2694 Chin Med J 2012;125(15):2694-2700

Original article
Functional organization of complex brain networks modulated by
acupuncture at different acupoints belonging to the same
anatomic segment
CHEN Shang-jie, MENG Lan, YAN Hao, BAI Li-jun, WANG Fang, HUANG Yong, LI Jian-ping,
PENG Xu-ming and SHI Xue-min
Downloaded from https://journals.lww.com/cmj by BhDMf5ePHKav1zEoum1tQfN4a+kJLhEZgbsIHo4XMi0hCywCX1AWnYQp/IlQrHD3fgGGXf0fUkCsUCQydWvpVAyNqQm5+mIGcC4MwJaRfb+I/WBScl7U4w== on 05/10/2020

Keywords: acupuncture; functional magnetic resonance imaging; complex brain networks

Background Noninvasive functional magnetic resonance imaging (fMRI) techniques have opened a “window” into the
brain, allowing us to investigate the anatomical and physiological function involving acupuncture needling. Imaging its
sustained effect rather than acute effect on the brain networks may further help elucidate the mechanisms by which
acupuncture achieves its therapeutic effects. In this study, we aimed to investigate the functional brain networks during
the post-resting state following acupuncture at KI3 in comparison with acupuncture at GB40.
Methods Needling at acupoints GB40 and KI3 was performed in twelve subjects. Six minutes of scanning at rest were
adopted before and after acupuncture at different acupoints. Then we divided the whole brain into 39 regions and
constructed functional brain networks during the post-acupuncture resting states (PARS).
Results For direct comparisons, increased correlations during post-resting state following acupuncture at KI3
compared to resting state (RS) were primarily located between the dorsolateral prefrontal cortex (DLPFC) and post
temporal cortex, ventromedial prefrontal cortex (vmPFC) and post temporal cortex. These brain regions were all
cognitive-related functions. In contrast, the increased connections between the anterior insula and temporal cortex
mainly emerged following acupuncture at GB40 compared with the RS.
Conclusions The present study demonstrates that acupuncture at different acupoints belonging to the same anatomic
segment can exert different modulatory effects on the reorganizations of post-acupuncture RS networks. The
heterogeneous modulation patterns between two
conditions may relate to the functional specific modulatory DOI: 10.3760/cma.j.issn.0366-6999.2012.15.009
effects of acupuncture. Department of Acupuncture, Baoan Hospital, Southern Medical
Chin Med J 2012;125(15):2694-2700 University, Shenzhen, Guangdong 518101, China (Chen SJ and
Wang F)
Department of Acupuncture, The First Affiliated Hospital, Tianjin
A cupuncture, originated in China over two millennia
ago, is emerging as an important modality of
complementary medicine in the Western world. For
University of Traditional Chinese Medicine, Tianjin 300193, China
(Chen SJ and Shi XM)
Department of Anesthesiology, Beijing Tiantan Hospital, Capital
example, a promising efficacy of acupuncture has been Medical University, Beijing 100050, China (Meng L)
shown in the treatments of headache, nausea and School of Psychology, Shaanxi Normal University, Xi’an, Shaanxi
710062, China (Yan H)
vomiting. It has also become a beneficial adjunct for pain Department of Linguistics, Xidian University, Xi’an, Shaanxi
1,2
management, earache, and vascular dementia. 710126, China (Yan H)
However, there is little unequivocal scientific explanation Institute of Automation, Chinese Academy of Sciences, Beijing
regarding the physiological mechanism of acupuncture 100190, China (Bai LJ)
and it awaits further investigations. Department of Radiology (Huang Y and Li JP), Department of
Acupuncture and Massage (Peng XM), the First Affiliated
Hospital, Guangzhou University of Traditional Chinese Medicine,
In the past decades, noninvasive fMRI techniques have Guangzhou, Guangdong 510405, China
opened a “window” into the brain, allowing us to Correspondence to: Dr. PENG Xu-ming, the First Affiliated
investigate the anatomical and physiological function Hospital, Guangzhou University of Traditional Chinese Medicine,
3–7 Guangzhou, Guangdong 510405, China (Fax: 86-755-27751033.
