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The application and prospect of combined functional magnetic resonance imaging and transcranial magnetic stimulation on the modulation of brain functional network
XIA Qingling  JIANG Bin  LIU Daihong  ZHU Xiuhong  QIU Jing  ZHANG Jiuquan 

Cite this article as: Xia QL, Jiang B, Liu DH, et al. The application and prospect of combined functional magnetic resonance imaging and transcranial magnetic stimulation on the modulation of brain functional network[J]. Chin J Magn Reson Imaging, 2022, 13(8): 117-120, 129. DOI:10.12015/issn.1674-8034.2022.08.026.


[Abstract] Transcranial magnetic stimulation (TMS) is a non-invasive neuromodulation technique based on Faraday's principle of electromagnetic induction. With the advantages of non-invasive, safe, and well-tolerated, TMS has made great progress in the clinical application of neurological psychiatric, and psychiatric disorders. However, it remains to be explored in the fields of the selection and localization of the stimulation target, the effects of TMS on the brain network functional connectivity, and how the brain network status affects the clinical outcome of TMS. Blood oxygen level-dependent functional magnetic resonance imaging (fMRI) can detect brain activity in the deep brain area with high spatial resolution, non-invasiveness, and no radiation. With such advantages of fMRI, the combination of fMRI and TMS (fMRI-TMS) has been increasingly put into clinical application and neuroscience research. This paper reviews the research of fMRI-TMS in the precise and personalized localization of TMS targets and its influence on the brain network. It also introduces the limitations and prospects of fMRI-TMS in brief.
[Keywords] transcranial magnetic stimulation;localization;functional connectivity;brain network;functional magnetic resonance imaging

XIA Qingling1, 2*   JIANG Bin1   LIU Daihong2   ZHU Xiuhong1   QIU Jing1   ZHANG Jiuquan2*  

1 School of Artificial Intelligence, Chongqing University of Technology, Chongqing, 401135, China

2 Department of Radiology, Chongqing University Cancer Hospital, Chongqing, 400030, China

Xia QL, E-mail: qingling@cqut.edu.cn Zhang JQ, E-mail: zhangjq_radiol@foxmail.com

Conflicts of interest   None.

Received  2022-01-31
Accepted  2022-08-05
DOI: 10.12015/issn.1674-8034.2022.08.026
Cite this article as: Xia QL, Jiang B, Liu DH, et al. The application and prospect of combined functional magnetic resonance imaging and transcranial magnetic stimulation on the modulation of brain functional network[J]. Chin J Magn Reson Imaging, 2022, 13(8): 117-120, 129.DOI:10.12015/issn.1674-8034.2022.08.026

