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Effects of Multi-Session Repetitive Transcranial Magnetic Stimulation on Motor Control and Spontaneous Brain Activity in Multiple System Atrophy: A Pilot Study

Background: Impaired motor control is one of the most common symptoms of multiple system atrophy (MSA). It arises from dysfunction of the cerebellum and its connected neural networks, including the primary motor cortex (M1), and is associated with altered spontaneous (i.e., resting-state) brain netw...

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Autores principales: Liu, Zhu, Ma, Huizi, Poole, Victoria, Wang, Xuemei, Wang, Zhan, Yang, Yaqin, Meng, Lanxi, Manor, Brad, Zhou, Junhong, Feng, Tao
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5954119/
https://www.ncbi.nlm.nih.gov/pubmed/29867391
http://dx.doi.org/10.3389/fnbeh.2018.00090
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author Liu, Zhu
Ma, Huizi
Poole, Victoria
Wang, Xuemei
Wang, Zhan
Yang, Yaqin
Meng, Lanxi
Manor, Brad
Zhou, Junhong
Feng, Tao
author_facet Liu, Zhu
Ma, Huizi
Poole, Victoria
Wang, Xuemei
Wang, Zhan
Yang, Yaqin
Meng, Lanxi
Manor, Brad
Zhou, Junhong
Feng, Tao
author_sort Liu, Zhu
collection PubMed
description Background: Impaired motor control is one of the most common symptoms of multiple system atrophy (MSA). It arises from dysfunction of the cerebellum and its connected neural networks, including the primary motor cortex (M1), and is associated with altered spontaneous (i.e., resting-state) brain network activity. Non-invasive repetitive transcranial magnetic stimulation (rTMS) selectively facilitates the excitability of supraspinal networks. Repeated rTMS sessions have been shown to induce long-term changes to both resting-state brain dynamics and behavior in several neurodegenerative diseases. Here, we hypothesized that a multi-session rTMS intervention would improve motor control in patients with MSA, and that such improvements would correlate with changes in resting-state brain activity. Methods: Nine participants with MSA received daily sessions of 5 Hz rTMS for 5 days. rTMS targeted both the cerebellum and the bilateral M1. Before and within 3 days after the intervention, motor control was assessed by the motor item of the Unified Multiple System Atrophy Rating Scale (UMSARS). Resting-state brain activity was recorded by blood-oxygen-level dependency (BOLD) functional magnetic resonance imaging. The “complexity” of resting-state brain activity fluctuations was quantified within seven well-known functional cortical networks using multiscale entropy, a technique that estimates the degree of irregularity of the BOLD time-series across multiple scales of time. Results: The rTMS intervention was well-attended and was not associated with any adverse events. Average motor scores were lower (i.e., better performance) following the rTMS intervention as compared to baseline (t(8) = 2.3, p = 0.003). Seven of nine participants exhibited such pre-to-post intervention improvements. A trend toward an increase in resting-state complexity was observed within the motor network (t(8) = 1.86, p = 0.07). Participants who exhibited greater increases in motor network resting-state complexity demonstrated greater improvement in motor control (r(2)= 0.72, p = 0.004). Conclusion: This pilot study demonstrated that a five-session rTMS intervention targeting the cerebellum and bilateral M1 is feasible and safe for those with MSA. More definitive, well-controlled trials are warranted to confirm our preliminary results that rTMS may alleviate the severity of motor dysfunction and modulate the multiscale dynamics of motor network brain activity.
