Multi-sensory and sensorimotor foundation of bodily self-consciousness - an interdisciplinary approach

Silvio Ionta, Roger Gassert, Olaf Blanke, Silvio Ionta, Roger Gassert, Olaf Blanke

Abstract

Scientific investigations on the nature of the self have so far focused on high-level mechanisms. Recent evidence, however, suggests that low-level bottom-up mechanisms of multi-sensory integration play a fundamental role in encoding specific components of bodily self-consciousness, such as self-location and first-person perspective (Blanke and Metzinger, 2009). Self-location and first-person perspective are abnormal in neurological patients suffering from out-of-body experiences (Blanke et al., 2004), and can be manipulated experimentally in healthy subjects by imposing multi-sensory conflicts (Lenggenhager et al., 2009). Activity of the temporo-parietal junction (TPJ) reflects experimentally induced changes in self-location and first-person perspective (Ionta et al., 2011), and dysfunctions in TPJ are causally associated with out-of-body experiences (Blanke et al., 2002). We argue that TPJ is one of the key areas for multi-sensory integration of bodily self-consciousness, that its levels of activity reflect the experience of the conscious "I" as embodied and localized within bodily space, and that these mechanisms can be systematically investigated using state of the art technologies such as robotics, virtual reality, and non-invasive neuroimaging.

Keywords: body; multi-sensory integration; neuroscience robotics; self consciousness.

References

    1. Aimola Davies A. M., White R. C., Thew G., Aimola N. M., Davies M. (2010). Visual capture of action, experience of ownership, and the illusion of self-touch: a new rubber hand paradigm. Perception 39, 830–83810.1068/p6610
    1. Annett M. K., Bischof W. F. (2010). Investigating the application of virtual reality systems to psychology and cognitive neuroscience research. Presence Teleop. Virt. 19, 131–14110.1162/pres.19.2.131
    1. Arzy S., Thut G., Mohr C., Michel C. M., Blanke O. (2006). Neural basis of embodiment: distinct contributions of temporoparietal junction and extrastriate body area. J. Neurosci. 26, 8074–808110.1523/JNEUROSCI.0745-06.2006
    1. Aspell J. E., Lavanchy T., Lenggenhager B., Blanke O. (2010). Seeing the body modulates audiotactile integration. Eur. J. Neurosci. 31, 1868–187310.1111/j.1460-9568.2010.07210.x
    1. Aspell J. E., Lenggenhager B., Blanke O. (2009). Keeping in touch with one’s self: multisensory mechanisms of self-consciousness. PLoS ONE 4, e6488.10.1371/journal.pone.0006488
    1. Bertelson P., Vroomen J., De Gelder B. (2003). Visual recalibration of auditory speech identification: a McGurk aftereffect. Psychol. Sci. 14, 592–59710.1046/j.0956-7976.2003.psci_1470.x
    1. Blanke O., Arzy S. (2005). The out-of-body experience: disturbed self-processing at the temporo-parietal junction. Neuroscientist. 11, 16–2410.1177/1073858404270885
    1. Blanke O., Gassert R. (2009). Total control in virtual reality and robotics. Front. Neurosci. 3, 110–111
    1. Blanke O., Ionta S., Fornari E., Mohr C., Maeder P. (2010). Mental imagery for full and upper human bodies: common right hemisphere activations and distinct extrastriate activations. Brain Topogr. 23, 321–33210.1007/s10548-010-0138-x
    1. Blanke O., Landis T., Spinelli L., Seeck M. (2004). Out-of-body experience and autoscopy of neurological origin. Brain 127, 243–25810.1093/brain/awh040
    1. Blanke O., Metzinger T. (2009). Full-body illusions and minimal phenomenal selfhood. Trends Cogn. Sci. (Regul. Ed.) 13, 7–1310.1016/j.tics.2008.10.003
    1. Blanke O., Metzinger T., Lenggenhager B. (2008). Olaf Blanke et al’s response to Kaspar Meyer’s E-letter. Sci. E Lett.
