Abstract
Purpose
Transcranial magnetic stimulation (TMS) usually investigates the corticospinal responses of the agonist muscle to strength training, despite the role of the antagonist muscle in strength development. We examined the intracortical responses from an agonist and antagonist muscle following a single session of heavy-loaded strength training (dominant-arm only) to identify the early antagonistic responses to a single session that may accompany improvements in strength.
Methods
Corticospinal and motor cortical excitability and inhibition was collected from agonist and antagonist muscles prior to and following a single session of heavy-loaded wrist flexor training in 18 individuals. Training consisted of four sets 6–8 repetitions at 80% of 1-repetition maximum (1-RM). Recruitment curves for corticospinal excitability and inhibition of the right wrist flexor and wrist extensor muscles were constructed and assessed by examining the area under the recruitment curve. Intracortical measures were obtained using paired-pulse TMS.
Results
Following a single training session, increases in corticospinal excitability were observed in both the agonist and antagonist muscles. This was accompanied by decreases in corticospinal inhibition in both muscles. Intracortical inhibition was reduced and intracortical facilitation was increased for the agonist muscle only. Intracortical measures in the antagonist muscle remained unchanged after training.
Conclusions
These findings indicate that the corticospinal responses to a single session of strength training are similar between agonist and antagonist muscles, but the intrinsic cortico-cortical circuitry of the antagonist remains unchanged. The corticospinal responses are likely due to increased involvement/co-activation of the antagonist muscle during training as the agonist muscle fatigues.
Similar content being viewed by others
Abbreviations
- 1-RM:
-
One-repetition maximum
- AURC:
-
Area under the recruitment curve
- CSE:
-
Corticospinal excitability
- CSP:
-
Corticospinal silent period
- ECR:
-
Extensor carpi radialis
- EMG:
-
Electromyography
- FCR:
-
Flexor carpi radialis
- GABA:
-
γ-Aminobutyric acid
- ICF:
-
Intracortical facilitation
- LICI:
-
Long-interval cortical inhibition
- MEP:
-
Motor-evoked potential
- MMAX :
-
Maximal compound wave
- 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) Increased rate of force development and neural drive of human skeletal muscle following resistance training. J Appl Physiol 93:1318–1326
Baldissera F, Hultborn H, Illert M (2011) Integration in spinal neuronal systems. Com Physiol. https://doi.org/10.1002/cphy.cp010212
Baratta R, Solomonow M, Zhou BH, Letson D, Chuinard R, D’ambrosia R (1988) Muscular coactivation: the role of the antagonist musculature in maintaining knee stability. Am J Sports Med 16:113–122
Basmajian JV, De Luca CJ (1985) Description and analysis of the EMG signal. Muscles alive: their functions revealed by electromyography. Williams & Wilkins, USA
Bazzucchi I, Riccio ME, Felici F (2008) Tennis players show a lower coactivation of the elbow antagonist muscles during isokinetic exercises. J Electromyo Kinesiol 18:752–759
Behm DG, Sale DG (1993) Velocity specificity of resistance training. Sports Med 15:374–388
Bertolasi L, Priori A, Tinazzi M, Bertasi V, Rothwell JC (1998) Inhibitory action of forearm flexor muscle afferents on corticospinal outputs to antagonist muscles in humans. J Physiol 511:947–956
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 103:1251–1263
Busse ME, Wiles CM, Van Deursen RWM (2005) Muscle co-activation in neurological conditions. Phys Ther Rev 10:247–253
Capaday C, Devanne H, Bertrand L, Lavoie BA (1998) Intracortical connections between motor cortical zones controlling antagonistic muscles in the cat: a combined anatomical and physiological study. Exp Brain Res 120:223–232
Capaday C, Ethier C, Van Vreeswijk C (2013) On the functional organization and operational principles of the motor cortex. Front Neural Circ 7:66
Carolan B, Cafarelli E (1992) Adaptations in coactivation after isometric resistance training. J Appl Physiol 73:911–917
Carroll TJ, Riek S, Carson RG (2001) Neural adaptations to resistance training. Sports Med 31:829–840
Christie A, Fling B, Crews RT, Mulwitz LA, Kamen G (2007) Reliability of motor-evoked potentials in the ADM muscle of older adults. J Neuro Methods 164:320–324
Cirillo J, Todd G, Semmler JG (2011) Corticomotor excitability and plasticity following complex visuomotor training in young and old adults. Eur J Neurosci 34:1847–1856
Classen J, Liepert J, Wise SP, Hallett M, Cohen LG (1998) Rapid plasticity of human cortical movement representation induced by practice. J Neurophysiol 79:1117–1123
