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Progress in Motor Control pp 143–157Cite as

What Do TMS-Evoked Motor Potentials Tell Us About Motor Learning?

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Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 957))

Abstract

Thirty years ago, the first magnetic device capable of stimulating the human brain without discomfort through the intact skull was unveiled in Sheffield, England (Barker et al. in Lancet 1:1106–1107, 1985). Since that time, transcranial magnetic stimulation (TMS) has become the tool of choice for many scientists investigating human motor control and learning. In light of the fact that there are limits to the information that can be provided by any experimental technique, we first make the case that the necessarily restricted explanatory scope of the TMS technique—and the motor-evoked potentials to which it gives rise, is not yet reflected adequately in the research literature. We also argue that this inattention, coupled with the pervasive adoption of TMS as an investigative tool, may be restricting the elaboration of knowledge concerning the neural processes that mediate human motor learning. In order to make these points, we use as an exemplar the study of cross-education—the interlimb transfer of functional capacity.

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References

  • Amassian VE, Stewart M, Quirk GJ, Rosenthal JL (1987) Physiological basis of motor effects of a transient stimulus to cerebral cortex. Neurosurgery 20(1):74–93

    CAS  PubMed  Google Scholar 

  • Anderson ML (2014) After phrenology: neural reuse and the interactive brain. MIT Press, Cambridge, MA

    Google Scholar 

  • Barker AT, Jalinous R, Freeston IL (1985) Non-invasive magnetic stimulation of human motor cortex. Lancet 1(8437):1106–1107

    Article  CAS  PubMed  Google Scholar 

  • Bestmann S, Krakauer, JW (2015) The uses and interpretations of the motor-evoked potential for understanding behaviour. Exp Brain Res 233(3):679–689. http://doi.org/10.1007/s00221-014-4183-7

    Google Scholar 

  • Brown KE, Neva JL, Ledwell NM, Boyd LA (2014) Use of transcranial magnetic stimulation in the treatment of selected movement disorders. Degenerative Neurol Neuromuscul Dis 4:133–151. http://doi.org/10.2147/DNND.S70079

  • Carroll TJ, 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. doi:10.1152/japplphysiol.01351.2007

    Article  PubMed  Google Scholar 

  • Carson R, Riek S, Mackey D, Meichenbaum D, Willms K, Forner M, Byblow W (2004) Excitability changes in human forearm corticospinal projections and spinal reflex pathways during rhythmic voluntary movement of the opposite limb. J Physiol-Lond 560(3):929–940

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coxon JP, Peat NM, Byblow WD (2014) Primary motor cortex disinhibition during motor skill learning. J Neurophysiol 112(1):156–164. http://doi.org/10.1152/jn.00893.2013

    Google Scholar 

  • DeFelipe J, Conley M, Jones EG (1986) Long-range focal collateralization of axons arising from corticocortical cells in monkey sensory-motor cortex. J Neurosci 6(12):3749–3766

    CAS  PubMed  Google Scholar 

  • Di Lazzaro V, Oliviero A, Saturno E, Pilato F, Insola A, Mazzone P et al (2001) The effect on corticospinal volleys of reversing the direction of current induced in the motor cortex by transcranial magnetic stimulation. Exp Brain Res. Experimentelle Hirnforschung. Expérimentation Cérébrale, 138(2):268–273

    Google Scholar 

  • Di Lazzaro V, Oliviero A, Pilato F, Saturno E, Dileone M, Mazzone P et al (2004) The physiological basis of transcranial motor cortex stimulation in conscious humans. Clin Neurophysiol 115(2):255–266

    Article  PubMed  Google Scholar 

  • Di Lazzaro V, Rothwell JC (2014) Corticospinal activity evoked and modulated by non-invasive stimulation of the intact human motor cortex. J Physiol 592(Pt 19):4115–4128. http://doi.org/10.1113/jphysiol.2014.274316

