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Adaptations in corticospinal excitability and inhibition are not spatially confined to the agonist muscle following strength training

European Journal of Applied Physiology Aims and scope Submit manuscript

Abstract

Purpose

We used transcranial magnetic stimulation (TMS) to determine the corticospinal responses from an agonist and synergist muscle following strength training of the right elbow flexors.

Methods

Motor-evoked potentials were recorded from the biceps brachii and flexor carpi radialis during a submaximal contraction from 20 individuals (10 women, 10 men, aged 18–35 years; training group; n = 10 and control group; n = 10) before and after 3 weeks of strength training at 80% of 1-repetition maximum (1-RM). To characterise the input–output properties of the corticospinal tract, stimulus–response curves for corticospinal excitability and inhibition of the right biceps brachii and flexor carpi radialis were constructed and assessed by examining the area under the recruitment curve (AURC).

Results

Strength training resulted in a 29% (P < 0.001) increase in 1-RM biceps brachii strength and this was accompanied by a 19% increase in isometric strength of the wrist flexors (P = 0.001). TMS revealed an increase in corticospinal excitability AURC and a decrease in silent period duration AURC for the biceps brachii and flexor carpi radialis following strength training (all P < 0.05). However, the changes in corticospinal function were not associated with increased muscle strength.

Conclusion

These findings show that the corticospinal responses to strength training of a proximal upper limb muscle are not spatially restricted, but rather, results in a change in connectivity, among an agonist and a synergistic muscle relevant to force production.

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Abbreviations

1RM:

One-repetition maximum

AURC:

Area under the recruitment curve

AMT:

Active motor threshold

CMEPs:

Cervicomedullary motor–evoked potentials

GABA:

γ-Aminobutyric acid

LTP:

Long-term potentiation

MEPs:

Motor-evoked potentials

MVIC:

Maximal voluntary isometric contraction

M1:

Primary motor cortex

rmsEMG:

Root-mean square electromyography

sEMG:

Surface electromyography

SICI:

Short-interval cortical inhibition

TMS:

Transcranial magnetic stimulation

References

  • Aagaard P, Simonsen EB, Andersen JL, Magnusson P, Dyhre-Poulsen P (2002) Neural adaptation to resistance training: changes in evoked V-wave and H-reflex responses. J Appl Physiol 92:2309–2318

    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 

  • Ashe J (1997) Force and the motor cortex. Behav Brain Res 86:1–15

    Article  CAS  PubMed  Google Scholar 

  • Baldissera F, Campadelli P, Piccinelli L (1987) The dynamic response of cat gastrocnemius motor units investigated by ramp-current injection into their motoneurones. J Physiol 387:317–330

    Article  CAS  PubMed  PubMed Central  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

    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. P Natl Acad Sci USA 97:3661–3665

    Article  CAS  Google Scholar 

  • Cannon RJ, Cafarelli E (1987) Neuromuscular adaptations to training. J Appl Physiol 63:2396–2402

    Article  CAS  PubMed  Google Scholar 

  • Capaday C, Ethier C, Darling W, Van Vreeswijk C (2013) On the functional organization and operational principles of the motor cortex. Front Neural Circuits 18:66

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carroll TJ, Selvanayagam VS, Riek S, Semmler JG (2011) Neural adaptations to strength training: Moving beyond transcranial magnetic stimulation and reflex studies. Acta Physiol 202:119–140

    Article  CAS  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 6:760–768

    Article  PubMed  Google Scholar 

  • Cheney PD, Fetz EE (1980) Functional classes of primate corticomotoneuronal cells and their relation to active force. J Neurophysiol 44:773–791

    Article  CAS  PubMed  Google Scholar 

  • Christie A, Kamen G (2013) Cortical inhibition is reduced following short-term training in young and older adults. AGE 36:749–758

    Article  PubMed  PubMed Central  Google Scholar 

  • Clark BC, Issac LC, Lane JL, Damron LA, Hoffman RL (2008) Neuromuscular plasticity during and following 3 wk of human forearm cast immobilization. J Appl Physiol 105:868–878

    Article  PubMed  Google Scholar 

  • Clark BC, Mahato NK, Nakazawa M, Law TD, Thomas JS (2014) The power of the mind: the cortex as a critical determinant of muscle strength/weakness. J Neurophysiol 112:3219–3226

    Article  PubMed  PubMed Central  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 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Luca CJ, Erim Z (2002) Common drive in motor units of a synergistic muscle pair. J Neurophysiol 87:2200–2204

    Article  PubMed  Google Scholar 

  • Devanne H, Cohen LG, Kouchtir-Devanne N, Capaday C (2002) Integrated motor cortical control of task-related muscles during pointing in humans. J Neurophysiol 87:3006–3017

    Article  PubMed  Google Scholar 

  • Di Lazzaro V, Restuccia D, Oliviero A, Profice P, Ferrara L, Insola A, Mazzone P, Tonali P, Rothwell JC (1998) Effects of voluntary contraction on descending volleys evoked by transcranial stimulation in conscious humans. J Physiol 508(Pt 2):625–633

