Original ArticleDissociable effects of sleep deprivation on functional connectivity in the dorsal and ventral default mode networks
Introduction
It is well known that the modern 24/7 lifestyle compromises sleep duration. According to a recent report, sleep problems affect one-third of the general population, and 60–70 million Americans suffer from chronic sleep problems [1]. Disrupted sleep has been suggested to be deleterious with regard to daily function and the development of heart disease [2], obesity [3], Alzheimer's disease [4], and even premature all-cause mortality [5].
A groundbreaking study on sleep deprivation was conducted in the 19th century, inspiring numerous physiologists and psychologists to investigate the effects of sleep deprivation on neurocognitive performance and physical function [6]. Sleep deprivation has been well documented to impair cognitive function, including attention, memory, and decision-making (for review, see Refs. [7], [8]) [9], [10], [11]. However, recent studies have repeatedly shown relatively preserved performance on complex cognitive tasks [12]. To date, most studies focused on the deleterious effects of sleep deprivation. Nonetheless, it is also important to explore compensatory changes that occur after sleep deprivation, to possibly tap the potential of such changes for shift-workers. To better understand the impact of one night of sleep deprivation and to possibly benefit shift workers, the present study investigated changes in the brain that are induced by sleep deprivation.
The brain is organized into multiple distributed large-scale networks, and the default mode network (DMN) is an anti-task network whose metabolic activation decreases during external cognitive tasks. The DMN has received substantial research attention since its discovery [13], [14], [15]. Studies that investigated functional connectivity within the DMN after sleep deprivation have consistently reported lower functional connectivity within the network [16], [17]. However, a growing number of studies suggest that this network comprises at least two functionally distinct subdivisions and not simply one homogeneous network: (i) one subdivision consisting of the dorsal and anterior regions (dorsal DMN [dDMN]) is involved in introspective, self-oriented processes and (ii) a second subdivision consisting of posterior and medial temporal regions (ventral DMN [vDMN]) is engaged in decision-making, which is a more complex process requiring higher cognitive function [18], [19], [20]. The vDMN has a significantly weaker anti-correlation with the attention network compared with the dDMN. Based on findings of impairments on simple cognitive tasks and preserved performance on complex tasks after sleep deprivation, the first hypothesis of the present study was that there is a dissociable effect of sleep deprivation on functional connectivity in the two subsystems of the DMN. Functional connectivity of the dDMN decreases, consistent with the reported impairments of cognitive function. Functional connectivity of the vDMN increases and communication between the dDMN and vDMN is enhanced to play a compensatory role in preserving performance.
Accumulating studies have focused on individual differences in vulnerability to sleep deprivation. Several studies have attempted to predict sensitivity or vulnerability to worse performance based on structural or functional connectivity of the DMN after sleep deprivation [21], [22]. Lower brain activation during a working memory task at resting baseline is associated with vulnerability to the effects of sleep deprivation [23]. Some studies have sought to identify biomarkers that can predict the vulnerability of cognitive function to sleep deprivation. The factors that influence the brain's response to sleep deprivation remain unclear. Our previous study found that working memory plays a protective role in response to sleep deprivation. People with greater working memory capacity exhibited preserved performance in instrumental learning [11]. A reasonable assumption is that working memory capacity is involved in compensatory adaptations of the brain's response to sleep deprivation.
Section snippets
Participants
Fifty-one healthy college students were enrolled in the study, after selection based on multiple criteria, through advertisements. All of the participants met the following inclusion criteria: (1) right-handed, (2) nonsmokers, (3) regular sleeping habits (>6.5 h and <10 h of sleep per night), (4) not on any long-term medications, (5) no history of sleep disorders or psychiatric/neurological disorders, (6) no shift work in the past three months, (7) no traveling to a time zone with more than a
Physiological data
Demographic data, psychological traits, and sleep characteristics are shown in Table 1. Independent-sample t-tests or Mann–Whitney U tests revealed no significant differences across the two groups in age, body mass index (BMI), years of education, BDI scores, HAMA scores, BIS scores (including all three dimensions), MoCA scores, working memory capacity, PSQI scores, habitual sleep duration during the past month, averaged sleep duration in the three days before the experiment, ESS scores, or MEQ
Discussion
Numerous studies have investigated the effects of total sleep deprivation on cognitive function, but the results have not been consistent. Two variables may cause such inconsistencies, the variability of cognitive tasks and individual differences. Even for the same cognitive function, different experimental tools have been applied across studies. Acute sleep deprivation mainly affects basic cognitive function, especially executive function and attentional processes, with less influence on
Acknowledgments
This study was supported in part by the National Basic Research Program of China (no. 2015CB856400), National Natural Science Foundation of China (no. 81501158, 81521063, 91432303, and 31230033), and National Key Technology Research and Development Program of the Ministry of Science and Technology of China (no. 2015BAI13B01).
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Authors who contributed equally to the research project.