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Progressive gray matter hypertrophy with severity stages of insomnia disorder and its relevance for mood symptoms

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Abstract

Objective

To investigate the gray matter (GM) alterations in patients with insomnia disorder (ID) at different severity stages and the relationship between GM alterations and sleep, mood, and cognitive measures.

Methods

One hundred one ID patients and 63 healthy controls (HC) were included. Each patient underwent structural MRI and completed sleep-, mood-, and cognitive-related questionnaires. The ID patients were further grouped into subthreshold insomnia (SI) group and clinical insomnia (CI) group. We investigated changes in GM volumes in ID patients via diffeomorphic anatomical registration through exponentiated lie algebra voxel-based morphometry (DARTEL-VBM). We first compared voxel-wise differences in GM volumes between the HC group and the ID group. Analysis of variance was performed on individual GM maps in the SI, CI, and HC groups to further investigate the effects of different stages of ID severity on GM volumes. Multiple regression was used to model the relationship between altered GM volumes in SI and CI groups and clinical measures.

Results

GM hypertrophies in the left anterior and middle cingulate gyrus, right middle and inferior temporal gyrus, and right cerebellum Crus II were detected in ID. Increased GM volume in the right middle temporal gyrus was detected in the SI group, whereas all three regions in the CI group. Regression analysis showed that mood- and cognitive-related measures had a positive correlation with GM volumes, while sleep-related measures had a negative correlation with GM volumes in the CI group.

Conclusions

Our findings of the progressively increased GM volumes in ID suggest that a hypertrophic cortical morphological mechanism may underlie the altered neuroanatomy induced by insomnia.

Key Points

• Insomnia-induced GM hypertrophies in the cingulate gyrus, temporal gyrus, and cerebellum Crus II.

• The middle temporal gyrus was early detectable in the SI group.

• The increased GM volumes in the CI group were correlated with clinical measures.

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Abbreviations

ACC:

Anterior cingulate cortex

CI:

Clinical insomnia

DARTEL:

Diffeomorphic anatomical registration through exponentiated lie algebra

GM:

Gray matter

HC:

Healthy controls

ID:

Insomnia disorder

MDD:

Major depressive disorder

SI:

Subthreshold insomnia

VBM:

Voxel-based morphometry

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Acknowledgements

We would like to thank all the participants involved in this project.

Funding

This study was funded by the National Natural Science Foundation of China (Grant Nos. 81901731, 81701111, 81471639, U1903120, 81771807), the Science and Technology Planning Project of Guangdong (202002030234), and the National Natural Science Foundation of Guangdong Province (2018A0303130129)

Author information

Author notes

  1. Shumei Li and Bin A. Wang contributed equally to this work.

Authors and Affiliations

  1. Department of Medical Imaging, Guangdong Second Provincial General Hospital, Guangzhou, China

    Shumei Li, Ying Feng, Meng Li, Tianyue Wang, Changhong Li, Wen Hua, Chulan Lin, Mengchen Liu, Xiaofen Ma, Jin Fang & Guihua Jiang

  2. Department of Neurology, BG University Hospital Bergmannsheil, Ruhr-University Bochum, Bochum, Germany

    Bin A. Wang

  3. Guangdong Traditional Medical and Sports Injury Rehabilitation Research Institute, Guangdong Second Provincial General Hospital, Guangzhou, China

    Cheng Li & Linghui Nie

  4. The Second School of Clinical Medicine, Southern Medical University, Guangzhou, China

    Ying Feng

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  1. Shumei Li
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Corresponding author

Correspondence to Guihua Jiang.

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Guarantor

The scientific guarantor of this publication is Guihua Jiang.

Conflict of interest

The authors of this manuscript declare no relationships with any companies, whose products or services may be related to the subject matter of the article.

Statistics and biometry

Bin A. Wang has significant statistical expertise.

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Written informed consent was obtained from all subjects (patients) in this study.

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Institutional Review Board approval was obtained.

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• prospective

• cross-sectional study

• performed at one institution

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Li, S., Wang, B.A., Li, C. et al. Progressive gray matter hypertrophy with severity stages of insomnia disorder and its relevance for mood symptoms. Eur Radiol 31, 6312–6322 (2021). https://doi.org/10.1007/s00330-021-07701-7

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  • DOI: https://doi.org/10.1007/s00330-021-07701-7

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