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Methodological issues with the assessment of voluntary activation using transcranial magnetic stimulation in the knee extensors

  • Jeanne DekerleEmail author
  • P. Ansdell
  • L. Schäfer
  • A. Greenhouse-Tucknott
  • J. Wrightson
Original Article

Abstract

Purpose

The assessment of voluntary activation of the knee extensors using transcranial magnetic stimulation (VATMS) is routinely performed to assess the supraspinal function. Yet methodological scrutiny of the technique is scarce. The aim of the present study was to examine face validity and reliability of VATMS and its two main determinants (superimposed twitch during a maximal voluntary contraction [SIT100%] and estimated resting twitch [ERT]).

Methods

SIT100%, ERT, and VATMS were measured on ten healthy males (age 24 ± 5 years) before and following intermittent isometric fatiguing exercise on two separate occasions.

Results

The findings indicated issues regarding the accuracy of ERT and suggested a three-point relationship should not be used to determine ERT. Reliabilities for VATMS, SIT100%, and ERT were acceptable pre- but much weaker post-exercise (especially for SIT100%). Despite statistically significant changes in main neuromuscular variables following the intermittent isometric fatiguing exercise (P < 0.05), when post-exercise reliability was considered, the exercise effect on VATMS was smaller than the smallest detectable change in 18 of the 20 individual tests performed, and for the whole sample for one of two visits. Finally, maximal voluntary contraction was reduced significantly following the neuromuscular assessment (NMA) pre-exercise but recovered during the NMA post-exercise.

Conclusion

This is the first study to demonstrate a lack of sensitivity of key neuromuscular measurements to exercise and to evidence both presence of neuromuscular fatigue following the NMA in itself, and recovery of the neuromuscular function during the NMA post-exercise. These results challenge the face validity of this routinely used protocol.

Keywords

Neuromuscular fatigue Central fatigue Exercise Isometric contraction Isokinetic dynanometer 

Abbreviations

ERT

Estimated resting twitch

ICC

Intraclass correlation

KE

Knee extensors

MEP

Motor evoked potential

MVC

Maximal voluntary contractions

NMA

Neuromuscular assessment

POT

Potentiated twitch force

SDC

Smallest detectable change

SIT

Superimposed twitch

SIT100%

Superimposed twitch during a maximal voluntary contraction

TMS

Transcranial magnetic stimulation

VA

Voluntary activation

VATMS

Voluntary activation using transcranial magnetic stimulation

VC

Voluntary contraction

Notes

Acknowledgements

The authors thank Dr. Rosie Twomey and Prof. Guillaume Millet for the valuable critical review of our manuscript.

Author contribution statement

All authors contributed to the conception and design of the study. PA, AGT, JW, LS collected the data. All authors were involved in the analysis and interpretation of the data. JD, AGT and PA wrote the manuscript. All authors reviewed and approved the final version of the manuscript.

Funding

No external funding was received for this work.

Compliance with ethical standards

Conflict of interest

The authors report no conflict of interest for this work.

