{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,2,26]],"date-time":"2025-02-26T08:40:19Z","timestamp":1740559219103,"version":"3.38.0"},"reference-count":39,"publisher":"Springer Science and Business Media LLC","issue":"2","license":[{"start":{"date-parts":[[2025,1,22]],"date-time":"2025-01-22T00:00:00Z","timestamp":1737504000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.springernature.com\/gp\/researchers\/text-and-data-mining"},{"start":{"date-parts":[[2025,1,22]],"date-time":"2025-01-22T00:00:00Z","timestamp":1737504000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/www.springernature.com\/gp\/researchers\/text-and-data-mining"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Exp Brain Res"],"published-print":{"date-parts":[[2025,2]]},"DOI":"10.1007\/s00221-024-06961-1","type":"journal-article","created":{"date-parts":[[2025,1,22]],"date-time":"2025-01-22T16:19:53Z","timestamp":1737562793000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Revisiting motor unit recruitment to TMS in amyotrophic lateral sclerosis: cortical inhibition is retained during voluntary contractions"],"prefix":"10.1007","volume":"243","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-7948-3599","authenticated-orcid":false,"given":"Blair","family":"Calancie","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Natalia","family":"Alexeeva","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2025,1,22]]},"reference":[{"key":"6961_CR1","doi-asserted-by":"publisher","first-page":"50","DOI":"10.1179\/2045772314Y.0000000279","volume":"39","author":"N Alexeeva","year":"2016","unstructured":"Alexeeva N, Calancie B (2016) Efficacy of QuadroPulse rTMS for improving motor function after spinal cord injury: three case studies. J Spinal Cord Med 39:50\u201357","journal-title":"J Spinal Cord Med"},{"key":"6961_CR2","doi-asserted-by":"publisher","first-page":"677","DOI":"10.1002\/mus.20519","volume":"33","author":"S Attarian","year":"2006","unstructured":"Attarian S, Vedel JP, Pouget J, Schmied A (2006) Cortical versus spinal dysfunction in amyotrophic lateral sclerosis. Muscle Nerve 33:677\u2013690. https:\/\/doi.org\/10.1002\/mus.20519","journal-title":"Muscle Nerve"},{"key":"6961_CR3","doi-asserted-by":"publisher","first-page":"310","DOI":"10.1002\/mus.21137","volume":"39","author":"S Attarian","year":"2009","unstructured":"Attarian S, Pouget J, Schmied A (2009) Changes in cortically induced inhibition in amyotrophic lateral sclerosis with time. Muscle Nerve 39:310\u2013317. https:\/\/doi.org\/10.1002\/mus.21137","journal-title":"Muscle Nerve"},{"key":"6961_CR4","doi-asserted-by":"publisher","first-page":"408","DOI":"10.1016\/0168-5597(93)90114-5","volume":"89","author":"F Awiszus","year":"1993","unstructured":"Awiszus F, Feistner H (1993) Abnormal EPSPs evoked by magnetic brain stimulation in hand muscle motoneurons of patients with amyotrophic lateral sclerosis. Electroencephalogr Clin Neurophysiol 89:408\u2013414. https:\/\/doi.org\/10.1016\/0168-5597(93)90114-5","journal-title":"Electroencephalogr Clin Neurophysiol"},{"key":"6961_CR5","doi-asserted-by":"publisher","first-page":"90","DOI":"10.1016\/0924-980x(94)00306-r","volume":"97","author":"F Awiszus","year":"1995","unstructured":"Awiszus F, Feistner H (1995) Comparison of single motor unit responses to transcranial