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. 2019 Dec;9(12):e01450.
doi: 10.1002/brb3.1450. Epub 2019 Oct 24.

Deep brain stimulation modulates pallidal and subthalamic neural oscillations in Tourette's syndrome

Guan-Yu Zhu  1 , Xin-Yi Geng  2   3 , Rui-Li Zhang  2   3 , Ying-Chuan Chen  1 , Yu-Ye Liu  1 , Shou-Yan Wang  2   3 , Jian-Guo Zhang  1   4
Affiliations

Deep brain stimulation modulates pallidal and subthalamic neural oscillations in Tourette's syndrome

Guan-Yu Zhu et al. Brain Behav. 2019 Dec.

Abstract

Introduction: Previous studies found subthalamic nucleus deep brain stimulation (STN-DBS) has clinical effect on Parkinson's disease, dystonia, and obsessive compulsive disorder. It is noteworthy that only a few studies report the STN-DBS for Tourette's syndrome (TS). Globus pallidus interna (GPi)-DBS is the one of the most common targets for TS. So, this paper aims to investigate the neural oscillations in STN and GPi as well as the DBS effect between these two targets in same patients.

Methods: The local field potentials (LFPs) were simultaneously recorded from the bilateral GPi and STN in four patients with TS. The LFPs were decomposed into neural oscillations, and the frequency and time-frequency characteristics of the neural oscillations were analyzed across the conditions of resting, poststimulation, and movement.

Results: No difference of resting LFP was found between the two targets. The poststimulation period spectral power revealed the high beta and gamma oscillations were recovered after GPi-DBS but remained attenuated after STN-DBS. The STN beta oscillation has fewer changes during tics than voluntary movement, and the gamma oscillation was elevated when the tics appeared.

Conclusion: The high beta and gamma oscillations in GPi restored after GPi-DBS, but not STN-DBS. High beta and gamma oscillations may have physiological function in resisting tics in TS. The cortex compensation effect might be interfered by the STN-DBS due to the influence on the hyper-direct pathway but not GPi-DBS.

Keywords: Tourette's syndrome; deep brain stimulation; globus pallidus interna; local field potential; subthalamic nucleus.

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Conflict of interest statement

We wish to confirm that there are no known conflicts of interest associated with this publication and there has been no significant financial support for this work that could have influenced its outcome. We confirm that the manuscript has been read and approved by all named authors and that there are no other persons who satisfied the criteria for authorship is missed. We further confirm that the order of authors listed in the manuscript has been approved by all of us. We confirm that we have given due consideration to the protection of intellectual property associated with this work and that there are no impediments to publication, including the timing of publication, with respect to intellectual property. In so doing, we confirm that we have followed the regulations of our institutions concerning intellectual property. We further confirm that any aspect of the work covered in this manuscript that has involved either experiment animals or human patients has been conducted with the ethical approval of all relevant bodies and that such approvals are acknowledged within the manuscript. We understand that the corresponding author is the sole contact for the editorial process (including editorial manager and direct communications with the office). He/she is responsible for communicating with the other authors about progress, submissions of revisions, and final approval of proofs. We confirm that we have provided a current, correct email address which is accessible by the corresponding author and which has been configured to accept email from zjguo65@163.com.

Figures

Figure 1
Figure 1
Signals and the power spectral density. The electromyography (EMGs) recorded from the symptom‐involved muscle and local field potentials (LFPs) recorded from ipsilateral globus pallidus interna (GPi) and subthalamic nucleus (STN) in case 2 are shown, respectively, in the time range of 0–150 and 117–119 s in panel (a). The percentage power spectra over 0–90 Hz of LFPs recorded at resting state and averaged across all cases are shown in panels (b and c). The alpha power peaks and high beta power peaks were found in both GPi and STN
Figure 2
Figure 2
Statistical comparison across resting and poststimulation conditions. Group‐averaged spectral power over 0–90 Hz and oscillatory bands compared across resting, stimulation with 2.5 V in the other nuclei and poststimulation in the other and the same nuclei. Each colored circle represented the integrated frequency power of an individual nucleus. Spectral power over 20–45 and 60–90 Hz in the globus pallidus interna (GPi) was significantly attenuated by subthalamic stimulation and stayed attenuated after the subthalamic stimulation. Spectral power over 20–45 and 60–90 Hz in the subthalamic nucleus (STN) was significantly attenuated by pallidal stimulation and stayed attenuated by the subthalamic stimulation. Moreover, the spectral power over 20–45 Hz significantly increased after the pallidal stimulation compared to the resting state. The statistical analyses were performed with the paired T‐test between the resting state and the stimulation/poststimulation states. **p < .008. Abbreviations: PS‐GPi, poststimulation in the GPi; PS‐STN, poststimulation in the STN; S‐GPi, stimulation in the GPi; S‐STN, stimulation in the STN
Figure 3
Figure 3
Oscillations modulated by tics and voluntary movement. (a) Power spectra of the local field potential signals in the subthalamic nucleus (STN) and the globus pallidus interna (GPi) at resting state with rare and frequent tics. (b) Trial‐averaged spectrogram of the tics and voluntary movement‐modulated oscillations in the STN and the electromyography (EMG) signals aligned at the time of maximum muscle contraction. (c) Trial‐averaged spectrogram of the tics and voluntary movement‐modulated oscillations in the GPi and the EMG signals aligned at the time of maximum muscle contraction. (d) time‐varying power dynamics of the movement‐modulated oscillations over theta (4–8 Hz), alpha (8–15 Hz), beta (15–30 Hz), and gamma (60–75 Hz) bands. The movement event‐related desynchronization (ERD) and postmovement event‐related synchronization (ERS) over beta band were seen in both nuclei during voluntary movement. The movement ERS over gamma band was seen in the STN during voluntary movement and tics
Figure 4
Figure 4
Schematic illustration of the possible mechanism of the different effect of globus pallidus interna‐deep brain stimulation (GPi‐DBS) and subthalamic nucleus (STN)‐DBS for TS. The low‐frequency oscillation in STN and GPi implicates the pathological state of tics. The high beta oscillation underlines a compensatory sustained inhibition effect, and the gamma oscillation underlines a sudden inhibition effect. The high beta and gamma oscillations in STN and GPi remained attenuated after STN‐DBS, while recovering after GPi‐DBS
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