Thalamic Local Field Potentials Are Related to Long-Term DBS Effects in Tourette Syndrome

Abstract

Background: Local field potential (LFP) recordings helped to clarify the pathophysiology of Tourette syndrome (TS) and to define new strategies for deep brain stimulation (DBS) treatment for refractory TS, based on the delivery of stimulation in accordance with changes in the electrical activity of the DBS target area. However, there is little evidence on the relationship between LFP pattern and DBS outcomes in TS.Objective: To investigate the relationship between LFP oscillations and DBS effects on tics and on obsessive compulsive behavior (OCB) comorbidities.Methods: We retrospectively analyzed clinical data and LFP recordings from 17 patients treated with DBS of the centromedian-parafascicular/ventralis oralis (CM-Pf/VO) complex, and followed for more several years after DBS in the treating center. In these patients, LFPs were recorded either in the acute setting (3–5 days after DBS electrode implant) or in the chronic setting (during impulse generator replacement surgery). LFP oscillations were correlated with the Yale Global Tic Severity Scale (YGTSS) and the Yale–Brown Obsessive–Compulsive Scale (Y-BOCS) collected at baseline (before DBS surgery), 1 year after DBS, and at the last follow-up available.Results: We found that, at baseline, in the acute setting, the power of the oscillations included in the 5–15-Hz band, previously identified as TS biomarker, is correlated with the pathophysiology of tics, being significantly correlated with total YGTSS before DBS (Spearman's ρ = 0.701, p = 0.011). The power in the 5–15-Hz band was also correlated with the improvement in Y-BOCS after 1 year of DBS (Spearman's ρ = −0.587, p = 0.045), thus suggesting a relationship with the DBS effects on OCB comorbidities.Conclusions: Our observations confirm that the low-frequency (5–15-Hz) band is a significant biomarker of TS, being related to the severity of tics and, also to the long-term response on OCBs. This represents a step toward both the understanding of the mechanisms underlying DBS effects in TS and the development of adaptive DBS strategies.

Myoclonus and other jerky movement disorders

“…The search for tic-related neurophysiological markers and their distinguishing features from voluntary actions has been further augmented by the therapeutic application of deep brain stimulation in tic disorders, as it provided a means to record neurophysiological signals from subcortical structures. Several studies by now have demonstrated that a low-frequency oscillatory signal (between 3 and 12 Hz) recorded from both thalamic (typically from the centromedian–parafascicular nucleus CM-Pf/ in proximity to the nucleus ventralis oralis internus, Voi) and pallidal (globus pallidus pars interna) structures correlates with tic severity measures,( Bour et al, 2015 , Cagle et al, 2020 , Jimenez-Shahed et al, 2016 , Marceglia et al, 2021 , Marceglia et al, 2010 , Neumann et al, 2018 , Shute et al, 2016 ). Importantly, one study demonstrated that the duration rather than the amplitude of theta burst activity by both structures was associated with preoperative tic severity ( Neumann et al, 2018 ).…”

Recent progress on Tourette syndrome

“…Local field potentials can be recorded during deep brain stimulation (DBS) implantation surgery. A retrospective clinical study of 17 patients with TS who underwent DBS of the thalamus showed that increased power in the low-frequency (5–15 Hz) band could be a biomarker for TS and correlated with the severity of tics 42 .…”