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Modulatory effect of International Standard Scalp Acupuncture on brain activation in the elderly as revealed by resting-state fMRI

Modulatory effect of International Standard Scalp Acupuncture on brain activation in the elderly... The specific mechanisms by which acupuncture affects the central nervous system are unclear. In the International Standard Scalp Acu- puncture system, acupuncture needles are applied at the middle line of the vertex, anterior parietal-temporal oblique line, and the posterior parietal-temporal oblique line. We conducted a single-arm prospective clinical trial in which seven healthy elderly volunteers (three men and four women; 50–70 years old) received International Standard Scalp Acupuncture at MS5 (the mid-sagittal line between Baihui (DU20) and Qianding (DU21)), the left MS6 (line joining Sishencong (EX-HN1) and Xuanli (GB6)), and the left MS7 (line joining DU20 and Qubin (GB7)). Aer ft acupuncture, resting-state functional magnetic resonance imaging demonstrated changes in the fractional amplitude of low frequency uc fl tuations and regional homogeneity in various areas, showing remarkable enhancement of regional homogeneity in the bilateral anterior cingulate, left medial frontal gyrus, supramarginal gyrus, right middle frontal gyrus, and inferior frontal gyrus. Functional connectivity based on a seed region at the right middle frontal gyrus (42, 51, 9) decreased at the bilateral medial superior frontal gyrus. Our data preliminarily indicates that the international standard scalp acupuncture in healthy elderly participants specifcally enhances the correlation between the brain regions involved in cognition and implementation of the brain network regulation system and the surrounding adjacent brain regions. e s Th tudy was approved by the Ethics Committee of the China-Japan Union Hospital at Jilin University, China, on July 18, 2016 (approval No. 2016ks043). Key Words: nerve regeneration; resting-state functional magnetic resonance imaging; International Standard Scalp Acupuncture; acupoint specici fi ty; brain functional connectivity; healthy elderly volunteers; low frequency fluctuation; regional homogeneity; functional connectivity; neural regeneration Chinese Library Classification No. R454; R741; R853.61 2126 Chung WY, Liu SY, Gao JC, Jiang YJ, Zhang J, Qu SS, Zhang JP, Tan XL, Chen JQ, Wang SX (2019) Modulatory effect of International Standard Scalp Acupuncture on brain activation in the elderly as revealed by resting-state fMRI. Neural Regen Res 14(12):2126-2131. doi:10.4103/1673-5374.262590 Introduction Participants and Methods The International Standard Scalp Acupuncture system Participants proposes that acupuncture needles are placed along “scalp This study was a single-arm clinical trial. The study was lines”, i.e., lines or arcs that connect groups of acupoints approved by the Ethics Committee of the China-Japan related to specific cerebral functional regions, to strengthen Union Hospital at Jilin University, China on July 18, 2016 the stimulation of such regions (No authors listed, 1990). (approval No. 2016ks043) and has been registered at the Scalp acupuncture has been used to treat various brain-relat- Chinese Clinical Trial Registry (registration number: ChiC- ed diseases according to the principle of acupoint selection TR-IOR-15007672). Ten healthy participants were recruited with respect to neighboring brain regions. Considering the from January to March 2017 via posters. This study followed increase in stroke cases observed in the aging society in Chi- the Standard Protocol Items: STrengthening the Reporting na, the MS5, MS6, and MS7 scalp acupuncture line groups of OBservational studies in Epidemiology (STROBE) guid- have been frequently selected for the use in the rehabilitation ance for study. of stroke-related motor and sensory dysfunctions (Wang et The inclusion criteria were (1) age between 50 and 70 al., 2017, 2018; You et al., 2017). However, the mechanisms years and any gender; (2) no history of hypertension, diabe- of action of scalp acupuncture in the central nervous system tes, thyroid disease, or cerebral ischemia; (3) normal eating are unclear, thus limiting the use of this form of acupunc- habits without smoking or alcohol consumption, no caffeine ture compared with other methods and treatment options, intake in the past 24 hours, normal sleeping pattern, normal such as those involving western medicine and rehabilitation. physical build; (4) no history of acupuncture in the past 1 The theory of acupoint specificity holds that the selection month; (5) no metallic implants or dentures; (6) right hand- of acupoints is a key factor in the efficacy of acupuncture edness; (7) provision of informed consent. therapy (Zhao et al., 2012; Zheng et al., 2015) and can be de- Of the 10 participants recruited, two were excluded be- fined according to cerebral function (Lai and Huang, 2007; cause of excessive head movement over 1.5 mm and 1.5 Rong et al., 2013). As the formulation of targets in scalp degrees during scanning, and an additional participant was acupuncture is based on acupoints, it has been hypothesized excluded because they fell asleep during scanning. Thus, we that the mechanisms of action of International Standard obtained usable data from seven participants. There were Scalp Acupuncture (MS5, MS6 and MS7) are associated with three men and four women with a mean age of 56.14 ± 4.06 changes in the activity of certain cerebral regions. years (Figure 1). The development of functional magnetic resonance im- aging (fMRI) has made it possible to observe changes in the Acupuncture central nervous system following scalp acupuncture. Rest- We focused on the International Standard Scalp Acupunc- ing-state fMRI (rs-fMRI) is obtained when participants are ture lines MS5, left MS6, and left MS7 (No authors listed, relaxed with their eyes closed, and are not involved in any 1990). MS5 is located at the mid-sagittal line between Baihui cognitive task. It is favorable in that it enables a simple study (DU20) and Qianding (DU21), which are located at 5 cun design and minimal instructions for participants