Table of Contents Author Guidelines Submit a Manuscript
Neural Plasticity
Volume 2018, Article ID 8713218, 7 pages
https://doi.org/10.1155/2018/8713218
Research Article

Effect of Cutaneous Heat Pain on Corticospinal Excitability of the Tibialis Anterior at Rest and during Submaximal Contraction

1Department of Rehabilitation, Université Laval, 1050 Avenue de la Médecine, Quebec City, QC, Canada G1V 0A6
2Center for Interdisciplinary Research in Rehabilitation and Social Integration (CIRRIS), 525 Boul. Wilfrid-Hamel, Quebec City, QC, Canada G1M 2S8

Correspondence should be addressed to Laurent J. Bouyer; ac.lavalu.aer@reyuob.tnerual

Received 15 December 2017; Accepted 27 March 2018; Published 26 April 2018

Academic Editor: Isaac O. Sorinola

Copyright © 2018 Maxime Billot et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. E. Sens, C. Knorr, C. Preul et al., “Differences in somatosensory and motor improvement during temporary functional deafferentation in stroke patients and healthy subjects,” Behavioural Brain Research, vol. 252, pp. 110–116, 2013. View at Publisher · View at Google Scholar · View at Scopus
  2. N. Mavromatis, M. Gagné, J. I. A. V. Voisin, K. T. Reilly, and C. Mercier, “Experimental tonic hand pain modulates the corticospinal plasticity induced by a subsequent hand deafferentation,” Neuroscience, vol. 330, pp. 403–409, 2016. View at Publisher · View at Google Scholar · View at Scopus
  3. V. M. Grant, A. Gibson, and N. Shields, “Somatosensory stimulation to improve hand and upper limb function after stroke—a systematic review with meta-analyses,” Topics in Stroke Rehabilitation, vol. 25, no. 2, pp. 150–160, 2017. View at Publisher · View at Google Scholar
  4. J. P. Lund, R. Donga, C. G. Widmer, and C. S. Stohler, “The pain-adaptation model: a discussion of the relationship between chronic musculoskeletal pain and motor activity,” Canadian Journal of Physiology and Pharmacology, vol. 69, no. 5, pp. 683–694, 1991. View at Publisher · View at Google Scholar · View at Scopus
  5. P. W. Hodges and K. Tucker, “Moving differently in pain: a new theory to explain the adaptation to pain,” Pain, vol. 152, no. 3, pp. S90–S98, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. M. J. Simmonds and B. Degenhardt, “Pain, mind, and movement: unraveling models, shifting paradigms, and the social dimension,” The Clinical Journal of Pain, vol. 28, no. 6, pp. 465-466, 2012. View at Publisher · View at Google Scholar · View at Scopus
  7. P. J. M. Bank, C. E. Peper, J. Marinus, P. J. Beek, and J. J. Van Hilten, “Motor consequences of experimentally induced limb pain: a systematic review,” European Journal of Pain, vol. 17, no. 2, pp. 145–157, 2013. View at Publisher · View at Google Scholar · View at Scopus
  8. S. A. Boudreau, K. Hennings, P. Svensson, B. J. Sessle, and L. Arendt-Nielsen, “The effects of training time, sensory loss and pain on human motor learning,” Journal of Oral Rehabilitation, vol. 37, no. 9, pp. 704–718, 2010. View at Publisher · View at Google Scholar · View at Scopus
  9. S. Boudreau, A. Romaniello, K. Wang, P. Svensson, B. J. Sessle, and L. Arendt-Nielsen, “The effects of intra-oral pain on motor cortex neuroplasticity associated with short-term novel tongue-protrusion training in humans,” Pain, vol. 132, no. 1, pp. 169–178, 2007. View at Publisher · View at Google Scholar · View at Scopus
  10. E. Dancey, B. A. Murphy, D. Andrew, and P. Yielder, “The effect of local vs remote experimental pain on motor learning and sensorimotor integration using a complex typing task,” Pain, vol. 157, no. 8, pp. 1682–1695, 2016. View at Publisher · View at Google Scholar · View at Scopus
