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Abnormal within- and cross-networks functional connectivity in different outcomes of herpes zoster patients

Abstract

Neuroimaging studies have displayed aberrant brain activities in individual sensory- and emotional-linked regions in postherpetic neuralgia (PHN) patients. However, multi-dimensional dysfunction in chronic pain may rely on the interplay between networks. Little is known about the changes in the functional architecture of resting state networks (RSNs) in PHN. In this cross-sectional study, we recruited 31 PHN patients, 33 RHZ patients and 34 HCs; all participants underwent resting-state functional magnetic resonance imaging scans. We investigated the differences of within- and cross-network connectivities between different outcomes of HZ patients [including PHN and recuperation from herpes zoster (RHZ)] and healthy controls (HCs) so as to extract a characteristic network pattern of PHN. The abnormal network connectivities were then correlated with clinical variables in respective groups. PHN and RHZ patients could be similarly characterized by abnormal within-default mode network (DMN), DMN-salience network (SN) and SN-basal ganglia network (BGN) connectivity relative to HCs. Of note, compared with RHZ patients, PHN patients could be characterized by abnormal DMN–BGN and within-BGN connectivity. Furthermore, the within-DMN connectivity was associated with pain-induced emotional scores among PHN patients. Our study presented that network-level imbalance could account for the pain-related dysfunctions in different outcomes of herpes zoster patients. These insights are potentially useful for understanding neuromechanism of PHN and providing central therapeutic targets for PHN.

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Abbreviations

BGN:

Basal ganglia network

DMN:

Default mode network

EPI:

Echo planar imaging

ERN:

Emotion regulation network

FC:

Functional connectivity

FDR:

False discovery rate

fMRI:

Functional magnetic resonance imaging

FOV:

Field of view

HAMA:

Hamilton anxiety scale

HAMD:

Hamilton depression scale

HCs:

Healthy controls

HZ:

Herpes zoster

IASP:

International Association for the Study of Pain

IC:

Insula cortex

ICA:

Independent components analysis

MNI:

Montreal Neurological Institute

mPFC:

Medial prefrontal cortex

MPQ:

McGill pain questionnaire

NAc:

Nucleus accumbens

PAG:

Periaqueductal gray

PANAS:

Positive Affect Negative Affect Score

PCC:

Posterior cingulate cortex

PHN:

Postherpetic neuralgia

RHZ:

Recuperation from herpes zoster

ROI:

Regions of interest

RSN:

Resting state network

SD:

Standard deviation

SF-36:

Medical Outcomes Study 36-item short form from health survey

SN:

Salience network

S1/S2:

Primary and second somatosensory

TE:

Echo time

TMD:

Temporomandibular disorder

TR:

Repetition time

VAS:

Visual analog scale

vmPFC:

Ventral medial prefrontal cortex

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Acknowledgements

Thanks to all medical workers for their contributions and all participants for their participation in this study.

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The authors have no sources of funding to declare for this manuscript.

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YW: This author performed the study, analyzed the data and completed the manuscript. CW: This author performed the study, helped review and modify the manuscript. LY: This author helped collect the subjects. WQ: This author helped to perform the study. XX: This author helped collect the subjects. MZ: This author helped design the study. MY: This author helped design the study.

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Correspondence to Minming Zhang or Min Yan.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the Ethics Committee of Second Affiliated Hospital of Zhejiang University, School of Medicine.

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

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11682_2021_510_MOESM1_ESM.tif

Supplementary file1 Figure S1. The comparison of within- and cross networks functional connectivities between PHN, RHZ patients and HCs. There were no significance of functional connectivity of (A)within-SN (B) DMN-ERN (C) within-ERN (D) ERN-BGN (E) SN-ERN between PHN, RHZ patients and HCs. PHN, postherpetic neuralgia; RHZ, recuperation from herpes zoster. DMN, Default mode network; SN,Salience network; ERN, Emotion regulation network; BGN, Basal ganglia network. (TIF 13283 kb)

11682_2021_510_MOESM2_ESM.tif

Supplementary file2 Figure S2. Partial correlation analysis between network connectivity and clinical varies. (A) The within DMN connectivity was negatively related to the PANAS positive scores in PHN patients; (B) The DMN-SN connectivity was negatively related to the HAMD scores in RHZ patients; (C) The DMN-SN connectivity was negatively related to the HAMA scores in RHZ patients; (D) The within-BGN connectivity was positively related to the duration in RHZ patients. PHN, postherpetic neuralgia; RHZ, recuperation from herpes zoster. DMN, Default mode network; SN, Salience network; ERN, Emotion regulation network; BGN, Basal ganglia network. (TIF 134 kb)

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Wu, Y., Wang, C., Yu, L. et al. Abnormal within- and cross-networks functional connectivity in different outcomes of herpes zoster patients. Brain Imaging and Behavior (2021). https://doi.org/10.1007/s11682-021-00510-y

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Keywords

  • Postherpetic neuralgia
  • Recuperation from herpes zoster
  • Resting-state networks
  • Network functional connectivity