compared and 3.5 cun above the midpoint of the anterior hairline, with task-based fMRI (Lu et al., 2011; He et al., 2015). Gen- respectively. MS6 is located at the line joining EX-HN1(A), erally, regional functional analysis is conducted by obtaining which is 1 cun anterior to DU20, and Xuanli (GB6), which the fractional amplitude of the low frequency fluctuation is three quarters down the side of the hairline between (fALFF) and the regional homogeneity (ReHo), while linear Touwei (ST8) (0.5 cun above the corner of the hairline) and analysis is obtained via functional connectivity (Golestani Qubin (GB7) (located at the vertical line from the hairline et al., 2017). This non-invasive technique has been widely anterior to the ear to the level of the apex of the ear). MS7 is adopted in the study of brain physiology and pathologies, located at the line joining DU20 and GB7. A single 30-min- such as ischemic stroke (i Th el and Vahdat, 2015; Baldassarre ute needling session was performed for each participant. et al., 2016), Parkinson’s disease (Cerasa et al., 2016; Tahma- sian et al., 2017), and depressive disorders (Deng et al., 2016; Totally ten healthy participants Wang et al., 2016; Brakowski et al., 2017). rs-fMRI has been used to examine acupuncture-induced changes in brain function. Specifically, it has been used to assess the effects of Excluding two participants with head movement various manipulation methods, the presence or absence of more than 1.5 mm and 1.5 degree Deqi (needling sensation), sham-vs-verum acupuncture ef- fects, and different acupoint groups (Bai et al., 2014; Goffaux Excluding one participant falling asleep during et al., 2014; Zhang et al., 2014, 2016; Shi et al., 2016; Yin et the test al., 2017; Cai et al., 2018). In the present study, we investigated the brain-related Including seven participants in the nal fi resting-state mechanisms of action of International Standard Scalp Acu- functional magnetic resonance imaging analysis puncture. We used resting-state fMRI to observe specific changes in brain activity induced by needling in healthy el- Figure 1 Flow chart of participant inclusion. derly participants. 2127 Chung WY, Liu SY, Gao JC, Jiang YJ, Zhang J, Qu SS, Zhang JP, Tan XL, Chen JQ, Wang SX (2019) Modulatory effect of International Standard Scalp Acupuncture on brain activation in the elderly as revealed by resting-state fMRI. Neural Regen Res 14(12):2126-2131. doi:10.4103/1673-5374.262590 Acupuncture and scanning sessions took place in the same whole brain data. Post-intervention changes in functional facility on the same day, in the following order: 1) pre-acu- connectivity were analyzed with paired t-tests, and statistical parameter maps were constructed. Brain regions were iden- puncture scanning session, 2) acupuncture treatment, and tified and functional connectivity maps were constructed 3) post-acupuncture scanning session. Following routine using Brain Net Viewer software (https://www.nitrc.org/ local disinfection, stainless steel needles (0.3 mm × 40 mm, projects/bnv/). Huatuo, Suzhou, China) were inserted at acute angles (15–30 Finally, experienced neurologists verified significant degrees) with respect to the epicranial aponeurosis and left post-intervention changes in fALFF, ReHo, and functional in place for 30 mm. When the participant reported that the connectivity based on anatomical knowledge and clinical needles had elicited Deqi sensations, they were twisted at a experience. frequency of 200 turns per minute, causing a distending sen- sation. Twisting was repeated at 10-minute intervals during the 30-minute period. Results After acupuncture, fALFF decreased at the right cuneus, sur- fMRI data acquisition roundings cortices of the calcarine sulcus, and BA17. This Brain scans were acquired using a MRI system (Siemens change in activity extended to the bilateral lingual gyrus as 3.0T, Siemens Healthineers, Germany) before and within well as the left cuneus, surroundings cortices of the calcarine 20–30 minutes after the acupuncture session. We conducted sulcus, and BA17. T1-weighted magnetization-prepared rapid acquisition of ReHo decreased at the right precuneus and cuneus. This gradient-echo and fMRI-BOLD echo-planar images. Each decrease extended to the right cortex surrounding the cal- participant lay supine on the examination bed with their carine sulcus and lingua gyrus. ReHo also decreased at the head fixed in a coil. We reduced the influence of visual and left precentral gyrus and postcentral gyrus (representing the auditory stimulation by fitting the participants with eye head and facial region), and extended to the left posterior masks and earplugs. They were asked to avoid any active superior temporal gyrus (BA41, BA42, and BA22). ReHo mental activity. increased at the left anterior cingulate cortex (BA32), which The parameters for T1-weighted magnetization-prepared extended to the left medial frontal gyrus and right anterior rapid acquisition of gradient-echo scanning were as fol- cingulate cortex. ReHo also increased at the right middle lows. We conducted three-dimensional (3D) TFE sequence frontal gyrus extending to the right inferior frontal gyrus cross-sectional scans for whole brain high resolution T1WI (BA46) and at the left supramarginal gyrus (BA40). images with repetition time = 2300 ms, echo time = 2.45 ms, Based on the seed region at the left anterior cingulate cor- flip angle = 8°, field of view = 250 mm, slice thickness = 1 tex (–6, 33, –3), functional connectivity decreased at the left mm, voxel = 1.0 mm × 1.0 mm × 1.0 mm, and matrix = 256 supplementary motor area extending to the bilateral para- × 256. central lobule, and also decreased at the right supplemen- The fMRI-BOLD scanning parameters were as follows. tary motor area, medial frontal gyrus, and BA6. Functional connectivity based on the seed region at the right middle We used a single provocation echo-planar imaging sequence frontal gyrus (42, 51, 9) decreased at the left medial superior with repetition time = 2000 ms, echo time = 30 ms, flip an- frontal gyrus, extending to the right medial superior frontal. gle = 90°, slice thickness = 3.5 mm, gap = 0.7 mm, voxel = 3.5 Changes in functional connectivity based on all other ReHo mm × 3.5 mm × 3.5 mm, field of view = 224 mm × 224 mm, clusters were not significant. phases per location = 240, matrix = 64 × 64, and number of e Th brain regions with changes in fALFF, ReHo, and func - slices = 37. tional connectivity are shown in Table 1 and Figures 2 and 3. Data analysis Data were pre-processed using statistical parametric map- Discussion ping 12 software (https://www.fil.ion.ucl.ac.uk/spm/) and Our data indicate that scalp acupuncture at MS5, the left Dpabi software (http://rfmri.org/dpabi) in Matlab 2012a MS6, and the left MS7 led to a decreased fALFF value (in - (MathWorks, Natick, MA, USA). Pre-processing included dicating negative activation) in a number of brain regions. slice time correction, smoothing, motion correction, spa- fALFF represents the intensity of regional brain activity. tial and temporal filtering, and detrending. We used the We found decreased fALFF values mainly at the bilateral resting-state fMRI Data Analysis Toolkit (REST 1.8, http:// occipital lobe, including the lingual gyrus, cuneus, and the www.restfmri.net/forum/REST_V1.8) to analyze the data. surrounding cortices of the calcarine sulcus, as well as the Post-intervention changes were evaluated using paired BA17. We found these areas, together with the right precu- t-tests, and we generated statistical parameter maps for neus, to have decreased ReHo values. The ReHo represents identification and correction (AlphaSim correction, Cluster the level of synchronous neuronal activity with respect to Size = 165, cluster connectivity criterion = 4 rmm, P < 0.05). neighboring neurons. The cuneus and precuneus are integral We obtained the anatomical locations and activation inten- parts of the default-mode network, which is involved in sev- sity of clusters with significant changes in fALFF and ReHo. eral cognitive functions including self-reflection, environ- To obtain the functional connectivity, all significant chang- ment detection, and emotions. Downward activation in the es in ReHo were further analyzed for consistency with the default-mode network is observed when activation in other 2128 Chung WY, Liu SY, Gao JC, Jiang YJ, Zhang J, Qu SS, Zhang JP, Tan XL, Chen JQ, Wang SX (2019) Modulatory effect of International Standard Scalp Acupuncture on brain activation in the elderly as revealed by resting-state fMRI. Neural Regen Res 14(12):2126-2131. doi:10.4103/1673-5374.262590 Table 1 Brain regions and locations in healthy elderly participants with changes in fALFF, ReHo, and functional connectivity after International s tandard s calp Acupuncture MNI coordinate Intensity Parameter Effect Brain region X Y Z (T-value) fALFF Reduced Bilateral cuneus, lingual gyrus, surrounding cortices of calcarine sulcus, BA17 18 –96 –6 –5.8991 ReHo Reduced Right precuneus, cuneus, surrounding cortices of calcarine sulcus, lingual gyrus 15 72 21 6.996 – – Reduced Left precentral gyrus and postcentral gyrus (representing head and facial region), left –48 –12 27 –7.3221 posterior superior temporal lobule (BA41, BA42, BA22) Enhanced Bilateral anterior cingulate cortex, left medial frontal gyrus –6 33 –3 8.9454 Enhanced Right middle frontal gyrus, inferior frontal gyrus (BA46) 42 51 9 14.5384 Enhanced Left supramarginal gyrus (BA40) –48 –48 39 8.558 Functional Reduced Bilateral supplemental motor area and paracentral lobule, right medial frontal gyrus and 0 –12 57 –9.7768 connectivity BA6 Reduced Bilateral medial superior frontal gyrus 0 54 3 –9.0382 X, Y, Z coordinates represent the left-right, anterior-posterior, and superior-inferior axes in MNI space, respectively. The left anterior cingulate cortex (–6, 33, –3) and right medial frontal gyrus #(42, 51, 9) were used as the seed regions for functional connectivity analysis. fALFF: Fractional amplitude of low frequency fluctuation; ReHo: regional homogeneity; MNI: Montreal Neurological Institute. A B Figure 2 Brain regions with changes in fALFF (A) and ReHo (B) values after international standard scalp acupuncture. Transition from yellow to red indicates differences in activation. Transition from green to blue indicates differences in deactivation. fALFF: Frac- tional amplitude of low frequency fluctuation; ReHo: regional homogeneity. brain regions is evoked during the transition from a resting state to a task state (Cavanna and Trimble, 2006; Zhong et al., 2011; Goffaux et al., 2014). We found negative activation, indicated by a decline in both fALFF and ReHo values, in the right lingual gyrus, surrounding cortices of the calcarine sulcus, and BA17. The lingual gyrus is located between the calcarine sulcus and the collateral sulcus, and is a processing center for visual infor- mation, particularly visual memory and visual imagery (Bo- gousslavsky et al., 1987; Olivetti Belardinelli et al., 2009). The cortices surrounding the calcarine sulcus process visual sig- nals. BA17 is the primary visual cortex. The observed decrease in activation in these two sites was likely caused by the lack of visual sensation, induced by the presence of the eye mask. We found negative activation in terms of ReHo values in Figure 3 Regional changes in functional connectivity after international the left precentral gyrus, postcentral gyrus (representing the standard scalp acupuncture in healthy elderly participants. head and facial region), and posterior superior temporal gy- The red dots and connecting line represent the functional connectivity rus (BA41, BA42, and BA22). The precentral gyrus and post- based on the seed point at the left anterior cingulate cortex ( –6, 33, –3). The purple dots and connecting line represent the functional connectivi - central gyrus are known as the somatic motor and sensory ty based on the seed point at the right middle frontal gyrus (42, 51, 9). cortices, respectively. The left BA41 and BA42 are known as 2129 Chung WY, Liu SY, Gao JC, Jiang YJ, Zhang J, Qu SS, Zhang JP, Tan XL, Chen JQ, Wang SX (2019) Modulatory effect of International Standard Scalp Acupuncture on brain activation in the elderly as revealed by resting-state fMRI. Neural Regen Res 14(12):2126-2131. doi:10.4103/1673-5374.262590 the