Experimental Brain Research

, Volume 233, Issue 6, pp 1921–1929 | Cite as

Altered visual feedback modulates cortical excitability in a mirror-box-like paradigm

  • Irene Senna
  • Cristina Russo
  • Cesare Valerio Parise
  • Irene Ferrario
  • Nadia Bolognini
Research Article


Watching self-generated unilateral hand movements reflected in a mirror–oriented along the midsagittal plane–enhances the excitability of the primary motor cortex (M1) ipsilateral to the moving hand of the observer. Mechanisms detecting sensory–motor conflicts generated by the mirror reflection of such movements might mediate this effect; if so, cortical excitability should be modulated by the magnitude of sensory–motor conflict. To this end, we explored the modulatory effects of an altered visual feedback on M1 excitability in a mirror-box-like paradigm, by increasing or decreasing the speed of the observed movement. Healthy subjects performed movements with their left index finger while watching a video of a hand superimposed to their right static hand, which was hidden from view. The hand observed in the video executed the same movement as the observer’s left hand, but at slower, same, or faster paces. Motor evoked potentials (MEPs) induced by transcranial magnetic stimulation were measured from the first dorsal interosseous and the abductor digiti minimi of the participant’s hidden resting hand. The excitability of the M1 ipsilateral to the moving hand was systematically modulated by the speed of the observed hand movement: the slower the observed movement, the greater the MEP amplitude from both muscles. This evidence shows that the magnitude of the visual–motor conflicts can be used to adjust the activity of the observer’s motor system. Hence, an appropriate alteration of the visual feedback, here the reduction in the movement speed, may be useful to increase its modulatory effect on motor cortical excitability.


Mirror box Visual feedback Transcranial magnetic stimulation Motor evoked potentials Visual–motor mismatch 



The authors would like to thank Carlo Toneatto for technical assistance and Alessandro Moscatelli for helpful suggestions.