  11. E. Dancey, B. Murphy, D. Andrew, and P. Yielder, “Interactive effect of acute pain and motor learning acquisition on sensorimotor integration and motor learning outcomes,” Journal of Neurophysiology, vol. 116, no. 5, pp. 2210–2220, 2016. View at Publisher · View at Google Scholar · View at Scopus
  12. J. Bouffard, L. J. Bouyer, J.-S. Roy, and C. Mercier, “Tonic pain experienced during locomotor training impairs retention despite normal performance during acquisition,” The Journal of Neuroscience, vol. 34, no. 28, pp. 9190–9195, 2014. View at Publisher · View at Google Scholar · View at Scopus
  13. J. Bouffard, L. J. Bouyer, J. S. Roy, and C. Mercier, “Pain induced during both the acquisition and retention phases of locomotor adaptation does not interfere with improvements in motor performance,” Neural Plasticity, vol. 2016, Article ID 8539096, 9 pages, 2016. View at Publisher · View at Google Scholar · View at Scopus
  14. M. Lamothe, J.-S. Roy, J. Bouffard, M. Gagné, L. J. Bouyer, and C. Mercier, “Effect of tonic pain on motor acquisition and retention while learning to reach in a force field,” PLoS One, vol. 9, no. 6, article e99159, 2014. View at Publisher · View at Google Scholar · View at Scopus
  15. M. C. Bilodeau, M. Roosink, and C. Mercier, “Effect of local versus remote tonic heat pain during training on acquisition and retention of a finger-tapping sequence task,” Experimental Brain Research, vol. 234, no. 2, pp. 475–482, 2016. View at Publisher · View at Google Scholar · View at Scopus
  16. N. Mavromatis, C. Neige, M. Gagné, K. Reilly, and C. Mercier, “Effect of experimental hand pain on training-induced changes in motor performance and corticospinal excitability,” Brain Sciences, vol. 7, no. 12, p. 15, 2017. View at Publisher · View at Google Scholar · View at Scopus
  17. E. Dancey, B. Murphy, J. Srbely, and P. Yielder, “The effect of experimental pain on motor training performance and sensorimotor integration,” Experimental Brain Research, vol. 232, no. 9, pp. 2879–2889, 2014. View at Publisher · View at Google Scholar · View at Scopus
  18. J. A. Dubé and C. Mercier, “Effect of pain and pain expectation on primary motor cortex excitability,” Clinical Neurophysiology, vol. 122, no. 11, pp. 2318–2323, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. S. Farina, M. Valeriani, T. Rosso et al., “Transient inhibition of the human motor cortex by capsaicin-induced pain. A study with transcranial magnetic stimulation,” Neuroscience Letters, vol. 314, no. 1-2, pp. 97–101, 2001. View at Publisher · View at Google Scholar · View at Scopus
  20. S. Farina, M. Tinazzi, D. Le Pera, and M. Valeriani, “Pain-related modulation of the human motor cortex,” Neurological Research, vol. 25, no. 2, pp. 130–142, 2003. View at Publisher · View at Google Scholar · View at Scopus
  21. D. Le Pera, T. Graven-Nielsen, M. Valeriani et al., “Inhibition of motor system excitability at cortical and spinal level by tonic muscle pain,” Clinical Neurophysiology, vol. 112, no. 9, pp. 1633–1641, 2001. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Valeriani, D. Restuccia, V. di Lazzaro et al., “Inhibition of the human primary motor area by painful heat stimulation of the skin,” Clinical Neurophysiology, vol. 110, no. 8, pp. 1475–1480, 1999. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Valeriani, D. Restuccia, V. Di Lazzaro et al., “Inhibition of biceps brachii muscle motor area by painful heat stimulation of the skin,” Experimental Brain Research, vol. 139, no. 2, pp. 168–172, 2001. View at Publisher · View at Google Scholar · View at Scopus