    Article  PubMed  PubMed Central  Google Scholar 

  • Enoka RM (1997) Neural adaptations with chronic physical activity. J Biomech 30:447–455

    Article  CAS  PubMed  Google Scholar 

  • Frazer A, Williams J, Spittles M, Rantalainen T, Kidgell D (2016) Anodal transcranial direct current stimulation of the motor cortex increases cortical voluntary activation and neural plasticity. Muscle Nerve 54:903–913

    Article  PubMed  Google Scholar 

  • Fuhr P, Agostino R, Hallett M (1991) Spinal motor neuron excitability during the silent period after cortical stimulation. Electroencephalogr Clin Neurophysiol 81:257–262

    Article  CAS  PubMed  Google Scholar 

  • Gabriel DA, Kamen G, Frost G (2006) Neural adaptations to resistive exercise: mechanisms and recommendations for training practices. Sports Med 36:133–149

    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 

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

    Article  CAS  PubMed  Google Scholar 

  • Häkkinen K, Kallinen M, Izquierdo M, Jokelainen K, Lassila H, Lki M, Kraemer WJ, Newton RJ, Alen M (1998) Changes in agonist-antagonist EMG, muscle CSA, and force during strength training in middle-aged and older people. J Appl Physiol 84:1341–1349

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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 99:1558–1568

    Article  PubMed  Google Scholar 

  • 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 59:1334–1338

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Kidgell D, Pearce A (2011) What has transcranial magnetic stimulation taught us about neural adaptations to strength training? A brief rReview. J Strength Cond Res 25:3208–3217

    Article  PubMed  Google Scholar 

  • Kidgell D, Stokes M, Castricum T, Pearce A (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, 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. Neurosci 300:566–575

    Article  CAS  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 T (2009) Short-term strength training does not change cortical voluntary activation. Med Sci Sports Exerc 41:1452–1460

    Article  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Munn J, Herbert RD, Hancock MJ, Gandevia SC (2005) Resistance training for strength: Effect of number of sets and contraction speed. Med Sci Sports Exerc 37:1622–1626

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ortu E, Deriu F, Suppa A, Tolu E, Rothwell JC (2008) Effects of volitional contraction on intracortical inhibition and facilitation in the human motor cortex. J Physiol 586:5147–5159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pearce AJ, Kidgell DJ (2011) Neuroplasticity following skill and strength training, 1st edn. Nova Biomedical, New York

    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 23:740–748

    Article  CAS  PubMed  Google Scholar 

  • Porter R, Lemon RN (1993) Corticospinal function and voluntary movement, Monographs of the Physiological Society, vol 45. Oxford Science Publications, New York

    Google Scholar 

  • Pucci AR, Griffin L, Cafarelli E (2006) Maximal motor unit firing rates during isometric resistance training in men. Exp Physiol 91:171–178

    Article  CAS  PubMed  Google Scholar 

  • Reeves ND, Maganaris CN, Narici MV (2005) Plasticity of dynamic muscle performance with strength training in elderly humans. Muscle Nerve 31:355–364

    Article  PubMed  Google Scholar 

  • Ridding MC, Taylor JL, Rothwell JC (1995) The effect of voluntary contraction on cortico-cortical inhibition in human motor cortex. J Physiol 487:541–548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Sale DG (1988) Neural adaptation to resistance training. M Med Sci Sport Exerc 20:S135–S145

    Article  CAS  Google Scholar 

  • Sale MV, Semmler JG (2005) Age-related differences in corticospinal control during functional isometric contractions in left and right hands. J Appl Physiol 99:1483–1493

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Smith WS, Fetz EE (2009) Synaptic linkages between corticomotoneuronal cells affecting forelimb muscles in behaving primates. J Neurophysiol 102:1040–1048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Talelli P, Waddingham W, Ewas A, Rothwell JC, Ward NS (2008) The effect of age on task-related modulation of interhemispheric balance. Exp Brain Res 186:59–66

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Werhahn KJ, Classen J, Benecke R (1995) The silent period induced by transcranial magnetic stimulation in muscles supplied by cranial nerves: normal data and changes in patients. J Neurol Neurosurg Psychiatry 59:586–596

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilson S, Lockwood R, Thickbroom G, Mastaglia F (1993) The muscle silent period following transcranial magnetic cortical stimulation. J Neurol Sci 114:216–222

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

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

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Correspondence to Dawson Kidgell.

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Communicated by Toshio Moritani.

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Mason, J., Frazer, A., Horvath, D.M. et al. Adaptations in corticospinal excitability and inhibition are not spatially confined to the agonist muscle following strength training. Eur J Appl Physiol 117, 1359–1371 (2017). https://doi.org/10.1007/s00421-017-3624-y

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  • DOI: https://doi.org/10.1007/s00421-017-3624-y

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