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Altschuler EL (2005) Interaction of vision and movement via a mirror. Perception 34:1153–1155CrossRefPubMedGoogle Scholar
  2. Altschuler EL, Wisdom SB, Stone L, Foster C, Galasko D, Llewellyn DME, Ramachandran VS (1999) Rehabilitation of hemiparesis after stroke with a mirror. Lancet 353:2035–2036CrossRefPubMedGoogle Scholar
  3. Avenanti A, Bolognini N, Maravita A, Aglioti SM (2007) Somatic and motor components of action simulation. Curr Biol 17:2129–2135CrossRefPubMedGoogle Scholar
  4. Bakola S, Gamberini M, Passarelli L, Fattori P, Galletti C (2010) Cortical connections of parietal field PEc in the macaque: linking vision and somatic sensation for the control of limb action. Cereb Cortex 20:2592–2604CrossRefPubMedGoogle Scholar
  5. Botvinick M, Cohen J (1998) Rubber hands ‘feel’ touch that eyes see. Nature 391:756CrossRefPubMedGoogle Scholar
  6. Brown H, Prescott R (2006) Applied mixed models in medicine. In: Barnett V (ed) Repeated measures data, 1st edn. Wiley, Chichester, pp 199–259Google Scholar
  7. Cauraugh JH, Summers JJ (2005) Neural plasticity and bilateral movements: a rehabilitation approach for chronic stroke. Prog Neurobiol 75:309–320CrossRefPubMedGoogle Scholar
  8. Cavanna AE, Trimble MR (2006) The precuneus: a review of its functional anatomy and behavioural correlates. Brain 129(3):564–583CrossRefPubMedGoogle Scholar
  9. Chan BL, Witt R, Charrow AP, Magee A, Howard R, Pasquina PF, Heilman KM, Tsao JW (2007) Mirror therapy for phantom limb pain. N Engl J Med 357:2206–2207CrossRefPubMedGoogle Scholar
  10. Dohle C, Pullen J, Nakaten A, Kust J, Rietz C, Karbe H (2009) Mirror therapy promotes recovery from severe hemiparesis: a randomized controlled trial. Neurorehabil Neural Repair 23:209–217CrossRefPubMedGoogle Scholar
  11. Ehrsson HH, Rosén B, Stockselius A, Ragnö C, Köhler P, Lundborg G (2008) Upper limb amputees can be induced to experience a rubber hand as their own. Brain 131:3443–3452CrossRefPubMedCentralPubMedGoogle Scholar
  12. Fadiga L, Fogassi L, Pavesi G, Rizzolatti G (1995) Motor facilitation during action observation: a magnetic stimulation study. J Neurophysiol 73:2608–2611PubMedGoogle Scholar
  13. Fadiga L, Craighero L, Olivier E (2005) Human motor cortex excitability during the perception of others’ action. Curr Opin Neurobiol 15(2):213–218CrossRefPubMedGoogle Scholar
  14. Fink GA, Marshall JC, Halligan PW, Frith CD, Driver J, Frackowiak RSJ, Dolan RJ (1999) The neural consequences of conflict between intention and the senses. Brain 122:497–512CrossRefPubMedGoogle Scholar
  15. Franz EA, Packman T (2004) Fooling the brain into thinking it sees both hands moving enhances bimanual spatial coupling. Exp Brain Res 157:174–180CrossRefPubMedGoogle Scholar
  16. Frith CD, Blakemore S-J, Wolpert DM (2000) Abnormalities in the awareness and control of action. Philos Trans R Soc Lond 355:1771–1788CrossRefGoogle Scholar
  17. Fukumura K, Sugawara K, Tanabe S, Ushiba J, Tomita Y (2007) Influence of mirror therapy on human motor cortex. Int J Neurosci 117:1039–1048CrossRefPubMedGoogle Scholar
  18. Funase K, Tabira T, Higashi T, Liang N, Kasai T (2007) Increased corticospinal excitability during direct observation of self-movement and indirect observation with a mirror box. Neurosci Lett 419(2):108–112CrossRefPubMedGoogle Scholar
  19. Garry MI, Loftus A, Summers JJ (2005) Mirror, mirror on the wall: viewing a mirror reflection of unilateral hand movements facilitates ipsilateral M1 excitability. Exp Brain Res 163(1):118–122CrossRefPubMedGoogle Scholar
  20. Guerraz M, Provost S, Narison R, Brugnon A, Virolle S, Bresciani JP (2012) Integration of visual and proprioceptive afferents in kinesthesia. Neuroscience 223:258–268CrossRefPubMedGoogle Scholar
