Hierarchical clustering of brain activity during human nonrapid eye movement sleep

Abstract

Consciousness is reduced during nonrapid eye movement (NREM) sleep due to changes in brain function that are still poorly understood. Here, we tested the hypothesis that impaired consciousness during NREM sleep is associated with an increased modularity of brain activity. Cerebral connectivity was quantified in restingstate functional magnetic resonance imaging times series acquired in 13 healthy volunteers during wakefulness and NREM sleep. The analysis revealed a modification of the hierarchical organization of large-scale networks into smaller independent modules during NREM sleep, independently from EEG markers of the slow oscillation. Such modifications in brain connectivity, possibly driven by sleep ultraslow oscillations, could hinder the brain's ability to integrate information and account for decreased consciousness during NREM sleep.complexity | integration D uring nonrapid eye movement (NREM) sleep, we are less aware of ourselves and our environment and, if we awaken, are less able to recollect any mental representation than during full-blown wakefulness (1). The mechanisms underpinning the reduction in conscious content during NREM sleep are still uncertain. Consciousness has been associated with the ability of a system to integrate information (2), which could be altered during NREM sleep. Here, in contrast to previous work (3, 4), we quantified changes in information integration from wakefulness to NREM sleep in large-scale brain networks and computed both their total integration and their degree of functional clustering. Functional clustering estimates how integration is hierarchically organized within and across the constituent parts of a system. It has been proposed as an empirically tractable measure for complexity of brain integration (5), which is considered a better estimate of the capacity to integrate information than total integration (6).We assessed brain functional connectivity on functional MRI (fMRI) data, which reflect the slow dynamics of local field potentials rather than instantaneous neural activities (7). Data were collected in a single nocturnal session in 13 participants who maintained periods of steady NREM sleep. At awakening, none of the subjects could recall any mental conscious content since sleep onset. From this dataset, we extracted for each subject two subsets of consecutive volumes recorded, respectively, during wakefulness and NREM sleep. Six spatially independent patterns, which we refer to as networks (Fig. 1A), were identified at the group level on wakefulness data, using a data-driven method (independent component analysis). These networks [visual (VIS), motor (MOT), default mode (DM), dorsal attentional (dATT), executive control (EC), and salience (SAL)] were previously identified in many studies investigating restingstate fMRI correlations in the literature (8-10). Network composition was very similar in data obtained during NREM sleep compared with wakefulness, in terms of within-networks areas distribution and Euclidian distance between networks (SI Results ...

What Is Lost During Dreamless Sleep: The Relationship Between Neural Connectivity Patterns and Consciousness

“…functional segregation of the different brain modules). The results are in line with IIT, as an increase in brain modularity should impair the brain's ability for functional interactions (Boly et al, 2012b). The authors also collected mentation reports, and all subjects reported no conscious experience prior to being awakened from NREM sleep, which provides a verification of the assumption that participants were in a state of reduced consciousness during this stage, and adds to the credibility of the postulated inverse relationship between brain modularity and conscious state.…”

“…EEG/fMRI data were collected in NREM sleep in the first half of the night. The authors first extracted six different resting-state networks with ICA and analysed them by calculating a measure called functional clustering ratio, or FCR (Boly et al, 2012b). FCR refers to the proportion of interactions within each subsystem, relative to between subsystems.…”

EEG Functional Connectivity Prior to Sleepwalking: Evidence of Interplay Between Sleep and Wakefulness

“…20 Testing the hypothesis that impaired consciousness during NREM sleep is associated with increased modularity in brain activity, fMRI studies have shown that NREM sleep is characterized by a decrease of large-scale networks and increase of smaller independent modules as reflected by high clustering ratios and low inter-modular connectivity. [21][22][23][24] Using transcranial magnetic stimulation (TMS) and high density (HD) EEG to assess how a TMS pulse delivered to the premotor cortex propagates in the brain during both sleep and wakefulness, Massimini and colleagues 25 found that when compared to a wakefulness propagated response, the response during NREM sleep (as recorded with HD-EEG) was stronger but extinguished more rapidly and did not propagate beyond the stimulation site. Thus, the fading of consciousness observed during deeper sleep stages may be related to a breakdown in long-range cortical connectivity.…”

Breakdown of long-range temporal dependence in default mode and attention networks during deep sleep

“…In particular, the default mode network (DMN; a set of task-deactivated regions implied with internal conscious cognitive processes) (9, 10) was repeatedly observed during deep sleep, albeit with reduced frontal connectivity (11,12). Although brain modules are preserved, even in the absence of conscious awareness, their functional integration is greatly impaired (8,13,14), which was predicted by an information integration account of consciousness (15). These results suggest that ongoing conscious mentation is not the only origin of RSN activity, whereas the level of consciousness is reflected in the interaction of functional networks.…”

“…Remarkably, although human nonrapid eye movement (NREM) sleep is characterized by impaired awareness and reduced conscious mentation, organization into RSNs is preserved in light sleep (6) and to a large extent, deeper sleep stages (7,8) (SI Appendix, Fig. S8.1).…”