Functional and Neural Signatures of Body-ownership M Tsakiris (
[email protected]) Wellcome Department of Imaging Neuroscience & Institute of Cognitive Neuroscience, UCL
Keywords: agency, body-ownership, body-representation, multisensory integration, self
Abstract As agents, we act upon the world with our body, and we experience ourselves, and the world through the same body. This fact implies that the sense of self is crucially dependent on motor-efferent and sensoryafferent signals. The exact nature of sensory-motor interactions that generate a sense of self is still unknown. This research aims to empirically identify the basic neuro-cognitive principles governing an embodied sense of self. 1. Introduction The relationship between the body and the self is taken for granted in life (e.g. “this is my hand I see before me”). However, the cognitive processes by which the body is linked to the self are not fully understood (Gillihan & Farah, 2005). Cognitive neurosciences should explain why percepts of action and bodily states are so clearly and inexorably “mine”. Sensory events related to one’s own body (e.g. touch) are characterized by a sense of body-ownership, and motor events generated by one’s own body (e.g. actions) are characterized by a sense of agency (Gallagher, 2000). The precise conditions for bodyownership and agency, and their functional relationship remain unknown. Agency implies ownership (one knows one is controlling one’s own body), but ownership does not imply agency. That is, the presence of self-generated movements is necessary for agency, but not for body-ownership. I know my body is ‘mine’, and I correctly link somatosensory signals to myself even in the absence of any voluntary movement. Therefore, ownership is possible in the absence of agency. Previous experimental studies have confounded agency and body-ownership, by focusing exclusively on awareness of voluntary movement (Farrer et al., 2003; Sirigu et al., 1999; van den Bos & Jeannerod, 2003). Voluntary movements involve an inseparable combination of motor and sensory information. Thus, previous studies failed to isolate the additional component due to agency, over and above bodyownership. 2. A methodological comment
Recent neuroimaging studies have focused on the sense of controlling one’s own body (often called “sense of agency”), rather than on the sense of body-ownership. Inferior parietal cortex and insular cortex have been consistently activated in studies of agency. For example, Farrer et al. (2003) presented subjects with visual feedback of their own actions. The feedback was distorted to varying degrees by an angular bias. The less the subjects felt in control of the viewed action, the more pronounced was the activity in the right inferior parietal lobe. Conversely, the activity in the right posterior insula was correlated with the match between the performed and viewed movement, suggesting that the posterior insular cortex is related to self-attribution (see also Farrer & Frith, 2002). A third brain area may play a rather different role in body awareness. The dorsolateral prefrontal cortex (DLPFC) is involved in conflict monitoring between one’s own intentions and sensory feedback. Fink et al. (1999) showed that the mismatch between intention, proprioception, and visual feedback specifically activated the right dorsolateral prefrontal cortex (BA 9/46, and BA 44/45). Leube and colleagues (2003a) showed that when normal participants observed their hand becoming “anarchic” due to an experimental manipulation of the temporal delay of the visual feedback, a right fronto-parietal network, including BA44 and superior parietal cortex, was activated. The foregoing studies used action recognition tasks to investigate the sense of controlling one’s body (agency) rather than the sense of having or being one’s body (ownership). Agency implies ownership (one knows one is controlling one’s own body), but ownership does not imply agency. That is, the presence of self-generated movements is necessary for agency, but not for body-ownership. I know my body is ‘mine’, and I correctly link somatosensory signals to myself even in the absence of any voluntary movement. Moreover, ownership may be easier to analyse experimentally than agency. Voluntary action always involves an inseparable combination of efferent and afferent information. This makes it difficult to isolate experimentally the specific contributions of efferent and afferent signals to body representations (Tsakiris & Haggard, 2005b; Tsakiris et al., 2005; Tsakiris, Prabhu & Haggard, 2005). To that extent, it is yet unclear whether the brain areas underlying self-attribution of action reflect the experience of agency or the experience body-ownership. 3. Body-ownership 3.1. How does body-ownership arise? It is difficult to study experimentally the neural and functional signatures of body-ownership, simply because the body is “always there” (James, 1890). Classical experimental designs cannot therefore isolate the sense of body-ownership, by direct manipulations which make the body present in one
