Elsevier

Brain and Cognition

Volume 72, Issue 1, February 2010, Pages 56-65
Brain and Cognition

Review article
Sleep EEG changes during adolescence: An index of a fundamental brain reorganization

https://doi.org/10.1016/j.bandc.2009.09.008Get rights and content

Abstract

Delta (1–4 Hz) EEG power in non-rapid eye movement (NREM) sleep declines massively during adolescence. This observation stimulated the hypothesis that during adolescence the human brain undergoes an extensive reorganization driven by synaptic elimination. The parallel declines in synaptic density, delta wave amplitude and cortical metabolic rate during adolescence further support this model. These late brain changes probably represent the final ontogenetic manifestation of nature’s strategy for constructing nervous systems: an initial overproduction of neural elements followed by elimination. Errors in adolescent brain reorganization may cause mental illness; this could explain the typical age of onset of schizophrenia. Longitudinal studies of sleep EEG are enhancing our knowledge of adolescent brain maturation. Our longitudinal study of sleep EEG changes in adolescence showed that delta power, which may reflect frontal cortex maturation, begins its decline between ages 11 and 12 years and falls by 65% by age 17 years. In contrast, NREM theta power begins its decline much earlier. Delta and theta EEG frequencies are important to sleep theory because they behave homeostatically. Surprisingly, these brain changes are unrelated to pubertal maturation but are strongly linked to age. In addition to these (and other) maturational EEG changes, sleep schedules in adolescence change in response to a complex interaction of circadian, social and other influences. Our data demonstrate that the daytime sleepiness that emerges in adolescence is related to the decline in NREM delta as well as to altered sleep schedules. These longitudinal sleep data provide guideposts for studying cognitive and behavioral correlates of adolescent brain reorganization.

Introduction

The ontogeny of non-rapid eye movement (NREM) sleep EEG demonstrates that the biology of the human brain changes massively during adolescence. The magnitude of the EEG changes can be appreciated by a simple fact: the decline of NREM delta EEG over 6 years of adolescence exceeds the decline over the subsequent 50 years of life. In addition to the developmental changes in sleep EEG, sleep behaviors change. Adolescents go to bed later in response to circadian and social influences. These sleep schedule changes and the maturational EEG changes are each, independently, related to the daytime sleepiness that emerges during adolescence. Interestingly, once preadolescent children outgrow daytime naps, they do not manifest daytime sleepiness unless they are ill or sleep deprived.

In this paper we first recapitulate the arguments set forth to support the proposition that the human brain undergoes a pervasive reorganization during adolescence (Feinberg, 1982/1983). These arguments were stimulated by sleep EEG observations and by Huttenlocher’s (1979) finding that synaptic density decreases across adolescence. This model proposed that brain reorganization during adolescence is required for normal cognitive development and that errors in this process could cause schizophrenia. Supporting the thesis of major brain reorganization is the finding that the maturational curves of three entirely different brain measures – synaptic density, cerebral metabolism, and delta wave amplitude – show strikingly similar shapes with all three declining steeply across adolescence. We next present recent data from our ongoing longitudinal study of sleep EEG. These findings have enabled us to delineate more precisely the maturational trajectories of NREM delta and theta, the EEG frequency bands that behave homeostatically. Activity in these frequency bands declines by over 60% between ages 11 and 16 years, but the age of onset of the decline is much earlier for theta. Defining these longitudinal trajectories provides new temporal guidelines for investigating the biological and behavioral correlates of adolescent brain maturation. These trajectories also have basic implications for developmental neuroscience. In the last section of this review, we briefly discuss the circadian and sleep schedule changes in adolescence and their relationships to the emergence of daytime sleepiness.

Section snippets

NREM and REM sleep

Most people now know that there are two kinds of sleep, non-rapid eye movement (NREM) and rapid eye movement (REM) sleep that have different brain wave patterns. NREM sleep brain waves differ strikingly from those of waking; they are typically taller (higher amplitude, especially early in the night) and slower (more spread out in time). REM sleep brain waves resemble those of waking and are accompanied by sporadic bursts of rapid eye movements (Aserinsky & Kleitman, 1953). Periods of NREM and

Sleep EEG and the pruning hypothesis of adolescent brain reorganization

The hypothesis that the brain undergoes pervasive maturational changes during adolescence stemmed from observations on sleep EEG. Feinberg and colleagues (1977) noted that the amplitude of large, slow (delta) waves during NREM sleep increased steeply during the first years of life, reached a maximum in early childhood, and then declined markedly across adolescence. They noted that the growth in amplitude during the first years of life would be expected from the striking post-natal increase in

Parallel ontogenetic curves for synaptic density, cerebral metabolic rate and delta wave amplitude

We noted in our 1982/1983 article that it would be important to supplement the evidence for a decline in average (whole brain) CMRO2 across adolescence with PET data that would measure metabolism in the cerebral cortex. Chugani et al. (1987) subsequently reported PET data showing that cortical glucose utilization was low in infancy, increased steeply in early childhood and then declined across adolescence. Examining the Chugani et al. (1987) data, we were struck by the similar shape of the

Longitudinal sleep studies across adolescence

EEG recording is the main research tool used to study human sleep. Electrodes applied to the scalp detect the constantly varying, tiny (millionths of a volt) electrical potentials produced by the brain. To perform these studies, we send trained undergraduate technicians to the subjects’ homes with portable EEG recorders. The children are paid volunteers who are clinically normal and performing at grade level or better in school. The technicians attach metal electrodes (each about the size of a

Sex differences and relation to pubertal development of EEG maturation

In an early publication of our longitudinal data, we reported a sex difference in the timing of the delta power decline across adolescence (Feinberg, Higgins, Khaw, & Campbell, 2006). After 2 years of longitudinal study of the C12 cohort, average delta power between ages 12 and 14 years was significantly lower in girls at each of four semi-annual recordings (see Fig. 7) but the slopes of the declines did not differ. The C9 cohort showed no sex difference between ages 9 and 11. Thus, these data

Sleep schedule and circadian changes in adolescence

Sleep behaviors, as well as sleep EEG, change during adolescence. The changes are most clearly apparent in changing sleep schedules. Similar schedule changes seem to occur throughout the developed world. Studies of children in Taiwan, Korea, Japan, United States, Canada, Iceland, Switzerland and Finland show that bedtimes become later with increasing age or school grade level. In longitudinal study, bedtime advanced from 21:01 ± :05 at age 9.3 years to 22:54 ± :06 at age 17 years. The later

Adolescent daytime sleepiness

Adolescent changes in sleep schedule tend to reduce total sleep time and are associated with an increase in daytime sleepiness. However, sleep loss is not the only factor in adolescent daytime sleepiness. In a groundbreaking study, Carskadon et al. (1980) found greater sleepiness, with multiple sleep latency tests, in more mature adolescents even when time in bed was held constant at 10 h for all participants. This finding indicates that there is a maturational component of daytime sleepiness

Conclusions

Our presentation here has only scratched the surface of the large body of longitudinal data we have already collected. Thus, we have analyzed the developmental data of only two frequency bands, and we have presented only the data for FFT power in these frequencies; other EEG measures derived from period-amplitude analysis (Feinberg et al., 1978), including the number, peak-trough amplitude and mean frequency, will be analyzed and reported. Rates of change across NREM sleep in these measures

Acknowledgments

We congratulate Professor Luciana for this timely and important issue. We thank her for the opportunity to participate. The longitudinal adolescent sleep data presented in this article was supported by United States Public Health Service grant R01 MH62521.

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