{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,9]],"date-time":"2026-05-09T16:33:13Z","timestamp":1778344393954,"version":"3.51.4"},"update-to":[{"DOI":"10.1371\/journal.pcbi.1011027","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2023,11,27]],"date-time":"2023-11-27T00:00:00Z","timestamp":1701043200000}}],"reference-count":95,"publisher":"Public Library of Science (PLoS)","issue":"11","license":[{"start":{"date-parts":[[2023,11,13]],"date-time":"2023-11-13T00:00:00Z","timestamp":1699833600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"National Institute of Health","award":["1RO1NS109498"],"award-info":[{"award-number":["1RO1NS109498"]}]},{"DOI":"10.13039\/501100002347","name":"Bundesministerium f\u00fcr Bildung und Forschung","doi-asserted-by":"publisher","award":["01GQ2205A"],"award-info":[{"award-number":["01GQ2205A"]}],"id":[{"id":"10.13039\/501100002347","id-type":"DOI","asserted-by":"publisher"}]},{"name":"bwHPC and the German Research Foundation","award":["INST 39\/963-1"],"award-info":[{"award-number":["INST 39\/963-1"]}]}],"content-domain":{"domain":["www.ploscompbiol.org"],"crossmark-restriction":false},"short-container-title":["PLoS Comput Biol"],"abstract":"<jats:p>Repetitive transcranial magnetic stimulation (rTMS) is a non-invasive brain stimulation technique used to induce neuronal plasticity in healthy individuals and patients. Designing effective and reproducible rTMS protocols poses a major challenge in the field as the underlying biomechanisms of long-term effects remain elusive. Current clinical protocol designs are often based on studies reporting rTMS-induced long-term potentiation or depression of synaptic transmission. Herein, we employed computational modeling to explore the effects of rTMS on long-term structural plasticity and changes in network connectivity. We simulated a recurrent neuronal network with homeostatic structural plasticity among excitatory neurons, and demonstrated that this mechanism was sensitive to specific parameters of the stimulation protocol (i.e., frequency, intensity, and duration of stimulation). Particularly, the feedback-inhibition initiated by network stimulation influenced the net stimulation outcome and hindered the rTMS-induced structural reorganization, highlighting the role of inhibitory networks. These findings suggest a novel mechanism for the lasting effects of rTMS, i.e., rTMS-induced homeostatic structural plasticity, and highlight the importance of network inhibition in careful protocol design, standardization, and optimization of stimulation.<\/jats:p>","DOI":"10.1371\/journal.pcbi.1011027","type":"journal-article","created":{"date-parts":[[2023,11,13]],"date-time":"2023-11-13T13:46:12Z","timestamp":1699883172000},"page":"e1011027","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":26,"title":["Repetitive transcranial magnetic stimulation (rTMS) triggers dose-dependent homeostatic rewiring in recurrent neuronal networks"],"prefix":"10.1371","volume":"19","author":[{"ORCID":"https:\/\/orcid.org\/0009-0004-5976-1717","authenticated-orcid":true,"given":"Swathi","family":"Anil","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Han","family":"Lu","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3534-6530","authenticated-orcid":true,"given":"Stefan","family":"Rotter","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2646-3770","authenticated-orcid":true,"given":"Andreas","family":"Vlachos","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2023,11,13]]},"reference":[{"issue":"8437","key":"pcbi.1011027.ref001","doi-asserted-by":"crossref","first-page":"1106","DOI":"10.1016\/S0140-6736(85)92413-4","article-title":"Non-invasive magnetic stimulation of human motor cortex","volume":"1","author":"AT Barker","year":"1985","journal-title":"Lancet (London, England)"},{"issue":"2","key":"pcbi.1011027.ref002","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1016\/j.neuron.2007.06.026","article-title":"Transcranial magnetic stimulation: a primer","volume":"55","author":"M Hallett","year":"2007","journal-title":"Neuron"},{"key":"pcbi.1011027.ref003","doi-asserted-by":"crossref","first-page":"381","DOI":"10.1016\/j.neubiorev.2017.10.006","article-title":"Transcranial magnetic stimulation in basic and clinical neuroscience: A comprehensive review of fundamental