    1. Blanke O., Mohr C. (2005). Out-of-body experience, heautoscopy, and autoscopic hallucination of neurological origin implications for neurocognitive mechanisms of corporeal awareness and self-consciousness. Brain Res. Brain Res. Rev. 50, 184–19910.1016/j.brainresrev.2005.05.008
    1. Blanke O., Mohr C., Michel C. M., Pascual-Leone A., Brugger P., Seeck M., Landis T., Thut G. (2005). Linking out-of-body experience and self processing to mental own-body imagery at the temporoparietal junction. J. Neurosci. 25, 550–55710.1523/JNEUROSCI.2612-04.2005
    1. Blanke O., Ortigue S., Landis T., Seeck M. (2002). Stimulating illusory own-body perceptions. Nature 419, 269–27010.1038/419269a
    1. Botvinick M., Cohen J. (1998). Rubber hands ‘feel’ touch that eyes see. Nature 391, 756.10.1038/35784
    1. Brandt C., Brechtelsbauer D., Bien C. G., Reiners K. (2005). Out-of-body experience as possible seizure symptom in a patient with a right parietal lesion. Nervenarzt 76, 1259, 1261–125210.1007/s00115-005-1904-y
    1. Bremmer F., Klam F., Duhamel J. R., Ben Hamed S., Graf W. (2002). Visual-vestibular interactive responses in the macaque ventral intraparietal area (VIP). Eur. J. Neurosci. 16, 1569–158610.1046/j.1460-9568.2002.02206.x
    1. Brugger P. (2002). Reflective mirrors: perspective-taking in autoscopic phenomena. Cogn. Neuropsychiatry 7, 179–19410.1080/13546800244000076
    1. Brugger P., Regrad M., Landis T. (1997). Illusory reduplication of own’s own body: phenomenology and classification of autoscopic phenomena. Cogn. Neuropsychiatry 19–3810.1080/135468097396397
    1. Carlin A. S., Hoffman H. G., Weghorst S. (1997). Virtual reality and tactile augmentation in the treatment of spider phobia: a case report. Behav. Res. Ther. 35, 153–15810.1016/S0005-7967(96)00085-X
    1. Corbetta M., Shulman G. L. (2002). Control of goal-directed and stimulus-driven attention in the brain. Nat. Rev. Neurosci. 3, 201–21510.1038/nrn755
    1. Corbetta M., Shulman G. L. (2011). Spatial neglect and attention networks. Annu. Rev. Neurosci. 34, 569–59910.1146/annurev-neuro-061010-113731
    1. Damasio A. (1999). The Feeling of What Happens. London: Random House
    1. De Ridder D., Van Laere K., Dupont P., Menovsky T., Van De Heyning P. (2007). Visualizing out-of-body experience in the brain. N. Engl. J. Med. 357, 1829–183310.1056/NEJMoa070010
    1. Dieguez S., Mercier M. R., Newby N., Blanke O. (2009). Feeling numbness for someone else’s finger. Curr. Biol. 19, R1108–R110910.1016/j.cub.2009.10.055
    1. Dueñas J., Chapuis C., Pfeiffer C., Martuzzi R., Ionta S., Blanke O., Gassert R. (2011). Neuroscience robotics to investigate multisensory integration and bodily awareness. Proc. IEEE Eng. Med. Biol. Conf. 8348–8352
    1. Duhamel J. R., Colby C. L., Goldberg M. E. (1998). Ventral intraparietal area of the macaque: congruent visual and somatic response properties. J. Neurophysiol. 79, 126–136
    1. Ehrsson H. H. (2007). The experimental induction of out-of-body experiences. Science 317, 1048.10.1126/science.1142175
    1. Ehrsson H. H., Spence C., Passingham R. E. (2004). That’s my hand! Activity in premotor cortex reflects feeling of ownership of a limb. Science 305, 875–87710.1126/science.1097011
    1. Ellis R. R., Flanagan J. R., Lederman S. J. (1999). The influence of visual illusions on grasp position. Exp. Brain Res. 125, 109–11410.1007/s002210050665
    1. Ernst M. O., Banks M. S. (2002). Humans integrate visual and haptic information in a statistically optimal fashion. Nature 415, 429–43310.1038/415429a
