Advertisement

Sense of ownership and not the sense of agency is spatially bounded within the space reachable with the unaugmented hand

  • Madhur MangalamEmail author
  • Sarah A. Cutts
  • Dorothy M. Fragaszy
Research Article

Abstract

While reaching for a coffee cup, we are aware that the hand we see belongs to us and it moves at our will (reflecting our senses of ownership and agency, respectively), and that the cup is within our hand’s reach rather than beyond it (i.e., in reachable space, RS, rather than in non-reachable space, NRS). Accepted psychological explanations of our sense of ownership, sense of agency, and our perception of space surrounding the body as RS or NRS propose a unitary dependence on Euclidean distance from the body. Here, we propose an alternate, affordance-based explanation of experienced ownership, agency, and perception of space surrounding the body as RS and NRS. Adult participants experienced the static rubber hand illusion (RHI) and its dynamic variant, while the rubber hand was either within their arm’s reach (i.e., in self-identified RS) or beyond it (i.e., in self-identified NRS). We found that when the participants experienced synchronous visual and tactile signals in the static RHI, and synchronous visual and kinesthetic signals in the dynamic RHI, they felt illusory ownership when the rubber hand was in RS but not when it was in NRS. Conversely, when the participants experienced synchronous visual and kinesthetic signals in the dynamic RHI, they felt agency, regardless of the rubber hand’s location. In addition, illusory ownership was accompanied by proprioceptive drift, a feeling that their hand was closer to the rubber hand than it actually was, but agency was not accompanied by proprioceptive drift. Together, these results indicate that our sense of ownership, while malleable enough to incorporate visible non-corporeal objects resembling a body part, is spatially constrained by proprioceptive signals specifying that body part’s actual location. In contrast, our sense of agency can incorporate a visible non-corporeal object, independent of its location with respect to the body. We propose that the psychological processes mediating our sense of ownership are closely linked with our perception of space surrounding the body, and that the spatial independence of our sense of agency reflects the coupling between our actions and perception of the environment, such as while using handheld tools as extensions of our body.

Keywords

Body ownership Forward model Multisensory integration Rubber hand illusion Self-attribution Self-recognition 

Notes

Acknowledgements

We thank the two anonymous reviewers for their comments and insightful suggestions that generated much discussion among the authors and helped significantly improve the final draft of this manuscript.

Author contributions

Conceptualization, MM and SAC; investigation, MM and SAC; data curation, MM and SAC; analysis, MM; visualization, MM; writing—original draft, MM, SAC, and DMF; writing—review and editing, MM, SAC, and DMF; supervision, MM and DMF.

Compliance with ethical standards

Conflict of interest

The authors declare that no competing interests exist.

