Advertisement

Time course of changes in corticospinal excitability induced by motor imagery during action observation combined with peripheral nerve electrical stimulation

  • Takahito Yasui
  • Tomofumi Yamaguchi
  • Shigeo Tanabe
  • Tsuyoshi Tatemoto
  • Yoko Takahashi
  • Kunitsugu Kondo
  • Michiyuki Kawakami
Research Article
  • 28 Downloads

Abstract

While previous studies assessed corticospinal excitability changes during and after motor imagery (MI) or action observation (AO) combined with peripheral nerve electrical stimulation (ES), we examined, for the first time, the time course of corticospinal excitability changes for MI during AO combined with ES (AO–MI + ES) using transcranial magnetic stimulation to measure motor evoked potentials (MEPs) in healthy individuals. Fourteen healthy volunteers participated in the following three sessions on different days: AO–MI alone, ES alone, and AO–MI + ES. In the AO–MI task, participants imagined squeezing and relaxing a ball, along with the respective actions shown in a movie, while passively holding the ball. We applied ES (intensity, 90% of the motor threshold) to the ulnar nerve at the wrist, which innervates the first dorsal interosseous (FDI) muscle. We assessed the FDI muscle MEPs at baseline and after every 5 min of the task for a total of 20 min. Additionally, participants completed the Vividness of Movement Imagery Questionnaire-2 (VMIQ-2) at the beginning of the experiment. Compared to baseline, AO–MI + ES significantly increased corticospinal excitability after 10 min, while AO–MI or ES alone had no effect on corticospinal excitability after 20 min. Moreover, the AO–MI + ES-induced cortical excitability changes were correlated with the VMIQ-2 scores for visual and kinaesthetic imagery. Collectively, our findings indicate that AO–MI + ES induces cortical plasticity earlier than does AO–MI or ES alone and that an individual’s imagery ability plays an important role in inducing cortical excitability changes following AO–MI + ES.

Keywords

Motor imagery Action observation Peripheral nerve electrical stimulation Neural plasticity Rehabilitation 

Notes

Acknowledgements

This work was partially supported by grants from the Funds for a Grant-in-Aid for Young Scientists (15K16370 and 18K17723) to Tomofumi Yamaguchi and JSPS KAKENHI Grant Number JP16K19521 to Michiyuki Kawakami.

Compliance with ethical standards

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Conflict of interest

The authors declare that they have no conflicts of interest.

