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Longitudinal trajectories of non-rapid eye movement delta and theta EEG as indicators of adolescent brain maturation
Open accessAbstract
It is now recognized that extensive maturational changes take place in the human brain during adolescence, and that the trajectories of these changes are best studied longitudinally. We report the first longitudinal study of the adolescent decline in non-rapid eye movement (NREM) delta (1–4 Hz) and theta (4–8 Hz) EEG. Delta and theta are the homeostatic frequencies of human sleep. We recorded sleep EEG in 9- and 12-year-old cohorts twice yearly over a 5-year period. Delta power density (PD) was unchanged between age 9 and 11 years and then fell precipitously, decreasing by 66% between age 11 and 16.5 years ( P < .000001). The decline in theta PD began significantly earlier than that in delta PD and also was very steep (by 60%) between age 11 and 16.5 years ( P < .000001). These data suggest that age 11–16.5 years is a critically important maturational period for the brain processes that underlie homeostatic NREM EEG, a finding not suggested in previous cross-sectional data. We hypothesize that these EEG changes reflect synaptic pruning. Comparing our data with published longitudinal declines in MRI-estimated cortical thickness suggests the theta age curve parallels the earlier maturational thinning in 3-layer cortex, whereas the delta curve tracks the later changes in 5-layer cortex. This comparison also reveals that adolescent declines in NREM delta and theta are substantially larger than decreases in cortical thickness (>60% vs. <20%). The magnitude, interindividual difference, and tight link to age of these EEG changes indicate that they provide excellent noninvasive tools for investigating neurobehavioral correlates of adolescent brain maturation.
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“The EEG during SWS also shows typical changes during development: the amplitude and slope of slow waves as well as SWA (i.e., spectral power in the 0.5-4 Hz band, including both Ͻ1 Hz slow oscillation and 1-4 Hz delta activity) increases until the beginning of puberty at the age of 10 -12 years to levels distinctly higher than in adults, and thereafter starts to decrease (169, 604, 680).”
From About Sleep's Role in Memory (2013) · cites this paper as [169]
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“5–4 Hz band, including both 1 Hz slow oscillation and 1–4 Hz delta activity) increases until the beginning of puberty at the age of 10–12 years to levels distinctly higher than in adults, and thereafter starts to decrease (169, 604, 680).”
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“Campbell and Feinberg alluded to the similarity of the time course of synapse density and SWA (Feinberg, 1982; Campbell and Feinberg, 2009), proposing that the decrease in SWA observed during adolescence reflects the decrease or pruning of synapses (Campbell and Feinberg, 2009; Feinberg and…”
BackgroundInfluentialEEG sleep slow-wave activity as a mirror of cortical maturation
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Self-citationSleep deprivation, oxidative stress and inflammation
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“…in strength during sleep and wake occur in the adult brain as well as during early developmental periods characterized by high neuronal plasticity, extensive synaptogenesis, and massive synaptic pruning (Feinberg, 1982; Cowan et al., 1984; Carskadon et al., 2004; Campbell and Feinberg, 2009).”
BackgroundBecker, S. P., Langberg, J. M., & Byars, K. C. (2014) · Journal of Youth and Adolescence · doi:10.1007/s10964-014-0248-y · Cited by 214
“…is a decrease of slow wave sleep across adolescence (Colrain and Baker 2011; Ohayon et al. 2004), with delta power [assessed with sleep electroencephalogram (EEG)] starting to decline notably around age 11 and theta power also showing a steep decline from age 11–16.5 (Campbell and Feinberg 2009).”
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Campbell, I. G., Grimm, K. J., de Bie, E., & Feinberg, I. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1120860109 · Cited by 165
“1 y, 95% confidence intervals do not overlap), confirming our previous report of earlier theta than delta power decline (1).”
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Kurth, S., Ringli, M., LeBourgeois, M. K., Geiger, A., Buchmann, A., Jenni, O. G., & Huber, R. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.03.053 · Cited by 136
“Because the development of SWA parallels major changes in cortical maturation (e.g., the formation and subsequent elimination of synapses (Huttenlocher and Dabholkar, 1997)), slow waves were proposed to be related to these brain plasticity processes (Campbell and Feinberg, 2009; Feinberg, 1982).”
