Skip to main content

The corticospinal responses of metronome-paced, but not self-paced strength training are similar to motor skill training

European Journal of Applied Physiology volume 117, pages 2479–2492 (2017)Cite this article

Abstract

Purpose

The corticospinal responses to skill training may be different to strength training, depending on how the strength training is performed. It was hypothesised that the corticospinal responses would not be different following skill training and metronome-paced strength training (MPST), but would differ when compared with self-paced strength training (SPST).

Methods

Corticospinal excitability, short-interval intra-cortical inhibition (SICI) and strength and tracking error were measured at baseline and 2 and 4 weeks. Participants (n = 44) were randomly allocated to visuomotor tracking, MPST, SPST or a control group.

Results

MPST increased strength by 7 and 18%, whilst SPST increased strength by 12 and 26% following 2 and 4 weeks of strength training. There were no changes in strength following skill training. Skill training reduced tracking error by 47 and 58% at 2 and 4 weeks. There were no changes in tracking error following SPST; however, tracking error reduced by 24% following 4 weeks of MPST. Corticospinal excitability increased by 40% following MPST and by 29% following skill training. There was no change in corticospinal excitability following 4 weeks of SPST. Importantly, the magnitude of change between skill training and MPST was not different. SICI decreased by 41 and 61% following 2 and 4 weeks of MPST, whilst SICI decreased by 41 and 33% following 2 and 4 weeks of skill training. Again, SPST had no effect on SICI at 2 and 4 weeks. There was no difference in the magnitude of SICI reduction between skill training and MPST.

Conclusions

This study adds new knowledge regarding the corticospinal responses to skill and MPST, showing they are similar but different when compared with SPST.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Abbreviations

1-RM:

One-repetition maximum

AURC:

Area under the recruitment curve

AMT:

Active motor threshold

CNS:

Central nervous system

EMG:

Electromyography

GABA:

γ-Aminobutyric acid

FDI:

First dorsal interosseous

MMAX :

Maximum compound wave

MEPs:

Motor-evoked potentials

MPST:

Metronome-paced strength training

MVIC:

Maximal voluntary isometric contraction

M1:

Primary motor cortex

rmsEMG:

Root-mean square electromyography

SPST:

Self-paced strength training

SICI:

Short-interval cortical inhibition

TMS:

Transcranial magnetic stimulation

References

  • Ackerley SJ, Stinear CM, Byblow WD (2007) The effect of coordination mode on use-dependent plasticity. Clin Neurophysiol 118(8):1759–1766

    PubMed  Google Scholar 

  • Ackerley SJ, Stinear CM, Byblow WD (2011) Promoting use-dependent plasticity with externally-paced training. Clin Neurophysiol 122(12):2462–2468

    PubMed  Google Scholar 

  • Adkins DL, Boychuk J, Remple MS, Kleim JA (2006) Motor training induces experience-specific patterns of plasticity across motor cortex and spinal cord. J Appl Physiol 101:1176–1782

    Google Scholar 

  • Beck S, Taube W, Gruber M, Amtage F, Gollhofer A, Schubert M (2007) Task-specific changes in motor evoked potentials of lower limb muscles after different training interventions. Brain Res 1179:(51–60)

    CAS  PubMed  Google Scholar 

  • Borich M, Furlong M, Holsman D, Kimberley TJ (2011) Goal-directed visuomotor skill learning: off-line enhancement and the importance of the primary motor cortex. Restor Neurol Neurosci 29(2):105–113

    PubMed  PubMed Central  Google Scholar 

  • Boudreau SA, Lontis ER, Caltenco H, Svensson P, Sessle BJ, Andreasen Struijk LN, Arendt-Nielsen L (2013) Features of cortical neuroplasticity associated with multidirectional novel motor skill training: a TMS mapping study. Exp Brain Res 225(4):513–526

    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(7):3661–3665

    CAS  PubMed  Google Scholar 

  • Camus M, Ragert P, Vandermeeren Y, Cohen LG (2009) Mechanisms controlling motor output to a transfer hand after learning a sequential pinch force skill with the opposite hand. Clin Neurophysiol 120(10):1859–1865