References

  1. Aoki T, Francis PR, Kinoshita H (2003) Differences in the abilities of individual fingers during the performance of fast, repetitive tapping movements. Exp Brain Res 152:270–280.  https://doi.org/10.1007/s00221-003-1552-z CrossRefPubMedGoogle Scholar
  2. Arbib MA, Bonaiuto JB, Jacobs S, Frey SH (2009) Tool use and the distalization of the end-effector. Psychol Res 73:441–462.  https://doi.org/10.1007/s00426-009-0242-2 CrossRefPubMedGoogle Scholar
  3. Barnsley N, McAuley JH, Mohan R et al (2011) The rubber hand illusion increases histamine reactivity in the real arm. Curr Biol 21:R945–R946.  https://doi.org/10.1016/j.cub.2011.10.039 CrossRefPubMedGoogle Scholar
  4. Beckerle P, Castellini C, Lenggenhager B (2018) Robotic interfaces for cognitive psychology and embodiment research: a research roadmap. Wiley Interdiscip Rev Cogn Sci.  https://doi.org/10.1002/wcs.1486 PubMedGoogle Scholar
  5. Berger CC, Gonzalez-Franco M, Ofek E, Hinckley K (2018) The uncanny valley of haptics. Sci Robot 3:eaar7010.  https://doi.org/10.1126/scirobotics.aar7010 CrossRefGoogle Scholar
  6. Berti A, Frassinetti F (2000) When far becomes near: remapping of space by tool use. J Cogn Neurosci 12:415–420.  https://doi.org/10.1162/089892900562237 CrossRefPubMedGoogle Scholar
  7. Biran II, Chatterjee AA (2004) Alien hand syndrome. Arch Neurol 61:292–294.  https://doi.org/10.1001/archneur.61.2.292 CrossRefPubMedGoogle Scholar
  8. Blanke O (2012) Multisensory brain mechanisms of bodily self-consciousness. Nat Rev Neurosci 13:556–571.  https://doi.org/10.1038/nrn3292 CrossRefPubMedGoogle Scholar
  9. Botvinick M, Cohen J (1998) Rubber hands ‘feel’ touch that eyes see. Nature 391:756.  https://doi.org/10.1038/35784 CrossRefPubMedGoogle Scholar
  10. Bufacchi RJ, Iannetti GD (2018) An action field theory of peripersonal space. Trends Cogn Sci 22:1076–1090.  https://doi.org/10.1016/j.tics.2018.09.004 CrossRefPubMedGoogle Scholar
  11. Caggiano V, Fogassi L, Rizzolatti G et al (2009) Mirror neurons differentially encode the peripersonal and extrapersonal space of monkeys. Science (80-) 324:403–406.  https://doi.org/10.1126/science.1166818 CrossRefGoogle Scholar
  12. Canzoneri E, Marzolla M, Amoresano A et al (2013a) Amputation and prosthesis implantation shape body and peripersonal space representations. Sci Rep 3:2844.  https://doi.org/10.1038/srep02844 CrossRefPubMedGoogle Scholar
  13. Canzoneri E, Ubaldi S, Rastelli V et al (2013b) Tool-use reshapes the boundaries of body and peripersonal space representations. Exp Brain Res 228:25–42.  https://doi.org/10.1007/s00221-013-3532-2 CrossRefPubMedGoogle Scholar
  14. Chambon V, Wenke D, Fleming SM et al (2013) An online neural substrate for sense of agency. Cereb Cortex 23:1031–1037.  https://doi.org/10.1093/cercor/bhs059 CrossRefPubMedGoogle Scholar
  15. Cisek P, Kalaska JF (2010) Neural mechanisms for interacting with a world full of action choices. Annu Rev Neurosci 33:269–298.  https://doi.org/10.1146/annurev.neuro.051508.135409 CrossRefPubMedGoogle Scholar
  16. Costantini M, Haggard P (2007) The rubber hand illusion: sensitivity and reference frame for body ownership. Conscious Cogn 16:229–240.  https://doi.org/10.1016/j.concog.2007.01.001 CrossRefPubMedGoogle Scholar
  17. D’Angelo M, di Pellegrino G, Seriani S et al (2018) The sense of agency shapes body schema and peripersonal space. Sci Rep 8:13847.  https://doi.org/10.1038/s41598-018-32238-z CrossRefPubMedGoogle Scholar
