Shared neurocognitive mechanisms of attenuating self-touch and illusory self-touch

Maria Pyasik, Adriana Salatino, Dalila Burin, Anna Berti, Raffaella Ricci, Lorenzo Pia, Maria Pyasik, Adriana Salatino, Dalila Burin, Anna Berti, Raffaella Ricci, Lorenzo Pia

Abstract

Despite the fact that any successful achievement of willed actions necessarily entails the sense of body ownership (the feeling of owning the moving body parts), it is still unclear how this happens. To address this issue at both behavioral and neural levels, we capitalized on sensory attenuation (SA) phenomenon (a self-generated stimulus is perceived as less intense than an identical externally generated stimulus). We compared the intensity of somatosensory stimuli produced by one's own intended movements and by movements of an embodied fake hand. Then, we investigated if in these two conditions SA was equally affected by interfering with the activity of the supplementary motor area (SMA; known to be related to motor intention and SA) using single-pulse transcranial magnetic stimulation. We showed that ownership of the fake hand triggered attenuation of somatosensory stimuli generated by its movements that were comparable to the attenuation of self-generated stimuli. Furthermore, disrupting the SMA eliminated the SA effect regardless of whether it was triggered by actual participant's movements or by illusory ownership. Our findings suggest that SA triggered by body ownership relies, at least in part, on the activation of the same brain structures as SA triggered by motor-related signals.

Keywords: body ownership; sense of agency; sensory attenuation; supplementary motor area; transcranial magnetic stimulation.

© The Author(s) 2019. Published by Oxford University Press.

Figures

Fig. 1
Fig. 1
Experimental setup: timeline and procedure of a single trial in SA (1A and 1B) and RHI + SA (1C and 1D) paradigms.
Fig. 2
Fig. 2
Results of RHI paradigm: 2A, mean proprioceptive drift in synchronous and asynchronous condition; 2B, mean ratings in real and control statements of the ownership questionnaire in synchronous and asynchronous condition. Error bars represent standard error of means; *, significant.
Fig. 3
Fig. 3
Results of SA and RHI + SA paradigm (mean ratings of the somatosensory electrical stimuli intensity): 3A, mean intensity ratings in self, other and self + TMS conditions; 3B, mean intensity ratings in embodiment condition compared to embodiment + TMS condition. Error bars represent standard error of means; *, significant.