principles and novel insights","volume":"83","author":"A Valero-Cabr\u00e9","year":"2017","journal-title":"Neuroscience & Biobehavioral Reviews"},{"issue":"1","key":"pcbi.1011027.ref004","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1097\/00004691-199101000-00005","article-title":"An introduction to the basic principles of magnetic nerve stimulation","volume":"8","author":"AT Barker","year":"1991","journal-title":"Journal of Clinical Neurophysiology"},{"issue":"2","key":"pcbi.1011027.ref005","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1016\/S0165-0270(97)02242-5","article-title":"Techniques and mechanisms of action of transcranial stimulation of the human motor cortex","volume":"74","author":"JC Rothwell","year":"1997","journal-title":"Journal of Neuroscience Methods"},{"issue":"4","key":"pcbi.1011027.ref006","doi-asserted-by":"crossref","first-page":"322","DOI":"10.1097\/00004691-200208000-00006","article-title":"Basic mechanisms of TMS","volume":"19","author":"Y Terao","year":"2002","journal-title":"Journal of Clinical Neurophysiology"},{"issue":"4","key":"pcbi.1011027.ref007","doi-asserted-by":"crossref","first-page":"333","DOI":"10.1097\/00004691-199807000-00005","article-title":"Study and modulation of human cortical excitability with transcranial magnetic stimulation","volume":"15","author":"A Pascual-Leone","year":"1998","journal-title":"Journal of clinical neurophysiology: official publication of the American Electroencephalographic Society"},{"issue":"6","key":"pcbi.1011027.ref008","doi-asserted-by":"crossref","first-page":"1002","DOI":"10.1016\/S1388-2457(00)00284-4","article-title":"Effects of low-frequency transcranial magnetic stimulation on motor excitability and basic motor behavior","volume":"111","author":"W Muellbacher","year":"2000","journal-title":"Clinical Neurophysiology"},{"issue":"3","key":"pcbi.1011027.ref009","doi-asserted-by":"crossref","first-page":"529","DOI":"10.1212\/WNL.52.3.529","article-title":"Low-frequency repetitive transcranial magnetic stimulation of the motor cortex in writer\u2019s cramp","volume":"52","author":"HR Siebner","year":"1999","journal-title":"Neurology"},{"issue":"4","key":"pcbi.1011027.ref010","doi-asserted-by":"crossref","first-page":"1593","DOI":"10.1096\/fj.11-194878","article-title":"Transcranial pulsed magnetic field stimulation facilitates reorganization of abnormal neural circuits and corrects behavioral deficits without disrupting normal connectivity","volume":"26","author":"J Rodger","year":"2012","journal-title":"FASEB journal: official publication of the Federation of American Societies for Experimental Biology"},{"issue":"32","key":"pcbi.1011027.ref011","doi-asserted-by":"crossref","first-page":"10780","DOI":"10.1523\/JNEUROSCI.0723-14.2014","article-title":"Low-intensity repetitive transcranial magnetic stimulation improves abnormal visual cortical circuit topography and upregulates BDNF in mice","volume":"34","author":"K Makowiecki","year":"2014","journal-title":"The Journal of Neuroscience"},{"issue":"48","key":"pcbi.1011027.ref012","doi-asserted-by":"crossref","first-page":"17514","DOI":"10.1523\/JNEUROSCI.0409-12.2012","article-title":"Repetitive magnetic stimulation induces functional and structural plasticity of excitatory postsynapses in mouse organotypic hippocampal slice cultures","volume":"32","author":"A Vlachos","year":"2012","journal-title":"The Journal of Neuroscience"},{"issue":"6","key":"pcbi.1011027.ref013","doi-asserted-by":"crossref","first-page":"3323","DOI":"10.1007\/s00429-014-0859-9","article-title":"Repetitive magnetic stimulation induces plasticity of excitatory postsynapses on proximal dendrites of cultured mouse CA1 pyramidal neurons","volume":"220","author":"M Lenz","year":"2015","journal-title":"Brain Structure & Function"},{"issue":"6","key":"pcbi.1011027.ref014","doi-asserted-by":"crossref","first-page":"1498","DOI":"10.1016\/j.brs.2021.10.001","article-title":"Subthreshold repetitive transcranial magnetic stimulation drives structural synaptic plasticity in the young and aged motor cortex","volume":"14","author":"AD Tang","year":"2021","journal-title":"Brain Stimulation"},{"issue":"4","key":"pcbi.1011027.ref015","doi-asserted-by":"crossref","first-page":"583","DOI":"10.1007\/s00221-007-0991-3","article-title":"Transcranial magnetic stimulation