linear increase in spindle frequency (39, 40). Although the mechanism resulting in the increase in spindle frequency is unclear, one hypothesis is that the decrease of slow wave sleep across adolescence results in a decline in thalamic hyperpolarization (40). Since spindle frequency is inversely related to the duration and degree of thalamocortical hyperpolarization (41), the adolescent decline in slow wave sleep results in an increase in spindle frequency. An alternate hypothesis is that the increase in spindle frequency reflects increased efficiency and strength of existing brain circuits through axonal myelination (42). To summarize, both slow waves and sleep spindles undergo declines in amplitude across adolescent development, while sleep spindles increase in frequency and density (43), and decrease in duration (43). While, the decline in spindle amplitude and increase in spindle frequency likely reflects changes in cortical grey and white matter volume respectively, the mechanism(s) underlying the changes to spindle duration and density are less clear. Furthermore, whether slow waves and spindles serve differing functions during adolescent development as compared to adulthood is unclear due to the scarcity of studies comparing the role of these oscillations in adults to adolescents (44).
Despite these changes, some sleep EEG features (for example, the morphology of the power spectra (45) and fast spindle duration (46)) demonstrate trait-like behavior, suggesting a potentially strong genetic contribution. Indeed, recent research has provided evidence for genetic determination of sleep EEG power (47) and topography (48) in adolescence. These studies find that over posterior regions, 80-90% of the observed variance in SWA and sigma power is explained by genetic factors, while over anterior regions the majority of variance is explained by environmental factors (47). These findings indicate a regional variation in genetic contribution to sleep EEG power and imply that the factors shaping the sleep EEG depend on frequency and, thus, might reflect differential mechanisms of brain function.
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REM Sleep During Adolescence: Because the emphasis of recent research has been on the oscillations of NREM sleep, less is known about the role of REM sleep in adolescent development. What is known is that some of the adolescent changes to NREM sleep, such as the decline in power (26, 27) (49) and increase in coherence (35), are mirrored in REM sleep. The state independence of these changes suggests the maturation of brain anatomy summarized above underlie this decline.
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Most of the research to date has focused on changes to REM sleep architecture across the adolescent period. Under sleep-satiated conditions (i.e., sufficient sleep prior to PSG measurement), the duration of REM sleep does not change across the adolescent period (26, 27). On the other hand, a recent study has shown that when sleep duration is experimentally truncated, the reduction in REM sleep duration is proportionally greater than NREM sleep (50). In this study, a decrease of both NREM and REM sleep upon reducing sleep duration from 10 to 7 hours in 10- to 14-year-olds was observed, however, the reduction in REM sleep was proportionally greater than that of NREM sleep suggesting that under sleep deprived condition NREM sleep may have biological priority (50). Further evidence of this is the first REM sleep episode may be “skipped” (27, 51) in some adolescents, likely due to high NREM sleep pressure at this age. To summarize, there is a significant knowledge gap in our understanding of the role of REM sleep in adolescent development. Given the importance of REM sleep in infant brain maturation (2), understanding the function of REM sleep in adolescence is of the utmost importance.
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Sleep behavior during adolescence and its impact on daily life Despite the stable “need” for sleep across adolescence and the importance of sleep in adolescent brain development, most adolescents do not obtain an adequate amount of sleep (reviewed in (52)). This sleep deficit is largely due to an interaction of biological systems with environmental factors, which push and pull in opposite directions. The circadian system pushes adolescents towards later bedtimes while the decline in homeostatic sleep pressure described above allows for adolescents to stay up later than their younger counterparts (reviewed in (53)). Environmental factors pushing sleep later include newly gained bedtime autonomy (e.g., (53, 54)), homework (e.g., (55)) the use of electronic devices (e.g. cellphone, internet) (e.g., (54, 56, 57)) and social media use (57). Pulling rise times towards the early morning hours is school start time, which does not change across the adolescent period (58) (59). This push and pull leads to chronic sleep deprivation in adolescents and to tired teenagers (52). Newer experimental and observational studies in adolescents have reported that multiple nights of sleep restriction, typical during adolescence, have a negative effect on various cognitive functions as well as mood (reviewed in (52)). For example, insufficient sleep has a negative impact on various complex mental processes and cognitive abilities as executive function (Lo, Ong, Leong, Gooley, & Chee, 2016), cognitive flexibility (Tee, Gan,
Tan, & Chin, 2018), processing speed (Cohen-Zion, Shabi, Levy, Glasner, & Wiener, 2016; Lim, Lo, & Chee, 2017) working memory (Lo et al., 2016; Tee et al., 2018).and mental health (Bei, Manber, Allen, Trinder, & Wiley, 2017; Brand et al., 2019). Although the consequences of insufficient sleep in adolescents mirror those observed in adults, it is unclear whether they are more pronounced in adolescents as compared to adults. This knowledge gap is due to the dearth of studies measuring the same cognitive constructs in adults and adolescents. Furthermore, the long-term consequences of short sleep, which may have a stronger impact on the developing brain are unknown and should be addressed by future research.
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Conclusion Taken together, evidence is emerging that sleep actively supports brain development through the shaping of synaptic connections. Whether sleep also plays a role in establishing network connectivity has not yet been studied. Although preliminary evidence suggests changes in network connectivity across the course of a night of sleep in young children (60), whether such changes have long-term implication is unknown. What is clear, however, is that sleep supports manifold biological functions, many of them critical to healthy development.
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Acknowledgements The authors would like to acknowledge the following source of funding: Interfaculty Research Cooperation grant “Decoding Sleep: From Neurons to Health & Mind” from the University of Bern (to LT).
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Box 1: What and when is adolescence? In humans, adolescence is understood to be the stage of development that begins with the onset of physical maturation (puberty) and ends with gaining adult autonomy (e.g. driving license, independent living, financial self-responsibility, etc.) (61). However, the boundaries of adolescence are blurry and it is not a single event that signals its beginning or end. Nonetheless, based on these guidelines, the world health organization (WHO) defines human adolescence as the second decade of life (ages 10 to 19 years). In mice, adolescence typically encompasses the period from weaning (≈ P21) to sexual maturity (P37-48). In both humans and mice, adolescence is characterized by behavioral and biological hallmarks that make this period unique. Behaviorally, adolescence is accompanied by increased risktaking, novelty-seeking and peer-directed social interaction in both species. Biologically, a period of rapid synaptic pruning is seen, wherein the number of synaptic connections undergoes marked decline. Generally speaking in both species this pruning commences around the time of puberty and continues to the end of the adolescent period defined above. We note, however, nuances in this process, with certain brain regions beginning and ending the synaptic pruning phase at different times (e.g., (23)). For a thorough review of the brain and behavioral changes occurring in human and rodent adolescence see (62).
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