Subthalamic high-beta oscillation informs the outcome of deep brain stimulation in patients with Parkinson's disease

Po-Lin Chen; Yi-Chieh Chen; Po-Hsun Tu; Tzu-Chi Liu; Min-Chi Chen; Hau-Tieng Wu; Mun-Chun Yeap; Chih-Hua Yeh; Chin-Song Lu; Chiung-Chu Chen

doi:10.3389/fnhum.2022.958521

Subthalamic high-beta oscillation informs the outcome of deep brain stimulation in patients with Parkinson's disease

Front Hum Neurosci. 2022 Sep 8:16:958521. doi: 10.3389/fnhum.2022.958521. eCollection 2022.

Authors

Po-Lin Chen^{1

2}, Yi-Chieh Chen^{1

2

3}, Po-Hsun Tu^{3

4}, Tzu-Chi Liu^{2

5}, Min-Chi Chen^{6

7}, Hau-Tieng Wu^{8

9}, Mun-Chun Yeap⁴, Chih-Hua Yeh^{3

10}, Chin-Song Lu¹¹, Chiung-Chu Chen^{1

2

3}

Affiliations

¹ Division of Movement Disorders, Department of Neurology, Chang Gung Memorial Hospital, Taoyuan, Taiwan.
² Neuroscience Research Center, Chang Gung Memorial Hospital, Taoyuan, Taiwan.
³ College of Medicine, Chang Gung University, Taoyuan, Taiwan.
⁴ Department of Neurosurgery, Chang Gung Memorial Hospital, Taoyuan, Taiwan.
⁵ Department of Mathematics, National Taiwan University, Taipei, Taiwan.
⁶ Department of Public Health, Biostatistics Consulting Center, College of Medicine, Chang Gung University, Taoyuan, Taiwan.
⁷ Department of Obstetrics and Gynecology, Chang Gung Memorial Hospital, Chiayi, Taiwan.
⁸ Department of Mathematics, Duke University, Durham, NC, United States.
⁹ Department of Statistical Science, Duke University, Durham, NC, United States.
¹⁰ Department of Neuroradiology, Chang Gung Memorial Hospital, Taoyuan, Taiwan.
¹¹ Professor Lu Neurological Clinic, Taoyuan, Taiwan.

Abstract

Background: The therapeutic effect of deep brain stimulation (DBS) of the subthalamic nucleus (STN) for Parkinson's disease (PD) is related to the modulation of pathological neural activities, particularly the synchronization in the β band (13-35 Hz). However, whether the local β activity in the STN region can directly predict the stimulation outcome remains unclear.

Objective: We tested the hypothesis that low-β (13-20 Hz) and/or high-β (20-35 Hz) band activities recorded from the STN region can predict DBS efficacy.

Methods: Local field potentials (LFPs) were recorded in 26 patients undergoing deep brain stimulation surgery in the subthalamic nucleus area. Recordings were made after the implantation of the DBS electrode prior to its connection to a stimulator. The maximum normalized powers in the theta (4-7 Hz), alpha (7-13 Hz), low-β (13-20 Hz), high-β (20-35 Hz), and low-γ (40-55 Hz) subbands in the postoperatively recorded LFP were correlated with the stimulation-induced improvement in contralateral tremor or bradykinesia-rigidity. The distance between the contact selected for stimulation and the contact with the maximum subband power was correlated with the stimulation efficacy. Following the identification of the potential predictors by the significant correlations, a multiple regression analysis was performed to evaluate their effect on the outcome.

Results: The maximum high-β power was positively correlated with bradykinesia-rigidity improvement (r _s = 0.549, p < 0.0001). The distance to the contact with maximum high-β power was negatively correlated with bradykinesia-rigidity improvement (r _s = -0.452, p < 0.001). No significant correlation was observed with low-β power. The maximum high-β power and the distance to the contact with maximum high-β power were both significant predictors for bradykinesia-rigidity improvement in the multiple regression analysis, explaining 37.4% of the variance altogether. Tremor improvement was not significantly correlated with any frequency.

Conclusion: High-β oscillations, but not low-β oscillations, recorded from the STN region with the DBS lead can inform stimulation-induced improvement in contralateral bradykinesia-rigidity in patients with PD. High-β oscillations can help refine electrode targeting and inform contact selection for DBS therapy.

Keywords: Parkinson's disease; beta oscillations; deep brain stimulation; stimulation efficacy; subthalamic nucleus (STN).