Advertisement

Effects of transcutaneous electrical nerve stimulation and visuotactile synchrony on the embodiment of an artificial hand

  • Akihiko Asao
  • Kenichi Shibuya
  • Kazuki Yamada
  • Yuina Kazama
Research Article
  • 6 Downloads

Abstract

The rubber hand illusion (RHI) is an experimental paradigm known to produce a bodily illusion. Transcutaneous electrical nerve stimulation (TENS) combined with the RHI induces a stronger illusion than the RHI alone. Visuotactile stimulus synchrony is an important aspect of the RHI. However, the effect of TENS and visuotactile stimulus synchrony in TENS combined with the RHI remains unknown. The purpose of this study was to investigate the effects of TENS and visuotactile stimulus synchrony on the embodiment of an artificial hand when using TENS combined with the RHI. The participants underwent four experimental conditions in random order: TENS/noTENS × Synchronous/Asynchronous. TENS was set at an intensity such that it generated a feeling of electrical paresthesia in the radial nerve area of the hand but did not cause pain, i.e., 100-Hz pulse frequency, 80-µs pulse duration, and a constant pulse pattern. A visuotactile stimulus, either temporally synchronous or asynchronous, was generated using paintbrush strokes. To evaluate the outcome measures, the participants completed a questionnaire report and proprioceptive drift assessments (motor response and perceptual response). There were significant main effects of TENS and visuotactile synchrony, but no interaction between these factors, on the results of the questionnaire and the perceptual response. In contrast, there was no significant effect on the result of the motor response. These findings indicate that TENS and visuotactile synchrony might affect differently the embodiment of an artificial hand when using TENS combined with the RHI.

Keywords

Rubber hand illusion Transcutaneous electrical nerve stimulation Visuotactile synchrony Sense of body ownership Proprioceptive drift 

Notes

Acknowledgements

This work was supported by a Grant-in-Aid for Exploratory Research from Niigata University of Health and Welfare, 2017. The authors would like to thank Editage for editorial assistance with the manuscript.

Author contributions

AA and KS conceived of the study and designed the experimental paradigm. AA, KY, and YK performed the experiment and analyzed the data. AA wrote the manuscript. KS provided feedback and edited the manuscript. All authors read and approved the final manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

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.