    1. Ernst M. O., Bulthoff H. H. (2004). Merging the senses into a robust percept. Trends Cogn. Sci. (Regul. Ed.) 8, 162–16910.1016/j.tics.2004.02.002
    1. Farrell M. J., Robertson I. H. (2000). The automatic updating of egocentric spatial relationships and its impairment due to right posterior cortical lesions. Neuropsychologia 38, 585–59510.1016/S0028-3932(99)00123-2
    1. Farrer C., Franck N., Georgieff N., Frith C. D., Decety J., Jeannerod M. (2003). Modulating the experience of agency: a positron emission tomography study. Neuroimage 18, 324–33310.1016/S1053-8119(02)00041-1
    1. Flanagan J. R., Wing A. M. (1997). The role of internal models in motion planning and control: evidence from grip force adjustments during movements of hand-held loads. J. Neurosci. 17, 1519–1528
    1. Frith C. (2005). The self in action: lessons from delusions of control. Conscious. Cogn. 14, 752–77010.1016/j.concog.2005.04.006
    1. Frith U., Frith C. D. (2003). Development and neurophysiology of mentalizing. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358, 459–47310.1098/rstb.2002.1218
    1. Gallagher S. (2005). How the Body Shapes the Mind. Oxford, NY: Clarendon Press
    1. Gassert R., Burdet E., Chinzei K. (2008a). MRI-compatible robotics. IEEE Eng. Med. Biol. Mag. 27, 12–1410.1109/EMB.2007.910265
    1. Gassert R., Burdet E., Chinzei K. (2008b). Opportunities and challenges in MR-compatible robotics: reviewing the history, mechatronic components, and future directions of this technology. EEE Eng. Med. Biol. Mag. 27, 15–2210.1109/EMB.2007.910265
    1. Gassert R., Yamamoto A., Chapuis D., Dovat L., Bleuler H., Burdet E. (2006). Actuation methods for applications in MR environments. Concepts Magn. Reson. Part B Magn. Reson. Eng. 29B, 191–20910.1002/cmr.b.20070
    1. Graziano M. S., Cooke D. F., Taylor C. S. (2000). Coding the location of the arm by sight. Science 290, 1782–178610.1126/science.290.5497.1782
    1. Grusser O. J., Pause M., Schreiter U. (1990). Localization and responses of neurones in the parieto-insular vestibular cortex of awake monkeys (Macaca fascicularis). J. Physiol. (Lond.) 430, 537–557
    1. Gusnard D. A., Akbudak E., Shulman G. L., Raichle M. E. (2001). Medial prefrontal cortex and self-referential mental activity: relation to a default mode of brain function. Proc. Natl. Acad. Sci. U.S.A. 98, 4259–426410.1073/pnas.071043098
    1. Gusnard D. A., Raichle M. E. (2001). Searching for a baseline: functional imaging and the resting human brain. Nat. Rev. Neurosci. 2, 685–69410.1038/35094500
    1. Haggard P., Taylor-Clarke M., Kennett S. (2003). Tactile perception, cortical representation and the bodily self. Curr. Biol. 13, R170–R17310.1016/S0960-9822(03)00115-5
    1. Halligan P. W., Fink G. R., Marshall J. C., Vallar G. (2003). Spatial cognition: evidence from visual neglect. Trends Cogn. Sci. (Regul. Ed.) 7, 125–13310.1016/S1364-6613(03)00032-9
    1. Hansel A., Lenggenhager B., von Kanel R., Curatolo M., Blanke O. (2011). Seeing and identifying with a virtual body decreases pain perception. Eur. J. Pain. 15, 874–87910.1016/j.ejpain.2011.03.013
    1. Heatherton T. F. (2011). Neuroscience of self and self-regulation. Annu. Rev. Psychol. 62, 363–39010.1146/annurev.psych.121208.131616
    1. Held R., Freedman S. J. (1963). Plasticity in human sensorimotor control. Science 142, 455–46210.1126/science.142.3591.455
