Spontaneous eyelid closures link vigilance fluctuation with fMRI dynamic connectivity states

Abstract

Fluctuations in resting-state functional connectivity occur but their behavioral significance remains unclear, largely because correlating behavioral state with dynamic functional connectivity states (DCS) engages probes that disrupt the very behavioral state we seek to observe. Observing spontaneous eyelid closures following sleep deprivation permits nonintrusive arousal monitoring. During periods of low arousal dominated by eyelid closures, sliding-window correlation analysis uncovered a DCS associated with reduced withinnetwork functional connectivity of default mode and dorsal/ventral attention networks, as well as reduced anticorrelation between these networks. Conversely, during periods when participants' eyelids were wide open, a second DCS was associated with less decoupling between the visual network and higher-order cognitive networks that included dorsal/ventral attention and default mode networks. In subcortical structures, eyelid closures were associated with increased connectivity between the striatum and thalamus with the ventral attention network, and greater anticorrelation with the dorsal attention network. When applied to task-based fMRI data, these two DCS predicted interindividual differences in frequency of behavioral lapsing and intraindividual temporal fluctuations in response speed. These findings with participants who underwent a night of total sleep deprivation were replicated in an independent dataset involving partially sleep-deprived participants. Fluctuations in functional connectivity thus appear to be clearly associated with changes in arousal. T he existence of large-scale functional brain networks is evidenced by well-defined spatial patterns of correlated bloodoxygenation level-dependent (BOLD) signal fluctuation in fMRI data (1). Recent work has shown that functional connectivity (FC) within and between brain networks is dynamic, corresponding to the observation that even while we are performing a task, our mental focus fluctuates (2). Fluctuation of fMRI-based FC occurs over tens of seconds (3, 4) and exhibits different patterns across conscious and unconscious states (5, 6). Furthermore, just as interindividual differences in stationary FC relate to variation in human behavior and cognition (7-10), it seems likely that recurring patterns (11) of fluctuating FC have behavioral significance.Temporal fluctuations in FC can arise from conscious mental activity (12), episodes of random synchrony (3), or simply timevarying levels of physiological noise (13,14). The association between BOLD signal fluctuation in the default mode network (DMN) and mind-wandering episodes (15-17) has prompted investigations into the behavioral correlates of spontaneous resting-state FC fluctuations (11,18). Although these fluctuations in FC have been shown to correlate with several physiological markers, such as electroencephalogram (EEG) power, magnetoencephalography (MEG) power, and heart rate variability (19-21), their behavioral significance remains unclear.A key obstacle to elucidating clear FC...

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