Weakening the subjective sensation of own hand ownership does not interfere with rapid finger movements
Autoři:
Arran T. Reader aff001; H. Henrik Ehrsson aff001
Působiště autorů:
Department of Neuroscience, Karolinska Institutet, Stockholm, Sweden
aff001
Vyšlo v časopise:
PLoS ONE 14(10)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0223580
Souhrn
When we perform a movement we generally have a clear distinction between which parts of the world constitute our body and which parts do not. However, how the sense of ownership over our body supports movement is not yet fully understood. We aimed to see whether a sense of ownership over the hand supports the performance of rapid hand movements. In three experiments (n = 48, n = 30, n = 24), we presented participants with congruent and incongruent visuotactile and visuoproprioceptive information regarding their own hand. In keeping with previous experiments, multisensory disintegration resulted in a reduction in the subjective sensation of ownership over the hand, as reflected in questionnaire responses. Following sensory stimulation, participants were required to rapidly abduct their index finger whilst the movement was tracked. We examined the hypothesis that, should a sense of ownership over the limb be necessary for generating rapid movements with that limb, reaction time would increase when hand ownership was reduced, whilst the acceleration and velocity of the movement would decrease. We observed that reductions in own hand ownership did not interfere with rapid index finger abduction, suggesting that the motor system may not be reliant on a subjective sense of ownership over the body in order to generate movement.
Klíčová slova:
Body limbs – Sensory perception – Fingers – Rubber – Kinematics – Bayesian method – Motor system
Zdroje
1. Ehrsson HH. The Concept of Body Ownership and Its Relation to Multisensory Integration. In: Stein BE, editor. The New Handbook of Multisensory Processes. Cambridge: MIT Press; 2012. pp. 775–792.
2. Blanke O, Slater M, Serino A. Behavioral, Neural, and Computational Principles of Bodily Self-Consciousness. Neuron. 2015;88: 145–166. doi: 10.1016/j.neuron.2015.09.029 26447578
3. Botvinick M, Cohen J. Rubber hands ‘feel’ touch that eyes see. Nature. 1998;391: 756–756. doi: 10.1038/35784 9486643
4. Kilteni K, Maselli A, Kording KP, Slater M. Over my fake body: body ownership illusions for studying the multisensory basis of own-body perception. Front Hum Neurosci. 2015;9. doi: 10.3389/fnhum.2015.00141 25852524
5. Longo MR, Schüür F, Kammers MPM, Tsakiris M, Haggard P. What is embodiment? A psychometric approach. Cognition. 2008;107: 978–998. doi: 10.1016/j.cognition.2007.12.004 18262508
6. Longo MR, Schüür F, Kammers MPM, Tsakiris M, Haggard P. Self awareness and the body image. Acta Psychol (Amst). 2009;132: 166–172. doi: 10.1016/j.actpsy.2009.02.003 19286139
7. Preston C. The role of distance from the body and distance from the real hand in ownership and disownership during the rubber hand illusion. Acta Psychol (Amst). 2013;142: 177–183. doi: 10.1016/j.actpsy.2012.12.005 23333877
8. Lane T, Yeh S-L, Tseng P, Chang A-Y. Timing disownership experiences in the rubber hand illusion. Cogn Res Princ Implic. 2017;2: 4. doi: 10.1186/s41235-016-0041-4 28203632
9. Macaluso E, Maravita A. The representation of space near the body through touch and vision. Neuropsychologia. 2010;48: 782–795. doi: 10.1016/j.neuropsychologia.2009.10.010 19837101
10. Naito E, Morita T, Amemiya K. Body representations in the human brain revealed by kinesthetic illusions and their essential contributions to motor control and corporeal awareness. Neurosci Res. 2016;104: 16–30. doi: 10.1016/j.neures.2015.10.013 26562333
11. Proske U, Gandevia SC. The Proprioceptive Senses: Their Roles in Signaling Body Shape, Body Position and Movement, and Muscle Force. Physiol Rev. 2012;92: 1651–1697. doi: 10.1152/physrev.00048.2011 23073629
12. Heed T, Gründler M, Rinkleib J, Rudzik FH, Collins T, Cooke E, et al. Visual information and rubber hand embodiment differentially affect reach-to-grasp actions. Acta Psychol (Amst). 2011;138: 263–271. doi: 10.1016/j.actpsy.2011.07.003 21788001
13. Kammers MPM, Kootker JA, Hogendoorn H, Dijkerman HC. How many motoric body representations can we grasp? Exp Brain Res. 2010;202: 203–212. doi: 10.1007/s00221-009-2124-7 20039029
14. Newport R, Pearce R, Preston C. Fake hands in action: Embodiment and control of supernumerary limbs. Exp Brain Res. 2010;204: 385–395. doi: 10.1007/s00221-009-2104-y 20012536
15. Newport R, Preston C. Disownership and disembodiment of the real limb without visuoproprioceptive mismatch. Cogn Neurosci. 2011;2: 179–185. doi: 10.1080/17588928.2011.565120 24168533
16. van der Hoort B, Guterstam A, Ehrsson HH. Being barbie: The size of one’s own body determines the perceived size of the world. PLoS One. 2011;6. doi: 10.1371/journal.pone.0020195 21633503
17. van der Hoort B, Ehrsson HH. Body ownership affects visual perception of object size by rescaling the visual representation of external space. Attention, Perception, Psychophys. 2014;76: 1414–1428. doi: 10.3758/s13414-014-0664-9 24806404
18. Van der Hoort B, Ehrsson HH. Illusions of having small or large invisible bodies influence visual perception of object size. Sci Rep. 2016;6: 1–9.
