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European Journal of Applied Physiology

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01-04-2020 | Motor Evoked Potential | Original Article

Tracking the corticospinal responses to strength training

Authors: Joel Mason, Ashlyn K. Frazer, Janne Avela, Alan J. Pearce, Glyn Howatson, Dawson J. Kidgell

Published in: European Journal of Applied Physiology | Issue 4/2020

Abstract

Purpose

The motor cortex (M1) appears to be a primary site of adaptation following both a single session, and repeated strength-training sessions across multiple weeks. Given that a single session of strength-training is sufficient to induce modification at the level of the M1 and corticospinal tract, this study sought to determine how these acute changes in M1 and corticospinal tract might accumulate across the course of a 2-week heavy-load strength-training program.

Methods

Transcranial magnetic stimulation (TMS) was used to infer corticospinal excitability (CSE), intracortical facilitation (ICF), short and long-interval intracortical inhibition (SICI and LICI) and silent period duration prior to and following each training session during a 2-week heavy-load strength-training period.

Results

Following 2-weeks of strength-training, increases in strength (15.5%, P = 0.01) were accompanied by an increase in CSE (44%, P = 0.006) and reductions in both silent period duration (14%, P < 0.0001) and SICI (35%, P = 0.0004). Early training sessions acutely increased CSE and ICF, and acutely reduced silent period duration and SICI. However, later training sessions failed to modulate SICI and ICF, with substantial adaptations occurring offline between training sessions. No acute or retained changes in LICI were observed. Co-contraction of antagonists reduced by 36% following 2-weeks of strength-training.

Conclusions

Collectively, these results indicate that corticospinal plasticity occurs within and between training sessions throughout a training period in distinct early and later stages that are modulated by separate mechanisms of plasticity. The development of strength is akin to the previously reported changes that occur following motor skill training.

Aagaard P, Simonsen EB, Andersen JL, Magnusson P, Dyhre-Poulsen P (2002) Increased rate of force development and neural drive of human skeletal muscle following resistance training. J Appl Physiol 93:1318–1326PubMed

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 101:1776–1782PubMed

Ahtiainen JP, Pakarinen A, Alen M, Kraemer WJ, Häkkinen K (2003) Muscle hypertrophy, hormonal adaptations and strength development during strength training in strength-trained and untrained men. Eur J Appl Physiol 89:555–563PubMed

Baker SN, Perez MA (2017) Reticulospinal contributions to gross hand function after human spinal cord injury. J Neurosci 37:9778–9784PubMedPubMedCentral

Bestmann S, Krakauer JW (2015) The uses and interpretations of the motor-evoked potential for understanding behaviour. Exp Brain Res 233:679–689PubMed

Brownstein CG, Ansdell P, Škarabot J, Frazer A, Kidgell DJ, Howatson G, Thomas K (2018) Motor cortical and corticospinal function differ during an isometric squat compared with isometric knee extension. Exp Physiol 103:1251–1263PubMed

Bütefisch 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 97(7):3661–3665PubMedPubMedCentral

Carolan B, Cafarelli E (1992) Adaptations in coactivation after isometric resistance training. J Appl Physiol 73:911–917PubMed

Carroll TJ, Riek S, Carson RG (2002) The sites of neural adaptation induced by resistance training in humans. J Physiol 544:641–652PubMedPubMedCentral

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 116:1757–1769PubMed

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

Del Vecchio A, Casolo A, Negro F, Scorcelletti M, Bazzucchi I, Enoka R, Felici F, Farina D (2019) The increase in muscle force after 4 weeks of strength training is mediated by adaptations in motor unit recruitment and rate coding. J Physiol 597:1873–1887PubMedPubMedCentral

Di Lazzaro V, Rothwell JC (2014) Corticospinal activity evoked and modulated by non-invasive stimulation of the intact human motor cortex. J Physiol 592:4115–4128PubMedPubMedCentral

Duchateau J, Enoka RM (2002) Neural adaptations with chronic activity patterns in able-bodied humans. Am J Phys Med Rehabil 81:S17–27PubMed

Duchateau J, Semmler JG, Enoka RM (2006) Training adaptations in the behavior of human motor units. J Appl Physiol 101:1766–1775PubMed

Farina D, Holobar A (2016) Characterization of human motor units from surface EMG decomposition. Proc IEEE 104:353–373

Floyer-Lea A, Matthews PM (2005) Distinguishable brain activation networks for short-and long-term motor skill learning. J Neurophysiol 94:512–518PubMed

Floyer-Lea A, Wylezinska M, Kincses T, Matthews PM (2006) Rapid modulation of GABA concentration in human sensorimotor cortex during motor learning. J Neurophysiol 95:1639–1644PubMed