primary and secondary auditory cortices. When grouped comparison with a small sample that had an unequal male- with BA22, which is involved in language processing, these to-female ratio. Our study also lacked a control group with regions form Wernicke’s area (Lichteim, 1885). We found sham needles and participants with a medical condition. that synchronous activity was reduced among the sensory Thus, further investigation of scalp acupuncture is necessary language center, the motor cortex, and the sensory cortex, in other participant groups. which are all associated with pronunciation. We speculate This study preliminarily indicates that the international that this reduction in activation was due to the experimental standard scalp acupuncture in healthy elderly participants conditions, particularly, the participants wore earplugs and specifically enhanced the correlation between the brain re- were asked to remain silent. gions involved in cognition and implementation of the brain Conversely, we found enhanced local synchronous neu- network regulation system and the surrounding adjacent ronal activity among the bilateral anterior cingulate cortex brain regions. (BA32), left medial frontal gyrus, supramarginal gyrus Author contributions: Project holder: JQC; study design: JQC and (BA40), right middle frontal gyrus, and inferior frontal gy- SXW; subject recruitment: SYL and JZ; manuscript writing and editing: rus (BA46). The anterior cingulate cortex is thought of as WYC and JCG; acupuncture and fMRI acquisition supervision: YJJ, SSQ a high-level functional unit in the frontal parietal network, and XLT; data analysis: JPZ. All authors approved the final version of the paper. where it allocates attentional resources and coordinates Conflicts of interest: None declared. decision-making when there is a conflict among external/ Financial support: This study was funded by the National Natural internal cognition and mentally-derived outcomes (Vincent Science Foundation of China, No. 81403455 (to JQC). The funding body et al., 2008). The left medial frontal gyrus plays a high-level played no role in the study design, in the collection, analysis and inter- pretation of data, in the writing of the paper, or in the decision to submit role in coordinating execution, fear control, adjustment, the paper for publication. language processing, and recognition of auditory signals Institutional review board statement: This study was approved by the (Talati and Hirsch, 2005; Tomoda et al., 2012; Frascarelli et Ethics Committee of the China-Japan Union Hospital of Jilin University, China (No. 2016ks043) on July 18, 2016. The study was performed in al., 2015; Myung et al., 2016). The left supramarginal gyrus, accordance with the relevant laws and regulations of the Declaration of positioned in the parietal lobe, is implicated in the integra- Helsinki, and the hospital’s relevant ethical principles. tion of conceptual knowledge and motor representations Declaration of participant consent: The authors certify that they have into meaningful actions (Króliczak et al., 2016). BA46 is also obtained all appropriate participant consent forms. In the forms, the participants have given their consent for their images and other clinical involved in working memory, attention, behavioral control, information to be reported in the journal. The participants understand and emotions (Zhang et al., 2003; Koike et al., 2011). Tak- that their names and initials will not be published and due efforts will be en together, our data indicate that International Standard made to conceal their identity. Scalp Acupuncture modulated the experience of being in the Reporting statement: This study followed the STrengthening the Re- porting of OBservational studies in Epidemiology (STROBE) guidance. scanner, and enhanced the synchronous activities of several Biostatistics statement: The statistical methods of this study were re- brain areas associated with cognitive and executive control viewed by the biostatistician of School of Traditional Chinese Medicine, networks. Southern Medical University, China. In addition, we found that activation of the seed region at Copyright license agreement: The Copyright License Agreement has been signed by all authors before publication. the anterior cingulate cortex and nearby regions suppressed Data sharing statement: Individual participant data that underlie the functional connectivity among the bilateral supplementary results reported in this article, after deidentification (text, tables, figures, motor area, paracentral lobule (which is involved in the and appendices) will be in particular shared. Study protocol and in- regulation of defecation and micturition), and the left BA6, formed consent form will be promulgated within 6 months after the com- pletion of the trial. Anonymized trial data will be available indefinitely which is associated with the right premotor cortex. This at www.figshare.com. implies that International Standard Scalp Acupuncture spe- Plagiarism check: Checked twice by iThenticate. cifically enhanced the regulation of cognitive and executive Peer review: Externally peer reviewed. control networks without further engaging the above-men- Open access statement: This is an open access journal, and articles are distributed under the terms of the Creative Commons Attribu- tioned areas. Furthermore, that we found enhanced connec- tion-Non-Commercial-ShareAlike 4.0 License, which allows others to tivity in the left medial frontal gyrus but reduced connectivi- remix, tweak, and build upon the work non-commercially, as long as ty in the right medial frontal gyrus relative to the seed region appropriate credit is given and the new creations are licensed under the identical terms. at the anterior cingulate cortex indicates that International Open peer reviewer: Min Cheol Chang, University of Ulsan College of Standard Scalp Acupuncture had a major regulatory effect Medicine, Republic of Korea. on activity in the dominant hemisphere. Additional file: Open peer review report 1. 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Complement Ther Med 25:71-77. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Neural Regeneration Research Pubmed Central