References

  1. Abbas AL, Lucas MF, Teixeira S, Paes F, Velasques B, Ribeiro P, Nardi AE, Machado S (2011) Motor imagery and stroke neurorehabilitation: an overview of basic concepts and therapeutic effects. Am J Neurosci 2:59–64Google Scholar
  2. Berends HI, Wolkorte R, Ijzerman MJ, van Putten MJ (2013) Differential cortical activation during observation and observation-and-imagination. Exp Brain Res 229:337–345CrossRefPubMedGoogle Scholar
  3. Bisio A, Avanzino L, Gueugneau N, Pozzo T, Ruggeri P, Bove M (2015a) Observing and perceiving: a combined approach to induce plasticity in human motor cortex. Clin Neurophysiol 126:1212–1220CrossRefPubMedGoogle Scholar
  4. Bisio A, Avanzino L, Lagravinese G, Biggio M, Ruggeri P, Bove M (2015b) Spontaneous movement tempo can be influenced by combining action observation and somatosensory stimulation. Front Behav Neurosci 9:228CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bisio A, Avanzino L, Biggio M, Ruggeri P, Bove M (2017) Motor training and the combination of action observation and peripheral nerve stimulation reciprocally interfere with the plastic changes induced in primary motor cortex excitability. Neuroscience 348:33–40CrossRefPubMedGoogle Scholar
  6. Bonassi G, Biggio M, Bisio A, Ruggeri P, Bove M, Avanzino L (2017) Provision of somatosensory inputs during motor imagery enhances induced plasticity in human motor cortex. Sci Rep 7:9300CrossRefPubMedPubMedCentralGoogle Scholar
  7. Braun SM, Beurskens AJ, Borm PJ, Schack T, Wade DT (2006) The effects of mental practice in stroke rehabilitation: a systematic review. Arch Phys Med Rehabil 87:842–852CrossRefPubMedGoogle Scholar
  8. Calvo-Merino B, Grèzes J, Glaser DE, Passingham RE, Haggard P (2006) Seeing or doing? Influence of visual and motor familiarity in action observation. Curr Biol 16:1905–1910CrossRefPubMedGoogle Scholar
  9. Chipchase LS, Schabrun SM, Hodges PW (2011) Peripheral electrical stimulation to induce cortical plasticity: a systematic review of stimulus parameters. Clin Neurophysiol 122:456–463CrossRefPubMedGoogle Scholar
  10. Corbet T, Iturrate I, Pereira M, Perdikis S, Millán JDR (2018) Sensory threshold neuromuscular electrical stimulation fosters motor imagery performance. Neuroimage 176:268–276CrossRefPubMedGoogle Scholar
  11. de Vries S, Mulder T (2007) Motor imagery and stroke rehabilitation: a critical discussion. J Rehabil Med 39:5–13CrossRefPubMedGoogle Scholar
  12. de Kroon JR, Ijzerman MJ, Chae J, Lankhorst GJ, Zilvold G (2005) Relation between stimulation characteristics and clinical outcome in studies using electrical stimulation to improve motor control of the upper extremity in stroke. J Rehabil Med 37:65–74CrossRefPubMedGoogle Scholar
  13. Eaves DL, Riach M, Holmes PS, Wright DJ (2016) Motor imagery during action observation: a brief review of evidence, theory and future research opportunities. Front Neurosci 10:514CrossRefPubMedPubMedCentralGoogle Scholar
  14. Facchini S, Muellbacher W, Battaglia F, Boroojerdi B, Hallett M (2002) Focal enhancement of motor cortex excitability during motor imagery: a transcranial magnetic stimulation study. Acta Neurol Scand 105:146–151CrossRefPubMedGoogle Scholar
  15. Fujiwara T, Kasashima Y, Honaga K, Muraoka Y, Tsuji T, Osu R, Hase K, Masakado Y, Liu M (2009) Motor improvement and corticospinal modulation induced by hybrid assistive neuromuscular dynamic stimulation (HANDS) therapy in patients with chronic stroke. Neurorehabil Neural Repair 23:125–132CrossRefPubMedGoogle Scholar
  16. Guillot A, Collet C, Nguyen VA, Malouin F, Richards C, Doyon J (2009) Brain activity during visual versus kinesthetic imagery: an fMRI study. Hum Brain Mapp 30:2157–2172CrossRefPubMedGoogle Scholar
  17. Hanakawa T, Immisch I, Toma L, Dimyan MA, Van Gelderen P, Hallett M (2003) Functional properties of brain areas associated with motor execution and imagery. J Neurophysiol 89:989–1002CrossRefPubMedGoogle Scholar
  18. Hanakawa T, Dimyan MA, Hallett M (2008) Motor planning, imagery, and execution in the distributed motor network: a time-course study with functional MRI. Cereb Cortex 18:2775–2788CrossRefPubMedPubMedCentralGoogle Scholar