  24. C. Mercier, M. Gagné, K. Reilly, and L. Bouyer, “Effect of experimental cutaneous hand pain on corticospinal excitability and short afferent inhibition,” Brain Sciences, vol. 6, no. 4, p. 45, 2016. View at Publisher · View at Google Scholar · View at Scopus
  25. F. Del Santo, F. Gelli, R. Spidalieri, and A. Rossi, “Corticospinal drive during painful voluntary contractions at constant force output,” Brain Research, vol. 1128, no. 1, pp. 91–98, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. D. A. Rice, T. Graven-Nielsen, G. N. Lewis, P. J. McNair, and N. Dalbeth, “The effects of experimental knee pain on lower limb corticospinal and motor cortex excitability,” Arthritis Research & Therapy, vol. 17, no. 1, p. 204, 2015. View at Publisher · View at Google Scholar · View at Scopus
  27. H. Tsao, K. J. Tucker, and P. W. Hodges, “Changes in excitability of corticomotor inputs to the trunk muscles during experimentally-induced acute low back pain,” Neuroscience, vol. 181, pp. 127–133, 2011. View at Publisher · View at Google Scholar · View at Scopus
  28. S. M. Schabrun, E. Jones, J. Kloster, and P. W. Hodges, “Temporal association between changes in primary sensory cortex and corticomotor output during muscle pain,” Neuroscience, vol. 235, pp. 159–164, 2013. View at Publisher · View at Google Scholar · View at Scopus
  29. A. Romaniello, G. Cruccu, A. S. McMillan, L. Arendt-Nielsen, and P. Svensson, “Effect of experimental pain from trigeminal muscle and skin on motor cortex excitability in humans,” Brain Research, vol. 882, no. 1-2, pp. 120–127, 2000. View at Publisher · View at Google Scholar · View at Scopus
  30. L. Fadiga, L. Craighero, G. Dri, P. Facchin, M. F. Destro, and C. A. Porro, “Corticospinal excitability during painful self-stimulation in humans: a transcranial magnetic stimulation study,” Neuroscience Letters, vol. 361, no. 1–3, pp. 250–253, 2004. View at Publisher · View at Google Scholar · View at Scopus
  31. M. Kofler, F. X. Glocker, A. A. Leis et al., “Modulation of upper extremity motoneurone excitability following noxious finger tip stimulation in man: a study with transcranial magnetic stimulation,” Neuroscience Letters, vol. 246, no. 2, pp. 97–100, 1998. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Kofler, P. Fuhr, A. A. Leis et al., “Modulation of upper extremity motor evoked potentials by cutaneous afferents in humans,” Clinical Neurophysiology, vol. 112, no. 6, pp. 1053–1063, 2001. View at Publisher · View at Google Scholar · View at Scopus
  33. P. P. Urban, M. Solinski, C. Best, R. Rolke, H. C. Hopf, and M. Dieterich, “Different short-term modulation of cortical motor output to distal and proximal upper-limb muscles during painful sensory nerve stimulation,” Muscle and Nerve, vol. 29, no. 5, pp. 663–669, 2004. View at Publisher · View at Google Scholar · View at Scopus
  34. S. Ngomo, G. Leonard, H. Moffet, and C. Mercier, “Comparison of transcranial magnetic stimulation measures obtained at rest and under active conditions and their reliability,” Journal of Neuroscience Methods, vol. 205, no. 1, pp. 65–71, 2012. View at Publisher · View at Google Scholar · View at Scopus
  35. B. Fierro, M. De Tommaso, F. Giglia, G. Giglia, A. Palermo, and F. Brighina, “Repetitive transcranial magnetic stimulation (rTMS) of the dorsolateral prefrontal cortex (DLPFC) during capsaicin-induced pain: modulatory effects on motor cortex excitability,” Experimental Brain Research, vol. 203, no. 1, pp. 31–38, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. M. Martel, M.-P. Harvey, F. Houde, F. Balg, P. Goffaux, and G. Léonard, “Unravelling the effect of experimental pain on the corticomotor system using transcranial magnetic stimulation and electroencephalography,” Experimental Brain Research, vol. 235, no. 4, pp. 1223–1231, 2017. View at Publisher · View at Google Scholar · View at Scopus
