Single-pulse transcranial magnetic stimulation for assessment of motor development in infants with early brain injury

References

• Dunbar M, Kirton A. Perinatal Stroke. Semin Pediatr Neurol. 2019 Dec;32:100767. doi: 10.1016/j.spen.2019.08.003
   PubMed Web of Science ®Google Scholar
• Novak CM, Ozen M, Burd I. Perinatal brain injury: mechanisms, prevention, and outcomes. Clin Perinatol. 2018 Jun;45(2):357–375. doi: 10.1016/j.clp.2018.01.015
   PubMed Web of Science ®Google Scholar
• Novak I, Morgan C, Adde L, et al. Early, accurate diagnosis and early intervention in cerebral palsy: advances in diagnosis and treatment. JAMA Pediatr. 2017 Sep 1;171(9):897–907. doi: 10.1001/jamapediatrics.2017.1689
   PubMed Web of Science ®Google Scholar
• Kirton A, Metzler MJ, Craig BT, et al. Perinatal stroke: mapping and modulating developmental plasticity. Nat Rev Neurol. 2021 Jul;17(7):415–432.
   PubMed Web of Science ®Google Scholar
• Hallett M. Transcranial magnetic stimulation: a primer. Neuron. 2007 Jul 19;55(2):187–199. doi: 10.1016/j.neuron.2007.06.026
   PubMed Web of Science ®Google Scholar
• Rossini PM, Burke D, Chen R, et al. Non-invasive electrical and magnetic stimulation of the brain, spinal cord, roots and peripheral nerves: basic principles and procedures for routine clinical and research application. An updated report from an I.F.C.N.Committee. Clin Neurophysiol. 2015 Jun;126(6):1071–1107. doi: 10.1016/j.clinph.2015.02.001
   PubMed Web of Science ®Google Scholar
• Garvey MA, Ziemann U, Bartko JJ, et al. Cortical correlates of neuromotor development in healthy children. Clin Neurophysiol. 2003 Sep;114(9):1662–1670.
   PubMed Web of Science ®Google Scholar
• Eyre JA, Taylor JP, Villagra F, et al. Evidence of activity-dependent withdrawal of corticospinal projections during human development. Neurology. 2001 Nov 13;57(9):1543–1554. doi: 10.1212/WNL.57.9.1543
   PubMed Web of Science ®Google Scholar
• Garvey MA, Mall V. Transcranial magnetic stimulation in children. Clin Neurophysiol. 2008 May;119(5):973–984. doi: 10.1016/j.clinph.2007.11.048
   PubMed Web of Science ®Google Scholar
• Muller K, Homberg V, Lenard HG. Magnetic stimulation of motor cortex and nerve roots in children. Maturation of cortico-motoneuronal projections. Electroencephalogr Clin Neurophysiol. 1991 Feb;81(1):63–70. doi: 10.1016/0168-5597(91)90105-7
   PubMedGoogle Scholar
• Groppa S, Oliviero A, Eisen A, et al. A practical guide to diagnostic transcranial magnetic stimulation: report of an IFCN committee. Clin Neurophysiol. 2012 May;123(5):858–882.
   PubMed Web of Science ®Google Scholar
• Fietzek UM, Heinen F, Berweck S, et al. Development of the corticospinal system and hand motor function: central conduction times and motor performance tests. Dev Med Child Neurol. 2007;42(4):220–227. doi: 10.1111/j.1469-8749.2000.tb00076.x
   Google Scholar
• Eyre JA, Miller S, Clowry GJ, et al. Functional corticospinal projections are established prenatally in the human foetus permitting involvement in the development of spinal motor centres. Brain. 2000 Jan;123(Pt 1):51–64.
   PubMedGoogle Scholar
• Hupfeld KE, Swanson CW, Fling BW, et al. TMS-induced silent periods: a review of methods and call for consistency. J Neurosci Methods. 2020 Dec 1;346:108950. doi: 10.1016/j.jneumeth.2020.108950
   PubMed Web of Science ®Google Scholar
• Narayana S, Gibbs SK, Fulton SP, et al. Clinical utility of Transcranial Magnetic Stimulation (TMS) in the presurgicalresurgical evaluation of motor, speech, and language functions in young children with refractory epilepsy or brain tumor: preliminary evidence. Front Neurol. 2021;12:650830. doi: 10.3389/fneur.2021.650830
   PubMed Web of Science ®Google Scholar
• Bijsterbosch JD, Barker AT, Lee KH, et al. Where does transcranial magnetic stimulation (TMS) stimulate? Modelling of induced field maps for some common cortical and cerebellar targets. Med Biol Eng Comput. 2012 Jul;50(7):671–681.
