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Neuropediatrics 2004; 35(2): 120-125
DOI: 10.1055/s-2004-815834
Original Article

Georg Thieme Verlag KG Stuttgart · New York

Low Level of Intracortical Inhibition in Children Shown by Transcranial Magnetic Stimulation

V. Mall1 , S. Berweck2 , U. M. Fietzek2 , F.-X. Glocker3 , U. Oberhuber1 , M. Walther1 , J. Schessl1 , J. Schulte-Mönting4 , R. Korinthenberg1 , F. Heinen2
  • 1Department of Neuropediatrics and Muscle Disorders, University of Freiburg, Freiburg,. Germany
  • 2Department of Paediatric Neurology and Developmental Neuroscience, Children's University Hospital, Munich, Germany
  • 3Department of Neurology, University of Freiburg, Freiburg, Germany
  • 4Department of Medical Biometry and Statistics, University of Freiburg, Freiburg, Germany
Further Information

Publication History

Received: January 27, 2003

Accepted after Revision: December 12, 2003

Publication Date:
04 May 2004 (online)

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Abstract

Transcranial magnetic stimulation (TMS) is an established neurophysiological tool to evaluate the integrity and maturation of the corticospinal tract. TMS was used in this study to compare intracortical inhibition (ICI) in children, adolescents, and adults. The paired-pulse technique of TMS with interstimulus intervals of 2 ms was used to determine the ratio of conditioned (cMEP) and unconditioned amplitudes (ucMEP) that measures ICI. In experiment 1 (Exp 1) stimulus intensity was adapted to motor threshold (50 healthy subjects; 24 male, 26 female, median age 13.5 years, range 6.3 - 34 years) and in experiment 2 (Exp 2) stimulus intensity was adapted to the ucMEP (200 - 400 µV). Children (quotient of cMEP and ucMEP: Exp. 1: 0.71 ± 0.41, Exp. 2: 0.82 ± 0.25) had significantly less ICI compared to adults (Exp. 1: 0.21 ± 0.19, mean ± STD, Exp. 2: 0.35 ± 0.22, in both experiments p < 0.001). Recently, ICI has been linked to the regulating function of GABAergic cortical interneurons on practice-dependent neuronal plasticity. Therefore, the lower ICI in children points to maturation processes that may have implications for the greater capacity of practice-dependent neuronal plasticity in children.

Key words

Children - corticospinal system - intracortical inhibition - motor development - motor threshold - transcranial magnetic stimulation

