Upper limb amputees can be induced to experience a rubber hand as their own

H Henrik Ehrsson, Birgitta Rosén, Anita Stockselius, Christina Ragnö, Peter Köhler, Göran Lundborg, H Henrik Ehrsson, Birgitta Rosén, Anita Stockselius, Christina Ragnö, Peter Köhler, Göran Lundborg

Abstract

We describe how upper limb amputees can be made to experience a rubber hand as part of their own body. This was accomplished by applying synchronous touches to the stump, which was out of view, and to the index finger of a rubber hand, placed in full view (26 cm medial to the stump). This elicited an illusion of sensing touch on the artificial hand, rather than on the stump and a feeling of ownership of the rubber hand developed. This effect was supported by quantitative subjective reports in the form of questionnaires, behavioural data in the form of misreaching in a pointing task when asked to localize the position of the touch, and physiological evidence obtained by skin conductance responses when threatening the hand prosthesis. Our findings outline a simple method for transferring tactile sensations from the stump to a prosthetic limb by tricking the brain, thereby making an important contribution to the field of neuroprosthetics where a major goal is to develop artificial limbs that feel like a real parts of the body.

Figures

Fig. 1
Fig. 1
The experimental set-up. The stump was hidden under a table and synchronous brushstrokes were applied to the stump and the index finger of a rubber hand placed in full view in front of the participant (A). After experiencing the illusion, the participant was asked to demonstrate where he or she had felt the touches by making a horizontal pointing movement along a ruler with eyes closed (B). We also stabbed the rubber hand with a needle whilst simultaneously measuring the associated changes in the participant's skin conductance as an objective measure of any fear and anticipated pain. (See the Methods section for details.)
Fig. 2
Fig. 2
The results of the questionnaire. The responses to Questions 1–3 reflect the experiences of the illusion: Q1—‘I felt the touch of the brush on the prosthetic hand’; ‘Q2—It seemed as if the brush caused the sensation touch that I experienced’; Q3—It felt as if the prosthetic hand was my hand’. The responses to Questions 4–9 served as controls for suggestibility and task compliance (see Methods section). The scores for the illusion questions (Q1–Q3) were significantly greater (P < 0.01) than those for the control conditions after the period of synchronous stimulation on the stump and the prosthetic hand (blue). Further, on average, the scores on the three illusion-related questions were greater in the stump condition than in the control condition when contralateral intact arm was stimulated (P < 0.05). Finally, it can be noted that the illusion ratings when stroking the participants’ stumps were lower than when testing the classical rubber hand illusion by stroking their intact contralateral hand (yellow). For details, see the Results section.
Fig. 3
Fig. 3
Behavioural evidence that people perceived a change in the location of the sensation of touch from the stump (and phantom in the cases of referred sensations) towards the rubber hand. When asked to indicate where they had sensed the touches of the paintbrush, by pointing with the intact hand with their eyes closed, the participant indicated greater drift in the perceived location of the touch towards the rubber hand after the illusion condition with synchronous stimulation (Sync) than after the asynchronous control condition (Async; P < 0.05).
Fig. 4
Fig. 4
Objective physiological evidence that the participants experienced an increase in the ownership of the prosthetic hand when we brushed the stump and the prosthetic hand synchronously. Greater psychologically induced sweating, as measured with the skin conductance response (in micro Sievert), was observed when the prosthetic hand was stabbed with a needle in the illusion condition (sync-stump) than in the asynchronous control condition (async-stump; P < 0.05).
Fig. 5
Fig. 5
Significant relationship between the time since amputation and the strength of the illusion as indicated by the illusion-items in the questionnaire (Pearson's correlation = −0.474, N = 18, P = 0.047, two-tailed P < 0.05). See the Results section for details.

