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

• Published in: NeuroImage (Orlando, Fla.) Fla.), 2022-07, Vol.255, p.119196-119196, Article 119196
• Main Authors: Chu, Chunguang, He, Naying, Zeljic, Kristina, Zhang, Zhen, Wang, Jiang, Li, Jun, Liu, Yu, Zhang, Youmin, Sun, Bomin, Li, Dianyou, Yan, Fuhua, Zhang, Chencheng, Liu, Chen
• Format: Article
• Language: English
• Subjects: Brain mapping; Deep brain stimulation; Deep Brain Stimulation - methods; Electrical stimuli; Frontal gyrus; Functional magnetic resonance imaging; Functional morphology; Globus Pallidus; Humans; Information processing; Magnetic Resonance Imaging; Movement disorders; Network topology; Neural networks; Neurodegenerative diseases; Neuroimaging; Parkinson Disease - diagnostic imaging; Parkinson Disease - therapy; Parkinson's disease; Patients; Resting-state functional mri; Solitary tract nucleus; Subthalamic Nucleus; Time series
• ISSN: 1053-8119; 1095-9572
• DOI: 10.1016/j.neuroimage.2022.119196

•STN-DBS and GPi-DBS exhibit a similar effect of topological restoration on the motor brain network.•The ability of STN-DBS and GPi-DBS to improve motor function is reflected in enhanced local efficiency of motor brain regions.•STN-DBS and GPi-DBS decrease and increase, respectively, regional information processing capacity and transmission efficiency of distinct non-motor regions.•The effect of STN-DBS on non-motor topological features persists after DBS is switched off, while that of GPi-DBS dose not. 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 b