Relations between sleep patterns early in life and brain development: A review
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“Further, slow wave activity (SWA; slow oscillatory neocortical activity between 0.5 and 4 Hz) increases during the first few years of life and begins to decrease around adolescence (Campbell and Feinberg, 2009; Jenni and Carskadon, 2004).”
BackgroundInfluentialConsolidation of vocabulary is associated with sleep in children
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“These changes in the brain appear to parallel the rapid development of cognitive abilities at similar ages [31, 33, 38–43].”
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“Similarly, we find an increase in NREM theta power in the occipital region over adolescence, while others have reported decreased absolute theta power over this period of development (Campbell and Feinberg, 2009; Baker et al., 2011).”
BackgroundResultInfluentialDevelopmental changes in brain connectivity assessed using the sleep EEG
Tarokh, L., Carskadon, M. A., & Achermann, P. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.08.071 · Cited by 73
“, In Press) and sleep (Campbell and Feinberg, 2009) (Tarokh and Carskadon, In Press-a) EEG power.”
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“urational trajectory of the peak in SFP; (2) the maturational”
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Developmental change in EEG theta activity in the medial prefrontal cortex during response control
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“Neural oscillatory analyses have been successfully used to study brain maturation (Albrecht et al., 2010; Campbell and Feinberg, 2009; Cragg et al., 2011; Kikuchi et al., 2011; Le Van Quyen et al., 2006; Minlebaev et al., 2011; Müller et al., 2009; Sander et al., 2012; Uhlhaas et al., 2009, 2010; Yordanova and Kolev,…”
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“SWA undergoes a steep decline of approximately 65% during adolescence, typically beginning at ages 11–12 years (Campbell et al. 2011; Campbell and Feinberg 2009).”
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Topographic Differences in the Adolescent Maturation of the Slow Wave EEG during NREM Sleep
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“1 NREM delta has been of special interest for two biologically related reasons: (1) it behaves homeostatically,2,3 and (2) it changes markedly with age.”
BackgroundSelf-citationSleep EEG Provides Evidence that Cortical Changes Persist into Late Adolescence
Tarokh, L., Reen, E. V., LeBourgeois, M. K., Seifer, R., & Carskadon, M. A. (2011) · SLEEP · doi:10.5665/sleep.1284 · Cited by 59
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“This can be observed by the gradual shift from low to high frequency synchronization during development [53,54].”
BackgroundTrait-Like Characteristics of the Sleep EEG across Adolescent Development
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“For example, a significant decline is seen in the waking and sleep EEG amplitude starting in late childhood/early adolescence (Campbell and Feinberg, 2009; Kurth et al., 2010a,b; Tarokh and Carskadon, 2010).”
BackgroundDevelopmental changes in sleep and their relationships to psychiatric illnesses
Tesler, N., Gerstenberg, M., & Huber, R. (2013) · Current Opinion in Psychiatry · doi:10.1097/yco.0b013e328365a335 · Cited by 58
Synaptic Potentiation and Sleep Need: Clues from Molecular and Electrophysiological Studies
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“In humans, SWA changes during the lifespan in a way that seems to follow cortical synaptic density [113, 116, 117], as indicated directly by electron microscopy on post-mortem tissue [118],”
BackgroundPage, J. M., Lustenberger, C., & Frӧhlich, F. (2018) · SLEEP · doi:10.1093/sleep/zsy024 · Cited by 64
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“SO amplitude declined with age, consistent with a body of literature showing decreased slow-wave activity and sleep depth during adolescence [35, 36, 39] that has been hypothesized to reflect the functional optimization of cortical circuits through a process of synaptic refinement that increases the specificity of con…”
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“NREM delta power is maintained between age 9 and 11 years, followed by a steep decline of about 66% beginning between age 11 and 12 years (Campbell and Feinberg, 2009).”
BackgroundResultInfluentialDissipation of sleep pressure is stable across adolescence
Tarokh, L., Carskadon, M. A., & Achermann, P. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.04.055 · Cited by 53
“Because sleep EEG power decreases with age (e.g., (Tarokh and Carskadon, 2010) (Kurth et al., 2010) (Campbell and Feinberg, 2009)) and affects our measure (i.e., greater power will result in steeper slope), we normalized the data by setting power at the peak to 1 (see Figure 1C and 1F).”