    Google Scholar 

  • Di Lazzaro V, Ziemann U, Lemon RN (2008) State of the art: physiology of transcranial motor cortex stimulation. Brain Stimulation 1(4):345–362. http://doi.org/10.1016/j.brs.2008.07.004

    Google Scholar 

  • Di Lazzaro V, Ziemann U (2013) The contribution of transcranial magnetic stimulation in the functional evaluation of microcircuits in human motor cortex. Front Neural Circuits 7:18. http://doi.org/10.3389/fncir.2013.00018

  • Dickins DSE, Sale MV, Kamke MR (2015) Intermanual transfer and bilateral cortical plasticity is maintained in older adults after skilled motor training with simple and complex tasks. Front Aging Neurosci 7:73. doi:10.3389/fnagi.2015.00073

    Article  PubMed  PubMed Central  Google Scholar 

  • Dum RP, Strick PL (1996) Spinal cord terminations of the medial wall motor areas in macaque monkeys. J Neurosci 16:6513–6525

    CAS  PubMed  Google Scholar 

  • Dum RP, Strick PL (2002) Motor areas in the frontal lobe of the primate. Physiol Behav 77:677–682

    Article  CAS  PubMed  Google Scholar 

  • Esser SK, Hill SL, Tononi G (2005) Modeling the effects of transcranial magnetic stimulation on cortical circuits. J Neurophysiol 94(1):622–639

    Google Scholar 

  • Fodor J (1999) Diary: why the brain? London Rev Books 21(19):68–69

    Google Scholar 

  • Harrington A (1992) So human a brain: knowledge and values in the neurosciences. Birkhauser Verlag AG, Basel

    Book  Google Scholar 

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

    Google Scholar 

  • Henry FM, Rogers DE (1960) Increased response latency for complicated movements and a “memory drum” theory of neuromotor reaction. Res Q. Am Assoc Health Phys Educ Recreation 31(3):448–458. http://doi.org/10.1080/10671188.1960.10762052

    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(1):166–175. http://doi.org/10.1152/japplphysiol.00958.2010

    Google Scholar 

  • Hirano M, Kubota S, Tanabe S, Koizume Y, Funase K (2015) Interactions among learning stage, retention, and primary motor cortex excitability in motor skill learning. Brain Stimulation 8(6):1195–1204

    Article  PubMed  Google Scholar 

  • Holland L, Murphy B, Passmore S, Yielder P (2015) Time course of corticospinal excitability changes following a novel motor training task. Neurosci Lett 591:81–85. http://doi.org/10.1016/j.neulet.2015.02.022

    Google Scholar 

  • Hortobagyi T, Taylor J, Petersen N, Russell G, Gandevia S (2003) Changes in segmental and motor cortical output with contralateral muscle contractions and altered sensory inputs in humans. J Neurophysiol 90(4):2451–2459

    Article  PubMed  Google Scholar 

  • Hortobágyi T, Richardson SP, Lomarev M, Shamim E, Meunier S, Russman H, et al (2011) Interhemispheric plasticity in humans. Med Sci Sports Exerc 43(7):1188–1199. http://doi.org/10.1249/MSS.0b013e31820a94b8

    Google Scholar 

  • Jensen JL, Marstrand PCD, Nielsen JB (2005) Motor skill training and strength training are associated with different plastic changes in the central nervous system. J Appl Physiol 99(4):1558–1568

    Article  PubMed  Google Scholar 

  • Kujirai T, Caramia MD, Rothwell JC, Day BL, Thompson PD, Ferbert A et al (1993) Corticocortical inhibition in human motor cortex. J Physiol 471:501–519

    Article  CAS  PubMed  PubMed Central  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. doi:10.1113/jphysiol.2009.183855

    Article  CAS  PubMed  Google Scholar 

  • Lemon R, Pascual-Leone A, Davey N, Rothwell J, Wassermann E, Puri B (2002) Basic physiology of transcranial magnetic stimulation. Handbook of transcranial magnetic stimulation, pp 61–77

