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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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Darchia, N., Campbell, I. G., Basishvili, T., Eliozishvili, M., Tchintcharauli, T., Oniani, N., Sakhelashvili, I., & Feinberg, I. (2022) · SLEEP · doi:10.1093/sleep/zsac163 · Cited by 9
Self-citationVojnits, B., Magyar, T. Z., Szalárdy, O., Reicher, V., Takács, M., Bunford, N., & Bódizs, R. (2024) · Research in Developmental Disabilities · doi:10.1016/j.ridd.2024.104693 · Cited by 10
Neurodevelopmental Pathways of Childhood ADHD into Adulthood: Maturational Lag, Deviation, or Both?
Burke, A., & Edge, A. (2013) · InTech eBooks · doi:10.5772/53865 · Cited by 10
Sleep/Wake Dynamics Changes during Maturation in Rats
Gradwohl, G., Berdugo-Boura, N., Segev, Y., & Tarasiuk, A. (2015) · PLoS ONE · doi:10.1371/journal.pone.0125509 · Cited by 10
Practice and nap schedules modulate children's motor learning
Ren, J., Guo, W., Yan, J. H., Liu, G., & Jia, F. (2015) · Developmental Psychobiology · doi:10.1002/dev.21380 · Cited by 12
Furrer, M., Ringli, M., Kurth, S., Brandeis, D., Jenni, O. G., & Huber, R. (2019) · Sleep Medicine · doi:10.1016/j.sleep.2019.09.018 · Cited by 12
Fitzroy, A. B., Kainec, K. A., & Spencer, R. M. C. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.15468 · Cited by 10
“Campbell and Feinberg (2009) posited that while developmental changes in delta reflect changes in frontal cortex and other neocortical structures, changes in non-REM theta may reflect development of allocortical structures such as the hippocampus.”
BackgroundResultInfluentialMaturational trend of daytime sleep propensity in adolescents
Campbell, I. G., Figueroa, J. G., Bottom, V. B., Cruz-Basilio, A., Zhang, Z. Y., & Grimm, K. J. (2023) · SLEEP · doi:10.1093/sleep/zsad263 · Cited by 9
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“49 Moreover, during NREM sleep, this study also observed that low-frequency bands (SWA, theta, and low alpha bands) were signi fi cantly increased in children with ADHD compared to those in the healthy control group.”
Jussila, M., Saarenpää‐Heikkilä, O., Huupponen, E., Lapinlampi, A.-M., Penttala, J., & Himanen, S. (2016) · Clinical Neurophysiology · doi:10.1016/j.clinph.2016.02.016 · Cited by 10
“In children, SWA can also be considered to express the synaptic density and development of neural plasticity (Kurth et al., 2010a, 2012; Campbell et al., 2011; Campbell and Feinberg, 2009).”
BackgroundFeinberg, I., & Campbell, I. G. (2010) · SLEEP · doi:10.1093/sleep/33.6.737 · Cited by 9
Self-citationBergamo, D., Handjaras, G., Petruso, F., Talami, F., Ricciardi, E., Benuzzi, F., Vaudano, A. E., Meletti, S., Bernardi, G., & Betta, M. (2023) · Sleep Medicine · doi:10.1016/j.sleep.2023.12.001 · Cited by 10
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“517 Similarly, a longitudinal study in children and adolescents revealed that NREM delta and theta 518 activity drops sharply at the age of 10 and continues to decline until the age of 16.(64) In humans, 519 the reduction of slow waves is linked with reduction of gray matter during the course of cortical 520 maturatio…”
The Somnolent Youth-Sleep and the Influence of Exercise: A Narrative Review
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“It is hypothesized that this decline is potentially due to pervasive changes due to the brain maturation processes [64,65].”
BackgroundAerobic fitness and the sleeping brain of adolescents—a pilot study
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“5 years, preceding developmental changes in delta activity [6, 8].”
BackgroundInfluentialLocal sleep: A new concept in brain plasticity
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Campbell, I. G., Zhang, Z. Y., & Grimm, K. J. (2023) · SLEEP · doi:10.1093/sleep/zsad071 · Cited by 7
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Sleep Slow Oscillations and Cortical Maturation
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Adolescent Sleep Disruption: Implications for Psychiatric Morbidity
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Do naps benefit novel word learning? Developmental differences and white matter correlates
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Variations in habitual sleep and relational memory in 6-month-olds
Tham, E. K. H., Richmond, J. L., Gooley, J. J., Jafar, N. K. A., Chong, Y. S., Yap, F. K. P., Teoh, O.-H., Goh, D. Y. T., Broekman, B. F. P., & Rifkin‐Graboi, A. (2019) · Sleep Health · doi:10.1016/j.sleh.2018.12.007 · Cited by 7
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“Delta power is maintained between the age of 9 and 11 years, followed by a steep decline of about 66% beginning between the age of 11 and 12 years (about 15% per year; Campbell and Feinberg, 2009; Feinberg et al., 2012).”
Sleep/wake movement velocities, trajectories and micro-arousals during maturation in rats
Gradwohl, G., Olini, N., & Huber, R. (2017) · BMC Neuroscience · doi:10.1186/s12868-017-0343-6 · Cited by 7
“We extracted state dynamic parameters across early sleep and late sleep in the frontal and parietal lobes, which revealed noticeable changes of SWA in maturation in humans [7, 34] and rodents [11].”
Co-evolution of sleep spindles, learning and memory in children
Hoedlmoser, K. (2020) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2020.03.005 · Cited by 6
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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