Neuropediatrics 2021; 52(04): 268-273
DOI: 10.1055/s-0041-1726127
Original Article

Bilateral Motor Responses to Transcranial Magnetic Stimulation in Preterm Children at 9 Years of Age

1   Department of Children and Adolescents, Oulu University Hospital, Oulu, Finland
2   PEDEGO Research Center, University of Oulu, Oulu, Finland
3   Medical Research Center Oulu, University of Oulu, Oulu, Finland
,
Seppo O. Rytky
4   Department of Clinical Neurophysiology, Oulu University Hospital, Oulu, Finland
,
Päivi M. Olsén
1   Department of Children and Adolescents, Oulu University Hospital, Oulu, Finland
2   PEDEGO Research Center, University of Oulu, Oulu, Finland
› Author Affiliations

Abstract

Objective This study was aimed to evaluate motor tracts integrity in nondisabled preterm-born (PT) children at 9 years of age.

Methods Overall, 18 PT and 13 term-born (T) children without motor disability were assessed by transcranial magnetic stimulation (TMS). Motor-evoked potentials (MEPs) were measured bilaterally from the abductor pollicis brevis (APB) and the tibialis anterior (TA) muscles. Muscle responses could be stimulated from all patients.

Results Overall, 83.3 and 23.1% of PT and T children, respectively, had mild clumsiness (p = 0.001). One PT and three T children had immediate bilateral responses in the upper extremities. Seven PT children had delayed ipsilateral APB responses after left and ten after right TMS. Three controls had delayed ipsilateral responses. Ipsilateral lower extremity responses were seen in one PT after right and two PT children and one T child after left TMS. The results did not correlate to groups, genders, clumsiness, or handedness.

Conclusion Children of PT and T may have bilateral motor responses after TMS at 9 years of age. Ipsilateral conduction emerges immediately or more often slightly delayed and more frequently in upper than in lower extremities.

Significance Bilateral motor conduction reflects developmental and neurophysiological variability in children at 9 years of age. MEPs can be used as a measure of corticospinal tract integrity in PT children.



