Brain and Cognition 146 (2020) 105641

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Brain and Cognition

journal homepage: www.elsevier.com/locate/b&c

How is psychological stress linked to sleep quality? The mediating role of

functional connectivity between the sensory/somatomotor network and the
cingulo-opercular control network
Li Zhang , Dan Li , Huazhan Yin *
School of Education Science, Hunan Normal University, Chang Sha, 410081, China
Cognition and Human Behavior Key Laboratory of Hunan Province, Hunan Normal University, Chang Sha 410081, China

A R T I C L E I N F O A B S T R A C T

Keywords: How the functional connectivity of brain networks affects the relationship between psychological stress and sleep
Psychological stress quality remains unclear. To better understand the associations between psychological stress, resting-state
Sleep quality functional connectivity (RSFC), and sleep quality, we used the RSFC, Pittsburgh Sleep Quality Index (PSQI),
SM
and Psychosomatic Tension Relaxation Inventory (PSTRI) to investigate the relationship between psychological
CO
Functional connectivity
stress, sleep quality, and RSFC in four brain networks, the sensory/somatomotor (SM) network, cigulo-opercular
control (CO) network, default mode (DM) network, and dorsal attention (DA) network, in a large healthy sample
of 315 college students from Southwest University. Results showed that the brain functional connectivity in the
SM, CO, DM, and DA networks was significantly correlated to sleep quality. Meanwhile, we also found that the
brain functional connectivity between the SM and CO networks partially mediated the relationship between
psychological stress and sleep quality, suggesting that psychological stress has an important effect on individuals’
sleep quality, and increased functional connectivity between the SM and CO networks provides a neural basis for
the association between psychological stress and poor sleep quality.

1. Introduction hypothalamic arousal centers (e.g., posterior hypothalamus, locus

A number of studies have found that college students have sleep
problems. For instance, Buboltz, Brown, and Soper (2001) found that
89% of students experienced sleep problems ranging from occasional to
chronic. Suen et al. (2010) revealed that at least 60% of college students
were described as having poor quality of sleep, and were sleepless on
weeknights and frequently “pull all-nighters.” Norbury and Evans
(2019) found that 46% of participants rated their sleep as fairly bad or
very bad. To sum up, a large number of college students suffer sleep
problems.
In the face of this phenomenon, many researchers have explored
sleep problems. Buysse et al. (2011) advanced a neurobiological model
of insomnia that posits that the characteristic of insomnia is that sleep
and wake-like activation patterns, used to regulate sleep-wake state and
self-awareness, simultaneously exist in specific brain regions, including
the cortico-limbic circuits, the default mode network, the hypothalamic
centers (including the median and ventrolateral preoptic areas and
lateral hypothalamic hypocretin neurons), and the brainstem-
coeruleus, raphe nuclei, and cholinergic brainstem nuclei) (Buysse et al.,
2011). Meanwhile, numerous task-state studies and resting-state studies
in fMRI have been conducted on sleep quality to date. For example, one
study found smaller differences between wakefulness and early NREM
sleep in insomnia individuals than in healthy people in the temporal
cortex, thalamus, anterior cingulate, and brainstem arousal centers
(Nofzinger et al., 2004). Steriade and McCarley (2005) indicated that
sleep was accompanied by increased neuronal activity in the ventro­
lateral and median preoptic areas of the anterior hypothalamus. Addi­
tionally, Murphy et al. (2009) found that slow wave sleep mainly
originates from the left fronto-insular cortex and cingulate gyrus and
then spreads to the posterior regions. Consistent with this, sleep quality
was found to be significantly correlated with the gray matter volume of
the right insular (Yin et al., 2019). Furthermore, another fMRI study
revealed that sleep quality was significantly correlated with the pre­
cuneus cortex, the anterior cingulate cortex, the lateral orbitofrontal
cortex, the hippocampus and parahippocampal cortex, and some motor
areas (Cheng et al., 2018). While these regions could be reflected in

* Corresponding author.