[1]
Lefaucheur JP, Aleman A, Baeken C, et al. Evidence-based guidelines on the therapeutic use of repetitive transcranial magnetic stimulation (rTMS): An update (2014-2018)[J]. Clin Neurophysiol, 2020, 131(2): 474-528. DOI: 10.1016/j.clinph.2019.11.002.
[2]
Cohen SL, Bikson M, Badran BW, et al. A visual and narrative timeline of US FDA milestones for Transcranial Magnetic Stimulation (TMS) devices[J]. Brain Stimul, 2021, 15(1): 73-75. DOI: 10.1016/j.brs.2021.11.010.
[3]
Buchbinder BR. Functional magnetic resonance imaging[J]. Handb Clin Neurol, 2016, 135: 61-92. DOI: 10.1016/B978-0-444-53485-9.00004-0.
[4]
Navarro De Lara LI, Tik M, Woletz M, et al. High-sensitivity TMS/fMRI of the Human Motor Cortex Using a Dedicated Multichannel MR Coil[J]. Neuroimage, 2017, 150: 262-269. DOI: 10.1016/j.neuroimage.2017.02.062.
[5]
Jung J, Bungert A, Bowtell R, et al. Modulating Brain Networks With Transcranial Magnetic Stimulation Over the Primary Motor Cortex: A Concurrent TMS/fMRI Study[J/OL]. Front Hum Neurosci, 2020, 14 [2022-01-31]. https://www.frontiersin.org/articles/10.3389/fnhum.2020.00031. DOI: 10.3389/fnhum.2020.00031.
[6]
Neacsiu AD, Luber BM, Davis SW, et al. On the Concurrent Use of Self-System Therapy and Functional Magnetic Resonance Imaging-Guided Transcranial Magnetic Stimulation as Treatment for Depression[J]. J ECT, 2018, 34(4): 266-273. DOI: 10.1097/YCT.0000000000000545.
[7]
Mathieu W, Popovich M, Farivar R. Radio-Frequency Coil Array for Improved Concurrent Transcranial Magnetic Stimulation and Functional Magnetic Resonance Imaging[J]. Annu Int Conf IEEE Eng Med Biol Soc, 2019, 2019: 6814-6817. DOI: 10.1109/EMBC.2019.8857215.
[8]
Hawco C, Voineskos AN, Steeves JKE, et al. Spread of activity following TMS is related to intrinsic resting connectivity to the salience network: A concurrent TMS-fMRI study[J]. Cortex, 2018, 108: 160-172. DOI: 10.1016/j.cortex.2018.07.010.
[9]
Jung J, Bungert A, Bowtell R, et al. Vertex Stimulation as a Control Site for Transcranial Magnetic Stimulation: A Concurrent TMS/fMRI Study[J]. Brain Stimul, 2016, 9(1): 58-64. DOI: 10.1016/j.brs.2015.09.008.
[10]
Ma YQ, Xie RX, Zheng Z, et al. Application and Progress of Real-time Interleaved Transcranial Magnetic Stimulation Functional Magnetic Resonance Imaging[J]. Journal of Sichuan University (Medical Science Edition), 2020, 51(5): 592-598. DOI: 10.12182/20200960202.
[11]
Zheng Y, Zhang Z, Yang B, et al. Can individualized targets for transcranial magnetic stimulation increase treatment effectiveness in psychiatric disorders? A systematic review and meta-analysis[J/OL]. medRxiv, 2021 [2022-01-31]. https://www.medrxiv.org/content/10.1101/2021.10.14.21265029v1. DOI: 10.1101/2021.10.14.21265029.
[12]
George MS, Wassermann EM, Williams WA, et al. Daily repetitive transcranial magnetic stimulation (rTMS) improves mood in depression[J]. NeuroReport, 1995, 6(14): 1853-1856. DOI: 10.1097/00001756-199510020-00008.
[13]
Pascual-Leone A, Rubio B, Pallardó F, et al. Rapid-rate transcranial magnetic stimulation of left dorsolateral prefrontal cortex in drug-resistant depression[J]. Lancet, 1996, 348(9022): 233-237. DOI: 10.1016/s0140-6736(96)01219-6.
[14]
Herwig U, Padberg F, Unger J, et al. Transcranial magnetic stimulation in therapy studies: examination of the reliability of "standard" coil positioning by neuronavigation[J]. Biological Psychiatry, 2001, 50(1): 58-61. DOI: 10.1016/s0006-3223(01)01153-2.
[15]
Herwig U, Satrapi P, Schönfeldt-Lecuona C. Using the international 10-20 EEG system for positioning of transcranial magnetic stimulation[J]. Brain Topogr, 2003, 16(2): 95-99. DOI: 10.1023/b:brat.0000006333.93597.9d.