magnetic and peroneal nerve stimulation in the tibialis anterior muscle of patients with amyotrophic lateral sclerosis. Electroencephalogr Clin Neurophysiol 97:90\u201395. https:\/\/doi.org\/10.1016\/0924-980x(94)00306-r","journal-title":"Electroencephalogr Clin Neurophysiol"},{"key":"6961_CR6","doi-asserted-by":"publisher","first-page":"65","DOI":"10.3988\/jcn.2013.9.2.65","volume":"9","author":"JS Bae","year":"2013","unstructured":"Bae JS, Simon NG, Menon P, Vucic S, Kiernan MC (2013) The puzzling case of hyperexcitability in amyotrophic lateral sclerosis. J Clin Neurol 9:65\u201374. https:\/\/doi.org\/10.3988\/jcn.2013.9.2.65","journal-title":"J Clin Neurol"},{"key":"6961_CR7","doi-asserted-by":"publisher","first-page":"740","DOI":"10.1139\/y04-069","volume":"82","author":"P Bawa","year":"2004","unstructured":"Bawa P, Calancie B (2004) Rate-coding of spinal motoneurons with high frequency magnetic stimulation of human motor cortex. Can J Physiol Pharmacol 82:740\u2013748","journal-title":"Can J Physiol Pharmacol"},{"key":"6961_CR8","doi-asserted-by":"publisher","first-page":"293","DOI":"10.1080\/146608200300079536","volume":"1","author":"Brooks BR, Miller RG, Swash M, Munsat TL, World Federation of Neurology Research Group on Motor Neuron D","year":"2000","unstructured":"Brooks BR, Miller RG, Swash M, Munsat TL, World Federation of Neurology Research Group on Motor Neuron D (2000) El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph Lateral Scler Other Motor Neuron Disord 1:293\u2013299. https:\/\/doi.org\/10.1080\/146608200300079536","journal-title":"Amyotroph Lateral Scler Other Motor Neuron Disord"},{"key":"6961_CR9","doi-asserted-by":"publisher","first-page":"1168","DOI":"10.1152\/jn.1987.58.5.1168","volume":"58","author":"B Calancie","year":"1987","unstructured":"Calancie B, Nordin M, Wallin R, Hagbarth KE (1987) Motor-unit responses in human wrist flexor and extensor muscles to transcranial cortical stimuli. J Neurophysiol 58:1168\u20131185. https:\/\/doi.org\/10.1152\/jn.1987.58.5.1168","journal-title":"J Neurophysiol"},{"key":"6961_CR10","doi-asserted-by":"publisher","first-page":"1205","DOI":"10.1007\/s00221-018-5212-8","volume":"236","author":"B Calancie","year":"2018","unstructured":"Calancie B, Wang D, Young E, Alexeeva N (2018) Four-pulse transcranial magnetic stimulation using multiple conditioning inputs. Norm MEP Responses Exp Brain Res 236:1205\u20131218. https:\/\/doi.org\/10.1007\/s00221-018-5212-8","journal-title":"Exp Brain Res"},{"key":"6961_CR11","doi-asserted-by":"publisher","first-page":"2087","DOI":"10.1007\/s00221-019-05573-4","volume":"237","author":"B Calancie","year":"2019","unstructured":"Calancie B, Young E, Watson ML, Wang D, Alexeeva N (2019) Superconditioning TMS for examining upper motor neuron function in MND. Exp Brain Res 237:2087\u20132103. https:\/\/doi.org\/10.1007\/s00221-019-05573-4","journal-title":"Exp Brain Res"},{"key":"6961_CR12","doi-asserted-by":"publisher","first-page":"331","DOI":"10.1097\/WNP.0000000000000891","volume":"40","author":"BM Calancie","year":"2023","unstructured":"Calancie BM, Chin S, Wang D (2023) Establishing the minimum intensity of transcranial magnetic stimulation superconditioning pulses to effect inhibition and facilitation of motor evoked potentials. J Clin Neurophysiol 