World Journal of Urology

https://doi.org/10.1007/s00345-019-02838-z

ORIGINAL ARTICLE

Intra‑ and inter‑resting‑state networks abnormalities in overactive

bladder syndrome patients: an independent component analysis
of resting‑state fMRI
Long Zuo1 · Jingnan Chen2 · Shuangkun Wang1   · Yang Zhou1 · Biao Wang3 · Hua Gu1

Received: 15 February 2019 / Accepted: 3 June 2019

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Abstract
Purpose  This study aims to determine whether intra-network and inter-network brain connectivities are altered using an
independent component analysis (ICA).
Methods  Resting-state functional MRI (rs-fMRI) data were acquired from 26 patients with OAB and 28 healthy controls
(HC). Eleven resting-state networks (RSNs) were identified via ICA. General linear model (GLM) was used to compare
intra-network FC and inter-network FC of RSNs between the two groups. Pearson correlation analyses were performed to
investigate the relationship between the identified RSNs and clinical variables.
Results  Compared with HC, the OAB group showed abnormal FC within the sensorimotor-related network (SMN), the
dorsal attention network (DAN), the dorsal visual network (dVN), and the left frontoparietal network (LFPN). With respect
to inter-network interactions, decreased FC was detected between the SMN and the anterior default mode network (aDMN).
Conclusion  This study demonstrated that abnormal FC between RSNs may reflect the altered resting state of the brain–
bladder network. The findings of this study provide complementary evidence that can help further understand the neural
substrates of the overactive bladder.

Keywords  Overactive bladder syndrome · Functional magnetic resonance · Independent component analysis

Introduction Besides the sacral neuromodulation (SNM) theory, the

“Overactive bladder” (OAB) is defined as a syndrome char-
acterized by symptoms of urgency, usually with increased
daytime frequency and nocturia, with or without urgency
incontinence [1]. Although the OAB is highly prevalent
worldwide and has a significant impact on the quality of life
and mental health [2, 3], the underlying pathophysiology
remains unclear.
Long Zuo and Jingnan Chen contributed equally to this work.
* Shuangkun Wang
shuangkunwang@126.com
1 neuronal circuits process the afferent signals arising from
Department of Radiology, Beijing Chao-Yang Hospital,
Capital Medical University, 8 Gongren Tiyuchang Nanlu,
Chaoyang District, Beijing 100020, China
2
School of Economics and Management, Beihang University,
Beijing, China
3
Department of Urology, Beijing Chao‑Yang Hospital, Capital
Medical University, Beijing, China
brain–bladder control network has been put forward recently,
which adds new information to the current knowledge of
micturition [4]. The control of micturition is recognized
as complex switching mechanisms based on a reciprocal
relationship between the bladder and the spinal cord which
is regulated by the brain initiating the micturition reflex
[5]. However, the circuitry controlling micturition from
the higher regions of the brain needs further investigation.
Many functional MRI studies have identified several cortical
regions that are involved in the micturition, such as the PFC,
ACC, insula, hypothalamus, basal ganglia, and cerebellum
[6].
Previous fMRI researchers have reported that several
an increasingly filled bladder to make decisions accord-
ing to the social context [7]. However, few studies focused
on the resting-state networks (RSNs) of the whole brain
of the OAB patients. Different from the seed-based FC
analysis approach, independent component analysis (ICA)
is a data-driven approach to decode spatially independent