References

  • 1 Abbruzzese G, Assini A, Buccolieri A, Schieppati M, Trompetto C. Comparison of intracortical inhibition and facilitation in distal and proximal arm muscles in humans.  J Physiol. 1999;  514 895-903
    CrossrefPubMedSearch in Google Scholar
  • 2 Amassian V E, Eberle L, Maccabee P J, Cracco R Q. Modelling magnetic coil excitation of human cerebral cortex with a peripheral nerve immersed in a brain-shaped volume conductor: the significance of fiber bending in excitation.  Electroencephalogr Clin Neurophysiol. 1992;  85 291-301
    PubMedSearch in Google Scholar
  • 3 Ben-Ari Y, Tseeb V, Raggozzino D, Khazipov R, Gaiarsa J L. Gamma-Aminobutyric acid (GABA): a fast excitatory transmitter which may regulate the development of hippocampal neurones in early postnatal life.  Prog Brain Res. 1994;  102 261-273
    PubMedSearch in Google Scholar
  • 4 Brooks-Kayal A R, Pritchett D B. Developmental changes in human gamma-aminobutyric acidA receptor subunit composition.  Ann Neurol. 1993;  34 687-693
    CrossrefPubMedSearch in Google Scholar
  • 6 Chen R, Tam A, Bütefisch C, Corwell B, Ziemann U, Rothwell J C. et al . Intracortical inhibition and facilitation in different representations of the human motor cortex.  J Neurophysiol. 1998;  80 2870-2881
    PubMedSearch in Google Scholar
  • 7 Chugani D C, Muzik O, Juhasz C, Janisse J J, Ager J, Chugani H T. Postnatal maturation of human GABAA receptors measured with positron emission tomography.  Ann Neurol. 2001;  49 618-626
    CrossrefPubMedSearch in Google Scholar
  • 8 Eyre J A, Miller S, Clowry G J, Conway E A, Watts C. Functional corticospinal projections are established prenatally in the human foetus permitting involvement in the development of spinal motor centres.  Brain. 2000;  123 51-64
    CrossrefPubMedSearch in Google Scholar
  • 9 Eyre J A, Miller S, Ramesh V. Constancy of central conduction delays during development in man: investigation of motor and somatosensory pathways.  J Physiol (Lond). 1991;  434 441-452
    PubMedSearch in Google Scholar
  • 10 Fietzek U M, Heinen F, Berweck S, Maute S, Hufschmidt A, Schulte-Mönting J. et al . Development of the corticospinal system and hand motor function: central conduction times and motor performance tests.  Dev Med Child Neurol. 2000;  42 220-227
    CrossrefPubMedSearch in Google Scholar
  • 11 Fisher R J, Nakamura Y, Bestmann S, Rothwell J C, Bostock H. Two phases of intracortical inhibition revealed by transcranial magnetic threshold tracking.  Exp Brain Res. 2002;  143 240-248
    CrossrefPubMedSearch in Google Scholar
  • 12 Gerloff C, Cohen L G, Floeter M K, Chen R, Corwell B, Hallett M. Inhibitory influence of the ipsilateral motor cortex on responses to stimulation of the human cortex and pyramidal tract.  J Physiol (Lond). 1998;  510 249-259
    CrossrefPubMedSearch in Google Scholar
  • 13 Hanajima R, Furubayashi T, Iwata N K, Shiio Y, Okabe S, Kanazawa I. et al . Further evidence to support different mechanisms underlying intracortical inhibition of the motor cortex.  Exp Brain Res. 2003;  151 427-434
    CrossrefPubMedSearch in Google Scholar
  • 14 Heinen F, Glocker F X, Fietzek U M, Meyer B-U, Lücking C H, Korinthenberg R. Absence of transcallosal inhibition following focal magnetic stimulation in pre-school children.  Ann Neurol. 1998;  43 608-612
    CrossrefPubMedSearch in Google Scholar
  • 15 Ilic T V, Meintzschel F, Cleff U, Ruge D, Kessler K R, Ziemann U. Short-interval paired-pulse inhibition and facilitation of human motor cortex: the dimension of stimulus intensity.  J Physiol. 2002;  545 153-167
    CrossrefPubMedSearch in Google Scholar
  • 16 Kujirai T, Caramia M D, Rothwell J C, Day B L, Thompson P D, Ferbert A. et al . Corticocortical inhibition in human motor cortex.  J Physiol (Lond). 1993;  471 501-519
    CrossrefPubMedSearch in Google Scholar
  • 17 Liepert J, Classen J, Cohen L G, Hallett M. Task-dependent changes of intracortical inhibition.  Exp Brain Res. 1998;  118 421-426
    CrossrefPubMedSearch in Google Scholar
  • 18 Maccabee P J, Amassian V E, Eberle L P, Cracco R Q. Magnetic coil stimulation of straight and bent amphibian and mammalian peripheral nerve in vitro: locus of excitation.  J Physiol. 1993;  460 201-219
    PubMedSearch in Google Scholar
  • 19 Moll G H, Heinrich H, Trott G E, Wirth S, Bock N, Rothenberger A. Children with comorbid attention-deficit-hyperactivity disorder and tic disorder: evidence for additive inhibitory deficits within the motor system.  Ann Neurol. 2001;  49 393-396
    CrossrefPubMedSearch in Google Scholar
  • 20 Müller K, Hömberg V. Development of speed of repetitive movements in children is determined by structural changes in corticospinal efferents.  Neurosci Letts. 1992;  144 57-60
    PubMedSearch in Google Scholar
  • 21 Müller K, Hömberg V, Aulich A, Lenard H-G. Magnetoelectrical stimulation of motor cortex in children with motor disturbances.  Electroencephalogr Clin Neurophysiol. 1992;  85 86-94
    PubMedSearch in Google Scholar
  • 22 Rossini P M, Barker A T, Berardelli A, Caramia M D, Caruso G, Cracco R Q. et al . Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee.  Electroencephalogr Clin Neurophysiol. 1994;  91 79-92
    PubMedSearch in Google Scholar
  • 23 Rothwell J C. The use of paired pulse stimulation to investigate the intrinsic circuitry of human motor cortex. Nilsson J, Panizza, Grandori F Advances in Magnetic Stimulation. Mathematical Modeling and Clinical Applications. Pavia; PI-ME Press 1996: 99-104
    Search in Google Scholar
  • 24 Shimizu T, Filippi M M, Almieri M G, Liveri M, Ernieri F, Asqualetti P. et al . Modulation of intracortical excitability for different muscles in the upper extremity: paired magnetic stimulation study with focal versus non-focal coils.  Clinical Neurophysiology. 1999;  110 575-581
    CrossrefPubMedSearch in Google Scholar
  • 25 Stefan K, Kunesch E, Benecke R, Cohen L G, Classen J. Mechanisms of enhancement of human motor cortex excitability induced by interventional paired associative stimulation.  J Physiol. 2002;  543 699-708
    CrossrefPubMedSearch in Google Scholar
  • 26 Stinear C M, Byblow W D. Role of intracortical inhibition in selective hand muscle activation.  J Neurophysiol. 2003;  89 2014-2020
    PubMedSearch in Google Scholar
  • 27 Zanette G F, Tamburin S FAU, Manganotti P, Manganotti P F, Refatti N F, Forgione A F, Rizzuto N. Changes in motor cortex inhibition over time in patients with amyotrophic lateral sclerosis.  J Neurol. 2002;  249 1723
    PubMedSearch in Google Scholar
  • 28 Ziemann U, Lönnecker S, Steinhoff B J, Paulus W. Effects of antiepileptic drugs on motor cortex excitability in humans: a transcranial magnetic stimulation study.  Ann Neurol. 1996;  40 367-378
    CrossrefPubMedSearch in Google Scholar
  • 29 Ziemann U, Lönnecker S, Steinhoff B J, Paulus W. The effect of lorazepam on the motor cortical excitability in man.  Exp Brain Res. 1996;  109 127-135
    PubMedSearch in Google Scholar
  • 30 Ziemann U, Muellbacher W, Hallett M, Cohen L G. Modulation of practice-dependent plasticity in human motor cortex.  Brain. 2001;  124 1171-1181
    CrossrefPubMedSearch in Google Scholar
  • 31 Ziemann U F, Tam A F, Butefisch C F, Cohen L G. Dual modulating effects of amphetamine on neuronal excitability and stimulation-induced plasticity in human motor cortex.  Clin Neurophysiol. 2002;  113 1308-1315
    CrossrefPubMedSearch in Google Scholar

M. D. Volker Mall

Department of Neuropediatrics and Muscular Disorders
Children's University Hospital

Mathildenstraße 1

79106 Freiburg

Germany

Email: mall@kikli.ukl.uni-freiburg.de