Aberrant brain topological organization and granger causality connectivity in Parkinson's disease with impulse control disorders

Front Aging Neurosci. 2024 Apr 25:16:1364402. doi: 10.3389/fnagi.2024.1364402. eCollection 2024.

Abstract

Introduction: Impulse control disorders (ICDs) refer to the common neuropsychiatric complication of Parkinson's disease (PD). The white matter (WM) topological organization and its impact on brain networks remain to be established.

Methods: A total of 17 PD patients with ICD (PD-ICD), 17 without ICD (PD-NICD), and 18 healthy controls (HCs) were recruited. Graph theoretic analyses and Granger causality analyses were combined to investigate WM topological organization and the directional connection patterns of key regions.

Results: Compared to PD-NICD, ICD patients showed abnormal global properties, including decreased shortest path length (Lp) and increased global efficiency (Eg). Locally, the ICD group manifested abnormal nodal topological parameters predominantly in the left middle cingulate gyrus (MCG) and left superior cerebellum. Decreased directional connectivity from the left MCG to the right medial superior frontal gyrus was observed in the PD-ICD group. ICD severity was significantly correlated with Lp and Eg.

Discussion: Our findings reflected that ICD patients had excessively optimized WM topological organization, abnormally strengthened nodal structure connections within the reward network, and aberrant causal connectivity in specific cortical- limbic circuits. We hypothesized that the aberrant reward and motor inhibition circuit could play a crucial role in the emergence of ICDs.

Keywords: Parkinson’s disease; granger causality analyses; graph theory; impulse control disorders; white matter.

Grants and funding

The author(s) declare that financial support was received for the research, authorship, and/or publication of this article. This study was funded by the National Natural Science Foundation of China (grant number 81901297), the Opening Foundation of Jiangsu Key Laboratory of Neurodegeneration, Nanjing Medical University (grant number KF202201), the Postgraduate Research and Practice Innovation Program of Jiangsu Province (grant number SJCX22_0688) and Jiangsu Province Hospital (the First Affiliated Hospital with Nanjing Medical University) Clinical Capacity Enhancement Project (JSPH-MC-2022-25).