and synaptic plasticity: experimental framework and human models","volume":"180","author":"GW Thickbroom","year":"2007","journal-title":"Experimental Brain Research"},{"issue":"1","key":"pcbi.1011027.ref016","doi-asserted-by":"crossref","first-page":"10020","DOI":"10.1038\/ncomms10020","article-title":"Repetitive magnetic stimulation induces plasticity of inhibitory synapses","volume":"7","author":"M Lenz","year":"2016","journal-title":"Nature Communications"},{"key":"pcbi.1011027.ref017","doi-asserted-by":"crossref","first-page":"96","DOI":"10.3389\/fncir.2016.00096","article-title":"Releasing the cortical brake by non-invasive electromagnetic stimulation? rTMS induces LTD of GABAergic neurotransmission","volume":"10","author":"M Lenz","year":"2016","journal-title":"Frontiers in Neural Circuits"},{"issue":"12","key":"pcbi.1011027.ref018","doi-asserted-by":"crossref","first-page":"2584","DOI":"10.1016\/j.clinph.2006.06.712","article-title":"A comprehensive review of the effects of rTMS on motor cortical excitability and inhibition","volume":"117","author":"PB Fitzgerald","year":"2006","journal-title":"Clinical Neurophysiology"},{"issue":"4","key":"pcbi.1011027.ref019","doi-asserted-by":"crossref","first-page":"847","DOI":"10.1093\/brain\/117.4.847","article-title":"Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex","volume":"117","author":"A Pascual-Leone","year":"1994","journal-title":"Brain"},{"issue":"2","key":"pcbi.1011027.ref020","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1016\/S1388-2457(01)00726-X","article-title":"Intra- and interindividual variability of motor responses to repetitive transcranial magnetic stimulation","volume":"113","author":"M Sommer","year":"2002","journal-title":"Clinical Neurophysiology"},{"key":"pcbi.1011027.ref021","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1016\/j.cortex.2021.02.024","article-title":"Effects of rTMS on the brain: is there value in variability?","volume":"139","author":"MR Goldsworthy","year":"2021","journal-title":"Cortex"},{"issue":"10","key":"pcbi.1011027.ref022","doi-asserted-by":"crossref","first-page":"3404","DOI":"10.1111\/ejn.15195","article-title":"Selecting stimulation intensity in repetitive transcranial magnetic stimulation studies: A systematic review between 1991 and 2020","volume":"53","author":"Z Turi","year":"2021","journal-title":"European Journal of Neuroscience"},{"key":"pcbi.1011027.ref023","doi-asserted-by":"crossref","first-page":"639640","DOI":"10.3389\/fnhum.2021.639640","article-title":"Transcranial Magnetic Stimulation in Psychiatry: Is There a Need for Electric Field Standardization?","volume":"15","author":"Z Turi","year":"2021","journal-title":"Frontiers in Human Neuroscience"},{"key":"pcbi.1011027.ref024","doi-asserted-by":"crossref","first-page":"929814","DOI":"10.3389\/fnins.2022.929814","article-title":"Dosing Transcranial Magnetic Stimulation of the Primary Motor and Dorsolateral Prefrontal Cortices With Multi-Scale Modeling","volume":"16","author":"Z Turi","year":"2022","journal-title":"Frontiers in Neuroscience"},{"key":"pcbi.1011027.ref025","doi-asserted-by":"crossref","DOI":"10.3389\/fncir.2016.00026","article-title":"How Does Transcranial Magnetic Stimulation Influence Glial Cells in the Central Nervous System?","volume":"10","author":"CL Cullen","year":"2016","journal-title":"Frontiers in Neural Circuits"},{"issue":"7","key":"pcbi.1011027.ref026","doi-asserted-by":"crossref","first-page":"1035","DOI":"10.1002\/mds.26982","article-title":"Intermittent theta-burst stimulation rescues dopamine-dependent corticostriatal synaptic plasticity and motor behavior in experimental parkinsonism: Possible role of glial activity","volume":"32","author":"F Cacace","year":"2017","journal-title":"Movement Disorders"},{"issue":"1","key":"pcbi.1011027.ref027","doi-asserted-by":"crossref","first-page":"82","DOI":"10.1177\/1073858415618897","article-title":"Repetitive Transcranial Magnetic Stimulation of the Brain: Mechanisms from Animal and Experimental Models","volume":"23","author":"A Tang","year":"2017","journal-title":"The Neuroscientist"},{"key":"pcbi.1011027.ref028","article-title":"Microglia mediate synaptic plasticity induced by 10 Hz repetitive transcranial magnetic stimulation","author":"A Eichler","year":"2021","journal-title":"Journal of