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European Journal of Applied Physiology

, Volume 115, Issue 11, pp 2311–2319 | Cite as

The effect of transcranial direct current stimulation of the motor cortex on exercise-induced pain

  • Luca Angius
  • James G. Hopker
  • Samuele M. Marcora
  • Alexis R. Mauger
Original Article

Abstract

Purpose

Transcranial direct current stimulation (tDCS) provides a new exciting means to investigate the role of the brain during exercise. However, this technique is not widely used in exercise science, with little known regarding effective electrode montages. This study investigated whether tDCS of the motor cortex (M1) would elicit an analgesic response to exercise-induced pain (EIP).

Methods

Nine participants completed a VO2max test and three time to exhaustion (TTE) tasks on separate days following either 10 min 2 mA tDCS of the M1, a sham or a control. Additionally, seven participants completed 3 cold pressor tests (CPT) following the same experimental conditions (tDCS, SHAM, CON). Using a well-established tDCS protocol, tDCS was delivered by placing the anodal electrode above the left M1 with the cathodal electrode above dorsolateral right prefrontal cortex. Gas exchange, blood lactate, EIP and ratings of perceived exertion (RPE) were monitored during the TTE test. Perceived pain was recorded during the CPT.

Results

During the TTE, no significant differences in time to exhaustion, RPE or EIP were found between conditions. However, during the CPT, perceived pain was significantly (P < 0.05) reduced in the tDCS condition (7.4 ± 1.2) compared with both the CON (8.6 ± 1.0) and SHAM (8.4 ± 1.3) conditions.

Conclusion

These findings demonstrate that stimulation of the M1 using tDCS does not induce analgesia during exercise, suggesting that the processing of pain produced via classic measures of experimental pain (i.e., a CPT) is different to that of EIP. These results provide important methodological advancement in developing the use of tDCS in exercise.

Keywords

Fatigue Pain perception Performance tDCS Exercise 

Abbreviations

B[La−1]

Blood lactate concentration

CON

Control condition

CPT

Cold pressor test

DLPFC

Dorsolateral prefrontal cortex

EIP

Exercise-induced pain

EXP

Experimental condition (tDCS intervention)

M1

Motor cortex

RPE

Rating of perceived exertion

tDCS

Transcranial direct current stimulation

TTE

Time to exhaustion

Notes

Conflict of interest

None.