BackgroundMethodAnatomical markers of sleep slow wave activity derived from structural magnetic resonance images
Buchmann, A., Kurth, S., Ringli, M., Geiger, A., Jenni, O. G., & Huber, R. (2011) · Journal of Sleep Research · doi:10.1111/j.1365-2869.2011.00916.x · Cited by 55
“SWA also shows remarkable maturational changes from childhood through adolescence (Campbell and Feinberg, 2009): the activity of slow waves during sleep increases in the first years of life, reaches its maximum shortly before puberty and declines thereafter throughout adolescence.”
BackgroundThe Effects of Caffeine on Sleep and Maturational Markers in the Rat
Olini, N., Kurth, S., & Huber, R. (2013) · PLoS ONE · doi:10.1371/journal.pone.0072539 · Cited by 54
“Our findings show that sleep slow wave activity (SWA) in the rat follows a similar inverted U-shaped trajectory as already known for humans [18,40,41,42].”
BackgroundSleep in adolescent depression: physiological perspectives
Urrila, A. S., Paunio, T., Palomäki, E., & MARTTUNEN, M. J. (2015) · Acta Physiologica · doi:10.1111/apha.12449 · Cited by 56
Lázár, A. S., Lázár, Z. I., Bíró, A., Győri, M., Tárnok, Z., Prekop, C., Keszei, A. P., Stefanik, K., Gádoros, J., Halász, P., et al. (2010) · Clinical Neurophysiology · doi:10.1016/j.clinph.2010.03.054 · Cited by 51
“Vertical bars indicate standard errors; P values reflect the significance level of group differences according to Fisher LSD post hoc analysis. caused by an age-programmed synaptic pruning that decreases waking brain metabolic rate (Campbell and Feinberg, 2009).”
Increased frontal sleep slow wave activity in adolescents with major depression
Tesler, N., Gerstenberg, M., Franscini, M., Jenni, O. G., Walitza, S., & Huber, R. (2015) · NeuroImage Clinical · doi:10.1016/j.nicl.2015.10.014 · Cited by 56
“…(EEG) as slow waves (Steriade et al., 1993) and measured as slow wave activity (SWA; frequency range 0.75–4.5 Hz), have been shown to mirror the extensive synaptic reorganization of cortical areas from early childhood to late adolescence (Campbell and Feinberg, 2009; Kurth et al., 2010).”
BackgroundInfluentialSmith, F., Gaskell, M. G., Weighall, A., Warmington, M., Reid, A. M., & Henderson, L. M. (2017) · Developmental Science · doi:10.1111/desc.12639 · Cited by 55
Longitudinal Analysis of Sleep Spindle Maturation from Childhood through Late Adolescence
Zhang, Z. Y., Campbell, I. G., Dhayagude, P., Espino, H., & Feinberg, I. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.2370-20.2021 · Cited by 52
“We previously found that a Gompertz curve best fit the adolescent decline in d (1-4Hz) EEG power (Campbell and Feinberg, 2009).”
BackgroundSelf-citationYuan, H., Pinto, S. J., Huang, J., McDonough, J. M., Ward, M. B., Lee, Y. N., Bradford, R. M., Gallagher, P. R., Justine Shults, A., Konstantinopoulou, S., et al. (2012) · SLEEP · doi:10.5665/sleep.2082 · Cited by 49
Sleep EEG oscillations in neurodevelopmental disorders without intellectual disabilities
Gorgoni, M., Scarpelli, S., Reda, F., & Gennaro, L. D. (2019) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2019.101224 · Cited by 48
The iPSC perspective on schizophrenia
Räsänen, N., Tiihonen, J., Koskuvi, M., Lehtonen, Š., & Koıstınaho, J. (2021) · Trends in Neurosciences · doi:10.1016/j.tins.2021.11.002 · Cited by 56
“During early adolescence, the delta oscillatory power declines [122].”
Feinberg, I., Davis, N. M., de Bie, E., Grimm, K. J., & Campbell, I. G. (2011) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00532.2011 · Cited by 47
“We recently delineated the longitudinal time course of the adolescent decline in NREM delta (1–4 Hz) EEG power (5).”
BackgroundMethodResultInfluentialSelf-citationLüchinger, R., Michels, L., Martin, E., & Brandeis, D. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.01.031 · Cited by 49
“In general, increased low frequency power is a typical phenomenon in lower arousal functional states such as sleep (Cajochen et al., 2002; Campbell and Feinberg, 2009), neuropathology (Llinas et al.”
