Adolescence is now recognized as a period of major brain reorganization as well as rapid endocrine and physical development. Among the most prominent brain changes is a huge decline in the delta (<4 Hz) EEG of NREM sleep. Our ongoing study uses spectral and period-amplitude analyses to examine sleep and EEG longitudinally in semiannual 4-night recordings in two cohorts: C9 (N=30) ages 9-13 and C12 (N=38) ages 12-16. Data from the first two years yielded answers to important questions but raised new questions that require extending the study of these cohorts and adding a younger cohort, C6 (N=30) ages 6-10. Contrary to cross-sectional findings, our longitudinal results from C9 show little within-subject delta decline between 9 and 11 years. In contrast, C12 data show a strong delta decline across 12-14 years and levels were significantly lower in girls suggesting that they initiated the maturation process earlier. A striking result that contradicts previous suggestions is that, with age controlled, the delta decline was unrelated to pubertal (Tanner) status. The delta decline was also unrelated to the concurrent changes in sleep schedule. In C12 the increase in daytime sleepiness was related to the decline in delta but was not related to changes in sleep schedule. Extending the current study will enable us to determine within-individual patterns of delta decline from its start through its deceleration at the end of adolescence. We will also determine over a wider age range whether this decline is related to: pubertal development, the emergence of daytime sleepiness, performance on a daytime psychomotor vigilance task, and the ability to extend sleep. We have initiated a data sharing collaboration with Dr. Jay Giedd who has longitudinal MRI measures of cortical thickness over the same age ranges. The new 6 yr old cohort will provide quantitative benchmarks for sleep EEG across childhood over an age range where cortical grey matter is increasing. These data are the first within-S measurements of the decline in delta power across adolescence. We hypothesize that this decline is one component of a pervasive maturational reorganization during human adolescence. This reorganization is driven by synaptic pruning and includes a marked decline in waking brain metabolism. We have also hypothesized that errors in this process can give rise to mental illness, notably schizophrenia. Elucidating the normative trajectory of the delta changes across adolescence could provide an index of the related maturational brain events which could provide the platform necessary for the eventual study of patients at high-risk for schizophrenia. In addition, these data have implications for sleep homeostasis and for the public health implications for adolescent sleep schedules.

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National Institute of Mental Health (NIMH)
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Neural Basis of Psychopathology, Addictions and Sleep Disorders Study Section (NPAS)
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Zehr, Julia L
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University of California Davis
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Campbell, Ian G; Feinberg, Irwin (2016) Maturational Patterns of Sigma Frequency Power Across Childhood and Adolescence: A Longitudinal Study. Sleep 39:193-201
Feinberg, Irwin; Campbell, Ian G (2013) Longitudinal sleep EEG trajectories indicate complex patterns of adolescent brain maturation. Am J Physiol Regul Integr Comp Physiol 304:R296-303
Feinberg, Irwin; Davis, Nicole M; de Bie, Evan et al. (2012) The maturational trajectories of NREM and REM sleep durations differ across adolescence on both school-night and extended sleep. Am J Physiol Regul Integr Comp Physiol 302:R533-40
Campbell, Ian G; Grimm, Kevin J; de Bie, Evan et al. (2012) Sex, puberty, and the timing of sleep EEG measured adolescent brain maturation. Proc Natl Acad Sci U S A 109:5740-3
Feinberg, Irwin; de Bie, Evan; Davis, Nicole M et al. (2011) Topographic differences in the adolescent maturation of the slow wave EEG during NREM sleep. Sleep 34:325-33
Campbell, Ian G; Darchia, Nato; Higgins, Lisa M et al. (2011) Adolescent changes in homeostatic regulation of EEG activity in the delta and theta frequency bands during NREM sleep. Sleep 34:83-91
Feinberg, Irwin; Campbell, Ian G (2010) Cerebral metabolism and sleep homeostasis: a comment on Vyazovskiy et al. Brain Res Bull 81:1-2
Feinberg, Irwin; Campbell, Ian G (2010) Sleep EEG changes during adolescence: an index of a fundamental brain reorganization. Brain Cogn 72:56-65
Campbell, Ian G; Feinberg, Irwin (2009) Longitudinal trajectories of non-rapid eye movement delta and theta EEG as indicators of adolescent brain maturation. Proc Natl Acad Sci U S A 106:5177-80
Campbell, Ian G (2009) EEG recording and analysis for sleep research. Curr Protoc Neurosci Chapter 10:Unit10.2

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