    PubMed  Google Scholar 

  • Carey JR, Greer KR, Grunewald TK, Steele JL, Wiemiller JW, Bhatt E, Nagpal A, Lungu O, Auerbach EJ (2006) Primary motor area activation during precision-demanding versus simple finger movement. Neurorehabil Neural Repair 20(3):361–370

    PubMed  Google Scholar 

  • Carroll T, Riek S, Carson R (2002) The sites of neural adaptation induced by resistance training in humans. J Physiol 544(2):641–652

    CAS  PubMed  PubMed Central  Google Scholar 

  • Carroll TJ, Poh E, de Rugy A (2014) New visuomotor maps are immediately available to the opposite limb. J Neurophysiol 111(11):2232–2243

    PubMed  Google Scholar 

  • Carson RG, Nelson BD, Buick AR, Carroll TJ, Kennedy NC, Cann RM (2013) Characterizing changes in the excitability of corticospinal projections to proximal muscles of the upper limb. Brain Stimul 6(5):760–768

    PubMed  Google Scholar 

  • Christie A, Kamen G (2014) Cortical inhibition is reduced following short-term training in young and older adults. Age (Dordrecht Netherlands) 36(2):749–758

    Google Scholar 

  • Cirillo J, Todd G, Semmler JG (2011) Corticomotor excitability and plasticity following complex visuomotor training in young and old adults. Eur J Neurosci 34(11):1847–1856

    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(2):1117–1123

    CAS  PubMed  Google Scholar 

  • Coombs TA, Frazer AK, Horvath DM, Pearce AJ, Howatson G, Kidgell DJ (2016) Cross-education of wrist extensor strength is not influenced by non-dominant training in right-handers. Eur J Appl Physiol 116(9):1757–1769

    PubMed  Google Scholar 

  • Coxon JP, Peat NM, Byblow WD (2014) Primary motor cortex disinhibition during motor skill learning. J Neurophysiol 112(1):156–164

    PubMed  Google Scholar 

  • Dayan E, Cohen LG (2011) Neuroplasticity subserving motor skill learning. Neuron 72(3):443–454

    CAS  PubMed  PubMed Central  Google Scholar 

  • Deiber M, Ibanez V, Honda M, Sadato N, Raman R, Hallett M (1998) Cerebral processes related to visuomotor imagery and generation of simple finger movements studied with positron emission tomography. Neuroimage 2:73–85

    Google Scholar 

  • Gallasch E, Christova M, Krenn M, Kossev A, Rafolt D (2009) Changes in motor cortex excitability following training of a novel goal-directed motor task. Eur J Appl Physiol 105(1):47–54

    PubMed  Google Scholar 

  • Gentner R, Gorges S, Weise D, aufm Kampe K, Buttmann M, Classen J (2010) Encoding of motor skill in the corticomuscular system of musicians. Curr Biol 20(20):1869–1874

    CAS  PubMed  Google Scholar 

  • Gerloff C, Corwell B, Chen R, Hallett M, Cohen LG (1998a) The role of the human motor cortex in the control of complex and simple finger movement sequences. Brain 121(Pt 9):1695–1709

    PubMed  Google Scholar 

  • Gerloff C, Richard J, Hadley J, Schulman AE, Honda M, Hallett M (1998b) Functional coupling and regional activation of human cortical motor areas during simple, internally paced and externally paced finger movements. Brain 121(Pt 8):1513–1531

    PubMed  Google Scholar 

  • Gobel E, Parrish T, Reber P (2011) Neural correlates of skill acquisition: decreased cortical activity during a serial interception sequence learning task. Neuroimage 58:1150–1157

    PubMed  PubMed Central  Google Scholar 

  • Goodwill AM, Pearce AJ, Kidgell DJ (2012) Corticomotor plasticity following unilateral strength training. Muscle Nerve 46(3):384–393

    PubMed  Google Scholar 

  • Gorsler A, Zittel S, Weiller C, Munchau A, Liepert J (2004) Modulation of motor cortex excitability induced by pinch grip repetition. J Neural Transm 111:1005–1016

    CAS  PubMed  Google Scholar 

  • Griffin L, Cafarelli E (2007) Transcranial magnetic stimulation during resistance training of the tibialis anterior msucle. J Electromyogr Kinesiol 17:446–452