BackgroundLucien, J. N., Ortega, M. T., & Shaw, N. D. (2020) · Current Opinion in Endocrine and Metabolic Research · doi:10.1016/j.coemr.2020.09.009 · Cited by 48
Developmental Patterns of Sleep Slow Wave Activity and Synaptic Density in Adolescent Mice
de Vivo, L., Faraguna, U., Nelson, A. B., Pfister‐Genskow, M., Klapperich, M. E., Tononi, G., & Cirelli, C. (2014) · SLEEP · doi:10.5665/sleep.3570 · Cited by 45
Widespread reduction in sleep spindle activity in socially anxious children and adolescents
Wilhelm, I., Groch, S., Preiss, A., Walitza, S., & Huber, R. (2016) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2016.12.018 · Cited by 45
Developmental changes in sleep biology and potential effects on adolescent behavior and caffeine use
Carskadon, M. A., & Tarokh, L. (2014) · Nutrition Reviews · doi:10.1111/nure.12147 · Cited by 43
Early Life Sleep Deprivation and Brain Development: Insights From Human and Animal Studies
Alrousan, G., Hassan, A., Pillai, A. A., Atrooz, F., & Salim, S. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.833786 · Cited by 53
“Furthermore, in a longitudinal study of sleep EEG conducted during childhood and adolescence periods (Campbell and Feinberg, 2009), found a steep decline of NREM delta and theta waves during the adolescent stage (11–16.”
BackgroundDevelopment of nap neurophysiology: preliminary insights into sleep regulation in early childhood
Kurth, S., Lassonde, J. M., Pierpoint, L. A., Rusterholz, T., Jenni, O. G., McClain, I. J., Achermann, P., & LeBourgeois, M. K. (2016) · Journal of Sleep Research · doi:10.1111/jsr.12427 · Cited by 47
“Sleep regulation changesbetween infancy (Beset al., 1991; Jenni et al., 2004) and adolescence (Campbell and Feinberg, 2009; Jenni et al., 2005).”
BackgroundDaytime Sleepiness Increases With Age in Early Adolescence: A Sleep Restriction Dose–Response Study
Campbell, I. G., Burright, C. S., Kraus, A. M., Grimm, K. J., & Feinberg, I. (2017) · SLEEP · doi:10.1093/sleep/zsx046 · Cited by 43
Self-citationMental Sleep Activity and Disturbing Dreams in the Lifespan
Scarpelli, S., Bartolacci, C., D’Atri, A., Gorgoni, M., & De Gennaro, L. (2019) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph16193658 · Cited by 41
“During adolescence, the reduction in the grey matter, following the initial growth during the early infancy, is associated, during sleep, to a marked reduction of cortical oscillation power and amplitude [39,41,110,111].”
Marshall, L., & Binder, S. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00614 · Cited by 42
“Associations between slow wave and theta band activity exist at many levels, for instance theta nesting in delta activity (Laktos et al., 2005; Carracedo et al., 2013) and parallel modulations in ontogenetic development (Campbell and Feinberg, 2009).”
BackgroundReduced sleep pressure in young children with autism
Arazi, A., Meiri, G., Danan, D., Michaelovski, A., Flusser, H., Menashe, I., Tarasiuk, A., & Dinstein, I. (2019) · SLEEP · doi:10.1093/sleep/zsz309 · Cited by 42
EEG–BOLD correlations during (post-)adolescent brain maturation
Lüchinger, R., Michels, L., Martin, E., & Brandeis, D. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.02.050 · Cited by 46
“This effect also extends to sleep (Campbell and Feinberg, 2009; Feinberg and Campbell, 2010), and has been suspected to mirror the development of higher cognitive functions (Case, 1992; Thatcher, 1994), and deviations from normal oscillatory patterns has been”
BackgroundNeurobiological mechanisms underlying the sleep-pain relationship in adolescence: A review
Christensen, J., Noel, M. E., & Mychasiuk, R. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.11.006 · Cited by 44
“the ongoing synaptic pruning process, making this change a natural developmental event (Colrain and Baker, 2011; Campbell and Feinberg, 2009; Feinberg and Campbell, 2010).”
