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
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
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
4
Brooks-Kayal A R, Pritchett D B.
Developmental changes in human gamma-aminobutyric acidA receptor subunit composition.
Ann Neurol.
1993;
34
687-693
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
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
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
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
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
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
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
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
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
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
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
17
Liepert J, Classen J, Cohen L G, Hallett M.
Task-dependent changes of intracortical inhibition.
Exp Brain Res.
1998;
118
421-426
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
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
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
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
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
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
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
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
26
Stinear C M, Byblow W D.
Role of intracortical inhibition in selective hand muscle activation.
J Neurophysiol.
2003;
89
2014-2020
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
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
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
30
Ziemann U, Muellbacher W, Hallett M, Cohen L G.
Modulation of practice-dependent plasticity in human motor cortex.
Brain.
2001;
124
1171-1181
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
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