Modulatory effect of International Standard Scalp Acupuncture on brain activation in the elderly as revealed by resting-state fMRI

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Abstract

The specific mechanisms by which acupuncture affects the central nervous system are unclear. In the International Standard Scalp Acu- puncture system, acupuncture needles are applied at the middle line of the vertex, anterior parietal-temporal oblique line, and the posterior parietal-temporal oblique line. We conducted a single-arm prospective clinical trial in which seven healthy elderly volunteers (three men and four women; 50–70 years old) received International Standard Scalp Acupuncture at MS5 (the mid-sagittal line between Baihui (DU20) and Qianding (DU21)), the left MS6 (line joining Sishencong (EX-HN1) and Xuanli (GB6)), and the left MS7 (line joining DU20 and Qubin (GB7)). Aer ft acupuncture, resting-state functional magnetic resonance imaging demonstrated changes in the fractional amplitude of low frequency uc fl tuations and regional homogeneity in various areas, showing remarkable enhancement of regional homogeneity in the bilateral anterior cingulate, left medial frontal gyrus, supramarginal gyrus, right middle frontal gyrus, and inferior frontal gyrus. Functional connectivity based on a seed region at the right middle frontal gyrus (42, 51, 9) decreased at the bilateral medial superior frontal gyrus. Our data preliminarily indicates that the international standard scalp acupuncture in healthy elderly participants specifcally enhances the correlation between the brain regions involved in cognition and implementation of the brain network regulation system and the surrounding adjacent brain regions. e s Th tudy was approved by the Ethics Committee of the China-Japan Union Hospital at Jilin University, China, on July 18, 2016 (approval No. 2016ks043). Key Words: nerve regeneration; resting-state functional magnetic resonance imaging; International Standard Scalp Acupuncture; acupoint specici fi ty; brain functional connectivity; healthy elderly volunteers; low frequency fluctuation; regional homogeneity; functional connectivity; neural regeneration Chinese Library Classification No. R454; R741; R853.61 2126 Chung WY, Liu SY, Gao JC, Jiang YJ, Zhang J, Qu SS, Zhang JP, Tan XL, Chen JQ, Wang SX (2019) Modulatory effect of International Standard Scalp Acupuncture on brain activation in the elderly as revealed by resting-state fMRI. Neural Regen Res 14(12):2126-2131. doi:10.4103/1673-5374.262590 Introduction Participants and Methods The International Standard Scalp Acupuncture system Participants proposes that acupuncture needles are placed along “scalp This study was a single-arm clinical trial. The study was lines”, i.e., lines or arcs that connect groups of acupoints approved by the Ethics Committee of the China-Japan related to specific cerebral functional regions, to strengthen Union Hospital at Jilin University, China on July 18, 2016 the stimulation of such regions (No authors listed, 1990). (approval No. 2016ks043) and has been registered at the Scalp acupuncture has been used to treat various brain-relat- Chinese Clinical Trial Registry (registration number: ChiC- ed diseases according to the principle of acupoint selection TR-IOR-15007672). Ten healthy participants were recruited with respect to neighboring brain regions. Considering the from January to March 2017 via posters. This study followed increase in stroke cases observed in the aging society in Chi- the Standard Protocol Items: STrengthening the Reporting na, the MS5, MS6, and MS7 scalp acupuncture line groups of OBservational studies in Epidemiology (STROBE) guid- have been frequently selected for the use in the rehabilitation ance for study. of stroke-related motor and sensory dysfunctions (Wang et The inclusion criteria were (1) age between 50 and 70 al., 2017, 2018; You et al., 2017). However, the mechanisms years and any gender; (2) no history of hypertension, diabe- of action of scalp acupuncture in the central nervous system tes, thyroid disease, or cerebral ischemia; (3) normal eating are unclear, thus limiting the use of this form of acupunc- habits without smoking or alcohol consumption, no caffeine ture compared with other methods and treatment options, intake in the past 24 hours, normal sleeping pattern, normal such as those involving western medicine and rehabilitation. physical build; (4) no history of acupuncture in the past 1 The theory of acupoint specificity holds that the selection month; (5) no metallic implants or dentures; (6) right hand- of acupoints is a key factor in the efficacy of acupuncture edness; (7) provision of informed consent. therapy (Zhao et al., 2012; Zheng et al., 2015) and can be de- Of the 10 participants recruited, two were excluded be- fined according to cerebral function (Lai and Huang, 2007; cause of excessive head movement over 1.5 mm and 1.5 Rong et al., 2013). As the formulation of targets in scalp degrees during scanning, and an additional participant was acupuncture is based on acupoints, it has been hypothesized excluded because they fell asleep during scanning. Thus, we that the mechanisms of action of International Standard obtained usable data from seven participants. There were Scalp Acupuncture (MS5, MS6 and MS7) are associated with three men and four women with a mean age of 56.14 ± 4.06 changes in the activity of certain cerebral regions. years (Figure 1). The development of functional magnetic resonance im- aging (fMRI) has made it possible to observe changes in the Acupuncture central nervous system following scalp acupuncture. Rest- We focused on the International Standard Scalp Acupunc- ing-state fMRI (rs-fMRI) is obtained when participants are ture lines MS5, left MS6, and left MS7 (No authors listed, relaxed with their eyes closed, and are not involved in any 1990). MS5 is located at the mid-sagittal line between Baihui cognitive task. It is favorable in that it enables a simple study (DU20) and Qianding (DU21), which are located at 5 cun design and minimal instructions for participants compared and 3.5 cun above the midpoint