[16]
Beam W, Borckardt JJ, Reeves ST, et al. An efficient and accurate new method for locating the F3 position for prefrontal TMS applications[J]. Brain Stimul, 2009, 2(1): 50-54. DOI: 10.1016/j.brs.2008.09.006.
[17]
Mir-Moghtadaei A, Caballero R, Fried P, et al. Concordance Between BeamF3 and MRI-neuronavigated Target Sites for Repetitive Transcranial Magnetic Stimulation of the Left Dorsolateral Prefrontal Cortex[J]. Brain Stimul, 2015, 8(5): 965-973. DOI: 10.1016/j.brs.2015.05.008.
[18]
Rusjan PM, Barr MS, Farzan F, et al. Optimal transcranial magnetic stimulation coil placement for targeting the dorsolateral prefrontal cortex using novel magnetic resonance image-guided neuronavigation[J]. Hum Brain Mapp, 2010, 31(11): 1643-1652. DOI: 10.1002/hbm.20964.
[19]
Fitzgerald PB, Maller JJ, Hoy KE, et al. Exploring the optimal site for the localization of dorsolateral prefrontal cortex in brain stimulation experiments[J]. Brain Stimul, 2009, 2(4): 234-237. DOI: 10.1016/j.brs.2009.03.002.
[20]
Krieg SM. Navigated transcranial magnetic stimulation in Neurosurgery[M]. Cham: Springer, 2017. DOI: 10.1007/978-3-319-54918-7.
[21]
Cash RFH, Weigand A, Zalesky A, et al. Using Brain Imaging to Improve Spatial Targeting of Transcranial Magnetic Stimulation for Depression[J]. Biol Psychiatry, 2021, 90(10): 689-700. DOI: 10.1016/j.biopsych.2020.05.033.
[22]
Blumberger DM, Maller JJ, Thomson L, et al. Unilateral and bilateral MRI-targeted repetitive transcranial magnetic stimulation for treatment-resistant depression: a randomized controlled study[J/OL]. J Psychiatry Neurosci, 2016, 41(4) [2022-01-31]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4915938/. DOI: 10.1503/jpn.150265.
[23]
Zhang Z, Zhang H, Xie CM, et al. Task-related functional magnetic resonance imaging-based neuronavigation for the treatment of depression by individualized repetitive transcranial magnetic stimulation of the visual cortex[J]. Sci China Life Sci, 2021, 64(1): 96-106. DOI: 10.1007/s11427-020-1730-5.
[24]
Cash RFH, Zalesky A, Thomson RH, et al. Subgenual Functional Connectivity Predicts Antidepressant Treatment Response to Transcranial Magnetic Stimulation: Independent Validation and Evaluation of Personalization[J/OL]. Biol Psychiatry, 2019, 86(2) [2022-01-31]. https://www.biologicalpsychiatryjournal.com/article/S0006-3223(18)32059-6/fulltext. DOI: 10.1016/j.biopsych.2018.12.002.
[25]
Weigand A, Horn A, Caballero R, et al. Prospective Validation That Subgenual Connectivity Predicts Antidepressant Efficacy of Transcranial Magnetic Stimulation Sites[J]. Biol Psychiatry, 2018, 84(1): 28-37. DOI: 10.1016/j.biopsych.2017.10.028.
[26]
Fox MD, Buckner RL, White MP, et al. Efficacy of transcranial magnetic stimulation targets for depression is related to intrinsic functional connectivity with the subgenual cingulate[J]. Biol Psychiatry, 2012, 72(7): 595-603. DOI: 10.1016/j.biopsych.2012.04.028.
[27]
Siddiqi SH, Trapp NT, Hacker CD, et al. Repetitive Transcranial Magnetic Stimulation with Resting-State Network Targeting for Treatment-Resistant Depression in Traumatic Brain Injury: A Randomized, Controlled, Double-Blinded Pilot Study[J]. J Neurotrauma, 2019, 36(8): 1361-1374. DOI: 10.1089/neu.2018.5889.
[28]
Cole EJ, Stimpson KH, Bentzley BS, et al. Stanford Accelerated Intelligent Neuromodulation Therapy for Treatment-Resistant Depression[J]. Am J Psychiatry, 2020, 177(8): 716-726. DOI: 10.1176/appi.ajp.2019.19070720.
[29]