19. Kalckert A, Ehrsson HH. Moving a Rubber Hand that Feels Like Your Own: A Dissociation of Ownership and Agency. Front Hum Neurosci. 2012;6: 1–14.
20. Kalckert A, Ehrsson HH. The moving rubber hand illusion revisited: Comparing movements and visuotactile stimulation to induce illusory ownership. Conscious Cogn. 2014;26: 117–132. doi: 10.1016/j.concog.2014.02.003 24705182
21. Tsakiris M, Prabhu G, Haggard P. Having a body versus moving your body: How agency structures body-ownership. Conscious Cogn. 2006;15: 423–432. doi: 10.1016/j.concog.2005.09.004 16343947
22. Burin D, Livelli A, Garbarini F, Fossataro C, Folegatti A, Gindri P, et al. Are movements necessary for the sense of body ownership? evidence from the rubber hand illusion in pure hemiplegic patients. PLoS One. 2015;10: 1–12. doi: 10.1371/journal.pone.0117155 25775041
23. Burin D, Garbarini F, Bruno V, Fossataro C, Destefanis C, Berti A, et al. Movements and body ownership: Evidence from the rubber hand illusion after mechanical limb immobilization. Neuropsychologia. 2017;107: 41–47. doi: 10.1016/j.neuropsychologia.2017.11.004 29109038
24. Pyasik M, Salatino A, Pia L. Do movements contribute to sense of body ownership? Rubber hand illusion in expert pianists. Psychol Res. 2019;83: 185–195. doi: 10.1007/s00426-018-1137-x 30560294
25. Scandola M, Aglioti SM, Avesani R, Bertagnoni G, Marangoni A, Moro V. Corporeal illusions in chronic spinal cord injuries. Conscious Cogn. 2017;49: 278–290. doi: 10.1016/j.concog.2017.01.010 28222382
26. Tidoni E, Grisoni L, Liuzza MT, Aglioti SM. Rubber hand illusion highlights massive visual capture and sensorimotor face-hand remapping in a tetraplegic man. Restor Neurol Neurosci. 2014;32: 611–622. doi: 10.3233/RNN-130385 25015700
27. Fiorio M, Weise D, Önal-Hartmann C, Zeller D, Tinazzi M, Classen J. Impairment of the rubber hand illusion in focal hand dystonia. Brain. 2011;134: 1428–1437. doi: 10.1093/brain/awr026 21378099
28. della Gatta F, Garbarini F, Puglisi G, Leonetti A, Berti A, Borroni P. Decreased motor cortex excitability mirrors own hand disembodiment during the rubber hand illusion. Elife. 2016;5. doi: 10.7554/eLife.14972 27760692
29. Tsakiris M, Haggard P. The Rubber Hand Illusion Revisited: Visuotactile Integration and Self-Attribution. J Exp Psychol Hum Percept Perform. 2005;31: 80–91. doi: 10.1037/0096-1523.31.1.80 15709864
30. Abdulkarim Z, Ehrsson HH. No causal link between changes in hand position sense and feeling of limb ownership in the rubber hand illusion. Attention, Perception, Psychophys. 2016;78: 707–720. doi: 10.3758/s13414-015-1016-0 26555651
31. Kilteni K, Grau-Sánchez J, Veciana De Las Heras M, Rodríguez-Fornells A, Slater M. Decreased Corticospinal Excitability after the Illusion of Missing Part of the Arm. Front Hum Neurosci. 2016;10. doi: 10.3389/fnhum.2016.00145 27148005
32. Karabanov AN, Ritterband-Rosenbaum A, Christensen MS, Siebner HR, Nielsen JB. Modulation of fronto-parietal connections during the rubber hand illusion. Eur J Neurosci. 2017;45: 964–974. doi: 10.1111/ejn.13538 28186673
33. Isayama R, Vesia M, Jegatheeswaran G, Elahi B, Gunraj CA, Cardinali L, et al. Rubber hand illusion modulates the influences of somatosensory and parietal inputs to the motor cortex. J Neurophysiol. 2019;121: 563–573. doi: 10.1152/jn.00345.2018 30625001
34. Haggard P. Sense of agency in the human brain. Nat Rev Neurosci. 2017;18: 196–207. doi: 10.1038/nrn.2017.14 28251993