experimental condition but absent in another. One experimental paradigm that enables us to investigate the pure sense of body-ownership in the absence of movement and efferent information is the Rubber Hand Illusion. The Rubber Hand Illusion (RHI) allows for an external object to be treated as part of the body, or not, under experimental control. It is thus one of the few viable ways of investigating body ownership scientifically. Watching a rubber hand being stroked synchronously with one’s own unseen hand causes the rubber hand to be attributed to one’s own body, to “feel like it’s my hand” (Botvinick & Cohen, 1998; Tsakiris & Haggard, 2005a). How does the rubber hand come to be experienced as part of one’s own body? On one view, bodyownership arises by the interaction of bottom-up (i.e. multisensory signals) and top-down (i.e. body scheme representations) processes (Tsakiris & Haggard, 2005a). In a series of psychophysical studies, we used an induced change in the perceived location of the participant’s hand as a behavioural/phenomenal correlate of the RHI. Participants judged the felt position of their own unseen hand before and after visuo-tactile stimulation of their own hand and the rubber hand. Participants perceived their hand to be closer to the rubber hand after stimulation than before, suggesting an integration between the visually-perceived rubber hand and the tactile experience on the subject’s own hand. Importantly, this proprioceptive drift occurred only when the stimulation between the participant’s hand and the rubber hand was synchronized, and was absent or even reversed when visual and tactile stimulation was temporally asynchronous. Thus, one factor that modulates body-ownership in the RHI is multisensory correlation. However, not all multisensory stimuli are experienced as part of the body. Correlation of visual and tactile percepts is a necessary, but perhaps not sufficient, condition for the sense of ownership. In one experiment, participants were stimulated on their left hand, while viewing either a left or a right rubber hand (see Experiment 2 in Tsakiris & Haggard, 2005a). When subjects viewed a congruent rubber hand identity, they experienced the RHI: they perceived their hand to be significantly closer to the rubber hand after synchronous stimulation than after asynchronous stimulation. Conversely, when subjects viewed an incongruent rubber hand or a neutral object being stimulated, differences in the proprioceptive judgments between synchronous and asynchronous conditions were not significant. That is, synchronous stimulation between the participant’s left hand and a right rubber hand no longer induced the illusion. Ownership requires the viewed object to fit with a general pre-existing representation of the body scheme. Thus, body-ownership is also modulated by top-down influences based on prior visual, proprioceptive and functional representations of the body. These top-down
constrains on body-related multisensory percepts suggest that self-attribution, and hence, bodyownership is not a purely bottom-up process driven only by afferent signals. In addition, bodyownership cannot be simply a purely top-down process driven by abstract cognitive bodyrepresentations, because that would not explain how an attribution process of an external object is possible at all. Instead, body-ownership seems to arise as an interaction between bottom-up processes originating from the “body in the world” (i.e. multisensory perception) and top-down influences originating from the “body in the brain” (i.e. body representations). The synchronized visual and tactile stimulation causes the illusion, but the phenomenological effect within the illusion is a description of one’s own body, and not a description of the stimulation. 3.2. Neural correlates of body-ownership: We used PET to investigate the neural mechanisms of body-ownership in correlation with a quantitative measure of the RHI, namely the felt location of the participant’s own hand (Tsakiris et al., submitted). We investigated the neural basis of the sense of body-ownership by studying the causes and also the effects of the sense of body-ownership using the RHI. The experimental design was 2x2 factorial. Factor 1 was the mode of stimulation of the participant’s hand and the rubber hand (synchronous vs. asynchronous). Factor 2 was the identity of the rubber hand (congruent vs. incongruent with the identity of the participant’s own hand). Thus, participants were always stimulated on their unseen right hand, while they viewed a right or left rubber hand being stimulated either synchronously or asynchronously with respect to their own hand. Across all conditions participants judged the felt position of their own hand before and after stimulation. The proprioceptive drift was used as a behavioural measure for the induction of the RHI. The experimental design used the interaction between the bottom-up (i.e. synchronous vs. asynchronous visuo-tactile stimulation) and top-down (i.e. congruent vs. incongruent rubber hand identity) factors to investigate the causes of RHI, i.e., the sensory conditions that induce alterations in ownership. In an additional analysis, we correlated neural activity with the strength of the RHI as measured by the proprioceptive drift in the felt position of the subject’s hand. This analysis identified the neural correlates of the phenomenal effect of the RHI, namely the feeling that the rubber hand is part of one’s own body. The data were therefore analyzed in two ways: according to the 2x2 factorial design, and parametrically using the perceived hand position as a proxy for the phenomenal experience of the illusion. We predicted that the factorial interaction would show premotor and parietal areas (see Ehrsson et al., 2004) activated during the construction of body-ownership, and frontal areas (see Fink et al.,