E-mail address: yhz19791979@sina.com (H. Yin).

https://doi.org/10.1016/j.bandc.2020.105641
Received 29 April 2020; Received in revised form 17 October 2020; Accepted 20 October 2020
Available online 1 November 2020
0278-2626/© 2020 Elsevier Inc. All rights reserved.
L. Zhang et al.
different large-scale brain networks, such as somatomotor (SM)
network, cigulo-opercular control (CO), dorsal attention (DA) network,
network and default network (DM). These findings also been confirmed
by some studies, for example, Li et al. (2015) found the SM, DA, VA, and
DM network were affected by sleep deprivation and aging. Zhou, Wu,
Yu, and Lei (2017) also demonstrated that there were six brain net­
works, DM, CO, VA, DA, auditory network (AD) and memory retrieval
network (MR), which were more easily influenced by aging than SD.
Moreover, several studies found the importance of functional connec­
tivities in sleep quality. For instance, Cheng et al. (2018) also found poor
sleep quality was significantly positively correlated with functional
connectivities involving the lateral orbitofrontal cortex, the dorsolateral
prefrontal cortex, the cingulate cortex, and the precuneus. According to
these results, the present study selected four interesting networks and
concerned functional connectivities among these four networks,
including SM, CO, DM, and DA network.
Moreover, some studies have investigated the factors affecting sleep
quality, among which psychological stress is important. Previous studies
indicated that psychological stress could predict individuals’ sleep
quality (Li et al., 2019), such that the higher the psychological stress, the
worse the sleep quality. Moreover, several studies have also shown that
psychological stress could increase arousal and delay sleep onset (Bartel
et al., 2015; Short et al., 2013). In particular, research findings on col­
lege students indicate that sleep difficulties are positively associated
with perceived stress and that students not suffering from stress were
less likely to have poor sleep quality (Almojali et al., 2017; Amaral et al.,
2018).
According to the cognitive model of insomnia, uncontrollable
worries about stress events trigger emotional arousal before going to
sleep, which further leads to cognitive biases of events, so that people
make distorted cognitive evaluations of stress events and subjective
sleep quality declines (Harvey, 2002). According to this model, people
under psychological stress are more likely to have perceptual bias and
triggered negative emotion, leading to a serious decline in sleep quality.
On the one hand, several studies have indicated that psychological stress
is correlated with perceptual bias. For instance, Randall (2012) found
that information processing biases influenced genuinely stressful events
and negative biases were hypothesized to cause unnecessary and
excessive perceptions of stress. Urbańska et al. (2019) indicated that
stress had a negative impact on cognitive processes in schizophrenia
patients. On the other hand, a large number of studies have indicated
that psychological stress is related to emotion regulation and to the
specific brain regions involved in emotion regulation. For example,
Sinha (2001) found that psychological stress was associated with the
experience of various negative emotions. According to the neural
structure model of emotion regulation, emotion regulation involves the
interaction of various evaluation systems at different levels, specifically
the bottom-up system located in the posterior and subcortical areas,
including the basal nucleus and amygdala, and the top-down system
located in the cortical area, mainly including the frontal lobe. There
were two different types of systems. The first system includes the
dorsolateral prefrontal and cingulate areas, the second the orbital pre­
frontal, ventral prefrontal, and cingulate areas (Ochsner, and Gross,
2007). Furthermore, some empirical research has also indicated the
same brain regions. For instance, the prefrontal cortex (PFC), the ante­
rior cingulate cortex (ACC), and the amygdala play an important role in
the regulation of emotion and stress (Beauregard et al., 2001; Lévesque
et al., 2003; Taylor and Stanton, 2007). Another study indicated that
major stress was associated with decreased gray matter volume in the
corticostriatal-limbic regions, such as the hippocampus, orbitofrontal
cortex, insula, anterior cingulate, and medial prefrontal cortex (Gia­
naros et al., 2007). Meanwhile, Brewin et al. (2010) found that patients
who suffered from posttraumatic stress disorder usually rely on common
brain regions including the medial prefrontal regions, posterior regions
in the medial and lateral parietal cortices, medial temporal lobe, and
lateral temporal cortex.