  19. Hong IK, Choi JB, Lee JH (2012) Cortical changes after mental imagery training combined with electromyography-triggered electrical stimulation in patients with chronic stroke. Stroke 43:2506–2509CrossRefPubMedGoogle Scholar
  20. Imazu S, Sugio T, Tanaka S, Inui T (2007) Differences between actual and imagined usage of chopsticks: an fMRI study. Cortex 43:301–307CrossRefPubMedGoogle Scholar
  21. Jeannerod M (1995) Mental imagery in the motor context. Neuropsychologia 33:1419–1432CrossRefPubMedGoogle Scholar
  22. Kaneko F, Hayami T, Aoyama T, Kizuka T (2014) Motor imagery and electrical stimulation reproduce corticospinal excitabilities at levels similar to voluntary muscle contraction. J Neuroeng Rehabil 11:94CrossRefPubMedPubMedCentralGoogle Scholar
  23. Kaneko F, Shibata E, Hayami T, Nagahata K, Aoyama T (2016) The association of motor imagery and kinesthetic illusion prolongs the effect of transcranial direct current stimulation on corticospinal tract excitability. J Neuroeng Rehabil 13:36CrossRefPubMedPubMedCentralGoogle Scholar
  24. Kawakami M, Fujiwara T, Ushiba J, Nishimoto A, Abe K, Honaga K, Nishimura A, Mizuno K, Kodama M, Masakado Y, Liu M (2016) A new therapeutic application of brain-machine interface (BMI) training followed by hybrid assistive neuromuscular dynamic stimulation (HANDS) therapy for patients with severe hemiparetic stroke: a proof of concept study. Restor Neurol Neurosci 34:789–797PubMedGoogle Scholar
  25. Keysers C, Gazzola V (2010) Social neuroscience: mirror neurons recorded in humans. Curr Biol 20:R353–R354CrossRefPubMedGoogle Scholar
  26. Khaslavskaia S, Sinkjaer T (2005) Motor cortex excitability following repetitive electrical stimulation of the common peroneal nerve depends on the voluntary drive. Exp Brain Res 162:497–502CrossRefPubMedGoogle Scholar
  27. Lacourse MG, Orr EL, Cremer SC, Cohen MJ (2005) Brain activation during execution and motor imagery of novel and skilled sequential hand movements. Neuroimage 27:505–519CrossRefPubMedGoogle Scholar
  28. Lafleur MF, Jackson PL, Malouin F, Richards CL, Evans AC, Doyon J (2002) Motor learning produces parallel dynamic functional changes during the execution and imagination of sequential foot movements. Neuroimage 16:142–157CrossRefPubMedGoogle Scholar
  29. Lotze M, Halsband U (2007) Motor imagery. J Physiol Paris 99:386–395CrossRefGoogle Scholar
  30. Meng HJ, Pi YL, Liu K, Cao N, Wang YQ, Wu Y, Zhang J (2018) Differences between motor execution and motor imagery of grasping movements in the motor cortical excitatory circuit. PeerJ 6:e5588CrossRefPubMedPubMedCentralGoogle Scholar
  31. Mizuguchi N, Sakamoto M, Muraoka T, Moriyama N, Nakagawa K, Nakata H, Kanosue K (2012) Influence of somatosensory input on corticospinal excitability during motor imagery. Neurosci Lett 514:127–130CrossRefPubMedGoogle Scholar
  32. Mouthon A, Ruffieux J, Wälchli M, Keller M, Taube W (2015) Task-dependent changes of corticospinal excitability during observation and motor imagery of balance tasks. Neuroscience 303:535–543CrossRefPubMedGoogle Scholar
  33. Nedelko V, Hassa T, Hamzei F, Schoenfeld MA, Dettmers C (2012) Action imagery combined with action observation activates more corticomotor regions than action observation alone. J Neurol Phys Ther 36:182–188CrossRefPubMedGoogle Scholar
  34. Okuyama K, Ogura M, Kawakami M, Tsujimoto K, Okada K, Miwa K, Takahashi Y, Abe K, Tanabe S, Yamaguchi T, Liu M (2018) Effect of the combination of motor imagery and electrical stimulation on upper extremity motor function in patients with chronic stroke: preliminary results. Ther Adv Neurol Disord 11:1756286418804785CrossRefPubMedPubMedCentralGoogle Scholar
  35. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113CrossRefPubMedGoogle Scholar
  36. Ridding MC, Brouwer B, Miles TS, Pitcher JB, Thompson PD (2000) Changes in muscle responses to stimulation of the motor cortex induced by peripheral nerve stimulation in human subjects. Exp Brain Res 131:135–143CrossRefPubMedGoogle Scholar
  37. Roberts R, Callow N, Hardy L, Markland D, Bringer J (2008) Movement imagery ability: development and assessment of a revised version of the vividness of movement imagery questionnaire. J Sport Exerc Psychol 30:200–221CrossRefPubMedGoogle Scholar