1999) in the case when vision and touch provide conflicting information. Moreover, we hypothesized that the strength of the illusion as measured behaviourally would be positively correlated with brain areas linked with the sense of self, as those found in previous studies of self-attribution of one’s own action, in particular the insular cortex (Farrer et al., 2003). Our results suggest that the sense of body-ownership is related to activity in the right posterior insula and the right frontal operculum. These areas show a positive correlation between rCBF and the proprioceptive drift towards the rubber hand. Conversely, a negative correlation between rCBF and proprioceptive drift indicates a sense of dis-ownership, i.e. the feeling that an object is not linked to the body. A negative correlation was observed in the left parietal cortex, particularly the somatosensory cortices and posterior parietal lobe. We suggest that these areas form a network that plays a fundamental role in ‘tagging’ bodily events and generating special qualities which underlie bodily self-consciousness. 4. Conclusions Previous studies (Farrer & Frith, 2002; Farrer et al., 2003) used designs that did not clearly disentangle afferent and efferent components of the bodily awareness. Specifically, they may have misidentified neural signatures of body-ownership and signatures of motor agency, because they did not use designs that adequately disentangle afferent and efferent information. Our results suggest that areas previously linked to agency, such as the posterior insula, may in fact code body-ownership. Interestingly, in a recent lesion mapping study, Karnath, Baier & Naagele (2005) showed that the right posterior insula is commonly damaged in patients with anosognosia for hemiplegia/hemiparesis, but is significantly less involved in hemiplegic/hemiparetic patients without anosognosia (see also Berti et al., 2005; Cereda et al., 2002). The present findings support the hypothesis that the insular cortex is integral to bodily selfawareness. Berti and colleagues (2005) showed that anosognosia for hemiplegia is also associated with lesions in BA44 and BA6, suggesting that the denial of motor deficits arises, in part, by a failure to monitor the signals related to one’s own movement. One consequence of that failure would be to “ignore” the conflict between signals related to the intended and the actual states of the limbs, resulting in anosognosia. Thus, the patient might not register that their limb fails to move on command. Our work, however, suggests that the normal construction or rejection of bodily awareness can be based on purely sensory signals. No hypothesis of motor command monitoring, or of agency, is required to explain the activation in these areas, and their role in bodily self-consciousness. We suggest that a basic form of bodily self-consciousness is generated in the brain by sensory stimulation and assimilation to a pre-
existing body scheme. Agency would represent a special but important addition to this essentially sensory circuit for self-consciousness.
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CV: Manos Tsakiris Date of Birth: 21.12.1977 Email:
[email protected]
Nationality: Greek Address: 17 Queen Square, WC1N 3AR, UK
Current Position: ESRC Post-doctoral fellow, Institute of Neurology, UCL Academic Qualifications 2001-2005 PhD University College London (Psychology) 2000-2001 MSc in Cognitive Neuropsychology University College London 1999-2000 MSc in Philosophy of Mental Disorder, King’s College 1995-1999 BSc in Psychology Panteion Universty of Athens, Greece
Publications Tsakiris M & Haggard P (2003). Awareness of somatic events associated with a voluntary action. Experimental Brain Research, 149, 439-446. Tsakiris M & Haggard P (2005a). The rubber hand illusion revisited: visuotactile integration and self-attribution. Journal of Experimental Psychology: Human Perception and Performance, 31(1):80-91. Tsakiris M & Haggard P (2005b). Experimenting with the acting self. Cognitive Neuropsychology, 22(3/4), 387-407. Tsakiris M, Haggard P, Franck N, Mainy N & Sirigu A (2005). A specific role for efferent information in self-recognition. Cognition, 96(3), 215-231. Tsakiris M, Prabhu G & Haggard P (2006). Having a body versus moving your body: how agency structures body-ownership. Consciousness & Cognition, in press. De Vignemont F, Tsakiris, M & Haggard P (2006), ‘Body Mereology’. In G. Knoblich, I. Thornton, M. Grosjean, & M. Shiffrar (Eds.), Human Body Perception from the Inside Out (Advances in Visual Cognition). New York, NY: Oxford University Press. Tsakiris M & Haggard P. Neural, functional and phenomenological signatures of intentional actions. In F.Grammont, D.Legrand & P. Livet (Eds.), Naturalizing Intention in Action. An interdisciplinary approach, The MIT Press and ENS Editions. Forthcoming Tsakiris M & Frith C. Self: neurocognitive approaches. Entry to appear in Τ Bayne, Α Cleeremans & P Wilken (Eds.). Τhe Oxford Companion to Consciousness. Oxford: Oxford University Press.
Awards and Grants 2006 Royal Society, Outgoing Short Visit 2005-2006 ESRC Postdoctoral Fellowship (PTA-026-27-0889) 2005 Conference Travel Grant, Guarantors of “Brain, a journal of neurology” 2005 Novartis Foundation Bursary Scheme 2004 DAAD–German Academic Exchange Service Boehringer Ingelheim Fonds, Travel Allowance 2003 Conference Travel Grant, Guarantors of “Brain, a journal of neurology” Graduate School, UCL, Conference Travel Grant, Experimental Psychology Society, UK, Grindley Grant 2002 Experimental Psychology Society, UK, Research Travel Grant
