Visuotactile integration modulates motor performance in a perceptual decision-making task

. 2017 Jun 13 ; 7 (1) : 3333. [epub] 20170613

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid28611387
Odkazy

PubMed 28611387
PubMed Central PMC5469742
DOI 10.1038/s41598-017-03488-0
PII: 10.1038/s41598-017-03488-0
Knihovny.cz E-zdroje

Body ownership is critically dependent on multimodal integration as for instance revealed in the Rubber Hand Illusion (RHI) and a number of studies which have addressed the neural correlates of the processes underlying this phenomenon. Both experimental and clinical research have shown that the structures underlying body ownership seem to significantly overlap with those of motor control including the parietal and ventral premotor cortices, Temporal Parietal Junction (TPJ) and the insula. This raises the question of whether this structural overlap between body ownership and motor control structures is of any functional significance. Here, we investigate the specific question of whether experimentally induced ownership over a virtual limb can modulate the performance of that limb in a simple sensorimotor task. Using a Virtual reality (VR) environment we modulate body ownership in three experimental conditions with respect to the (in)congruence of stimulus configurations. Our results show that the degree of ownership directly modulates motor performance. This implies that body ownership is not exclusively a perceptual and/or subjective multimodal state but that it is tightly coupled to systems for decision-making and motor control.

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Ernst MO, Bülthoff HH. Merging the senses into a robust percept. Trends in cognitive sciences. 2004;8:162–169. doi: 10.1016/j.tics.2004.02.002. PubMed DOI

Makin TR, Holmes NP, Ehrsson HH. On the other hand: dummy hands and peripersonal space. Behavioural brain research. 2008;191:1–10. doi: 10.1016/j.bbr.2008.02.041. PubMed DOI

Graziano, M. S. & Botvinick, M. M. How the brain represents the body: insights from neurophysiology and psychology. Common mechanisms in perception and action: Attention and performance XIX 136–157 (2002).

Sober SJ, Sabes PN. Multisensory integration during motor planning. The Journal of Neuroscience. 2003;23:6982–6992. PubMed PMC

Johnson H, Haggard P. Motor awareness without perceptual awareness. Neuropsychologia. 2005;43:227–237. doi: 10.1016/j.neuropsychologia.2004.11.009. PubMed DOI

Berti A, et al. Shared cortical anatomy for motor awareness and motor control. Science. 2005;309:488–491. doi: 10.1126/science.1110625. PubMed DOI

Castiello U, Paulignan Y, Jeannerod M. Temporal dissociation of motor responses and subjective awareness. Brain. 1991;114:2639–2655. doi: 10.1093/brain/114.6.2639. PubMed DOI

Johnson H, van Beers RJ, Haggard P. Action and awareness in pointing tasks. Experimental Brain Research. 2002;146:451–459. doi: 10.1007/s00221-002-1200-z. PubMed DOI

Maravita A, Spence C, Driver J. Multisensory integration and the body schema: close to hand and within reach. Current biology. 2003;13:R531–R539. doi: 10.1016/S0960-9822(03)00449-4. PubMed DOI

Stein BE, Stanford TR. Multisensory integration: current issues from the perspective of the single neuron. Nature Reviews Neuroscience. 2008;9:255–266. doi: 10.1038/nrn2331. PubMed DOI

Head H, Holmes G. Sensory disturbances from cerebral lesions. Brain. 1911;34:102–254. doi: 10.1093/brain/34.2-3.102. DOI

Tsakiris M, Hesse MD, Boy C, Haggard P, Fink GR. Neural signatures of body ownership: a sensory network for bodily self-consciousness. Cerebral cortex. 2007;17:2235–2244. doi: 10.1093/cercor/bhl131. PubMed DOI

Gallagher S. Philosophical conceptions of the self: implications for cognitive science. Trends in cognitive sciences. 2000;4:14–21. doi: 10.1016/S1364-6613(99)01417-5. PubMed DOI

Tsakiris M, Carpenter L, James D, Fotopoulou A. Hands only illusion: multisensory integration elicits sense of ownership for body parts but not for non-corporeal objects. Experimental Brain Research. 2010;204:343–352. doi: 10.1007/s00221-009-2039-3. PubMed DOI

