{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,23]],"date-time":"2026-10-23T01:28:27Z","timestamp":1792718907217,"version":"4.5.0"},"reference-count":63,"publisher":"Public Library of Science (PLoS)","issue":"3","license":[{"start":{"date-parts":[[2014,3,19]],"date-time":"2014-03-19T00:00:00Z","timestamp":1395187200000},"content-version":"unspecified","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"DOI":"10.1371\/journal.pone.0091065","type":"journal-article","created":{"date-parts":[[2014,3,19]],"date-time":"2014-03-19T22:45:49Z","timestamp":1395269149000},"page":"e91065","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":72,"title":["Suppression of Motor Cortical Excitability in Anesthetized Rats by Low Frequency Repetitive Transcranial Magnetic Stimulation"],"prefix":"10.1371","volume":"9","author":[{"given":"Paul A.","family":"Muller","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sameer C.","family":"Dhamne","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andrew M.","family":"Vahabzadeh-Hagh","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alvaro","family":"Pascual-Leone","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Frances E.","family":"Jensen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alexander","family":"Rotenberg","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2014,3,19]]},"reference":[{"key":"ref1","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1016\/S1474-4422(03)00321-1","article-title":"Transcranial magnetic stimulation in neurology","volume":"2","author":"M Kobayashi","year":"2003","journal-title":"Lancet Neurol"},{"key":"ref2","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":"ref3","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 Stimul"},{"key":"ref4","first-page":"437","article-title":"Effect of slow repetitive TMS of the motor cortex on ipsilateral sequential simple finger movements and motor skill learning","volume":"28","author":"M Kobayashi","year":"2010","journal-title":"Restor Neurol Neurosci"},{"key":"ref5","doi-asserted-by":"crossref","first-page":"381","DOI":"10.1007\/s11920-005-0041-4","article-title":"Transcranial magnetic stimulation for the treatment of depression in neurologic disorders","volume":"7","author":"F Fregni","year":"2005","journal-title":"Curr Psychiatry Rep"},{"key":"ref6","doi-asserted-by":"crossref","first-page":"472","DOI":"10.1100\/tsw.2006.98","article-title":"Novel therapeutic approaches to the treatment of chronic abdominal visceral pain","volume":"6","author":"F Patrizi","year":"2006","journal-title":"ScientificWorldJournal"},{"key":"ref7","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1016\/j.expneurol.2009.04.020","article-title":"Repetitive transcranial magnetic stimulation of the prefrontal cortex in depression","volume":"219","author":"F Padberg","year":"2009","journal-title":"Exp Neurol"},{"key":"ref8","doi-asserted-by":"crossref","first-page":"253","DOI":"10.1016\/j.yebeh.2008.09.007","article-title":"Repetitive transcranial magnetic stimulation in the treatment of epilepsia partialis continua","volume":"14","author":"A Rotenberg","year":"2009","journal-title":"Epilepsy Behav"},{"key":"ref9","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1007\/s11916-009-0004-2","article-title":"Noninvasive transcranial brain stimulation and pain","volume":"13","author":"AC Rosen","year":"2009","journal-title":"Curr Pain Headache Rep"},{"key":"ref10","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1007\/s10548-009-0116-3","article-title":"Prospects for clinical applications of transcranial magnetic stimulation and real-time EEG in epilepsy","volume":"22","author":"A Rotenberg","year":"2010","journal-title":"Brain Topogr"},{"key":"ref11","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1016\/0959-4388(91)90018-3","article-title":"Learning-related synaptic plasticity: LTP and LTD","volume":"1","author":"SA Siegelbaum","year":"1991","journal-title":"Curr Opin Neurobiol"},{"key":"ref12","doi-asserted-by":"crossref","first-page":"800","DOI":"10.1016\/S1388-2457(99)00323-5","article-title":"Modulation