Tang N, Sun C, Wang Y, et al. Clinical Response of Major Depressive Disorder Patients With Suicidal Ideation to Individual Target-Transcranial Magnetic Stimulation[J/OL]. Front Psychiatry, 2021, 12 [2022-01-31]. https://www.frontiersin.org/articles/10.3389/fpsyt.2021.768819/full. DOI: 10.3389/fpsyt.2021.768819.
[30]
Zheng KY, Dai GY, Lan Y, et al. Trends of Repetitive Transcranial Magnetic Stimulation From 2009 to 2018: A Bibliometric Analysis[J]. Front Neurosci, 2020, 14: 106. DOI: 10.3389/fnins.2020.00106.
[31]
Miron JP, Jodoin VD, Lesperance P, et al. Repetitive transcranial magnetic stimulation for major depressive disorder: basic principles and future directions[J/OL]. Ther Adv Psychopharmacol, 2021, 11 [2022-01-31]. https://journals.sagepub.com/doi/10.1177/20451253211042696. DOI: 10.1177/20451253211042696.
[32]
Zhong G, Yang Z, Jiang T. Precise Modulation Strategies for Transcranial Magnetic Stimulation: Advances and Future Directions[J]. Neurosci Bull, 2021, 37(12): 1718-1734. DOI: 10.1007/s12264-021-00781-x.
[33]
Bestmann S, Baudewig J, Siebner HR, et al. Functional MRI of the immediate impact of transcranial magnetic stimulation on cortical and subcortical motor circuits[J]. Eur J Neurosci, 2004, 19(7): 1950-1962. DOI: 10.1111/j.1460-9568.2004.03277.x.
[34]
Guan M, Wang Z, Shi Y, et al. Altered Brain Function and Causal Connectivity Induced by Repetitive Transcranial Magnetic Stimulation Treatment for Major Depressive Disorder[J/OL]. Front Neurosci, 2022, 16 [2022-01-31]. https://www.frontiersin.org/articles/10.3389/fnins.2022.855483/full. DOI: 10.3389/fnins.2022.855483.
[35]
Li Y, Li K, Feng R, et al. Mechanisms of Repetitive Transcranial Magnetic Stimulation on Post-stroke Depression: A Resting-State Functional Magnetic Resonance Imaging Study[J]. Brain Topogr, 2022, 35(3): 363-374. DOI: 10.1007/s10548-022-00894-0.
[36]
Fox MD, Halko MA, Eldaief MC, et al. Measuring and manipulating brain connectivity with resting state functional connectivity magnetic resonance imaging (fcMRI) and transcranial magnetic stimulation (TMS)[J]. Neuroimage, 2012, 62(4): 2232-2243. DOI: 10.1016/j.neuroimage.2012.03.035.
[37]
Liston C, Chen AC, Zebley BD, et al. Default mode network mechanisms of transcranial magnetic stimulation in depression[J]. Biol Psychiatry, 2014, 76(7): 517-526. DOI: 10.1016/j.biopsych.2014.01.023.
[38]
Oathes DJ, Zimmerman JP, Duprat R, et al. Resting fMRI-guided TMS results in subcortical and brain network modulation indexed by interleaved TMS/fMRI[J]. Exp Brain Res, 2021, 239(4): 1165-1178. DOI: 10.1007/s00221-021-06036-5.
[39]
Tik M, Woletz M, Schuler AL, et al. TMS/fMRI demonstrates sgACC target engagement[J/OL]. Clinical Neurophysiology, 2020, 131(4) [2022-01-31]. https://linkinghub.elsevier.com/retrieve/pii/S1388245719315111. DOI: 10.1016/j.clinph.2019.12.145.
[40]
Wang JX, Rogers LM, Gross EZ, et al. Targeted enhancement of cortical-hippocampal brain networks and associative memory[J]. Science, 2014, 345(6200): 1054-1057. DOI: 10.1126/science.1252900.
[41]
Beynel L, Powers JP, Appelbaum LG. Effects of repetitive transcranial magnetic stimulation on resting-state connectivity: A systematic review[J/OL]. Neuroimage, 2020, 211 [2022-01-31]. https://linkinghub.elsevier.com/retrieve/pii/S1053811920300835. DOI: 10.1016/j.neuroimage.2020.116596.
[42]
Philip NS, Barredo J, Van'T Wout-Frank M, et al. Network Mechanisms of Clinical Response to Transcranial Magnetic Stimulation in Posttraumatic Stress Disorder and Major Depressive Disorder[J]. Biol Psychiatry, 2018, 83(3): 263-272. DOI: 10.1016/j.biopsych.2017.07.021.
