Altered Spontaneous Neural Activity and Functional Connectivity in Parkinson’s Disease With Subthalamic Microlesion

Abstract

BackgroundTransient improvement in motor symptoms are immediately observed in patients with Parkinson’s disease (PD) after an electrode has been implanted into the subthalamic nucleus (STN) for deep brain stimulation (DBS). This phenomenon is known as the microlesion effect (MLE). However, the underlying mechanisms of MLE is poorly understood.PurposeWe utilized resting state functional MRI (rs-fMRI) to evaluate changes in spontaneous brain activity and networks in PD patients during the microlesion period after DBS.MethodOverall, 37 PD patients and 13 gender- and age-matched healthy controls (HCs) were recruited for this study. Rs-MRI information was collected from PD patients three days before DBS and one day after DBS, whereas the HCs group was scanned once. We utilized the amplitude of low-frequency fluctuation (ALFF) method in order to analyze differences in spontaneous whole-brain activity among all subjects. Furthermore, functional connectivity (FC) was applied to investigate connections between other brain regions and brain areas with significantly different ALFF before and after surgery in PD patients.ResultRelative to the PD-Pre-DBS group, the PD-Post-DBS group had higher ALFF in the right putamen, right inferior frontal gyrus, right precentral gyrus and lower ALFF in right angular gyrus, right precuneus, right posterior cingulate gyrus (PCC), left insula, left middle temporal gyrus (MTG), bilateral middle frontal gyrus and bilateral superior frontal gyrus (dorsolateral). Functional connectivity analysis revealed that these brain regions with significantly different ALFF scores demonstrated abnormal FC, largely in the temporal, prefrontal cortices and default mode network (DMN).ConclusionThe subthalamic microlesion caused by DBS in PD was found to not only improve the activity of the basal ganglia-thalamocortical circuit, but also reduce the activity of the DMN and executive control network (ECN) related brain regions. Results from this study provide new insights into the mechanism of MLE.

Alterations of resting-state networks of Parkinson‘s disease patients after subthalamic DBS surgery

“…Since the high frequencies were not changed, this could imply a more important role of the low frequencies in network formation. Similar results were found for a motor task ( Jech et al, 2012 ) and in a resting-state fMRI study that found amplitude changes of low-frequency fluctuations in many brain regions ( Luo et al, 2021 ).…”

“…This effect is called stun effect and is probably caused by inflammatory processes and edema ( Chen et al, 2006 , Mann et al, 2009 ). To date, only one prior fMRI study has revealed altered cortical and subcortical functional connectivity due to the stun effect ( Luo et al, 2021 ). Thus, detailed investigation of changes in functional networks is missing.…”

Effect of Subthalamic Stimulation and Electrode Implantation in the Striatal Microenvironment in a Parkinson’s Disease Rat Model

“…Furthermore, it has been shown that the insertional effect itself may induce motor improvement even prior to initiating stimulation in individuals [ 40 , 41 ]. Indeed, STN-microlesions may present therapeutic responses similar to those observed in thalamotomies [ 35 , 42 , 43 ]. However, unlike therapeutic DBS, stereotactic ablative procedures are irreversible and may induce debilitating and permanent adverse effects [ 44 , 45 ].…”

Predicting Delayed Neurocognitive Recovery After Non-cardiac Surgery Using Resting-State Brain Network Patterns Combined With Machine Learning

“…The abnormal FC patterns of DMN were associated with various diseases related to cognitive impairment, such as mild cognitive impairment, AD, Parkinson’s disease, and attention-deficit/hyperactivity disorder ( Zhang H. et al, 2020 ; Duffy et al, 2021 ; Luo et al, 2021 ; Tang et al, 2021 ; Wang et al, 2021 ). Zhang et al investigated the subjects at high risk of AD compared to the low-risk subjects, presenting significantly altered FC in the PCC and middle frontal cortex ( Zhang X. Y. et al, 2020 ).…”