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components of coherent signals, allowing for hypothesis-
free and observer-independent measures of interactions
within and between RSNs [8]. Furthermore, the advantage
of group information-guided (GIG)-ICA lies in its sensitivity
and reproductivity by preserving independence among ICs
of each participant and simultaneously establishing spatial
correspondence of ICs across participants. Thus, we adopted
the GIG-ICA to investigate whether patients with OAB have
both intra- and inter-network-altered FC.
Materials and methods
Subjects and questionnaires
The study protocol was approved by the Ethics Commit-
tee of Beijing Chaoyang Hospital, Beijing, China. Written
informed consent was issued by each participant in accord-
ance with the Declaration of Helsinki. 26 subjects with
OAB and 28 healthy control participants were included
in this study. For OAB, patients must complain of urinary
urgency, with or without urgency incontinence, usually with
frequency and nocturia, in the absence of infection or other
identifiable causes, in accordance with the 2002 ICS (Inter-
national Continence Society) definition of OAB. Controls
must have no prior diagnosis of OAB or interstitial cystitis/
bladder pain syndrome, no significant lower urinary tract
symptoms (AUA symptom index < 7), no bladder or pelvic
pain, and no evidence of urinary infection. The inclusion
criteria were as follows: (1) ≥ 18 years old, (2) diagnosed as
having OAB, and (3) capable of participating in the study.
The exclusion criteria were the following: (1) suffering from
neurological disorders (such as stroke, spinal cord damage,
Parkinson’s disease, and multiple sclerosis), (2) urinary
infection within the last month of the survey, (3) a post-void
residual volume ≥ 150 mL, (4) pelvic floor dysfunction, (5)
history of urological surgery, (6) symptoms of pelvic pain
or discomfort and (7) history of recorded urinary tract infec-
tion. OAB symptoms were assessed using the questionnaire:
overactive bladder symptom score (OABSS). Overactive
bladder was divided into 3 groups according to the following
score: mild, a total score ≤ 5; moderate, a total score of 6–11;
severe, a total score ≥ 12. To assess cognitive function of
OAB patients, the Mini-Mental State Examination (MMSE)
was used for objective testing in this study. To quantify the
severity of anxiety or depression level of OAB patients, the
self-rating anxiety scale (SAS) and self-rating depression
scale (SDS) were administered before MRI.
Urinary system MRI assessment
The subjects emptied their bladder before undergoing
MRI. Urinary MRI was acquired at a 3.0-T MR system
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World Journal of Urology
(MAGNETOM Prisma, Siemens, Erlangen, Germany)
requiring a 32-channel body coil receiver at the Magnetic
Resonance Center of Beijing Chao-Yang Hospital. The
parameters of routine abdominal MRI sequences were as
follows: Coronal T2 W HASTE (TR/TE: 2000/130, field
of view (FOV): 420 mm, slice thickness 7 mm). Two expe-
rienced radiologists read the film and found no significant
changes in bladder volume before and after scanning and
no structural abnormalities or abnormal signal foci in uri-
nary organs.
Brain MRI data acquisition
Brain MRI data were acquired at the same MR system
requiring a standard 64-channel head coil receive. Foam
pads were utilized to reduce head movements and earplugs
were used to prevent the influence of scanner noise. High-
resolution T1-weighted anatomical images were obtained
prior to functional scan [repetition time (TR) = 1900 ms;
echo time (TE) = 2.52 ms; slices = 176; flip angle = 9°;
field of view (FOV) = 256  mm × 256  mm; data
matrix = 256 × 256; in-plane resolution = 1 mm × 1 mm].
Resting-state functional images were acquired with
a EPI-GRE sequence (TR = 2000  ms; TE = 30  ms;
slices = 33; flip angle = 90°; FOV = 224 mm × 224 mm;
in-plane matrix resolution = 64 × 64; in-plane resolu-
tion = 3.5 mm × 3.5 mm). During the scan, subjects were
instructed to simply lay still in the scanner with eyes
closed, to stay awake and think of nothing in particular
without falling asleep. The entire MRI scanning process
lasts about 12 min and no patient complained about urge
during the scan.
Data preprocessing
The resting-state BOLD data were preprocessed using
Data Processing and Analysis of Brain Imaging (DPABI)
software (http://rfmri​.org/dpabi​). The first 10 volumes of
each functional time series were discarded to allow for
scanner calibration, and for the subjects to adapt to the
scanning. The remaining 230 volumes were performed
slice timing and realignment for head motion correction.
Then, we used the Friston 24-parameter model (6 motion
parameters, 6 temporal derivatives, and their squares) to
regress out head motion effects and signals of linear drift.
After that, the data were spatially normalized to Montreal
Neurological Institute (MNI) space (resampling voxel
size = 3 × 3 × 3 mm)3. Finally, the functional images were
smoothed by convolution with an isotropic Gaussian ker-
nel [full width at half maximum (FWHW) = 8 mm].
World Journal of Urology