40:331\u2013338. https:\/\/doi.org\/10.1097\/WNP.0000000000000891","journal-title":"J Clin Neurophysiol"},{"key":"6961_CR13","doi-asserted-by":"publisher","first-page":"189","DOI":"10.1007\/s004150050561","volume":"247","author":"M de Carvalho","year":"2000","unstructured":"de Carvalho M, Miranda PC, Lourdes Sales Luis M, Ducla-Soares E (2000) Neurophysiological features of fasciculation potentials evoked by transcranial magnetic stimulation in amyotrophic lateral sclerosis. J Neurol 247:189\u2013194. https:\/\/doi.org\/10.1007\/s004150050561","journal-title":"J Neurol"},{"key":"6961_CR14","doi-asserted-by":"publisher","first-page":"141","DOI":"10.1055\/s-2001-15261","volume":"21","author":"A Eisen","year":"2001","unstructured":"Eisen A (2001) Clinical electrophysiology of the upper and lower motor neuron in amyotrophic lateral sclerosis. Semin Neurol 21:141\u2013154. https:\/\/doi.org\/10.1055\/s-2001-15261","journal-title":"Semin Neurol"},{"key":"6961_CR15","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1017\/S031716710004734x","volume":"20","author":"A Eisen","year":"1993","unstructured":"Eisen A, Pant B, Stewart H (1993) Cortical excitability in amyotrophic lateral sclerosis: a clue to pathogenesis. Can J Neurol Sci 20:11\u201316. https:\/\/doi.org\/10.1017\/S031716710004734x","journal-title":"Can J Neurol Sci"},{"key":"6961_CR16","doi-asserted-by":"publisher","first-page":"1396","DOI":"10.1212\/wnl.46.5.1396","volume":"46","author":"A Eisen","year":"1996","unstructured":"Eisen A, Entezari-Taher M, Stewart H (1996) Cortical projections to spinal motoneurons: changes with aging and amyotrophic lateral sclerosis. Neurology 46:1396\u20131404. https:\/\/doi.org\/10.1212\/wnl.46.5.1396","journal-title":"Neurology"},{"issue":"1","key":"6961_CR17","doi-asserted-by":"publisher","first-page":"S64","DOI":"10.1016\/s0022-510x(98)00200-7","volume":"160","author":"A Eisen","year":"1998","unstructured":"Eisen A, Nakajima M, Weber M (1998) Corticomotorneuronal hyper-excitability in amyotrophic lateral sclerosis. J Neurol Sci 160(1):S64\u2013S68. https:\/\/doi.org\/10.1016\/s0022-510x(98)00200-7","journal-title":"J Neurol Sci"},{"key":"6961_CR18","doi-asserted-by":"publisher","first-page":"65","DOI":"10.1002\/(SICI)1097-4598(199701)20:1<65::AID-MUS9>3.0.CO;2-F","volume":"20","author":"M Enterzari-Taher","year":"1997","unstructured":"Enterzari-Taher M, Eisen A, Stewart H, Nakajima M (1997) Abnormalities of cortical inhibitory neurons in amyotrophic lateral sclerosis. Muscle Nerve 20:65\u201371. https:\/\/doi.org\/10.1002\/(SICI)1097-4598(199701)20:1%3c65::AID-MUS9%3e3.0.CO;2-F","journal-title":"Muscle Nerve"},{"key":"6961_CR19","doi-asserted-by":"publisher","first-page":"2643","DOI":"10.1016\/j.clinph.2016.04.025","volume":"127","author":"W Huynh","year":"2016","unstructured":"Huynh W, Simon NG, Grosskreutz J, Turner MR, Vucic S, Kiernan MC (2016) Assessment of the upper motor neuron in amyotrophic lateral sclerosis. Clin Neurophysiol 127:2643\u20132660. https:\/\/doi.org\/10.1016\/j.clinph.2016.04.025","journal-title":"Clin Neurophysiol"},{"key":"6961_CR20","doi-asserted-by":"publisher","first-page":"521","DOI":"10.3389\/fneur.2017.00521","volume":"8","author":"N Katyal","year":"2017","unstructured":"Katyal N, Govindarajan R (2017) Shortcomings in the current amyotrophic lateral sclerosis trials and