Dataset Information

The altered spontaneous neural activity in patients with Parkinson's disease and its predictive value for the motor improvement of deep brain stimulation.

ABSTRACT:

Background

This study aims to investigate the altered spontaneous neural activity in patients with Parkinson's disease (PD) revealed by amplitudes of low-frequency fluctuations (ALFF) of resting-state fMRI, and the feasibility of using ALFF as neuroimaging predictors for motor improvement after bilateral subthalamic nucleus (STN) deep brain stimulation (DBS).

Methods

Fourty-four patients and 44 healthy controls were included in this study. First, the ALFF of patients with PD was compared with that of controls; then significant clusters were correlated with motor improvement after DBS (unified Parkinson's disease rating scale (UPDRS-III)) and other clinical variables. Second, regression and classification of the machine learning models were conducted to predict motor improvement after DBS. Receiver operating characteristic (ROC) analysis was used to evaluate the performance of the classification model.

Results

Compared with healthy controls, patients with PD showed increased ALFF in the bilateral motor area and decreased ALFF in the bilateral temporal cortex and cerebellum. The Hoehn-Yahr stages correlated with ALFF within the bilateral cerebellum (p = 0.021), and UPDRS-III improvement correlated with ALFF in the left (p < 0.001) and right (p = 0.005) motor areas. The regression model showed a significant correlation between the predicted and observed UPDRS-III changes (R = 0.65, p < 0.001). The ROC analysis revealed an area under the curve (AUC) of 0.94 which differentiated moderate and superior DBS responders.

Conclusion

The results revealed altered ALFF patterns in patients with PD and their correlations with clinical variables. Both binary and continuous ALFF can potentially serve as predictive biomarkers for DBS response.

SUBMITTER: Yang B

PROVIDER: S-EPMC10197096 | biostudies-literature | 2023 May

REPOSITORIES: biostudies-literature

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Publications

The altered spontaneous neural activity in patients with Parkinson's disease and its predictive value for the motor improvement of deep brain stimulation.

Yang Bowen B Wang Xiu X Mo Jiajie J Li Zilin Z Hu Wenhan W Zhang Chao C Zhao Baotian B Gao Dongmei D Zhang Xin X Zou Liangying L Zhao Xuemin X Guo Zhihao Z Zhang Jianguo J Zhang Kai K

NeuroImage. Clinical 20230509

<h4>Background</h4>This study aims to investigate the altered spontaneous neural activity in patients with Parkinson's disease (PD) revealed by amplitudes of low-frequency fluctuations (ALFF) of resting-state fMRI, and the feasibility of using ALFF as neuroimaging predictors for motor improvement after bilateral subthalamic nucleus (STN) deep brain stimulation (DBS).<h4>Methods</h4>Fourty-four patients and 44 healthy controls were included in this study. First, the ALFF of patients with PD was c ...[more]

PMID: 37182459

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Project description:Deep brain stimulation is an established therapy for Parkinson's disease; however, its effectiveness is hindered by limited understanding of therapeutic mechanisms and the lack of a robust feedback signal for tailoring stimulation. We recently reported that subthalamic nucleus deep brain stimulation evokes a neural response resembling a decaying high-frequency (200-500 Hz) oscillation that typically has a duration of at least 10 ms and is localizable to the dorsal sub-region. As the morphology of this response suggests a propensity for the underlying neural circuitry to oscillate at a particular frequency, we have named it evoked resonant neural activity. Here, we determine whether this evoked activity is modulated by therapeutic stimulation - a critical attribute of a feedback signal. Furthermore, we investigated whether any related changes occurred in spontaneous local field potentials. Evoked and spontaneous neural activity was intraoperatively recorded from 19 subthalamic nuclei in patients with Parkinson's disease. Recordings were obtained before therapeutic stimulation and during 130 Hz stimulation at increasing amplitudes (0.67-3.38 mA), 'washout' of therapeutic effects, and non-therapeutic 20 Hz stimulation. Therapeutic efficacy was assessed using clinical bradykinesia and rigidity scores. The frequency and amplitude of evoked resonant neural activity varied with the level of 130 Hz stimulation (p < .001). This modulation coincided with improvement in bradykinesia and rigidity (p < .001), and correlated with spontaneous beta band suppression (p < .001). Evoked neural activity occupied a similar frequency band to spontaneous high-frequency oscillations (200-400 Hz), both of which decreased to around twice the 130 Hz stimulation rate. Non-therapeutic stimulation at 20 Hz evoked, but did not modulate, resonant activity. These results indicate that therapeutic deep brain stimulation alters the frequency of evoked and spontaneous oscillations recorded in the subthalamic nucleus that are likely generated by loops within the cortico-basal ganglia-thalamo-cortical network. Evoked resonant neural activity therefore has potential as a tool for providing insight into brain network function and has key attributes of a dynamic feedback signal for optimizing therapy.

