Article

Cortical network functional connectivity in the descent to sleep

Department of Radiology, Washington University School of Medicine, 4525 Scott Avenue, St. Louis, MO 63110, USA.
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 04/2009; 106(11):4489-94. DOI: 10.1073/pnas.0900924106
Source: PubMed

ABSTRACT

Descent into sleep is accompanied by disengagement of the conscious brain from the external world. It follows that this process should be associated with reduced neural activity in regions of the brain known to mediate interaction with the environment. We examined blood oxygen dependent (BOLD) signal functional connectivity using conventional seed-based analyses in 3 primary sensory and 3 association networks as normal young adults transitioned from wakefulness to light sleep while lying immobile in the bore of a magnetic resonance imaging scanner. Functional connectivity was maintained in each network throughout all examined states of arousal. Indeed, correlations within the dorsal attention network modestly but significantly increased during light sleep compared to wakefulness. Moreover, our data suggest that neuronally mediated BOLD signal variance generally increases in light sleep. These results do not support the view that ongoing BOLD fluctuations primarily reflect unconstrained cognition. Rather, accumulating evidence supports the hypothesis that spontaneous BOLD fluctuations reflect processes that maintain the integrity of functional systems in the brain.

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    • "Electroencephalography (EEG) microstates are preserved across wakefulness and deep sleep (Brodbeck et al., 2012), and the association of ICNs with microstates (Britz et al., 2010) further supports the similarity of intrinsic brain activity during wakefulness and sleep. Furthermore, even the modest sleep-related changes in the topology of functional connectivity networks (see Tagliazucchi et al., 2013B for in depth discussion) largely exclude sensory cortex (e.g., Horovitz et al., 2008; Larson-Prior et al., 2009). Similarly, Uehara et al. (2014) documented local changes in nodal efficiency in transition from wakefulness to stage 1 sleep but these did not include any sensory region. "
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    ABSTRACT: Sleep has been shown to subtly disrupt the spatial organization of functional connectivity networks in the brain, but in a way that largely preserves the connectivity within sensory cortices. Here we evaluated the hypothesis that sleeps does impact sensory cortices, but through alteration of activity dynamics. We therefore examined the impact of sleep on hemodynamics using a method for quantifying non-random, high frequency signatures of the Blood-Oxygen-Level dependent (BOLD) signal (amplitude variance asymmetry; AVA). We found that sleep was associated with the elimination of these dynamics in a manner that is restricted to auditory, motor and visual cortices. This elimination was concurrent with increased variance of activity in these regions. Functional connectivity between regions showing AVA during wakefulness maintained a relatively consistent hierarchical structure during wakefulness and N1 and N2 sleep, despite a gradual reduction of connectivity strength as sleep progressed. Thus, sleep is related to elimination of high frequency non-random activity signatures in sensory cortices that are robust during wakefulness. The elimination of these AVA signatures conjointly with preservation of the structure of functional connectivity patterns may be linked to the need to suppress sensory inputs during sleep while still maintaining the capacity to react quickly to complex multimodal inputs.
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    • "It has been suggested that the variety of spontaneous activity patterns that the brain enters during task-free conditions reflects the naturally itinerant and variegated quality of normal consciousness [Raichle, 2011]. However, spatio-temporal patterns of resting state activity are globally well preserved in states such as sleep [Boly et al., 2009, 2012; Brodbeck et al., 2012; Larson-Prior et al., 2009; Tagliazucchi et al., 2013a,b,c] in which there is a reduced level of awareness—although very specific changes in connectivity occur across NREM sleep, allowing the decoding of the sleep stage from fMRI data [Tagliazucchi et al., 2012c; Tagliazucchi and Laufs, 2014]. Thus, if the subjective quality of consciousness is markedly different in deep sleep relative to the normal wakeful state (for example) yet FC measures remain largely preserved, this would suggest that these measures provide limited information about the biological mechanisms underlying different conscious states. "
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    • "These changes in local neural activity within a sleep stage play an essential but not exclusive role in functions of sleep such as memory maintenance and homeostasis; modulation of functional interactions among brain regions is also needed (Diekelmann and Born, 2010; Tononi and Cirelli, 2006). In fact, previous human neuroimaging studies compared functional connectivity patterns between wakefulness and sleep periods such as NREM sleep (Andrade et al., 2011; Horovitz et al., 2009; Koike et al., 2011; Sämann et al., 2011; Spoormaker et al., 2012), sleep stage 1 (Horovitz et al., 2008; Larson-Prior et al., 2009, 2011; Spoormaker et al., 2012; Uehara et al., 2013; van Dongen et al., 2011), SWS (Chow et al., 2013; Koike et al., 2011; Spoormaker et al., 2012), and REM sleep (Chow et al., 2013; Laureys et al., 2001; Maquet et al., 2000). Nevertheless, to compare the connectivity across different types of sleep stages, these neuroimaging studies implicitly assumed that functional connectivity was stable during a given sleep stage. "
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    ABSTRACT: Brain activity dynamically changes even during sleep. A line of neuroimaging studies has reported changes in functional connectivity and regional activity across different sleep stages such as slow-wave sleep (SWS) and rapid-eye-movement (REM) sleep. However, it remains unclear whether and how the large-scale network activity of human brains changes within a given sleep stage. Here, we investigated modulation of network activity within sleep stages by applying the pairwise maximum entropy model to brain activity obtained by functional magnetic resonance imaging from sleeping healthy subjects. We found that the brain activity of individual brain regions and functional interactions between pairs of regions significantly increased in the default-mode network during SWS and decreased during REM sleep. In contrast, the network activity of the fronto-parietal and sensory-motor networks showed the opposite pattern. Furthermore, in the three networks, the amount of the activity changes throughout REM sleep was negatively correlated with that throughout SWS. The present findings suggest that the brain activity is dynamically modulated even in a sleep stage and that the pattern of modulation depends on the type of the large-scale brain networks.
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