potential solutions for improvement. Front Neurol 8:521. https:\/\/doi.org\/10.3389\/fneur.2017.00521","journal-title":"Front Neurol"},{"key":"6961_CR21","doi-asserted-by":"publisher","first-page":"720","DOI":"10.1016\/S1388-2457(00)00518-6","volume":"112","author":"JC Keel","year":"2001","unstructured":"Keel JC, Smith MJ, Wassermann EM (2001) A safety screening questionnaire for transcranial magnetic stimulation. Clin Neurophysiol 112:720","journal-title":"Clin Neurophysiol"},{"key":"6961_CR22","doi-asserted-by":"publisher","DOI":"10.1002\/acn3.51887","author":"NJ Maragakis","year":"2023","unstructured":"Maragakis NJ, de Carvalho M, Weiss MD (2023) Therapeutic targeting of ALS pathways: refocusing an incomplete picture. Ann Clin Transl Neurol. https:\/\/doi.org\/10.1002\/acn3.51887","journal-title":"Ann Clin Transl Neurol"},{"key":"6961_CR23","doi-asserted-by":"publisher","first-page":"1918","DOI":"10.1111\/ene.14393","volume":"27","author":"P Masrori","year":"2020","unstructured":"Masrori P, Van Damme P (2020) Amyotrophic lateral sclerosis: a clinical review. Eur J Neurol 27:1918\u20131929. https:\/\/doi.org\/10.1111\/ene.14393","journal-title":"Eur J Neurol"},{"issue":"4","key":"6961_CR24","doi-asserted-by":"publisher","first-page":"971","DOI":"10.1093\/brain\/118.4.971","volume":"118","author":"KR Mills","year":"1995","unstructured":"Mills KR (1995) Motor neuron disease. Studies of the corticospinal excitation of single motor neurons by magnetic brain stimulation. Brain 118(4):971\u2013982. https:\/\/doi.org\/10.1093\/brain\/118.4.971","journal-title":"Brain"},{"key":"6961_CR25","doi-asserted-by":"publisher","first-page":"1617","DOI":"10.1016\/j.mayocp.2018.04.007","volume":"93","author":"B Oskarsson","year":"2018","unstructured":"Oskarsson B, Gendron TF, Staff NP (2018) Amyotrophic lateral sclerosis: an update for 2018. Mayo Clin Proc 93:1617\u20131628. https:\/\/doi.org\/10.1016\/j.mayocp.2018.04.007","journal-title":"Mayo Clin Proc"},{"issue":"S2","key":"6961_CR26","doi-asserted-by":"publisher","first-page":"S19","DOI":"10.1212\/WNL.47.4_Suppl_2.19S","volume":"47","author":"JD Rothstein","year":"1996","unstructured":"Rothstein JD (1996) Excitotoxicity hypothesis. Neurology 47(S2):S19\u2013S26. https:\/\/doi.org\/10.1212\/WNL.47.4_Suppl_2.19S","journal-title":"Neurology"},{"key":"6961_CR27","doi-asserted-by":"publisher","first-page":"229","DOI":"10.1007\/s00221-008-1420-y","volume":"189","author":"A Schmied","year":"2008","unstructured":"Schmied A, Attarian S (2008) Enhancement of single motor unit inhibitory responses to transcranial magnetic stimulation in amyotrophic lateral sclerosis. Exp Brain Res 189:229\u2013242. https:\/\/doi.org\/10.1007\/s00221-008-1420-y","journal-title":"Exp Brain Res"},{"key":"6961_CR28","doi-asserted-by":"publisher","first-page":"1171","DOI":"10.1001\/archneur.57.8.1171","volume":"57","author":"BJ Traynor","year":"2000","unstructured":"Traynor BJ, Codd MB, Corr B, Forde C, Frost E, Hardiman OM (2000) Clinical features of amyotrophic lateral sclerosis according to the El Escorial and Airlie House diagnostic criteria: a population-based study. Arch Neurol 57:1171\u20131176. https:\/\/doi.org\/10.1001\/archneur.57.8.1171","journal-title":"Arch Neurol"},{"key":"6961_CR29","doi-asserted-by":"publisher","first-page":"e1610","DOI":"10.1212\/WNL.0000000000007242","volume":"92","author":"LH