References

  1. Almeida TF, Roizenblatt S, Tufik S (2004) Afferent pain pathways: a neuroanatomical review. Brain Res 1000:40–56CrossRefPubMedGoogle Scholar
  2. Amann M, Proctor LT, Sebranek JJ, Pegelow DF, Dempsey JA (2009) Opioid-mediated muscle afferents inhibit central motor drive and limit peripheral muscle fatigue development in humans. J Physiol 15:271–283CrossRefGoogle Scholar
  3. Amann M, Blain GM, Proctor LT, Sebranek JJ, Pegelow DF, Dempsey JA (2011) Implications of group III and IV muscle afferents for high-intensity endurance exercise performance in humans. J Physiol (1)589: 299–309Google Scholar
  4. Bachmann CG, Muschinsky S, Nitsche MA, Rolke R, Magerl W, Treede RD, Paulus W, Happe S (2010) Transcranial direct current stimulation of the motor cortex induces distinct changes in thermal and mechanical sensory percepts. Clin Neurophysiol 212:2083–2089CrossRefGoogle Scholar
  5. Boggio PS, Zaghi S, Lopes M, Fregni F (2008) Modulatory effects of anodal transcranial direct current stimulation on perception and pain thresholds in healthy volunteers. Eur J Neurol 15(10):1124–1130CrossRefPubMedGoogle Scholar
  6. Boggio PS, Zaghi S, Fregni F (2009) Modulation of emotions associated with the images of human pain using anodal transcranial direct current stimulation (tDCS). Neuropsychologica 47:212–217CrossRefGoogle Scholar
  7. Borg GA (1998) Borg’s perceived exertion and pain scales. Human Kinetics, ChampaignGoogle Scholar
  8. Brodal A (1981) Neurological anatomy, 3rd edn. Oxford University Press, New YorkGoogle Scholar
  9. Chen AC, Rappelsberger P, Filz O (1998) Topology of EEG coherence changes may reflect differential neural network activation in cold and pain perception. Brain Topogr 11(2):125–132CrossRefPubMedGoogle Scholar
  10. Cogiamanian F, Marceglia S, Ardolin G, Barbieri S, Priori A (2007) Improved isometric force endurance after transcranial direct current stimulation over the human motor cortical areas. Eur J Neurosci 26:242–24910CrossRefPubMedGoogle Scholar
  11. Cook DB, O’Connor PJ, Eubanks SA, Smith JC, Lee M (1997) Naturally occurring muscle pain during exercise: assessment and experimental evidence. Med Sci Sports Exerc 29(8):999–1012CrossRefPubMedGoogle Scholar
  12. Craig AD, Bushnell MC, Zhang ET, Blomqvist A (1994) A thalamic nucleus specific for pain and temperature sensation. Nature 22–29:372Google Scholar
  13. Foster J, Taylor L, Chrismas BC, Watkins SL, Mauger AR (2014) The influence of acetaminophen on repeated sprint cycling performance. Eur J Appl Physiol 114(1):41–48CrossRefPubMedGoogle Scholar
  14. García-Larrea L, Peyron R, Mertens P, Grégoire MC, Lavenne F, Bonnefoi F, Mauguière F, Laurent B, Sindou M (1997) Positron emission tomography during motor cortex stimulation for pain control. Stereotact Funct Neurosurg 68(1–4 Pt 1):141–148CrossRefPubMedGoogle Scholar
  15. García-Larrea L, Peyron R, Mertens P, Gregoire MC, Lavenne F, Le Bars D, Convers P, Mauguière F, Sindou M, Laurent B (1999) Electrical stimulation of motor cortex for pain control: a combined PET-scan and electrophysiological study. Pain 83(2):259–273CrossRefPubMedGoogle Scholar
  16. Hollander DB, Reeves GV, Clavier JD, Francois MR, Thomas C, Kraemer RR (2010) Partial occlusion during resistance exercise alters effort sense and pain. J Strength Cond Res 24(1):235–243CrossRefPubMedGoogle Scholar
  17. Kaufman MP (2012) The exercise pressor reflex in animals. Exp Physiol 97(1):51–58CrossRefPubMedGoogle Scholar
  18. Khan SI, McNeil CJ, Gandevia SC, Taylor JL (2011) Effect of experimental muscle pain on maximal voluntary activation of human biceps brachii muscle. J Appl Physiol 111(3):743–750CrossRefPubMedGoogle Scholar
  19. Lampropoulou SI, Nowicky AV (2013) The effect of transcranial direct current stimulation on perception of effort in an isolated isometric elbow flexion task. Mot Control 17(4):412–426Google Scholar
  20. Lang N, Siebner HR, Ward NS, Lee L, Nitsche MA, Paulus W, Rothwell JC, Lemon RN, Frackowiak RS (2005) How does transcranial DC stimulation of the primary motor cortex alter regional neuronal activity in the human brain? Eur J Neurosci 22:495–504PubMedCentralCrossRefPubMedGoogle Scholar
  21. Lefaucheur JP, Antal A, Ahdab R, Ciampi de Andrade D, Fregni F, Khedr EM, Nitsche M, Paulus W (2008) The use of repetitive transcranial magnetic stimulation (rTMS) and transcranial direct current stimulation (tDCS) to relieve pain. Brain Stimul 1(4):337–344CrossRefPubMedGoogle Scholar
  22. Linton SJ, Shaw WS (2001) Impact of psychological factors in the experience of pain. Phys Ther 91(5):700–711CrossRefGoogle Scholar
  23. Lorenz J, Minoshima S, Casey KL (2003) Keeping pain out of the mind: the role of the dorsolateral prefrontal cortex in pain modulation. Brain 126(5):1079–1091CrossRefPubMedGoogle Scholar
