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Altered Amplitude of Low-Frequency Fluctuation Induced by Acupuncture at Baihui Acupoint: A Pilot Functional MRI Study

Demao Deng1, Gaoxiong Duan1, Yanfei Liu2, Hai Liao1, Geliang Wang2, Huimei Liu3, Lijun Tang3, Yong Pang3, Jie Tao3 and Peng Liu2*
1Department of Radiology, First Affiliated Hospital, Guangxi University of Chinese Medicine, Nanning, Guangxi 530023, China
2Life Science Research Center, School of Life Science and Technology, Xidian University, Xi’an, Shaanxi 710071, China
3Department of Acupuncture, First Affiliated Hospital, Guangxi University of Chinese Medicine, Nanning, Guangxi 530023, China
Corresponding Author : Peng Liu
Life Sciences Research Center, School of Life Sciences and Technology
Xidian University, Xi’an, Shaanxi 710071, China
Tel: +86 29 81891070
E-mail: liupengphd@gmail.com
Received: July 24, 2015 Accepted: August 28, 2015 Published: September 4, 2015
Citation: Deng D, Duan G, Liu Y, Liao H, Liu P, et al. (2015) Altered Amplitude of Low-Frequency Fluctuation Induced by Acupuncture at Baihui Acupoint: A Pilot Functional MRI Study. Altern Integr Med 4:197. doi:10.4172/2327-5162.1000197
Copyright: © 2015, Deng D, et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
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Abstract

Baihui (GV20), an important acupoint of the Governor Vessel according to the traditional Chinese medicine (TCM) theory of acupuncture, is usually used for treatments of psychiatric disorders. However, studies about relationships between the brain activities and GV20 are limited. In the present study, we thereby tried to investigate specific pattern of brain activities induced by electroacupuncture stimulation (EAS) at GV20. Thirty three healthy subjects were enrolled in this study for MRI scanning. Each subject underwent EAS at GV20 and at sham acupoint, separately. Based on sustained effects of acupuncture, amplitude of low-frequency fluctuation and fractional amplitude of low-frequency fluctuation (ALFF/fALFF) methods were used to examine different ALFF and fALFF patterns of the whole brain induced by GV20 with comparison to the ones induced by sham acupoint. Results showed that GV20 induced altered ALFF/fALFF in the brain regions, including the medial prefrontal cortex (mPFC), orbital frontal cortex (OFC), dorsolateral prefrontal cortex (dlPFC) and middle cingulate cortex (MCC), temporal cortex (TC), supplementary motor area (SMA), precuneus, thalamus, hippocampus (HIPP), insula, putamen and cerebellum compared to sham acupoint. Our findings might present the specific neural responses to EAS at GV20 using ALFF and fALFF methods, and may further provide preliminary evidence for understanding the mechanisms of GV20.

Keywords
Acupuncture; Baihui; Amplitude low-frequency fluctuation; fMRI
Introduction
As a vital part of traditional Chinese medicine (TCM), acupuncture has been used in the Orient for thousands of years. Because of its treatment effects, safety and convenience, acupuncture has been recognized as an alternative and complementary therapeutic intervention in Western medicine [1]. Nowadays, acupuncture has emerged as indispensable component of modern medicine. However, the elusive neural mechanisms underlying acupuncture hampers its progress. There is a need to explore acupuncture mechanisms. To date, modulatory effects on central nervous system (CNS) have been proposed as an important mechanism of acupuncture [2].
With the development of functional magnetic resonance imaging (fMRI), changes in blood flow in cerebral functional regions can be monitored by the blood oxygenation-level-dependent (BOLD) method. Consequently, the central mechanisms of acupuncture can be identified using this neuroimaging methods. Based on healthy subjects, functionally specific effects of certain acupoints on activities of brain regions have been examined [3-11]. For example, Hui et al. found the integrated response of the cerebro-cerebellar and limbic systems induced by acupuncture stimulation at Hegu (LI4) or Zusanli (ST36) in normal subjects [6,7]. Napadow et al investigated differences of brain activities between electroacupuncture versus manual acupuncture in healthy subjects measured by fMRI [11]. Moreover, it has been reported that the default mode (DMN) and/or sensorimotor brain networks of healthy subject could be modulated by acupuncture at different acupoints compared to a sham or placebo control procedure [5,8]. Evidence from these studies have revealed that neuroimaging studies centering on healthy subjects are potentially valuable to investigate central mechanism of acupuncture.