Neuroscience"},{"key":"pcbi.1011027.ref029","doi-asserted-by":"crossref","first-page":"256","DOI":"10.1016\/j.exger.2014.08.011","article-title":"Repetitive transcranial magnetic stimulation (rTMS) influences spatial cognition and modulates hippocampal structural synaptic plasticity in aging mice","volume":"58","author":"J Ma","year":"2014","journal-title":"Experimental Gerontology"},{"key":"pcbi.1011027.ref030","article-title":"High frequency repetitive transcranial magnetic stimulation alleviates cognitive impairment and modulates hippocampal synaptic structural plasticity in aged mice","volume":"11","author":"Q Ma","year":"2019","journal-title":"Frontiers in Aging Neuroscience"},{"issue":"5","key":"pcbi.1011027.ref031","doi-asserted-by":"crossref","first-page":"1096","DOI":"10.1038\/s41386-021-01256-3","article-title":"Large-scale structural network change correlates with clinical response to rTMS in depression","volume":"47","author":"SM Nestor","year":"2022","journal-title":"Neuropsychopharmacology"},{"key":"pcbi.1011027.ref032","doi-asserted-by":"crossref","DOI":"10.1017\/S2045796021000482","article-title":"Connectivity changes in major depressive disorder after rTMS: A review of functional and structural connectivity data","volume":"30","author":"G Schiena","year":"2021","journal-title":"Epidemiology and Psychiatric Sciences"},{"issue":"1","key":"pcbi.1011027.ref033","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1007\/s00406-020-01135-w","article-title":"Longitudinal effects of rTMS on neuroplasticity in chronic treatment-resistant depression","volume":"271","author":"I Dalhuisen","year":"2020","journal-title":"European Archives of Psychiatry and Clinical Neuroscience"},{"key":"pcbi.1011027.ref034","doi-asserted-by":"crossref","DOI":"10.3389\/fnsyn.2014.00007","article-title":"Homeostatic structural plasticity increases the efficiency of small-world networks","volume":"6","author":"M Butz","year":"2014","journal-title":"Frontiers in Synaptic Neuroscience"},{"issue":"1","key":"pcbi.1011027.ref035","doi-asserted-by":"crossref","first-page":"3754","DOI":"10.1038\/s41598-018-22077-3","article-title":"Associative properties of structural plasticity based on firing rate homeostasis in recurrent neuronal networks","volume":"8","author":"JV Gallinaro","year":"2018","journal-title":"Scientific Reports"},{"issue":"4","key":"pcbi.1011027.ref036","doi-asserted-by":"crossref","first-page":"924","DOI":"10.1162\/netn_a_00097","article-title":"Network remodeling induced by transcranial brain stimulation: A computational model of tDCS-triggered cell assembly formation","volume":"3","author":"H Lu","year":"2019","journal-title":"Network Neuroscience"},{"key":"pcbi.1011027.ref037","unstructured":"Fardet T, Vennemo SB, Mitchell J, M\u00f8rk H, Graber S, Hahne J, et al. NEST 2.20.0; 2020. Available from: https:\/\/doi.org\/10.5281\/zenodo.3605514."},{"issue":"3","key":"pcbi.1011027.ref038","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1023\/A:1008925309027","article-title":"Dynamics of Sparsely Connected Networks of Excitatory and Inhibitory Spiking Neurons","volume":"8","author":"N Brunel","year":"2000","journal-title":"Journal of Computational Neuroscience"},{"issue":"2","key":"pcbi.1011027.ref039","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1088\/0954-898X_6_2_001","article-title":"Rapid state switching in balanced cortical network models","volume":"6","author":"MV Tsodyks","year":"1995","journal-title":"Network: Computation in Neural Systems"},{"issue":"5293","key":"pcbi.1011027.ref040","doi-asserted-by":"crossref","first-page":"1724","DOI":"10.1126\/science.274.5293.1724","article-title":"Chaos in neuronal networks with balanced excitatory and inhibitory activity","volume":"274","author":"C van Vreeswijk","year":"1996","journal-title":"Science"},{"issue":"2","key":"pcbi.1011027.ref041","doi-asserted-by":"crossref","first-page":"e1009836","DOI":"10.1371\/journal.pcbi.1009836","article-title":"Homeostatic control of synaptic rewiring in recurrent networks induces the formation of stable memory engrams","volume":"18","author":"JV Gallinaro","year":"2022","journal-title":"PLOS Computational Biology"},{"issue":"4-5","key":"pcbi.1011027.ref042","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1007\/BF00318417","article-title":"Self-stabilization