Folland JP, Williams AG (2007) Morphological and neurological contributions to increased strength. Sports Med 37:145–168PubMed

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

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

Guizelini PC, de AguiaR RA, Denadai BS, Caputo F, Greco CC (2018) Effect of resistance training on muscle strength and rate of force development in healthy older adults: a systematic review and meta-analysis. Exp Gerontol 102:51–58PubMed

Hendy AM, Kidgell DJ (2013) Anodal tDCS applied during strength training enhances motor cortical plasticity. Med Sci Sports Exerc 45:1721–1729PubMed

Hess G, Donoghue JP (1994) Long-term potentiation of horizontal connections provides a mechanism to reorganize cortical motor maps. J Neurophysiol 71:2543–2547PubMed

Hess GR, Aizenman CD, Donoghue JP (1996) Conditions for the induction of longterm potentiation in layer II/III horizontal connections of the rat motor cortex. J Neurophysiol 75(5):1765–1778PubMed

Hight RE, Beck TW, Bemben DA, Black CD (2017) Adaptations in antagonist co-activation: role in the repeated-bout effect. PLoS ONE 12:e0189323PubMedPubMedCentral

Hood LB, Forward EM (1965) Strength variations in two determinations of maximal isometric contractions. Phys Ther 45:1046–1053PubMed

Hortobágyi T, Richardson SP, Lomarev M, Shamim E, Meunier S, Russman H, Dang N, Hallett M (2009) Chronic low-frequency rTMS of primary motor cortex diminishes exercise training-induced gains in maximal voluntary force in humans. J Appl Physiol 106:403–411PubMed

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 99:1558–1568PubMed

Kamen G, Knight CA (2004) Training-related adaptations in motor unit discharge rate in young and older adults. J Gerontol A Biol Sci Med Sci 59:1334–1338PubMed

Kandel ER, Schwartz JH, Jessell TM (eds) (2000) Principles of neural science, vol 4. McGraw-hill, New York, pp 1227–1246

Karni A, Meyer G, Rey-Hipolito C, Jezzard P, Adams MM, Turner R, Ungerleider LG (1998) The acquisition of skilled motor performance: fast and slow experience-driven changes in primary motor cortex. Proc Natl Acad Sci 95:861–868PubMedPubMedCentral

Keel JC, Smith MJ, Wassermann EM (2001) A safety screening questionnaire for transcranial magnetic stimulation. Clin Neurophysiol 112:720PubMed

Kida H, Tsuda Y, Ito N, Yamamoto Y, Owada Y, Kamiya Y, Mitsushima D (2016) Motor training promotes both synaptic and intrinsic plasticity of layer II/III pyramidal neurons in the primary motor cortex. Cereb Cortex 26(8):3494–3507PubMedPubMedCentral

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

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 24:3123–3132PubMed

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

Kidgell DJ, Bonanno DR, Frazer AK, Howatson G, Pearce AJ (2017) Corticospinal responses following strength training: a systematic review and meta-analysis. Eur J Neurosci 46:2648–2661PubMed

Kleim JA, Hogg TM, VandenBerg PM, Cooper NR, Bruneau R, Remple M (2004) Cortical synaptogenesis and motor map reorganization occur during late, but not early, phase of motor skill learning. J Neurosci 24:628–633PubMedPubMedCentral

Kleim JE, Kleim E, Schallert K, Chan S, Cramer SC (2006) Coordinated short and long-term motor cortex plasticity with motor skill learning. Soc Neurosci 32:60.8/FF2

Kleim JA, Jones TA (2008) Principles of experience-dependent neural plasticity: implications for rehabilitation after brain damage. J Speech Lang Hear Res 51:S225–S239PubMed

Kroll W (1963) Reliability variations of strength in test–retest situations. Res Q 34:50–55

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

Latella C, Teo WP, Harris D, Major B, VanderWesthuizen D, Hendy AM (2017) Effects of acute resistance training modality on corticospinal excitability, intra-cortical and neuromuscular responses. Eur J Appl Physiol 117(11):2211–2224PubMed

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

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

Leung M, Rantalainen T, Teo WP, Kidgell D (2017) The corticospinal responses of metronome-paced, but not self-paced strength training are similar to motor skill training. Eur J Appl Physiol 117(12):2479–2492PubMed

McNeil CJ, Martin PG, Gandevia SC, Taylor JL (2011) Long-interval intracortical inhibition in a human hand muscle. Exp Brain Res 209(2):287–297PubMed

Mason J, Frazer AK, Horvath DM, Pearce AJ, Avela J, Howatson G, Kidgell DJ (2017) Adaptations in corticospinal excitability and inhibition are not spatially confined to the agonist muscle following strength training. Eur J Appl Physiol 117:1359–1371PubMed

