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Motor skill training induces changes in the excitability of the leg cortical area in healthy humans

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Abstract

Training-induced changes in cortical excitability may play an important role in rehabilitation of gait ability in patients with neurological disorders. In this study, we investigated the effect of a 32-min period of motor skill, non-skill and passive training involving the ankle muscles on leg motor cortical excitability in healthy humans. Transcranial magnetic stimulation (TMS) at a range of intensities was applied to obtain a recruitment curve of the motor evoked potentials (MEPs) in the tibialis anterior (TA) muscle before and after training. We also explored the effect of training on inhibitory and facilitatory cortical circuits by using a paired-pulse TMS technique at intervals of 2.5 ms (short-interval intracortical inhibition, SICI) and 8 ms (intracortical facilitation, ICF). During motor skill training, subjects were instructed to make a cursor follow a series of target lines on a computer screen by performing voluntary ankle dorsi- and plantarflexion movements. Non-skill and passive training consisted of repeated voluntary and assisted dorsi- and plantarflexion movements, respectively. Recruitment curves increased significantly after 32 min of motor skill training but not after non-skill and passive training, suggesting that only skill motor training increases motor cortical excitability. Motor skill training was not accompanied by any changes in the recruitment curves of TA MEPs evoked by transcranial electrical stimulation, suggesting that the increased MEPs to TMS was likely caused by changes in excitability at a cortical site. SICI was decreased after 32 min of motor skill training but no changes were observed in ICF. We conclude that similar plastic changes as have previously been reported for the hand motor following motor skill training may also be observed for the leg motor area. The observed plastic changes appeared to be related to the degree of difficulty in the motor task, and may be of relevance for rehabilitation of gait disorders.

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References

  • Armstrong DM (1988) The supraspinal control of mammalian locomotion. J Physiol 405:1–37

    CAS  PubMed  Google Scholar 

  • Brouwer B, Ashby P (1990) Corticospinal projections to upper and lower limb spinal motoneurons in man. Electroencephalogr Clin Neurophysiol 76:509–519

    Article  CAS  PubMed  Google Scholar 

  • Burke D, Hicks R, Gandevia SC, Stephen J, Woodforth I, Crawford M (1993) Direct comparison of corticospinal volleys in human subjects to transcranial magnetic and electrical stimulation. J Physiol 470:383–393. Erratum in: J Physiol (Lond) 1994 476:553

    Google Scholar 

  • Burridge JH, Wood DE, Taylor PN, McLellan DL (2001) Indices to describe different muscle activation patterns, identified during treadmill walking, in people with spastic drop-foot. Med Eng Phys 23:427–434

    Article  CAS  PubMed  Google Scholar 

  • Butefisch CM, Davis BC, Wise SP, Sawaki L, Kopylev L, Classen J, Cohen LG (2000) Mechanisms of use-dependent plasticity in the human motor cortex. Proc Natl Acad Sci USA 97:3661–3665

    Article  CAS  PubMed  Google Scholar 

  • Capaday C, Lavoie BA, Barbeau H, Schneider C, Bonnard M (1999) Studies on the corticospinal control of human walking. I. Responses to focal transcranial magnetic stimulation of the motor cortex. J Neurophysiol 81:129–139

    CAS  PubMed  Google Scholar 

  • Classen J, Liepert J, Wise SP, Hallett M, Cohen LG (1998) Rapid plasticity of human cortical movement representation induced by practice. J Neurophysiol 79:1117–1123

    CAS  PubMed  Google Scholar 

  • Classen J, Liepert J, Hallett M, Cohen L (1999) Plasticity of movement representation in the human motor cortex. Electroencephalogr Clin Neurophysiol Suppl 51:162–173

    CAS  PubMed  Google Scholar 

  • Day BL, Dressler D, Maertens de Noordhout A, Marsden CD, Nakashima K, Rothwell JC, Thompson PD (1989) Electric and magnetic stimulation of human motor cortex: surface EMG and single motor unit responses. J Physiol 412:449–73. Erratum in: J Physiol (Lond) 1990 430:617

    Google Scholar 

  • Di Lazzaro V, Oliviero A, Profice P, Meglio M, Cioni B, Tonali P, Rothwell JC (2001) Descending spinal cord volleys evoked by transcranial magnetic and electrical stimulation of the motor cortex leg area in conscious humans. J Physiol 537:1047–1058

    Article  PubMed  Google Scholar 

  • Drew T, Jiang W, Widajewicz W (2002) Contributions of the motor cortex to the control of the hindlimbs during locomotion in the cat. Brain Res Brain Res Rev 40:178–191

    Article  PubMed  Google Scholar 

  • Elbert T, Pantev C, Wienbruch C, Rockstroh B, Taub E (1995) Increased cortical representation of the fingers of the left hand in string players. Science 270:305–307