    Google Scholar 

  • Liepert J, Terborg C, Weiller C (1999) Motor plasticity induced by synchronized thumb and foot movements. Exp Brain Res 125:435–439

    Article  CAS  PubMed  Google Scholar 

  • Lopez-Alonso V, Cheeran B, Fernandez Del Olmo M (2015) Relationship between non-invasive brain stimulation-induced plasticity and capacity for motor learning. Brain Stimulation 8(6):1209–1219

    Article  PubMed  Google Scholar 

  • Lotze M, Braun C, Birbaumer N, Anders S, Cohen LG (2003) Motor learning elicited by voluntary drive. Brain 126(Pt 4):866–872

    Article  PubMed  Google Scholar 

  • Ljubisavljevic M (2006) Transcranial magnetic stimulation and the motor learning-associated cortical plasticity. Exp Brain Res. Experimentelle Hirnforschung. Expérimentation Cérébrale, 173(2):215–222. http://doi.org/10.1007/s00221-006-0538-z

    Google Scholar 

  • Magill RA (2004) Motor learning and control: concepts and applications, 7th edn. McGraw-Hill, New York

    Google Scholar 

  • McNickle E (2016) Electrophysiological and functional responses to associative brain stimulation. PhD thesis. Trinity College Dublin

    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. Experimentelle Hirnforschung. Expérimentation Cérébrale, 136(4):431–438

    Google Scholar 

  • Murray EA, Coulter JD (1981) Organization of corticospinal neurons in the monkey. J Comp Neurol 195:339–365. doi:10.1002/cne.901950212

    Article  CAS  PubMed  Google Scholar 

  • Nojima I, Mima T, Koganemaru S, Thabit MN, Fukuyama H, Kawamata T (2012) Human motor plasticity induced by mirror visual feedback. J Neurosci 32:1293–1300. doi:10.1523/JNEUROSCI.5364-11.2012

    Article  CAS  PubMed  Google Scholar 

  • Olivier E, Bawa P, Lemon RN (1995) Excitability of human upper limb motoneurones during rhythmic discharge tested with transcranial magnetic stimulation. J Physiol 485(Pt 1):257–269

    Article  CAS  PubMed  PubMed Central  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(5151):1287–1289

    Article  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(3):1037–1045

    CAS  PubMed  Google Scholar 

  • Pierrot-Deseilligny E (1996) Transmission of the cortical command for human voluntary movement through cervical propriospinal premotoneurons. Prog Neurobiol 48:489–517

    Article  CAS  PubMed  Google Scholar 

  • Perez MA, Lungholt BKS, Nyborg K, Nielsen JB (2004) Motor skill training induces changes in the excitability of the leg cortical area in healthy humans. Exp Brain Res. Experimentelle Hirnforschung. Expérimentation Cérébrale, 159(2):197–205. http://doi.org/10.1007/s00221-004-1947-5

    Google Scholar 

  • Perez MA, Wise SP, Willingham DT, Cohen LG (2007) Neurophysiological mechanisms involved in transfer of procedural knowledge. J Neurosci 27:1045–1053. doi:10.1523/JNEUROSCI.4128-06.2007

    Article  CAS  PubMed  Google Scholar 

  • Poh E, Riek S, Carroll TJ (2013) Ipsilateral corticospinal responses to ballistic training are similar for various intensities and timings of TMS. Acta Physiol (Oxf) 207:385–396. doi:10.1111/apha.12032

    Article  CAS  Google Scholar 

  • Porter R, Lemon R (1995) Corticospinal function and voluntary movement. Oxford University Press, Oxford

    Google Scholar 

  • Reissig P, Stöckel T, Garry MI, Summers JJ, Hinder MR (2015) Age-specific effects of mirror-muscle activity on cross-limb adaptations under mirror and non-mirror visual feedback conditions. Front Aging Neurosci 7:222. doi:10.3389/fnagi.2015.00222

    Article  PubMed  PubMed Central  Google Scholar 

  • Robertson EM (2007) The serial reaction time task: implicit motor skill learning? J Neurosci 27(38):10073–10075. http://doi.org/10.1523/JNEUROSCI.2747-07.2007