References

  1. Arzy S, Thut G, Mohr C, Michel CM, Blanke O (2006) Neural basis of embodiment: distinct contributions of temporopariet al. junction and extrastriate body area. J Neurosci 26:8074–80781.  https://doi.org/10.1523/JNEUROSCI.0745-06.2006 CrossRefPubMedGoogle Scholar
  2. Botvinick M, Cohen J (1998) Rubber hands feel touch that eyes see. Nature 391:756.  https://doi.org/10.1038/35784 CrossRefPubMedGoogle Scholar
  3. Christ O, Reiner M (2014) Perspectives and possible applications of the rubber hand and virtual hand illusion in non-invasive rehabilitation: technological improvements and their consequences. Neurosci Biobehav Rev 44:33–44.  https://doi.org/10.1016/j.neubiorev.2014.02.013 CrossRefPubMedGoogle Scholar
  4. Costantini M, Robinson J, Migliorati D, Donno B, Ferri F, Northoff G (2016) Temporal limits on rubber hand illusion reflect individuals’ temporal resolution in multisensory perception. Cognition 157:39–48.  https://doi.org/10.1016/j.cognition.2016.08.010 CrossRefPubMedGoogle Scholar
  5. Ehrsson HH, Spence C, Passingham RE (2004) That’s my hand! activity in premotor cortex reflects feeling of ownership of a limb. Science 305:875–877CrossRefGoogle Scholar
  6. Ehrsson HH, Holmes NP, Passingham RE (2005) Touching a rubber hand: feeling of body ownership is associated with activity in multisensory brain areas. J Neurosci 25:10564–10573.  https://doi.org/10.1523/JNEUROSCI.0800-05.2005 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Fuchs X, Riemer M, Diers M, Flor H, Trojan J (2016) Perceptual drifts of real and artificial limbs in the rubber hand illusion. Sci Rep 22(6):24362.  https://doi.org/10.1038/srep24362 CrossRefGoogle Scholar
  8. Funk M, Shiffrar M, Brugger P (2005) Hand movement observation by individuals born without hands: phantom limb experience constrains visual limb perception. Exp Brain Res 164:341–346.  https://doi.org/10.1007/s00221-005-2255-4 CrossRefPubMedGoogle Scholar
  9. Gallagher S (2000) Philosophical conceptions of the self: implications for cognitive science. Trends Cogn Sci 4:14–21CrossRefGoogle Scholar
  10. Gallagher S (2005) How the body shapes the mind. Oxford University, New YorkCrossRefGoogle Scholar
  11. Gallagher S (2011) The oxford handbook of the self. Oxford University, New YorkCrossRefGoogle Scholar
  12. Gallese V, Sinigaglia C (2010) The bodily self as power for action. Neuropsychologia Rev 48:746–755.  https://doi.org/10.1016/j.neuropsychologia.2009.09.038 CrossRefGoogle Scholar
  13. Gandevia SC, Phegan CM (1999) Perceptual distortions of the human body image produced by local anaesthesia, pain and cutaneous stimulation. J Physiol 514.2:609–616.  https://doi.org/10.1111/j.1469-7793.1999.609ae.x CrossRefGoogle Scholar
  14. Giummarra MJ, Gibson SJ, Georgiou-Karistianis N, Bradshaw JL (2008) Mechanisms underlying embodiment, disembodiment and loss of embodiment. Neurosci Biobehav Rev 32:143–160.  https://doi.org/10.1016/j.neubiorev.2007.07.001 CrossRefPubMedGoogle Scholar
  15. Head H, Holms G (1911) Sensory disturbances from cerebral lesions. Brain 34:102–254CrossRefGoogle Scholar
  16. Inui N, Walsh LD, Taylor JL, Gandevia SC (2011) Dynamic changes in the perceived posture of the hand during ischaemic anaesthesia of the arm. J Physiol 589:5775–5784.  https://doi.org/10.1113/jphysiol.2011.219949 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Johnson MI, Bjordal JM (2011) Transcutaneous electrical nerve stimulation for the management of painful conditions: focus on neuropathic pain. Expert Rev Neurother 11:735–753.  https://doi.org/10.1586/ern.11.48 CrossRefPubMedGoogle Scholar
  18. Kalckert A, Ehrsson HH (2012) Moving a rubber hand that feels like your own: a dissociation of ownership and agency. Front Hum Neurosci 14:40.  https://doi.org/10.3389/fnhum.2012.00040 CrossRefGoogle Scholar
  19. Kammers MP, de Vignemont F, Verhagen L, Dijkerman HC (2009a) The rubber hand illusion in action. Neuropsychologia 47:204–211.  https://doi.org/10.1016/j.neuropsychologia.2008.07.028 CrossRefPubMedGoogle Scholar
  20. Kammers MP, Longo MR, Tsakiris M, Dijkerman HC, Haggard P (2009b) Specificity and coherence of body representations. Perception 38:1804–1820.  https://doi.org/10.1068/p6389 CrossRefPubMedGoogle Scholar
  21. Lin S, Sun Q, Wang H, Xie G (2017) Influence of transcutaneous electrical nerve stimulation on spasticity, balance, and walking speed in stroke patients: a systematic review and meta-analysis. J Rehabil Med 50:3–7.  https://doi.org/10.2340/16501977-2266 CrossRefGoogle Scholar
  22. Lloyd DM, Gillis V, Lewis E, Farrell MJ, Morrison I (2013) Pleasant touch moderates the subjective but not objective aspects of body perception. Front Behav Neurosci 23:7:207.  https://doi.org/10.3389/fnbeh.2013.00207 CrossRefGoogle Scholar
  23. Longo MR, Schüür F, Kammers MP, Tsakiris M, Haggard P (2008) What is embodiment? A psychometric approach. Cognition 107:978–998.  https://doi.org/10.1016/j.cognition.2007.12.004 CrossRefPubMedGoogle Scholar
  24. Makin TR, Holmes NP, Ehrsson HH (2008) On the other hand: dummy hands and peripersonal space. Behav Brain Res Rev 5(191):1–10.  https://doi.org/10.1016/j.bbr.2008.02.041 CrossRefGoogle Scholar
