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European Journal of Applied Physiology

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01-07-2017 | Original Article

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

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

Published in: European Journal of Applied Physiology | Issue 7/2017

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.

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 92:2309–2318CrossRefPubMed

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 101:1776–1782CrossRefPubMed

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

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 387:317–330CrossRefPubMedPubMedCentral

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 1179:51–60CrossRefPubMed

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 97:3661–3665CrossRef

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

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 73:911–917PubMedCrossRef

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

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

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 6:760–768CrossRefPubMed

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

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

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 105:868–878CrossRefPubMed

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 112:3219–3226CrossRefPubMedPubMedCentral

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 116:1757–1769CrossRefPubMed

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

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

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

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):625–633CrossRefPubMedPubMedCentral

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

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 54:903–913CrossRefPubMed

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

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

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

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

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 84:1341–1349PubMedCrossRef

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

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 43:1188–1199CrossRef

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 99:1558–1568CrossRefPubMed

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 59:1334–1338CrossRefPubMed

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

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

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 25:3208–3217CrossRefPubMed

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 24:3123–3132CrossRefPubMed

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

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 300:566–575CrossRef

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 112:3097–3107CrossRefPubMed

Lee M, Gandevia SC, Carroll T (2009) Short-term strength training does not change cortical voluntary activation. Med Sci Sports Exerc 41:1452–1460CrossRefPubMed

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

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 37:1622–1626CrossRefPubMed

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

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

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 586:5147–5159CrossRefPubMedPubMedCentral

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 23:740–748CrossRefPubMed

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 91:171–178CrossRefPubMed

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

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

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

Sale DG (1988) Neural adaptation to resistance training. M Med Sci Sport Exerc 20:S135–S145CrossRef

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

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

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

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 186:59–66CrossRefPubMed

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

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

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 59:586–596CrossRefPubMedPubMedCentral

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

Title: Adaptations in corticospinal excitability and inhibition are not spatially confined to the agonist muscle following strength training
Authors: Joel Mason
Ashlyn Frazer
Deanna M. Horvath
Alan J. Pearce
Janne Avela
Glyn Howatson
Dawson Kidgell
Publication date: 01-07-2017
Publisher: Springer Berlin Heidelberg
Published in: European Journal of Applied Physiology / Issue 7/2017
Print ISSN: 1439-6319
Electronic ISSN: 1439-6327
DOI: https://doi.org/10.1007/s00421-017-3624-y

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

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

Abstract

Purpose

Methods

Results

Conclusion

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Purpose

Methods

Results

Conclusion

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