35. Collins KL, Guterstam A, Cronin J, Olson JD, Ehrsson HH, Ojemann JG. Ownership of an artificial limb induced by electrical brain stimulation. Proc Natl Acad Sci. 2017;114: 166–171. doi: 10.1073/pnas.1616305114 27994147
36. Ehrsson HH, Rosén B, Stockselius A, Ragnö C, Köhler P, Lundborg G. Upper limb amputees can be induced to experience a rubber hand as their own. Brain. 2008;131: 3443–3452. doi: 10.1093/brain/awn297 19074189
37. Schmalzl L, Kalckert A, Ragnö C, Ehrsson HH. Neural correlates of the rubber hand illusion in amputees: A report of two cases. Neurocase. 2014;20: 407–420. doi: 10.1080/13554794.2013.791861 23682688
38. Van Den Heiligenberg FMZ, Orlov T, MacDonald SN, Duff EP, Henderson Slater D, Beckmann CF, et al. Artificial limb representation in amputees. Brain. 2018;141: 1422–1433. doi: 10.1093/brain/awy054 29534154
39. Vallar G, Ronchi R. Somatoparaphrenia: A body delusion. A review of the neuropsychological literature. Exp Brain Res. 2009;192: 533–551. doi: 10.1007/s00221-008-1562-y 18813916
40. Brugger P, Lenggenhager B. The bodily self and its disorders. Curr Opin Neurol. 2014;27: 644–652. doi: 10.1097/WCO.0000000000000151 25333602
41. Ronchi R, Park HD, Blanke O. Bodily self-consciousness and its disorders [Internet]. 1st ed. Handbook of Clinical Neurology. Elsevier B.V.; 2018. doi: 10.1016/B978-0-444-63622-5.00015-2
42. Jenkinson PM, Moro V, Fotopoulou A. Definition: Asomatognosia. Cortex. 2018;101: 300–301. doi: 10.1016/j.cortex.2018.02.001 29510834
43. Tieri G, Morone G, Paolucci S, Iosa M. Virtual reality in cognitive and motor rehabilitation: facts, fiction and fallacies. Expert Rev Med Devices. 2018;15: 107–117. doi: 10.1080/17434440.2018.1425613 29313388
44. van Stralen HE, van Zandvoort MJE, Kappelle LJ, Dijkerman HC. The Rubber Hand Illusion in a patient with hand disownership. Perception. 2013;42: 991–993. doi: 10.1068/p7583 24386718
45. Martinaud O, Besharati S, Jenkinson PM, Fotopoulou A. Ownership illusions in patients with body delusions: Different neural profiles of visual capture and disownership. Cortex. 2017;87: 174–185. doi: 10.1016/j.cortex.2016.09.025 27839786
46. Lenggenhager B, Hilti L, Brugger P. Disturbed body integrity and the “rubber foot illusion”. Neuropsychology. 2015;29: 205–211. doi: 10.1037/neu0000143 25265068
47. Zeller D, Gross C, Bartsch A, Johansen-Berg H, Classen J. Ventral Premotor Cortex May Be Required for Dynamic Changes in the Feeling of Limb Ownership: A Lesion Study. J Neurosci. 2011;31: 4852–4857. doi: 10.1523/JNEUROSCI.5154-10.2011 21451023
48. Gentile G, Guterstam A, Brozzoli C, Ehrsson HH. Disintegration of Multisensory Signals from the Real Hand Reduces Default Limb Self-Attribution: An fMRI Study. J Neurosci. 2013;33: 13350–13366. doi: 10.1523/JNEUROSCI.1363-13.2013 23946393
49. Newport R, Gilpin HR. Multisensory disintegration and the disappearing hand trick. Curr Biol. 2011;21: R804–R805. doi: 10.1016/j.cub.2011.08.044 21996499
50. Kannape OA, Smith EJT, Moseley P, Roy MP, Lenggenhager B. Experimentally induced limb-disownership in mixed reality. Neuropsychologia. 2019;124: 161–170. doi: 10.1016/j.neuropsychologia.2018.12.014 30576686
51. Graham KT, Martin-Iverson MT, Holmes NP, Waters FA. The projected hand illusion: component structure in a community sample and association with demographics, cognition, and psychotic-like experiences. Attention, Perception, Psychophys. 2014;77: 207–219. doi: 10.3758/s13414-014-0748-6 25120179