Blanke O. Multisensory brain mechanisms of bodily self-consciousness. Nature Reviews Neuroscience. 2012;13:556–571. PubMed

Ito M. Control of mental activities by internal models in the cerebellum. Nature Reviews Neuroscience. 2008;9:304–313. doi: 10.1038/nrn2332. PubMed DOI

Kawato M. Internal models for motor control and trajectory planning. Current opinion in neurobiology. 1999;9:718–727. doi: 10.1016/S0959-4388(99)00028-8. PubMed DOI

Wolpert DM, Ghahramani Z, Jordan MI. An internal model for sensorimotor integration. Science. 1995;269:1880. doi: 10.1126/science.7569931. PubMed DOI

Körding KP, Wolpert DM. Bayesian decision theory in sensorimotor control. Trends in cognitive sciences. 2006;10:319–326. doi: 10.1016/j.tics.2006.05.003. PubMed DOI

Tsakiris M, Costantini M, Haggard P. The role of the right temporo-parietal junction in maintaining a coherent sense of one’s body. Neuropsychologia. 2008;46:3014–3018. doi: 10.1016/j.neuropsychologia.2008.06.004. PubMed DOI

Ehrsson HH, Spence C, Passingham RE. That’s my hand! activity in premotor cortex reflects feeling of ownership of a limb. Science. 2004;305:875–877. doi: 10.1126/science.1097011. PubMed DOI

Tsakiris M, Haggard P. The rubber hand illusion revisited: visuotactile integration and self-attribution. Journal of Experimental Psychology: Human Perception and Performance. 2005;31:80. PubMed

Botvinick M, Cohen J, et al. Rubber hands’ feel’touch that eyes see. Nature. 1998;391:756–756. doi: 10.1038/35784. PubMed DOI

Ehrsson HH, Holmes NP, Passingham RE. Touching a rubber hand: feeling of body ownership is associated with activity in multisensory brain areas. The Journal of Neuroscience. 2005;25:10564–10573. doi: 10.1523/JNEUROSCI.0800-05.2005. PubMed DOI PMC

Vogeley K, et al. Neural correlates of first-person perspective as one constituent of human self-consciousness. Journal of cognitive neuroscience. 2004;16:817–827. doi: 10.1162/089892904970799. PubMed DOI

Farrer C, Frith CD. Experiencing oneself vs another person as being the cause of an action: the neural correlates of the experience of agency. Neuroimage. 2002;15:596–603. doi: 10.1006/nimg.2001.1009. PubMed DOI

Devue C, et al. Here i am: the cortical correlates of visual self-recognition. Brain research. 2007;1143:169–182. doi: 10.1016/j.brainres.2007.01.055. PubMed DOI

Farrer C, et al. Modulating the experience of agency: a positron emission tomography study. Neuroimage. 2003;18:324–333. doi: 10.1016/S1053-8119(02)00041-1. PubMed DOI

Gentile G, Petkova VI, Ehrsson HH. Integration of visual and tactile signals from the hand in the human brain: an fmri study. Journal of Neurophysiology. 2011;105:910–922. doi: 10.1152/jn.00840.2010. PubMed DOI PMC

Vallar G, Ronchi R. Somatoparaphrenia: a body delusion. a review of the neuropsychological literature. Experimental Brain Research. 2009;192:533–551. doi: 10.1007/s00221-008-1562-y. PubMed DOI

Craig, A. D. How do you feel–now? the anterior insula and human awareness. Nature reviews neuroscience10 (2009). PubMed

Karnath H-O, Baier B, Nägele T. Awareness of the functioning of one’s own limbs mediated by the insular cortex? The Journal of Neuroscience. 2005;25:7134–7138. doi: 10.1523/JNEUROSCI.1590-05.2005. PubMed DOI PMC

Baier B, Karnath H-O. Tight link between our sense of limb ownership and self-awareness of actions. Stroke. 2008;39:486–488. doi: 10.1161/STROKEAHA.107.495606. PubMed DOI