2
Brain and Cognition 146 (2020) 105641
According to these findings of previous brain imaging studies, we
hypothesize that psychological stress and sleep quality might both be
associated with the brain regions involved in emotion regulation (e.g.,
the SM, CO, DM, and DA network). To some extent, the brain imaging
studies of psychological stress and sleep quality could contribute to an
understanding of the neural substrates of psychological stress and stress-
related mental problems (e.g., poor sleep quality).
Previous behavioral and brain imaging studies have explored the
relationship between psychological stress and sleep quality and its
neural basis. However, how brain network interactions affect the rela­
tionship between psychological stress and sleep quality remains unclear.
Resting-state functional connectivity (RSFC), the temporal correlation of
intrinsic activation between different brain regions, has become one of
the most fascinating fields in functional imaging studies. To better un­
derstand the associations among psychological stress, RSFC, and sleep
quality, we investigated the relationships among the neural network
(SM, CO, DM, and DA network), psychological stress, and sleep quality.
Furthermore, we conducted a mediation analysis to explore whether the
functional connectivity of brain networks could account for the associ­
ation between psychological stress and sleep quality. We expected that
(a) psychological stress would be positively associated with the global
PSQI score; (b) the functional connectivity of the brain network in the
SM, CO, DM, and DA networks would be associated with sleep quality;
and (c) the functional connectivity among the four brain networks
would mediate the relationship between psychological stress and sleep
quality .
2. Methods
2.1. Participants
A total of 315 participants (144 males and 171 females ranging from
17 to 27 years of age, mean age = 20.02 years, SD = 1.31 years) vol­
unteered to participate in our project. All participants were under­
graduate or postgraduate students at Southwest University, China. None
of them reported any history of psychiatric or neurological illness or
substance abuse according to the self-assessment questionnaire. This
study was funded by the Institutional Human Participants Review Board
of the Southwest University Imaging Center for Brain Research and the
protocol was approved by the Ethics Committee of Southwest Univer­
sity, Chongqing. All participants provided written informed consent.
2.2. Behavioral assessment
Sleep quality was measured by the Pittsburgh Sleep Quality Index
(PSQI). It includes 19 self-rated items and 5 other-rated items, of which
18 items were included in the scoring. There were seven subcomponents
of the 18 items: sleep latency, sleep duration, habitual sleep activity, use
of sleeping medication, the presence of sleep disturbances, daytime
dysfunction, and subjective sleep quality assessment. The total score of
these 7 components constitutes the PSQI, a global sleep quality score,
which ranges from 0 to 21 points. The PSQI score is inversely propor­
tional to the quality of sleep, meaning that a high PSQI score is indica­
tive of bad sleep quality (Shan et al., 2017). A total PSQI score of 5 or
greater was reflective of poor sleep quality (Buysse et al., 1989; Ong
et al., 2011). The PSQI had a high degree of internal homogeneity
(Cronbach’s α = 0.83). The PSQI was known for its high sensitivity
(89.6%) and specificity (86.5%) in assessing sleep quality (Buysse et al.,
1989)..
Psychological stress was measured by the Psychosomatic Tension
Relaxation Inventory (PSTRI) (Wallace, 1980), which includes 50 self-
rated items. Each item is scored from 0 to 4 (never, rarely, sometimes,
frequently, and always), and the total score ranges from 0 to 200. Higher
scores were indicative of higher levels of psychosomatic stress (Chen
et al., 2002), and a total PSTRI score of 82 or greater is reflective of high
psychological stress. The PSTRI score had a high degree of internal
L. Zhang et al.
homogeneity (Cronbach’s α = 0.93).
