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.
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
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
Ashe J (1997) Force and the motor cortex. Behav Brain Res 86:1–15
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
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
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
Cannon RJ, Cafarelli E (1987) Neuromuscular adaptations to training. J Appl Physiol 63:2396–2402
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
Carolan B, Cafarelli E (1992) Adaptations in coactivation after isometric resistance training. J Appl Physiol 73:911–917
Carroll TJ, Riek S, Carson RG (2002) The sites of neural adaptation induced by resistance training in humans. J Physiol 544:641–652
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
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
Cheney PD, Fetz EE (1980) Functional classes of primate corticomotoneuronal cells and their relation to active force. J Neurophysiol 44:773–791
Christie A, Kamen G (2013) Cortical inhibition is reduced following short-term training in young and older adults. AGE 36:749–758
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
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
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
Dayan E, Cohen Leonardo G (2011) Neuroplasticity subserving motor skill learning. Neuron 72:443–454
De Luca CJ, Erim Z (2002) Common drive in motor units of a synergistic muscle pair. J Neurophysiol 87:2200–2204
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
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
Enoka RM (1997) Neural adaptations with chronic physical activity. J Biomech 30:447–455
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
Fuhr P, Agostino R, Hallett M (1991) Spinal motor neuron excitability during the silent period after cortical stimulation. Electroencephalogr Clin Neurophysiol 81:257–262
Gabriel DA, Kamen G, Frost G (2006) Neural adaptations to resistive exercise: mechanisms and recommendations for training practices. Sports Med 36:133–149
Goodwill AM, Pearce AJ, Kidgell DJ (2012) Corticomotor plasticity following unilateral strength training. Muscle Nerve 46:384–393
Griffin L, Cafarelli E (2007) Transcranial magnetic stimulation during resistance training of the tibialis anterior muscle. J Electromyogr Kinesiol 17:446–452
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
Hendy AM, Kidgell D (2013) Anodal tDCS applied during strength training enhances motor cortical plasticity. Med Sci Sport Exerc 45:1721–1729
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
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
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
Keel JC, Smith MJ, Wassermann EM (2001) A safety screening questionnaire for transcranial magnetic stimulation. Clin Neurophysiol 112:720
Kidgell DJ, Pearce AJ (2010) Corticospinal properties following short-term strength training of an intrinsic hand muscle. Hum Movement Sci 29:631–641
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
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
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, 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
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
Lee M, Gandevia SC, Carroll T (2009) Short-term strength training does not change cortical voluntary activation. Med Sci Sports Exerc 41:1452–1460
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
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
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
Oldfield R (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113
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
Pearce AJ, Kidgell DJ (2011) Neuroplasticity following skill and strength training, 1st edn. Nova Biomedical, New York
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
Porter R, Lemon RN (1993) Corticospinal function and voluntary movement, Monographs of the Physiological Society, vol 45. Oxford Science Publications, New York
Pucci AR, Griffin L, Cafarelli E (2006) Maximal motor unit firing rates during isometric resistance training in men. Exp Physiol 91:171–178
Reeves ND, Maganaris CN, Narici MV (2005) Plasticity of dynamic muscle performance with strength training in elderly humans. Muscle Nerve 31:355–364
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
Rossini PM, Rossi S, Pasqualetti P, Tecchio F (1999) Corticospinal excitability modulation to hand muscles during movement imagery. Cereb Cortex 9:161–167
Sale DG (1988) Neural adaptation to resistance training. M Med Sci Sport Exerc 20:S135–S145
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
Selvanayagam VS, Riek S, Carroll TJ (2011) Early neural responses to strength training. J Appl Physiol 111:367–375
Smith WS, Fetz EE (2009) Synaptic linkages between corticomotoneuronal cells affecting forelimb muscles in behaving primates. J Neurophysiol 102:1040–1048
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
Taube W (2011) “What trains together, gains together”: strength training strengthens not only muscles but also neural networks. J Appl Physiol 111:347–348
Weier AT, Pearce AJ, Kidgell DJ (2012) Strength training reduces intracortical inhibition. Acta Physiol 206:109–119
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
Wilson S, Lockwood R, Thickbroom G, Mastaglia F (1993) The muscle silent period following transcranial magnetic cortical stimulation. J Neurol Sci 114:216–222
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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