involving acupuncture needling. Converging evidences
Email: pxmgztcm@126.com)
from functional magnetic resonance imaging (fMRI) This study was supported by the grants from the National Natural
studies have demonstrated that acupuncture stimulation Science Foundation of China (No. 81071217 and 81173354), the
can modulate neural activities in a wide Project for the National Key Basic Research and Development
cortico-subcortical network.3,4,8,9 Most of these studies Program (973) (No. 2010CB530506), the Natural Science
generally adopted a multi-block experimental paradigm Foundation of Guangdong Province (No. 10451810101005862 and
10,11 8451040701000553), the Fundamental Research Funds for the
and the general linear model (GLM) approach. With Central University, the Beijing Nova Program (No.
this approach, a specific stimulus sequence (i.e., design Z111101054511116), Beijing Natural Science Foundation (No.
matrix) is used to define an ideal hemodynamic response 4122082) and the Administration of Traditional Chinese Medicine
function (HRF), which is convolved with the of Guangdong Province (No. 20111032).
Chinese Medical Journal 2012;125(15):2694-2700
experimental paradigm and produces predictors of the
blood oxygenation level-dependent (BOLD) response.
The inferences derived from the GLM estimates are
completely limited by the design of the experimental
paradigm and whether the stimuli are under relatively
precise experimental control (i.e., they can be turned on
and off repeatedly).11 For a block-designed fMRI
paradigm, the temporal changes in the BOLD signal, as
predicted by the GLM, conform to the “on-off”
specifications set by the experimenter. However,
abundant clinical evidence has demonstrated that
acupuncture effects can persist even beyond the
acupuncture needling being terminated.12 Psychophysical
analysis from Price et al13 further indicates that the
analgesic effects of acupuncture may actually peak long
after the needling session. Since the effects of
acupuncture may be sustained for relatively long
durations,14-16 the temporal profile of BOLD responses to
acupuncture may violate the assumptions of the
block-designed GLM estimates.17 Further analyses may
be susceptible to errors of statistical significance.11
Imaging its sustained effect rather than the acute effect on
the brain networks may further help elucidate the
mechanisms by which acupuncture achieves its
therapeutic effects.
Recently, increasing attention has been focused on
detecting interregional connectivity in the resting state
(RS) and demonstrated that the spontaneous fluctuations
of BOLD signals are coherent within specific
neuroanatomical systems in the human brain.18,19 Due to
the sustained effects of acupuncture, some studies began
to explore its modulatory effects on the reorganizations of
the functional brain networks.5,10 Acupuncture has shown
promise in treating chronic pain and other disorders by
mobilizing the neurophysiological system to modulate
multisystem functions.10,20 Thus, these vital functions
may be typically delayed from the needle stimulation
phase, 21 and exert a sustained modulatory effect on the
spontaneous coherences of the post-stimulus “resting”
brain.10 Moreover, it should also be noted that the
previous studies generally adopted the standard functional
connectivity (FC) analysis, and primarily focused on the
correlation patterns between a specific region (so-called
‘‘seed”) and other brain structures, depicting a network
only related to one certain brain function. Although
seed-based analysis can identify brain regions
functionally connected to the initially selected seed, it is
unable to completely characterize the joint interactions
among multiple brain regions.15
In the present study, we adopted a graph theory analysis
(GTA) to investigate the organization of complex brain
networks before and after acupuncture at two different
efficacy-related acupoints belonging to the same
anatomic segments. GTA has the advantages of
evaluating the strength as well as the temporal and spatial
patterns of interactions in the human brain, which defines
a graph as a set of nodes (brain regions) and edges
2695
(functional connections).15,22,23 Discerning the differences
between these graphs under different states may help us
to better understand the neural modulatory effects on the
resting brain networks underlying acupuncture.
METHODS
Subjects
In order to reduce the influence of individual variability,
all participants were recruited from a homogeneous group
of 12 college students (three female, ages of 22–26 years
old). All subjects were healthy, body weight index (BMI)
20–24 kg/m2, right handed, and acupuncture naive.