  38. Saito K, Yamaguchi T, Yoshida N, Tanabe S, Kondo K, Sugawara K (2013) Combined effect of motor imagery and peripheral nerve electrical stimulation on the motor cortex. Exp Brain Res 227:333–342CrossRefGoogle Scholar
  39. Stefan K, Kunesch E, Cohen LG, Benecke R, Classen J (2000) Induction of plasticity in the human motor cortex by paired associative stimulation. Brain 123:572–584CrossRefPubMedPubMedCentralGoogle Scholar
  40. Stinear CM, Byblow WD, Steyvers M, Levin O, Swinnen SP (2006) Kinesthetic, but not visual, motor imagery modulates corticomotor excitability. Exp Brain Res 168:157–164CrossRefPubMedGoogle Scholar
  41. Sugawara K, Yamaguchi T, Tanabe S, Suzuki T, Saito K, Higashi T (2014) Time-dependent changes in motor cortical excitability by electrical stimulation combined with voluntary drive. Neuroreport 25:404–409CrossRefPubMedGoogle Scholar
  42. Takahashi Y, Fujiwara T, Yamaguchi T, Kawakami M, Mizuno K, Liu M (2017) The effects of patterned electrical stimulation combined with voluntary contraction on spinal reciprocal inhibition in healthy individuals. Neuroreport 28:434–438CrossRefPubMedGoogle Scholar
  43. Takahashi Y, Fujiwara T, Yamaguchi T, Matsunaga H, Kawakami M, Honaga K, Mizuno K, Liu M (2018) Voluntary contraction enhances spinal reciprocal inhibition induced by patterned electrical stimulation in patients with stroke. Restor Neurol Neurosci 36:99–105PubMedGoogle Scholar
  44. Villiger M, Estevez N, Hepp-Reymond MC, Kiper D, Kollias SS, Eng K, Hotz-Boendermaker S (2013) Enhanced activation of motor execution networks using action observation combined with imagination of lower limb movements. PLoS One 8:e72403CrossRefPubMedPubMedCentralGoogle Scholar
  45. Vogt S, Rienzo FD, Collet C, Collins A, Guillot A (2013) Multiple roles of motor imagery during action observation. Front Hum Neurosci 7:807CrossRefPubMedPubMedCentralGoogle Scholar
  46. Ward NS, Cohen LG (2004) Mechanisms underlying recovery of motor function after stroke. Arch Neurol 61:1844–1848CrossRefPubMedPubMedCentralGoogle Scholar
  47. Williams J, Pearce AJ, Loporto M, Morris T, Holmes PS (2012) The relationship between corticospinal excitability during motor imagery and motor imagery ability. Behav Brain Res 226:369–375CrossRefPubMedGoogle Scholar
  48. Wolters A, Sandbrink F, Schlottmann A, Kunesch E, Stefan K, Cohen LG, Benecke R, Classen J (2003) A temporally asymmetric Hebbian rule governing plasticity in the human motor cortex. J Neurophysiol 89:2339–2345CrossRefPubMedGoogle Scholar
  49. Wright DJ, Williams J, Holmes PS (2014) Combined action observation and imagery facilitates corticospinal excitability. Front Hum Neurosci 8:951PubMedPubMedCentralGoogle Scholar
  50. Yahagi S, Shimura K, Kasai T (1996) An increase in cortical excitability with no change in spinal excitability during motor imagery. Percept Mot Skills 83:288–290CrossRefPubMedGoogle Scholar
  51. Yamaguchi T, Sugawara K, Tanaka S, Yoshida N, Saito K, Tanabe S, Muraoka Y, Liu M (2012) Real-time changes in corticospinal excitability during voluntary contraction with concurrent electrical stimulation. PLoS One 7:e46122CrossRefPubMedPubMedCentralGoogle Scholar
  52. Yamaguchi T, Fujiwara T, Tsai YA, Tang SC, Kawakami M, Mizuno K, Kodama M, Masakado Y, Liu M (2016) The effects of anodal transcranial direct current stimulation and patterned electrical stimulation on spinal inhibitory interneurons and motor function in patients with spinal cord injury. Exp Brain Res 234:1469–1478CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Takahito Yasui
    • 1
  • Tomofumi Yamaguchi
    • 2
    • 3
    • 4
    • 5
  • Shigeo Tanabe
    • 6
  • Tsuyoshi Tatemoto
    • 6
  • Yoko Takahashi
    • 1
    • 5
  • Kunitsugu Kondo
    • 1
  • Michiyuki Kawakami
    • 1
    • 5
  1. 1.Tokyo Bay Rehabilitation HospitalNarashino-shiJapan
  2. 2.Department of Physical TherapyYamagata Prefectural University of Health SciencesYamagata-shiJapan
  3. 3.JSPS Postdoctoral Fellow for Research AbroadTokyoJapan
  4. 4.Department of NeuroscienceUniversity of CopenhagenCopenhagen NDenmark
  5. 5.Department of Rehabilitation MedicineKeio University School of MedicineTokyoJapan
  6. 6.Faculty of Rehabilitation, School of Health SciencesFujita Health UniversityToyoake-shiJapan

Personalised recommendations