Developmental changes in brain connectivity assessed using the sleep EEG

Abstract

Adolescence represents a time of significant cortical restructuring. Current theories posit that during this period connections between frequently utilized neural networks are strengthened while underutilized synaptic connections are discarded. The aim of the present study was to examine the developmental evolution of connectivity between brain regions using the sleep EEG. All-night sleep EEG recordings in two longitudinal cohorts (children and teens) followed at 1.5-3 year intervals and one cross-sectional cohort (adults) were analyzed. The children and teen cohorts were 9/10 and 15/16 years at the initial assessment; ages of the adults were 20 to 23 years. Intrahemispheric, interhemispheric, and diagonal coherence was measured between all six possible pairings of two central (C3/A2 and C4/A1) and two occipital (O2/A1 and O1/A2) derivations during slow wave, stage 2, and, REM sleep. Within-subjects analyses were performed for the children and teen cohorts, and a linear regression analysis was performed across every assessment of all cohorts. Within-subject analyses revealed a maturational increase in coherence for both age cohorts, though the frequencies, sleep states, and regions differed between cohorts. Regression analysis across all age cohorts showed an overall linear increase in left and right intrahemispheric coherence for all sleep states across frequencies. Furthermore, coherence between diagonal electrode pairs also increased in a linear manner for stage 2 and REM sleep. No age-related trend was found in interhemispheric coherence. Our results indicate that sleep EEG coherence increases with age and that these increases are confined to specific brain regions. This analysis highlights the utility of the sleep EEG to measure developmental changes in brain maturation.

Figure 1. Intra- and Inter- Hemispheric and Diagonal Coherence for SWS, Stage 2 and REM sleep

The top plots correspond to mean interhemispheric coherence between the two central (left figure) and two occipital (right figure) electrodes, the second row correspond to left (left figure) and right (right figure) intrahemispheric coherence, and the third row is coherence between diagonal electrodes. At the bottom of each individual plot, separated from the rest of the plot by a horizontal line, are the statistical results obtained from the bootstrap analysis. Asterisks correspond to frequency bins that were statistically significantly different between the Initial and Follow-Up session for the children (Children) and teen (Teens) cohorts at p < .05.

Figure 2. Individual data for right intrahemispheric coherence during SWS for Children (Top) and Teens (Bottom)

Coherence at the follow-up session minus coherence at the initial session for all frequency bins and subjects are illustrated. Warm colors are indicative of increases in coherence between assessments, cool colors denote decreases in coherence and values of zero (no change in coherence) are shown in white. Note that the two plots are on different scales, and changes in coherence are larger for the teen cohort.

Figure 3. Exemplary figure of coherence as a function of age

Plot of intrahemispheric coherence for the left and right hemispheres for all participants at every age assessment during slow wave sleep (SWS) in the low delta band (0.8 to 1.6 Hz). On the left is the intrahemispheric coherence between the left central (C3/A2) and left occipital (O1/A2) electrodes and on the right is coherence between the right central (C4/A1) and right occipital (O2/A1) electrodes. A significant linear trend was detected for both these channels during SWS (slope = 0.01 Hz/Year, Intercept = 0.22, R² = 0.20, and p-value = 0.0004).