Independent component analysis (ICA) Results

The independent components (ICs) for all subjects were ana- Group demographics and neuropsychological tests
lyzed by GIG-ICA (the GIFT software; https​://www.nitrc​ conducted
.org/ projects/gift, version 2.0a). The procedures based on
this toolbox include three steps: (i) data reduction, (ii) apply- No significant differences in gender, age, or education level
ing ICA algorithm, and (iii) back reconstruction for individ- were found between patients and control subjects (p > 0.05).
ual-level components. Finally, 20 ICs were auto-estimated The overactive bladder symptom score (OABSS) was
through the minimum description length (MDL) criteria used to define and classify OAB as mild (n = 4), moderate
and GIG-ICA was performed 100 times. Eleven meaning- (n = 16), or severe (n = 6). All subjects had normal scores of
ful RSNs were identified as anatomically and functionally MMSE, while SAS and SDS scores were significantly higher
classical RSNs via visual inspection. in patients than controls. Demographics and clinical data of
both OAB patients and healthy controls are listed in Table 1.
Functional network connectivity analysis
Identification of RSNs for HC and OAB
Functional connectivity (FC) refers to the neurophysiologi-
cal relationship between spatially separated brain regions, A total of 20 components were estimated through GIG-ICA.
reflecting whether there is a connection or interactive infor- Ten meaningful RSNs were extracted from all subjects,
mation between two brain functional areas. Each IC was including anterior default mode network (aDMN), poste-
thresholded using a random-effect one-sample t test by a rior default mode network (pDMN), auditory network (AN),
familywise error correction (FWE correction) (p < 0.05) to dorsal visual network (dVN), medial visual network (mVN),
remove atypical voxels with small correlation coefficients sensorimotor-related network (SMN), right frontoparietal
and retain highly correlated voxels. Here, we set the t value network (RFPN), left frontoparietal network (LFPN), dorsal
at 8 and the cluster size at 100 voxels based on previous attention network (DAN), and supplementary motor areas
studies. The mean time course was calculated by averag- (SMA).
ing the time courses within each RSN mask obtained from
the ICA processing. Pearson’s correlation coefficients of the Group comparisons of FC in RSNs
mean time courses between each pair of RSNs of individual
patients were calculated and then performed Fisher’s z trans- Compared with healthy controls, patients showed signifi-
formation to improve normality. cant FC differences in multiple RSNs (Fig. 1 and Table 2).
The next step was to determine whether the correlation For the SMN, FC decreased in both supramarginal gyrus
between each pair of the RSNs in each group was statisti- (Fig. 1a). For the DAN, FC decreased in the precentral
cally significant. Each subject’s z values were introduced
in a one-sample t test (p < 0.05). Intra-network FC differ-
ences in all RSNs extracted between the OAB patients and
Table 1  Demographic and clinical data in patients with OAB and
the HCs were tested using GLM analysis with age, sex, Healthy Control Group
and years of education as covariates. Multiple compari-
OAB (n = 26) Control group p value
sons were corrected using Gaussian Random Field (GRF)
(n = 28)
theory (uncorrected voxel p value < 0.001, corrected cluster
p value < 0.05). Inter-group comparisons were performed Sex (male/female) 23/3 26/2 NA
using the general linear model (GLM) to explore whether Age (years) 43.58 ± 13.42 50.12 ± 12.11 0.0654
pairs of inter-network FC reached significant differences Handedness (right/ 26/0 28/0 NA
between the OAB patients and the HCs (FDR correction, left)
p < 0.05). Levels of education 12.27 ± 4.74 14.02 ± 2.37 0.0887
(years)
MMSE 28.42 ± 1.31 29.23 ± 1.78 0.0640
Correlation analyses of FC with neuropsychological
Duration of OAB symptoms
test scores and clinical characteristics
 < 1 year 13 NA
 > 1 year 9
Pearson’s correlation between FC and neuropsychological
 Do not know 4
scores was observed through partial correlation analysis with
OABSS 8.43 ± 2.83 NA NA
sex, age, and years of education as covariates (p < 0.05),
SAS 45.82 ± 1.78 39.48 ± 1.30 0.0047
which were carried out in Statistical Product and Service
SDS 53.61 ± 1.78 43.15 ± 1.50 0.0001
Solutions (SPSS) version 18 (SPSS Inc., Chicago, IL, USA).