Mason J, Frazer AK, Pearce AJ, Goodwill AM, Howatson G, Jaberzadeh S, Kidgell DJ (2019) Determining the early corticospinal-motoneuronal responses to strength training: a systematic review and meta-analysis. Rev Neurosci 30:463–476PubMed

Mawase F, Uehara S, Bastian AJ, Celnik P (2017) Motor learning enhances use-dependent plasticity. J Neurosci 37:2673–2685PubMedPubMedCentral

Mednick SC, Cai DJ, Shuman T, Anagnostaras S, Wixted JT (2011) An opportunistic theory of cellular and systems consolidation. Trends Neurosci 34:504–514PubMedPubMedCentral

Mooney RA, Cirillo J, Byblow WD (2019) Neurophysiological mechanisms underlying motor skill learning in young and older adults. Exp Brain Res 237:2331–2344PubMed

Monfils MH, Plautz EJ, Kleim JA (2005) In search of the motor engram: motor map plasticity as a mechanism for encoding motor experience. Neuroscientist 11:471–483PubMed

Nuzzo JL, Taylor JL, Gandevia SC (2019) CORP: measurement of upper and lower limb muscle strength and voluntary activation. J Appl Physiol 126:513–543PubMed

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

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 23:740–748PubMed

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 123:133–141PubMed

Riddle CN, Edgley SA, Baker SN (2009) Direct and indirect connections with upper limb motoneurons from the primate reticulospinal tract. J Neurosci 29:4993–4999PubMedPubMedCentral

Rioult-Pedotti MS, Friedman D, Hess G, Donoghue JP (1998) Strengthening of horizontal cortical connections following skill learning. Nat Neurosci 1:230PubMed

Rioult-Pedotti MS, Friedman D, Donoghue JP (2000) Learning-induced LTP in neocortex. Science 290:533–536PubMed

Rosenkranz K, Kacar A, Rothwell JC (2007) Differential modulation of motor cortical plasticity and excitability in early and late phases of human motor learning. J Neurosci 27:12058–12066PubMedPubMedCentral

Rossini PM, Rossi S, Pasqualetti P, Tecchio F (1999) Corticospinal excitability modulation to hand muscles during movement imagery. Cereb Cortex 9:161–167PubMed

Schubert M, Beck S, Taube W, Amtage F, Faist M, Gruber M (2008) Balance training and ballistic strength training are associated with task-specific corticospinal adaptations. Eur J Neurosci 27:2007–2018PubMed

Selvanayagam VS, Riek S, Carroll TJ (2011) Early neural responses to strength training. J Appl Physiol 111:367–375PubMed

Semmler JG, Enoka RM (2000) Neural contributions to changes in muscle strength. In: Zatsiorsky (ed) Biomechanics in sport: performance enhancement and injury prevention. https://doi.org/10.1002/9780470693797.ch1

Siddique U, Rahman S, Frazer A, Pearce AJ, Howatson G, Kidgell D (2020) Determining the sites of neural adaptations to resistance training: a systematic review and meta-analysis. Sports Med. https://doi.org/10.1007/s40279-020-01258-z CrossRefPubMed

Stagg CJ, Bachtiar V, Johansen-Berg H (2011) The role of GABA in human motor learning. Curr Biol 21:480–484PubMedPubMedCentral

Taube W (2011) What trains together, gains together: strength training strengthens not only muscles but also neural networks. J Appl Phys 111:347–348

Van Cutsem M, Duchateau J, Hainaut K (1998) Changes in single motor unit behaviour contribute to the increase in contraction speed after dynamic training in humans. J Physiol 513:295–305PubMedPubMedCentral

Vila-Chã C, Falla D, Farina D (2010) Motor unit behavior during submaximal contractions following six weeks of either endurance or strength training. J Appl Physiol 109:1455–1466PubMed

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

Title: Tracking the corticospinal responses to strength training
Authors: Joel Mason
Ashlyn K. Frazer
Janne Avela
Alan J. Pearce
Glyn Howatson
Dawson J. Kidgell
Publication date: 01-04-2020
Publisher: Springer Berlin Heidelberg
Keywords: Motor Evoked Potential
Transcranial Magnetic Stimulation
Motor Evoked Potential
Transcranial Magnetic Stimulation
Published in: European Journal of Applied Physiology / Issue 4/2020
Print ISSN: 1439-6319
Electronic ISSN: 1439-6327
DOI: https://doi.org/10.1007/s00421-020-04316-6

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Springer Medicine

Tracking the corticospinal responses to strength training

Abstract

Purpose

Methods

Results

Conclusions

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Purpose

Methods

Results

Conclusions

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