of the anterior hairline, with task-based fMRI (Lu et al., 2011; He et al., 2015). Gen- respectively. MS6 is located at the line joining EX-HN1(A), erally, regional functional analysis is conducted by obtaining which is 1 cun anterior to DU20, and Xuanli (GB6), which the fractional amplitude of the low frequency fluctuation is three quarters down the side of the hairline between (fALFF) and the regional homogeneity (ReHo), while linear Touwei (ST8) (0.5 cun above the corner of the hairline) and analysis is obtained via functional connectivity (Golestani Qubin (GB7) (located at the vertical line from the hairline et al., 2017). This non-invasive technique has been widely anterior to the ear to the level of the apex of the ear). MS7 is adopted in the study of brain physiology and pathologies, located at the line joining DU20 and GB7. A single 30-min- such as ischemic stroke (i Th el and Vahdat, 2015; Baldassarre ute needling session was performed for each participant. et al., 2016), Parkinson’s disease (Cerasa et al., 2016; Tahma- sian et al., 2017), and depressive disorders (Deng et al., 2016; Totally ten healthy participants Wang et al., 2016; Brakowski et al., 2017). rs-fMRI has been used to examine acupuncture-induced changes in brain function. Specifically, it has been used to assess the effects of Excluding two participants with head movement various manipulation methods, the presence or absence of more than 1.5 mm and 1.5 degree Deqi (needling sensation), sham-vs-verum acupuncture ef- fects, and different acupoint groups (Bai et al., 2014; Goffaux Excluding one participant falling asleep during et al., 2014; Zhang et al., 2014, 2016; Shi et al., 2016; Yin et the test al., 2017; Cai et al., 2018). In the present study, we investigated the brain-related Including seven participants in the nal fi resting-state mechanisms of action of International Standard Scalp Acu- functional magnetic resonance imaging analysis puncture. We used resting-state fMRI to observe specific changes in brain activity induced by needling in healthy el- Figure 1 Flow chart of participant inclusion. derly participants. 2127 Chung WY, Liu SY, Gao JC, Jiang YJ, Zhang J, Qu SS, Zhang JP, Tan XL, Chen JQ, Wang SX (2019) Modulatory effect of International Standard Scalp Acupuncture on brain activation in the elderly as revealed by resting-state fMRI. Neural Regen Res 14(12):2126-2131. doi:10.4103/1673-5374.262590 Acupuncture and scanning sessions took place in the same whole brain data. Post-intervention changes in functional facility on the same day, in the following order: 1) pre-acu- connectivity were analyzed with paired t-tests, and statistical parameter maps were constructed. Brain regions were iden- puncture scanning session, 2) acupuncture treatment, and tified and functional connectivity maps were constructed 3) post-acupuncture scanning session. Following routine using Brain Net Viewer software (https://www.nitrc.org/ local disinfection, stainless steel needles (0.3 mm × 40 mm, projects/bnv/). Huatuo, Suzhou, China) were inserted at acute angles (15–30 Finally, experienced neurologists verified significant degrees) with respect to the epicranial aponeurosis and left post-intervention changes in fALFF, ReHo, and functional in place for 30 mm. When the participant reported that the connectivity based on anatomical knowledge and clinical needles had elicited Deqi sensations, they were twisted at a experience. frequency of 200 turns per minute, causing a distending sen- sation. Twisting was repeated at 10-minute intervals during the 30-minute period. Results After acupuncture, fALFF decreased at the right cuneus, sur- fMRI data acquisition roundings cortices of the calcarine sulcus, and BA17. This Brain scans were acquired using a MRI system (Siemens change in activity extended to the bilateral lingual gyrus as 3.0T, Siemens Healthineers, Germany) before and within well as the left cuneus, surroundings cortices of the calcarine 20–30 minutes after the acupuncture session. We conducted sulcus, and BA17. T1-weighted magnetization-prepared rapid acquisition of ReHo decreased at the right precuneus and cuneus. This gradient-echo and fMRI-BOLD echo-planar images. Each decrease extended to the right cortex surrounding the cal- participant lay supine on the examination bed with their carine sulcus and lingua gyrus. ReHo also decreased at the head fixed in a coil. We reduced the influence of visual and left precentral gyrus and postcentral gyrus (representing the auditory stimulation by fitting the participants with eye head and facial region), and extended to the left posterior masks and earplugs. They were asked to avoid any active superior temporal gyrus (BA41, BA42, and BA22). ReHo mental activity. increased at the left anterior cingulate cortex (BA32), which The parameters for T1-weighted magnetization-prepared extended to the left medial frontal gyrus and right anterior rapid acquisition of gradient-echo scanning were as fol- cingulate cortex. ReHo also increased at the right middle lows. We conducted three-dimensional (3D) TFE sequence frontal gyrus extending to the right inferior frontal gyrus cross-sectional scans for whole brain high resolution T1WI (BA46) and at the left supramarginal gyrus (BA40). images with repetition time = 2300 ms, echo time = 2.45 ms, Based on the seed region at the left anterior cingulate cor- flip angle = 8°, field of view = 250 mm, slice thickness = 1 tex (–6, 33, –3), functional connectivity decreased at the left mm, voxel = 1.0 mm × 1.0 mm × 1.0 mm, and matrix = 256 supplementary motor area extending to the bilateral para- × 256. central lobule, and also decreased at the right supplemen- The fMRI-BOLD scanning parameters were as follows. tary motor area, medial frontal gyrus, and BA6. Functional connectivity based on the seed region at the right middle We used a single provocation echo-planar imaging sequence frontal gyrus (42, 51, 9) decreased at the left medial superior with repetition time = 2000 ms, echo time = 30 ms, flip an- frontal gyrus, extending to the right medial superior frontal. gle = 90°, slice thickness = 3.5 mm, gap = 0.7 mm, voxel = 3.5 Changes in functional connectivity