Publication History

Received: 23 March 2020

Accepted: 20 January 2021

Article published online:
11 March 2021

© 2021. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 
  • References

  • 1 Pitcher JB, Schneider LA, Burns NR. et al. Reduced corticomotor excitability and motor skills development in children born preterm. J Physiol 2012; 590 (22) 5827-5844
  • 2 Pitcher JB, Riley AM, Doeltgen SH. et al. Physiological evidence consistent with reduced neuroplasticity in human adolescents born preterm. J Neurosci 2012; 32 (46) 16410-16416
  • 3 Müller K, Hömberg V, Lenard HG. Magnetic stimulation of motor cortex and nerve roots in children. Maturation of cortico-motoneuronal projections. Electroencephalogr Clin Neurophysiol 1991; 81 (01) 63-70
  • 4 Nezu A, Kimura S, Uehara S, Kobayashi T, Tanaka M, Saito K. Magnetic stimulation of motor cortex in children: maturity of corticospinal pathway and problem of clinical application. Brain Dev 1997; 19 (03) 176-180
  • 5 Eyre JA, Miller S, Clowry GJ, Conway EA, Watts C. Functional corticospinal projections are established prenatally in the human foetus permitting involvement in the development of spinal motor centres. Brain 2000; 123 (Pt 1): 51-64
  • 6 Frye RE, Rotenberg A, Ousley M, Pascual-Leone A. Transcranial magnetic stimulation in child neurology: current and future directions. J Child Neurol 2008; 23 (01) 79-96
  • 7 Krishnan C, Santos L, Peterson MD, Ehinger M. Safety of noninvasive brain stimulation in children and adolescents. Brain Stimul 2015; 8 (01) 76-87
  • 8 Allen CH, Kluger BM, Buard I. Safety of transcranial magnetic stimulation in children: a systematic review of the literature. Pediatr Neurol 2017; 68: 3-17
  • 9 Müller K, Kass-Iliyya F, Reitz M. Ontogeny of ipsilateral corticospinal projections: a developmental study with transcranial magnetic stimulation. Ann Neurol 1997; 42 (05) 705-711
  • 10 Chen CY, Georgieff M, Elison J. et al. Understanding brain reorganization in infants with perinatal stroke through neuroexcitability and neuroimaging. Pediatr Phys Ther 2017; 29 (02) 173-178
  • 11 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; 8 (08) 1208
  • 12 Tekgul H, Saz U, Yilmaz S. et al. A transcranial magnetic stimulation study for the investigation of corticospinal motor pathways in children with cerebral palsy. J Clin Neurosci 2020; 78: 153-158
  • 13 Maegaki Y, Maeoka Y, Ishii S. et al. Central motor reorganization in cerebral palsy patients with bilateral cerebral lesions. Pediatr Res 1999; 45 (4 Pt 1): 559-567
  • 14 Nemanich ST, Chen CY, Chen M. et al. Safety and feasibility of transcranial magnetic stimulation as an exploratory assessment of corticospinal connectivity in infants after perinatal brain injury: an observational study. Phys Ther 2019; 99 (06) 689-700
  • 15 Kuo HC, Friel KM, Gordon AM. Neurophysiological mechanisms and functional impact of mirror movements in children with unilateral spastic cerebral palsy. Dev Med Child Neurol 2018; 60 (02) 155-161
  • 16 Maegaki Y, Maeoka Y, Ishii S. et al. Mechanisms of central motor reorganization in pediatric hemiplegic patients. Neuropediatrics 1997; 28 (03) 168-174
  • 17 Olsén P, Pääkkö E, Vainionpää L, Pyhtinen J, Järvelin MR. Magnetic resonance imaging of periventricular leukomalacia and its clinical correlation in children. Ann Neurol 1997; 41 (06) 754-761
  • 18 Mayston MJ, Harrison LM, Stephens JA. A neurophysiological study of mirror movements in adults and children. Ann Neurol 1999; 45 (05) 583-594
  • 19 Lehtinen SS, Huuskonen UE, Harila-Saari AH, Tolonen U, Vainionpää LK, Lanning BM. Motor nervous system impairment persists in long-term survivors of childhood acute lymphoblastic leukemia. Cancer 2002; 94 (09) 2466-2473
  • 20 Koh TH, Eyre JA. Maturation of corticospinal tracts assessed by electromagnetic stimulation of the motor cortex. Arch Dis Child 1988; 63 (11) 1347-1352
  • 21 Largo RH, Caflisch JA, Hug F, Muggli K, Molnar AA, Molinari L. Neuromotor development from 5 to 18 years. Part 2: associated movements. Dev Med Child Neurol 2001; 43 (07) 444-453
  • 22 Hamilton SS. Evaluation of clumsiness in children. Am Fam Physician 2002; 66 (08) 1435-1440
  • 23 Goyen TA, Lui K. Developmental coordination disorder in “apparently normal” schoolchildren born extremely preterm. Arch Dis Child 2009; 94 (04) 298-302
  • 24 Edwards J, Berube M, Erlandson K. et al. Developmental coordination disorder in school-aged children born very preterm and/or at very low birth weight: a systematic review. J Dev Behav Pediatr 2011; 32 (09) 678-687
  • 25 Zwicker JG, Missiuna C, Harris SR, Boyd LA. Developmental coordination disorder: a review and update. Eur J Paediatr Neurol 2012; 16 (06) 573-581
  • 26 Dewey D, Creighton DE, Heath JA. et al. Assessment of developmental coordination disorder in children born with extremely low birth weights. Dev Neuropsychol 2011; 36 (01) 42-56
  • 27 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; 42 (04) 220-227
  • 28 Vry J, Linder-Lucht M, Berweck S. et al. Altered cortical inhibitory function in children with spastic diplegia: a TMS study. Exp Brain Res 2008; 186 (04) 611-618
  • 29 Koerte I, Heinen F, Fuchs T. et al. Anisotropy of callosal motor fibers in combination with transcranial magnetic stimulation in the course of motor development. Invest Radiol 2009; 44 (05) 279-284
  • 30 Lebel C, Walker L, Leemans A, Phillips L, Beaulieu C. Microstructural maturation of the human brain from childhood to adulthood. Neuroimage 2008; 40 (03) 1044-1055
  • 31 Walther M, Juenger H, Kuhnke N. et al. Motor cortex plasticity in ischemic perinatal stroke: a transcranial magnetic stimulation and functional MRI study. Pediatr Neurol 2009; 41 (03) 171-178
  • 32 Marzbani H, Parvin S, Amiri S. et al. The correlation between transcranial magnetic stimulation parameters and neuromuscular properties in children with cerebral palsy. Annu Int Conf IEEE Eng Med Biol Soc 2016; 2016: 5473-5476
  • 33 Lin KL, Pascual-Leone A. Transcranial magnetic stimulation and its applications in children. Chang Gung Med J 2002; 25 (07) 424-436
  • 34 Alagona G, Delvaux V, Gérard P. et al. Ipsilateral motor responses to focal transcranial magnetic stimulation in healthy subjects and acute-stroke patients. Stroke 2001; 32 (06) 1304-1309
  • 35 Garvey MA, Mall V. Transcranial magnetic stimulation in children. Clin Neurophysiol 2008; 119 (05) 973-984
  • 36 Holmström L, Vollmer B, Tedroff K. et al. Hand function in relation to brain lesions and corticomotor-projection pattern in children with unilateral cerebral palsy. Dev Med Child Neurol 2010; 52 (02) 145-152
  • 37 Säisänen L, Julkunen P, Lakka T, Lindi V, Könönen M, Määttä S. Development of corticospinal motor excitability and cortical silent period from mid-childhood to adulthood - a navigated TMS study. Neurophysiol Clin 2018; 48 (02) 65-75
  • 38 Kamen G. Reliability of motor-evoked potentials during resting and active contraction conditions. Med Sci Sports Exerc 2004; 36 (09) 1574-1579