  21. Kang YJ, Park HK, Kim HJ, Lim T, Ku J, Cho S, Kim SI, Park ES (2012) Upper extremity rehabilitation of stroke: facilitation of corticospinal excitability using virtual mirror paradigm. J Neuroeng Rehabil 9:71CrossRefPubMedCentralPubMedGoogle Scholar
  22. Liepert J, Dettmers C, Terborg C, Weiller C (2001) Inhibition of ipsilateral motor cortex during phasic generation of low force. Clin Neurophysiol 112:114–121CrossRefPubMedGoogle Scholar
  23. Longo MR, Betti V, Aglioti SM, Haggard P (2009) Visually induced analgesia: seeing the body reduces pain. J Neurosci 29(39):12125–12130CrossRefPubMedGoogle Scholar
  24. MacLachlan M, McDonald D, Waloch J (2004) Mirror treatment of lower limb phantom pain: a case study. Disabil Rehabil 26:901–904CrossRefPubMedGoogle Scholar
  25. Matthys K, Smits M, Van der Geest JN, Van der Lugt A, Seurinck R, Stam HJ, Selles RW (2009) Mirror-induced visual illusion of hand movements: a functional magnetic resonance imaging study. Arch Phys Med Rehabil 90:675–681CrossRefPubMedGoogle Scholar
  26. McCabe CS, Blake DR (2007) Evidence for a mismatch between the brain’s movement control system and sensory system as an explanation for some pain-related disorders. Curr Pain Headache Rep 11(2):104–108CrossRefPubMedGoogle Scholar
  27. Metral M, Blettery B, Bresciani JP, Luyat M, Guerraz M (2013) Trying to move your unseen static arm modulates visually-evoked kinesthetic illusion. PLoS One 8(11):e80360CrossRefPubMedCentralPubMedGoogle Scholar
  28. Michielsen ME, Smits M, Ribbers GM, Stam HJ, van der Geest JN, Bussmann JB, Selles RW (2011) The neuronal correlates of mirror therapy: an fMRI study on mirror induced visual illusions in patients with stroke. J Neurol Neurosurg Psychiatry 82:393–398CrossRefPubMedGoogle Scholar
  29. Mills KR, Boniface SJ, Schubert M (1992) Magnetic brain stimulation with a double coil: the importance of coil orientation. Electroencephalogr Clin Neurophysiol 85:17–21CrossRefPubMedGoogle Scholar
  30. Muellbacher W, Facchini S, Boroojerdi B, Hallett M (2000) Changes in motor cortex excitability during ipsilateral hand muscle activation in humans. Clin Neurophysiol 111:344–349CrossRefPubMedGoogle Scholar
  31. Nojima I, Mima T, Koganemaru S, Thabit MN, Fukuyama H, Kawamata T (2012) Human motor plasticity induced by mirror visual feedback. J Neurosci 32(4):1293–1300CrossRefPubMedGoogle Scholar
  32. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113CrossRefPubMedGoogle Scholar
  33. Pinheiro JC, Bates DM (2000) Mixed effects models in S and S-plus. Springer, New YorkCrossRefGoogle Scholar
  34. Ramachandran VS, Altschuler EL (2009) The use of visual feedback, in particular mirror visual feedback, in restoring brain function. Brain 132:1693–1710CrossRefPubMedGoogle Scholar
  35. Ramachandran VS, Rogers-Ramachandran D (1996) Synaesthesia in phantom limbs induced with mirrors. Proc R Soc Lond B Biol Sci 263:377–386CrossRefGoogle Scholar
  36. Ramachandran VS, Rogers-Ramachandran D, Cobb S (1995) Touching the phantom limb. Nature 377:489–490CrossRefPubMedGoogle Scholar
  37. Romano D, Bottini G, Maravita A (2013) Perceptual effects of the mirror box training in normal subjects. Restor Neurol Neurosci 31(4):373–386PubMedGoogle Scholar
  38. Rossi S, Hallett M, Rossini PM, Pascual-Leone A, The Safety of TMS Consensus Group (2009) Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol 120:2008–2039CrossRefPubMedCentralPubMedGoogle Scholar
  39. Rossini PM, Barker AT, Berardelli A, Caramia MD, Caruso G, Cracco RQ, Dimitrijević MR, Hallett M, Katayama Y, Lücking CH, Maertens de Noordhout AL, Marsden CD, Murray NMF, Rothwell JC, Swash M, Tomberg C (1994) Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. Electroencephalogr Clin Neurophysiol 91:79–92CrossRefPubMedGoogle Scholar
  40. Sadibolova R, Longo MR (2014) Seeing the body produces limb-specific modulation of skin temperature. Biol Lett 10(4):20140157CrossRefPubMedCentralPubMedGoogle Scholar
