Subthalamic and pallidal stimulation in Parkinson's disease induce distinct brain topological reconstruction

Chunguang Chu; Naying He; Kristina Zeljic; Zhen Zhang; Jiang Wang; Jun Li; Yu Liu; Youmin Zhang; Bomin Sun; Dianyou Li; Fuhua Yan; Chencheng Zhang; Chen Liu

doi:10.1016/j.neuroimage.2022.119196

Subthalamic and pallidal stimulation in Parkinson's disease induce distinct brain topological reconstruction

Neuroimage. 2022 Jul 15:255:119196. doi: 10.1016/j.neuroimage.2022.119196. Epub 2022 Apr 9.

Authors

Chunguang Chu¹, Naying He², Kristina Zeljic³, Zhen Zhang¹, Jiang Wang¹, Jun Li⁴, Yu Liu², Youmin Zhang², Bomin Sun⁵, Dianyou Li⁵, Fuhua Yan⁶, Chencheng Zhang⁷, Chen Liu⁸

Affiliations

¹ School of Electrical and Information Engineering, Tianjin University, Tianjin, China.
² Department of Radiology, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China.
³ School of Health Sciences, City, University of London, London, EC1V 0HB, UK.
⁴ School of Information Science and Technology, Shanghai Tech University, Shanghai, China.
⁵ Department of Neurosurgery, Center for Functional Neurosurgery, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China; Clinical Neuroscience Center, Ruijin Hospital LuWan Branch, Shanghai Jiao Tong University School of Medicine, Shanghai, China.
⁶ Department of Radiology, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China. Electronic address: yfh11655@rjh.com.cn.
⁷ Department of Neurosurgery, Center for Functional Neurosurgery, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China; Clinical Neuroscience Center, Ruijin Hospital LuWan Branch, Shanghai Jiao Tong University School of Medicine, Shanghai, China; Shanghai Research Center for Brain Science and Brain-Inspired Technology, Shanghai, China. Electronic address: i@cczhang.org.
⁸ School of Electrical and Information Engineering, Tianjin University, Tianjin, China. Electronic address: liuchen715@tju.edu.cn.

PMID: 35413446
DOI: 10.1016/j.neuroimage.2022.119196

Abstract

The subthalamic nucleus (STN) and globus pallidus internus (GPi) are the two most common and effective target brain areas for deep brain stimulation (DBS) treatment of advanced Parkinson's disease. Although DBS has been shown to restore functional neural circuits of this disorder, the changes in topological organization associated with active DBS of each target remain unknown. To investigate this, we acquired resting-state functional magnetic resonance imaging (fMRI) data from 34 medication-free patients with Parkinson's disease that had DBS electrodes implanted in either the subthalamic nucleus or internal globus pallidus (n = 17 each), in both ON and OFF DBS states. Sixteen age-matched healthy individuals were used as a control group. We evaluated the regional information processing capacity and transmission efficiency of brain networks with and without stimulation, and recorded how stimulation restructured the brain network topology of patients with Parkinson's disease. For both targets, the variation of local efficiency in motor brain regions was significantly correlated (p < 0.05) with improvement rate of the Uniform Parkinson's Disease Rating Scale-III scores, with comparable improvements in motor function for the two targets. However, non-motor brain regions showed changes in topological organization during active stimulation that were target-specific. Namely, targeting the STN decreased the information transmission of association, limbic and paralimbic regions, including the inferior frontal gyrus angle, insula, temporal pole, superior occipital gyri, and posterior cingulate, as evidenced by the simultaneous decrease of clustering coefficient and local efficiency. GPi-DBS had a similar effect on the caudate and lenticular nuclei, but enhanced information transmission in the cingulate gyrus. These effects were not present in the DBS-OFF state for GPi-DBS, but persisted for STN-DBS. Our results demonstrate that DBS to the STN and GPi induce distinct brain network topology reconstruction patterns, providing innovative theoretical evidence for deciphering the mechanism through which DBS affects disparate targets in the human brain.

Keywords: Deep brain stimulation; Network topology; Parkinson's disease; Resting-state functional mri.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Deep Brain Stimulation* / methods
Globus Pallidus
Humans
Magnetic Resonance Imaging
Parkinson Disease* / diagnostic imaging
Parkinson Disease* / therapy
Subthalamic Nucleus*