    1. Heydrich L., Lopez C., Seeck M., Blanke O. (2011). Partial and full own-body illusions of epileptic origin in a child with right temporoparietal epilepsy. Epilepsy Behav. 20, 583–58610.1016/j.yebeh.2011.01.008
    1. Holden M. K. (2005). Virtual environments for motor rehabilitation: review. Cyberpsychol. Behav. 8, 187–211; discussion 212–189.10.1089/cpb.2005.8.187
    1. Ionta S., Ferretti A., Merla A., Tartaro A., Romani G. L. (2010). Step-by-step: the effects of physical practice on the neural correlates of locomotion imagery revealed by fMRI. Hum. Brain Mapp. 31, 694–70210.1002/hbm.20898
    1. Ionta S., Heydrich L., Lenggenhager B., Mouthon M., Fornari E., Chapuis D., Gassert R., Blanke O. (2011). Multisensory mechanisms in temporo-parietal cortex support self-location and first-person perspective. Neuron 70, 363–37410.1016/j.neuron.2011.03.009
    1. Iriki A., Tanaka M., Iwamura Y. (1996). Coding of modified body schema during tool use by macaque postcentral neurones. Neuroreport 7, 2325–233010.1097/00001756-199610020-00010
    1. Irwin H. J. (1985). Flight of Mind: A Psychological Study of the Out-of-Body Experience. Metuchen, NJ: Scarecrow Press
    1. Jacquin-Courtois S., Rode G., Pavani F., O’Shea J., Giard M. H., Boisson D., Rossetti Y. (2010). Effect of prism adaptation on left dichotic listening deficit in neglect patients: glasses to hear better? Brain 133(Pt 3), 895–90810.1093/brain/awp327
    1. Jang D. P., Ku J. H., Choi Y. H., Wiederhold B. K., Nam S. W., Kim I. Y., Kim S. I. (2002). The development of virtual reality therapy (VRT) system for the treatment of acrophobia and therapeutic case. IEEE Trans. Inf. Technol. Biomed. 6, 213–21710.1109/TITB.2002.802374
    1. Jeannerod M. (2006). Motor Cognition: What Actions Tell the Self. Oxford, NY: Oxford University Press
    1. Jeannerod M. (2007). Being oneself. J. Physiol. Paris 101, 161–16810.1016/j.jphysparis.2007.11.005
    1. Kannape O. A., Schwabe L., Tadi T., Blanke O. (2010). The limits of agency in walking humans. Neuropsychologia 48, 1628–163610.1016/j.neuropsychologia.2010.02.005
    1. Karnath H. O. (1994). Subjective body orientation in neglect and the interactive contribution of neck muscle proprioception and vestibular stimulation. Brain 117(Pt 5), 1001–101210.1093/brain/117.5.1001
    1. Karnath H. O., Ferber S., Himmelbach M. (2001). Spatial awareness is a function of the temporal not the posterior parietal lobe. Nature 411, 950–95310.1038/35082075
    1. Krebs H. I., Brashers-Krug T., Rauch S. L., Savage C. R., Hogan N., Rubin R. H., Fischman A. J., Alpert N. M. (1998). Robot-aided functional imaging: application to a motor learning study. Hum. Brain Mapp. 6, 59–7210.1002/(SICI)1097-0193(1998)6:1<59::AID-HBM5>;2-K
    1. Lenggenhager B., Mouthon M., Blanke O. (2009). Spatial aspects of bodily self-consciousness. Conscious. Cogn. 18, 110–11710.1016/j.concog.2008.11.003
    1. Lenggenhager B., Tadi T., Metzinger T., Blanke O. (2007). Video ergo sum: manipulating bodily self-consciousness. Science 317, 1096–109910.1126/science.1143439
    1. Lopez C., Halje P., Blanke O. (2008). Body ownership and embodiment: vestibular and multisensory mechanisms. Neurophysiol. Clin. 38, 149–16110.1016/j.neucli.2007.12.006
    1. Lopez C., Heydrich L., Seeck M., Blanke O. (2010). Abnormal self-location and vestibular vertigo in a patient with right frontal lobe epilepsy. Epilepsy Behav. 17, 289–29210.1016/j.yebeh.2009.12.016
