{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,11,2]],"date-time":"2025-11-02T10:40:43Z","timestamp":1762080043085,"version":"build-2065373602"},"reference-count":51,"publisher":"MDPI AG","issue":"12","license":[{"start":{"date-parts":[[2022,12,16]],"date-time":"2022-12-16T00:00:00Z","timestamp":1671148800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Chancellerie des Universit\u00e9s de Paris","award":["109-2636-B-110-001"],"award-info":[{"award-number":["109-2636-B-110-001"]}]},{"name":"Fondation de France","award":["109-2636-B-110-001"],"award-info":[{"award-number":["109-2636-B-110-001"]}]},{"name":"Fondation M\u00e9disite","award":["109-2636-B-110-001"],"award-info":[{"award-number":["109-2636-B-110-001"]}]},{"name":"INSERM","award":["109-2636-B-110-001"],"award-info":[{"award-number":["109-2636-B-110-001"]}]},{"name":"Universit\u00e9 de Versailles Saint-Quentin-en-Yvelines","award":["109-2636-B-110-001"],"award-info":[{"award-number":["109-2636-B-110-001"]}]},{"name":"Ministry of Science and Technology","award":["109-2636-B-110-001"],"award-info":[{"award-number":["109-2636-B-110-001"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Biology"],"abstract":"<jats:p>Peripheral nerve injuries induce long-lasting physiological and severe functional impairment due to motor, sensory, and autonomic denervation. Preclinical models allow us to study the process of nerve damage, evaluate the capacity of the peripheral nervous system for spontaneous recovery, and test diagnostic tools to assess the damage and subsequent recovery. Methods: In this study on Sprague\u2013Dawley rats, we: (1) compared the use of two different anesthetics (isoflurane and urethane) for the evaluation of motor evoked potentials (MEPs) induced by trans-spinal magnetic stimulation (TSMS) in gastrocnemius and brachioradialis muscles; (2) monitored the evolution of gastrocnemius MEPs by applying paired-pulse stimulation to evaluate the neuromuscular junction activity; and (3) evaluated the MEP amplitude before and after left tibialis nerve crush (up to 7 days post-injury under isoflurane anesthesia). The results showed that muscle MEPs had higher amplitudes under isoflurane anesthesia, as compared with urethane anesthesia in the rats, demonstrating higher motoneuronal excitability under isoflurane anesthesia evaluated by TSMS. Following tibial nerve crush, a significant reduction in gastrocnemius MEP amplitude was observed on the injured side, mainly due to axonal damage from the initial crush. No spontaneous recovery of MEP amplitude in gastrocnemius muscles was observed up to 7 days post-crush; even a nerve section did not induce any variation in residual MEP amplitude, suggesting that the initial crush effectively severed the axonal fibers. These observations were confirmed histologically by a drastic reduction in the remaining myelinated fibers in the crushed tibial nerve. These data demonstrate that TSMS can be reliably used to noninvasively evaluate peripheral nerve function in rats. This method could therefore readily be applied to evaluate nerve conductance in the clinical environment.<\/jats:p>","DOI":"10.3390\/biology11121834","type":"journal-article","created":{"date-parts":[[2022,12,16]],"date-time":"2022-12-16T02:54:02Z","timestamp":1671159242000},"page":"1834","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Evaluation of Gastrocnemius Motor Evoked Potentials Induced by Trans-Spinal Magnetic Stimulation Following Tibial Nerve Crush in Rats"],"prefix":"10.3390","volume":"11","author":[{"given":"Pauline","family":"Michel-Flutot","sequence":"first","affiliation":[{"name":"END-ICAP, UVSQ, Inserm, Universit\u00e9 Paris-Saclay, 78000 Versailles, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Isley","family":"Jesus","sequence":"additional","affiliation":[{"name":"END-ICAP, UVSQ, Inserm, Universit\u00e9 Paris-Saclay, 78000 Versailles, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1442-8924","authenticated-orcid":false,"given":"Arnaud","family":"Mansart","sequence":"additional","affiliation":[{"name":"Infection et Inflammation (2I), UVSQ, Inserm, Universit\u00e9 Paris-Saclay, 78000 Versailles, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1446-7456","authenticated-orcid":false,"given":"Marcel","family":"Bonay","sequence":"additional","affiliation":[{"name":"END-ICAP, UVSQ, Inserm, Universit\u00e9 Paris-Saclay, 78000 Versailles, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5654-6502","authenticated-orcid":false,"given":"Kun-Ze","family":"Lee","sequence":"additional","affiliation":[{"name":"Department of Biological Sciences, National Sun Yat-sen University, Kaohsiung 80424, Taiwan"},{"name":"Department of Biomedical Science and Environmental Biology, Kaohsiung Medical University, Kaohsiung 80424, Taiwan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Karine","family":"Aur\u00e9","sequence":"additional","affiliation":[{"name":"Department of Neurophysiology, Foch Hospital, 75073 Suresnes, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7013-1741","authenticated-orcid":false,"given":"St\u00e9phane","family":"Vinit","sequence":"additional","affiliation":[{"name":"END-ICAP, UVSQ, Inserm, Universit\u00e9 Paris-Saclay, 78000 Versailles, France"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2022,12,16]]},"reference":[{"key":"ref_1","first-page":"273","article-title":"Iatrogenic nerve injuries: Prevalence, diagnosis and treatment","volume":"111","author":"Antoniadis","year":"2014","journal-title":"Dtsch. Arztebl. Int."