After participants gave written consent, they completed question­
naires under the supervision of the researcher. Participants were
assessed collectively in the laboratory using uniform instructions. The
questionnaires were collected immediately after completion.
2.3. MRI data acquisition
The resting-state fMRI data were collected at the Southwest Uni­
versity Brain Imaging Center on a 3T Trio scanner (Siemens Medical,
Erlangen, Germany). When participants began to be scanned, they were
asked to close their eyes but not to fall sleep. In total, 242 volumes were
acquired based on a gradient echo planar imaging sequence: repetition
time = 2000 ms; slices = 32; echo time = 30 ms; thickness = 3 mm;
resolution matrix = 64 × 64; flip angle = 90◦ ; field of view = 220 × 220
mm2; slice gap = 1 mm; and voxel size = 3.4 × 3.4 × 4 mm3.
2.4. Imaging preprocessing
All fMRI data were analyzed using SPM8 (http://www.fil.ion.ucl.ac.
uk/spm) and the Data Processing Assistant for Resting-State fMRI
(DPARSF) (Yan et al., 2016; Yan and Zang, 2010). We discarded the first
10 EPI scans to suppress equilibration effects, regarded as representing
the environmental adaptation of individuals. The remaining scans were
then preprocessed by slice timing, realigned, and normalized to a MNI
(Montreal Neurological Institute) template and resampled to 3 × 3 × 3
mm3. We then conducted a series of processing, including spatial
smoothing (8 mm full width at half maximum) and band-pass temporal
filtering (0.01–0.1 Hz). Nuisance signals (white matter and cerebrospi­
nal fluid signals, global mean signal, six rigid-body motion correction
parameters) were regressed to eliminate the potential impact of physi­
ological artifacts.
2.5. Functional network construction
To build the connectivity network, a 264-functional-node template
defined by Power was used that included 14 large-scale brain networks.
To focus on the SM, CO, DA, and DM network, we left 112 nodes
belonging to the four networks to build the functional network, then for
each subject we selected 28 nodes belonging to the SM network and 14
nodes belonging to the CO network, established a 28 × 14 correlation
matrix according to the template defined by Power, and obtained 392
functional connectivities.
2.6. Statistical analysis
The Pearson’s correlation analysis was performed between the
functional connectivity and sleep quality, psychological stress and sleep
quality. The multiple regression analysis was performed between the
functional connectivity and sleep quality. The multiple comparisons
were corrected by using Bonferroni procedure in the present study.
2.7. Mediation analysis
Mediation analyses of the relationship between psychological stress,
sleep quality, and brain functional connectivity were performed using
the PROCESS version 3.3 procedure in SPSS 22.0 (Preacher and Hayes,
2004). The concept of a mediation analysis is as follows. The relation­
ship between a predictor (x) and an outcome variable (y) can be
explained by their relationship to a third variable (the mediator (m)).
The mediation model included psychological stress as the predictor (x),
change in sleep quality as the outcome variable (y), and change in the
brain functional connectivity as the mediator (m). Additional covariates
were added to the model for adjustments (covariates: age and gender).
Indirect effects were considered significant if the value of 0 was not
contained in the confidence intervals and the indirect effect standard
3
Brain and Cognition 146 (2020) 105641
errors were estimated using the bootstrap methods with accelerated
95% confidence intervals (with 5000 samples).
3. Results
3.1. Behavioral results
Pearson’s correlation was performed to explore the relationship be­
tween psychological stress and sleep quality, revealing a significant
positive correlation between psychological stress and PSQI scores (r =
0.277, p < 0.001). The specific results are shown in Table 1.
3.2. Relationship between brain network and sleep quality
We employed a multiple regression analysis to predict sleep quality.
We found that these four networks significantly predicted sleep quality.