Subjects were screened to assure their safety and
compatibility with MRI recording. Exclusion criteria
were a history of surgery, severe hearing and speech
dysfunction, any neurological or medical disorder that
would impact the central nervous system, any
contraindications to a high magnetic field, as well as any
past or current history of psychiatric disorder, substance
abuse or treatment with psychiatric medications. After a
complete description of the study was given to all
subjects, written informed consent was obtained, as
approved by a local institutional review board for human
studies. All subjects were treated in accordance with the
Declaration of Helsinki.
fMRI task design
The fMRI scanning consisted of three runs. Acupuncture
stimulus incorporated a block design paradigm with three
cycles, 1 minute OFF and 1 minute ON epoch. There was
also a 6-minute RS scanning before and after
acupuncture. According to both the converging clinical
reports and the theory of the traditional Chinese medicine
(TCM), the effects of acupuncture may induce
long-lasting post-administration effects, even for several
hours.12 Therefore, RS after acupuncture stimulus was
employed to investigate the sustained effects of
acupuncture in the current study, compared with the RS
before acupuncture intervention. Acupuncture needling
manipulation was performed at acupoints KI3 and GB40
(Figure 1) on the right leg.
All participants were asked to remain relaxed without
engaging in any mental tasks. To facilitate blinding, they
were also instructed to keep their eyes closed to prevent
observing the procedures. According to participants’
reports after the scanning, they affirmed staying awake
during the whole process. The presentation sequence of
acupuncture at different acupoints was randomized and
balanced throughout the population, and every participant
experienced only one acupuncture stimulus each day. In
order to eliminate potential long-lasting effects following
acupuncture administration, the two sessions were
performed at an interval of at least one week, depending
on scanner availability and the scheduling needs of the
subjects.
The acupoint KI3 is located in the depression between the
2696
Figure 1. A: Anatomical locations of the acupuncture stimulation points of KI3 (right) and GB40 (right). B: Experimental paradigm.
Functional run incorporates the block design paradigm with three cycles, 1 minute ON (A1/A2/A3) and 1 minute OFF (R1/R2/R3) epoch.
A 6-minute RS scanning was done before and after acupuncture.
prominence of the medial malleolus and heel tendon. The
acupoint GB40 is located at anterior of and inferior to the
external malleolus, in the depression on the lateral side of
the tendon of extensor digitorum longus (Figure 1).
Acupuncture was performed by first inserting a
non-magnetic (85% silver content), 0.32 mm diameter, 25
mm long acupuncture needle (Acupuncture Supplies
Company in Suzhou, China) into acupoints to a depth of
approximately 15 mm. During stimulation, the needle
was manually twirled (about ±60°) at approximately a
rate of 120 times per minute. The procedure was
performed on all the subjects by the same experienced
and licensed acupuncturist.
fMRI image acquisitions
Images were obtained on a 3-T Phillips scanner using a
standard whole head coil. A custom-built head-holder was
used to prevent head movement. fMRIs were obtained
using a gradient echo T2*-weighted pulse sequence with
TR = 2000 ms, TE = 50 ms, matrix = 64 × 64, field of
view (FOV) = 230 mm × 230 mm and flip angle (FA) =
90°. Then thirty slices (6 mm thickness, no gap) oriented
parallel to the AC-PC line were collected to cover the
whole brain. The scan covered the entire brain, including
both the cerebellum and the brainstem. Prior to the
functional run, high-resolution structural information on
each subject was acquired using 3D MRI sequences
(TR=25 ms, TE=4 ms, FOV=230 mm × 230 mm,
Matrix=256 × 256, slices=140) for anatomical localizations.
Deqi sensations
After each scan, the subjects were asked to quantify on a
10-point scale to self-rate the intensities of the deqi
sensations they had felt during the stimulation (0=no
sensation, 1–3=mild, 4–6=moderate, 7–8=strong,
9=severe and 10=unbearable sensation). The deqi
sensations consist of the following sensations: aching,
pressure, soreness, heaviness, fullness, warmth, coolness,
numbness, tingling, and dull pain.