Most of previous neuroimaging studies have mainly focused on neural responses to acupuncture stimulation at the acupoints associated with vision, auditory and pain processing on healthy subjects [3-11]. However, limited neuroimaging studies have demonstrated neural responses induced by stimulations at certain acupoint involved in treatments of psychiatric disorders. Baihui (GV20), located at the intersection of the line connecting the midsagittal line of the head and the apexes of the two auricles, is an important acupoint of the Du meridian on the basis with TCM theory.
GV20 is commonly applied to treatments of psychiatric disorders such as dizziness, headache, stroke and anxiety [12,13]. Recently, it is has been reported that stimulations at the combination of GV20 and other acupoints improve cognitive impairment in dementia [14,15], and modulate mental disorders [16-19]. This raised one interesting question: whether acupuncture stimulation at GV20 might produce functionally specific effects in brain with comparison to a sham acupoint as control. To our knowledge, few studies have attempted to explore relationship between specific effects of GV20 and activated neural pattern of the whole brain.
In the current study, we thereby tried to conduct a pilot study to investigate specific patterns of brain activities induced by electroacupuncture stimulation (EAS) at GV20 in healthy subjects using fMRI. Based on sustained effects of acupuncture, the nonrepeated event-related (NRER) paradigm [20] and amplitude lowfrequency fluctuation [21,22] and fractional amplitude low-frequency fluctuation [23] (ALFF/fALFF) method were applied to examine differences between GV20 and sham acupoint in this study. Here, we hypothesized that there were distinct patterns of the whole brain activities induced by EAS at GV20 compared to sham acupoint, and the modulated brain regions could be associated with emotion and pain processing, which could attributed to specific characteristics of GV20.
Materials and Methods
Subjects
Thirty three healthy right-handed subjects participated in the present study (15 males, 18 females; 25.10 ± 1.67 years old; 167.52 ± 9.17 centimeter height and 60.24 ± 13.50 kilogram weight). Subjects were acupuncture-naïve, no smokers, and had no history of neurological or psychiatric disorder and had refrained from alcohol or drug consumption in the previous at least 48 hours. Female subjects were required to be out of menstrual and suckling period. Every subject was given informed consent approved by the local review board for human studies. All research procedures of the present study were conducted in accordance with the Declaration of Helsinki.
The NRER paradigm was adopted in the current study [20]. EAS was separately performed at GV20 or sham acupoint on each subject (Figure 1A). Sham acupoint was chosen approximately 5 cm at the right side of GV20, and was located out any classically defined acupoint or meridian structure.
EAS was delivered using pure stainless steel disposable needle with 0.30 mm in diameter and 25 mm in length (HuaTuo-brand, Suzhou, Jiangsu, China). Two electrodes were separately attached to acupuncture needle and another needle inserted point 1 cm nearby GV20 or sham acupoint. EAS was operated by the same professional acupuncturist with 1 Hz, 2 mA, and continuous-wave (HuaTuobrand, SDZ-V-type, Shanghai). Before the first scanning, each subject was also introduced to the principles of acupuncture and fMRI to reduce anxiety.
During each scanning, the experiment lasted 32 minutes, including a 6-minute natural resting scanning, a 20-minute EAS and another 6- minute resting scanning after EAS with needle removed (Figure 1B). At the end of scanning, each subject was required to recall acupuncture sensations including aching, soreness, numbness, fullness, sharp or dull pain, pressure, heaviness, warmth, coolness, tingling, itching and any others. The intensity of each sensation was measured using a 100-point visual analogue scale (0=no sensation, 10-30=mild, 40-60=moderate, 70-80=strong, 90=severe and 100=unbearable sensation). Considering sustained effects of acupuncture, each subject underwent EAS at sham acupoint, and seven days later, EAS at GV20 (Figure 1C).
Imaging data acquisition
Images were collected using a 3T Siemens scanner (Allegra; Siemens Medical System) at the Department of Radiology, First Affiliated Hospital, Guangxi University of Chinese Medicine, Nanning, Guangxi, China. In order to minimize the head motion to diminish scanner noise, a standard birdcage head coil was used along with a restraining foam pad. Functional images were acquired with a single-shot gradient-recalled echo planar imaging (EPI) sequence (TR/ TE=2000 ms/30 ms, FOV=240 mm × 240 mm, matrix size=64 × 64, flip angle=90° and 31 slices). A set of T1-weighted high-resolution structural images was also collected (TR/TE=1900 ms/2.22 ms, FOV=250 mm × 250 mm, matrix size: 250 × 250, flip angle=9°, slice thickness=1 mm and 176 slices).