   PubMed Web of Science ®Google Scholar
• Janssen AM, Rampersad SM, Lucka F, et al. The influence of sulcus width on simulated electric fields induced by transcranial magnetic stimulation. Phys Med Biol. 2013 Jul 21;58(14):4881–4896. doi: 10.1088/0031-9155/58/14/4881
   PubMed Web of Science ®Google Scholar
• Thielscher A, Opitz A, Windhoff M. Impact of the gyral geometry on the electric field induced by transcranial magnetic stimulation. Neuroimage. 2011 Jan 1;54(1):234–243. doi: 10.1016/j.neuroimage.2010.07.061
   PubMed Web of Science ®Google Scholar
• Weissman JD, Epstein CM, Davey KR. Magnetic brain stimulation and brain size: relevance to animal studies. Electroencephalogr Clin Neurophysiol. 1992 Jun;85(3):215–219. doi: 10.1016/0168-5597(92)90135-X
   PubMedGoogle Scholar
• Wagner T, Eden U, Fregni F, et al. Transcranial magnetic stimulation and brain atrophy: a computer-based human brain model study. Exp Brain Res. 2008 Apr;186(4):539–550.
   PubMed Web of Science ®Google Scholar
• Wagner T, Fregni F, Eden U, et al. Transcranial magnetic stimulation and stroke: a computer-based human model study. Neuroimage. 2006 Apr 15;30(3):857–870. doi: 10.1016/j.neuroimage.2005.04.046
   PubMed Web of Science ®Google Scholar
• O’Brien AT, Amorim R, Rushmore RJ, et al. Motor cortex neurostimulation technologies for chronic post-stroke pain: implications of tissue damage on stimulation currents. Front Hum Neurosci. 2016;10:545. doi: 10.3389/fnhum.2016.00545
   PubMed Web of Science ®Google Scholar
• Mantell KE, Sutter EN, Shirinpour S, et al. Evaluating transcranial magnetic stimulation (TMS) induced electric fields in pediatric stroke. NeuroImage Clin. 2021;29:102563. doi: 10.1016/j.nicl.2021.102563
   PubMed Web of Science ®Google Scholar
• Eyre JA, Miller S, Ramesh V. Constancy of central conduction delays during development in man: investigation of motor and somatosensory pathways. J Physiol. 1991 Mar;434(1):441–452. doi: 10.1113/jphysiol.1991.sp018479
   PubMedGoogle Scholar
• Koh TH, Eyre JA. Maturation of corticospinal tracts assessed by electromagnetic stimulation of the motor cortex. Arch Dis Child. 1988 Nov;63(11):1347–1352. doi: 10.1136/adc.63.11.1347
   PubMed Web of Science ®Google Scholar
• Eyre JA, Smith M, Dabydeen L, et al. Is hemiplegic cerebral palsy equivalent to amblyopia of the corticospinal system? Ann Neurol. 2007 Nov;62(5):493–503.
   PubMed Web of Science ®Google Scholar
• Colon AJ, Vredeveld JW, Blaauw G. Motor evoked potentials after transcranial magnetic stimulation support hypothesis of coexisting central mechanism in obstetric brachial palsy. J Clin Neurophysiol. 2007 Feb;24(1):48–51. doi: 10.1097/01.wnp.0000237075.85689.33
   PubMed Web of Science ®Google Scholar
• Dabydeen L, Thomas JE, Aston TJ, et al. High-energy and -protein diet increases brain and corticospinal tract growth in term and preterm infants after perinatal brain injury. Pediatrics. 2008 Jan;121(1):148–156.
   PubMed Web of Science ®Google Scholar
• Muller K, Homberg V, Aulich A, et al. Magnetoelectrical stimulation of motor cortex in children with motor disturbances. Electroencephalogr Clin Neurophysiol. 1992 Apr;85(2):86–94.
   PubMedGoogle Scholar
• Collado-Corona MA, Mora-Magana I, Cordero GL, et al. Transcranial magnetic stimulation and acoustic trauma or hearing loss in children. Neurol Res. 2001 Jun;23(4):343–346.
   PubMed Web of Science ®Google Scholar
• Santiago-Rodriguez E, Leon-Castillo C, Harmony T, et al. Motor potentials by magnetic stimulation in periventricular leukomalacia. Pediatr Neurol. 2009 Apr;40(4):282–288.