52. Osumi M, Nobusako S, Zama T, Taniguchi M, Shimada S, Morioka S. Sensorimotor incongruence alters limb perception and movement. Hum Mov Sci. 2018;57: 251–257. doi: 10.1016/j.humov.2017.09.003 28943027
53. Lesur MR, Weijs ML, Simon C, Kannape OA, Lenggenhager B. Achronopresence: how temporal visuotactile and visuomotor mismatches modulate embodiment. bioRxiv Neurosci. 2019; doi: 10.1101/596858
54. Longo MR, Haggard P. Sense of agency primes manual motor responses. Perception. 2009;38: 69–78. doi: 10.1068/p6045 19323137
55. Folegatti A, de Vignemont F, Pavani F, Rossetti Y, Farné A, Farnè A. Losing one’s hand: Visual-proprioceptive conflict affects touch perception. Harris J, editor. PLoS One. 2009;4: e6920. doi: 10.1371/journal.pone.0006920 19738900
56. de Vignemont F. Embodiment, ownership and disownership. Conscious Cogn. 2011;20: 82–93. doi: 10.1016/j.concog.2010.09.004 20943417
57. Rossini PM, Zarola F, Stalberg E, Caramia M. Pre-movement facilitation of motor-evoked potentials in man during transcranial stimulation of the central motor pathways. Brain Res. 1988;458: 20–30. doi: 10.1016/0006-8993(88)90491-x 3208099
58. Starr A, Caramia M, Zarola F, Rossini PM. Enhancement of motor cortical excitability in humans by non-invasive electrical stimulation appears prior to voluntary movement. Electroencephalogr Clin Neurophysiol. 1988;70: 26–32. doi: 10.1016/0013-4694(88)90191-5 2455627
59. Chen R, Yaseen Z, Cohen LG, Hallett M. Time course of corticospinal excitability in reaction time and self-paced movements. Ann Neurol. 1998;44: 317–325. doi: 10.1002/ana.410440306 9749597
60. Davey NJ, Rawlinson SR, Maskill DW, Ellaway PH. Facilitation of a hand muscle response to stimulation of the motor cortex preceding a simple reaction task. Motor Control. 1998;2: 241–250.
61. Leocani L, Cohen LG, Wassermann EM, Ikoma K, Hallett M. Human corticospinal excitability evaluated with transcranial magnetic stimulation during different reaction time paradigms. Brain. 2000;123: 1161–1173. doi: 10.1093/brain/123.6.1161 10825355
62. MacKinnon CD, Rothwell JC. Time-varying changes in corticospinal excitability accompanying the triphasic EMG pattern in humans. J Physiol. 2000;528: 633–645. doi: 10.1111/j.1469-7793.2000.00633.x 11060136
63. Duque J, Greenhouse I, Labruna L, Ivry RB. Physiological Markers of Motor Inhibition during Human Behavior. Trends Neurosci. 2017;40: 219–236. doi: 10.1016/j.tins.2017.02.006 28341235
64. Faul F, Erdfelder E, Lang A-G, Buchner A. G*Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods. 2007;39: 175–191. doi: 10.3758/BF03193146 17695343
65. Abdulkarim Z, Ehrsson HH. Recalibration of hand position sense during unconscious active and passive movement. Exp Brain Res. 2018;236: 551–561. doi: 10.1007/s00221-017-5137-7 29243136
66. 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. doi: 10.1126/science.1097011 15232072
67. Weiss C, Tsakiris M, Haggard P, Schütz-Bosbach S. Agency in the sensorimotor system and its relation to explicit action awareness. Neuropsychologia. 2014;52: 82–92. doi: 10.1016/j.neuropsychologia.2013.09.034 24096174
68. Benjamini Y, Yekutieli D. The control of the false discovery rate in multiple testing under dependency. Ann Stat. 2001;29: 1165–1188. doi: 10.1214/aos/1013699998