Specifically, the functional connections between the SM network and the
CO network (β = 0.308, t = 2.650, p < 0.05), between the DA network
and the DM network (β = 0.250, t = 2.442, p < 0.05), and within the SM
network (β = 0.223, t = 2.442, p < 0.05) and CO network (β = 0.194, t =
2.076, p < 0.05) were positively correlated with the total global PSQI
(see Figs. 1 and 2).
3.3. Additional analysis
In order to show that it is more appropriate to select the functional
connections between the SM network and the CO network, we con­
ducted whole brain predictive analysis. We selected 28 nodes belonging
to the SM network and 14 nodes belonging to the CO network, estab­
lished the correlation matrix of 28 × 14 according to the template
defined by Power, and obtained 392 functional connections for each
participant. We then repeated the same multiple regression analysis. The
results showed that the prediction of functional connectivity in all nodes
reached significance, ps < 0.05. The specific results are shown in
Table 2.
3.4. Results of the mediation analysis
Based on the behavioral and functional connectivity results, we
performed a mediation analysis to further explore whether psychologi­
cal stress affects sleep quality through the functional connection
strength of the sleep quality network. In the present study, we consid­
ered psychological stress an independent variable and measured it with
psychological stress scores, whereas the functional connection strength
of sleep quality network was considered a mediator and sleep quality an
independent variable measured with the PSQI. Gender and age were also
regarded as covariates in all mediation analyses. As expected, mediation
analysis showed that: (1) the functional connection strength of the sleep
quality network (the functional connection between the SM network and
the CO network) partially mediated the relationship between psycho­
logical stress and sleep quality (path a = 0.0003, p = 0.0013; path b =
7.9096, p = 0.0390; path ab = 0.0025, bootstrapped 95% CI = 0.0001,
0.0055) (see Fig. 3).
Table 1
Participant demographics (N = 315; males = 144, females = 171).
Mean SD Range PSQI Stress
Age (years) 20.02 1.26 17–27
PSQI 5.85 2.62 0–16 – 0.277***
stress 47.56 22.56 3–117 – –
Pearsons bivariate correlations, shown are r values.
N: number, SD: standard deviation, PSQI: Pittsburgh Sleep Quality Index.
*** p < 0.001.
L. Zhang et al.
Fig. 1. The corresponding partial correlation scatterplots illustrated the rela­
tionship between the total of PSQI score and functional connectivity between
the SSM network and the CO network. The x-axis of the scatterplots represents
the standardized residuals of the total of PSQI score, and the y-axis represents
standardized residuals of the values of functional connectivity between the SSM
network and the CO network.
4. Discussion
In this study, we investigated the associations among psychological
stress, RSFC, and sleep quality. First, Pearson’s correlation analysis
showed that psychological stress was positively correlated with PSQI.
That was to say, psychological stress was negatively correlated with
sleep quality. In addition, the brain functional connectivity between the
SM network and the CO network, between the DA network and the DM
network, and within the SM network and CO network was positively
associated with the global PSQI score and negatively associated with
sleep quality. Thus, the interaction of these four brain networks could
predict and affect the individuals’ sleep quality. More importantly, a
mediation analysis revealed that the brain functional connectivity
Fig. 2. The brain showed all the nodes and edges of the SSM network and the CO network which were correlated to the sleep quality. The size of the node rep­
resented the size of the node degree, the larger the node degree, the larger the node. The edges between the SSM network and the CO network were picked out which
the relationship between the two network of functional connectivity and sleep quality was significant.
4
Brain and Cognition 146 (2020) 105641
between the SM and CO networks partially mediated the association
between psychological stress and sleep quality. In summary, our find­
ings suggest that the increased functional connectivity between the SM
and CO networks may play an important role in the relationship between
psychological stress and sleep quality.