  37. L. Halkjaer, B. Melsen, A. S. McMillan, and P. Svensson, “Influence of sensory deprivation and perturbation of trigeminal afferent fibers on corticomotor control of human tongue musculature,” Experimental Brain Research, vol. 170, no. 2, pp. 199–205, 2006. View at Publisher · View at Google Scholar · View at Scopus
  38. J. Y. Cheong, T. S. Yoon, and S. J. Lee, “Evaluations of inhibitory effect on the motor cortex by cutaneous pain via application of capsaicin,” Electromyography and Clinical Neurophysiology, vol. 43, no. 4, pp. 203–210, 2003. View at Google Scholar
  39. P. G. Martin, N. Weerakkody, S. C. Gandevia, and J. L. Taylor, “Group III and IV muscle afferents differentially affect the motor cortex and motoneurones in humans,” The Journal of Physiology, vol. 586, no. 5, pp. 1277–1289, 2008. View at Publisher · View at Google Scholar · View at Scopus
  40. E. Burns, L. S. Chipchase, and S. M. Schabrun, “Primary sensory and motor cortex function in response to acute muscle pain: a systematic review and meta-analysis,” European Journal of Pain, vol. 20, no. 8, pp. 1203–1213, 2016. View at Publisher · View at Google Scholar · View at Scopus
  41. C. Capaday, B. A. Lavoie, H. Barbeau, C. Schneider, and M. Bonnard, “Studies on the corticospinal control of human walking. I. Responses to focal transcranial magnetic stimulation of the motor cortex,” Journal of Neurophysiology, vol. 81, no. 1, pp. 129–139, 1999. View at Publisher · View at Google Scholar
  42. D. Barthélemy, S. Alain, M. J. Grey, J. B. Nielsen, and L. J. Bouyer, “Rapid changes in corticospinal excitability during force field adaptation of human walking,” Experimental Brain Research, vol. 217, no. 1, pp. 99–115, 2012. View at Publisher · View at Google Scholar · View at Scopus
  43. H. K. Parson, V. T. Nguyen, M.-A. Orciga, A. L. Boyd, C. M. Casellini, and A. I. Vinik, “Contact heat-evoked potential stimulation for the evaluation of small nerve fiber function,” Diabetes Technology & Therapeutics, vol. 15, no. 2, pp. 150–157, 2013. View at Publisher · View at Google Scholar · View at Scopus
  44. A. Stančák, H. Poláček, J. Vrána, and J. Mlynář, “Cortical oscillatory changes during warming and heating in humans,” Neuroscience, vol. 147, no. 3, pp. 842–852, 2007. View at Publisher · View at Google Scholar · View at Scopus
  45. G. Misra, E. Ofori, J. W. Chung, and S. A. Coombes, “Pain-related suppression of beta oscillations facilitates voluntary movement,” Cerebral Cortex, vol. 27, no. 4, pp. 2592–2606, 2017. View at Publisher · View at Google Scholar · View at Scopus
  46. A. Pogosyan, L. D. Gaynor, A. Eusebio, and P. Brown, “Boosting cortical activity at beta-band frequencies slows movement in humans,” Current Biology, vol. 19, no. 19, pp. 1637–1641, 2009. View at Publisher · View at Google Scholar · View at Scopus
  47. R. Chen, A. Tam, C. Bütefisch et al., “Intracortical inhibition and facilitation in different representations of the human motor cortex,” Journal of Neurophysiology, vol. 80, no. 6, pp. 2870–2881, 1998. View at Publisher · View at Google Scholar
  48. B. Brouwer and P. Ashby, “Corticospinal projections to lower limb motoneurons in man,” Experimental Brain Research, vol. 89, no. 3, pp. 649–654, 1992. View at Publisher · View at Google Scholar · View at Scopus