van den Berg","year":"2019","unstructured":"van den Berg LH, Sorenson E, Gronseth G et al (2019) Revised Airlie House consensus guidelines for design and implementation of ALS clinical trials. Neurology 92:e1610\u2013e1623. https:\/\/doi.org\/10.1212\/WNL.0000000000007242","journal-title":"Neurology"},{"key":"6961_CR30","doi-asserted-by":"publisher","first-page":"2084","DOI":"10.1016\/S0140-6736(17)31287-4","volume":"390","author":"MA van Es","year":"2017","unstructured":"van Es MA, Hardiman O, Chio A, Al-Chalabi A, Pasterkamp RJ, Veldink JH, van den Berg LH (2017) Amyotrophic lateral sclerosis. Lancet 390:2084\u20132098. https:\/\/doi.org\/10.1016\/S0140-6736(17)31287-4","journal-title":"Lancet"},{"key":"6961_CR31","doi-asserted-by":"publisher","first-page":"177","DOI":"10.1016\/j.expneurol.2009.08.017","volume":"220","author":"S Vucic","year":"2009","unstructured":"Vucic S, Cheah BC, Kiernan MC (2009) Defining the mechanisms that underlie cortical hyperexcitability in amyotrophic lateral sclerosis. Exp Neurol 220:177\u2013182. https:\/\/doi.org\/10.1016\/j.expneurol.2009.08.017","journal-title":"Exp Neurol"},{"key":"6961_CR32","doi-asserted-by":"publisher","first-page":"561","DOI":"10.1016\/B978-0-444-53497-2.00045-0","volume":"116","author":"S Vucic","year":"2013","unstructured":"Vucic S, Kiernan MC (2013) Utility of transcranial magnetic stimulation in delineating amyotrophic lateral sclerosis pathophysiology. Handb Clin Neurol 116:561\u2013575. https:\/\/doi.org\/10.1016\/B978-0-444-53497-2.00045-0","journal-title":"Handb Clin Neurol"},{"key":"6961_CR33","doi-asserted-by":"publisher","first-page":"1161","DOI":"10.1136\/jnnp-2012-304019","volume":"84","author":"S Vucic","year":"2013","unstructured":"Vucic S, Ziemann U, Eisen A, Hallett M, Kiernan MC (2013) Transcranial magnetic stimulation and amyotrophic lateral sclerosis: pathophysiological insights. J Neurol Neurosurg Psychiatry 84:1161\u20131170. https:\/\/doi.org\/10.1136\/jnnp-2012-304019","journal-title":"J Neurol Neurosurg Psychiatry"},{"key":"6961_CR34","doi-asserted-by":"publisher","DOI":"10.1001\/jamaneurol.2020.4300","author":"BJ Wainger","year":"2020","unstructured":"Wainger BJ, Macklin EA, Vucic S et al (2020) Effect of ezogabine on cortical and spinal motor neuron excitability in amyotrophic lateral sclerosis: a randomized clinical trial. JAMA Neurol. https:\/\/doi.org\/10.1001\/jamaneurol.2020.4300","journal-title":"JAMA Neurol"},{"key":"6961_CR35","doi-asserted-by":"publisher","first-page":"299","DOI":"10.1002\/(SICI)1097-4598(199903)22:3<299::AID-MUS2>3.0.CO;2-D","volume":"22","author":"M Weber","year":"1999","unstructured":"Weber M, Eisen A (1999) Assessment of upper and lower motor neurons in Kennedy\u2019s disease: implications for corticomotoneuronal PSTH studies. Muscle Nerve 22:299\u2013306. https:\/\/doi.org\/10.1002\/(SICI)1097-4598(199903)22:3%3c299::AID-MUS2%3e3.0.CO;2-D","journal-title":"Muscle Nerve"},{"issue":"2","key":"6961_CR36","doi-asserted-by":"publisher","first-page":"S51","DOI":"10.1080\/14660820052415826","volume":"1","author":"M Weber","year":"2000","unstructured":"Weber M, Eisen A (2000) Peristimulus time histograms (PSTHs)\u2013a marker for upper motor neuron involvement in ALS? Amyotroph Lateral Scler Other Motor Neuron Disord 