The present study found a significant correlation between psycho­
logical stress and sleep quality consistent with prior findings (Amaral
et al., 2018; Bartel et al., 2015; Short et al., 2013). For example, Amaral
et al. (2018) showed that sleep difficulties were positively associated
with perceived stress, such that higher stress may led to greater sleep
difficulties. This might be explained by the cognitive model of insomnia
(Harvey, 2002), such that the individual suffers from uncontrollable
worries about stress events that could trigger emotional arousal, and
then makes distorted cognitive evaluations of stress events, causing
subjective sleep quality to decline. Based on these findings, it was not
surprising that psychological stress was negatively correlated with sleep
quality in the participants.
Network model was increasingly considered as a useful tool to study
the core intrinsic activity characteristics and clinical biomarkers of
major neuropsychiatric disorders (e. g., Khazaie, Veronese, Noori et al.,
2017; Tahmasian, Shao, Meng, 2016). Khazaie et al. (2017) concluded
that most of findings in insomnia disorder discussed in previous studies
implicate three major neural networks: the DMN, CEN and SN. More­
over, the sleep quality was correlated to the functional connectivity
between the DMN and insular, hippocampus, anterior cingulate cortex
and etc (Khazaie, Veronese, Noori et al., 2017; Regen et al., 2016).
Meanwhile, Dong et al. (2018) found that the DAN (dorsal attention
network) – FPC (frontoparietal control network) functional connectivity
was significantly increased and the strength of aDMN - pDMN functional
connectivity was significantly decreased in insomniacs. In the present
study, consistent with previous studies, the functional connectivity be­
tween the SM network and the CO network, and between the DA
network and the DM network played a crucial role in sleep quality
(Horovitz et al., 2009). For example, a recent study using graph theo­
retical approaches to investigate network changes in sleep reported that
sleep reflects the strength of the somatomotor (SM) network (Horovitz
et al., 2009) and the DA network (Larson-Prior et al., 2009). Kaufmann
et al. (2016) identified 17 edges showing significant effects of sleep
deprivation on connectivity, involving the DM network, the DA
network, the frontal network, the visual network, the SMA network, the
auditory/speech network, the amygdala/hippocampus network, and the
cerebellar network. Zhang et al. (2019) showed by analysis of resting-
L. Zhang et al. Brain and Cognition 146 (2020) 105641

Table 2 brain areas, such as the frontal cortex, the anterior cingulate cortex, and
Functional connectivity of nodes links correlated with the pittsburgh sleep insula (Cristofori et al., 2015; van Noordt et al., 2015; Wang et al.,
quality index score. 2019). The SM network and CO network are related to emotional
Node 1 Node 2 r p reactivity to psychological stress (Goldin and Gross, 2010; Goldin et al.,
Cingulate Gyrus (R) Juxtapositional Lobule Cortex 0.12* 0.043
2009). These findings support the neural structure model of emotion
(L) regulation (Ochsner and Gross, 2007) that posits that individuals
Cingulate Gyrus (R) Superior Frontal Gyrus (L) 0.147** 0.029 suffering from psychological stress modulate their negative emotion
Cingulate Gyrus (R) Juxtapositional Lobule Cortex 0.144* 0.031 through the correlated brain regions of emotion regulation, including
(L)
the cingulate areas, amygdala, and frontal lobe.