Imaging data analysis
Resting-state fMRI data preprocessing was carried out using statistical parametric mapping software (SPM8, http:// www.fil.ion.ucl.ac.uk/spm). The first 10 functional volumes were removed because of instability of the initial MRI signal and adaptation of participants to the environment. The remaining volumes were analyzed. For each subject, fMRI images were slice-time corrected, head-motion corrected (a least squares approach and a six-parameter spatial transformation). Subjects with head motion >1.5 mm of maximal displacement (in any direction of x, y, or z) or 1.5°of maximal rotation throughout the course of scanning were excluded from further analysis. After realignment, all of the data were normalized to the standard Montreal Neurological Institute (MNI) template, and then resampled into 3×3×3 mm3 resolution. Next, smoothing with a Gaussian kernel of 4-mm full-width at half maximum (FWHM) and then removed the linear trend. To reduce low-frequency drift and high-frequency respiratory and heart rhythms, fMRI data were temporally bandpass filtered (0.01-0.08 Hz). Six head motion parameters, the global mean signal, the cerebrospinal fluid (CSF), and the signals from white matter as nuisance covariates to reduce the effects of head motion and non-neuronal BOLD fluctuations [24,25].
For calculating ALFF and fALFF, data processing assistant for resting-state fMRI (DPARSF) software [26] was applied in our study. The time series of each voxel was transformed to a frequency domain with a fast Fourier transform (FFT) and the power spectrum was obtained. Due to the fact that the power of a given frequency was proportional to the square of the amplitude of the frequency component of original time sequence in the time domain, the square root calculation was taken at each frequency in the power spectrum, and then the averaged square root was managed across 0.01-0.08 Hz at each pixel. This averaged square root which was supposed to report the absolute intensity of brain spontaneous activity was known as the ALFF [27]. fALFF was calculated as the ratio of power spectrum of low-frequency to that of the entire frequency range [28]. To reduce the global effects of variability across the subjects, the ALFF/fALFF of each voxel was standardized by dividing the global mean ALFF/fALFF value [27,29].
At the second-level analysis, a paired t-test was to evaluate differences of the baselines before EAS at GV20 and at sham acupoint. Differences of ALFF/fALFF between GV20 and sham acupoint were then examined by a paired t-test. All of the contrasts were threshold at P<0.05 (family discovery rate (FDR) corrected) and the cluster size >5 voxels. Meanwhile, the age, gender and BMI were deemed as covariates of no interest in the analysis.
Results
Psychophysical data result
All subject kept awake according to their reports after scanning. But four subjects did not complete the whole study. The data of the left twenty-nine subjects (15 males and 14 females) were analyzed in this study. The main sensations included the fullness numbness, soreness and dull pain. The prevalence of Deqi sensations were expressed as the intensity of sensations of individuals as follows: The average soreness rating was 38.66 ± 29.33 at GV20 and 43.00 ± 29.60 at sham acupoint. The average numbness rating was 50.86 ± 32.52 at GV20 and 43.90 ± 33.43 at sham acupoint. The average fullness rating was 63.62 ± 27.58 at GV20 and 56.38 ± 28.78 at sham acupoint. The average dull pain rating was 30.52 ± 33.18 at GV20 and 26.90 ± 23.16 at sham acupoint. There were not significantly statistical differences of Deqi sensations between GV20 and sham acupoint (P>0.05) (Figure 2).
Imaging data result
There were not any differences of ALFF/fALFF during the baseline state (before EAS at GV20 and sham acupoint). However, there were distinct brain maps of ALFF/fALFF after EAS. Results showed that compared to sham acupoint, EAS at GV20 induced increased ALFF in the medial prefrontal cortex (mPFC), orbital frontal cortex (OFC), dorsolateral prefrontal cortex (dlPFC) and temporal cortex (TC). Decreased ALFF was located in the middle cingulate cortex (MCC), supplementarymotorarea (SMA), thalamus, putamen and cerebellum (Figure 3). Meanwhile, results showed that EAS at GV20 also induced increased fALFF in the precuneus (preCUN) and hippocampus (HIPP), and decreased fALFF was found in the MCC, SMA, insula, putamen, cerebellum and brainstem (Figure 4).
Discussion
The goal of the current study was to understand neural responses to EAS at GV20 by examining modulatory amplitude low-frequency fluctuation in the whole brain. Results showed that EAS at GV20 mainly induced altered ALFF/fALFF in the mPFC, OFC, dlPFC, MCC, insula, SMA, preCUN, TC, HIPP, putamen, cerebellum and brainstem. These results may provide further information regarding neurobiological basis of EAS at GV20, and reveal that specific effects of GV20 may attribute to modulating the wide brain regions involved in emotion and pain processing.