of corticospinal excitability by repetitive transcranial magnetic stimulation","volume":"111","author":"F Maeda","year":"2000","journal-title":"Clin Neurophysiol"},{"key":"ref13","doi-asserted-by":"crossref","first-page":"483","DOI":"10.1113\/jphysiol.2003.048777","article-title":"Shaping the excitability of human motor cortex with premotor rTMS","volume":"554","author":"V Rizzo","year":"2004","journal-title":"J Physiol"},{"key":"ref14","doi-asserted-by":"crossref","first-page":"1519","DOI":"10.1016\/j.clinph.2004.02.005","article-title":"Long-lasting increase in corticospinal excitability after 1800 pulses of subthreshold 5 Hz repetitive TMS to the primary motor cortex","volume":"115","author":"A Peinemann","year":"2004","journal-title":"Clin Neurophysiol"},{"key":"ref15","doi-asserted-by":"crossref","first-page":"86","DOI":"10.1016\/j.brainresbull.2005.11.003","article-title":"A direct demonstration of cortical LTP in humans: a combined TMS\/EEG study","volume":"69","author":"SK Esser","year":"2006","journal-title":"Brain Res Bull"},{"key":"ref16","doi-asserted-by":"crossref","first-page":"140","DOI":"10.1016\/j.clinph.2006.09.006","article-title":"Modulation of motor cortical excitability following rapid-rate transcranial magnetic stimulation","volume":"118","author":"EM Khedr","year":"2007","journal-title":"Clin Neurophysiol"},{"key":"ref17","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1007\/s00221-008-1356-2","article-title":"High- and low-frequency repetitive transcranial magnetic stimulation differentially activates c-Fos and zif268 protein expression in the rat brain","volume":"188","author":"S Aydin-Abidin","year":"2008","journal-title":"Exp Brain Res"},{"key":"ref18","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1016\/j.pneurobio.2010.10.003","article-title":"Modulation of cortical excitability induced by repetitive transcranial magnetic stimulation: influence of timing and geometrical parameters and underlying mechanisms","volume":"93","author":"GS Pell","year":"2011","journal-title":"Prog Neurobiol"},{"key":"ref19","doi-asserted-by":"crossref","first-page":"104","DOI":"10.1016\/j.clinph.2009.09.008","article-title":"Lateralization of forelimb motor evoked potentials by transcranial magnetic stimulation in rats","volume":"121","author":"A Rotenberg","year":"2010","journal-title":"Clin Neurophysiol"},{"key":"ref20","doi-asserted-by":"crossref","first-page":"615","DOI":"10.1152\/jn.00660.2010","article-title":"Measures of cortical inhibition by paired-pulse transcranial magnetic stimulation in anesthetized rats","volume":"105","author":"AM Vahabzadeh-Hagh","year":"2011","journal-title":"J Neurophysiol"},{"key":"ref21","doi-asserted-by":"crossref","first-page":"296","DOI":"10.1111\/j.1525-1403.2012.00482.x","article-title":"Translational neuromodulation: approximating human transcranial magnetic stimulation protocols in rats","volume":"15","author":"AM Vahabzadeh-Hagh","year":"2012","journal-title":"Neuromodulation"},{"key":"ref22","doi-asserted-by":"crossref","first-page":"2697","DOI":"10.1016\/j.clinph.2008.09.003","article-title":"Seizure suppression by EEG-guided repetitive transcranial magnetic stimulation in the rat","volume":"119","author":"A Rotenberg","year":"2008","journal-title":"Clin Neurophysiol"},{"key":"ref23","doi-asserted-by":"crossref","unstructured":"Muller PA, Pascual-Leone A, Rotenberg A (2012) Safety and tolerability of repetitive transcranial magnetic stimulation in patients with pathologic positive sensory phenomena: a review of literature. Brain Stimul 5: 320\u2013329 e327.","DOI":"10.1016\/j.brs.2011.05.003"},{"key":"ref24","doi-asserted-by":"crossref","first-page":"1782","DOI":"10.1111\/j.1528-1167.2012.03626.x","article-title":"Low-frequency repetitive transcranial magnetic stimulation for the treatment of refractory partial epilepsy: a controlled clinical study","volume":"53","author":"W Sun","year":"2012","journal-title":"Epilepsia"},{"key":"ref25","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1016\/0920-1211(90)90080-F","article-title":"The