of neuronal networks: I. The compensation algorithm for synaptogenesis","volume":"54","author":"IE Dammasch","year":"1986","journal-title":"Biological Cybernetics"},{"issue":"1","key":"pcbi.1011027.ref043","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1006\/jtbi.1994.1047","article-title":"Activity-dependent Outgrowth of Neurons and Overshoot Phenomena in Developing Neural Networks","volume":"167","author":"A van Ooyen","year":"1994","journal-title":"Journal of Theoretical Biology"},{"issue":"1","key":"pcbi.1011027.ref044","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1006\/jtbi.1995.0005","article-title":"Implications of activity dependent neurite outgrowth for neuronal morphology and network development","volume":"172","author":"A Van Ooyen","year":"1995","journal-title":"Journal of Theoretical Biology"},{"key":"pcbi.1011027.ref045","doi-asserted-by":"crossref","DOI":"10.3389\/neuro.10.010.2009","article-title":"A model for cortical rewiring following deafferentation and focal stroke","volume":"3","author":"M Butz","year":"2009","journal-title":"Frontiers in Computational Neuroscience"},{"key":"pcbi.1011027.ref046","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1016\/B978-0-12-803784-3.00004-4","volume-title":"The Rewiring Brain","author":"M Butz-Ostendorf","year":"2017"},{"issue":"12","key":"pcbi.1011027.ref047","doi-asserted-by":"crossref","first-page":"e1001013","DOI":"10.1371\/journal.pcbi.1001013","article-title":"Self-Organized Criticality in Developing Neuronal Networks","volume":"6","author":"C Tetzlaff","year":"2010","journal-title":"PLoS Computational Biology"},{"issue":"10","key":"pcbi.1011027.ref048","doi-asserted-by":"crossref","first-page":"1490","DOI":"10.1016\/j.neunet.2006.07.007","article-title":"A theoretical network model to analyse neurogenesis and synaptogenesis in the dentate gyrus","volume":"19","author":"M Butz","year":"2006","journal-title":"Neural Networks"},{"issue":"9","key":"pcbi.1011027.ref049","doi-asserted-by":"crossref","first-page":"879","DOI":"10.1002\/hipo.20445","article-title":"Inverse relationship between adult hippocampal cell proliferation and synaptic rewiring in the dentate gyrus","volume":"18","author":"M Butz","year":"2008","journal-title":"Hippocampus"},{"key":"pcbi.1011027.ref050","doi-asserted-by":"crossref","DOI":"10.3389\/fnana.2016.00057","article-title":"Automatic Generation of Connectivity for Large-Scale Neuronal Network Models through Structural Plasticity","volume":"10","author":"S Diaz-Pier","year":"2016","journal-title":"Frontiers in Neuroanatomy"},{"issue":"5","key":"pcbi.1011027.ref051","doi-asserted-by":"crossref","first-page":"336","DOI":"10.1002\/sce.37303405110","article-title":"The organization of behavior: A neuropsychological theory. New York: John Wiley and Sons, Inc., 1949. 335 p. $4.00","volume":"34","author":"DO Hebb","year":"1950","journal-title":"Science Education"},{"issue":"1","key":"pcbi.1011027.ref052","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1146\/annurev.cellbio.23.090506.123221","article-title":"Calcium signaling in neuronal motility","volume":"23","author":"JQ Zheng","year":"2007","journal-title":"Annual Review of Cell and Developmental Biology"},{"issue":"12","key":"pcbi.1011027.ref053","doi-asserted-by":"crossref","first-page":"4034","DOI":"10.1523\/JNEUROSCI.07-12-04034.1987","article-title":"Calcium regulation of neurite elongation and growth cone motility","volume":"7","author":"M Mattson","year":"1987","journal-title":"The Journal of Neuroscience"},{"issue":"2","key":"pcbi.1011027.ref054","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1016\/S0165-3806(00)00148-6","article-title":"The role of calcium signaling in early axonal and dendritic morphogenesis of rat cerebral cortex neurons under non-stimulated growth conditions","volume":"126","author":"GJA Ramakers","year":"2001","journal-title":"Developmental Brain Research"},{"issue":"5","key":"pcbi.1011027.ref055","doi-asserted-by":"crossref","first-page":"399","DOI":"10.1038\/nmeth.1453","article-title":"High-speed in vivo calcium imaging reveals neuronal network activity with near-millisecond precision","volume":"7","author":"BF Grewe","year":"2010","journal-title":"Nature Methods"},{"issue":"1","key":"pcbi.1011027.ref056","doi-asserted-by":"crossref","DOI":"10.1038\/s41467-019-10638-7","article-title":"Neural