Project description:ObjectiveA motor speech disorder or dysarthria commonly arises in patients with Parkinson's disease (PD). The impact of subthalamic nucleus (STN) deep brain stimulation (DBS) on motor speech and the potential of intraoperative motor speech testing to predict outcomes are unknown. This study examined 1) the types and prevalence of motor speech changes observed with STN DBS and their relation to the preoperative condition, 2) the ability of intraoperative testing to predict postoperative changes in motor speech, and 3) the spatial relationship between stimulation sites producing maximal motor improvement, as measured by the Movement Disorder Society Unified Parkinson's Disease Rating Scale (MDS-UPDRS), and maximal motor speech deterioration.MethodsComprehensive preoperative, intraoperative, and postoperative motor speech/dysarthria evaluations were performed in consecutive patients with advanced idiopathic PD who underwent STN DBS surgery in the period from 2011 to 2016. Preoperative type of dysarthria and overall dysarthria severity rating along with intraoperative motor speech testing results were evaluated as predictors of postoperative change. Atlas-independent, fully individualized field modeling was used to identify stimulation sites associated with maximal MDS-UPDRS motor improvement and motor speech deterioration.ResultsForty-three patients with PD treated with STN DBS were prospectively studied. Improved MDS-UPDRS motor scores and worsened dysarthria were demonstrated by a subset of patients (16/43). Preoperative dysarthria characteristics did not predict postoperative deterioration. Intraoperative assessment of motor speech strongly predicted postoperative outcomes (OR 4.4, p = 0.02). Sites of maximal MDS-UPDRS motor improvement and worsened dysarthria were distinct. Worsened dysarthria was associated with capsular stimulation, anterior and ventral to the site of maximal MDS-UPDRS motor improvement.ConclusionsThe predictive reliability of intraoperative motor speech testing, together with the identification of distinct stimulation sites for motor speech impairment and improved MDS-UPDRS motor function, raise the possibility that DBS lead repositioning or reprogramming could reduce adverse effects on motor speech without impacting MDS-UPDRS motor outcomes in patients undergoing STN DBS.

Project description:BackgroundParkinson's disease is a common neurodegenerative disease, with depression being a common non-motor symptom. Bilateral subthalamic nucleus deep brain stimulation is an effective method for the treatment of Parkinson's disease. Thus, this study aimed to establish a nomogram of the possibility of achieving a better depression improvement rate after subthalamic nucleus deep brain stimulation in patients with Parkinson's disease.MethodsWe retrospectively analyzed 103 patients with Parkinson's disease who underwent subthalamic nucleus deep brain stimulation and were followed up for the improvement of their Hamilton Depression scale scores 1 year postoperatively. Univariate and multivariate logistic regression analyses were used to select factors affecting the improvement rate of depression. A nomogram was then developed to predict the possibility of achieving better depression improvement. Furthermore, the discrimination and fitting performance was evaluated using a calibration diagram, receiver operating characteristics, and decision curve analysis.ResultsThe mean and median improvement rates of Hamilton Depression scores were 13.1 and 33.3%, respectively. Among the 103 patients, 70.8% had an improved depression, 23.3% had a worsened depression, and 5.8% remained unchanged. Logistic multivariate regression analysis showed that age, preoperative Parkinson's Disease Questionnaire, Hamilton Anxiety, and Hamilton Depression scores were independent factors for the possibility of achieving a better depression improvement rate. Based on these results, a nomogram model was developed. The nomogram had a C-index of 0.78 (95% confidence interval: 0.69-0.87) and an area under the receiver operating characteristics of 0.78 (95% confidence interval: 0.69-0.87). The calibration plot and decision curve analysis further demonstrated goodness-of-fit between the nomogram predictions and actual observations.ConclusionWe developed a nomogram to predict the possibility of achieving good depression improvement 1 year after subthalamic nucleus deep brain stimulation in patients with Parkinson's disease, which showed a certain value in judging the expected depression improvement of these patients.

Project description: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.

Dataset Information

The altered spontaneous neural activity in patients with Parkinson's disease and its predictive value for the motor improvement of deep brain stimulation.

Background

Methods

Results

Conclusion

Publications

The altered spontaneous neural activity in patients with Parkinson's disease and its predictive value for the motor improvement of deep brain stimulation.

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