Skip to main content
Log in

The ipsilateral corticospinal responses to cross-education are dependent upon the motor-training intervention

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

This study aimed to identify the ipsilateral corticospinal responses of the contralateral limb following different types of unilateral motor-training. Three groups performing unilateral slow-paced strength training (SPST), non-paced strength training (NPST) or visuomotor skill training (VT) were compared to a control group. It was hypothesised that 4 weeks of unilateral SPST and VT, but not NPST, would increase ipsilateral corticospinal excitability (CSE) and reduce short-interval cortical inhibition (SICI), resulting in greater performance gains of the untrained limb. Tracking error of the untrained limb reduced by 29 and 41% following 2 and 4 weeks of VT. Strength of the untrained limb increased by 8 and 16% following 2 and 4 weeks of SPST and by 6 and 13% following NPST. There was no difference in cross-education of strength or tracking error. For the trained limb, SPST and NPST increased strength (28 and 26%), and VT improved by 47 and 58%. SPST and VT increased ipsilateral CSE by 89 and 71% at 2 weeks. Ipsilateral CSE increased 105 and 81% at 4 weeks following SPST and VT. The NPST group and control group showed no changes at 2 and 4 weeks. SPST and VT reduced ipsilateral SICI by 45 and 47% at 2 weeks; at 4 weeks, SPST and VT reduced SICI by 48 and 38%. The ipsilateral corticospinal responses are determined by the type of motor-training. There were no differences in motor performance between SPST, NPST and VT. The data suggests that the corticospinal responses to cross-education are different and determined by the type of motor-training.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Ackerley S, Stinear C, Byblow W (2011) Promoting use-dependent plasticity with externally-paced training. Clin Neurophysiol 122:2462–2468

    Article  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 101:1776–1782

    Article  PubMed  Google Scholar 

  • Bestmann S, Krakauer JW (2015) The uses and interpretations of the motor-evoked potential for understanding behaviour. Exp Brain Res 2015:1e11

    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  PubMed Central  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carroll TJ, Herbert RD, Munn J, Lee M, Gandevia SC (2006) Contralateral effects of unilateral strength training: evidence and possible mechanisms. J Appl Physiol 101:1514–1522

    Article  PubMed  Google Scholar 

  • Carroll T, Lee M, Hsu M, Sayde J (2008) Unilateral practice of a ballistic movement causes bilateral increases in performance and corticospinal excitability. J Appl Physiol 104:1656–1664

    Article  PubMed  Google Scholar 

  • Christiansen L, Larsen MN, Grey MJ, Nielsen JB, Lundbye-Jensen J (2017) Long-term progressive motor skill training enhances corticospinal excitability for the ipsilateral hemisphere and motor performance of the untrained hand. Eur J Neurosci 45:1490–1500

    Article  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 116:1757–1769

    Article  PubMed  Google Scholar 

  • Criscimagna-Hemminger SE, Donchin O, Gazzaniga MS, Shadmehr R (2003) Learned dynamics of reaching movements generalize from dominant to nondominant arm. J Neurophysiol 89:168–176

    Article  PubMed  Google Scholar 

  • Doyon J, Benali H (2005) Reorganization and plasticity in the adult brain during learning of motor skills. Curr Opin Neurobiol 15:161–167

    Article  CAS  PubMed  Google Scholar 

  • Farthing J (2009) Cross-education of strength depends on limb dominance: Implications for theory and application. Exerc Sport Sci Rev 37:179–187

    PubMed  Google Scholar 

  • Farthing J, Zehr P (2014) Restoring symmetry: clinical applications of cross-education. Exerc Sport Sci Rev 42:70–75

    Article  PubMed  Google Scholar 

  • Farthing JP, Borowsky R, Chilibeck P, Binsted G, Sarty G (2007) Neuro-physiological adaptations associated with cross-education of strength. Brain Topogr 20:77–88

    Article  PubMed  Google Scholar 

  • Fimland M, Helgerud J, Solstad GM, Iversen VM, Leivseth G, Hoff J (2009) Neural adaptations underlying cross-education after unilateral strength training. Eur J Appl Physiol 107:723–730

    Article  PubMed  Google Scholar 

  • Frazer AK, Williams J, Spittle M, Kidgell DJ (2017) Cross-education of muscular strength is facilitated by homeostatic plasticity. Eur J Appl Physiol 117:665–677

    Article  PubMed  Google Scholar 

  • Fu QG, Flament D, Coltz JD, Ebner TJ (1995) Temporal encoding of movement kinematics in the discharge of primate primary motor and premotor neurons. J Neurophysiol 73:836–854

    Article  CAS  PubMed  Google Scholar 

  • Garry M, Loftus A, Summers JJ (2005) Mirror, mirror on the wall: viewing a mirror reflection of unilateral hand movements facilitates ipsilateral M1 excitability. Exp Brain Res 163:118–122

