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Impaired white matter microstructure associated with severe depressive symptoms in patients with PD

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Abstract

Depression is a common occurrence in patients with Parkinson's disease (PD); however, its pathophysiology is still unclear. This study assessed the association between the integrity of white matter and depressive symptoms in patients with PD. 67 patients with PD were divided into a non-depressed PD group (ndPD, n = 30) and a depressed PD group (dPD, n = 37). The dPD group was further subdivided into a mild-moderately depressed PD (mdPD, n = 22) and a severely depressed PD group (sdPD, n = 15). Tract-Based Spatial Statistics was used to compare fractional anisotropy (FA) between groups. Region-of-interest analysis was used to explore changes in diffusivity indices in the regions showing FA abnormalities. The sdPD patients exhibited significantly reduced FA in the left superior longitudinal fasciculus, uncinate fasciculus, anterior corona radiata, corticospinal tract, and bilateral inferior fronto-occipital fasciculus when compared with the ndPD patients, but the decreased FA was within a smaller area when compared with the mdPD patients. No significant difference in FA was found between the mdPD and ndPD groups. Among the dPD patients, FA values in the left superior longitudinal fasciculus negatively correlated with BDI scores. Impaired white matter integrity in the prefronto-limbic/temporal circuitry, mainly in the left hemisphere, is associated with severe, but not mild-moderate depressive symptoms in patients with PD.

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Abbreviations

PD:

Parkinson’s disease

WM:

White matter

BDI:

21-Item Beck’s Depression Inventory

ndPD:

Non-depressed patients with PD

dPD:

Depressed patients with PD

mdPD:

Mild-moderately depressed patients with PD

sdPD:

Severely depressed patients with PD

DTI:

Diffusion tensor imaging

TBSS:

Tract-Based Spatial Statistics

FA:

Fractional anisotropy

AD:

Axial diffusivity

RD:

Radial diffusivity

MD:

Mean diffusivity

ROI:

Region of interest

UF:

Uncinate fasciculus

IFOF:

Inferior fronto-occipital fasciculus

SLF:

Superior longitudinal fasciculus

ACR:

Anterior corona radiata

CST:

Corticospinal tract

MDD:

Major depressive disorder

PET:

Positron emission tomography

fMRI:

Functional magnetic resonance imaging

UPDRS-III:

The motor part of the Unified Parkinson’s Disease Rating Scale

H-Y:

Hoehn & Yahr

CDR:

Clinical Dementia Rating scale

MMSE:

The Mini Mental State Exam

FSL:

FMRI software library

FWE:

Family-wise error

JHU:

John Hopkins University

TFCE:

Threshold-free cluster-enhancement

DLPFC:

Dorsolateral prefrontal cortex

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Funding

This study was supported by the National Natural Science Foundation of China (81471646), the Science Foundation of Hunan Province (14JJ2027) and Clinical Research Center for Medical Imaging in Hunan Province (2020SK4001).

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Authors and Affiliations

  1. Department of Radiology, the Second Xiangya Hospital, Central South University, 139 Renmin Zhong Road, Changsha, 410011, Hunan, China

    Qin Shen, Yijuan Xiang, Haiyan Liao, Sainan Cai, Bing Zhou, Min Wang, Siyu Liu, Zishu Zhang & Changlian Tan

  2. Institute of Clinical Medicine - Neurology, University of Eastern Finland, Kuopio, Finland

    Yawu Liu

  3. Department of Radiology, Kuopio University Hospital, Kuopio, Finland

    Yawu Liu

  4. National Institution of Drug Clinical Trial, Xiangya Hospital, Central South University, Changsha, China

    Jie Guo

  5. Department of Radiology, the First Affiliated Hospital, University of Science and Technology of China, Hefei, China

    Hongchun Zhang

  6. Medical Psychological Center, the Second Xiangya Hospital, Central South University, Changsha, China

    Jinyao Yi

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  1. Qin Shen
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  2. Yawu Liu
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  9. Min Wang
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  10. Siyu Liu
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  11. Jinyao Yi
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  13. Changlian Tan
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Corresponding author

Correspondence to Changlian Tan.

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Informed consent was obtained from all individual participants.

Research involving human participants

All procedures performed in this study were in accordance with the ethical standards of the Second Xiangya Hospital, Central South University.

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All authors declared no potential conflict of interests.

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Supplementary Information

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11682_2021_488_MOESM1_ESM.png

Supplementary file1 (PNG 201 KB) Supplemental material Fig. 1. White matter regions with lower fractional anisotropy (FA) in sdPD than ndPD patients were analyzed by more detailed DTI measures. (A) FA was decreased in four clusters; (B) Radial diffusivity (RD) was increased in three clusters; (C) Axonal diffusivity (AD) was decreased in one cluster; (D) Mean diffusivity (MD) was increased in one cluster. The bars and whiskers represent mean values of the DTI metrics and standard deviations, respectively. Cluster 1: left superior longitudinal fasciculus, left anterior corona radiata, left uncinate fasciculi; cluster 2: right inferior fronto-occipital fasciculus (IFOF); cluster 3: left IFOF, left corticospinal tract; and cluster 4: right IFOF. *P < 0.05

11682_2021_488_MOESM2_ESM.png

Supplementary file2 (PNG 111 KB) Supplemental material Fig. 2. White matter regions with lower fractional anisotropy (FA) in sdPD than mdPD patients were analyzed by more detailed DTI measures. (A) FA was decreased in three clusters; (B) Radial diffusivity (RD) was increased in two clusters; (C) Axonal diffusivity (AD) showed no significant difference between the two groups; (D) Mean diffusivity (MD) was increased in one cluster. The bars and whiskers represent mean values of the DTI metrics and standard deviations, respectively. Cluster 1: left superior longitudinal fasciculus; cluster 2: right inferior fronto-occipital fasciculus (IFOF); and cluster 3: left uncinate fasciculi and left IFOF. *P < 0.05.

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Shen, Q., Liu, Y., Guo, J. et al. Impaired white matter microstructure associated with severe depressive symptoms in patients with PD. Brain Imaging and Behavior 16, 169–175 (2022). https://doi.org/10.1007/s11682-021-00488-7

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