  18. David N, Newen A, Vogeley K (2008) The “sense of agency” and its underlying cognitive and neural mechanisms. Conscious Cogn 17:523–534.  https://doi.org/10.1016/j.concog.2008.03.004 CrossRefPubMedGoogle Scholar
  19. di Pellegrino G, Làdavas E (2015) Peripersonal space in the brain. Neuropsychologia 66:126–133.  https://doi.org/10.1016/j.neuropsychologia.2014.11.011 CrossRefPubMedGoogle Scholar
  20. Doody RS, Jankovic J (1992) The alien hand and related signs. J Neurol Neurosurg Psychiatry 55:806–810.  https://doi.org/10.1136/jnnp.55.9.806 CrossRefPubMedGoogle Scholar
  21. Dummer T, Picot-Annand A, Neal T, Moore C (2009) Movement and the rubber hand illusion. Perception 38:271–280.  https://doi.org/10.1068/p5921 CrossRefPubMedGoogle Scholar
  22. Ehrsson HH (2012) The concept of body ownership and its relation to multisensory integration. In: Stein BE (ed) The new handbook of multisensory processes. MIT Press, Cambridge, pp 775–792Google Scholar
  23. Ehrsson HH, Spence C, Passingham RE (2004) That’s my hand! Activity in premotor cortex reflects feeling of ownership of a limb. Science (80-) 305:875–877.  https://doi.org/10.1126/science.1097011 CrossRefGoogle Scholar
  24. 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 CrossRefPubMedGoogle Scholar
  25. Ehrsson HH, Wiech K, Weiskopf N et al (2007) Threatening a rubber hand that you feel is yours elicits a cortical anxiety response. Proc Natl Acad Sci 104:9828–9833.  https://doi.org/10.1073/pnas.0610011104 CrossRefPubMedGoogle Scholar
  26. Engbert K, Wohlschläger A, Haggard P (2008) Who is causing what? The sense of agency is relational and efferent-triggered. Cognition 107:693–704.  https://doi.org/10.1016/j.cognition.2007.07.021 CrossRefPubMedGoogle Scholar
  27. Farnè A, Làdavas E (2000) Dynamic size-change of hand peripersonal space following tool use. Neuroreport 11:1645–1649.  https://doi.org/10.1016/S0010-9452(08)70468-4 CrossRefPubMedGoogle Scholar
  28. Flor H, Nikolajsen L, Jensen TS (2006) Phantom limb pain: a case of maladaptive CNS plasticity? Nat Rev Neurosci 7:873–881.  https://doi.org/10.1038/nrn1991 CrossRefPubMedGoogle Scholar
  29. Fogassi L, Gallese V, Fadiga L et al (1996) Coding of peripersonal space in inferior premotor cortex (area F4). J Neurophysiol 76:141–157.  https://doi.org/10.1152/jn.1996.76.1.141 CrossRefPubMedGoogle Scholar
  30. Fragaszy DM, Mangalam M (2018) Tooling. Adv Study Behav 50:177–241.  https://doi.org/10.1016/bs.asb.2018.01.001 CrossRefGoogle Scholar
  31. Gallivan JP, McLean DA, Valyear KF, Culham JC (2013) Decoding the neural mechanisms of human tool use. Elife 2:e00425.  https://doi.org/10.7554/eLife.00425 CrossRefPubMedGoogle Scholar
  32. Gibson JJ (1966) The senses considered as perceptual systems. Houghton Mifflin, BostonGoogle Scholar
  33. Gibson JJ (1977) The theory of affordances. In: Shaw RE, Bransford J (eds) Perceiving, acting, and knowing: toward an ecological psychology. Lawrence Erlbaum, Hillsdale, pp 67–82Google Scholar
  34. Gibson JJ (1979) The ecological approach to visual perception. Houghton Mifflin, BostonGoogle Scholar
  35. Giummarra MJ, Gibson SJ, Georgiou-Karistianis N, Bradshaw JL (2007) Central mechanisms in phantom limb perception: the past, present and future. Brain Res Rev 54:219–232.  https://doi.org/10.1016/j.brainresrev.2007.01.009 CrossRefPubMedGoogle Scholar
  36. Haggard P (2017) Sense of agency in the human brain. Nat Rev Neurosci 18:196–207.  https://doi.org/10.1038/nrn.2017.14 CrossRefPubMedGoogle Scholar