Cingulate Gyrus (R) Superior Frontal Gyrus (R) 0.182** 0.021
Cingulate Gyrus (R) Frontal Operculum Cortex (R) 0.158** 0.021 Furthermore, the results of the mediation analysis show that the
Superior Parietal Lobule Supramarginal Gyrus (R) 0.158** 0.021 strength of the functional connections of sleep quality networks medi­
(L) ates the association between psychological stress and sleep quality. This
Superior Parietal Lobule Superior Frontal Gyrus (L) 0.128* 0.039 study found that the brain network most strongly associated with the
(L)
Superior Parietal Lobule Frontal Operculum Cortex (R) 0.171** 0.021
effects of psychological stress on sleep quality was the SM network. The
(L) SM network is anchored in the cingulate gyrus, superior parietal lobule,
Superior Parietal Lobule Insular Cortex (L) 0.129* 0.039 and precentral gyrus, which are related to attention regulation during
(L) the cognitive reappraisal of emotional reactivity to psychological stress
Superior Parietal Lobule Insular Cortex (R) 0.122* 0.043
(Goldin and Gross, 2010; Goldin et al., 2009). Meanwhile, psychological
(L)
Precentral Gyrus (R) Juxtapositional Lobule Cortex 0.138* 0.036 stress is correlated with lower activation in the precentral gyrus and
(L) higher activation in the anterior cingulate cortex (Shah et al., 2019). In
Precentral Gyrus (R) Superior Frontal Gyrus (L) 0.135* 0.036 addition, a large area within the cingulate cortex showed structural al­
Precentral Gyrus (L) Juxtapositional Lobule Cortex 0.162** 0.021 terations in the participants of obstructive sleep apnea (Macey et al.,
(L)
2008), and sleep times were significantly correlated with decreased
Precentral Gyrus (L) Superior Frontal Gyrus (L) 0.141* 0.032
Precentral Gyrus (L) Juxtapositional Lobule Cortex 0.159** 0.021 activation in the frontal cortex, precuneus cortex, and anterior cingulate
(L) cortex (Christensen et al., 2019; Urrila et al., 2017). Thus, it was not
Precentral Gyrus (L) Paracingulate Gyrus (R) 0.156** 0.021 difficult to find that psychological stress affected college students’ sleep
Precentral Gyrus (L) Central Opercular Cortex (L) 0.125* 0.040
quality through the SM network.
Precentral Gyrus (L) Frontal Operculum Cortex (R) 0.155** 0.021
Precentral Gyrus (R) Juxtapositional Lobule Cortex 0.124* 0.040 Another brain network strongly associated with the correlations
(L) between psychological stress and sleep quality was the CO network.
According to the study of Dosenbach et al. (2006, 2007), the CO network
* p < 0.05, ** p < 0.01.
is associated with the maintenance of tonic alertness and is closely
related to “task-set maintenance.” On the basis of the findings of this
study, we propose that the task maintenance should require high con­
centration, in this case causing more stress for the individual, and the
results of some studies support this view. Specifically, the superior
frontal gyrus is a core brain region for cognitive control and emotion-
regulation-related processes. Importantly, the superior frontal gyrus is
a neurofunctional marker of perceived stress in individuals (Wang et al.,
2019). Psychological stress is consistently associated with altered neural
oscillations in certain brain areas, such as the frontal cortex, anterior
cingulate cortex, and insula (Cristofori et al., 2015; van Noordt et al.,
2015; Wang et al., 2019). This reveals the importance of the CO network
Fig. 3. Mediation analysis. Path a, b, and c’ were statistically significant
in psychological stress. Moreover, the CO network includes the juxta­
(bootstrapped 95% CI: 0.0001, 0.0055). The mediation results suggested that
positional lobule cortex, supramarginal gyrus, superior frontal gyrus,
the values of functional connectivity between the SSM network and the CO
network partially mediated the association between psychological stress and
and insular cortex. According to previous studies, activation of the
sleep quality. *p < 0.05;**p < 0.01; ***p < 0.001. insula was detected during the occurrence of sleep-spindle-key features
of sleep stage II (Schabus et al., 2007) that are regarded as an index of
sleep stability (Dangvu et al., 2010; Kim et al., 2012). Hypersomnolence
state EEG data that sleep deprivation decreased the connectivity from
disorder is also associated with slow wave activity in bilateral cen­
the right middle occipital gyrus to the left parahippocampal gyrus (LPH/
troparietal regions and maps to portions of the somatosensory cortex
LFG). Meanwhile, directed high-frequency connectivity increased from
and supramarginal gyrus (Plante et al., 2019). Regions with highest
the left precuneus to the left superior frontal gyrus and left middle oc­
activation are located in the frontal and parietal lobe, specifically in the
cipital gyrus. Moreover, these findings support the proposed neurobio­
prefrontal cortex and the postcentral gyrus, where the effects of sleep
logical model of insomnia (Buysse et al., 2011) that the specific brain
deprivation are most significant (Latreille et al., 2019). To sum up, these
regions related to sleep include the cortico-limbic circuits, the default
findings show that the CO network plays an important role in the rela­
mode network, the hypothalamic centers, and the brainstem-
tionship between psychological stress and sleep quality.
hypothalamic arousal centers.
