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The participation of basolateral amygdala in the efficacy of acupuncture with deqi treating for functional dyspepsia

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Abstract

Deqi is taken as an indispensable requirement to achieve acupuncture efficacy. This study aimed to explore the central influence of deqi on the efficacy of acupuncture for functional dyspepsia (FD). 70 FD patients were randomized to receive 20 sessions’ acupuncture treatment with (n = 35) and without deqi (n = 35). In each group, 25 FD patients randomly selected underwent functional magnetic resonance imaging (fMRI) scans before and after treatment. After group re-division according to deqi response, changes of amygdala subregions-based resting-state functional connectivity (rsFC) were compared between the acupuncture with and without obvious deqi group. The clinical changes of the Nepean Dyspepsia Symptom Index (NDSI) measuring FD symptoms were also used to further assess the correlation with amygdala subregions rsFC in FD patients. The decrease in the NDSI scores (pre-pos) in the obvious deqi group was significantly greater than that in the acupuncture without obvious deqi group (p < 0.05). Compared to the without obvious deqi group, the obvious deqi group showed significantly decreased the left basolateral amygdala (BLA) rsFC with bilateral insular (INS), putamen and middle/posterior cingulate cortex (MCC/PCC), right pallidum and hippocampus (HIPP) after treatment. The changed NDSI scores(pre-post) of all 41 FD patients was significantly positively correlated with their Fisher’s transformed z value of the left BLA rsFC with left INS (r = 0.376, FDR corrected p = 0.015), and rsFC with right HIPP (r = 0.394, FDR corrected p = 0.015). The changed NDSI scores(pre-post) of the obvious deqi group was significantly negatively correlated with their Fisher’s transformed z value of the right centromedial amygdala (CMA) rsFC with left medial prefrontal cortex (mPFC) (r = −0.463, p = 0.035). The results tested the hypothesis that the advantage of deqi on efficacy is related to affecting the BLA and CMA rsFC. It suggested that deqi might influence the abnormal rsFC within the salience network (SN), and participate in the adaptive modulation of disrupted relationship between the SN and default mode network (DMN).

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Abbreviations

FD:

functional dyspepsia

fMRI:

functional magnetic resonance imaging

rsFC:

resting-state functional connectivity

NDSI:

the Nepean Dyspepsia Symptom Index

BLA:

the basolateral amygdala subregions

INS:

insular cortex

MCC:

middle cingulate cortex

PCC:

posterior cingulate cortex

HIPP:

hippocampus

FDR:

false discovery rate

CMA:

the centromedial amygdala subregions

mPFC:

medial prefrontal cortex

SN:

the salience network

DMN:

the default mode network

FGID:

functional gastrointestinal disorder

QOL:

quality of life

HS:

healthy subjects

TCM:

Traditional Chinese Medicine

PDS:

Postprandial Distress Syndrome

EPS:

Epigastric Pain Syndrome

SAS:

Zung Self-Rating Anxiety Scale

SDS:

Zung Self-Rating Depression Scale

C-MASS:

Chinese version of modified Massachusetts General Hospital Acupuncture Sensation Scale

VAS:

Visual Analogue Scale

BOLD-fMRI:

Blood oxygenation level dependent fMRI

RCTs:

Randomized Controlled Trials

mean ± SD:

Means and standard deviations

SPM:

statistical parametric mapping

MNI:

Montreal Neurological Institute

FWHM:

full-width at half maximum

ROIs:

Regions of Interests

MPM:

Maximum Probabilistic Map

SFA:

the Superficial Amygdala

OFC:

orbital frontal cortex

PrG:

precentral gyrus

PoG:

postcentral gyrus

ACC:

anterior cingulate cortex

MTG:

middle temporal gyrus

PET-CT:

Positron Emission Tomography-Computed Tomography

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Acknowledgements

We were grateful to Dr. Peiming Feng, Dr. Tingting Ma and Prof. Jie Wu for the patient recruitment, Dr. Baiwan Zhou, PhD. for MRI data acquisition and interpretation, Liangsheng Zhang for language and grammar editing.

Funding

This study was supported by grants from the National Natural Science Foundation of Outstanding Youth Fund in China (NO.81622052), National Natural Science Foundation of China (NO.81473602), the major program of the National Natural Science Foundation of China (NO.81590950), the Ten Thousand Talent Program (W02020595) and Youth Science and Technology Innovative Team of Sichuan Province (2019JDTD0011).

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Authors and Affiliations

Authors

Contributions

Fang Zeng, Fanrong Liang, Ruirui Sun, Zhaoxuan He and Peihong Ma designed the study; Ruirui Sun, Zhaoxuan He and Peihong Ma drafted the manuscript; Tao Yin, Xiaoyan Liu and Yuzhu Qu recruited participants and performed the clinical measurement; Jin Lu and Shuai Yin completed the acupuncture procedure; Tingting Zhang and Liuyang Huang collected the clinical data; Xueling Suo, Du Lei and Qiyong Gong designed the fMRI scan and collected images; Ruirui Sun did the data analysis. All authors discussed, read, revised the manuscript, and all approved the publication of this paper.

Corresponding authors

Correspondence to Fanrong Liang or Fang Zeng.

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Conflict of interest

The authors have declared that no conflict of interest exists.

Ethical approval

This study protocol has been approved by the institutional review boards and ethics committees of the 1st Teaching Hospital of Chengdu University of TCM with the ethical approval identifier 2015KL-002. This study has been registered in the Chinese Clinical Trial Registry, ChiCTR-IOR-15006523. This trial follows the principles of the Declaration of Helsinki (Version Edinburgh 2000). Only patients signed the informed consent form will be included. In addition, all researchers were trained and signed a pledge to protect the confidentiality of study participants.

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Informed consent was obtained from all individual participants included in the study.

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Sun, R., He, Z., Ma, P. et al. The participation of basolateral amygdala in the efficacy of acupuncture with deqi treating for functional dyspepsia. Brain Imaging and Behavior 15, 216–230 (2021). https://doi.org/10.1007/s11682-019-00249-7

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