    CAS  PubMed  Google Scholar 

  • Halsband U, Lange R (2006) Motor learning in man: a review of functional and clinical studies. J Physiol Paris 2006:414–424

  • Hendy AM, Kidgell DJ (2014) Anodal-tDCS applied during unilateral strength training increases strength and corticospinal excitability in the untrained homologous muscle. Exp Brain Res 232(10):3243–3252

    PubMed  Google Scholar 

  • Hinder MR, Carroll TJ, Summers JJ (2013) Inter-limb transfer of ballistic motor skill following non-dominant limb training in young and older adults. Exp Brain Res 227(1):19–29

    PubMed  Google Scholar 

  • Hortobagyi T, Lambert NJ, Hill JP (1997) Greater cross education following training with muscle lengthening than shortening. Med Sci Sports Exerc 29(1):107–112

    CAS  PubMed  Google Scholar 

  • Hyde KL, Lerch J, Norton A, Forgeard M, Winner E, Evans AC, Schlaug G (2009) Musical training shapes structural brain development. J Neurosci 10:3019–3025

    Google Scholar 

  • Jelic MB, Stevanovic VB, Milanovic SD, Ljubisavljevic MR, Filipovic SR (2013) Transcranial magnetic stimulation has no placebo effect on motor learning. Clin Neurophysiol 124:1646–1651

  • Jensen JL, Marstrand PC, Nielsen JB (2005) Motor skill training and strength training are associated with different plastic changes in the central nervous system. J Appl Physiol (1985) 99:1558–1568

    PubMed  Google Scholar 

  • Kidgell DJ, Pearce AJ (2010) Corticospinal properties following short-term strength training of an intrinsic hand muscle. Hum Mov Sci 29:631–641

    PubMed  Google Scholar 

  • Kidgell DJ, Stokes MA, Castricum TJ, Pearce AJ (2010) Neurophysiological responses after short-term strength training of the biceps brachii muscle. J Strength Cond Res 24(11):3123–3132

    PubMed  Google Scholar 

  • Kidgell DJ, Stokes M, Pearce AJ (2011) Strength training of one limb increases corticomotor excitability projecting to the contralateral homologous limb. Motor Control 15:247–266

    PubMed  Google Scholar 

  • Kidgell DJ, Frazer AK, Rantalainen T, Ruotsalainen I, Ahtiainen J, Avela J, Howatson G (2015) Increased cross-education of muscle strength and reduced corticospinal inhibition following eccentric strength training. Neuroscience 300:566–575

    CAS  PubMed  Google Scholar 

  • Kouchtir-Devanne N, Capaday C, Cassim F, Derambure P, Devanne H (2012) Task-dependent changes of motor cortical network excitability during precision grip compared to isolated finger contraction. J Neurophysiol 107(5):1522–1529

    PubMed  Google Scholar 

  • Krakauer J (2009) Motor learning and consolidation: the case of visuomotor rotation. Adv Exp Med Biol 629:405–421

    PubMed  PubMed Central  Google Scholar 

  • Latella C, Kidgell DJ, Pearce AJ (2011) Reduction in corticospinal inhibition in the trained and untrained limb following unilateral leg strength training. Eur J Appl Physiol (Epub ahead of print)

  • Lee M, Gandevia SC, Carroll T (2009) Short-term strength training does not change cortical voluntary activation. Med Sci Sports Exerc 41:1452–1460

    PubMed  Google Scholar 

  • Lee M, Hinder MR, Gandevia SC, Carroll TJ (2010) The ipsilateral motor cortex contributes to cross-limb transfer of performance gains after ballistic motor practice. J Physiol 588(1):201–212

    CAS  PubMed  Google Scholar 

  • Lemon RN (2008) Descending pathways in motor control. Annu Rev Neurosci 31:195–218

    CAS  PubMed  Google Scholar 

  • Leung M, Rantalainen T, Teo WP, Kidgell D (2015) Motor cortex excitability is not differentially modulated following skill and strength training. Neuroscience 305:99–108