  37. Haggard P, Chambon V (2012) Sense of agency. Curr Biol 22:R390–R392.  https://doi.org/10.1016/j.cub.2012.02.040 CrossRefPubMedGoogle Scholar
  38. Holmes NP, Spence C (2004) The body schema and multisensory representation(s) of peripersonal space. Cogn Process 5:94–105.  https://doi.org/10.1007/s10339-004-0013-3 CrossRefPubMedGoogle Scholar
  39. Holmes NP, Calvert GA, Spence C (2004) Extending or projecting peripersonal space with tools? Multisensory interactions highlight only the distal and proximal ends of tools. Neurosci Lett 372:62–67.  https://doi.org/10.1016/j.neulet.2004.09.024 CrossRefPubMedGoogle Scholar
  40. Kalckert A, Ehrsson H (2012) Moving a rubber hand that feels like your own: a dissociation of ownership and agency. Front Hum Neurosci 6:40.  https://doi.org/10.3389/fnhum.2012.00040 CrossRefPubMedGoogle Scholar
  41. Kalckert A, Ehrsson HH (2014a) The moving rubber hand illusion revisited: comparing movements and visuotactile stimulation to induce illusory ownership. Conscious Cogn 26:117–132.  https://doi.org/10.1016/j.concog.2014.02.003 CrossRefPubMedGoogle Scholar
  42. Kalckert A, Ehrsson HH (2014b) The spatial distance rule in the moving and classical rubber hand illusions. Conscious Cogn 30:118–132.  https://doi.org/10.1016/j.concog.2014.08.022 CrossRefPubMedGoogle Scholar
  43. Kalckert A, Perera AT-M, Ganesan Y, Tan E (2019) Rubber hands in space: the role of distance and relative position in the rubber hand illusion. Exp Brain Res 237:1821–1832.  https://doi.org/10.1007/s00221-019-05539-6 CrossRefPubMedGoogle Scholar
  44. Làdavas E (2002) Functional and dynamic properties of visual peripersonal space. Trends Cogn Sci 6:17–22.  https://doi.org/10.1016/S1364-6613(00)01814-3 CrossRefGoogle Scholar
  45. Latash ML, Li Z-M, Zatsiorsky VM (1998) A principle of error compensation studied within a task of force production by a redundant set of fingers. Exp Brain Res 122:131–138.  https://doi.org/10.1007/s002210050500 CrossRefPubMedGoogle Scholar
  46. Lloyd DM (2007) Spatial limits on referred touch to an alien limb may reflect boundaries of visuo-tactile peripersonal space surrounding the hand. Brain Cogn 64:104–109.  https://doi.org/10.1016/j.bandc.2006.09.013 CrossRefPubMedGoogle Scholar
  47. Longo MR, Lourenco SF (2006) On the nature of near space: effects of tool use and the transition to far space. Neuropsychologia 44:977–981.  https://doi.org/10.1016/j.neuropsychologia.2005.09.003 CrossRefPubMedGoogle Scholar
  48. Longo MR, Schüür F, Kammers MPM et al (2008) What is embodiment? A psychometric approach. Cognition 107:978–998.  https://doi.org/10.1016/j.cognition.2007.12.004 CrossRefPubMedGoogle Scholar
  49. Makin TR, Wilf M, Schwartz I, Zohary E (2009) Amputees “neglect” the space near their missing hand. Psychol Sci 21:55–57.  https://doi.org/10.1177/0956797609354739 CrossRefPubMedGoogle Scholar
  50. Makin TR, de Vignemont F, Faisal AA (2017) Neurocognitive barriers to the embodiment of technology. Nat Biomed Eng 1:14.  https://doi.org/10.1038/s41551-016-0014 CrossRefGoogle Scholar
  51. Mangalam M, Fragaszy DM (2016) Transforming the body-only system into the body-plus-tool system. Anim Behav 117:115–122.  https://doi.org/10.1016/j.anbehav.2016.04.016 CrossRefGoogle Scholar
  52. Martel M, Cardinali L, Roy AC, Farnè A (2016) Tool-use: an open window into body representation and its plasticity. Cogn Neuropsychol 33:82–101.  https://doi.org/10.1080/02643294.2016.1167678 CrossRefPubMedGoogle Scholar