69. JASP Team. JASP (Version 0.9). JASP Team; 2018.
70. Rouder JN, Speckman PL, Sun D, Morey RD, Iverson G. Bayesian t tests for accepting and rejecting the null hypothesis. Psychon Bull Rev. 2009;16: 225–237. doi: 10.3758/PBR.16.2.225 19293088
71. Jarosz AF, Wiley J. What Are the Odds? A Practical Guide to Computing and Reporting Bayes Factors. J Probl Solving. 2014;7: 2–9. doi: 10.7771/1932-6246.1167
72. van Doorn J, Ly A, Marsman M, Wagenmakers E-J. Bayesian Inference for Kendall’s Rank Correlation Coefficient. Am Stat. 2018;72: 303–308. doi: 10.1080/00031305.2016.1264998
73. Costantini M, Haggard P. The rubber hand illusion: Sensitivity and reference frame for body ownership. Conscious Cogn. 2007;16: 229–240. doi: 10.1016/j.concog.2007.01.001 17317221
74. Fossataro C, Bruno V, Giurgola S, Bolognini N, Garbarini F. Losing my hand. Body ownership attenuation after virtual lesion of the primary motor cortex. Eur J Neurosci. 2018;48: 2272–2287. doi: 10.1111/ejn.14116 30117217
75. Smit M, Van Stralen HE, Van den Munckhof B, Snijders TJ, Dijkerman HC. The man who lost his body: Suboptimal multisensory integration yields body awareness problems after a right temporoparietal brain tumour. J Neuropsychol. 2018; doi: 10.1111/jnp.12153 29532598
76. Kilteni K, Ehrsson HH. Body ownership determines the attenuation of self-generated tactile sensations. Proc Natl Acad Sci. 2017;114: 8426–8431. doi: 10.1073/pnas.1703347114 28716932
77. Fossataro C, Gindri P, Mezzanato T, Pia L, Garbarini F. Bodily ownership modulation in defensive responses: Physiological evidence in brain-damaged patients with pathological embodiment of other’s body parts. Sci Rep. 2016;6: 1–11.
78. Burin D, Pyasik M, Salatino A, Pia L. That’s my hand! Therefore, that’s my willed action: How body ownership acts upon conscious awareness of willed actions. Cognition. 2017;166: 164–173. doi: 10.1016/j.cognition.2017.05.035 28577446
79. Burin D, Pyasik M, Ronga I, Cavallo M, Salatino A, Pia L. “As long as that is my hand, that willed action is mine”: Timing of agency triggered by body ownership. Conscious Cogn. 2018;58: 186–192. doi: 10.1016/j.concog.2017.12.005 29305042
80. Perepelkina O, Vorobeva V, Melnikova O, Arina G, Nikolaeva V. Artificial hand illusions dynamics: Onset and fading of static rubber and virtual moving hand illusions. Conscious Cogn. 2018;65: 216–227. doi: 10.1016/j.concog.2018.09.005 30218944
81. Bergouignan L, Nyberg L, Ehrsson HH. Out-of-body-induced hippocampal amnesia. Proc Natl Acad Sci. 2014;111: 4421–4426. doi: 10.1073/pnas.1318801111 24616529
82. Guterstam A, Abdulkarim Z, Ehrsson HH. Illusory ownership of an invisible body reduces autonomic and subjective social anxiety responses. Sci Rep. 2015;5: 9831. doi: 10.1038/srep09831 25906330
83. Lloyd DM. Spatial limits on referred touch to an alien limb may reflect boundaries of visuo-tactile peripersonal space surrounding the hand. Brain Cogn. 2007;64: 104–109. doi: 10.1016/j.bandc.2006.09.013 17118503
84. Aimola Davies AM, White RC, Davies M, Aimola AM, White RC, Davies M, et al. Spatial limits on the nonvisual self-touch illusion and the visual rubber hand illusion: Subjective experience of the illusion and proprioceptive drift. Conscious Cogn. 2013;22: 613–636. doi: 10.1016/j.concog.2013.03.006 23644413
Článok vyšiel v časopise
PLOS One
2019 Číslo 10
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Nejasný stín na plicích – kazuistika
- Masturbační chování žen v ČR − dotazníková studie
- Eliquis (apixaban) nově hrazen ze zdravotního pojištění
Najčítanejšie v tomto čísle
- Correction: Low dose naltrexone: Effects on medication in rheumatoid and seropositive arthritis. A nationwide register-based controlled quasi-experimental before-after study
- Combining CDK4/6 inhibitors ribociclib and palbociclib with cytotoxic agents does not enhance cytotoxicity
- Risk factors associated with IgA vasculitis with nephritis (Henoch–Schönlein purpura nephritis) progressing to unfavorable outcomes: A meta-analysis
- Prevalence of pectus excavatum (PE), pectus carinatum (PC), tracheal hypoplasia, thoracic spine deformities and lateral heart displacement in thoracic radiographs of screw-tailed brachycephalic dogs