References

  1. Atkinson G, Nevill AM (1998) Statistical methods for assessing measurement error (reliability) in variables relevant to sports medicine. Sports Med 26:217–238.  https://doi.org/10.2165/00007256-199826040-00002 CrossRefGoogle Scholar
  2. Bachasson D, Temesi J, Gruet M, Yokoyama K, Rupp T, Millet GY, Verges S (2016) Transcranial magnetic stimulation intensity affects exercise-induced changes in corticomotoneuronal excitability and inhibition and voluntary activation. Neuroscience 314:125–133.  https://doi.org/10.1016/j.neuroscience.2015.11.056 CrossRefGoogle Scholar
  3. Beaulieu LD, Flamand VH, Masse-Alarie H, Schneider C (2017) Reliability and minimal detectable change of transcranial magnetic stimulation outcomes in healthy adults: a systematic review. Brain Stimul 10:196–213.  https://doi.org/10.1016/j.brs.2016.12.008 CrossRefGoogle Scholar
  4. Brownstein CG, Dent JP, Parker P, Hicks KM, Howatson G, Goodall S, Thomas K (2017) Etiology and recovery of neuromuscular fatigue following competitive soccer match-play. Front Physiol 8:831.  https://doi.org/10.3389/Fphys.2017.00831 CrossRefGoogle Scholar
  5. Carroll TJ, Taylor JL, Gandevia SC (2017) Recovery of central and peripheral neuromuscular fatigue after exercise. J Appl Physiol 122:1068–1076.  https://doi.org/10.1152/japplphysiol.00775.2016 CrossRefGoogle Scholar
  6. Clark BC, Cook SB, Ploutz-Snyder LL (2007) Reliability of techniques to assess human neuromuscular function in vivo. J Electromyogr Kines 17:90–101.  https://doi.org/10.1016/j.jelekin.2005.11.008 CrossRefGoogle Scholar
  7. Contessa P, Puleo A, De Luca CJ (2016) Is the notion of central fatigue based on a solid foundation? J Neurophysiol 115:967–977.  https://doi.org/10.1152/jn.00889.2015 CrossRefGoogle Scholar
  8. Di Lazzaro V et al (1998) Effects of voluntary contraction on descending volleys evoked by transcranial stimulation in conscious humans. J Physiol 508(Pt 2):625–633CrossRefGoogle Scholar
  9. Froyd C, Millet GY, Noakes TD (2013) The development of peripheral fatigue and short-term recovery during self-paced high-intensity exercise. J Physiol 591:1339–1346.  https://doi.org/10.1113/jphysiol.2012.245316 CrossRefGoogle Scholar
  10. Gandevia SC (2001) Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 81:1725–1789CrossRefGoogle Scholar
  11. Gandevia SC, Allen GM, Butler JE, Taylor JL (1996) Supraspinal factors in human muscle fatigue: Evidence for suboptimal output from the motor cortex. J Physiol 490:529–536.  https://doi.org/10.1113/jphysiol.1996.sp021164 CrossRefGoogle Scholar
  12. Girard O, Racinais S (2014) Combining heat stress and moderate hypoxia reduces cycling time to exhaustion without modifying neuromuscular fatigue characteristics. Eur J Appl Physiol 114:1521–1532.  https://doi.org/10.1007/s00421-014-2883-0 CrossRefGoogle Scholar
  13. Girard O, Bishop DJ, Racinais S (2013) Hot conditions improve power output during repeated cycling sprints without modifying neuromuscular fatigue characteristics. Eur J Appl Physiol 113:359–369.  https://doi.org/10.1007/s00421-012-2444-3 CrossRefGoogle Scholar
  14. Goodall S, Romer LM, Ross EZ (2009) Voluntary activation of human knee extensors measured using transcranial magnetic stimulation. Exp Physiol 94:995–1004.  https://doi.org/10.1113/expphysiol.2009.047902 CrossRefGoogle Scholar
  15. Goodall S, Ross EZ, Romer LM (2010) Effect of graded hypoxia on supraspinal contributions to fatigue with unilateral knee-extensor contractions. J Appl Physiol 109:1842–1851.  https://doi.org/10.1152/japplphysiol.00458.2010 CrossRefGoogle Scholar
  16. Goodall S et al (2017) The assessment of neuromuscular fatigue during 120 min of simulated soccer exercise. Eur J Appl Physiol 117:687–697.  https://doi.org/10.1007/s00421-017-3561-9 CrossRefGoogle Scholar
  17. Green S, Robinson E, Wallis E (2014) Assessment of calf muscle fatigue during submaximal exercise using transcranial magnetic stimulation versus transcutaneous motor nerve stimulation. Eur J Appl Physiol 114:113–121.  https://doi.org/10.1007/s00421-013-2757-x CrossRefGoogle Scholar
  18. Gruet M, Temesi J, Rupp T, Levy P, Verges S, Millet GY (2014) Dynamics of corticospinal changes during and after high-intensity quadriceps exercise. Exp Physiol 99:1053–1064.  https://doi.org/10.1113/expphysiol.2014.078840 CrossRefGoogle Scholar
