Topographic differences in the adolescent maturation of the slow wave EEG during NREM sleep.

STUDY OBJECTIVES Our ongoing longitudinal study has shown that NREM delta (1-4 Hz) and theta (4-8 Hz) power measured at C3 and C4 decrease by more than 60% between ages 11 and 17 years. Here, we investigate the age trajectories of delta and theta power at frontal, central, and occipital electrodes. DESIGN Baseline sleep EEG was recorded twice yearly for 6 years in 2 cohorts, spanning ages 9-18 years, with overlap at 12-15 years. SETTING Sleep EEG was recorded in the subjects' homes with ambulatory recorders. PARTICIPANTS Sixty-seven subjects in 2 cohorts, one starting at age 9 (n = 30) and one at age 12 years (n = 37). MEASUREMENTS AND RESULTS Sleep EEG recorded from Fz, Cz, C3, C4, and O1 was referred to mastoids. Visual scoring and artifact elimination was followed by FFT power analysis. Delta and theta EEG power declined steeply across this age range. The maturational trajectories of delta power showed a "back to front" pattern, with O1 delta power declining earliest and Fz delta power declining latest. Theta EEG power did not show this topographic difference in the timing of its decline. Delta, and to a lesser extent, theta power became frontally dominant in early adolescence. CONCLUSIONS We maintain our interpretation that the adolescent decline in EEG power reflects a widespread brain reorganization driven by synaptic pruning. The late decline in frontally recorded delta power indicates that plasticity is maintained in these circuits until a later age. Although delta and theta have similar homeostatic properties, they have different age and topographic patterns that imply different functional correlates.

[1]  A. Rechtschaffen,et al.  A manual of standardized terminology, technique and scoring system for sleep stages of human subjects , 1968 .

[2]  J. Carrier,et al.  Age‐related modifications of NREM sleep EEG: from childhood to middle age , 2001, Journal of sleep research.

[3]  T. A. Roberts,et al.  The effect of sodium chloride and temperature on the rate and extent of growth of Clostridium botulinum type A in pasteurized pork slurry. , 1987, The Journal of applied bacteriology.

[4]  P. Achermann,et al.  Unihemispheric enhancement of delta power in human frontal sleep EEG by prolonged wakefulness , 2001, Brain Research.

[5]  I. Feinberg,et al.  Adolescent changes in homeostatic regulation of EEG activity in the delta and theta frequency bands during NREM sleep. , 2011, Sleep.

[6]  M. Ferrara,et al.  The effects of sleep deprivation in humans: topographical electroencephalogram changes in non‐rapid eye movement (NREM) sleep versus REM sleep , 2009, Journal of sleep research.

[7]  V. R. Carlson,et al.  Sleep Variables as a Function of Age in Man , 1968 .

[8]  Irwin Feinberg,et al.  Longitudinal trajectories of non-rapid eye movement delta and theta EEG as indicators of adolescent brain maturation , 2009, Proceedings of the National Academy of Sciences.

[9]  F. Rombouts,et al.  Modeling of the Bacterial Growth Curve , 1990, Applied and environmental microbiology.

[10]  M. Carskadon,et al.  Spectral analysis of the sleep electroencephalogram during adolescence. , 2004, Sleep.

[11]  H W Agnew,et al.  The displacement of stages 4 and REM sleep with a full night of sleep. , 1968, Psychophysiology.

[12]  I Feinberg,et al.  Changes in sleep cycle patterns with age. , 1974, Journal of psychiatric research.

[13]  Laird Ak DYNAMICS OF TUMOR GROWTH. , 1964 .

[14]  P. Huttenlocher,et al.  The development of synapses in striate cortex of man. , 1987, Human neurobiology.

[15]  D. Kupfer,et al.  Electroencephalographic sleep of healthy children. Part II: Findings using automated delta and REM sleep measurement methods. , 1987, Sleep.

[16]  I. Feinberg,et al.  The adolescent decline of NREM delta, an indicator of brain maturation, is linked to age and sex but not to pubertal stage. , 2006, American journal of physiology. Regulatory, integrative and comparative physiology.

[17]  M. Carskadon,et al.  Regional differences of the sleep electroencephalogram in adolescents , 2005, Journal of sleep research.

[18]  A A Borbély,et al.  Brain topography of the human sleep EEG: antero‐posterior shifts of spectral power , 1996, Neuroreport.

[19]  G. Tononi,et al.  Sleep and synaptic homeostasis: a hypothesis , 2003, Brain Research Bulletin.

[20]  Thomas F. Nugent,et al.  Dynamic mapping of human cortical development during childhood through early adulthood. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[21]  I. Feinberg,et al.  Schizophrenia: caused by a fault in programmed synaptic elimination during adolescence? , 1982, Journal of psychiatric research.

[22]  Irwin Feinberg,et al.  Maturational changes in amplitude, incidence and cyclic pattern of the 0 to 3 Hz (Delta) electroencephalogram of human sleep , 1990 .

[23]  A. Borbély A two process model of sleep regulation. , 1982, Human neurobiology.

[24]  D. Kupfer,et al.  EEG sleep of normal healthy children. Part I: Findings using standard measurement methods. , 1984, Sleep.

[25]  D. Mathalon,et al.  A quantitative magnetic resonance imaging study of changes in brain morphology from infancy to late adulthood. , 1994, Archives of neurology.

[26]  D. Kupfer,et al.  Effects of age on delta and REM sleep parameters. , 1989, Electroencephalography and clinical neurophysiology.

[27]  H C Thode,et al.  Gamma distribution model describes maturational curves for delta wave amplitude, cortical metabolic rate and synaptic density. , 1990, Journal of theoretical biology.

[28]  W W Webb,et al.  Sleep patterns in late middle age males: an EEG study. , 1967, Electroencephalography and clinical neurophysiology.

[29]  P. Huttenlocher Synaptic density in human frontal cortex - developmental changes and effects of aging. , 1979, Brain research.

[30]  D Lehmann,et al.  Sleep deprivation: effect on sleep stages and EEG power density in man. , 1981, Electroencephalography and clinical neurophysiology.

[31]  Judith D. Singer,et al.  Using SAS PROC MIXED to Fit Multilevel Models, Hierarchical Models, and Individual Growth Models , 1998 .

[32]  Kazuhiko Fukuda,et al.  Proposed supplements and amendments to ‘A Manual of Standardized Terminology, Techniques and Scoring System for Sleep Stages of Human Subjects’, the Rechtschaffen & Kales (1968) standard , 2001, Psychiatry and clinical neurosciences.

[33]  P. Achermann,et al.  Fronto‐occipital EEG power gradients in human sleep , 1997, Journal of sleep research.

[34]  I. Feinberg Slow wave sleep and release of growth hormone. , 2000, JAMA.

[35]  T H Monk,et al.  The effects of age and gender on sleep EEG power spectral density in the middle years of life (ages 20-60 years old). , 2001, Psychophysiology.

[36]  M. Carskadon,et al.  Developmental changes in the human sleep EEG during early adolescence. , 2010, Sleep.

[37]  I. Feinberg,et al.  A Comparison of Period Amplitude Analysis and FFT Power Spectral Analysis of All-Night Human Sleep EEG , 1999, Physiology & Behavior.

[38]  N. McNaughton,et al.  Frontal-midline theta from the perspective of hippocampal “theta” , 2008, Progress in Neurobiology.

[39]  G Fein,et al.  Period and amplitude analysis of 0.5-3 c/sec activity in NREM sleep of young adults. , 1978, Electroencephalography and clinical neurophysiology.