Furthermore, increased resting state functional connectivity between
Networks in which functional connectivity was associated with
the SM and CO networks suggests that psychological stress may enhance
psychological stress problems and their effects on sleep quality included
the ability of the CO network to exert cognitive control and emotion
the SM network and the CO network. There was increasing evidence that
regulation and decrease sleep quality via strengthening of the SM
the SM network and the CO network were key brain networks associated
network. For instance, Gu et al. (2013) found that the insula has bidi­
with psychological stress (Gianaros et al., 2007; Karl et al., 2006). For
rectional connections with the frontal, parietal, and the cingulate gyrus.
instance, Shah et al. (2019) indicated that psychological stress was
The functional connectivity between the cingulate gyrus and the insula
correlated with lower activation in the precentral gyrus and higher
is related to emotion. According to this result, we should find that the
activation in the anterior cingulate cortex. Meanwhile, psychological
functional connectivity could affect the individual’s emotion, including
stress is consistently associated with altered neural oscillations in certain
psychological stress. Meanwhile, in the previous paragraph, we have

5
L. Zhang et al.
outlined the relationship between functional connectivity and sleep
quality. On the basis of the findings of this study, we propose that the SM
network and the CO network contribute to the negative emotions in
psychological stress and their association with sleep quality, and that the
SM network has high functional connectivity with the CO network.
According to this study, we found that psychological stress can affect
sleep quality through the brain functional connectivity between the SM
and CO networks among the college students. On the one hand, SM
network was related to emotional reactivity (Goldin and Gross, 2010;
Goldin et al., 2009) that college students with poor sleep should master
some ways to adjust their emotion and keep calm. On the other hand, CO
network was thought to be associated with cognitive control and alert­
ness maintaining (Coste & Kleinschmidt, 2016; Sheffield et al., 2015;
Zhou et al., 2017). Moreover, the functional connectivity was signifi­
cantly positively correlated to cognitive performance (Sheffield et al.,
2015; Zhou et al., 2017). Based on this, we could pay attention to and
cultivate students’ cognitive ability, such as observation, attention, and
creativity, to improve students’ sleep quality.
Three limitations must be borne in mind. First, our participants were
all healthy college students mainly suffering stress from learning.
However, the cause of psychological stress is not just academic, and thus
these results cannot be generalized to other people who are not students.
Second, the results of the mediation analysis in the present study could
only be determined based on psychological stress and sleep quality in
the brain, but the exact area in the cortex could not be pinpointed.
Finally, as this study is cross-sectional, the mechanism of the brain
functional connectivity in the causal relations between psychological
stress and sleep quality cannot be determined. In future studies, longi­
tudinal research or multiple experimental designs could be considered to
explore the causal relationship between the three variables.
5. Conclusion
For the first time we explored the relationship between psychological
stress and sleep quality, showing that psychological stress was nega­
tively correlated with sleep quality. Second, this study explored the
brain network of the functional connectivity associated with sleep
quality. The results showed that the large-scale brain network composed
of the SM, CO, DM, and DA network could significantly predict sleep
quality. The mediation results also showed that the functional connec­
tion between the SM and CO networks plays an important role in the
relationship between psychological stress and sleep quality.
Funding
This work was supported by the National Natural Science Foundation
of China (31671125).
CRediT authorship contribution statement
Li Zhang: Methodology, Software, Writing - original draft. Dan Li:
Writing - review & editing. Huazhan Yin: Conceptualization,
Supervision.
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