  25. Melzack R, Wall PD (1965) Pain mechanisms: a new theory. Science 150:971–979CrossRefGoogle Scholar
  26. Milne S, Welch V, Brosseau L, Saginur M, Shea B, Tugwell P, Wells G (2001) Transcutaneous electrical nerve stimulation (TENS) for chronic low-back pain. Cochrane Database Syst Rev 2:CD003008.  https://doi.org/10.1002/14651858.CD003008/full CrossRefGoogle Scholar
  27. Mulvey MR, Fawkner HJ, Radford HE, Johnson MI (2012) Perceptual embodiment of prosthetic limbs by transcutaneous electrical nerve stimulation. Neuromodulation 15:42–47.  https://doi.org/10.1111/j.1525-1403.2011.00408.x CrossRefPubMedGoogle Scholar
  28. Mulvey MR, Fawkner HJ, Johnson MI (2015) An investigation of the effects of different pulse patterns of transcutaneous electrical nerve stimulation (TENS) on perceptual embodiment of a rubber hand in healthy human participants with intact limbs. Neuromodulation 18:744–750.  https://doi.org/10.1111/ner.12329 CrossRefPubMedGoogle Scholar
  29. Nnoaham KE, Kumbang J (2008) Transcutaneous electrical nerve stimulation (TENS) for chronic pain. Cochrane Database Syst Rev 3:CD003222.  https://doi.org/10.1002/14651858.CD003222.pub2 CrossRefGoogle Scholar
  30. Ocklenburg S, Peterburs J, Rüther N, Güntürkün O (2012) The rubber hand illusion modulates pseudoneglect. Neurosci Lett 523:158–161.  https://doi.org/10.1016/j.neulet.2012.06.068 CrossRefPubMedGoogle Scholar
  31. Olausson H, Wessberg J, Morrison I, McGlone F, Vallbo A (2010) The neurophysiology of unmyelinated tactile afferents. Neurosci Biobehav Rev 34:185–191.  https://doi.org/10.1016/j.neubiorev.2008.09.011 CrossRefPubMedGoogle Scholar
  32. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113CrossRefGoogle Scholar
  33. Paqueron X, Leguen M, Rosenthal D, Coriat P, Willer JC, Danziger N (2003) The phenomenology of body image distortions induced by regional anaesthesia. Brain 126.3:702–712CrossRefGoogle Scholar
  34. Proske U, Gandevia SC (2012) The proprioceptive senses: their roles in signaling body shape, body position and movement, and muscle force. Physiol Rev 92:1651–1697.  https://doi.org/10.1152/physrev.00048.2011 CrossRefPubMedGoogle Scholar
  35. Riemer M, Kleinböhl D, Hölzl R, Trojan J (2013) Action and perception in the rubber hand illusion. Exp Brain Res 229:383–393.  https://doi.org/10.1007/s00221-012-3374-3373 CrossRefPubMedGoogle Scholar
  36. Rohde M, Di Luca M, Ernst MO (2011) The rubber hand illusion: feeling of ownership and proprioceptive drift do not go hand in hand. PLoS One 6:e21659.  https://doi.org/10.1371/journal.pone.0021659 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Shimada S, Fukuda K, Hiraki K (2009) Rubber hand illusion under delayed visual feedback. PLoS One 4:e6185.  https://doi.org/10.1371/journal.pone.0006185 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Sluka KA, Walsh D (2003) Transcutaneous electrical nerve stimulation: basic science mechanisms and clinical effectiveness. J Pain 4:109–121.  https://doi.org/10.1054/jpai.2003.434 CrossRefPubMedGoogle Scholar
  39. Tsakiris M (2010) My body in the brain: a neurocognitive model of body-ownership. Neuropsychologia 48:703–712.  https://doi.org/10.1016/j.neuropsychologia.2009.09.034 CrossRefPubMedGoogle Scholar
  40. Tsakiris M, Haggard P (2005) Experimenting with the acting self. Cogn Neuropsychol 22:387–407.  https://doi.org/10.1080/02643290442000158 CrossRefPubMedGoogle Scholar
  41. Tsakiris M, Prabhu G, Haggard P (2006) Having a body versus moving your body: how agency structures body-ownership. Conscious Cogn 15:423–432.  https://doi.org/10.1016/j.concog.2005.09.004 CrossRefPubMedGoogle Scholar
  42. Tsakiris M, Hesse MD, Boy C, Haggard P, Fink GR (2007) Neural signatures of body ownership: a sensory network for bodily self-consciousness. Cereb Cortex 17:2235–2244.  https://doi.org/10.1093/cercor/bhl131 CrossRefPubMedGoogle Scholar
  43. van Stralen HE, van Zandvoort MJ, Hoppenbrouwers SS, Vissers LM, Kappelle LJ, Dijkerman HC (2014) Affective touch modulates the rubber hand illusion. Cognition 131:147–158.  https://doi.org/10.1016/j.cognition.2013.11.020 CrossRefPubMedGoogle Scholar
  44. Walsh LD, Hoad D, Rothwell JC, Gandevia SC, Haggard P (2015) Anaesthesia changes perceived finger width but not finger length. Exp Brain Res 233:1761–1771.  https://doi.org/10.1007/s00221-015-4249-1 CrossRefPubMedGoogle Scholar
  45. Zeller D, Hullin M (2018) Spatial attention and the malleability of bodily self in the elderly. Conscious Cogn 59:32–39.  https://doi.org/10.1016/j.concog.2018.01.006 CrossRefPubMedGoogle Scholar
  46. Zhu Y, Feng Y, Peng L (2017) Effect of transcutaneous electrical nerve stimulation for pain control after total knee arthroplasty: a systematic review and meta-analysis. J Rehabil Med 49:700–704.  https://doi.org/10.2340/16501977-2273 CrossRefPubMedGoogle Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Department of Occupational Therapy, Faculty of RehabilitationNiigata University of Health and WelfareNiigataJapan
  2. 2.Department of Health and Nutrition, Faculty of Health SciencesNiigata University of Health and WelfareNiigataJapan

Personalised recommendations