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. 2022 Jul 8:14:944925.
doi: 10.3389/fnagi.2022.944925. eCollection 2022.

Structural Brain Network Abnormalities in Parkinson's Disease With Freezing of Gait

Chaoyang Jin  1 , Lei Yang  1 , Shouliang Qi  1   2 , Yueyang Teng  1 , Chen Li  1 , Yudong Yao  3 , Xiuhang Ruan  4 , Xinhua Wei  4
Affiliations

Structural Brain Network Abnormalities in Parkinson's Disease With Freezing of Gait

Chaoyang Jin et al. Front Aging Neurosci. .

Abstract

Objective: Diffusion tensor imaging (DTI) studies have investigated white matter (WM) integrity abnormalities in Parkinson's disease (PD). However, little is known about the topological changes in the brain network. This study aims to reveal these changes by comparing PD without freezing of gait (FOG) (PD FOG-), PD with FOG (PD FOG+), and healthy control (HC).

Methods: 21 PD FOG+, 34 PD FOG-, and 23 HC were recruited, and DTI images were acquired. The graph theoretical analysis and network-based statistical method were used to calculate the topological parameters and assess connections.

Results: PD FOG+ showed a decreased normalized clustering coefficient, small-worldness, clustering coefficient, and increased local network efficiency compared with HCs. PD FOG+ showed decreased centrality, degree centrality, and nodal efficiency in the striatum, frontal gyrus, and supplementary motor area (SMA). PD FOG+ showed decreased connections in the frontal gyrus, cingulate gyrus, and caudate nucleus (CAU). The between centrality of the left SMA and left CAU was negatively correlated with FOG questionnaire scores.

Conclusion: This study demonstrates that PD FOG+ exhibits disruption of global and local topological organization in structural brain networks, and the disrupted topological organization can be potential biomarkers in PD FOG+. These new findings may provide increasing insight into the pathophysiological mechanism of PD FOG+.

Keywords: Parkinson’s disease; diffusion tensor imaging; freezing of gait; graph theory analysis; network-based statistic.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

FIGURE 1
FIGURE 1
Schematic representation of the inclusion and exclusion criteria for this study. HC, health control; PD FOG- Parkinson’s disease without freezing of gait; PD FOG+, Parkinson’s disease with freezing of gait.
FIGURE 2
FIGURE 2
The study procedure of graph theory analysis of structural brain network (DTI, diffusion tensor imaging; AAL, automated anatomical labeling; HC, health control; PD FOG- Parkinson’s disease without freezing of gait; PD FOG+, Parkinson’s disease with freezing of gait).
FIGURE 3
FIGURE 3
Small-world property comparison among the PD FOG+, PD FOG- and HC groups. (A) The normalized clustering coefficient (Gamma). (B) The normalized characteristic path length (Lambda). (C) The small-worldness (Sigma) (HC, healthy control; PD FOG- Parkinson’s disease without freezing of gait; PD FOG+, Parkinson’s disease with freezing of gait).
FIGURE 4
FIGURE 4
Comparisons of the global properties among the PD FOG+, PD FOG– and HC groups. (A) Clustering coefficient (Cp). (B) Characteristic path length (Lp). (C) Global efficiency (Eglob). (D) Local efficiency (Eloc).
FIGURE 5
FIGURE 5
Brain regions with abnormal or significantly different properties among the PD FOG+, PD FOG– and HC groups. (A) Significantly different between centrality. (B) With significantly different degree centrality. (C) With significantly different nodal efficiency. The only red sphere indicates the increased centrality in PD FOG+ patients, and the other blue spheres indicate the decreased measures in the first group in the comparison. No brain regions with significant differences were observed for degree centrality and nodal efficiency in PD FOG– vs. HC and PD FOG+ vs. PD FOG–.
FIGURE 6
FIGURE 6
The connections with significantly different structural connectivity strengths among the PD FOG+, PD FOG–, and HC groups.
FIGURE 7
FIGURE 7
The correlation between FOGQ (freezing of gait questionnaire scores) and network topological properties in PD FOG+ patients. (A) The between centrality of the left supplementary motor area is negatively related to FOGQ scores. (B) The centrality of the right caudate nucleus was negatively related to FOGQ scores.
FIGURE 8
FIGURE 8
Schematic diagram of the main conclusions.
See this image and copyright information in PMC

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