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spelling pubmed-59541192018-06-04 Effects of Multi-Session Repetitive Transcranial Magnetic Stimulation on Motor Control and Spontaneous Brain Activity in Multiple System Atrophy: A Pilot Study Liu, Zhu Ma, Huizi Poole, Victoria Wang, Xuemei Wang, Zhan Yang, Yaqin Meng, Lanxi Manor, Brad Zhou, Junhong Feng, Tao Front Behav Neurosci Neuroscience Background: Impaired motor control is one of the most common symptoms of multiple system atrophy (MSA). It arises from dysfunction of the cerebellum and its connected neural networks, including the primary motor cortex (M1), and is associated with altered spontaneous (i.e., resting-state) brain network activity. Non-invasive repetitive transcranial magnetic stimulation (rTMS) selectively facilitates the excitability of supraspinal networks. Repeated rTMS sessions have been shown to induce long-term changes to both resting-state brain dynamics and behavior in several neurodegenerative diseases. Here, we hypothesized that a multi-session rTMS intervention would improve motor control in patients with MSA, and that such improvements would correlate with changes in resting-state brain activity. Methods: Nine participants with MSA received daily sessions of 5 Hz rTMS for 5 days. rTMS targeted both the cerebellum and the bilateral M1. Before and within 3 days after the intervention, motor control was assessed by the motor item of the Unified Multiple System Atrophy Rating Scale (UMSARS). Resting-state brain activity was recorded by blood-oxygen-level dependency (BOLD) functional magnetic resonance imaging. The “complexity” of resting-state brain activity fluctuations was quantified within seven well-known functional cortical networks using multiscale entropy, a technique that estimates the degree of irregularity of the BOLD time-series across multiple scales of time. Results: The rTMS intervention was well-attended and was not associated with any adverse events. Average motor scores were lower (i.e., better performance) following the rTMS intervention as compared to baseline (t(8) = 2.3, p = 0.003). Seven of nine participants exhibited such pre-to-post intervention improvements. A trend toward an increase in resting-state complexity was observed within the motor network (t(8) = 1.86, p = 0.07). Participants who exhibited greater increases in motor network resting-state complexity demonstrated greater improvement in motor control (r(2)= 0.72, p = 0.004). Conclusion: This pilot study demonstrated that a five-session rTMS intervention targeting the cerebellum and bilateral M1 is feasible and safe for those with MSA. More definitive, well-controlled trials are warranted to confirm our preliminary results that rTMS may alleviate the severity of motor dysfunction and modulate the multiscale dynamics of motor network brain activity. Frontiers Media S.A. 2018-05-09 /pmc/articles/PMC5954119/ /pubmed/29867391 http://dx.doi.org/10.3389/fnbeh.2018.00090 Text en Copyright © 2018 Liu, Ma, Poole, Wang, Wang, Yang, Meng, Manor, Zhou and Feng. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Liu, Zhu
Ma, Huizi
Poole, Victoria
Wang, Xuemei
Wang, Zhan
Yang, Yaqin
Meng, Lanxi
Manor, Brad
Zhou, Junhong
Feng, Tao
Effects of Multi-Session Repetitive Transcranial Magnetic Stimulation on Motor Control and Spontaneous Brain Activity in Multiple System Atrophy: A Pilot Study
title Effects of Multi-Session Repetitive Transcranial Magnetic Stimulation on Motor Control and Spontaneous Brain Activity in Multiple System Atrophy: A Pilot Study
title_full Effects of Multi-Session Repetitive Transcranial Magnetic Stimulation on Motor Control and Spontaneous Brain Activity in Multiple System Atrophy: A Pilot Study
title_fullStr Effects of Multi-Session Repetitive Transcranial Magnetic Stimulation on Motor Control and Spontaneous Brain Activity in Multiple System Atrophy: A Pilot Study
title_full_unstemmed Effects of Multi-Session Repetitive Transcranial Magnetic Stimulation on Motor Control and Spontaneous Brain Activity in Multiple System Atrophy: A Pilot Study
title_short Effects of Multi-Session Repetitive Transcranial Magnetic Stimulation on Motor Control and Spontaneous Brain Activity in Multiple System Atrophy: A Pilot Study
title_sort effects of multi-session repetitive transcranial magnetic stimulation on motor control and spontaneous brain activity in multiple system atrophy: a pilot study
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5954119/
https://www.ncbi.nlm.nih.gov/pubmed/29867391
http://dx.doi.org/10.3389/fnbeh.2018.00090
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