Topographical relocation of adolescent sleep spindles reveals a new maturational pattern in the human brain

Abstract

Current theories of human neural development and brain maturation emphasize the posterior-to-anterior or back-to-front pattern as an unequivocal ontogenetic feature that is largely due to the late maturing frontal lobes. The back-to-front pattern has received substantial support from both anatomical and electrophysiological studies, the latter looking at the age-related changes in the topography of sleep slow waves. However, the above scenario of a unidirectional developmental and anatomical route disregards the major hub of the so-called default-mode network, which is a human-specific and late maturing neural structure of the brain, undergoing significant differentiation during adolescence: the precuneus. In order to understand how the late maturation of the precuneus might modify the presently accepted large-scale maturational pattern of the human brain, here we focus on sleep spindles that are known to be involved in neural plasticity with major sources in the precuneus in adults. We provide evidence for the posteriorization in the prevailing anatomical localization of fast sleep spindles. The predominantly central maxima in density and amplitude of fast spindles at the age of 12 years becomes gradually shifted to the parietal regions until the age of 20. Similar changes, albeit at a smaller anatomical distance take place in terms of fast sleep spindle frequency. These findings indicate a front-to-back pattern of brain maturation and correspond with reports on an increased differentiation of the precuneus during adolescence.

The adolescent pattern of sleep spindle development revealed by HD‐EEG

“…We analysed an existing database of full night polysomnography recordings of 60 young adult and adolescent subjects (Gombos et al, 2021). The participants were recruited through social media with 10 males and 10 females in each age group: 12-year-olds The participants spent two consecutive nights in the sleep laboratory of the PPCU Budapest where 128 channel HD-EEG polysomnography was recorded.…”

“…Subjects went to bed between 10 p.m. and 11.30 p.m. and woke up spontaneously in the morning. For the procedure of EEG recordings, hardware environment, data processing, and sleep spindle extraction method see the study by Gombos et al (2021).…”

“…We only analysed the data from the experimental night. The sleep states of 20 second epochs of the whole-night NREM EEG recordings were scored according to standardised criteria (Gombos et al, 2021). For the detailed information of basic sleep architecture see Table S1.…”

“…For sleep data processing (classification of sleep states, rejection of artefacts, and spindle detection using IAM), we used the program FerciosEEGPlus 1.3 (Gombos et al, 2021). For the calculation of CoG values, we used Microsoft Excel.…”

“…Most of our findings are confirmatory with respect to the pre-existing studies employing only a few electrodes and wide age-groups, and we also find a clear difference between the development of slow and fast spindles. The topographical analysis of the changes in spindle parameters throughout adolescence is presented in our parallel study (Gombos et al, 2021).…”