13

Fig. 1  Comparison of intra-network FC between the OAB and HC
groups. Compared with HC, the OAB group showed abnormal FC
within the SMN, DAN, dVN, LFPN (p < 0.05, GRF corrected). Color
scale denotes the t value. Warm color represents positive functional
connectivities; cold color represents negative functional connectivity.
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World Journal of Urology
X, Y, Z, Montreal Neurological Institute coordinates. L left, R right,
SMN sensorimotor-related network, DAN dorsal attention network,
dVN dorsal visual network, LFPN left frontoparietal network, FC
functional connectivity, OAB overactive bladder, HC healthy control
World Journal of Urology

Table 2  Brain regions with Regions Side Brodmann MNI coordinates Peak T value Cluster size
significant differences in intra- area
network functional connectivity X Y Z
(FC) between OAB patients and
healthy controls SMN
 Paracentral lobule L 2 − 18 − 42 63 − 6.220 1035
DAN
 Precentral gyrus L 6 − 27 − 9 60 − 5.657 270
ECN
 Supramarginal gyrus L 40 − 60 − 42 33 − 12.493 1944
 Supramarginal gyrus R 2 60 − 33 33 − 11.773 1320
LVN
 Cuneus L 16 − 15 − 78 36 − 5.084 209
LFPN
 Superior frontal gyrus L 9 − 21 39 48 − 4.999 324

gyrus (Fig. 1b). Within the dVN, FC decreased in the left
cuneus (Fig. 1c). In the LFPN, the functional connectivity
of the superior frontal gyrus decreased (Fig. 1d).
Group comparisons of FC between RSNs
Compared with HC, the OAB group exhibited signifi-
cantly decreased FC between SMN and aDMN (p = 0.0008)
(Fig. 2).

Fig. 2  Comparisons of inter-network FC alterations between the
RSNs in the OAB and HC groups. OAB group exhibited increased
FC between the SMN and aDMN compared with HC (p < 0.05, FDR
corrected). Color scale denotes the t value. Warm color represents
positive functional connectivity; cold color represents negative func-
tional connectivity. X, Y, Z, Montreal Neurological Institute coordi-
nates. L left, R right, SMN sensorimotor-related network, aDMN
anterior default mode network, OAB overactive bladder, HC healthy
control