    CAS  PubMed  Google Scholar 

  • Fisher RJ, Nakamura Y, Bestmann S, Rothwell JC, Bostock H (2002) Two phases of intracortical inhibition revealed by transcranial magnetic threshold tracking. Exp Brain Res 143:240–248

    Article  CAS  PubMed  Google Scholar 

  • Hoffman DS, Strick PL (1995) Effects of a primary motor cortex lesion on step-tracking movements of the wrist. J Neurophysiol 73:891–895

    CAS  PubMed  Google Scholar 

  • Hund-Georgiadis M, von Cramon DY (1999) Motor-learning-related changes in piano players and non-musicians revealed by functional magnetic-resonance signals. Exp Brain Res 125:417–425

    Article  CAS  PubMed  Google Scholar 

  • Iles JF, Cummings R (1992) Electrical and magnetic stimulation of motor cortex in humans. J Physiol 452:287P

    Google Scholar 

  • Jacobs KM, Donoghue JP (1991) Reshaping the cortical motor map by unmasking latent intracortical connections. Science 251:944–947

    CAS  PubMed  Google Scholar 

  • Jankowska E, Padel Y, Tanaka R (1975) Projections of pyramidal tract cells to alpha-motoneurones innervating hind-limb muscles in the monkey. J Physiol 249:637–667

    CAS  PubMed  Google Scholar 

  • Karni A, Meyer G, Jezzard P, Adams MM, Turner R, Ungerleider LG (1995) Functional MRI evidence for adult motor cortex plasticity during motor skill learning. Nature 377:155–158

    Article  CAS  PubMed  Google Scholar 

  • Kleim JA, Lussnig E, Schwarz ER, Comery TA, Greenough WT (1996) Synaptogenesis and Fos expression in the motor cortex of the adult rat after motor skill learning. J Neurosci 16:4529–4535

    CAS  PubMed  Google Scholar 

  • Kleim JA, Barbay S, Nudo RJ (1998) Functional reorganization of the rat motor cortex following motor skill learning. J Neurophysiol 80:3321–3325

    CAS  PubMed  Google Scholar 

  • Kleim JA, Barbay S, Cooper NR, Hogg TM, Reidel CN, Remple MS, Nudo RJ (2002) Motor learning-dependent synaptogenesis is localized to functionally reorganized motor cortex. Neurobiol Learn Mem 77:63–77

    Article  PubMed  Google Scholar 

  • Kujirai T, Caramia MD, Rothwell JC, Day BL, Thompson PD, Ferbert A, Wroe S, Asselman P, Marsden CD (1993) Corticocortical inhibition in human motor cortex. J Physiol 471:501–519

    CAS  PubMed  Google Scholar 

  • Lech M, Skibinska A, Kossut M (2001) Delayed upregulation of GABA(A) alpha1 receptor subunit mRNA in somatosensory cortex of mice following learning-dependent plasticity of cortical representations. Brain Res Mol Brain Res 96:82–86

    Article  CAS  PubMed  Google Scholar 

  • Liepert J, Classen J, Cohen LG, Hallett M (1998) Task-dependent changes of intracortical inhibition. Exp Brain Res 118:421–426

    Article  CAS  PubMed  Google Scholar 

  • Lotze M, Braun C, Birbaumer N, Anders S, Cohen LG (2003) Motor learning elicited by voluntary drive. Brain 126:866–872

    Article  PubMed  Google Scholar 

  • Nielsen JB (2002) Motoneuronal drive during human walking. Brain Res Rev 40:192–201

    Article  PubMed  Google Scholar 

  • Nielsen J, Petersen N, Deuschl G, Ballegaard M (1993) Task-related changes in the effect of magnetic brain stimulation on spinal neurones in man. J Physiol 471:223–243

    CAS  PubMed  Google Scholar 

  • Nielsen J, Petersen N, Ballegaard M (1995) Latency of effects evoked by electrical and magnetic brain stimulation in lower limb motoneurones in man. J Physiol 484:791–802

    CAS  PubMed  Google Scholar 

  • Nordstrom MA, Butler SL (2002) Reduced intracortical inhibition and facilitation of corticospinal neurons in musicians. Exp Brain Res 144:336–342

    Article  PubMed  Google Scholar 

  • Nudo RJ (2003) Functional and structural plasticity in motor cortex: implications for stroke recovery. Phys Med Rehabil Clin N Am 14:57–76

    PubMed  Google Scholar 

  • Nudo RJ, Milliken GW, Jenkins WM, Merzenich MM (1996) Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys. J Neurosci 16:785–807

    CAS  PubMed  Google Scholar 

  • Pascual-Leone A, Grafman J, Hallett M (1994) Modulation of cortical motor output maps during development of implicit and explicit knowledge. Science 263:1287–1289

    CAS  PubMed  Google Scholar 

  • Pascual-Leone A, Nguyet D, Cohen LG, Brasil-Neto JP, Cammarota A, Hallett M (1995) Modulation of muscle responses evoked by transcranial magnetic stimulation during the acquisition of new fine motor skills. J Neurophysiol 74:1037–1045