References

    1. Arai N., Müller-Dahlhaus F., Murakami T., et al. (2011). State-dependent and timing-dependent bidirectional associative plasticity in the human SMA-M1 network. Journal of Neuroscience, 31(43), 15376–15383.
    1. Banakou D., Slater M. (2014). Body ownership causes illusory self-attribution of speaking and influences subsequent real speaking. Proceedings of the National Academy of Sciences of the United States of America, 111(49), 17678–17683.
    1. Bays P.M., Wolpert D.M., Flanagan J.R. (2005). Perception of the consequences of self-action is temporally tuned and event driven. Current Biology, 15(12), 1125–1128.
    1. Blakemore S.J., Frith C.D., Wolpert D.M. (1999). Spatio-temporal prediction modulates the perception of self-produced stimuli. Journal of Cognitive Neuroscience, 11(5), 551–559. 10.1162/089892999563607.
    1. Blakemore S.J., Wolpert D.M., Frith C.D. (1998). Central cancellation of self-produced tickle sensation. Nature Neuroscience, 1(7), 635–640.
    1. Blakemore S.J., Wolpert D.M., Frith C.D. (2002). Abnormalities in the awareness of action. Trends in Cognitive Sciences, 6(6), 237–242. 10.1016/S1364-6613(02)01907-1.
    1. Borhani K., Beck B., Haggard P. (2017). Choosing, doing, and controlling: implicit sense of agency over somatosensory events. Psychological Science, 28(7), 882–893.
    1. Botvinick M. (2004). Neuroscience. Probing the neural basis of body ownership. Science, 305(5685), 782–783. DOI: 10.1126/science.1101836
    1. Botvinick M., Cohen J. (1998). Rubber hands `feel’ touch that eyes see. Nature, 391(6669), 756. doi:10.1126/science.1101836305/5685/782
    1. Burin D., Battaglini A., Pia L., Falvo G., Palombella M., Salatino A. (2017a). Comparing intensities and modalities within the sensory attenuation paradigm: preliminary evidence. Journal of Advanced Research, 8(6), 649–653.
    1. Burin D., Garbarini F., Bruno V., et al. (2017b). Movements and body ownership: evidence from the rubber hand illusion after mechanical limb immobilization. Neuropsychologia, 107, 41–47.
    1. Burin D., Pyasik M., Ronga I., Cavallo M., Salatino A., Pia L. (2018). `As long as that is my hand, that willed action is mine’: timing of agency triggered by body ownership. Consciousness and Cognition, 58, 186–192.
    1. Burin D., Pyasik M., Salatino A., Pia L. (2017c). That's my hand! Therefore, that's my willed action: how body ownership acts upon conscious awareness of willed actions. Cognition, 166, 164–173.
    1. Carlsen A.N., Eagles J.S., MacKinnon C.D. (2015). Transcranial direct current stimulation over the supplementary motor area modulates the preparatory activation level in the human motor system. Behavioural Brain Research, 279, 68–75.
    1. Costantini M., Haggard P. (2007). The rubber hand illusion: sensitivity and reference frame for body ownership. Consciousness and Cognition, 16(2), 229–240.
    1. Cunnington R., Windischberger C., Deecke L., Moser E. (2002). The preparation and execution of self-initiated and externally-triggered movement: a study of event-related fMRI. NeuroImage, 15(2), 373–85.
    1. Desmurget M., Sirigu A. (2012). Conscious motor intention emerges in the inferior parietal lobule. Current Opinion in Neurobiology, 22(6), 1004–1011.
    1. Dewey J.A., Knoblich G. (2014). Do implicit and explicit measures of the sense of agency measure the same thing? PLoS One, 9(10).
    1. Ehrsson H.H. (2012). The concept of body ownership and its relation to multisensory integration In: Stein B.E., editor. The New Handbook of Multisensory Processes, MA: MIT Press (Cambridge), 775–792.
    1. Ehrsson H.H., Holmes N.P., Passingham R.E. (2005). Touching a rubber hand: feeling of body ownership is associated with activity in multisensory brain areas. Journal of Neuroscience, 25(45), 10564–10573.
    1. Fossataro C., Gindri P., Mezzanato T., Pia L., Garbarini F. (2016). Bodily ownership modulation in defensive responses: physiological evidence in brain-damaged patients with pathological embodiment of other's body parts. Scientific Reports, 6, 27737
    1. Gallagher S. (2000). Philosophical conceptions of the self: implications for cognitive science. Trends in Cognitive Sciences, 4(1), 14–21.
    1. Gallese V., Sinigaglia C. (2010). The bodily self as power for action. Neuropsychologia, 48(3), 746–755. doi: 10.1016/j.neuropsychologia.2009.09.038.
    1. Garbarini F., Pia L., Piedimonte A., Rabuffetti M., Gindri P., Berti A. (2013). Embodiment of an alien hand interferes with intact-hand movements. Current Biology, 23(2), R57–8.
    1. Garbarini F., Rabuffetti M., Piedimonte A., Solito G., Berti A. (2015). Bimanual coupling effects during arm immobilization and passive movements. Human Movement Science, 41, 114–126.