excitatory amino acid antagonist amino-phosphono-valeric acid (APV) provides protection against penicillin-induced epileptic activity in the rat","volume":"6","author":"C Loeb","year":"1990","journal-title":"Epilepsy Res"},{"key":"ref26","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1016\/S1059-1311(05)80146-3","article-title":"The antiepileptic effect of low-dose amino-phosphono-valeric acid (APV) is not enhanced by phosphatidylserine association","volume":"2","author":"C Loeb","year":"1993","journal-title":"Seizure"},{"key":"ref27","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/0165-3806(96)00023-5","article-title":"Effects of excitatory amino acids on the hypothalamic-pituitary-adrenal axis of the neonatal rat","volume":"94","author":"S Kent","year":"1996","journal-title":"Brain Res Dev Brain Res"},{"key":"ref28","doi-asserted-by":"crossref","first-page":"6057","DOI":"10.1523\/JNEUROSCI.17-16-06057.1997","article-title":"Glutamate-dependent activation of NF-kappaB during mouse cerebellum development","volume":"17","author":"L Guerrini","year":"1997","journal-title":"J Neurosci"},{"key":"ref29","doi-asserted-by":"crossref","first-page":"942","DOI":"10.1152\/japplphysiol.01274.2006","article-title":"Formation and maintenance of ventilatory long-term facilitation require NMDA but not non-NMDA receptors in awake rats","volume":"105","author":"M McGuire","year":"2008","journal-title":"J Appl Physiol (1985)"},{"key":"ref30","doi-asserted-by":"crossref","first-page":"780","DOI":"10.1002\/hipo.10124","article-title":"Long-term synaptic depression in the adult entorhinal cortex in vivo","volume":"13","author":"R Bouras","year":"2003","journal-title":"Hippocampus"},{"key":"ref31","doi-asserted-by":"crossref","first-page":"1347","DOI":"10.1016\/j.neuroscience.2009.09.022","article-title":"Neurodegeneration and prolonged immediate early gene expression throughout cortical areas of the rat brain following acute administration of dizocilpine","volume":"164","author":"S de Olmos","year":"2009","journal-title":"Neuroscience"},{"key":"ref32","doi-asserted-by":"crossref","first-page":"367","DOI":"10.1007\/s12264-009-0608-x","article-title":"NMDA receptor antagonist MK-801 reduces neuronal damage and preserves learning and memory in a rat model of traumatic brain injury","volume":"25","author":"RZ Han","year":"2009","journal-title":"Neurosci Bull"},{"key":"ref33","doi-asserted-by":"crossref","first-page":"441","DOI":"10.1203\/PDR.0b013e3181b337d2","article-title":"Epileptogenesis is increased in rats with neonatal isolation and early-life seizure and ameliorated by MK-801: a long-term MRI and histological study","volume":"66","author":"MC Lai","year":"2009","journal-title":"Pediatr Res"},{"key":"ref34","doi-asserted-by":"crossref","first-page":"719","DOI":"10.1016\/0031-9384(77)90304-3","article-title":"The variability of the interaural line vs the stability of bregma in rat stereotaxic surgery","volume":"19","author":"IQ Whishaw","year":"1977","journal-title":"Physiol Behav"},{"key":"ref35","doi-asserted-by":"crossref","first-page":"1398","DOI":"10.1212\/WNL.48.5.1398","article-title":"Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation","volume":"48","author":"R Chen","year":"1997","journal-title":"Neurology"},{"key":"ref36","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":"Clin Neurophysiol"},{"key":"ref37","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":"J Neurosci"},{"key":"ref38","doi-asserted-by":"crossref","first-page":"4423","DOI":"10.1113\/jphysiol.2011.206573","article-title":"Modulation of cortical inhibition by rTMS - findings obtained from animal models","volume":"589","author":"K Funke","year":"2011","journal-title":"J Physiol"},{"key":"ref39","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1007\/s12031-009-9311-7","article-title":"The restoration after repetitive transcranial magnetic stimulation treatment on cognitive ability of vascular dementia rats and its impacts on synaptic plasticity in hippocampal CA1 area","volume":"41","author":"F Wang","year":"2010","journal-title":"J