[43]
Ge R, Humaira A, Gregory E, et al. Predictive Value of Acute Neuroplastic Response to rTMS in Treatment Outcome in Depression: A Concurrent TMS-fMRI Trial[J]. Am J Psychiatry, 2022, 179(7): 500-508. DOI: 10.1176/appi.ajp.21050541.
[44]
Chen AC, Oathes DJ, Chang C, et al. Causal interactions between fronto-parietal central executive and default-mode networks in humans[J]. Proc Natl Acad Sci U S A, 2013, 110(49): 19944-19949. DOI: 10.1073/pnas.1311772110.
[45]
Zhang H, Sollmann N, Castrillon G, et al. Intranetwork and Internetwork Effects of Navigated Transcranial Magnetic Stimulation Using Low- and High-Frequency Pulse Application to the Dorsolateral Prefrontal Cortex: A Combined rTMS-fMRI Approach[J]. J Clin Neurophysiol, 2020, 37(2): 131-139. DOI: 10.1097/WNP.0000000000000528.
[46]
Broyd SJ, Demanuele C, Debener S, et al. Default-mode brain dysfunction in mental disorders: a systematic review[J]. Neuroscience & biobehavioral reviews, 2009, 33(3): 279-296. DOI: 10.1016/j.neubiorev.2008.09.002.
[47]
Kaiser RH, Andrews-Hanna JR, Wager TD, et al. Large-Scale Network Dysfunction in Major Depressive Disorder: A Meta-analysis of Resting-State Functional Connectivity[J]. JAMA Psychiatry, 2015, 72(6): 603-611. DOI: 10.1001/jamapsychiatry.2015.0071.
[48]
Eshel N, Keller CJ, Wu W, et al. Global connectivity and local excitability changes underlie antidepressant effects of repetitive transcranial magnetic stimulation[J]. Neuropsychopharmacology, 2020, 45(6): 1018-1025. DOI: 10.1038/s41386-020-0633-z.
[49]
Hanlon CA, Dowdle LT, Moss H, et al. Mobilization of Medial and Lateral Frontal-Striatal Circuits in Cocaine Users and Controls: An Interleaved TMS/BOLD Functional Connectivity Study[J]. Neuropsychopharmacology, 2016, 41(13): 3032-3041. DOI: 10.1038/npp.2016.114.
[50]
Jin L, Yuan M, Zhang W, et al. Repetitive transcranial magnetic stimulation modulates coupling among large-scale brain networks in heroin-dependent individuals: A randomized resting-state functional magnetic resonance imaging study[J/OL]. Addict Biol, 2022, 27(2) [2022-01-31]. https://onlinelibrary.wiley.com/doi/10.1111/adb.13121. DOI: 10.1111/adb.13121.
[51]
Mantovani A, Neri F, D'urso G, et al. Functional connectivity changes and symptoms improvement after personalized, double-daily dosing, repetitive transcranial magnetic stimulation in obsessive-compulsive disorder: A pilot study[J]. J Psychiatr Res, 2021, 136: 560-570. DOI: 10.1016/j.jpsychires.2020.10.030.
[52]
Ruff CC, Blankenburg F, Bjoertomt O, et al. Concurrent TMS-fMRI and psychophysics reveal frontal influences on human retinotopic visual cortex[J]. Curr Biol, 2006, 16(15): 1479-1488. DOI: 10.1016/j.cub.2006.06.057.
[53]
Li M, Dahmani L, Wang D, et al. Co-activation patterns across multiple tasks reveal robust anti-correlated functional networks[J/OL]. Neuroimage, 2021, 227 [2022-01-31]. https://linkinghub.elsevier.com/retrieve/pii/S1053811920311654. DOI: 10.1016/j.neuroimage.2020.117680.
[54]
Avissar M, Powell F, Ilieva I, et al. Functional connectivity of the left DLPFC to striatum predicts treatment response of depression to TMS[J]. Brain Stimul, 2017, 10(5): 919-925. DOI: 10.1016/j.brs.2017.07.002.
[55]
Iwabuchi SJ, Auer DP, Lankappa ST, et al. Baseline effective connectivity predicts response to repetitive transcranial magnetic stimulation in patients with treatment-resistant depression[J]. Eur Neuropsychopharmacol, 2019, 29(5): 681-690. DOI: 10.1016/j.euroneuro.2019.02.012.

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