    CAS  PubMed  Google Scholar 

  • Paz R, Boraud T, Natan C, Bergman H, Vaadia E (2003) Preparatory activity in motor cortex reflects learning of local visuomotor skills. Nat Neurosci 6:882–890

    Article  CAS  PubMed  Google Scholar 

  • Petersen N, Christensen LO, Nielsen J (1998) The effect of transcranial magnetic stimulation on the soleus H reflex during human walking. J Physiol 513:599–610

    CAS  PubMed  Google Scholar 

  • Petersen NT, Butler JE, Marchand-Pauvert V, Fisher R, Ledebt A, Pyndt HS, Hansen NL, Nielsen JB (2001) Suppression of EMG activity by transcranial magnetic stimulation in human subjects during walking. J Physiol 537:651–656

    CAS  PubMed  Google Scholar 

  • Petersen NT, Pyndt HS, Nielsen JB (2003) Investigating human motor control by transcranial magnetic stimulation. Exp Brain Res 152:1–16

    Article  PubMed  Google Scholar 

  • Priori A, Bertolasi L, Dressler D, Rothwell JC, Day BL, Thompson PD, Marsden CD (1993) Transcranial electric and magnetic stimulation of the leg area of the human motor cortex: single motor unit and surface EMG responses in the tibialis anterior muscle. Electroencephalogr Clin Neurophysiol 89:131–137

    Article  CAS  PubMed  Google Scholar 

  • Remple MS, Bruneau RM, VandenBerg PM, Goertzen C, Kleim JA (2001) Sensitivity of cortical movement representations to motor experience: evidence that skill learning but not strength training induces cortical reorganization. Behav Brain Res 123:133–141

    Article  CAS  PubMed  Google Scholar 

  • Ridding MC, Rothwell JC (1997) Stimulus/response curves as a method of measuring motor cortical excitability in man. Electroencephalogr Clin Neurophysiol 105:340–344

    Article  CAS  PubMed  Google Scholar 

  • Roche RA, O’Mara SM (2003) Behavioural and electrophysiological correlates of visuomotor learning during a visual search task. Brain Res Cogn Brain Res 15:127–136

    Article  PubMed  Google Scholar 

  • Rossini PM, Barker AT, Berardelli A, Caramia MD, Caruso G, Cracco RQ, Dimitrijevic MR, Hallett M, Katayama Y, Lucking CH, et al (1994) 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 91:79–92

    Article  CAS  PubMed  Google Scholar 

  • Rothwell JC (1991) Physiological studies of electric and magnetic stimulation of the human brain. Electroencephalogr Clin Neurophysiol 43:29–35

    CAS  PubMed  Google Scholar 

  • Schubert M, Curt A, Jensen L, Dietz V (1997) Corticospinal input in human gait: modulation of magnetically evoked motor responses. Exp Brain Res 115:234–246

    CAS  PubMed  Google Scholar 

  • Tinazzi M, Farina S, Tamburin S, Facchini S, Fiaschi A, Restivo D, Berardelli A (2003) Task-dependent modulation of excitatory and inhibitory functions within the human primary motor cortex. Exp Brain Res 150:222–229

    PubMed  Google Scholar 

  • Toner LV, Cook K, Elder GC (1998) Improved ankle function in children with cerebral palsy after computer-assisted motor learning. Dev Med Child Neurol 40:829–835

    CAS  PubMed  Google Scholar 

  • Uy J, Ridding MC, Hillier S, Thompson PD, Miles TS (2003) Does induction of plastic change in motor cortex improve leg function after stroke? Neurology 61:982–984

    CAS  PubMed  Google Scholar 

  • VandenBerg PM, Hogg TM, Kleim JA, Whishaw IQ (2002) Long-Evans rats have a larger cortical topographic representation of movement than Fischer-344 rats: a microstimulation study of motor cortex in naive and skilled reaching-trained rats. Brain Res Bull 59:197–203

    Article  PubMed  Google Scholar 

  • Winter DA, Bishop PJ (1992) Lower extremity injury. Biomechanical factors associated with chronic injury to the lower extremity. Sports Med 14:149–156

    CAS  PubMed  Google Scholar 

  • Ziemann U, Rothwell JC, Ridding MC (1996) Interaction between intracortical inhibition and facilitation in human motor cortex. J Physiol 496:873–881

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors are very grateful to Torill Bjugan, Dinah Merklin and Lene Østerby for their help during this study. This work was supported by grants from the Danish Health Research Council, The Danish Society of Multiple Sclerosis, The Novo Nordisk Foundation and The Danish Ministry of Culture.

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Correspondence to Jens B. Nielsen.

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Perez, M.A., Lungholt, B.K.S., Nyborg, K. et al. Motor skill training induces changes in the excitability of the leg cortical area in healthy humans. Exp Brain Res 159, 197–205 (2004). https://doi.org/10.1007/s00221-004-1947-5

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