Statistical analysis
Datasets were corrected initially for geometrical
displacements because of estimated head movement and
coregistration with the Montreal Neurological Institute
(MNI) EPI template image, using an affine transform
implemented in SPM5 software (www.fil.ion.ucl.ac.uk/
spm). Due to the instability of the initial signals and to
Chin Med J 2012;125(15):2694-2700
allow for the subjects’ adaptation to the situation, the first
10 images were discarded.24,25 The remaining images
were first corrected for within-scan acquisition time
differences between slices and then realigned to the first
volume to correct for head motion (none of the subjects
had head movements exceeding 2 mm on any axis or
head rotation greater than 1.5 degree). The data were not
specially smoothed before regional parcellation. This
parcellation divided each cerebral hemisphere into 39
anatomical regions of interest (Table 1). Regional mean
time series was estimated for each individual by
averaging the fMRI time series over all voxels in each of
the 39 regions. Each regional mean time series was
further corrected for the effects of head movement by
regression on the time series of translations and rotations
obtained from the initial movement correction of image
realignment.
Each ROI was correlated to every other ROI to obtain a
39×39 matrix of correlation coefficients, and the mean
FC matrix was computed by averaging the entirety of
correlation matrixes. We then created an unweighted
binary graph in which the nodes were connected if the
correlation coefficients exceeded the threshold (Fisher’s
r-to-z transformation was applied). For direct analysis of
the brain network, single nodes were deleted by the
artificial settings. To characterize the interregional
relations for our defined ROIs, GTA defined a graph as a
set of nodes and edges.26 In our study, we applied the
correlation method of estimation of the inter-regional
partial correlations and testing for non-zero partial
correlations described by Salvador et al to construct the
brain networks.27 Given a set of random variables, the
partial correlation matrix is a symmetric matrix in which
each off-diagonal element is the correlation coefficient
between a pair of variables after partialling out
(conditioning under normality) the contributions to the
pairwise correlation of all other variables included in the
dataset. To estimate the partial correlation matrix, we
used the method based on the fairly general assumption
of multivariate normality of the observations. However,
we were dealing with a series of time points and we
therefore needed to assume jointly Gaussian stationary
multivariate stochastic processes. The partial correlation
matrices individually obtained from each one of the
volunteers were averaged to estimate the group mean
inter-regional functional connectivity matrix.27
Chinese Medical Journal 2012;125(15):2694-2700 2697

Table 1. The coordinates of the 39 anatomical regions of interest

Coordinates
Brain regions
X Y Z
R IPS 30 –61 39
L IPS –31 –59 42
R frontal cortex 41 3 36
L frontal cortex –41 3 36
R precuneus 10 –69 39
L precuneus –9 –72 37
Midcingulate 0 –29 30
R IPL 51 –47 42
L IPL –51 –51 36
R dlPFC 43 22 34
L dlPFC –43 22 34
R al/fO 36 16 4
L al/fO –35 14 5
dACC/msFC –1 10 46
R aPFC 27 50 23
L aPFC –28 51 15
R ant thalamus 10 –15 8
L ant thalamus –12 –15 7
R lat cerebellum 31 –61 –29
L lat cerebellum –32 –66 –29
R inf cerebellum 18 –80 –33
L inf cerebellum –19 –78 –33
R TPJ 53 –46 17
L TPJ –53 –46 17
R midoccipital 27 –89 3
L midoccipital –27 –89 3
R lingual 8 –82 4 Figure 2. Results of psychophysical analysis. A: Percentage of
L lingual –8 –82 4 subjects who reported having experienced the given sensations.
R posttemporal 44 –74 26 B: The intensity of the reported sensations measured by an
L posttemporal –40 –78 24 averaged score (with standard error bars) on a scale from 0
R postcingulate 10 –56 16 (denoting no sensations) to 10 (denoting an unbearable
L postcingulate –11 –57 13 sensation).