13

Correlation analysis of FC with neuropsychological
test scores and clinical characteristics
The Pearson correlation analysis demonstrated no significant
correlation between altered FC values and any clinical vari-
ables in patients with OAB.
Discussion
In this study, we analyzed the intra-network and inter-net-
work FC of the RSN based on the resting-state ICA. We
found that the intra-network FC within the SMN, DAN,
dVN, and LFPN was decreased in OAB patients. The inter-
network FC between the SMN and the aDMN decreased in
OAB patients. The results indicate that OAB might lead to
abnormal FC of intra- and inter-RSNs.
The SMN includes somatosensory (e.g., postcentral
gyrus) and motor (e.g., precentral gyrus) regions and extends
to the supplementary motor areas. Studies have shown that
this network is activated during bimanual motor tasks, indi-
cating that these regions may involve a pre-mediated state
that prompts the brain in performing/co-ordinating a motor
task [9]. Specially, the sensorimotor networks are now con-
sidered to participate in bladder control [10]. The overactive
bladder may be represented in persistent or disordered pro-
cessing of bladder signals. Sensorimotor integration coor-
dinated the function of multiple brain regions in preparation
for motor responses to sensory inputs (i.e., bladder signals)
[11]. The supramarginal gyrus is an important node of the
SMN, which is activated under micturition condition using
fMRI with simultaneous recordings of urodynamic prop-
erties during slow bladder filling and voiding [12]. In our
study, we found that FC decreased in bilateral supramarginal
gyrus in OAB patients compared to healthy controls.
Referring to the inter-network comparison, FC between
the SMN and the aDMN decreased in OAB patients. Recent
fMRI studies have highlighted the default mode network
(DMN), which consists of the medial prefrontal cortex
(mPFC), posterior cingulate cortex (PCC)/precuneus (PCu),
inferior parietal lobe, lateral temporal cortex, and hippocam-
pal formation [13]. Activities of DMN were enhanced during
rest and sleep, and suppressed when performing tasks [14].
An extensive body of literature on the ICA has indicated that
the DMN was generally divided into two portions: anterior
DMN (aDMN) and posterior DMN (pDMN) [15]. Among
the primary nodes of the aDMN, the PFC and ACC have
been identified as cortical regions that are involved in mictu-
rition, controlling the inferior architecture in the hierarchical
brain–bladder control network. The PFC plays a vital role
in planning complex cognitive behaviors and performing
appropriate social behaviors. It is currently thought that the
PFC inhibits and excites the micturition process [5]. The
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World Journal of Urology
activation of the PFC is specifically relevant to determining
whether to start micturition [16]. In previous studies, the
ACC was implicated in not only the sensation of bladder
volume and micturition control, but also the emotional and
motivational aspects of micturition [17, 18].
Consistent across all these findings is that the integration
of these RSNs, such as the SMN and aDMN, is affected in
OAB patients. It is acknowledged that the structure connec-
tivity is the substrate of FC, and the aDMN and SMN are
extensive anatomical connections with each other [19]. As
mentioned previously, our results suggested that decreased
FC between SMN and aDMN may reflect decreased func-
tional interactions between these two RSNs, which may fur-
ther lead to bladder dysfunction. The aDMN and the SMN
are more likely to be parts of a circuit that processes sensory
evidence to compute a decision and translates this evidence
into an action.
Apart from the SMN, we also found decreased FC within
the DAN, LFPN, and dVN. It is generally accepted that the
DAN and the LFPN are the subsystems of the frontoparietal
control system [20]. Extensive evidence suggests that the
frontoparietal control system consists of highly intercon-
nected cortical regions and implements cognitive control
[21]. The LFPN, mainly including the superior parietal
lobule, middle frontal gyrus, and inferior parietal lobule,
is thought to be especially involved in highly adaptive
control processes [22]. The DAN, mainly including the
superior parietal lobe, intraparietal sulcus, and frontal eye
fields, is thought to coordinate attentions to external stimuli
[23]. The visual network (VN) is classified into dorsal VN
(dVN) and ventral VN [24]. According to the existing lit-
erature, the dVN processes information about object loca-
tions, and mediates the visual control of skilled actions [25].
The brain–bladder control network performs complicated
sensory, motor, emotional, and cognitive processing of the
afferent signals arising from a filling bladder, to appraise
them in the social context and react appropriately [26].
Thus, decreased FC within the DMN, LFPN, and mVN,
respectively, may have an effect on overactive bladder. Fur-
thermore, we proposed that the FC within the DAN, dVN,
and LFPN may also be the foundation of the brain–bladder
control network.
Several limitations should be considered in this study.
First, the current study was built on only a cross-sectional
design. It would be more helpful for us to examine the
dynamic changes in multiple network functional connectivi-
ties longitudinally to understand the mechanism of OAB.
Further studies should focus on the alteration of multiple
network functions after treatment and investigate whether
these alterations can be used to predict long-term blad-
der functions. Second, the cohort of our patients is rela-
tively small, and further subdivisions of OAB patients may
exhibit more detailed relationships between the patterns of
World Journal of Urology
functional connectivity and severity of symptoms. Finally,
we did not assess the task-state fMRI, which may serve to
clarify the functional role of our findings. Task-state studies
are necessary to validate these interpretations of our results.
Conclusions
We demonstrated that abnormal FC between RSNs may
reflect the neuroimaging characteristics of the brain–bladder
network. The RSNs in OAB patients are not restricted to the
SMN, but rather spread to other neural networks. The intra-
and inter-network FC alterations involved several important
hubs in the brain–bladder network. Our findings provide
complementary evidence that can help further understand
the neural substrates of the overactive bladder, shedding
light on potential behavioral treatments of the OAB based
on fMRI in clinical practice.
Author contributions  LZ: data collection or management, data analy-
sis, manuscript writing and editing. JC: data analysis, manuscript writ-
ing and editing. SW: protocol/project development. YZ: data collection
or management. BW: data collection or management. HG: protocol/
project development.
Funding  This study was supported by grants from the National Nature
Science Foundation of China (No. Grant nos. 81541129, 81301016,
KZ73100001) and the Beihang University Research Fund Program
under Project ZG216S1871.
Compliance with ethical standards  4):781–789
Conflict of interest  All the authors declare that they have no conflict
of interest to declare.
Research involving human participants and/or animals  Human par-
ticipants: yes; animals: no. This study was approved by the Committee
for Human Research in Beijing Chaoyang Hospital and followed by all
regulations (Grant nos. 2015-ke-21).
Informed consent  All the patients have provided informed consent.
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