effects of transcranial magnetic stimulation at the single-cell level","volume":"10","author":"MC Romero","year":"2019","journal-title":"Nature Communications"},{"key":"pcbi.1011027.ref057","doi-asserted-by":"crossref","DOI":"10.3389\/fncel.2014.00145","article-title":"Patch-clamp recordings of rat neurons from acute brain slices of the somatosensory cortex during magnetic stimulation","volume":"8","author":"T Pashut","year":"2014","journal-title":"Frontiers in Cellular Neuroscience"},{"key":"pcbi.1011027.ref058","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1186\/1743-0003-6-7","article-title":"Transcranial magnetic stimulation, synaptic plasticity and network oscillations","volume":"6","author":"PT Huerta","year":"2009","journal-title":"Journal of NeuroEngineering and Rehabilitation"},{"issue":"1","key":"pcbi.1011027.ref059","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1016\/j.brs.2021.11.010","article-title":"A visual and narrative timeline of US FDA milestones for transcranial magnetic stimulation (TMS) devices","volume":"15","author":"SL Cohen","year":"2022","journal-title":"Brain Stimulation: Basic, Translational, and Clinical Research in Neuromodulation"},{"issue":"2","key":"pcbi.1011027.ref060","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1016\/j.neuron.2004.12.033","article-title":"Theta Burst Stimulation of the Human Motor Cortex","volume":"45","author":"YZ Huang","year":"2005","journal-title":"Neuron"},{"issue":"6","key":"pcbi.1011027.ref061","doi-asserted-by":"crossref","first-page":"1470","DOI":"10.1016\/j.brs.2021.09.004","article-title":"Multi-scale modeling toolbox for single neuron and subcellular activity under Transcranial Magnetic Stimulation","volume":"14","author":"S Shirinpour","year":"2021","journal-title":"Brain Stimulation"},{"issue":"6","key":"pcbi.1011027.ref062","doi-asserted-by":"crossref","first-page":"066023","DOI":"10.1088\/1741-2552\/aadbb1","article-title":"Biophysically realistic neuron models for simulation of cortical stimulation","volume":"15","author":"AS Aberra","year":"2018","journal-title":"Journal of Neural Engineering"},{"issue":"1","key":"pcbi.1011027.ref063","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1016\/j.brs.2019.10.002","article-title":"Simulation of transcranial magnetic stimulation in head model with morphologically-realistic cortical neurons","volume":"13","author":"AS Aberra","year":"2020","journal-title":"Brain Stimulation"},{"key":"pcbi.1011027.ref064","first-page":"11","volume-title":"Cellular and Molecular Mechanisms of rTMS-induced Neural Plasticity","author":"M Lenz","year":"2016"},{"issue":"1","key":"pcbi.1011027.ref065","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1007\/s00702-021-02436-7","article-title":"Synaptic plasticity mechanisms behind TMS efficacy: insights from its application to animal models","volume":"129","author":"M Ferro","year":"2022","journal-title":"Journal of Neural Transmission (Vienna, Austria: 1996)"},{"key":"pcbi.1011027.ref066","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1016\/j.brainres.2014.10.034","article-title":"Theta-burst LTP","volume":"1621","author":"J Larson","year":"2015","journal-title":"Brain Research"},{"issue":"2","key":"pcbi.1011027.ref067","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1016\/j.brs.2009.10.005","article-title":"Physiology of repetitive transcranial magnetic stimulation of the human brain","volume":"3","author":"JM Hoogendam","year":"2010","journal-title":"Brain Stimulation"},{"key":"pcbi.1011027.ref068","doi-asserted-by":"crossref","DOI":"10.3389\/fneur.2020.599918","article-title":"How to Design Optimal Accelerated rTMS Protocols Capable of Promoting Therapeutically Beneficial Metaplasticity","volume":"11","author":"AC Thomson","year":"2020","journal-title":"Frontiers in Neurology"},{"key":"pcbi.1011027.ref069","volume-title":"No. 89 in Neuromethods","author":"A Rotenberg","year":"2014"},{"key":"pcbi.1011027.ref070","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1155\/2012\/350574","article-title":"Plasticity-Inducing TMS Protocols to Investigate Somatosensory Control of Hand Function","volume":"2012","author":"M Jacobs","year":"2012","journal-title":"Neural