References

    1. Armel KC, Ramachandran VS. Projecting sensations to external objects: evidence from skin conductance response. Proc Biol Sci. 2003;270:1499–506.
    1. Botvinick M. Neuroscience. Probing the neural basis of body ownership. Science. 2004;305:782–83.
    1. Botvinick M, Cohen J. Rubber hands ‘feel’ touch that eyes see. Nature. 1998;391:756.
    1. Brock D, Chiu S. Environment perception of an articulated robot hand using contact sensors. Robot Manuf Automat. 1985;15:89–96.
    1. Brodie EE, Whyte A, Niven CA. Analgesia through the looking-glass? A randomized controlled trial investigating the effect of viewing a ‘virtual’ limb upon phantom limb pain, sensation and movement. Eur J Pain. 2007;11:428–36.
    1. Carpaneto J, Micera S, Zaccone F, Vecchi F, Dario PA. Sensorized thumb for force closed-loop control of hand neuroprostheses. IEEE Trans Neural Syst Rehabil Eng. 2003;11:346–53.
    1. Carrozza MC, Cappiello G, Micera S, Edin BB, Beccai L, Cipriani C. Design of a cybernetic hand for perception and action. Biol Cybern. 2006;95:629–44.
    1. Chan BL, Witt R, Charrow AP, Magee A, Howard R, Pasquina PF, et al. Mirror therapy for phantom limb pain. N Engl J Med. 2007;22:2206–7.
    1. Cohen LG, Bandinelli S, Findley TW, Hallett M. Motor reorganization after upper limb amputation in man. A study with focal magnetic stimulation. Brain. 1991;114:615–27.
    1. Costantini M, Haggard P. The rubber hand illusion: sensitivity and reference frame for body ownership. Conscious Cogn. 2007;16:229–40.
    1. Dario P, Buttazzo G. An anthropomorphic robot finger for investigating artificial tactile perception. Int J Robot Res. 1987;6:25–48.
    1. Dawson ME, Schell AM, Filion DL. The electrodermal system. In: Cacioppo JT, Tassinary LG, Berntson GG, editors. The handbook of psychophysiology. Cambridge, UK: Cambridge University Press; 2007. pp. 152–91.
    1. Edin BB, Ascari L, Beccai L, Roccella S, Cabibihan JJ, Carrozza MC. Bio-inspired sensorization of a biomechatronic robot hand for the grasp-and-lift task. Brain Res Bull. 2008;15:785–95.
    1. Ehrsson HH, Holmes NP, Passingham RE. Touching a rubber hand: feeling of body ownership is associated with activity in multisensory brain areas. J Neurosci. 2005;25:10564–73.
    1. Ehrsson HH, Spence C, Passingham RE. That's my hand! Activity in premotor cortex reflects feeling of ownership of a limb. Science. 2004;305:875–7.
    1. Ehrsson HH, Weich K, Weiskopf N, Dolan RJ, Passingham RE. Threatening a rubber hand that you feel is yours elicits a cortical anxiety response. Proc Natl Acad Sci USA. 2007;104:9828–33.
    1. Elbert T, Flor H, Birbaumer N, Knecht S, Hampson S, Larbig W, Taub E. Extensive reorganization of the somatosensory cortex in adult humans after nervous system injury. Neuroreport. 1994;20:2593–7.
    1. Flor H, Elbert T, Knecht S, Wienbruch C, Pantev C, Birbaumer N, et al. Phantom-limb pain as a perceptual correlate of cortical reorganization following arm amputation. Nature. 1995;375:482–4.
    1. Flor H, Nikolajsen L, Staehelin JT. Phantom limb pain: a case of maladaptive CNS plasticity? Nat Rev Neurosci. 2006;7:873–81.
    1. Florence SL, Kaas JH. Large-scale reorganization at multiple levels of the somatosensory pathway follows therapeutic amputation of the hand in monkeys. J Neurosci. 1995;15:8083–95.
    1. Giraux P, Sirigu A. Illusory movements of the paralyzed limb restore motor cortex activity. Neuroimage. 2003;20:S107–11.
    1. Grüsser SM, Winter C, Mühlnickel W, Denke C, Karl A, Villringer K, et al. The relationship of perceptual phenomena and cortical reorganization in upper extremity amputees. Neuroscience. 2001;102:263–72.
    1. Hochberg LR, Serruya MD, Friehs GM, Mukand JA, Saleh M, Caplan AH, et al. Neuronal ensemble control of prosthetic devices by a human with tetraplegia. Nature. 2006;442:164–71.
    1. Holmes NP, Snijders HJ, Spence C. Reaching with alien limbs: visual exposure to prosthetic hands in a mirror biases proprioception without accompanying illusions of ownership. Percept Psychophys. 2006;68:685–701.
    1. Hunter JP, Katz J, Davis KD. The effect of tactile and visual sensory inputs on phantom limb awareness. Brain. 2003;126:579–89.
    1. Johansson RS. Sensory control of dexterous manipulation. In: Wing AM, Haggard P, Flanagan JR, editors. Hand and brain: the neurophysiology and psychology of hand movements. San Diego: Academic; 1996. pp. 381–412.