    Google Scholar 

  • Rockel AJ, Hiorns RW, Powell TP (1980) The basic uniformity in structure of the neocortex. Brain 103(2):221–244

    Article  CAS  PubMed  Google Scholar 

  • Rothwell JC (1997) Techniques and mechanisms of action of transcranial stimulation of the human motor cortex. J Neurosci Methods 74(2):113–122

    Article  CAS  PubMed  Google Scholar 

  • Rothwell JC (2002) Spinal interneurones: re-evaluation and controversy. Adv Exp Med Biol 508:259–263

    Article  PubMed  Google Scholar 

  • Ruddy KL, Carson RG (2013) Neural pathways mediating cross education of motor function. Front Human Neurosci 7:397. http://doi.org/10.3389/fnhum.2013.00397

  • Ruddy KL, Rudolf AK, Kalkman B, King M, Daffertshofer A, Carroll TJ, Carson RG (2016) Neural adaptations associated with interlimb transfer in a ballistic wrist flexion task. Front Human Neurosci. http://doi.org/10.3389/fnhum.2016.00204

  • Rusu CV, Murakami M, Ziemann U, Triesch J (2014) A model of TMS-induced I-waves in motor cortex. Brain Stimulation 7(3):401–414. http://doi.org/10.1016/j.brs.2014.02.009

    Google Scholar 

  • Sherrington CS (1942) Man on his nature. Cambridge University Press, Cambridge, p 178

    Google Scholar 

  • Sporns O (2011) Networks of the brain. MIT Press, Cambridge, MA

    Google Scholar 

  • Singh AM, Neva JL, Staines WR (2016) Aerobic exercise enhances neural correlates of motor skill learning. Behav Brain Res 301:19–26. http://doi.org/10.1016/j.bbr.2015.12.020

    Google Scholar 

  • Sutor B, Schmolke C, Teubner B, Schirmer C, Willecke K (2000) Myelination defects and neuronal hyperexcitability in the neocortex of connexin 32-deficient mice. Cereb Cortex 10(7):684–697

    Article  CAS  PubMed  Google Scholar 

  • Taylor JL (2006) Stimulation at the cervicomedullary junction in human subjects. J Electromyogr Kinesiol: Official J Int Soc Electrophysiological Kinesiol 16(3):215–223. http://doi.org/10.1016/j.jelekin.2005.07.001

    Google Scholar 

  • Terao Y, Ugawa Y (2002) Basic mechanisms of TMS. J Clin Neurophysiol 19(4):322

    Article  PubMed  Google Scholar 

  • Ziemann U, Rothwell JC (2000) I-waves in motor cortex. J Clin Neurophysiol 17(4):397–405

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Trinity College Institute of Neuroscience and School of Psychology, Trinity College Dublin, Dublin 2, Ireland

    Richard G. Carson & Emmet McNickle

  2. School of Psychology, Queen’s University Belfast, Northern Ireland, UK

    Richard G. Carson

  3. Neural Control of Movement Lab, ETH, Zurich, Switzerland

    Kathy L. Ruddy

Authors
  1. Richard G. Carson
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  2. Kathy L. Ruddy
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  3. Emmet McNickle
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Correspondence to Richard G. Carson .

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Editors and Affiliations

  1. Department of Information Technology and Biorobotics, Faculty of Science, University of Pécs, Pecs, Hungary

    Jozsef Laczko

  2. Department of Kinesiology, Pennsylvania State University, University Park, Pennsylvania, USA

    Mark L. Latash

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Carson, R.G., Ruddy, K.L., McNickle, E. (2016). What Do TMS-Evoked Motor Potentials Tell Us About Motor Learning?. In: Laczko, J., Latash, M. (eds) Progress in Motor Control. Advances in Experimental Medicine and Biology, vol 957. Springer, Cham. https://doi.org/10.1007/978-3-319-47313-0_8

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