    1. Georgieff N., Jeannerod M. (1998). Beyond consciousness of external reality: a `who’ system for consciousness of action and self-consciousness. Consciousness and Cognition, 7(3), 465–477.
    1. Haggard P. (2017). Sense of agency in the human brain. Nature Reviews. Neuroscience, 18(4), 196–207.
    1. Haggard P., Chambon V. (2012). Sense of agency. Current Biology, 22(10), R390–2.
    1. Haggard P., Whitford B. (2004). Supplementary motor area provides an efferent signal for sensory suppression. Cognitive Brain Research, 19(1), 52–58.
    1. Heinen K., Ruff C.C., Bjoertomt O., et al. (2011). Concurrent TMS-fMRI reveals dynamic interhemispheric influences of the right parietal cortex during exogenously cued visuospatial attention. The European Journal of Neuroscience, 33(5), 991–1000. DOI: 10.1016/j.cub.2005.08.058
    1. Holmes N.P., Spence C. (2005). Multisensory integration: space, time and superadditivity. Current Biology, 15(18), R762–4. DOI: 10.1016/j.cub.2005.08.058
    1. Hughes G., Desantis A., Waszak F. (2012). Mechanisms of intentional binding and sensory attenuation: the role of temporal prediction, temporal control, identity prediction, and motor prediction. Psychological Bulletin, 139(1), 133–151. 10.1037/a0028566.
    1. Jeannerod M. (2003). The mechanism of self-recognition in humans. Behavioural Brain Research, 142(1–2), 1–15. [pii]
    1. Kalckert A., Ehrsson H.H. (2012). Moving a rubber hand that feels like your own: a dissociation of ownership and agency. Frontiers in Human Neuroscience, 6(40).
    1. Kalckert A., Ehrsson H.H. (2014). The moving rubber hand illusion revisited: comparing movements and visuotactile stimulation to induce illusory ownership. Consciousness and Cognition, 26, 117–132.
    1. Kilteni K., Ehrsson H.H. (2017). Body ownership determines the attenuation of self-generated tactile sensations. Proceedings of the National Academy of Sciences of the United States of America, 114(31), 8426–8431.
    1. Kokkinara E., Kilteni K., Blom K.J., Slater M. (2016). First person perspective of seated participants over a walking virtual body leads to illusory agency over the walking. Scientific Reports, 6, 28879
    1. Longo M.R., Schüür F., Kammers M.P.M., Tsakiris M., Haggard P. (2008). What is embodiment? A psychometric approach. Cognition, 107(3), 978–998.
    1. Moore J.W. (2016). What is the sense of agency and why does it matter? Frontiers in Psychology, 7, 1272
    1. Oldfield R.C. (1971). The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia, 9(1), 97–113. 10.1016/0028-3932(71)90067-4.
    1. Petkova V.I., Björnsdotter M., Gentile G., Jonsson T., Li T.Q., Ehrsson H.H. (2011). From part- to whole-body ownership in the multisensory brain. Current Biology, 21(13), 1118–1122.
    1. Pia L., Garbarini F., Fossataro C., Burin D., Berti A. (2016). Sensing the body, representing the body: evidence from a neurologically based delusion of body ownership. Cognitive Neuropsychology, 33(1–2), 112–119.
    1. Pyasik M., Burin D., Pia L. (2018). On the relation between body ownership and sense of agency: a link at the level of sensory-related signals. Acta Psychologica, 185, 219–228.
    1. Ricci R., Salatino A., Li X., et al. (2012). Imaging the neural mechanisms of TMS neglect-like bias in healthy volunteers with the interleaved TMS/fMRI technique: preliminary evidence. Frontiers in Human Neuroscience, 6(326), 1–13.
    1. Rossi S., Hallett M., Rossini P.M., Pascual-Leone A., Safety of TMS Consensus Group (2009). Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clinical Neurophysiology, 120(12), 2008–2039.
    1. Stenner M.P., Bauer M., Sidarus N., Heinze H.J., Haggard P., Dolan R.J. (2014). Subliminal action priming modulates the perceived intensity of sensory action consequences. Cognition, 130(2), 227–235.
    1. Timm J., SanMiguel I., Keil J., Schröger E., Schönwiesner M. (2014). Motor intention determines sensory attenuation of brain responses to self-initiated sounds. Journal of Cognitive Neuroscience, 26(7), 1481–9.
    1. Tsakiris M., Haggard P. (2005). The rubber hand illusion revisited: visuotactile integration and self-attribution. Journal of Experimental Psychology. Human Perception and Performance, 31(1), 80–91.
    1. Voss M., Ingram J.N., Haggard P., Wolpert D.M. (2006). Sensorimotor attenuation by central motor command signals in the absence of movement. Nature Neuroscience, 9(1), 26–27. doi: 10.1038/nn1592
    1. Voss M., Ingram J.N., Wolpert D.M., Haggard P. (2008). Mere expectation to move causes attenuation of sensory signals. PLoS One, 3(8), e2866
    1. Weller L., Schwarz K.A., Kunde W., Pfister R. (2017). Was it me?—Filling the interval between action and effects increases agency but not sensory attenuation. Biological Psychology, 123, 241–249.

Source: PubMed

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