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"84","DOI":"10.1097\/00003086-200008000-00012","article-title":"Nerve injury in traumatic dislocation of the hip","volume":"377","author":"Cornwall","year":"2000","journal-title":"Clin. Orthop. Relat. Res."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"E1","DOI":"10.3171\/foc.2004.16.5.2","article-title":"Pathophysiology of peripheral nerve injury: A brief review","volume":"16","author":"Burnett","year":"2004","journal-title":"Neurosurg. Focus"},{"key":"ref_4","first-page":"37","article-title":"Effects of trapidil after crush injury in peripheral nerve","volume":"59","author":"Kurtoglu","year":"2005","journal-title":"Acta Med. Okayama"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"391","DOI":"10.1053\/jhsu.2000.4165","article-title":"A 25-year perspective of peripheral nerve surgery: Evolving neuroscientific concepts and clinical significance","volume":"25","author":"Lundborg","year":"2000","journal-title":"J. Hand Surg. Am."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1466404","DOI":"10.1080\/2331205X.2018.1466404","article-title":"Peripheral nerve injury and axonotmesis: State of the art and recent advances","volume":"5","author":"Alvites","year":"2018","journal-title":"Cogent Med."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"531","DOI":"10.1055\/s-2001-17755","article-title":"Standardizing nerve crushes with a non-serrated clamp","volume":"17","author":"Beer","year":"2001","journal-title":"J. Reconstr. Microsurg."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1016\/j.jneumeth.2015.01.021","article-title":"The sciatic nerve injury model in pre-clinical research","volume":"243","author":"Geuna","year":"2015","journal-title":"J. Neurosci. Methods"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"166","DOI":"10.1016\/j.jneumeth.2014.01.020","article-title":"Sciatic nerve injury: A simple and subtle model for investigating many aspects of nervous system damage and recovery","volume":"227","author":"Savastano","year":"2014","journal-title":"J. Neurosci. Methods"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1860","DOI":"10.1097\/PRS.0b013e3181bcee47","article-title":"Sensory protection of rat muscle spindles following peripheral nerve injury and reinnervation","volume":"124","author":"Elsohemy","year":"2009","journal-title":"Plast. Reconstr. Surg."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"E253","DOI":"10.1002\/lary.26583","article-title":"Nerve transection repair using laser-activated chitosan in a rat model","volume":"127","author":"Bhatt","year":"2017","journal-title":"Laryngoscope"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1016\/j.jneumeth.2008.01.022","article-title":"Is the Sciatic Functional Index always reliable and reproducible?","volume":"170","author":"Barbieri","year":"2008","journal-title":"J. Neurosci. Methods"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1097\/00006534-198901000-00024","article-title":"Functional evaluation of complete sciatic, peroneal, and posterior tibial nerve lesions in the rat","volume":"83","author":"Bain","year":"1989","journal-title":"Plast. Reconstr. Surg."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"226","DOI":"10.1002\/micr.1920100317","article-title":"Self-evaluation of walking-track measurement using a Sciatic Function Index","volume":"10","author":"Brown","year":"1989","journal-title":"Microsurgery"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"216","DOI":"10.1111\/j.1529-8027.2007.00142.x","article-title":"Two-dimensional digital video ankle motion analysis for assessment of function in the rat sciatic nerve model","volume":"12","author":"Spinner","year":"2007","journal-title":"J. Peripher. Nerv. Syst."},{"key":"ref_16","first-page":"e60267","article-title":"3D Kinematic Analysis for the Functional Evaluation in the Rat Model of Sciatic Nerve Crush Injury","volume":"156","author":"Wang","year":"2020","journal-title":"J. Vis. Exp."