Abstract

We used tomographic analysis of MEG signals to characterize regional spectral changes in the brain at sleep onset and during light sleep. We identified two key processes that may causally link to loss of consciousness during the quiet or “core” periods of NREM1. First, active inhibition in the frontal lobe leads to delta and theta spectral power increases. Second, activation suppression leads to sharp drop of spectral power in alpha and higher frequencies in posterior parietal cortex. During NREM2 core periods, the changes identified in NREM1 become more widespread, but focal increases also emerge in alpha and low sigma band power in frontal midline cortical structures, suggesting reemergence of some monitoring of internal and external environment. Just before spindles and K-complexes (KCs), the hallmarks of NREM2, we identified focal spectral power changes in pre-frontal cortex, mid cingulate, and areas involved in environmental and internal monitoring, i.e., the rostral and sub-genual anterior cingulate. During both spindles and KCs, alpha and low sigma bands increases. Spindles emerge after further active inhibition (increase in delta power) of the frontal areas responsible for environmental monitoring, while in posterior parietal cortex, power increases in low and high sigma bands. KCs are correlated with increase in alpha power in the monitoring areas. These specific regional changes suggest strong and varied vigilance changes for KCs, but vigilance suppression and sharpening of cognitive processing for spindles. This is consistent with processes designed to ensure accurate and uncorrupted memory consolidation. The changes during KCs suggest a sentinel role: evaluation of the salience of provoking events to decide whether to increase processing and possibly wake up, or to actively inhibit further processing of intruding influences. The regional spectral patterns of NREM1, NREM2, and their dynamic changes just before spindles and KCs reveal an edge effect facilitating the emergence of spindles and KCs and defining the precise loci where they might emerge. In the time domain, the spindles are seen in widespread areas of the cortex just as reported from analysis of intracranial data, consistent with the emerging consensus of a differential topography that depends on the kind of memory stored.

Highlights

  • Normal sleep proceeds in 90-min cycles of rapid eye movement (REM) and non-REM (NREM) phases

  • Assuming we found evidence for these regional spectral signatures, we further hypothesized that the emergence of spindles and KCs that so far appears random may emerge as their continuation: the changes in core states will intensify on the approach and culminating into the apparent wild excursions during spindles and KCs

  • With the first we examined the changes in regional spectral power changes from wakefulness to light sleep (NREM1 and NREM2) leading to the generation of spindles and KCs

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Summary

Introduction

Normal sleep proceeds in 90-min cycles of rapid eye movement (REM) and non-REM (NREM) phases. Spindle-related activity is found in medial parietal, central and frontal areas (Manshanden et al, 2002; Ishii et al, 2003; Urakami, 2008; Gumenyuk et al, 2009; Dehghani et al, 2010a); KC-related brain activity has been identified in frontal cortical areas, along the cingulate gyrus, the precuneus, and the insula (Murphy et al, 2009), as well as in deep central temporal (Yoshida et al, 1996) and parietal areas (Lu et al, 1992; Numminen et al, 1996) These and other studies using intracranial recordings (Wennberg, 2010; Andrillon et al, 2011; Peter-Derex et al, 2012; Frauscher et al, 2015) and hemodynamic methods (Larson-Prior et al, 2009; Maquet, 2010; Caporro et al, 2012) have identified a wide range of brain areas showing high activation in the time periods of spindles and KCs, but no clearcut hints about the underlying mechanisms that are responsible for their generation

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