    1. Kew JJ, Ridding MC, Rothwell JC, Passingham RE, Leigh PN, Sooriakumaran S, et al. Reorganization of cortical blood flow and transcranial magnetic stimulation maps in human subjects after upper limb amputation. J Neurophysiol. 1994;72:2517–24.
    1. Kew JJ, Halligan PW, Marshall JC, Passingham RE, Rothwell JC, Ridding MC, et al. Abnormal access of axial vibrotactile input to deafferented somatosensory cortex in human upper limb amputees. J Neurophysiol. 1997;77:2753–64.
    1. Kuiken TA, Miller LA, Lipschutz RD, Lock BA, Stubblefield K, Marasco PD, et al. Targeted reinnervation for enhanced prosthetic arm function in a woman with a proximal amputation: a case study. Lancet. 2007;369:371–80.
    1. Lebedev MA, Nicolelis MA. Brain-machine interfaces: past, present and future. Trends Neurosci. 2006;29:536–46.
    1. London BM, Jordan LR, Jackson CR, Miller LE. Electrical stimulation of the proprioceptive cortex (area 3a) used to instruct a behaving monkey. IEEE Trans Neural Syst Rehabil Eng. 2008;16:32–6.
    1. Lotze M, Flor H, Grodd W, Larbig W, Birbaumer N. Phantom movements and pain. An fMRI study in upper limb amputees. Brain. 2001;124:2268–77.
    1. Lundborg G, Rosén B. Sensory substitution in prosthetics. Hand Clin. 2001;17:481–8.
    1. Makin T, Holmes N, Ehrsson HH. On the other hand: dummy hands and peripersonal space. Behav Brain Res. 2008;191:1–10.
    1. Merzenich MM, Jenkins WM. Reorganization of cortical representations of the hand following alterations of skin inputs induced by nerve injury, skin island transfers, and experience. J Hand Ther. 1993;6:89–104.
    1. Merzenich MM, Nelson RJ, Stryker MP, Cynader MS, Schoppmann A, Zook JM. Somatosensory cortical map changes following digit amputation in adult monkeys. J Comp Neurol. 1984;224:591–605.
    1. Miller LA, Stubbefield KA, Lipschutz RD, Lock BA, Kuiken TA. Improved myoelectric prosthesis control using targeted reinnervation surgery: a case series. IEEE Trans Neural Syst Rehabil Eng. 2008;16:46–50.
    1. Navarro X, Krueger TB, Lago N, Micera S, Stieglitz T, Dario P. A critical review of interfaces with the peripheral nervous system for the control of neuroprostheses and hybrid bionic systems. J Peripher Nerv Syst. 2005;10:229–58.
    1. Nicolelis MA. Brain-machine interfaces to restore motor function and probe neural circuits. Nat Rev Neurosci. 2003;4:417–22.
    1. Pons TP, Garraghty PE, Ommaya AK, Kaas JH, Taub E, Mishkin M. Massive cortical reorganization after sensory deafferentation in adult macaques. Science. 1991;252:1857–60.
    1. Ramachandran VS, Hirstein W. The perception of phantom limbs. The D. O. Hebb lecture. Brain. 1998;121:1603–30.
    1. Ramachandran VS, Rogers-Ramachandran D, Stewart M. Perceptual correlates of massive cortical reorganization. Science. 1992;258:1159–60.
    1. Ramachandran VS, Rogers-Ramachandran D. Synaesthesia in phantom limbs induced with mirrors. Proc Biol Sci. 1996;263:377–86.
    1. Ramachandran VS, Rogers-Ramachandran D. Sensations referred to a patient's phantom arm from another subjects intact arm: Perceptual correlates of mirror neurons. Med Hypotheses. 2008;70:1233–34.
    1. Riso RR. Strategies for providing upper extremity amputees with tactile and hand position feedback—moving closer to the bionic arm. Technol Health Care. 1999;7:401–9.
    1. Roux FE, Lotterie JA, Cassol E, Lazorthes Y, Sol JC, Berry I. Cortical areas involved in virtual movement of phantom limbs: comparison with normal subjects. Neurosurgery. 2003;53:1342–52.
    1. Sacks O. The man who mistook his wife for a hat and other clinical tales. London: Harper Perennial; 1987.
    1. Schwartz AB. Cortical neural prosthetics. Annu Rev Neurosci. 2004;27:487–507.
    1. Sebelius FC, Rosén BN, Lundborg GN. Refined myoelectric control in below-elbow amputees using artificial neural networks and a data glove. J Hand Surg. 2005;30:780–9.
    1. Tsakiris M, Haggard P. The rubber hand illusion revisited: visuotactile integration and self-attribution. J Exp Psychol Hum Percept Perform. 2005;31:80–91.
    1. Velliste M, Perel S, Spalding MC, Whitford AS, Schwartz AB. Cortical control of a prosthetic arm for self-feeding. Nature. 2008;453:1098–101.
    1. Wall JT, Xu J, Wang X. Human brain plasticity: an emerging view of the multiple substrates and mechanisms that cause cortical changes and related sensory dysfunctions after injuries of sensory inputs from the body. Brain Res Brain Res Rev. 2002;39:181–215.
    1. Yang TT, Gallen C, Schwartz B, Bloom FE, Ramachandran VS, Cobb S. Sensory maps in the human brain. Nature. 1994;368:592–93.

Source: PubMed

3
Abonneren