},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Wang, T., Ito, A., Aoyama, T., Nakahara, R., Nakahata, A., Ji, X., Zhang, J., Kawai, H., and Kuroki, H. (2018). Functional evaluation outcomes correlate with histomorphometric changes in the rat sciatic nerve crush injury model: A comparison between sciatic functional index and kinematic analysis. PLoS ONE, 13.","DOI":"10.1371\/journal.pone.0208985"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"644","DOI":"10.1002\/micr.20685","article-title":"Functional assessment after sciatic nerve injury in a rat model","volume":"29","author":"Dinh","year":"2009","journal-title":"Microsurgery"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"377","DOI":"10.1016\/j.ultrasmedbio.2019.10.004","article-title":"Evaluation of the Crushed Sciatic Nerve and Denervated Muscle with Multimodality Ultrasound Techniques: An Animal Study","volume":"46","author":"Zhu","year":"2020","journal-title":"Ultrasound Med. Biol."},{"key":"ref_20","first-page":"123","article-title":"Magnetic resonance imaging evaluation of acute crush injury of rabbit sciatic nerve: Correlation with histology","volume":"59","author":"Li","year":"2008","journal-title":"Can. Assoc. Radiol. J."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"497","DOI":"10.1002\/jemt.20577","article-title":"A simple protocol for paraffin-embedded myelin sheath staining with osmium tetroxide for light microscope observation","volume":"71","author":"Scipio","year":"2008","journal-title":"Microsc. Res. Tech."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1657","DOI":"10.4103\/1673-5374.141798","article-title":"Histological assessment in peripheral nerve tissue engineering","volume":"9","author":"Carriel","year":"2014","journal-title":"Neural Regen. Res."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"128","DOI":"10.3171\/jns.1969.31.2.0128","article-title":"Evaluation of Nerve Injuries by Evoked Potentials and Electromyography","volume":"31","author":"David","year":"1969","journal-title":"J. Neurosurg."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"417","DOI":"10.1002\/mus.24171","article-title":"Assessment of rat sciatic nerve function following acute implantation of high density Utah slanted electrode array (25 electrodes\/mm2) based on neural recordings and evoked muscle activity","volume":"50","author":"Mathews","year":"2014","journal-title":"Muscle Nerve"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1127","DOI":"10.1152\/jn.01035.2006","article-title":"Recovery of electromyographic activity after transection and surgical repair of the rat sciatic nerve","volume":"97","author":"English","year":"2007","journal-title":"J. Neurophysiol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"43","DOI":"10.3389\/fncom.2016.00043","article-title":"Topography of Synchronization of Somatosensory Evoked Potentials Elicited by Stimulation of the Sciatic Nerve in Rat","volume":"10","author":"Qu","year":"2016","journal-title":"Front. Comput. Neurosci."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1016\/S0266-7681(96)80012-X","article-title":"Sciatic nerve regeneration in the rat after frozen muscle grafting. A comparative study using somatosensory evoked potentials","volume":"21","author":"Delaere","year":"1996","journal-title":"J. Hand Surg. Br."},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Vinit, S., Keomani, E., Deramaudt, T.B., Spruance, V.M., Bezdudnaya, T., Lane, M.A., Bonay, M., and Petitjean, M. (2014). Interdisciplinary approaches of transcranial magnetic stimulation applied to a respiratory neuronal circuitry model. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0113251"},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Vinit, S., Keomani, E., Deramaudt, T.B., Bonay, M., and Petitjean, M. (2016). Reorganization of Respiratory Descending Pathways following Cervical Spinal Partial Section Investigated by Transcranial Magnetic Stimulation in the Rat. PLoS ONE, 11.","DOI":"10.1371\/journal.pone.0148180"},{"key":"ref_30","unstructured":"Hiwaki, O., and Ueno, S. (1990, January 1\u20134). Selective Magnetic Stimulation Of The Spinal Cord. Proceedings of the [1990] Twelfth Annual International Conference of the IEEE Engineering in Medicine and Biology Society, Philadelphia, PA, USA."},{"key":"ref_31","first-page":"205","article-title":"Magnetic motor evoked potential monitoring in the rat","volume":"91","author":"Linden","year":"1999","journal-title":"J. Neurosurg."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"80","DOI":"10.3389\/fncir.2016.00080","article-title":"Differences in Motor Evoked Potentials Induced in Rats by Transcranial Magnetic Stimulation under Two Separate Anesthetics: Implications for Plasticity Studies","volume":"10","author":"Sykes","year":"2016","journal-title":"Front. Neural Circuits"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"47","DOI":"10.3389\/fncir.2016.00047","article-title":"Construction and Evaluation of Rodent-Specific rTMS Coils","volume":"10","author":"Tang","year":"2016","journal-title":"Front. Neural Circuits"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"98","DOI":"10.1016\/j.neuroscience.2015.08.030","article-title":"Segmental distribution of the motor neuron columns that supply the rat hindlimb: A muscle\/motor neuron tract-tracing analysis targeting the motor end plates","volume":"307","author":"Mohan","year":"2015","journal-title":"Neuroscience"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"676","DOI":"10.1038\/nmeth.2019","article-title":"Fiji: An open-source platform for biological-image analysis","volume":"9","author":"Schindelin","year":"2012","journal-title":"Nat. Methods"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"562","DOI":"10.1007\/s00221-001-0952-1","article-title":"Modulation of rodent cortical motor excitability by somatosensory input","volume":"142","author":"Luft","year":"2002","journal-title":"Exp. Brain Res."