    CAS  PubMed  Google Scholar 

  • Manca A, Ginatempo F, Cabboi MP, Mercante B, Ortu E, Dragone D, De Natale ER, Dvir Z, Rothwell JC, Deriu F (2016) No evidence of neural adaptations following chronic unilateral isometric training of the intrinsic muscles of the hand: a randomized controlled study. Eur J Appl Physiol 116(10):1993–2005

    CAS  PubMed  Google Scholar 

  • Mason J, Frazer K, Horvath D, Pearce A, Avela J, Howatson G, Kidgell (2017) Adaptations in corticospinal excitability and inhibition are not spatially confined to the agonist muscle following strength training. Euro J Appl Physiol 117:1359–1371

    CAS  Google Scholar 

  • Muellbacher W, Ziemann U, Boroojerdi B, Cohen L, Hallett M (2001) Role of the human motor cortex in rapid motor learning. Exp Brain Res 136(4):431–438

    CAS  PubMed  Google Scholar 

  • Nuzzo JL, Barry BK, Gandevia SC, Taylor JL (2016) Acute strength training increases responses to stimulation of corticospinal axons. Med Sci Sports Exerc 48(1):139–150

    PubMed  Google Scholar 

  • Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9(1):97–113

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pascual-Leone A, Torres F (1993) Plasticity of the sensorimotor cortex representation of the reading finger in Braille readers. Brain 116(Pt 1):39–52

    PubMed  Google Scholar 

  • Pascual-Leone A, Bguyet D, Cohen L, Brasil-Net J, 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 

  • Pascual-Leone A, Tarazona F, Catala MD (1999) Applications of transcranial magnetic stimulation in studies on motor learning. Electroencephalogr Clin Neurophysiol Suppl 51:157–161

    CAS  PubMed  Google Scholar 

  • Pearce AJ, Kidgell DJ (2010) Comparison of corticomotor excitability during visuomotor dynamic and static tasks. J Sci Med Sport 13(1):167–171

    PubMed  Google Scholar 

  • Pearce AJ, Hendy A, Bowen WA, Kidgell DJ (2013) Corticospinal adaptations and strength maintenance in the immobilized arm following 3 weeks unilateral strength training. Scand J Med Sci Sports 23(6):740–748

    CAS  PubMed  Google Scholar 

  • Perez MA, Cohen LG (2008) Mechanisms underlying functional changes in the primary motor cortex ipsilateral to an active hand. J Neurosci 28(22):5631–5640

    CAS  PubMed  PubMed Central  Google Scholar 

  • Perez M, Cohen L (2009) Interhemispheric inhibtion between primary motor cortices: What have we learned? J Physiol 587(4):725–726

    CAS  PubMed  PubMed Central  Google Scholar 

  • Perez MA, Lungholt BK, Nyborg K, Nielsen JB (2004) Motor skill training induces changes in the excitability of the leg cortical area in healthy humans. Exp Brain Res 159(2):197–205

    PubMed  Google Scholar 

  • Perez M, Lundbye-Jensen J, Nielsen J (2006) Changes in corticospinal drive to spinal motoneurones following visuomotor skill learning in humans. J Physiol 573:843–855

    CAS  PubMed  PubMed Central  Google Scholar 

  • Plautz EJ, Milliken GW, Nudo RJ (2000) Effects of repetitive motor training on movement representations in adult squirrel monkeys: role of use versus learning. Neurobiol Learn Mem 74(1):27–55

    CAS  PubMed  Google Scholar 

  • Plow EB, Carey JR (2012) Pilot fMRI investigation of representational plasticity associated with motor skill learning and its functional consequences. Brain Imaging Behav 6(3):437–453

    PubMed  PubMed Central  Google Scholar 

  • Poh E, Wallis G, Riek S, de Rugy A, Carroll T Visuomotor adaptation generalizes partially according to an eye-centred coordinate frame. Frontiers in Human Neuroscience

  • Rogasch NC, Dartnall TJ, Cirillo J, Nordstrom MA, Semmler JG (2009) Corticomotor plasticity and learning of a ballistic thumb training task are diminished in older adults. J Appl Physiol (1985) 107(6):1874–1883

    PubMed  Google Scholar 

  • Rothwell JC, Hallett M, Berardelli A, Eisen A, Rossini PM, Paulus W (1999) Magnetic stimulation: motor evoked potentials. Electroencephalogr Clin Neurophysiol 52:97–103