BackgroundFurrer, M., Jaramillo, V., Volk, C., Ringli, M., Aellen, R., Wehrle, F. M., Pugin, F., Kurth, S., Brandeis, D., Schmid, M., et al. (2019) · Translational Psychiatry · doi:10.1038/s41398-019-0659-3 · Cited by 50
The interplay between sleep behavior and affect in elementary school children’s daily life
Könen, T., Dirk, J., Leonhardt, A., & Schmiedek, F. (2016) · Journal of Experimental Child Psychology · doi:10.1016/j.jecp.2016.04.003 · Cited by 41
Modulation of gamma and spindle-range power by slow oscillations in scalp sleep EEG of children
Piantoni, G., Astill, R. G., Raymann, R., Vis, J. C., Coppens, J. E., & Someren, E. J. W. V. (2013) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2013.01.017 · Cited by 40
“Synaptic density peaks, depending on the cortical area (Huttenlocher and Dabholkar, 1997), some time before puberty (Feinberg et al., 1990; Campbell and Feinberg, 2009).”
BackgroundSleep to Internalizing Pathway in Young Adolescents (SIPYA): A proposed neurodevelopmental model
Akbar, S. A., Mattfeld, A. T., Laird, A. R., & McMakin, D. L. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104780 · Cited by 40
Chua, E. C.-P., Yeo, S. C., Lee, I. T.-G., Tan, L.-C., Lau, P., Tan, S. S., Mien, I. H., & Gooley, J. J. (2014) · Physiological Reports · doi:10.14814/phy2.12129 · Cited by 37
Mapping changes in cortical activity during sleep in the first 4 years of life
Novelli, L., D’Atri, A., Marzano, C., Finotti, E., Ferrara, M., Bruni, O., & Gennaro, L. D. (2016) · Journal of Sleep Research · doi:10.1111/jsr.12390 · Cited by 42
“Sleep exhibits substantial changes from birth to the first 3–4 months of life (Jenni and Carskadon, 2004) and from early childhood throughout adolescence, when important changes in brain morphology and function occur (Campbell and Feinberg, 2009).”
BackgroundGeiger, A., Achermann, P., & Jenni, O. G. (2010) · Progress in brain research · doi:10.1016/b978-0-444-53702-7.00010-5 · Cited by 37
Co-maturation of theta and low-beta rhythms during child development
Rodríguez-Martínez, E. I., Barriga-Paulino, C. I., Rojas-Benjumea, M. A., & Gómez, C. M. (2015) · Brain Topography · doi:10.1007/s10548-014-0369-3 · Cited by 36
Heritability of Sleep EEG Topography in Adolescence: Results from a Longitudinal Twin Study
Markovic, A., Achermann, P., Rusterholz, T., & Tarokh, L. (2018) · Scientific Reports · doi:10.1038/s41598-018-25590-7 · Cited by 37
Spiess, M., Bernardi, G., Kurth, S., Ringli, M., Wehrle, F. M., Jenni, O. G., Huber, R., & Siclari, F. (2018) · NeuroImage · doi:10.1016/j.neuroimage.2018.05.024 · Cited by 37
“SWA has been shown to follow a trajectory resembling an inverted U-shape: it increases progressively in early childhood before it declines during adolescence (Feinberg, 1982; Gaudreau et al., 2001; Campbell and Feinberg, 2009; Jenni et al., 2004; Feinberg and Campbell, 2010; Kurth et al., 2010).”
Metadata
- Authors
- Campbell, I. G., & Feinberg, I.
- Affiliations
- University of California, Davis (US)
- ORCID
- Campbell, Ian G.
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2009-03-31
- Volume
- 106
- Issue
- 13
- Pages
- 5177-5180
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC2664015
- OpenAlex
- W2073925770
- Cited by
- 280
- References
- 29
- Citations by year
- 2026: 8 · 2025: 16 · 2024: 18 · 2023: 20 · 2022: 16 · 2021: 19 · 2020: 19 · 2019: 18 · 2018: 9 · 2017: 17 · 2016: 17 · 2015: 17 · 2014: 16 · 2013: 19 · 2012: 20
- FWCI
- 8.23
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Mental Health (R01MH062521, 1R01 MH62521)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Sleep and related disorders
- Keywords
- adolescent brain development, sleep homeostasis, synaptic pruning, cortical thickness
- MeSH terms
- Adolescent, Aging, Brain, Cerebral Cortex, Child, Electroencephalography, Eye Movements, Humans, Longitudinal Studies, Sleep
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