Developmental changes in the human sleep EEG during early adolescence.

A CASCADE OF BIOLOGICAL CHANGES ACCOMPANIES THE TRANSITION FROM CHILDHOOD TO ADOLESCENCE. THIS TRANSFORMATION IS AMONG THE most significant neurodevelopmental changes occurring after the perinatal period.1 The transition is marked by major brain reorganization that typically begins between the ages of 9 and 10 years and continues until the end of adolescence, about ages 18 to 20 years. These changes are reflected in a number of neural measures (e.g., waking cerebral blood glucose metabolism as measured by positron emission tomography2). Furthermore, cortical grey matter as measured by magnetic resonance imaging (MRI) in humans3–5 declines during this developmental period. The decreases in cortical grey matter and cerebral blood glucose metabolism are thought to indicate a decline in the number of active synapses during adolescence. Indeed, Huttenlocher and Dabholkar6 showed that dramatic synaptic pruning occurs in the healthy human adolescent cortex. These findings have been corroborated in the macaque monkey.7 EEG amplitude derives from synchronous synaptic activity across the cortex; a reduction in the number of synapses results in dampened EEG amplitude. Therefore, synaptic pruning across adolescence is reflected in the amplitude of the EEG signal. Several cross-sectional studies have shown a negative correlation between waking EEG amplitude over all frequency bands and age across adolescence.8–10 A recent cross-sectional study by Whitford and colleagues11 used resting waking EEG and MRI measures in the same participants to quantify neuroanatomical and neurophysiological differences in healthy participants across the span of ages 10 to 30 years. These authors report a negative correlation between log of age and gray matter volume, as well as with overall waking EEG power. The greatest change in these measures occurred across the second decade and reached an asymptote in the mid-twenties. The authors attribute the reduction in EEG power to the loss of grey matter and elimination of active synapses. If the elimination of active synapses results in a reduction of EEG power during adolescence, the phenomenon should be state nonspecific. Several cross-sectional studies show that sleep EEG power also declines across adolescence. One cross-sectional study comparing the sleep EEG of prepubertal (ages 9.6 to 12.9) and mature adolescents (ages 11.8 to 15.9 years) found that more mature participants had less EEG power across a wide range of frequencies during NREM and REM sleep.12 This effect was statistically significant at frequencies below 7 Hz for both REM and NREM sleep, in the sigma (11.8-12.6 Hz) and beta (16.2 – 16.8 Hz) bands for NREM, and at all frequencies below 15 Hz except for the alpha range (8.6 – 9.4 Hz) for REM sleep. The differences in EEG spectral power were accompanied by increased time spent in stage 2 sleep and less time spent in stage 4 sleep in the more mature adolescents, which is in line with previous cross-sectional13 and longitudinal14 studies. A second cross-sectional study performed by Gaudreau and colleagues15 examined EEG power in discrete frequency bands in children (6 – 10 years), adolescents (14 – 16 years), young adults (19 – 29) years, and middle age adults (36 – 60 years) across the first five hours of the night. These authors reported an inverse association between age group and NREM sleep EEG power in all the frequency bands examined: delta (0.75 – 4.5 Hz), theta (4.0 – 7.75 Hz), alpha (8.0 – 12.0 Hz), sigma (12.25 – 15 Hz), and beta (15.25 – 31.0 Hz). Compared to the other groups, the power difference in all frequency bands between the young adults and middle-aged adults was least pronounced. The above studies were cross-sectional, and large individual variability in EEG power limits interpretation of the results. A longitudinal study performed by Feinberg and colleagues16 examined the sleep EEG of thirty-one 9 year olds and thirty-eight 12 year olds at 6-month intervals for two years. These authors reported that delta power (0.3 to 3 Hz) did not differ significantly between the ages of 9 and 11 years, yet they showed a 25% decline in delta power between the ages of 12 and 14. Furthermore, the decline in delta power began earlier in girls than boys by an average of one year, but once initiated, the decay rate of delta power was similar in boys and girls.16 Despite this sex difference, the authors attributed the decline in power to age, and not pubertal stage, height, weight, body mass index (BMI), or sleep schedules. In this study, only sleep EEG power in the delta band (0.3 to 3 Hz) was examined, thus leaving open the question whether similar changes in power occurred in other frequency bands. Feinberg17 has shown that the ontogenetic curves for cortical metabolic rate, synaptic density, and power in the delta band overlap across the first three decades of life in humans, and he has hypothesized that these processes are biologically related and mark a major brain reorganization taking place during human adolescence. The aim of the present study is to add to the knowledge base on adolescent brain development by using spectral analysis to characterize longitudinal changes that occur during early adolescent development over (1) the course of the night (2) from several brain regions and (3) EEG frequencies up to 16 Hz. We hypothesize that, as in other studies, we will see a decline in SWS and an increase in stage 2 sleep with maturation. Additionally, we expect that these changes will be accompanied by a generalized developmental reduction in the amplitude of the sleep EEG signal across frequencies over the entire night.