  41. Saleh S, Adamovich SV, Tunik E (2014) Mirrored feedback in chronic stroke: recruitment and effective connectivity of ipsilesional sensorimotor networks. Neurorehabil Neural Repair 28(4):344–354CrossRefPubMedCentralPubMedGoogle Scholar
  42. Sathian K, Greenspan AI, Wolf SL (2000) Doing it with mirrors: a case study of a novel approach to neurorehabilitation. Neurorehabil Neural Repair 14(1):73–76CrossRefPubMedGoogle Scholar
  43. Scully DM (1988) Visual perception of human movement: The use of demonstrations in teaching motor skills. Br J Phys Educ Res 4(suppl.):12–14Google Scholar
  44. Senna I, Bolognini N, Maravita A (2014a) Grasping with the foot: goal and motor expertise in action observation. Hum Brain Mapp 35(4):1750–1760CrossRefPubMedGoogle Scholar
  45. Senna I, Maravita A, Bolognini N, Parise CV (2014b) The marble hand illusion. PLoS One 9(3):e91688CrossRefPubMedCentralPubMedGoogle Scholar
  46. Snijders HJ, Holmes NP, Spence C (2007) Direction-dependent integration of vision and proprioception in reaching under the influence of the mirror illusion. Neuropsychologia 45(3):496–505CrossRefPubMedCentralPubMedGoogle Scholar
  47. Stinear JW, Byblow WD (2004) Rhythmic bilateral movement training modulates corticomotor excitability and enhances upper limb motoricity poststroke: a pilot study. J Clin Neurophys 21:124–131CrossRefGoogle Scholar
  48. Strafella AP, Paus T (2000) Modulation of cortical excitability during action observation: a transcranial magnetic stimulation study. NeuroReport 11:2289–2292CrossRefPubMedGoogle Scholar
  49. Sumitani M, Miyauchi S, McCabe CS, Shibata M, Maeda L, Saitoh Y, Tashiro T, Mashimo T (2008) Mirror visual feedback alleviates deafferentation pain, depending on qualitative aspects of the pain: a preliminary report. Rheumatology (Oxford) 47:1038–1043CrossRefGoogle Scholar
  50. Sütbeyaz S, Yavuzer G, Sezer N, Koseoglu BF (2007) Mirror therapy enhances lower-extremity motor recovery and motor functioning after stroke: a randomized controlled trial. Arch Phys Med Rehabil 88(5):555–559CrossRefPubMedGoogle Scholar
  51. Swinnen SP (2002) Intermanual coordination: from behavioural principles to neural-network interactions. Nat Rev Neurosci 3(5):348–359CrossRefPubMedGoogle Scholar
  52. Tominaga W, Matsubayashi J, Deguchi Y, Minami C, Kinai T, Nakamura M, Nagamine T, Matsuhashi M, Mima T, Fukuyama H, Mitani A (2009) A mirror reflection of a hand modulates stimulus-induced 20-Hz activity. Neuroimage 46:500–504CrossRefPubMedGoogle Scholar
  53. Touzalin-Chretien P, Dufour A (2008) Motor cortex activation induced by a mirror: evidence from lateralized readiness potentials. J Neurophysiol 100(1):19–23CrossRefPubMedGoogle Scholar
  54. Tunik E, Saleh S, Bagce H, Merians A, Adamovich SV (2011) Mirror feedback in virtual reality elicits ipsilesional motor cortex activation in chronic stroke patients. In: International Conference on Virtual Rehabilitation, Zurich, Switzerland. IEEE, Washington, DCGoogle Scholar
  55. Woodworth RS (1899) The accuracy of voluntary movement. Psychol Rev Monogr Suppl 3:1–119Google Scholar
  56. Yavuzer G, Selles R, Sezer N, Sütbeyaz S, Bussmann JB, Köseoglu F, Atay MB, Stam HJ (2008) Mirror therapy improves hand function in subacute stroke: a randomized controlled trial. Arch Phys Med Rehabil 89:393–398CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Irene Senna
    • 1
    • 2
  • Cristina Russo
    • 1
  • Cesare Valerio Parise
    • 2
  • Irene Ferrario
    • 1
  • Nadia Bolognini
    • 1
    • 3
  1. 1.Department of PsychologyUniversity of Milano BicoccaMilanItaly
  2. 2.Cognitive Neuroscience Department and Cognitive Interaction Technology-Center of ExcellenceBielefeld UniversityBielefeldGermany
  3. 3.Laboratory of NeuropsychologyIRCCS Istituto Auxologico ItalianoMilanItaly

Personalised recommendations