Mol Neurosci"},{"key":"ref40","doi-asserted-by":"crossref","first-page":"2881","DOI":"10.1111\/j.0953-816X.2004.03390.x","article-title":"Frequency-dependent requirement for calcium store-operated mechanisms in induction of homosynaptic long-term depression at hippocampus CA1 synapses","volume":"19","author":"M Nakano","year":"2004","journal-title":"Eur J Neurosci"},{"key":"ref41","doi-asserted-by":"crossref","first-page":"1827","DOI":"10.1016\/S1388-2457(03)00181-0","article-title":"Suprathreshold 0.3 Hz repetitive TMS prolongs the cortical silent period: potential implications for therapeutic trials in epilepsy","volume":"114","author":"M Cincotta","year":"2003","journal-title":"Clin Neurophysiol"},{"key":"ref42","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":"Clin Neurophysiol"},{"key":"ref43","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1590\/S0004-282X2004000100004","article-title":"Experimental therapy of epilepsy with transcranial magnetic stimulation: lack of additional benefit with prolonged treatment","volume":"62","author":"JP Brasil-Neto","year":"2004","journal-title":"Arq Neuropsiquiatr"},{"key":"ref44","doi-asserted-by":"crossref","first-page":"398","DOI":"10.1016\/j.otohns.2007.11.035","article-title":"Repetitive transcranial magnetic stimulation in veterans with debilitating tinnitus: a pilot study","volume":"138","author":"SL Lee","year":"2008","journal-title":"Otolaryngol Head Neck Surg"},{"key":"ref45","doi-asserted-by":"crossref","first-page":"528","DOI":"10.1002\/mds.10109","article-title":"Therapeutic efficacy of bilateral prefrontal slow repetitive transcranial magnetic stimulation in depressed patients with Parkinson&apos;s disease: an open study","volume":"17","author":"N Dragasevic","year":"2002","journal-title":"Mov Disord"},{"key":"ref46","doi-asserted-by":"crossref","first-page":"619","DOI":"10.1007\/s10803-008-0662-7","article-title":"Effects of low frequency repetitive transcranial magnetic stimulation (rTMS) on gamma frequency oscillations and event-related potentials during processing of illusory figures in autism","volume":"39","author":"EM Sokhadze","year":"2009","journal-title":"J Autism Dev Disord"},{"key":"ref47","doi-asserted-by":"crossref","first-page":"699","DOI":"10.1113\/jphysiol.2002.023317","article-title":"Mechanisms of enhancement of human motor cortex excitability induced by interventional paired associative stimulation","volume":"543","author":"K Stefan","year":"2002","journal-title":"J Physiol"},{"key":"ref48","doi-asserted-by":"crossref","first-page":"6197","DOI":"10.1523\/JNEUROSCI.4673-09.2010","article-title":"L-type voltage-gated Ca2+ channels: a single molecular switch for long-term potentiation\/long-term depression-like plasticity and activity-dependent metaplasticity in humans","volume":"30","author":"K Wankerl","year":"2010","journal-title":"J Neurosci"},{"key":"ref49","doi-asserted-by":"crossref","first-page":"1525","DOI":"10.1097\/01.wnr.0000177005.14108.f1","article-title":"A study of the effects of lorazepam and dextromethorphan on the response to cortical 1 Hz repetitive transcranial magnetic stimulation","volume":"16","author":"PB Fitzgerald","year":"2005","journal-title":"Neuroreport"},{"key":"ref50","doi-asserted-by":"crossref","first-page":"3303","DOI":"10.1523\/JNEUROSCI.17-09-03303.1997","article-title":"Group 1 and 2 metabotropic glutamate receptors play differential roles in hippocampal long-term depression and long-term potentiation in freely moving rats","volume":"17","author":"D Manahan-Vaughan","year":"1997","journal-title":"J Neurosci"},{"key":"ref51","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1016\/j.brainres.2007.06.049","article-title":"Long-term depression induced by local tetanic stimulation in the rat auditory cortex","volume":"1166","author":"K Watanabe","year":"2007","journal-title":"Brain Res"},{"key":"ref52","doi-asserted-by":"crossref","first-page":"840374","DOI":"10.1155\/2008\/840374","article-title":"Postsynaptic signals mediating induction of long-term synaptic depression in the entorhinal