Bourbonnais D, Noven SV. Weakness in patients with hemiparesis. American Journal of Occupational Therapy. 1989;43:313–319. doi: 10.5014/ajot.43.5.313. PubMed DOI

Coslett HB. Evidence for a disturbance of the body schema in neglect. Brain and cognition. 1998;37:527–544. doi: 10.1006/brcg.1998.1011. PubMed DOI

Haggard P. Conscious intention and motor cognition. Trends in cognitive sciences. 2005;9:290–295. doi: 10.1016/j.tics.2005.04.012. PubMed DOI

Pia L, Neppi-Modona M, Ricci R, Berti A. The anatomy of anosognosia for hemiplegia: a meta-analysis. Cortex. 2004;40:367–377. doi: 10.1016/S0010-9452(08)70131-X. PubMed DOI

Schwoebel J, Friedman R, Duda N, Coslett HB. Pain and the body schema. Brain. 2001;124:2098–2104. doi: 10.1093/brain/124.10.2098. PubMed DOI

Halligan PW, Marshall JC, Wade DT. Unilateral somatoparaphrenia after right hemisphere stroke: a case description. Cortex. 1995;31:173–182. doi: 10.1016/S0010-9452(13)80115-3. PubMed DOI

Crapse TB, Sommer MA. Corollary discharge across the animal kingdom. Nature Reviews Neuroscience. 2008;9:587–600. doi: 10.1038/nrn2457. PubMed DOI PMC

Ramachandran, V. S., Blakeslee, S. & Sacks, O. W. Phantoms in the brain: Probing the mysteries of the human mind (William Morrow New York, 1998).

IJsselsteijn WA, de Kort YAW, Haans A. Is this my hand i see before me? the rubber hand illusion in reality, virtual reality, and mixed real. ity. Presence: Teleoperators and Virtual Environments. 2006;15:455–464. doi: 10.1162/pres.15.4.455. DOI

Slater M, Pérez Marcos D, Ehrsson H, Sanchez-Vives MV. Towards a digital body: the virtual arm illusion. Frontiers in human neuroscience. 2008;2:6. doi: 10.3389/neuro.09.006.2008. PubMed DOI PMC

Armel KC, Ramachandran VS. Projecting sensations to external objects: evidence from skin conductance response. Proceedings of the Royal Society of London B: Biological Sciences. 2003;270:1499–1506. doi: 10.1098/rspb.2003.2364. PubMed DOI PMC

Ehrsson HH, Wiech K, Weiskopf N, Dolan RJ, Passingham RE. Threatening a rubber hand that you feel is yours elicits a cortical anxiety response. Proceedings of the National Academy of Sciences. 2007;104:9828–9833. doi: 10.1073/pnas.0610011104. PubMed DOI PMC

van Ee R, van Boxtel JJ, Parker AL, Alais D. Multisensory congruency as a mechanism for attentional control over perceptual selection. The Journal of Neuroscience. 2009;29:11641–11649. doi: 10.1523/JNEUROSCI.0873-09.2009. PubMed DOI PMC

Rock I, Victor J. Vision and touch: An experimentally created conflict between the two senses. Science. 1964;143:594–596. doi: 10.1126/science.143.3606.594. PubMed DOI

Hecht D, Reiner M. Sensory dominance in combinations of audio, visual and haptic stimuli. Experimental brain research. 2009;193:307–314. doi: 10.1007/s00221-008-1626-z. PubMed DOI

Salomon, R. et al. Changing motor perception by sensorimotor conflicts and body ownership. Scientific reports6 (2016). PubMed PMC

Taimela S. Factors affecting reaction-time testing and the interpretation of results. Perceptual and Motor skills. 1991;73:1195–1202. doi: 10.2466/pms.1991.73.3f.1195. DOI

Zhang, J. & Rowe, J. B. Dissociable mechanisms of speed-accuracy tradeoff during visual perceptual learning are revealed by a hierarchical drift-diffusion model. Toward a Unified View of the Speed-Accuracy Trade-Off: Behaviour, Neurophysiology and Modelling 71 (2016). PubMed PMC

Slater M. Place illusion and plausibility can lead to realistic behaviour in immersive virtual environments. Philosophical Transactions of the Royal Society B: Biological Sciences. 2009;364:3549–3557. doi: 10.1098/rstb.2009.0138. PubMed DOI PMC

Rognini G, et al. Visuo-tactile integration and body ownership during self-generated action. European Journal of Neuroscience. 2013;37:1120–1129. doi: 10.1111/ejn.12128. PubMed DOI

Banzi, M., Cuartielles, D., Igoe, T., Martino, G. & Mellis, D. Site arduino (2013).