Crone C, Nielsen JENS (1989) Spinal mechanisms in man contributing to reciprocal inhibition during voluntary dorsiflexion of the foot. J Phsyiol 416:255–272
Dal Maso F, Longcamp M, Cremoux S, Amarantini D (2017) Effect of training status on beta-range corticomuscular coherence in agonist vs. antagonist muscles during isometric knee contractions. Exp Brain Res 235:3023–3031
De Luca CJ, Mambrito B (1987) Voluntary control of motor units in human antagonist muscles: coactivation and reciprocal activation. J Neurophysiol 58:525–542
Desmyttere G, Mathieu E, Begon M, Simoneau-Buessinger E, Cremoux S (2018) Effect of the phase of force production on corticomuscular coherence with agonist and antagonist muscles. Eur J Neurosci 48:3288–3298
Frazer AK, Howatson G, Ahtiainen JP, Avela J, Rantalainen T, Kidgell DJ (2019) Priming the motor cortex with anodal transcranial direct current stimulation affects the acute inhibitory corticospinal responses to strength training. J Strength Cond Res 33:307–317
Gorassini M, Yang JF, Siu M, Bennett DJ (2002) Intrinsic activation of human motoneurons: reduction of motor unit recruitment thresholds by repeated contractions. J Neurophysiol 87:1859–1866
Gribble PL, Mullin LI, Cothros N, Mattar A (2003) Role of cocontraction in arm movement accuracy. J Neurophysiol 89:2396–2405
Häkkinen K, Kallinen M, Izquierdo M, Jokelainen K, Lassila H, Malkia E, 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
Häkkinen K, Alen M, Kallinen M, Newton RU, Kraemer WJ (2000) Neuromuscular adaptation during prolonged strength training, detraining and re-strength-training in middle-aged and elderly people. Eur J Appl Physiol 83:51–62
Hallett M (2000) Transcranial magnetic stimulation and the human brain. Nature 406:147
Hautier CA, Arsac LM, Deghdegh K, Souquet J, Belli A, Lacour JR (2000) Influence of fatigue on EMG/force ratio and cocontraction in cycling. Med Sci Sports Exerc 32:839–843
Hendy AM, Kidgell DJ (2013) Anodal tDCS applied during strength training enhances motor cortical plasticity. Med Sci Sports Exerc 45:1721–1729
Hendy AM, Kidgell DJ (2014) Anodal-tDCS applied during unilateral strength training increases strength and corticospinal excitability in the untrained homologous muscle. Exp Brain Res 232:3243–3252
Hight RE, Beck TW, Bemben DA, Black CD (2017) Adaptations in antagonist co-activation: role in the repeated-bout effect. PLoS One 12(12):e0189323
Hortobágyi T, DeVita P (2006) Mechanisms responsible for the age-associated increase in coactivation of antagonist muscles. Exerc Sport Sci Rev 34:29–35
Jarić S, Radovanović S, Milanović S, Ljubisavljević M, Anastasijević R (1997) A comparison of the effects of agonist and antagonist muscle fatigue on performance of rapid movements. Eur J Appl Physiol 76:41–47
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
Karst GM, Hasan Z (1987) Antagonist muscle activity during human forearm movements under varying kinematic and loading conditions. Exp Brain Res 67:391–401
Keel JC, Smith MJ, Wassermann EM (2001) A safety screening questionnaire for transcranial magnetic stimulation. Clin Neurophysiol 112:720
Keen DA, Yue GH, Enoka RM (1994) Training-related enhancement in the control of motor output in elderly humans. J Appl Physiol 77:2648–2658
Kellis E (1998) Quantification of quadriceps and hamstring antagonist activity. Sports Med 25:37–62
Kidgell DJ, Pearce AJ (2010) Corticospinal properties following short-term strength training of an intrinsic hand muscle. Hum Mov Sci 29:631–641
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 JP, Avela J, Howatson G (2015) Increased cross-education of muscle strength and reduced corticospinal inhibition following eccentric strength training. Neuroscience 300:566–575
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 46:2648–2661
Latella C, Hendy AM, Pearce AJ, Vander Westhuizen D, Teo WP (2016) The time-course of acute changes in corticospinal excitability, intra-cortical inhibition and facilitation following a single-session heavy strength training of the biceps brachii. Front Hum Neurosci 10:607
Latella C, Teo WP, Harris D, Major B, Vander Westhuizen D, Hendy AM (2017) Effects of acute resistance training modality on corticospinal excitability, intra-cortical and neuromuscular responses. Eur J Appl Physiol 117:2211–2224
Leung M, Rantalainen T, Teo WP, Kidgell DJ (2015) Motor cortex excitability is not differentially modulated following skill and strength training. Neuroscience 305:99–108
Lévénez M, Garland SJ, Klass M, Duchateau J (2008) Cortical and spinal modulation of antagonist coactivation during a submaximal fatiguing contraction in humans. J Neurophysiol 99:554–563