  19. Hermens HJ, Freriks B, Disselhorst-Klug C, Rau G (2000) Development of recommendations for SEMG sensors and sensor placement procedures. J Electromyogr Kines 10:361–374.  https://doi.org/10.1016/S1050-6411(00)00027-4 CrossRefGoogle Scholar
  20. Hopkins WG (2000) Measures of reliability in sports medicine and science. Sports Med 30:1–15.  https://doi.org/10.2165/00007256-200030010-00001 CrossRefGoogle Scholar
  21. Hunter SK, Butler JE, Todd G, Gandevia SC, Taylor JL (2006) Supraspinal fatigue does not explain the sex difference in muscle fatigue of maximal contractions. J Appl Physiol 101:1036–1044.  https://doi.org/10.1152/japplphysiol.00103.2006 CrossRefGoogle Scholar
  22. Johnson MA, Sharpe GR, Williams NC, Hannah R (2015) Locomotor muscle fatigue is not critically regulated after prior upper body exercise. J Appl Physiol 119:840–850.  https://doi.org/10.1152/japplphysiol.00072.2015 CrossRefGoogle Scholar
  23. Jubeau M et al (2014) Changes in voluntary activation assessed by transcranial magnetic stimulation during prolonged cycling exercise. Plos One 9:e89157.  https://doi.org/10.1371/journal.pone.0089157 CrossRefGoogle Scholar
  24. Kufel TJ, Pineda LA, Mador MJ (2002) Comparison of potentiated and unpotentiated twitches as an index of muscle fatigue. Muscle Nerve 25:438–444.  https://doi.org/10.1002/mus.10047 CrossRefGoogle Scholar
  25. Lagan J, Lang P, Strutton PH (2008) Measurement of voluntary activation of the back muscles using transcranial magnetic stimulation. Clin Neurophysiol 119:2839–2845.  https://doi.org/10.1016/j.clinph.2008.09.013 CrossRefGoogle Scholar
  26. Lee M, Gandevia SC, Carroll TJ (2008) Cortical voluntary activation can be reliably measured in human wrist extensors using transcranial magnetic stimulation. Clin Neurophysiol 119:1130–1138.  https://doi.org/10.1016/j.clinph.2007.12.018 CrossRefGoogle Scholar
  27. Maffiuletti NA, Bizzini M, Desbrosses K, Babault N, Munzinger U (2007) Reliability of knee extension and flexion measurements using the Con-Trex isokinetic dynamometer. Clin Physiol Funct I 27:346–353.  https://doi.org/10.1111/j.1475-097X.2007.00758.x CrossRefGoogle Scholar
  28. McGraw KO, Wong SP (1996) Forming inferences about some intraclass correlation coefficients. Psychol Methods 1:30–46.  https://doi.org/10.1037/1082-989x.1.1.30 CrossRefGoogle Scholar
  29. Merton PA (1954) Voluntary strength and fatigue. J Physiol 123:553–564CrossRefGoogle Scholar
  30. Mira J, Lapole T, Souron R, Messonnier L, Millet GY, Rupp T (2017) Cortical voluntary activation testing methodology impacts central fatigue. Eur J Appl Physiol 117:1845–1857.  https://doi.org/10.1007/s00421-017-3678-x CrossRefGoogle Scholar
  31. Mokkink LB et al (2010) The COSMIN checklist for assessing the methodological quality of studies on measurement properties of health status measurement instruments: an international Delphi study. Qual Life Res 19:539–549.  https://doi.org/10.1007/s11136-010-9606-8 CrossRefGoogle Scholar
  32. O’Leary TJ, Morris MG, Collett J, Howells K (2016) Central and peripheral fatigue following non-exhaustive and exhaustive exercise of disparate metabolic demands. Scand J Med Sci Spor 26:1287–1300.  https://doi.org/10.1111/sms.12582 CrossRefGoogle Scholar
  33. Peacock B, Westers T, Walsh S, Nicholson K (1981) Feedback and maximum voluntary contraction. Ergonomics 24:223–228.  https://doi.org/10.1080/00140138108559236 CrossRefGoogle Scholar
  34. Periard JD, Christian RJ, Knez WL, Racinais S (2014) Voluntary muscle and motor cortical activation during progressive exercise and passively induced hyperthermia. Exp Physiol 99:136–148.  https://doi.org/10.1113/expphysiol.2013.074583 CrossRefGoogle Scholar
  35. Rossi S, Hallett M, Rossini PM, Pascual-Leone A (2011) Screening questionnaire before TMS: an update. Clin Neurophysiol 122:1686–1686.  https://doi.org/10.1016/j.clinph.2010.12.037 CrossRefGoogle Scholar
  36. Schambra HM et al (2015) The reliability of repeated TMS measures in older adults and in patients with subacute and chronic stroke. Front Cell Neurosci 9:335.  https://doi.org/10.3389/Fncel.2015.00335 CrossRefGoogle Scholar
  37. Sidhu SK, Bentley DJ, Carroll TJ (2009a) Cortical voluntary activation of the human knee extensors can be reliably estimated using transcranial magnetic stimulation. Muscle Nerve 39:186–196.  https://doi.org/10.1002/mus.21064 CrossRefGoogle Scholar