   PubMed Web of Science ®Google Scholar
• Chang D, Singhal NS, Tarapore PE, et al. Repetitive transcranial magnetic stimulation (rTMS) as therapy in an infant with epilepsia partialis continua. Epilepsy Behav Rep. 2022;18:100511. doi: 10.1016/j.ebr.2021.100511
   PubMedGoogle Scholar
• Kowalski JL, Nemanich ST, Nawshin T, et al. Motor evoked potentials as potential biomarkers of early atypical corticospinal tract development in infants with perinatal stroke. J Clin Med. 2019 Aug 13;8(8):1208. doi: 10.3390/jcm8081208
   PubMed Web of Science ®Google Scholar
• Nemanich ST, Chen CY, Chen M, et al. Safety and feasibility of transcranial magnetic stimulation as an exploratory assessment of corticospinal connectivityorticospinal connectivity in infants after perinatal brain injury: an observational study. Phys Ther. 2019 Jun 1;99(6):689–700. doi: 10.1093/ptj/pzz028
   PubMed Web of Science ®Google Scholar
• Fietzek UM, Heinen F, Berweck S, et al. Development of the corticospinal system and hand motor function: central conduction times and motor performance tests. Dev Med Child Neurol. 2000 Apr;42(4):220–227.
   PubMed Web of Science ®Google Scholar
• Yang JF, Livingstone D, Brunton K, et al. Training to enhance walking in children with cerebral palsy: are we missing the window of opportunity? Semin Pediatr Neurol. 2013 Jun;20(2):106–115.
   PubMed Web of Science ®Google Scholar
• Narayana S, Rezaie R, McAfee SS, et al. Assessing motor function in young children with transcranial magnetic stimulation. Pediatr Neurol. 2015 Jan;52(1):94–103.
   PubMed Web of Science ®Google Scholar
• Nezu A, Kimura S, Uehara S, et al. Magnetic stimulation of motor cortex in children: maturity of corticospinal pathway and problem of clinical application. Brain Dev. 1997 Apr;19(3):176–180.
   PubMed Web of Science ®Google Scholar
• Tamer SK, Misra S, Jaiswal S. Central motor conduction time in malnourished children. Arch Dis Child. 1997 Oct;77(4):323–325. doi: 10.1136/adc.77.4.323
   PubMed Web of Science ®Google Scholar
• Dachy B, Dan B. Electrophysiological assessment of the effect of intrathecal baclofen in spastic children. Clin Neurophysiol. 2002 Mar;113(3):336–40. doi: 10.1016/S1388-2457(02)00010-X
   PubMed Web of Science ®Google Scholar
• Geerdink N, Pasman JW, Roeleveld N, et al. Responses to lumbar magnetic stimulation in newborns with spina bifida. Pediatr Neurol. 2006 Feb;34(2):101–105.
   PubMed Web of Science ®Google Scholar
• Eyre JA. Corticospinal tract development and its plasticity after perinatal injury. Neurosci Biobehav Rev. 2007;31(8):1136–1149.
   PubMed Web of Science ®Google Scholar
• Koudijs SM, Leijten FS, Ramsey NF, et al. Lateralization of motor innervation in children with intractable focal epilepsy–a TMS and fMRI study. Epilepsy Res. 2010 Jun;90(1–2):140–150.
   PubMed Web of Science ®Google Scholar
• Narayana S, Mudigoudar B, Babajani-Feremi A, et al. Successful motor mapping with transcranial magnetic stimulation in an infant: A case report. Neurology. 2017 Nov 14;89(20):2115–2117. doi: 10.1212/WNL.0000000000004650
   PubMed Web of Science ®Google Scholar
• Zewdie E, Ciechanski P, Kuo HC, et al. Safety and tolerability of transcranial magnetic and direct current stimulation in children: prospective single center evidence from 3.5 million stimulations. Brain Stimul. 2020 May;13(3):565–575. doi: 10.1016/j.brs.2019.12.025
   PubMed Web of Science ®Google Scholar
• Rossi S, Antal A, Bestmann S, et al. Safety and recommendations for TMS use in healthy subjects and patient populations, with updates on training, ethical and regulatory issues: expert guidelines. Clin Neurophysiol. 2021 Jan;132(1):269–306. doi: 10.1016/j.clinph.2020.10.003
   PubMed Web of Science ®Google Scholar
• Allen KA, Brandon DH. Hypoxic Ischemic Encephalopathy: pathophysiology and experimental treatments. Newborn Infant Nurs Rev. 2011 Sep 1;11(3):125–133. doi: 10.1053/j.nainr.2011.07.004
   PubMedGoogle Scholar
• Kowalski JL, Hickey M, Rao R, et al. Safety of single-pulse TMS in two infants with implanted patent ductus arteriosus closure devices. Brain Stimul. 2020 May;13(3):861–862.