    1. Maguire E. A., Burgess N., Donnett J. G., Frackowiak R. S., Frith C. D., O’Keefe J. (1998). Knowing where and getting there: a human navigation network. Science 280, 921–92410.1126/science.280.5365.921
    1. Maillard L., Vignal J. P., Anxionnat R., Taillandiervespignani L. (2004). Semiologic value of ictal autoscopy. Epilepsia 45, 391–39410.1111/j.0013-9580.2004.09704.x
    1. Maravita A., Iriki A. (2004). Tools for the body (schema). Trends Cogn. Sci. (Regul. Ed.) 8, 79–8610.1016/j.tics.2003.12.008
    1. Maravita A., McNeil J., Malhotra P., Greenwood R., Husain M., Driver J. (2003). Prism adaptation can improve contralesional tactile perception in neglect. Neurology 60, 1829–1831
    1. Metzinger T. (2008). Empirical perspectives from the self-model theory of subjectivity: a brief summary with examples. Prog. Brain Res. 168, 215–24510.1016/S0079-6123(07)68018-2
    1. Milner A. D., Goodale M. A. (2006). The Visual Brain in Action. New York: Oxford University Press
    1. Mizumoto M., Ishikawa M. (2005). Immunity to error through misidentification and the bodily illusion experiment. J. Conscious. Stud. 12, 3–19
    1. Narumoto J., Okada T., Sadato N., Fukui K., Yonekura Y. (2001). Attention to emotion modulates fMRI activity in human right superior temporal sulcus. Brain Res. Cogn. Brain Res. 12, 225–23110.1016/S0926-6410(01)00053-2
    1. Northoff G., Bermpohl F. (2004). Cortical midline structures and the self. Trends Cogn. Sci. (Regul. Ed.) 8, 102–10710.1016/j.tics.2004.01.004
    1. Palluel E., Aspell J. E., Blanke O. (2011). Leg muscle vibration modulates bodily self-consciousness: integration of proprioceptive, visual, and tactile signals. J. Neurophysiol. 105, 2239–224710.1152/jn.00744.2010
    1. Pavani F., Spence C., Driver J. (2000). Visual capture of touch: out-of-the-body experiences with rubber gloves. Psychol. Sci. 11, 353–35910.1111/1467-9280.00270
    1. Penfield W. (1955). The twenty-ninth Maudsley lecture: the role of the temporal cortex in certain psychical phenomena. J. Ment. Sci. 101, 451–465
    1. Petkova V. I., Ehrsson H. H. (2008). If I were you: perceptual illusion of body swapping. PLoS ONE 3, e3832.10.1371/journal.pone.0003832
    1. Redding G. M., Wallace B. (1997). Prism adaptation during target pointing from visible and nonvisible starting locations. J. Mot. Behav. 29, 119–13010.1080/00222899709600827
    1. Rengachary J., He B. J., Shulman G. L., Corbetta M. (2011). A behavioral analysis of spatial neglect and its recovery after stroke. Front. Hum. Neurosci. 5:29.10.3389/fnhum.2011.00029
    1. Riva G. (2007). Virtual reality and telepresence. Science 318, 1240–124210.1126/science.318.5854.1240a
    1. Rode G., Klos T., Courtois-Jacquin S., Rossetti Y., Pisella L. (2006). Neglect and prism adaptation: a new therapeutic tool for spatial cognition disorders. Restor. Neurol. Neurosci. 24, 347–356
    1. Ruby P., Decety J. (2001). Effect of subjective perspective taking during simulation of action: a PET investigation of agency. Nat. Neurosci. 4, 546–550
    1. Samson D., Apperly I. A., Kathirgamanathan U., Humphreys G. W. (2005). Seeing it my way: a case of a selective deficit in inhibiting self-perspective. Brain 128(Pt 5), 1102–111110.1093/brain/awh464
    1. Sanchez-Vives M. V., Slater M. (2005). From presence to consciousness through virtual reality. Nat. Rev. Neurosci. 6, 332–33910.1038/nrn1651
