Investigating brain network dynamics in state-dependent stimulation: A concurrent electroencephalography and transcranial magnetic stimulation study using hidden Markov models

IF 7.6 1区 医学 Q1 CLINICAL NEUROLOGY
Saeed Makkinayeri , Roberto Guidotti , Alessio Basti , Mark W. Woolrich , Chetan Gohil , Mauro Pettorruso , Maria Ermolova , Risto J. Ilmoniemi , Ulf Ziemann , Gian Luca Romani , Vittorio Pizzella , Laura Marzetti
{"title":"Investigating brain network dynamics in state-dependent stimulation: A concurrent electroencephalography and transcranial magnetic stimulation study using hidden Markov models","authors":"Saeed Makkinayeri ,&nbsp;Roberto Guidotti ,&nbsp;Alessio Basti ,&nbsp;Mark W. Woolrich ,&nbsp;Chetan Gohil ,&nbsp;Mauro Pettorruso ,&nbsp;Maria Ermolova ,&nbsp;Risto J. Ilmoniemi ,&nbsp;Ulf Ziemann ,&nbsp;Gian Luca Romani ,&nbsp;Vittorio Pizzella ,&nbsp;Laura Marzetti","doi":"10.1016/j.brs.2025.03.020","DOIUrl":null,"url":null,"abstract":"<div><h3>Background</h3><div>Systems neuroscience studies have shown that baseline brain activity can be categorized into large-scale networks (resting-state-networks, RNSs), with influence on cognitive abilities and clinical symptoms. These insights have guided millimeter-precise selection of brain stimulation targets based on RSNs. Concurrently, Transcranial Magnetic Stimulation (TMS) studies revealed that baseline brain states, measured by EEG signal power or phase, affect stimulation outcomes. However, EEG dynamics in these studies are mostly limited to single regions or channels, lacking the spatial resolution needed for accurate network-level characterization.</div></div><div><h3>Objective</h3><div>We aim at mapping brain networks with high spatial and temporal precision and to assess whether the occurrence of specific network-level-states impact TMS outcome. To this end, we will identify large-scale brain networks and explore how their dynamics relates to corticospinal excitability.</div></div><div><h3>Methods</h3><div>This study leverages Hidden Markov Models to identify large-scale brain states from pre-stimulus source space high-density-EEG data collected during TMS targeting the left primary motor cortex in twenty healthy subjects. The association between states and fMRI-defined RSNs was explored using the Yeo atlas, and the trial-by-trial relation between states and corticospinal excitability was examined.</div></div><div><h3>Results</h3><div>We extracted fast-dynamic large-scale brain states with unique spatiotemporal and spectral features resembling major RSNs. The engagement of different networks significantly influences corticospinal excitability, with larger motor evoked potentials when baseline activity was dominated by the sensorimotor network.</div></div><div><h3>Conclusions</h3><div>These findings represent a step forward towards characterizing brain network in EEG-TMS with both high spatial and temporal resolution and underscore the importance of incorporating large-scale network dynamics into TMS experiments.</div></div>","PeriodicalId":9206,"journal":{"name":"Brain Stimulation","volume":"18 3","pages":"Pages 800-809"},"PeriodicalIF":7.6000,"publicationDate":"2025-03-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Brain Stimulation","FirstCategoryId":"3","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S1935861X25000774","RegionNum":1,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"CLINICAL NEUROLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

Background

Systems neuroscience studies have shown that baseline brain activity can be categorized into large-scale networks (resting-state-networks, RNSs), with influence on cognitive abilities and clinical symptoms. These insights have guided millimeter-precise selection of brain stimulation targets based on RSNs. Concurrently, Transcranial Magnetic Stimulation (TMS) studies revealed that baseline brain states, measured by EEG signal power or phase, affect stimulation outcomes. However, EEG dynamics in these studies are mostly limited to single regions or channels, lacking the spatial resolution needed for accurate network-level characterization.

Objective

We aim at mapping brain networks with high spatial and temporal precision and to assess whether the occurrence of specific network-level-states impact TMS outcome. To this end, we will identify large-scale brain networks and explore how their dynamics relates to corticospinal excitability.

Methods

This study leverages Hidden Markov Models to identify large-scale brain states from pre-stimulus source space high-density-EEG data collected during TMS targeting the left primary motor cortex in twenty healthy subjects. The association between states and fMRI-defined RSNs was explored using the Yeo atlas, and the trial-by-trial relation between states and corticospinal excitability was examined.

Results

We extracted fast-dynamic large-scale brain states with unique spatiotemporal and spectral features resembling major RSNs. The engagement of different networks significantly influences corticospinal excitability, with larger motor evoked potentials when baseline activity was dominated by the sensorimotor network.

Conclusions

These findings represent a step forward towards characterizing brain network in EEG-TMS with both high spatial and temporal resolution and underscore the importance of incorporating large-scale network dynamics into TMS experiments.
研究状态依赖刺激下的脑网络动力学:使用隐马尔可夫模型的并发脑电图和经颅磁刺激研究。
背景:系统神经科学研究表明,基线脑活动可分为大型网络(静息状态网络,RNSs),对认知能力和临床症状有影响。这些见解指导了基于rsn的精确到毫米的脑刺激目标选择。同时,经颅磁刺激(TMS)研究表明,通过脑电图信号功率或相位测量的基线脑状态会影响刺激结果。然而,这些研究中的脑电动态大多局限于单个区域或通道,缺乏准确的网络级表征所需的空间分辨率。目的:我们旨在以高时空精度绘制脑网络,并评估特定网络水平状态的发生是否影响经颅磁刺激结果。为此,我们将确定大规模的大脑网络,并探索其动态与皮质脊髓兴奋性的关系。方法:采用隐马尔可夫模型对20名健康受试者的左初级运动皮层经颅磁刺激前刺激源空间高密度脑电图数据进行大规模脑状态识别。使用Yeo图谱探索状态与fmri定义的rsn之间的关联,并检查状态与皮质脊髓兴奋性之间的逐试验关系。结果:我们提取了与主要rsn相似的具有独特时空和光谱特征的快速动态大尺度脑状态。不同网络的参与显著影响皮质脊髓兴奋性,当基线活动由感觉运动网络主导时,运动诱发电位更大。结论:这些发现代表了在高空间和时间分辨率的EEG-TMS中表征脑网络的一步,并强调了将大规模网络动力学纳入TMS实验的重要性。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 求助全文
来源期刊
Brain Stimulation
Brain Stimulation 医学-临床神经学
CiteScore
13.10
自引率
9.10%
发文量
256
审稿时长
72 days
期刊介绍: Brain Stimulation publishes on the entire field of brain stimulation, including noninvasive and invasive techniques and technologies that alter brain function through the use of electrical, magnetic, radiowave, or focally targeted pharmacologic stimulation. Brain Stimulation aims to be the premier journal for publication of original research in the field of neuromodulation. The journal includes: a) Original articles; b) Short Communications; c) Invited and original reviews; d) Technology and methodological perspectives (reviews of new devices, description of new methods, etc.); and e) Letters to the Editor. Special issues of the journal will be considered based on scientific merit.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术官方微信