We firstly found that EAS at GV20 modulated several subregions of frontal cortex compared to sham acupoint. mPFC is devoted to processing of emotional and social stimuli. mPFC is also associated with self-referential mental activity [30]. dlPFC is a crucial member of the cognitive control network that modulates the effortful control of negative emotion. OFC is implicated in reward processing [31]. Thereby, our results showed that EAS at GV20 improved ALFF in emotion-related brain regions, which might be a reason that GV20 was used to treat psychiatric disorders. Several studies of acupuncture have showed that changes of functional signals or positron emission tomography (PET) in the OFC are related with acupuncture analgesia [32]. Moreover, it has been reported that activities or glucose metabolism in the OFC are relate with episodic migraine [33]. We further speculated that our results might provide potential imaging evidence for understanding the mechanisms of GV20 involving in headache treatments. In addition, increased ALFF in the TC was found in our study. It is not well known that which function the TC is exactly implicated in. To certain extent, TC plays a crucial role in auditory, language processing and memory [34,35]. Furthermore, previous studies have indicated that patients with psychiatric disorders have abnormal activities or structure in the subregions of TC [36,37]. The increased ALFF in the TC might reveal that there existed the relationships between specific effects of EAS at GV20 and modulated TC activities.
Altered ALFF in the MCC and thalamus was found in this study. As a part of the limbic system, MCC is implicated in cognitive processes and emotional integration. Pereira et al found that MCC was an important site for the interaction between negative emotion and motor signals [38]. Thalamus is known as a relay station in relaying sensory and motor signals to the cerebral cortex [39]. Moreover, thalamus is a brain region of interest in the study of mood disorders because it connects subcortical limbic system structures such as the amygdala [40]. We speculated that the decreased ALFF in the MCC and thalamus meant that EAS at GV20 influenced some specific neural activities related with mood modulations.
The increased fALFF in the HIPP and decreased fALFF in the insula were found in the current study. HIPP is enrolled in memory and learned behavior [41]. And HIPP is an important brain region providing inhibitory feedback to the hypothalamic-pituitary-adrenal axis (HPA axis), reacting to stress. HIPP is affected by stress [42-44]. Insula is located in the depth of the cerebral hemisphere by the overlying frontal and temporal opercula, and it is widely connected with cortex, subcortex and brainstem structures. Function of insula is associated with emotion, cognition and pain-related modulation [45-48]. Altered fALFF in these regions further reflected GV20-related modulation for emotion processing.
In the field of resting-state fMRI, ALFF has been used to examine local spontaneous patterns during resting, which measures the total power of a given time course within a specific frequency range (e.g. 0.01-0.08 Hz). ALFF measures the total power of a given time course within a specific frequency range and has been used to examine local spontaneous patterns during resting. Although ALFF is effective at detecting low-frequency oscillations, it may also include lowfrequency oscillations fluctuations over 0.1 Hz. A normalized index of ALFF, fALFF can provide a more specific measure of low-frequency oscillations by measuring the power within a specific frequency range divided by the total power in the entire detectable frequency range.Moreover, the ALFF/fALFF method has been being used in neurological disease, healthy people and acupuncture researches. The present results suggested that the ALFF/fALFF approach was able to identify acupoint specific effects associated with GV20. All of our findings reflected a significant methodological contribution as well.
Some major limitations of this study should be mentioned: (I) our study was only performed on healthy subjects. Neural responses of EAS at GV 20 on patients with psychiatric disorders should be investigated in the future study. (II) Because there were individual differences in acupuncture Deqi sensation, whether variations of Deqi sensation might influence results should be examined in the future. (III) The sample size of subjects in this study was still not too large, the present findings should be retested with a larger sample size in the future as well.
In summary, the present fMRI study used the ALFF/fALFF approach to investigate possible mechanisms of EAS at GV20. Compared to sham acupiont, our results showed that EAS at GV20 induced ALFF/fALFF alternations in the extensive brain networks, including the PFC, OFC, MCC, insula, prePCU, SMA, thalamus, putamen, brainstem and cerebellum. This study might help us to better understand neurophysiological mechanisms underlying GV20 as well as provided potential feasibility of the amplitude of lowfrequency fluctuations method for acupuncture study.
Acknowledgements
This work was supported by the Guangxi Natural Science Foundation (Grant NO. 2011GXNSFA018176); the Guangxi Educational Commission Foundation (Grant NO. 200911LX200); the National Natural Science Foundation of China (Grant No. 81471738, 81303060); and the Fundamental Research Funds for the Central Universities.
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