  53. Miall RC, Wolpert DM (1996) Forward models for physiological motor control. Neural Netw 9:1265–1279.  https://doi.org/10.1016/S0893-6080(96)00035-4 CrossRefPubMedGoogle Scholar
  54. Moore JW (2016) What is the sense of agency and why does it matter? Front Psychol 7:1272.  https://doi.org/10.3389/fpsyg.2016.01272 PubMedGoogle Scholar
  55. Pavani F, Spence C, Driver J (2000) Visual capture of touch: out-of-the-body experiences with rubber gloves. Psychol Sci 11:353–359.  https://doi.org/10.1111/1467-9280.00270 CrossRefPubMedGoogle Scholar
  56. Pazzaglia M, Molinari M (2016) The embodiment of assistive devices—from wheelchair to exoskeleton. Phys Life Rev 16:163–175.  https://doi.org/10.1016/j.plrev.2015.11.006 CrossRefPubMedGoogle Scholar
  57. Pegna AJ, Leila P, Anne-Sarah C et al (2001) So near yet so far: neglect in far or near space depends on tool use. Ann Neurol 50:820–822.  https://doi.org/10.1002/ana.10058 CrossRefPubMedGoogle Scholar
  58. Pezzulo G, Cisek P (2016) Navigating the affordance landscape: feedback control as a process model of behavior and cognition. Trends Cogn Sci 20:414–424.  https://doi.org/10.1016/j.tics.2016.03.013 CrossRefPubMedGoogle Scholar
  59. Preston C (2013) 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) 142:177–183.  https://doi.org/10.1016/j.actpsy.2012.12.005 CrossRefGoogle Scholar
  60. 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/s00221-012-3374-3 CrossRefPubMedGoogle Scholar
  61. Sato A, Yasuda A (2005) Illusion of sense of self-agency: discrepancy between the predicted and actual sensory consequences of actions modulates the sense of self-agency, but not the sense of self-ownership. Cognition 94:241–255.  https://doi.org/10.1016/j.cognition.2004.04.003 CrossRefPubMedGoogle Scholar
  62. Stein BE, Stanford TR (2008) Multisensory integration: current issues from the perspective of the single neuron. Nat Rev Neurosci 9:255–266.  https://doi.org/10.1038/nrn2331 CrossRefPubMedGoogle Scholar
  63. 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
  64. Tsakiris M, Haggard P (2005) The rubber hand illusion revisited: visuotactile integration and self-attribution. J Exp Psychol Hum Percept Perform 31:80–91.  https://doi.org/10.1037/0096-1523.31.1.80 CrossRefPubMedGoogle Scholar
  65. 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
  66. Tsakiris M, Schütz-Bosbach S, Gallagher S (2007) On agency and body-ownership: phenomenological and neurocognitive reflections. Conscious Cogn 16:645–660.  https://doi.org/10.1016/j.concog.2007.05.012 CrossRefPubMedGoogle Scholar
  67. Umiltà MA, Escola L, Intskirveli I et al (2008) When pliers become fingers in the monkey motor system. Proc Natl Acad Sci USA 105:2209–2213.  https://doi.org/10.1073/pnas.0705985105 CrossRefPubMedGoogle Scholar
  68. Wolpert DM, Flanagan JR (2001) Motor prediction. Curr Biol 11:R729–R732.  https://doi.org/10.1016/S0960-9822(01)00432-8 CrossRefPubMedGoogle Scholar
  69. Wolpert DM, Ghahramani Z, Jordan MI (1995) An internal model for sensorimotor integration. Science (80-) 269:1880–1882.  https://doi.org/10.1126/science.7569931 CrossRefGoogle Scholar
  70. Yang G-Z, Bellingham J, Dupont PE et al (2018) The grand challenges of science robotics. Sci Robot 3:eaar7650.  https://doi.org/10.1126/scirobotics.aar7650 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Physical Therapy, Movement and Rehabilitation SciencesNortheastern UniversityBostonUSA
  2. 2.Department of PsychologyUniversity of GeorgiaAthensUSA

Personalised recommendations