R fusiform 35 –65 –9
L fusiform –34 –62 –15
40 belonging to the same anatomic segment. As shown in
R ant fusiform 25 –44 –12
L ant fusiform –25 –44 –12
Figure 3, before acupuncture, there existed significant
R midtemporal 51 –33 –2 functional connectivies in the DLPFC with the
L midtemporal –53 –31 –5 intraparietal sulcus (IPS), precuneus and frontal,
vmPFC 1 31 –2 connections of the anterior insula/frontal operculum
IPS: intraparietal sulcus. IPL: inferior-parietal lobule. dlPFC: dorsolateral (aI/fO) with the anterior prefrontal cortex (aPFC) and ant
prefrontal cortex. al/fO: anterior insula/frontal operculum. dACC/msFC: dorsal
thalamus, connection of the lingual with mid occipital, etc
anterior cingulate cortex/medial superior frontal cortex. aPFC: anterior prefrontal
cortex. ant thalamus: anterior thalamus. lat cerebellum: lateral cerebellum. inf (P <0.05). The network module remained stable after
cerebellum, inferior cerebellum. TPJ: temporal-parietal junction. ant fusiform: acupuncture in addition to change of the connection
anterior fusiform. vmPFC: ventral medial prefrontal cortex. patterns of local nuclei. Moreover, the connection modes
in acupuncture at different points after were also
different. Trends toward increases in the connections of
RESULTS the DLPFC with the parietal and temporal, vmPFC with
post temporal, mid occipital with lingual, thalamus with
The prevalence of these deqi sensations was expressed as fusiform were observed during PARS at KI3 in contrast to
the percentage of the individuals in the group that RS (P <0.05). However，an increased tendency was
reported the sensation (Figure 2). A statistical analysis presented in the connection of the aI/fO with temporal
found no significantly difference between the GB40 during PARS at GB40 compared with RS (P <0.05).
group and KI3 group in regard to the prevalence of these
sensations (paired t test, P >0.05). The stimulus intensity DISCUSSION
was expressed as the average score±SE (Figure 2). The
average stimulus intensities (mean±SE) were 2.72±0.65 Previous neuroimaging studies have typically focused on
at GB40 and 2.19±0.57 at KI3. Significant differences the acute effects of acupuncture and demonstrated
could be found in soreness, fullness, throbbing, tingling extensive BOLD signal changes. However, the
and sharp pain (paired t test, P <0.05). interactions of these wide brain areas following
acupuncture at different acupoints still need to be
We adopted a graph theory method to evaluate the illuminated.28,29 Understanding the organization of neural
reorganizations of complex brain networks before and activities at the whole-brain level is of great importance.
after acupuncture at two different acupoints KI 3 and GB Moreover, acupuncture has shown its promise in the
2698
Figure 3. Functional connectivities of brain network derived from resting state (A), post-acupuncture resting state (B) following
acupuncture at KI3 and GB40 (C).
treatment of chronic pain and other disorders by
mobilizing the neurophysiological system to modulate
multisystem functions.5,10 These vital functions may be
typically delayed from the needle stimulation phase, and
exert the sustained modulatory effect on the spontaneous
coherences of the post-stimulus resting brain.5,10,11,22 In
the present study, we investigated the organizations of
complex brain networks during the RS before and after
acupuncture at two different efficacy-related acupoints.
Recently, increasing attentions have been focused on
detecting interregional connectivity in the RS, which is
usually described in terms of FC.14,15 It should be noted
that the previously used standard FC analysis that
primarily focused on the correlation patterns between a
specific region (so-called ‘‘seed”) and other brain
structures, depicting a network related to one certain
brain function. Although seed voxel-based analysis can
identify brain regions functionally connected to the
initially selected seed region, it is unable to completely
characterize the joint interactions among multiple brain
regions. By the graph mode instead of conventional
pairwise FC analysis, not only can we use connectivity
degrees to quantify the importance of nuclei implicated in
the network, but also we can investigate the network
modulation patterns by detecting the changes in the nuclei
connectivity graph under different states.15
The pattern of the complex brain network during the RS
reflected connections of the DLPFC with IPS, precuneus
and frontal, connections of the al/fo with aPFC and ant
thalamus, connection of the lingual with mid occipital,
etc. Our results are consistent with many previous studies
of FC.22,30,31 However, there was a different complex
brain network when stimulating different acupionts in the
same anatomic segment. Although KI3 and GB40 are
located in the same anatomic segment, and there was no
significant difference between the GB40 group and KI3
group in regard to the prevalence of these sensations, our
results confirmed the different roles of acupoints related
to the theory of TCM.