    CAS  Google Scholar 

  • Sanes JN (2000) Motor cortex rules for learning and memory. Curr Biol 10(13):R495-497

    Google Scholar 

  • Sanes JN, Donoghue JP (2000) Plasticity and primary motor cortex. Annu Rev Neurosci 23:393–415

    CAS  PubMed  Google Scholar 

  • Smyth C, Summers JJ, Garry MI (2010) Differences in motor learning success are associated with differences in M1 excitability. Hum Mov Sci 29(5):618–630

    PubMed  Google Scholar 

  • Talelli P, Ewas A, Waddingham W, Rothwell JC, Ward NS (2008) Neural correlates of age-related changes in cortical neurophysiology. Neuroimage 40(4):1772–1781

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tanaka S, Honda M, Hanakawa T, Cohen LG (2010) Differential contribution of the supplementary motor area to stabilization of a procedural motor skill acquired through different practice schedules. Cereb Cortex 20(9):2114–2121

    PubMed  Google Scholar 

  • Thaut MH, Kenyon GP, Hurt CP, McIntosh GC, Hoemberg V (2002) Kinematic optimization of spatiotemporal patterns in paretic arm training with stroke patients. Neuropsychologia 40(7):1073–1081

    CAS  PubMed  Google Scholar 

  • Tinazzi M, Zanette G (1998) Modulation of ipsilateral motor cortex in man during unimanual finger movements of different complexities. Neurosci Lett 244(3):121–124

    CAS  PubMed  Google Scholar 

  • Weier AT, Pearce AJ, Kidgell DJ (2012) Strength training reduces intracortical inhibition. Acta Physiol 206(2):109–119

    CAS  Google Scholar 

  • Yue G, Cole K (1992) Strength increases from the motor program: comparison of training with maximal voluntary and imagined muscle contractions. J Neurophysiol 67(5):1114–1123

    CAS  PubMed  Google Scholar 

  • Ziemann U, Muellbacher W, Hallett M, Cohen LG (2001) Modulation of practice-dependent plasticity in human motor cortex. Brain 124(Pt 6):1171–1181

    CAS  PubMed  Google Scholar 

  • Zimerman M, Nitsch M, Giraux P, Gerloff C, Cohen LG, Hummel FC (2013) Neuroenhancement of the aging brain: restoring skill acquisition in old subjects. Ann Neurol 73(1):10–15

    PubMed  Google Scholar 

  • Zoghi M, Nordstrom MA (2007) Progressive suppression of intracortical inhibition during graded isometric contraction of a hand muscle is not influenced by hand preference. Exp Brain Res 177(2):266–274

    PubMed  Google Scholar 

  • Zoghi M, Pearce S, Nordstrom MA (2003) Differential modulation of intracortical inhibtion in human motor cortex during selective activation of an intrinsic hand muscle. J Physiol 550(3):933–946

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This research did not receive any specific grant from funding agencies in the public, commercial or not-for-profit sectors.

Author information

Affiliations

  1. Institute for Physical Activity and Nutrition, School of Exercise and Nutrition Sciences, Deakin University, Melbourne, Australia

    Michael Leung, Timo Rantalainen & Wei-Peng Teo

  2. Department of Physiotherapy, Faculty of Medicine, Nursing and Health Sciences, School of Primary and Allied Health Care, Monash University, Melbourne, Australia

    Dawson Kidgell

Authors
  1. Michael Leung
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Timo Rantalainen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wei-Peng Teo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dawson Kidgell
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dawson Kidgell.

Ethics declarations

Conflict of interest

None of the authors have potential conflicts of interest to be disclosed.

Additional information

Communicated by Toshio Moritani.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Leung, M., Rantalainen, T., Teo, WP. et al. The corticospinal responses of metronome-paced, but not self-paced strength training are similar to motor skill training. Eur J Appl Physiol 117, 2479–2492 (2017). https://doi.org/10.1007/s00421-017-3736-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00421-017-3736-4

Keywords

  • Corticospinal excitability
  • Intra-cortical inhibition
  • Primary motor cortex
  • Strength training
  • Skill straining
  • Voluntary strength