1(2):S51-56. https:\/\/doi.org\/10.1080\/14660820052415826","journal-title":"Amyotroph Lateral Scler Other Motor Neuron Disord"},{"key":"6961_CR37","doi-asserted-by":"publisher","first-page":"1505","DOI":"10.1093\/brain\/123.7.1505","volume":"123","author":"M Weber","year":"2000","unstructured":"Weber M, Eisen A, Stewart HG, Andersen PM (2000) Preserved slow conducting corticomotoneuronal projections in amyotrophic lateral sclerosis with autosomal recessive D90A CuZn-superoxide dismutase mutation. Brain 123:1505\u20131515. https:\/\/doi.org\/10.1093\/brain\/123.7.1505","journal-title":"Brain"},{"key":"6961_CR38","doi-asserted-by":"publisher","first-page":"371","DOI":"10.1002\/mus.27146","volume":"63","author":"MD Weiss","year":"2021","unstructured":"Weiss MD, Macklin EA, McIlduff CE et al (2021) Effects of mexiletine on hyperexcitability in sporadic amyotrophic lateral sclerosis: preliminary findings from a small phase II randomized controlled trial. Muscle Nerve 63:371\u2013383. https:\/\/doi.org\/10.1002\/mus.27146","journal-title":"Muscle Nerve"},{"key":"6961_CR39","doi-asserted-by":"publisher","first-page":"1292","DOI":"10.1212\/wnl.49.5.1292","volume":"49","author":"U Ziemann","year":"1997","unstructured":"Ziemann U, Winter M, Reimers CD, Reimers K, Tergau F, Paulus W (1997) Impaired motor cortex inhibition in patients with amyotrophic lateral sclerosis. Evidence from paired transcranial magnetic stimulation. Neurology 49:1292\u20131298. https:\/\/doi.org\/10.1212\/wnl.49.5.1292","journal-title":"Neurology"}],"container-title":["Experimental Brain Research"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00221-024-06961-1.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s00221-024-06961-1\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00221-024-06961-1.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,2,26]],"date-time":"2025-02-26T07:42:51Z","timestamp":1740555771000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s00221-024-06961-1"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,1,22]]},"references-count":39,"journal-issue":{"issue":"2","published-print":{"date-parts":[[2025,2]]}},"alternative-id":["6961"],"URL":"https:\/\/doi.org\/10.1007\/s00221-024-06961-1","relation":{},"ISSN":["0014-4819","1432-1106"],"issn-type":[{"type":"print","value":"0014-4819"},{"type":"electronic","value":"1432-1106"}],"subject":[],"published":{"date-parts":[[2025,1,22]]},"assertion":[{"value":"3 May 2024","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"10 October 2024","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"22 January 2025","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"The authors have no relevant financial or non-financial interests to disclose. No funds, grants, or other support was received for conducting this study.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflict of interest"}},{"value":"All the procedures performed were in accordance with the ethical standards of Upstate Medical University and with the 1964 Helsinki Declaration and its later amendments.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethical approval"}},{"value":"Informed consent was obtained from all individual participants included in the study.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Informed consent"}}],"article-number":"51"}}