based on all other ReHo mm × 3.5 mm × 3.5 mm, field of view = 224 mm × 224 mm, clusters were not significant. phases per location = 240, matrix = 64 × 64, and number of e Th brain regions with changes in fALFF, ReHo, and func - slices = 37. tional connectivity are shown in Table 1 and Figures 2 and 3. Data analysis Data were pre-processed using statistical parametric map- Discussion ping 12 software (https://www.fil.ion.ucl.ac.uk/spm/) and Our data indicate that scalp acupuncture at MS5, the left Dpabi software (http://rfmri.org/dpabi) in Matlab 2012a MS6, and the left MS7 led to a decreased fALFF value (in - (MathWorks, Natick, MA, USA). Pre-processing included dicating negative activation) in a number of brain regions. slice time correction, smoothing, motion correction, spa- fALFF represents the intensity of regional brain activity. tial and temporal filtering, and detrending. We used the We found decreased fALFF values mainly at the bilateral resting-state fMRI Data Analysis Toolkit (REST 1.8, http:// occipital lobe, including the lingual gyrus, cuneus, and the www.restfmri.net/forum/REST_V1.8) to analyze the data. surrounding cortices of the calcarine sulcus, as well as the Post-intervention changes were evaluated using paired BA17. We found these areas, together with the right precu- t-tests, and we generated statistical parameter maps for neus, to have decreased ReHo values. The ReHo represents identification and correction (AlphaSim correction, Cluster the level of synchronous neuronal activity with respect to Size = 165, cluster connectivity criterion = 4 rmm, P < 0.05). neighboring neurons. The cuneus and precuneus are integral We obtained the anatomical locations and activation inten- parts of the default-mode network, which is involved in sev- sity of clusters with significant changes in fALFF and ReHo. eral cognitive functions including self-reflection, environ- To obtain the functional connectivity, all significant chang- ment detection, and emotions. Downward activation in the es in ReHo were further analyzed for consistency with the default-mode network is observed when activation in other 2128 Chung WY, Liu SY, Gao JC, Jiang YJ, Zhang J, Qu SS, Zhang JP, Tan XL, Chen JQ, Wang SX (2019) Modulatory effect of International Standard Scalp Acupuncture on brain activation in the elderly as revealed by resting-state fMRI. Neural Regen Res 14(12):2126-2131. doi:10.4103/1673-5374.262590 Table 1 Brain regions and locations in healthy elderly participants with changes in fALFF, ReHo, and functional connectivity after International s tandard s calp Acupuncture MNI coordinate Intensity Parameter Effect Brain region X Y Z (T-value) fALFF Reduced Bilateral cuneus, lingual gyrus, surrounding cortices of calcarine sulcus, BA17 18 –96 –6 –5.8991 ReHo Reduced Right precuneus, cuneus, surrounding cortices of calcarine sulcus, lingual gyrus 15 72 21 6.996 – – Reduced Left precentral gyrus and postcentral gyrus (representing head and facial region), left –48 –12 27 –7.3221 posterior superior temporal lobule (BA41, BA42, BA22) Enhanced Bilateral anterior cingulate cortex, left medial frontal gyrus –6 33 –3 8.9454 Enhanced Right middle frontal gyrus, inferior frontal gyrus (BA46) 42 51 9 14.5384 Enhanced Left supramarginal gyrus (BA40) –48 –48 39 8.558 Functional Reduced Bilateral supplemental motor area and paracentral lobule, right medial frontal gyrus and 0 –12 57 –9.7768 connectivity BA6 Reduced Bilateral medial superior frontal gyrus 0 54 3 –9.0382 X, Y, Z coordinates represent the left-right, anterior-posterior, and superior-inferior axes in MNI space, respectively. The left anterior cingulate cortex (–6, 33, –3) and right medial frontal gyrus #(42, 51, 9) were used as the seed regions for functional connectivity analysis. fALFF: Fractional amplitude of low frequency fluctuation; ReHo: regional homogeneity; MNI: Montreal Neurological Institute. A B Figure 2 Brain regions with changes in fALFF (A) and ReHo (B) values after international standard scalp acupuncture. Transition from yellow to red indicates differences in activation. Transition from green to blue indicates differences in deactivation. fALFF: Frac- tional amplitude of low frequency fluctuation; ReHo: regional homogeneity. brain regions is evoked during the transition from a resting state to a task state (Cavanna and Trimble, 2006; Zhong et al., 2011; Goffaux et al., 2014). We found negative activation, indicated by a decline in both fALFF and ReHo values, in the right lingual gyrus, surrounding cortices of the calcarine sulcus, and BA17. The lingual gyrus is located between the calcarine sulcus and the collateral sulcus, and is a processing center for visual infor- mation, particularly visual memory and visual imagery (Bo- gousslavsky et al., 1987; Olivetti Belardinelli et al., 2009). The cortices surrounding the calcarine sulcus process visual sig- nals. BA17 is the primary visual cortex. The observed decrease in activation in these two sites was likely caused by the lack of visual sensation, induced by the presence of the eye mask. We found negative activation in terms of ReHo values in Figure 3 Regional changes in functional connectivity after international the left precentral gyrus, postcentral gyrus (representing the standard scalp acupuncture in healthy elderly participants. head and facial region), and posterior superior temporal gy- The red dots and connecting line represent the functional connectivity rus (BA41, BA42, and BA22). The precentral gyrus and post- based on the seed point at the left anterior cingulate cortex ( –6, 33, –3). The purple dots and connecting line represent the functional connectivi - central gyrus are known as the somatic motor and sensory ty based on the seed point at the right middle frontal gyrus (42, 51, 9). cortices, respectively. The left BA41 and BA42 are known as 2129 Chung WY, Liu SY, Gao JC, Jiang YJ, Zhang J, Qu SS, Zhang JP, Tan XL, Chen JQ, Wang SX (2019) Modulatory effect of International Standard Scalp Acupuncture on brain activation in the elderly as revealed by resting-state fMRI. Neural Regen Res 14(12):2126-2131. doi:10.4103/1673-5374.262590 the primary and secondary auditory cortices. When