   PubMed Web of Science ®Google Scholar
• Braden AA, Weatherspoon SE, Boardman T, et al. Image-guided TMS is safe in a predominately pediatric clinical population. Clin Neurophysiol. 2022 May;137:193–206.
   PubMed Web of Science ®Google Scholar
• Martin JH. The corticospinal system: from development to motor control. Neuroscientist. 2005 Apr;11(2):161–173. doi: 10.1177/1073858404270843
   PubMed Web of Science ®Google Scholar
• Friel KM, Kuo HC, Fuller J, et al. Skilled bimanual training drives motor cortex plasticity in children with unilateral cerebral palsy. Neurorehabil Neural Repair. 2016 Oct;30(9):834–844.
   PubMed Web of Science ®Google Scholar
• Smorenburg AR, Gordon AM, Kuo HC, et al. Does corticospinaorticospinal tract connectivity influence the response to intensive bimanual therapy in children with unilateral cerebral palsy? Neurorehabil Neural Repair. 2017 Mar;31(3):250–260.
   PubMed Web of Science ®Google Scholar
• Kuhnke N, Juenger H, Walther M, et al. Do patients with congenital hemiparesis and ipsilateral corticospinal projections respond differently to constraint-induced movement therapy? Dev Med Child Neurol. 2008 Dec;50(12):898–903.
   PubMed Web of Science ®Google Scholar
• Gillick B, Rich T, Nemanich S, et al. Transcranial direct current stimulation and constraint-induced therapy in cerebral palsy: a randomized, blinded, sham-controlled clinical trial. Eur J Paediatr Neurol. 2018 May;22(3):358–368.
   PubMed Web of Science ®Google Scholar
• Cavaleri R, Schabrun SM, Chipchase LS. The reliability and validity of rapid transcranial magnetic stimulation mapping. Brain Stimul. 2018;11(6):1291–1295. doi: 10.1016/j.brs.2018.07.043
   PubMed Web of Science ®Google Scholar
• van de Ruit M, Perenboom MJ, Grey MJ. TMS brain mapping in less than two minutes. Brain Stimul. 2015;8(2):231–239. doi: 10.1016/j.brs.2014.10.020
   PubMed Web of Science ®Google Scholar
• McIntyre S, Morgan C, Walker K, et al. Cerebral palsy–don’t delay. Dev Disabil Res Rev. 2011;17(2):114–129. doi: 10.1002/ddrr.1106
   PubMedGoogle Scholar
• Herskind A, Greisen G, Nielsen JB. Early identification and intervention in cerebral palsy. Dev Med Child Neurol. 2015 Jan;57(1):29–36. doi: 10.1111/dmcn.12531
   PubMed Web of Science ®Google Scholar
• Hoare BJ, Wallen MA, Thorley MN, et al. Constraint-induced movement therapy in children with unilateral cerebral palsy. Cochrane Database Syst Rev. 2019;4(4):CD004149. doi: 10.1002/14651858.CD004149.pub3
   PubMedGoogle Scholar
• Stinear CM, Barber PA, Petoe M, et al. The PREP algorithm predicts potential for upper limb recovery after stroke. Brain. 2012 Aug;135(Pt 8):2527–2535.
   PubMed Web of Science ®Google Scholar
• Cavaleri R, Schabrun SM, Chipchase LS. The number of stimuli required to reliably assess corticomotor excitability and primary motor cortical representations using transcranial magnetic stimulation (TMS): a systematic review and meta-analysis. Syst Rev. 2017 Mar 6;6(1):48. doi: 10.1186/s13643-017-0440-8
   PubMedGoogle Scholar
• Goldsworthy MR, Hordacre B, Ridding MC. Minimum number of trials required for within- and between-session reliability of TMS measures of corticospinal excitability. Neuroscience. 2016 Apr 21;320:205–209. doi: 10.1016/j.neuroscience.2016.02.012
   PubMed Web of Science ®Google Scholar
• Barkovich MJ, Li Y, Desikan RS, et al. Challenges in pediatric neuroimaging. Neuroimage. 2019 Jan 15;185:793–801. doi: 10.1016/j.neuroimage.2018.04.044
   PubMed Web of Science ®Google Scholar
• Kirton A. Advancing non-invasive neuromodulation clinical trials in children: Lessons from perinatal stroke. Eur J Paediatr Neurol. 2017 Jan;21(1):75–103. doi: 10.1016/j.ejpn.2016.07.002
   PubMed Web of Science ®Google Scholar
• O’Leary GH, Jenkins DD, Coker-Bolt P, et al. From adults to pediatrics: a review noninvasive brain stimulation (NIBS) to facilitate recovery from brain injury. Prog Brain Res. 2021;264:287–322.
   PubMed Web of Science ®Google Scholar