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

Abstract

The integration of segregated brain functional modules is a prerequisite for conscious awareness during wakeful rest. Here, we test the hypothesis that temporal integration, measured as longterm memory in the history of neural activity, is another important quality underlying conscious awareness. For this aim, we study the temporal memory of blood oxygen level-dependent signals across the human nonrapid eye movement sleep cycle. Results reveal that this property gradually decreases from wakefulness to deep nonrapid eye movement sleep and that such decreases affect areas identified with default mode and attention networks. Although blood oxygen level-dependent spontaneous fluctuations exhibit nontrivial spatial organization, even during deep sleep, they also display a decreased temporal complexity in specific brain regions. Conversely, this result suggests that long-range temporal dependence might be an attribute of the spontaneous conscious mentation performed during wakeful rest.T he human brain displays complex spatiotemporal patterns of energy-consuming activity, even in the absence of an explicit task or stimulation (1). Large efforts have been devoted to the study of spontaneous neural activity encoded in the slow (∼0.1 Hz) fluctuations of the blood oxygen level-dependent (BOLD) signal, which are measured with functional MRI (fMRI). Nontrivial spatial organization of functional brain activity in resting state networks (RSNs) was consistently shown (2-4), comprising brain regions with high BOLD signal coherence and anatomical consistency with systems activated during task performance or stimulation (5).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). 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.However, brain activity is not completely characterized in the spatial domain only. fMRI BOLD signals display rich temporal organization, including scale-free 1/f power spectra and long-range temporal autocorrelations (16)(17)(18), with activity at any given time being influenced by the previous history of the system up to several minutes into the past. These landmarks of complex information processing and rapid adaptability are shared by many systems found in nature (19,20). Evidence for such properties is also manifest...

Signature of consciousness in the dynamics of resting-state brain activity

“…S5 A and B) (H awake = 0.772; H deep = 0.722; bootstrap analysis, P = 0.03), and marginally lower in moderate sedation than in awake (H moderate = 0.724; bootstrap analysis, P = 0.05) but did not differ significantly between sedation conditions (P > 0.1). The drop in H value indicates, in agreement with previous work on sleep (35) and anesthesia (36), that there is a breakdown of temporal integration in the sedated brain. To relate the fluctuations in H value over different sessions with fluctuations in brain states, we calculated for every session the mean similarity score index, or the average similarity to the anatomical connectivity matrix score across all brain states present in a single session.…”

“…The latter observation is consistent with the literature on sleep (35) and anesthesia (36): a loss of consciousness is associated with a drop in H value toward 0.5, the value that arises when the dynamics of time series is close to white noise, lacking temporal memory. How could more stable brain states arise from noisier and increasingly memoryless time series?…”

Human cortical–hippocampal dialogue in wake and slow-wave sleep

“…Acquisition parameters and details for these data have been previously published (55). The fMRI was acquired using a 3T scanner (Siemens Trio) with optimized polysomnographic settings (1,505 vol of T2*-weighted echo planar images, repetition time/echo time = 2,080 ms/ 30 ms, matrix = 64 × 64, voxel size = 3 × 3 × 2 mm 3 , distance factor = 50%, field of view = 192 mm 2 ).…”

“…Included are 70 epochs of wakefulness and 38 epochs of N3 sleep (SWS). Detailed sleep architectures of each participant have been previously published (55).…”

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

“…They concluded that there is a reduction in functional integration in this state of consciousness. These results point to a general impairment of functional connectivity on the level of the thalamocortical system as a whole, possibly underlying the reduction of consciousness (Tagliazucchi et al, 2013a). A potential limitation of the studies discussed above is that they did not involve obtaining subject mentation reports in the sleep stages of interest.…”