Chin Med J 2012;125(15):2694-2700
Our study indicates that increased connections occur
between the DLPFC with the parietal and temporal,
between the vmPFC with the post temporal, between the
mid occipital with the lingual, between the thalamus with
the fusiform during PARS at KI3 in contrast to RS. The
DLPFC plays a role in sustaining attention and working
memory.32,33 Lesions to the DLPFC can impair the
short-term memory and cause difficulties in inhibiting
responses.32 In addition, the DLPFC has recently been
found to be involved in exhibiting self-control.33 The
vmPFC is a part of the prefrontal cortex in the
mammalian brain, which is shown on medial and ventral
views of the brain, reflecting the approximate location of
damage in patients with decision making deficits.34,35
Activity in the vmPFC is related with goal values
regardless of the amount of self-control. It incorporates
both taste and health in self-controllers but only taste in
non-self-controllers. From this evidence we speculated
that activity in the DLPFC increases when subjects
exercise self-control and is correlated with activity in the
vmPFC.33 The occipital lobe is the visual processing
center of the mammalian brain, containing most of the
anatomical region of the visual cortex.36 The lingual
gyrus is believed to play an important role in dreaming
and vision, especially in recognizing words, regardless of
such things as the size or the font. fMRI signals in the
human lateral geniculate nucleus (LGN) of the thalamus
are correlated with fluctuations in both visual attention
and visual awareness.37,38 From our results, the cognitive
and visual function-related brain networks emerged
following acupuncture at KI3. Based on TCM theory, KI3
is the Yuan-Source Point of the kidney channel which can
treat disease of the kidney and the kidney channel; such
as forgetfulness, dementia (cognitive impairment), and
myopia.39,40 Therefore, the cognitive and visual
function-related brain networks may relate to the
therapeutic effects of acupuncture at acupoint KI3.
In addition, our results also presented an increased
tendency in the connection of the aI/fO with the temporal
during PARS at GB40 compared with RS. The aI/fO is
the convergence of all sensory information. In humans, a
Chinese Medical Journal 2012;125(15):2694-2700
metarepresentation of the primary interoceptive activity is
engendered in the right anterior insula, which seems to
provide the basis for the subjective image of the material
self as a feeling (sentient) entity, that is, emotional
awareness. The primary auditory cortex is located in the
temporal lobe. The results show that the auditory
function-related brain network emerges following
acupuncture at GB40. Based on TCM theory, GB40, that
is Yuan-Source Point of the Gall-bladder (GB) Channel,
can treat disease of GB organ and GB channel, such as
tinnitus, cholecystitis, paralysis, pain in the malleolus
joint.39,40 The auditory function-related brain network
following acupuncture at GB40 may indicate the
therapeutic action of acupuncture at acupoint GB40
consistent with TCM theory.
In this paper, we demonstrate distinct modulatory effects
on the reorganization of brain networks during the PARS
following acupuncture at GB40 and KI3. It is reported
that the FC of this network maintains a dynamic
equilibrium and is reorganized by exerting distinct
functions on the human brain. Moreover, our findings
also indicate that acupuncture at different acupoints may
induce specific patterns of functional connectivities,
which are related to the therapeutic effects of
acupuncture. Our analysis for the development of distinct
brain networks following acupuncture was limited to
predefined ROIs. Therefore, we may not describe the
comprehensive characteristic of brain networks involving
acupuncture. Further evidence needs to be obtained about
the brain functional network after acupuncture
manipulation. Moreover, based on the theory of TCM, it
may exert a more direction role when acupuncture is
given to patients with a certain disease instead of normal
subjects. Therefore, we will further investigate the brain
functional network after acupuncture manipulation on
patients with particular disease.
In conclusion, the present study demonstrates that
acupuncture at different acupoints may exert different
modulatory effects on the reorganizations of
post-acupuncture RS networks. The heterogeneous
modulation patterns between two conditions may relate to
the functional specific modulatory effects of acupuncture.
The preliminary findings may help us to better understand
the long-lasting effects of acupuncture on the entire
resting brain, as well as the neurophysiological
mechanisms underlying acupuncture.
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(Received November 24, 2011)
Edited by WANG De