    Article  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

    Article  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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Grafton ST, Hazeltine E, Ivry RB (2002) Motor sequence learning with the nondominant left hand. Exp Brain Res 146:369–378

    Article  PubMed  Google Scholar 

  • Hardwick RM, Rottschy C, Miall RC, Eickhoff SB (2013) A quantitative meta-analysis and review of motor learning in the human brain. Neuroimage 67:283–297

    Article  PubMed  PubMed Central  Google Scholar 

  • Hellebrandt F (1951) Cross education: ipsilateral and contralateral effects of unimanual training. J Appl Physiol 4:136–144

    Article  CAS  PubMed  Google Scholar 

  • 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 232:3243–3252

    Article  PubMed  Google Scholar 

  • Hendy AM, Spittles M, Kidgell DJ (2012) Cross education and immobilisation: Mechanisms and implications for injury rehabilitation. J Sci Med Sport 15:94–101

    Article  PubMed  Google Scholar 

  • Hendy AM, Teo WP, Kidgell DJ (2015) Anodal tDCS prolongs the cross-education of strength and corticomotor plasticity. Med Sci Sports Exerc 47:1788–1797

    Article  PubMed  Google Scholar 

  • Heyes C (2010) Where do mirror neurons come from? Neurosci Biobehav Rev 34:575–583

    Article  PubMed  Google Scholar 

  • Hinder MR, Schmidt MW, Garry MI, Carroll TJ, Summers JJ (2011) Absence of cross-limb transfer of performance gains following ballistic motor practice in older adults. J Appl Physiol 110:166–175

    Article  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 227:19–29

    Article  PubMed  Google Scholar 

  • Hortobágyi T, Taylor JL, Petersen NT, Russell G, Gandevia SC (2003) Changes in segmental and motor cortical output with contralateral muscle contractions and altered sensory inputs in humans. J Neurophysiol 90:2451–2459

    Article  PubMed  Google Scholar 

  • Hortobágyi T, Richardson SP, Lomarev M, Shamim E, Meunier S, Russman H, Dang N, Hallett M (2011) Interhemispheric plasticity in humans. Med Sci Sports Exerc 43:1188–1199

    Article  PubMed  PubMed Central  Google Scholar 

  • Howatson G, Taylor MB, Rider P, Motawar BR, McNally MP, Solnik S, DeVita P, Hortobágyi T (2011) Ipsilateral motor cortical responses to TMS during lengthening and shortening of the contralateral wrist flexors. Eur J Neurosci 33:978–990

    Article  PubMed  PubMed Central  Google Scholar 

  • Howatson G, Zult T, Farthing JP, Zijdewind I, Hortobagyi T (2013) Mirror training to augment cross-education during resistance training: a hypothesis. Front Hum Neurosci 7:396

    Article  PubMed  PubMed Central  Google Scholar 

  • Iacoboni M (2005) Neural mechanisms of imitation. Curr Opin Neurobiol 15:632–637

    Article  CAS  PubMed  Google Scholar 

  • Kermadi Y (2000) Do bimanual motor actions involve the dorsal premotor (PMd), cingulate (CMA) and posterior parietal (PPC) cortices? Comparison with primary and supplementary motor cortical areas. Somatosens Mot Res 17:255–271

    Article  CAS  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 24:3123–3132

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Kidgell DJ, Daly RM, Young K, Lum J, Tooley G, Jaberzadeh S, Zoghi M, Paerce A (2013) Different current intensities of anodal transcranial direct current stimulation do not differentially modulate motor cortex plasticity. Neural Plast 2013:603502

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  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

    Article  CAS  PubMed  Google Scholar 

  • Koeneke S, Lutz K, Wüstenberg T, Jäncke L (2004) Bimanual versus unimanual coordination: what makes the difference? NeuroImage 22:1336–1350

    Article  PubMed  Google Scholar 

  • Lagerquist O, Zehr EP, Docherty D (2006) Increased spinal reflex excitability is not associated with neural plasticity underlying the cross-education effect. J Appl Physiol 100:83–90

    Article  PubMed  Google Scholar 

  • Latella C, Kidgell DJ, Pearce AJ (2012) Reduction in corticospinal inhibition in the trained and untrained limb following unilateral leg strength training. Eur J Appl Physiol 112:3097–3107

    Article  PubMed  Google Scholar 

  • Lee M, Gandevia SC, Carroll TJ (2009) Unilateral strength training increases voluntary activation of the opposite untrained limb. Clin Neurophysiol 120:802–808

    Article  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 588:201–212

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Leung M, Rantalainen T, Teo WP, Kidgell DJ (2017) 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