},{"key":"ref_37","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":"Muller","year":"2011","journal-title":"J. Neurophysiol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"722","DOI":"10.1002\/(SICI)1097-4598(199806)21:6<722::AID-MUS3>3.0.CO;2-9","article-title":"Conduction pathways of motor evoked potentials following transcranial magnetic stimulation: A rodent study using a \u201cfigure-8\u201d coil","volume":"21","author":"Kamida","year":"1998","journal-title":"Muscle Nerve"},{"key":"ref_39","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":"Rotenberg","year":"2010","journal-title":"Clin. Neurophysiol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1806","DOI":"10.1093\/cercor\/bht421","article-title":"Functional Dopaminergic Neurons in Substantia Nigra are Required for Transcranial Magnetic Stimulation-Induced Motor Plasticity","volume":"25","author":"Hsieh","year":"2015","journal-title":"Cereb. Cortex"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1093\/bja\/aef162","article-title":"Anaesthetic modulation of synaptic transmission in the mammalian CNS","volume":"89","author":"Richards","year":"2002","journal-title":"Br. J. Anaesth."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1213\/00000539-200202000-00015","article-title":"The Anesthetic Mechanism of Urethane: The Effects on Neurotransmitter-Gated Ion Channels","volume":"94","author":"Hara","year":"2002","journal-title":"Anesth. Analg."},{"key":"ref_43","unstructured":"Suckow, M.A., Weisbroth, S.H., and Franklin, C.L. (2006). Chapter 19\u2014Anesthesia and Analgesia. The Laboratory Rat, Academic Press. [2nd ed.]."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1016\/S0072-9752(07)01503-5","article-title":"The neuromuscular junction","volume":"91","author":"Engel","year":"2008","journal-title":"Handb. Clin. Neurol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"559","DOI":"10.1016\/B978-0-444-64032-1.00037-0","article-title":"Transcranial magnetic stimulation","volume":"160","author":"Lefaucheur","year":"2019","journal-title":"Handb. Clin. Neurol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"899","DOI":"10.1152\/physrev.1994.74.4.899","article-title":"Quantal acetylcholine release at the vertebrate neuromuscular junction","volume":"74","year":"1994","journal-title":"Physiol. Rev."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"641","DOI":"10.1113\/jphysiol.1963.sp007286","article-title":"Repetitive Stimulation at the Mammalian Neuromuscular Junction, and the Mobilization of Transmitter","volume":"169","author":"Hubbard","year":"1963","journal-title":"J. Physiol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1016\/j.jneumeth.2004.04.012","article-title":"Regeneration of unmyelinated and myelinated sensory nerve fibres studied by a retrograde tracer method","volume":"138","author":"Lozeron","year":"2004","journal-title":"J. Neurosci. Methods"},{"key":"ref_49","unstructured":"Derderian, C., and Tadi, P. (2021). Physiology, Withdrawal Response, StatPearls Publishing LLC."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"822","DOI":"10.1007\/s11055-012-9643-6","article-title":"The State of the Contralateral Gastrocnemius Muscle Motor Center in Rats with Unilateral Sciatic Nerve Injury","volume":"42","author":"Eremeev","year":"2012","journal-title":"Neurosci. Behav. Physiol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"2122","DOI":"10.1089\/neu.2021.0080","article-title":"Diaphragm Motor-Evoked Potential Induced by Cervical Magnetic Stimulation following Cervical Spinal Cord Contusion in the Rat","volume":"38","author":"Lee","year":"2021","journal-title":"J. Neurotrauma"}],"container-title":["Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2079-7737\/11\/12\/1834\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T01:42:27Z","timestamp":1760146947000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2079-7737\/11\/12\/1834"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,12,16]]},"references-count":51,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2022,12]]}},"alternative-id":["biology11121834"],"URL":"https:\/\/doi.org\/10.3390\/biology11121834","relation":{},"ISSN":["2079-7737"],"issn-type":[{"type":"electronic","value":"2079-7737"}],"subject":[],"published":{"date-parts":[[2022,12,16]]}}}