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Noninvasive theta-burst stimulation of the human striatum enhances striatal activity and motor skill learning.

ABSTRACT: The stimulation of deep brain structures has thus far only been possible with invasive methods. Transcranial electrical temporal interference stimulation (tTIS) is a novel, noninvasive technology that might overcome this limitation. The initial proof-of-concept was obtained through modeling, physics experiments and rodent models. Here we show successful noninvasive neuromodulation of the striatum via tTIS in humans using computational modeling, functional magnetic resonance imaging studies and behavioral evaluations. Theta-burst patterned striatal tTIS increased activity in the striatum and associated motor network. Furthermore, striatal tTIS enhanced motor performance, especially in healthy older participants as they have lower natural learning skills than younger subjects. These findings place tTIS as an exciting new method to target deep brain structures in humans noninvasively, thus enhancing our understanding of their functional role. Moreover, our results lay the groundwork for innovative, noninvasive treatment strategies for brain disorders in which deep striatal structures play key pathophysiological roles.

SUBMITTER: Wessel MJ

PROVIDER: S-EPMC10620076 | biostudies-literature | 2023 Nov

REPOSITORIES: biostudies-literature

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Noninvasive theta-burst stimulation of the human striatum enhances striatal activity and motor skill learning.

Wessel Maximilian J MJ Beanato Elena E Popa Traian T Windel Fabienne F Vassiliadis Pierre P Menoud Pauline P Beliaeva Valeriia V Violante Ines R IR Abderrahmane Hedjoudje H Dzialecka Patrycja P Park Chang-Hyun CH Maceira-Elvira Pablo P Morishita Takuya T Cassara Antonino M AM Steiner Melanie M Grossman Nir N Neufeld Esra E Hummel Friedhelm C FC

Nature neuroscience 20231019 11

The stimulation of deep brain structures has thus far only been possible with invasive methods. Transcranial electrical temporal interference stimulation (tTIS) is a novel, noninvasive technology that might overcome this limitation. The initial proof-of-concept was obtained through modeling, physics experiments and rodent models. Here we show successful noninvasive neuromodulation of the striatum via tTIS in humans using computational modeling, functional magnetic resonance imaging studies and b ...[more]

PMID: 37857774

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Project description:BackgroundTheta burst stimulation (TBS) is an efficient noninvasive neuromodulation paradigm that has been widely adopted, clinically. However, the efficacy of TBS treatment remains similarly modest as conventional 10 Hz repetitive transcranial magnetic stimulation (rTMS).Objective/hypothesisTo develop a new TBS paradigm that enhances the effects of TMS administration while maintaining high time-efficiency.MethodsWe describe here a new TMS paradigm, named High-Density Theta Burst Stimulation (hdTBS). This paradigm delivers up to 6 pulses per burst, as opposed to only 3 in conventional TBS, while maintaining the inter-burst interval of 200 ms (or 5 Hz) - a critical parameter in inducing long-term potentiation. This paradigm was implemented on a TMS stimulator developed in-house; its physiological effects were assessed in the motor cortex of awake rats using a rodent specific focal TMS coil. Microwire electrodes were implanted into each rat's limb muscles to longitudinally record motor-evoked potential (MEP). Four different TBS paradigms (3, 4, 5 or 6 pulses per burst, 200 s per session) were tested; MEP signals were recorded immediately before (baseline) and up to 35 min post each TBS session.ResultsWe developed a stimulator based on a printed-circuit board strategy. The stimulator was able to deliver stable outputs of up to 6 pulses per burst. Animal experiments (n = 15) revealed significantly different aftereffects induced by the four TBS paradigms (Friedman test, p = 0.018). Post hoc analysis further revealed that, in comparison to conventional 3-pulse TBS, 5- and 6-pulse TBS enhanced the aftereffects of MEP signals by 56% and 92%, respectively, while maintaining identical time efficiency.Conclusion(s)A new stimulation paradigm is proposed, implemented and tested in the motor cortex of awake rats using a focal TMS coil developed in the lab. We observed enhanced aftereffects as assessed by MEP, with no obvious adverse effects, suggesting the translational potentials of this paradigm.

Project description:BackgroundStroke is the second leading cause of death and the third leading cause of disability worldwide. Motor dysfunction is a common sequela, which seriously affects the lives of patients. Theta burst stimulation (TBS) is a new transcranial magnetic therapy for improving motor dysfunction after stroke. However, there remains a lack of studies on the mechanism, theoretical model, and effectiveness of TBS in improving motor dysfunction following stroke.ObjectiveThis paper provides a comprehensive overview and assessment of the current impact of TBS on motor rehabilitation following stroke and analyzes potential factors contributing to treatment effect disparities. The aim is to offer recommendations for further refining the TBS treatment approach in subsequent clinical studies while also furnishing evidence for devising tailored rehabilitation plans for stroke patients.MethodsThis study was conducted following PRISMA guidelines. PubMed, Embase, Web of Science, and the Cochrane Library were searched systematically from the establishment of the database to February 2024. Relevant studies using TBS to treat patients with motor dysfunction after stroke will be included. Data on study characteristics, interventions, outcome measures, and primary outcomes were extracted. The Modified Downs and Black Checklist was used to assess the potential bias of the included studies, and a narrative synthesis of the key findings was finally conducted.ResultsThe specific mechanism of TBS in improving motor dysfunction after stroke has not been fully elucidated, but it is generally believed that TBS can improve the functional prognosis of patients by regulating motor cortical excitability, inducing neural network reorganization, and regulating cerebral circulation metabolism. Currently, most relevant clinical studies are based on the interhemispheric inhibition model (IHI), the vicariation model, and the bimodal balance-recovery model. Many studies have verified the effectiveness of TBS in improving the motor function of stroke patients, but the therapeutic effect of some studies is controversial.ConclusionOur results show that TBS has a good effect on improving motor function in stroke patients, but more large-scale, high-quality, multicenter studies are still necessary in the future to further clarify the mechanism of TBS and explore the optimal TBS treatment.

Dataset Information

Noninvasive theta-burst stimulation of the human striatum enhances striatal activity and motor skill learning.

Publications

Noninvasive theta-burst stimulation of the human striatum enhances striatal activity and motor skill learning.

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