    Article  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 

  • Liepert J, Dettmers C, Terborg C, Weiller C (2001) Inhibition of ipsilateral motor cortex during phasic generation of low force. Clin Neurophysiol 112:114–121

    Article  CAS  PubMed  Google Scholar 

  • Manca A, Pisanu F, Ortu E, De Natale ER, Ginatempo F, Dragone D, Tolu E, Deriu F (2015) A comprehensive assessment of the cross-training effect in ankle dorsiflexors of healthy subjects: a randomized controlled study. Gait Posture 42:1–6

    Article  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 116:1993–2005

    Article  CAS  PubMed  Google Scholar 

  • Manca A, Dragone D, Dvir Z, Deriu F (2017) Cross-education of muscular strength following unilateral resistance training: a meta-analysis. Eur J Appl Physiol 117:2335–2354

    Article  CAS  PubMed  Google Scholar 

  • Mason J, Frazer K, Horvath D, Pearce A, Avela J, Howatson G, Kidgell (2017) Ipsilateral corticomotor responses are confined to the homologous muscle following cross-education of muscular strength. Appl Physiol Nut Metab. https://doi.org/10.1139/apnm-2017-0457

    Google Scholar 

  • Muellbacher W, Facchini S, Boroojerdi B, Hallett M (2000) Changes in motor cortex excitability during ipsilateral hand muscle activation in humans. Clin Neurophysiol 111:344–349

    Article  CAS  PubMed  Google Scholar 

  • Muellbacher W, Ziemann U, Wissel J, Dang N, Kofler M, Facchini S, Boroojerdi B, Poewe W, Hallett M (2002) Early consolidation in human primary motor cortex. Nature 415:640–644

    Article  CAS  PubMed  Google Scholar 

  • Nuzzo JL, Barry BK, Jones M, Gandevia SC, Taylor JL (2017) Effects of 4 weeks of strength training on the corticomotoneuronal pathway. Med Sci Sports Exerc 49:2286–2296

    Article  PubMed  Google Scholar 

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

    Article  CAS  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

    Article  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 28:5631–5640

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perez MA, Lundbye-Jensen J, Nielsen JB (2007) Task-specific depression of the soleus H-reflex after cococontraction training of antagonistic ankle muscles. J Neurophysiol 98:3677–3687

    Article  PubMed  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 74:27–55

    Article  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 6:437–453

    Article  PubMed  PubMed Central  Google Scholar 

  • Pruitt DT, Schmid AN, Danaphongse TT, Flanagan KE, Morrison RA, Kilgard MP, Rennaker RL, Hays SA (2016) Forelimb training drives transient map reorganization in ipsilateral motor cortex. Behav Br Res 313:10–16

    Article  Google Scholar 

  • Ray E, Heyes C (2011) Imitation in infancy: the wealth of the stimulus. Dev Sci 14:92–105

    Article  PubMed  Google Scholar 

  • Rizzolatti G, Craighero L (2004) The mirror-neuron system. Annu Rev Neurosci 27:169–192

    Article  CAS  PubMed  Google Scholar 

  • Rizzolatti G, Fadiga L, Fogassi L, Gallese V (1999) Resonance behaviors and mirror neurons. Arch Ital Biol 137:85–100

    CAS  PubMed  Google Scholar 

  • Rothwell JC, Day BL, Thompson PD, Kujirai T (2009) Short latency intracortical inhibition: one of the most popular tools in human motor neurophysiology. J Physiol 587:11–12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruddy KL, Carson RG (2013) Neural pathways mediating cross education of motor function. Front Hum Neurosci 7:39

    Article  Google Scholar 

  • Ruddy KL, Leemans A, Woolley DG, Wenderoth N, Carson RG (2017) Structural and functional cortical connectivity mediating cross education of motor function. J Neurosci 37:2555–2564

    Article  CAS  PubMed  PubMed Central  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 40:1073–1081

    Article  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 244:121–124

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Zult T, Howatson G, Kadar EE, Farthing JP, Hortobagyi T (2014) Role of the mirror-neuron system in cross-education. Sports Med 44:159–178

    Article  PubMed  Google Scholar 

  • Zult T, Goodall S, Thomas K, Solnick S, Hortobágyi T, Howatson G (2016) Mirror training augments the cross-education of strength and affects inhibitory paths. Med Sci Sports Exerc 48:1001–1013

    Article  CAS  PubMed  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

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dawson Kidgell.

Ethics declarations

Conflict of interest

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Leung, M., Rantalainen, T., Teo, WP. et al. The ipsilateral corticospinal responses to cross-education are dependent upon the motor-training intervention. Exp Brain Res 236, 1331–1346 (2018). https://doi.org/10.1007/s00221-018-5224-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-018-5224-4

Keywords

Navigation