    1. Sarri M., Kalra L., Greenwood R., Driver J. (2006). Prism adaptation changes perceptual awareness for chimeric visual objects but not for chimeric faces in spatial neglect after right-hemisphere stroke. Neurocase 12, 127–13510.1080/13554790600598774
    1. Saxe R., Kanwisher N. (2003). People thinking about thinking people. The role of the temporo-parietal junction in “theory of mind.” Neuroimage 19, 1835–184210.1016/S1053-8119(03)00230-1
    1. Saxe R., Wexler A. (2005). Making sense of another mind: the role of the right temporo-parietal junction. Neuropsychologia 43, 1391–139910.1016/j.neuropsychologia.2005.02.013
    1. Sforza A., Bufalari I., Haggard P., Aglioti S. M. (2010). My face in yours: Visuo-tactile facial stimulation influences sense of identity. Soc. Neurosci. 5, 148–16210.1080/17470910903205503
    1. Shadmehr R., Holcomb H. H. (1997). Neural correlates of motor memory consolidation. Science 277, 821–82510.1126/science.277.5327.821
    1. Shulman G. L., Corbetta M., Buckner R. L., Raichle M. E., Fiez J. A., Miezin F. M., Petersen S. E. (1997). Top-down modulation of early sensory cortex. Cereb. Cortex 7, 193–20610.1093/cercor/7.3.193
    1. Shulman G. L., Pope D. L., Astafiev S. V., McAvoy M. P., Snyder A. Z., Corbetta M. (2010). Right hemisphere dominance during spatial selective attention and target detection occurs outside the dorsal frontoparietal network. J. Neurosci. 30, 3640–365110.1523/JNEUROSCI.4085-09.2010
    1. Slater M., Spanlang B., Sanchez-Vives M. V., Blanke O. (2010). First person experience of body transfer in virtual reality. PLoS ONE 5, e10564.10.1371/journal.pone.0010564
    1. Stratton G. M. (1899). The spatial harmony of touch and sight. Mind 8, 492–550
    1. Striemer C. L., Danckert J. A. (2010). Through a prism darkly: re-evaluating prisms and neglect. Trends Cogn. Sci. (Regul. Ed.) 14, 308–31610.1016/j.tics.2010.04.001
    1. Tarr M. J., Warren W. H. (2002). Virtual reality in behavioral neuroscience and beyond. Nat. Neurosci. 5(Suppl.), 1089–109210.1038/nn948
    1. Tsakiris M. (2010). My body in the brain: a neurocognitive model of body-ownership. Neuropsychologia 48, 703–71210.1016/j.neuropsychologia.2010.05.021
    1. Tsakiris M., Haggard P. (2005). The rubber hand illusion revisited: visuotactile integration and self-attribution. J. Exp. Psychol. Hum. Percept. Perform. 31, 80–9110.1037/0096-1523.31.1.80
    1. Tsakiris M., Hesse M. D., Boy C., Haggard P., Fink G. R. (2007). Neural signatures of body ownership: a sensory network for bodily self-consciousness. Cereb. Cortex 17, 2235–224410.1093/cercor/bhl131
    1. Vallar G., Lobel E., Galati G., Berthoz A., Pizzamiglio L., Le Bihan D. (1999). A fronto-parietal system for computing the egocentric spatial frame of reference in humans. Exp. Brain Res. 124, 281–28610.1007/s002210050624
    1. Vogeley K., Fink G. R. (2003). Neural correlates of the first-person-perspective. Trends Cogn. Sci. (Regul. Ed.) 7, 38–4210.1016/S1364-6613(03)00106-2
    1. Vogeley K., May M., Ritzl A., Falkai P., Zilles K., Fink G. R. (2004). Neural correlates of first-person perspective as one constituent of human self-consciousness. J. Cogn. Neurosci. 16, 817–82710.1162/089892904970799
    1. Winston J. S., Strange B. A., O’Doherty J., Dolan R. J. (2002). Automatic and intentional brain responses during evaluation of trustworthiness of faces. Nat. Neurosci. 5, 277–28310.1038/nn816
    1. Wolpert D. M., Flanagan J. R. (2010). Q&A: Robotics as a tool to understand the brain. BMC Biol. 8, 92.10.1186/1741-7007-8-92

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