Macaluso A, Nimmo MA, Foster JE, Cockburn M, McMillan NC, De Vito G (2002) Contractile muscle volume and agonist-antagonist coactivation account for differences in torque between young and older women. Muscle Nerve 25:858–863
Manca A, Cabboi MP, Ortu E, Ginatempo F, Dragone D, Zarbo IR, Deriu F (2016) Effect of contralateral strength training on muscle weakness in people with multiple sclerosis: proof-of-concept case series. Phys Ther 96:828–838
Mason J, Frazer AK, Pearce AJ, Goodwill AM, Howatson G, Jaberzadeh S, Kidgell DJ (2018) Determining the early corticospinal-motoneuronal responses to strength training: a systematic review and meta-analysis. Rev Neurosci. https://doi.org/10.1515/revneuro-2018-0054
Mason J, Frazer AK, Jaberzadeh S, Ahtiainen J, Avela A, Rantalainen T, Leung M, Kidgell DJ (2019). Determining the corticospinal responses to single bouts of skill and strength training. J Strength Cond Res. In press
Morita H, Crone C, Christenhuis D, Petersen NT, Nielsen JB (2001) Modulation of presynaptic inhibition and disynaptic reciprocal Ia inhibition during voluntary movement in spasticity. Brain 124:826–837
Mullany H, O’Malley M, Gibson ASC, Vaughan C (2002) Agonist–antagonist common drive during fatiguing knee extension efforts using surface electromyography. J Electromyo Kinesiol 12:375–384
Nandi T, Hortobágyi T, van Keeken HG, Salem GJ, Lamoth CJ (2019) Standing task difficulty related increase in agonist-agonist and agonist-antagonist common inputs are driven by corticospinal and subcortical inputs respectively. Sci Rep 9:2439
Nepveu JF, Thiel A, Tang A, Fung J, Lundbye-Jensen J, Boyd LA, Roig M (2017) A single bout of high-intensity interval training improves motor skill retention in individuals with stroke. Neurorehabil Neural Rep 31:726–735
Nielsen JB (2004) Sensorimotor integration at spinal level as a basis for muscle coordination during voluntary movement in humans. J Appl Physiol 96:1961–1967
Nuzzo JL, Barry BK, Gandevia SC, Taylor JL (2016) Acute strength training increases responses to stimulation of corticospinal axons. Med Sci Sports Exerc 48:139–150
Oldfield R (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113
Osternig LR, Hamill J, Lander JE, Robertson R (1986) Co-activation of sprinter and distance runner muscles in isokinetic exercise. Med Sci Sports Exerc 18:431–435
Psek JA, Cafarelli E (1993) Behavior of coactive muscles during fatigue. J Appl Physiol 74:170–175
Rao G, Amarantini D, Berton E (2009) Influence of additional load on the moments of the agonist and antagonist muscle groups at the knee joint during closed chain exercise. J Electromyo Kinesiol 19:459–466
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. Med Sci Sports 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
Škarabot J, Mesquita RN, Brownstein CG, Ansdell P (2019) Myths and methodologies: how loud is the story told by the transcranial magnetic stimulation-evoked silent period? Exp Phsyiol. https://doi.org/10.1113/EP087557
Tanaka R (1974) Reciprocal Ia inhibition during voluntary movements in man. Exp Brain Res 21:529–540
Tillin NA, Pain MT, Folland JP (2011) Short-term unilateral resistance training affects the agonist–antagonist but not the force–agonist activation relationship. Muscle Nerve 43:375–384
Ushiyama J, Ushiba J (2013) Resonance between cortex and muscle: a determinant of motor precision? Clin Neurophysiol 124:5–7
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 513:295–305
Yacyshyn AF, Woo EJ, Price MC, McNeil CJ (2016) Motoneuron responsiveness to corticospinal tract stimulation during the silent period induced by transcranial magnetic stimulation. Exp Brain Res 234:3457–3463
Zoghi M, Nordstrom MA (2007) Progressive suppression of intracortical inhibition during graded isometric contraction of a hand muscle is not influenced by hand preference. Exp Brain Res 177:266–274
Funding
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Author information
Authors and Affiliations
Contributions
JM, AF, GH and DJK conceived and designed the study. JM, AF, GH and DJK conducted experiments, analyzed data, and drafted the first version of the manuscript. AJP, SJ, JA critically revised the manuscript. All authors read and approved the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
None of the authors have potential conflicts of interest to be disclosed.
Additional information
Communicated by Toshio Moritani.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Mason, J., Howatson, G., Frazer, A.K. et al. Modulation of intracortical inhibition and excitation in agonist and antagonist muscles following acute strength training. Eur J Appl Physiol 119, 2185–2199 (2019). https://doi.org/10.1007/s00421-019-04203-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00421-019-04203-9