cortex","volume":"2008","author":"S Kourrich","year":"2008","journal-title":"Neural Plast"},{"key":"ref53","doi-asserted-by":"crossref","first-page":"251","DOI":"10.1111\/j.1460-9568.2006.05274.x","article-title":"Low-frequency stimulation of the direct cortical input to area CA1 induces homosynaptic LTD and heterosynaptic LTP in the rat hippocampal-entorhinal cortex slice preparation","volume":"25","author":"R Wohrl","year":"2007","journal-title":"Eur J Neurosci"},{"key":"ref54","doi-asserted-by":"crossref","first-page":"744","DOI":"10.1038\/nn.2125","article-title":"Spike timing-dependent long-term depression requires presynaptic NMDA receptors","volume":"11","author":"A Rodriguez-Moreno","year":"2008","journal-title":"Nat Neurosci"},{"key":"ref55","doi-asserted-by":"crossref","first-page":"7521","DOI":"10.1523\/JNEUROSCI.6751-10.2011","article-title":"Long-term effects of repetitive transcranial magnetic stimulation on markers for neuroplasticity: differential outcomes in anesthetized and awake animals","volume":"31","author":"R Gersner","year":"2011","journal-title":"J Neurosci"},{"key":"ref56","doi-asserted-by":"crossref","first-page":"468","DOI":"10.1016\/j.yebeh.2012.07.026","article-title":"Possibly lifesaving, noninvasive, EEG-guided neuromodulation in anesthesia-refractory partial status epilepticus","volume":"25","author":"M Thordstein","year":"2012","journal-title":"Epilepsy Behav"},{"key":"ref57","doi-asserted-by":"crossref","first-page":"893","DOI":"10.1016\/j.seizure.2013.06.014","article-title":"Transcranial magnetic stimulation for refractory focal status epilepticus in the intensive care unit","volume":"22","author":"A Liu","year":"2013","journal-title":"Seizure"},{"key":"ref58","doi-asserted-by":"crossref","first-page":"395","DOI":"10.1016\/j.expneurol.2012.04.020","article-title":"Theta-burst stimulation and striatal plasticity in experimental parkinsonism","volume":"236","author":"V Ghiglieri","year":"2012","journal-title":"Exp Neurol"},{"key":"ref59","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1124\/pr.110.003020","article-title":"Remote control of neuronal signaling","volume":"63","author":"SC Rogan","year":"2011","journal-title":"Pharmacol Rev"},{"key":"ref60","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1016\/j.bbr.2013.02.037","article-title":"Development of transgenic animals for optogenetic manipulation of mammalian nervous system function: progress and prospects for behavioral neuroscience","volume":"255","author":"JT Ting","year":"2013","journal-title":"Behav Brain Res"},{"key":"ref61","doi-asserted-by":"crossref","first-page":"212","DOI":"10.1016\/j.neuroscience.2013.09.064","article-title":"Modulation of haloperidol-induced catalepsy in rats by GABAergic neural substrate in the inferior colliculus","volume":"255","author":"JG Tostes","year":"2013","journal-title":"Neuroscience"},{"key":"ref62","doi-asserted-by":"crossref","first-page":"238","DOI":"10.1016\/0168-5597(91)90077-B","article-title":"The measurement of electric field, and the influence of surface charge, in magnetic stimulation","volume":"81","author":"PS Tofts","year":"1991","journal-title":"Electroencephalogr Clin Neurophysiol"},{"key":"ref63","first-page":"1529","article-title":"Analysis of Electric Field in Real Rat Head Model during Transcranial Magnetic Stimulation","volume":"2","author":"J Zheng","year":"2005","journal-title":"Conf Proc IEEE Eng Med Biol Soc"}],"container-title":["PLoS ONE"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/dx.plos.org\/10.1371\/journal.pone.0091065","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,5,9]],"date-time":"2020-05-09T09:02:06Z","timestamp":1589014926000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0091065"}},"subtitle":[],"editor":[{"given":"Guglielmo","family":"Foffani","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2014,3,19]]},"references-count":63,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2014,3,19]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0091065","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2014,3,19]]}}}