Plasticity"},{"issue":"2","key":"pcbi.1011027.ref071","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1016\/j.neuron.2013.08.018","article-title":"Synaptic Scaling and Homeostatic Plasticity in the Mouse Visual Cortex In\u00c2 Vivo","volume":"80","author":"T Keck","year":"2013","journal-title":"Neuron"},{"issue":"1","key":"pcbi.1011027.ref072","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1016\/j.neuron.2012.10.033","article-title":"Mossy Fiber-CA3 Synapses Mediate Homeostatic Plasticity in Mature Hippocampal Neurons","volume":"77","author":"K Lee","year":"2013","journal-title":"Neuron"},{"issue":"2","key":"pcbi.1011027.ref073","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1038\/nrn1327","article-title":"Homeostatic plasticity in the developing nervous system","volume":"5","author":"GG Turrigiano","year":"2004","journal-title":"Nature Reviews Neuroscience"},{"issue":"17","key":"pcbi.1011027.ref074","doi-asserted-by":"crossref","first-page":"8026","DOI":"10.1073\/pnas.92.17.8026","article-title":"Rapid acquisition of dendritic spines by visual thalamic neurons after blockade of N-methyl-D-aspartate receptors","volume":"92","author":"M Rocha","year":"1995","journal-title":"Proceedings of the National Academy of Sciences"},{"issue":"10","key":"pcbi.1011027.ref075","doi-asserted-by":"crossref","first-page":"878","DOI":"10.1038\/13178","article-title":"Dendrites are more spiny on mature hippocampal neurons when synapses are inactivated","volume":"2","author":"SA Kirov","year":"1999","journal-title":"Nature Neuroscience"},{"issue":"8","key":"pcbi.1011027.ref076","doi-asserted-by":"crossref","first-page":"1574","DOI":"10.1093\/cercor\/bhab281","article-title":"Time course of homeostatic structural plasticity in response to optogenetic stimulation in mouse anterior cingulate cortex","volume":"32","author":"H Lu","year":"2022","journal-title":"Cerebral Cortex"},{"key":"pcbi.1011027.ref077","doi-asserted-by":"crossref","DOI":"10.3389\/fnana.2016.00075","article-title":"Opposing Effects of Neuronal Activity on Structural Plasticity","volume":"10","author":"M Fauth","year":"2016","journal-title":"Frontiers in Neuroanatomy"},{"issue":"16","key":"pcbi.1011027.ref078","doi-asserted-by":"crossref","first-page":"4040","DOI":"10.1523\/JNEUROSCI.4115-04.2005","article-title":"Diminished Neuronal Activity Increases Neuron-Neuron Connectivity Underlying Silent Synapse Formation and the Rapid Conversion of Silent to Functional Synapses","volume":"25","author":"K Nakayama","year":"2005","journal-title":"Journal of Neuroscience"},{"issue":"7939","key":"pcbi.1011027.ref079","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1038\/s41586-022-05483-6","article-title":"Filopodia are a structural substrate for silent synapses in adult neocortex","volume":"612","author":"D Vardalaki","year":"2022","journal-title":"Nature"},{"issue":"9","key":"pcbi.1011027.ref080","doi-asserted-by":"crossref","first-page":"557","DOI":"10.1016\/j.tins.2018.07.002","article-title":"The Eloquent Silent Synapse","volume":"41","author":"P Vincent-Lamarre","year":"2018","journal-title":"Trends in Neurosciences"},{"issue":"11","key":"pcbi.1011027.ref081","doi-asserted-by":"crossref","first-page":"813","DOI":"10.1038\/nrn2501","article-title":"Silent synapses and the emergence of a postsynaptic mechanism for LTP","volume":"9","author":"GA Kerchner","year":"2008","journal-title":"Nature Reviews Neuroscience"},{"issue":"6530","key":"pcbi.1011027.ref082","doi-asserted-by":"crossref","first-page":"400","DOI":"10.1038\/375400a0","article-title":"Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice","volume":"375","author":"D Liao","year":"1995","journal-title":"Nature"},{"issue":"2","key":"pcbi.1011027.ref083","doi-asserted-by":"crossref","first-page":"427","DOI":"10.1016\/0896-6273(95)90046-2","article-title":"Evidence for silent synapses: Implications for the expression of LTP","volume":"15","author":"JTR Isaac","year":"1995","journal-title":"Neuron"},{"issue":"1","key":"pcbi.1011027.ref084","doi-asserted-by":"crossref","DOI":"10.1101\/cshperspect.a005736","article-title":"Homeostatic synaptic plasticity: Local and global mechanisms for stabilizing neuronal function","volume":"4","author":"G Turrigiano","year":"2011","journal-title":"Cold Spring Harbor Perspectives in Biology"},{"issue":"10","key":"pcbi.1011027.ref085","doi-asserted-by":"crossref","first-page":"656","DOI":"10.1016\/j.tins.2016.08.004","article-title":"Homeostatic