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Altered gray matter structural covariance networks at both acute and chronic stages of mild traumatic brain injury

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Abstract

Cognitive and emotional impairments observed in mild traumatic brain injury (mTBI) patients may reflect variances of brain connectivity within specific networks. Although previous studies found altered functional connectivity (FC) in mTBI patients, the alterations of brain structural properties remain unclear. In the present study, we analyzed structural covariance (SC) for the acute stages of mTBI (amTBI) patients, the chronic stages of mTBI (cmTBI) patients, and healthy controls. We first extracted the mean gray matter volume (GMV) of seed regions that are located in the default-mode network (DMN), executive control network (ECN), salience network (SN), sensorimotor network (SMN), and the visual network (VN). Then we determined and compared the SC for each seed region among the amTBI, the cmTBI and the healthy controls. Compared with healthy controls, the amTBI patients showed lower SC for the ECN, and the cmTBI patients showed higher SC for the both DMN and SN but lower SC for the SMN. The results revealed disrupted ECN in the amTBI patients and disrupted DMN, SN and SMN in the cmTBI patients. These alterations suggest that early disruptions in SC between bilateral insula and the bilateral prefrontal cortices may appear in amTBI and persist into cmTBI, which might be potentially related to the cognitive and emotional impairments.

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Abbreviations

amTBI:

Acute stage of mild traumatic brain injury

BAI:

Beck Anxiety Inventory

BDI:

Beck Depression Inventory

cmTBI:

Chronic stage of mild traumatic brain injury

CSF:

Cerebrospinal fluid

DAN:

Dorsal attention network

dlPFC:

Dorsolateral prefrontal cortex

DMN:

Default-mode network

ECN:

Executive control network

FC:

Functional connectivity

FI:

Fronto-insular cortex

GCS:

Glasgow Coma Scale

GM:

Gray matter

GMV:

Gray matter volume

HC:

Healthy controls

ICNs:

Intrinsic connectivity networks

M1:

Primary motor cortex

MFG:

Middle frontal gyrus

mGMV:

Mean gray matter volume

MoCA:

Montreal Cognitive Assessment

MOG:

Middle occipital gyrus

mPFC:

Medial prefrontal cortex

mTBI:

Mild traumatic brain injury

OFC:

Orbitofrontal cortex

ORBinf:

Orbital part of inferior frontal gyrus

PFC:

Prefrontal cortex

PoCG:

Postcentral gyrus

PreCG:

Precentral gyrus

SC:

Structural covariance

SCNs:

Structural covariance networks

SFGmed:

Left medial superior frontal cortex

SMA:

Supplementary motor area.

SMN:

Sensorimotor network;

SN:

Salience network

STG:

Superior temporal gyrus

TBI:

Traumatic brain injury

TPN:

Task positive network

V1:

Primary visual cortex

VBM:

Voxel-based morphometry

VN:

Visual network

WM:

White matter

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Acknowledgements

The authors appreciate Drs. Rhoda E. and Edmund F. Perozzi for editing the manuscript.

Funding

This study was funded by the National Natural Science Foundation of China (Grant numbers: 81871338, 81371535, and 81271548), the National Key R&D Program of China (Grant number: 2018YFC1705006), and the Key Specialty Disease Specialist Project of Hangzhou City (Grant number: 20150733Q19). The funding organizations played no further role in study design, data collection, analysis and interpretation, or paper writing.

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Author notes

  1. Jie Song and Jie Li contributed equally to this work.

Authors and Affiliations

  1. Center for Studies of Psychological Application, South China Normal University, Guangzhou, 510631, China

    Jie Song, Lixiang Chen, Senning Zheng, Bolin Cao, Yihe Weng, Qinyuan Chen & Ruiwang Huang

  2. School of Psychology, South China Normal University, Guangzhou, 510631, China

    Jie Song, Lixiang Chen, Senning Zheng, Bolin Cao, Yihe Weng & Ruiwang Huang

  3. Guangdong Key Laboratory of Mental Health and Cognitive Science, South China Normal University, Guangzhou, 510631, China

    Jie Song, Lixiang Chen, Senning Zheng, Bolin Cao, Yihe Weng, Qinyuan Chen & Ruiwang Huang

  4. Department of Radiology, the Affiliated Hospital of Hangzhou Normal University, Hangzhou, 310015, China

    Jie Li, Xingqi Lu, Ying Yang & Jianping Ding

  5. Institute for Brain Research and Rehabilitation, South China Normal University, Guangzhou, 510631, China

    Qinyuan Chen

  6. School of Medicine, Hangzhou Normal University, Hangzhou, 310015, China

    Jianping Ding

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  1. Jie Song
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Correspondence to Jianping Ding or Ruiwang Huang.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. The study protocol was approved by the Institutional Review Board of the Affiliated Hospital of Hangzhou Normal University.

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Highlights

• The amTBI patients showed lower SC within the ECN than the controls.

• The cmTBI patients showed higher SC within both the DMN and SN, but lower SC within the SMN, than the controls.

• Altered SC for the DMN, ECN and SN was related to cognitive and emotional impairments in mTBI patients.

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Song, J., Li, J., Chen, L. et al. Altered gray matter structural covariance networks at both acute and chronic stages of mild traumatic brain injury. Brain Imaging and Behavior 15, 1840–1854 (2021). https://doi.org/10.1007/s11682-020-00378-4

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  • DOI: https://doi.org/10.1007/s11682-020-00378-4

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