grouped comparison with a small sample that had an unequal male- with BA22, which is involved in language processing, these to-female ratio. Our study also lacked a control group with regions form Wernicke’s area (Lichteim, 1885). We found sham needles and participants with a medical condition. that synchronous activity was reduced among the sensory Thus, further investigation of scalp acupuncture is necessary language center, the motor cortex, and the sensory cortex, in other participant groups. which are all associated with pronunciation. We speculate This study preliminarily indicates that the international that this reduction in activation was due to the experimental standard scalp acupuncture in healthy elderly participants conditions, particularly, the participants wore earplugs and specifically enhanced the correlation between the brain re- were asked to remain silent. gions involved in cognition and implementation of the brain Conversely, we found enhanced local synchronous neu- network regulation system and the surrounding adjacent ronal activity among the bilateral anterior cingulate cortex brain regions. (BA32), left medial frontal gyrus, supramarginal gyrus Author contributions: Project holder: JQC; study design: JQC and (BA40), right middle frontal gyrus, and inferior frontal gy- SXW; subject recruitment: SYL and JZ; manuscript writing and editing: rus (BA46). The anterior cingulate cortex is thought of as WYC and JCG; acupuncture and fMRI acquisition supervision: YJJ, SSQ a high-level functional unit in the frontal parietal network, and XLT; data analysis: JPZ. All authors approved the final version of the paper. where it allocates attentional resources and coordinates Conflicts of interest: None declared. decision-making when there is a conflict among external/ Financial support: This study was funded by the National Natural internal cognition and mentally-derived outcomes (Vincent Science Foundation of China, No. 81403455 (to JQC). The funding body et al., 2008). The left medial frontal gyrus plays a high-level played no role in the study design, in the collection, analysis and inter- pretation of data, in the writing of the paper, or in the decision to submit role in coordinating execution, fear control, adjustment, the paper for publication. language processing, and recognition of auditory signals Institutional review board statement: This study was approved by the (Talati and Hirsch, 2005; Tomoda et al., 2012; Frascarelli et Ethics Committee of the China-Japan Union Hospital of Jilin University, China (No. 2016ks043) on July 18, 2016. The study was performed in al., 2015; Myung et al., 2016). The left supramarginal gyrus, accordance with the relevant laws and regulations of the Declaration of positioned in the parietal lobe, is implicated in the integra- Helsinki, and the hospital’s relevant ethical principles. tion of conceptual knowledge and motor representations Declaration of participant consent: The authors certify that they have into meaningful actions (Króliczak et al., 2016). BA46 is also obtained all appropriate participant consent forms. In the forms, the participants have given their consent for their images and other clinical involved in working memory, attention, behavioral control, information to be reported in the journal. The participants understand and emotions (Zhang et al., 2003; Koike et al., 2011). Tak- that their names and initials will not be published and due efforts will be en together, our data indicate that International Standard made to conceal their identity. Scalp Acupuncture modulated the experience of being in the Reporting statement: This study followed the STrengthening the Re- porting of OBservational studies in Epidemiology (STROBE) guidance. scanner, and enhanced the synchronous activities of several Biostatistics statement: The statistical methods of this study were re- brain areas associated with cognitive and executive control viewed by the biostatistician of School of Traditional Chinese Medicine, networks. Southern Medical University, China. In addition, we found that activation of the seed region at Copyright license agreement: The Copyright License Agreement has been signed by all authors before publication. the anterior cingulate cortex and nearby regions suppressed Data sharing statement: Individual participant data that underlie the functional connectivity among the bilateral supplementary results reported in this article, after deidentification (text, tables, figures, motor area, paracentral lobule (which is involved in the and appendices) will be in particular shared. Study protocol and in- regulation of defecation and micturition), and the left BA6, formed consent form will be promulgated within 6 months after the com- pletion of the trial. Anonymized trial data will be available indefinitely which is associated with the right premotor cortex. This at www.figshare.com. implies that International Standard Scalp Acupuncture spe- Plagiarism check: Checked twice by iThenticate. cifically enhanced the regulation of cognitive and executive Peer review: Externally peer reviewed. control networks without further engaging the above-men- Open access statement: This is an open access journal, and articles are distributed under the terms of the Creative Commons Attribu- tioned areas. Furthermore, that we found enhanced connec- tion-Non-Commercial-ShareAlike 4.0 License, which allows others to tivity in the left medial frontal gyrus but reduced connectivi- remix, tweak, and build upon the work non-commercially, as long as ty in the right medial frontal gyrus relative to the seed region appropriate credit is given and the new creations are licensed under the identical terms. at the anterior cingulate cortex indicates that International Open peer reviewer: Min Cheol Chang, University of Ulsan College of Standard Scalp Acupuncture had a major regulatory effect Medicine, Republic of Korea. on activity in the dominant hemisphere. Additional file: Open peer review report 1. 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Neural Regeneration ResearchPubmed Central

Published: Aug 7, 2019

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