Plasticity of Subcellular Neuronal Structures: From Inputs to Outputs","volume":"39","author":"W Wefelmeyer","year":"2016","journal-title":"Trends in Neurosciences"},{"key":"pcbi.1011027.ref086","article-title":"Structural homeostasis in the nervous system: A balancing act for wiring plasticity and stability","volume":"8","author":"J Yin","year":"2015","journal-title":"Frontiers in Cellular Neuroscience"},{"key":"pcbi.1011027.ref087","doi-asserted-by":"crossref","first-page":"e13598","DOI":"10.7554\/eLife.13598","article-title":"Transcranial magnetic stimulation (TMS) inhibits cortical dendrites","volume":"5","author":"SC Murphy","year":"2016","journal-title":"eLife"},{"issue":"37","key":"pcbi.1011027.ref088","doi-asserted-by":"crossref","first-page":"13553","DOI":"10.1073\/pnas.1405508111","article-title":"Voltage-sensitive dye imaging of transcranial magnetic stimulation-induced intracortical dynamics","volume":"111","author":"V Kozyrev","year":"2014","journal-title":"Proceedings of the National Academy of Sciences of the United States of America"},{"issue":"25","key":"pcbi.1011027.ref089","doi-asserted-by":"crossref","first-page":"6476","DOI":"10.1073\/pnas.1802798115","article-title":"TMS-induced neuronal plasticity enables targeted remodeling of visual cortical maps","volume":"115","author":"V Kozyrev","year":"2018","journal-title":"Proceedings of the National Academy of Sciences"},{"issue":"4","key":"pcbi.1011027.ref090","doi-asserted-by":"crossref","first-page":"399","DOI":"10.3233\/RNN-2010-0566","article-title":"Cortical cellular actions of transcranial magnetic stimulation","volume":"28","author":"K Funke","year":"2010","journal-title":"Restorative Neurology and Neuroscience"},{"issue":"18","key":"pcbi.1011027.ref091","doi-asserted-by":"crossref","first-page":"4423","DOI":"10.1113\/jphysiol.2011.206573","article-title":"Modulation of cortical inhibition by rTMS\u2014findings obtained from animal models","volume":"589","author":"K Funke","year":"2011","journal-title":"The Journal of Physiology"},{"issue":"4","key":"pcbi.1011027.ref092","doi-asserted-by":"crossref","first-page":"1193","DOI":"10.1523\/JNEUROSCI.1379-10.2011","article-title":"Theta-Burst Transcranial Magnetic Stimulation Alters Cortical Inhibition","volume":"31","author":"A Benali","year":"2011","journal-title":"Journal of Neuroscience"},{"issue":"11","key":"pcbi.1011027.ref093","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pcbi.1010568","article-title":"Synaptic reshaping of plastic neuronal networks by periodic multichannel stimulation with single-pulse and burst stimuli","volume":"18","author":"JA Kromer","year":"2022","journal-title":"PLOS Computational Biology"},{"key":"pcbi.1011027.ref094","article-title":"Interplay between homeostatic synaptic scaling and homeostatic structural plasticity maintains the robust firing rate of neural networks","author":"H Lu","year":"2023","journal-title":"bioRxiv"},{"key":"pcbi.1011027.ref095","doi-asserted-by":"crossref","DOI":"10.3389\/fphys.2021.716556","article-title":"Long-term desynchronization by coordinated reset stimulation in a neural network model with synaptic and structural plasticity","volume":"12","author":"T Manos","year":"2021","journal-title":"Frontiers in Physiology"}],"updated-by":[{"DOI":"10.1371\/journal.pcbi.1011027","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2023,11,27]],"date-time":"2023-11-27T00:00:00Z","timestamp":1701043200000}}],"container-title":["PLOS Computational Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1011027","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,12,25]],"date-time":"2023-12-25T14:08:23Z","timestamp":1703513303000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1011027"}},"subtitle":[],"editor":[{"given":"Boris S.","family":"Gutkin","sequence":"first","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2023,11,13]]},"references-count":95,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2023,11,13]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pcbi.1011027","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2023.03.20.533396","asserted-by":"object"}]},"ISSN":["1553-7358"],"issn-type":[{"value":"1553-7358","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,11,13]]}}}