  24. Mauger AR (2013) Fatigue is a pain—the use of novel neurophysiological techniques to understand the fatigue-pain relationship. Front Physiol 13(4):104Google Scholar
  25. Mauger AR (2014) Factors affecting the regulation of pacing: current perspectives. Open Access J Sports Med 5:209PubMedCentralCrossRefPubMedGoogle Scholar
  26. Mauger AR, Hopker JG (2013) The effect of acetaminophen ingestion on cortico-spinal excitability. Can J Physiol Pharmacol 91(2):187–189CrossRefPubMedGoogle Scholar
  27. Mauger AR, Jones AM, Williams CA (2010) Influence of acetaminophen on performance during time trial cycling. J Appl Physiol 98(1):104Google Scholar
  28. Mauger AR, Taylor L, Harding C, Wright B, Foster J, Castle PC (2014) Acute acetaminophen (paracetamol) ingestion improves time to exhaustion during exercise in the heat. Exp Physiol 99(1):164–171CrossRefPubMedGoogle Scholar
  29. Millan MJ (2002) Descending control of pain. Prog Neurobiol 66(6):355–474CrossRefPubMedGoogle Scholar
  30. Muthalib M, Kan B, Nosaka K, Perrey S (2013) Effects of transcranial direct current stimulation of the motor cortex on prefrontal cortex activation during a neuromuscular fatigue task: an fNIRS study. Adv Exp Med Biol 789:73–79CrossRefPubMedGoogle Scholar
  31. Mylius V, Ayache SS, Zouari HG, Aoun-Sebaïti M, Farhat WH, Lefaucheur JP (2012) Stroke rehabilitation using noninvasive cortical stimulation: hemispatial neglect. Expert Rev Neurother 12(8):983–991CrossRefPubMedGoogle Scholar
  32. Nijs J, Kosek E, Van Oosterwijck J, Meeus M (2012) Dysfunctional endogenous analgesia during exercise in patients with chronic pain: to exercise or not to exercise? Pain Physician 15(3):205–213Google Scholar
  33. Nitsche MA, Cohen LG, Wassermann EM, Priori A, Lang N, Antal A, Paulus W, Hummel F, Boggio PS, Fregni F, Pascual-Leone A (2008) Transcranial direct current stimulation: State of the art. Brain Stimul 1(3):206–223CrossRefPubMedGoogle Scholar
  34. Noakes TD (2012) Fatigue is a brain-derived emotion that regulates the exercise behavior to ensure the protection of whole body homeostasis. Front Physiol 11(3):82Google Scholar
  35. O’Connor PJ, Cook DB (1999) Exercise and pain: the neurobiology, measurement, and laboratory study of pain in relation to exercise in humans. Exerc Sport Sci Rev 27:119–166CrossRefPubMedGoogle Scholar
  36. Okano AH, Fontes EB, Montenegro RA, Farinatti PD, Cyrino ES, Li LM, Bikson M, Noakes TD (2013) Brain stimulation modulates the autonomic nervous system, rating of perceived exertion and performance during maximal exercise. Br J Sports Med. doi: 10.1136/bjsports-2012-091658
  37. Olesen AE, Andresen T, Staahl C, Drewes AM (2012) Human experimental pain models for assessing the therapeutic efficacy of analgesic drugs. Pharmacol Rev 64(3):722–779CrossRefPubMedGoogle Scholar
  38. Peyron R, Laurent B, García-Larrea L (2000) Functional imaging of brain responses to pain. A review and meta-analysis. Neurophysiol Clin 30(5):263–288CrossRefPubMedGoogle Scholar
  39. Reis J, Fritsch B (2011) Modulation of motor performance and motor learning by transcranial direct current stimulation. Curr Opin Neurol 24(6):590–596CrossRefPubMedGoogle Scholar
  40. Schestatsky P, Simis M, Freeman R, Pascual-Leone A, Fregni F (2013) Non-invasive brain stimulation and the autonomic nervous system. Clin Neurophysiol 124(9):1716–1728CrossRefPubMedGoogle Scholar
  41. St Clair Gibson A, Noakes TD (2004) Evidence for complex system integration and dynamic neural regulation of skeletal muscle recruitment during exercise in humans. Br J Sports Med 38(6):797–806CrossRefPubMedGoogle Scholar
  42. Stepniewska I, Preuss TM, Kaas JH (1994) Thalamic connections of the primary motor cortex (M1) of owl monkeys. J Comp Neurol 349(4):558–582CrossRefPubMedGoogle Scholar
  43. Svensson P, Minoshima S, Beydoun A, Morrow TJ, Casey KL (1997) Cerebral processing of acute skin and muscle pain in humans. J Neurophysiol 78(1):450–460PubMedGoogle Scholar
  44. Wardman DL, Gandevia SC, Colebatch JG (2014) Cerebral, subcortical, and cerebellar activation evoked by selective stimulation of muscle and cutaneous afferents: an fMRI study. Physiol Rep 2(4):e00270PubMedCentralPubMedGoogle Scholar
  45. Zandieh A, Parhizgar SE, Fakhri M, Taghvaei M, Miri S, Shahbabaie A, Esteghamati S, Ekhtiari H (2013) Modulation of cold pain perception by transcranial direct current stimulation in healthy individuals. Neuromodulation 16(4):345–348CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Luca Angius
    • 1
  • James G. Hopker
    • 1
  • Samuele M. Marcora
    • 1
  • Alexis R. Mauger
    • 1
  1. 1.Endurance Research Group, School of Sport and Exercise Sciences, Faculty of ScienceUniversity of KentKentUK

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