  38. Sidhu SK, Bentley DJ, Carroll TJ (2009b) Locomotor exercise induces long-lasting impairments in the capacity of the human motor cortex to voluntarily activate knee extensor muscles. J Appl Physiol 106:556–565.  https://doi.org/10.1152/japplphysiol.90911.2008 CrossRefGoogle Scholar
  39. Sogaard K, Gandevia SC, Todd G, Petersen NT, Taylor JL (2006) The effect of sustained low-intensity contractions on supraspinal fatigue in human elbow flexor muscles. J Physiol 573:511–523.  https://doi.org/10.1113/jphysiol.2005.103598 CrossRefGoogle Scholar
  40. Tamm AS, Lagerquist O, Ley AL, Collins DF (2009) Chronotype influences diurnal variations in the excitability of the human motor cortex and the ability to generate torque during a maximum voluntary contraction. J Biol Rhythm 24:211–224.  https://doi.org/10.1177/0748730409334135 CrossRefGoogle Scholar
  41. Taylor JL, Todd G, Gandevia SC (2006) Evidence for a supraspinal contribution to human muscle fatigue. Clin Exp Pharmacol P 33:400–405.  https://doi.org/10.1111/j.1440-1681.2006.04363.x CrossRefGoogle Scholar
  42. Terwee CB, Mokkink LB, van Poppel MNM, Chinapaw MJM, van Mechelen W, de Vet HCW (2010) Qualitative attributes and measurement properties of physical activity questionnaires A checklist. Sports Med 40:525–537.  https://doi.org/10.2165/11531370-000000000-00000 CrossRefGoogle Scholar
  43. Thomas K, Goodall S, Stone M, Howatson G, Gibson AS, Ansley L (2015) Central and peripheral fatigue in male cyclists after 4-, 20-, and 40-km time trials. Med Sci Sport Exerc 47:537–546.  https://doi.org/10.1249/Mss.0000000000000448 CrossRefGoogle Scholar
  44. Thomas K, Elmeua M, Howatson G, Goodall S (2016) Intensity-dependent contribution of neuromuscular fatigue after constant-load cycling. Med Sci Sport Exer 48:1751–1760.  https://doi.org/10.1249/Mss.0000000000000950 CrossRefGoogle Scholar
  45. Todd G, Taylor JL, Gandevia SC (2003) Measurement of voluntary activation of fresh and fatigued human muscles using transcranial magnetic stimulation. J Physiol 551:661–671.  https://doi.org/10.1113/jphysiol.2003.044099 CrossRefGoogle Scholar
  46. Todd G, Taylor JL, Gandevia SC (2004) Reproducible measurement of voluntary activation of human elbow flexors with motor cortical stimulation. J Appl Physiol 97:236–242.  https://doi.org/10.1152/japplphysiol.01336.2003 CrossRefGoogle Scholar
  47. Todd G, Taylor JL, Butler JE, Martin PG, Gorman RB, Gandevia SC (2007) Use of motor cortex stimulation to measure simultaneously the changes in dynamic muscle properties and voluntary activation in human muscles. J Appl Physiol 102:1756–1766.  https://doi.org/10.1152/japplphysiol.00962.2006 CrossRefGoogle Scholar
  48. Todd G, Taylor JL, Gandevia SC (2016) Measurement of voluntary activation based on transcranial magnetic stimulation over the motor cortex. J Appl Physiol 121:678–686.  https://doi.org/10.1152/japplphysiol.00293.2016 CrossRefGoogle Scholar
  49. Tok S, Binboğa E, Guven S, Çatıkkas F, Dane S (2013) Trait emotional intelligence, the Big Five personality traits and isometric maximal voluntary contraction level under stress in athletes. Neurol Psychiatry Brain Res 19:133–138.  https://doi.org/10.1016/j.npbr.2013.04.005 CrossRefGoogle Scholar
  50. Ugawa Y, Terao Y, Hanajima R, Sakai K, Kanazawa I (1995) Facilitatory effect of tonic voluntary contraction on responses to motor cortex stimulation. Electromyogr Motor C 97:451–454.  https://doi.org/10.1016/0924-980x(95)00214-6 CrossRefGoogle Scholar
  51. Vigotsky AD, Halperin I, Lehman GJ, Trajano GS, Vieira TM (2017) Interpreting signal amplitudes in surface electromyography studies in sport and rehabilitation sciences. Front Physiol 8:985.  https://doi.org/10.3389/fphys.2017.00985 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Fatigue and Exercise Laboratory, Centre for Sport and Exercise Science and Medicine (SESAME)University of BrightonEastbourneUK
  2. 2.Department of Sport, Exercise and Rehabilitation, Faculty of Health and Life SciencesNorthumbria UniversityNorthumbriaUK
  3. 3.Human Performance Laboratory, Faculty of KinesiologyUniversity of CalgaryCalgaryCanada

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