Keele, S. W. Motor control. (1986).

Miall RC, Wolpert DM. Forward models for physiological motor control. Neural networks. 1996;9:1265–1279. doi: 10.1016/S0893-6080(96)00035-4. PubMed DOI

Stein BE. Neural mechanisms for synthesizing sensory information and producing adaptive behaviors. Experimental Brain Research. 1998;123:124–135. doi: 10.1007/s002210050553. PubMed DOI

Maffei, G., Sanchez-Fibla, M., Herreros, I. & Verschure, P. F. The role of a cerebellum-driven perceptual prediction within a robotic postural task. In International Conference on Simulation of Adaptive Behavior, pp. 76–87 (2014).

Samad, M., Chung, A. J. & Shams, L. Perception of body ownership is driven by bayesian sensory inference. PloS one10, e0117178 (2015). PubMed PMC

Beck JM, et al. Probabilistic population codes for bayesian decision making. Neuron. 2008;60:1142–1152. doi: 10.1016/j.neuron.2008.09.021. PubMed DOI PMC

Mamassian, P., Landy, M. S. & Maloney, L. T. Bayesian modelling of visual perception. Probabilistic models of the brain: Perception and neural function 13–36 (2002).

Limanowski, J. What can body ownership illusions tell us about minimal phenomenal selfhood? Frontiers in human neuroscience8 (2014). PubMed PMC

Tsakiris M, Prabhu G, Haggard P. Having a body versus moving your body: How agency structures body-ownership. Consciousness and cognition. 2006;15:423–432. doi: 10.1016/j.concog.2005.09.004. PubMed DOI

Jack D, et al. Virtual reality-enhanced stroke rehabilitation. IEEE transactions on neural systems and rehabilitation engineering. 2001;9:308–318. doi: 10.1109/7333.948460. PubMed DOI

Merians AS, et al. Virtual reality–augmented rehabilitation for patients following stroke. Physical therapy. 2002;82:898–915. PubMed

Cameirão MS, I Badia SB, Oller ED, Verschure PF. Neurorehabilitation using the virtual reality based rehabilitation gaming system: methodology, design, psychometrics, usability and validation. Journal of neuroengineering and rehabilitation. 2010;7:1. doi: 10.1186/1743-0003-7-48. PubMed DOI PMC

Saposnik G, et al. Effectiveness of virtual reality using wii gaming technology in stroke rehabilitation a pilot randomized clinical trial and proof of principle. Stroke. 2010;41:1477–1484. doi: 10.1161/STROKEAHA.110.584979. PubMed DOI PMC

Johansson BB. Brain plasticity and stroke rehabilitation the willis lecture. Stroke. 2000;31:223–230. doi: 10.1161/01.STR.31.1.223. PubMed DOI

Kleim JA, Jones TA. Principles of experience-dependent neural plasticity: implications for rehabilitation after brain damage. Journal of speech, language, and hearing research. 2008;51:S225–S239. doi: 10.1044/1092-4388(2008/018). PubMed DOI

Maier, M., Ballester, B. R., Duarte, E., Duff, A. & Verschure, P. F. Social integration of stroke patients through the multiplayer rehabilitation gaming system. In International Conference on Serious Games, 100–114 (Springer, 2014).

Ballester, B. R., Oliva, L. S., Duff, A. & Verschure, P. Accelerating motor adaptation by virtual reality based modulation of error memories. In 2015 IEEE International Conference on Rehabilitation Robotics (ICORR), 623–629 (IEEE, 2015).

Ballester, B. R. et al. The visual amplification of goal-oriented movements counteracts acquired non-use in hemiparetic stroke patients. Journal of NeuroEngineering and Rehabilitation12(1) (2015). PubMed PMC

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