The extrastriate body area is involved in illusory limb ownership
Introduction
To be oneself among others, one needs to identify with a particular body (Blanke and Metzinger, 2009, Gallagher, 2000, Jeannerod, 2007). Most accounts of body ownership have emphasized multimodal information integration in hierarchical cortical networks as a fundamental mechanism underlying a coherent self-representation (Apps and Tsakiris, 2013, Blanke, 2012, Hohwy, 2007, Hohwy, 2010, Petkova et al., 2011, Seth et al., 2011, Tsakiris, 2010). These theories are supported by recent neuroimaging experiments that have provided novel insights into how the brain self-attributes body parts based on such integration of visual, tactile, and proprioceptive information. In the Rubber Hand Illusion (RHI; Botvinick and Cohen, 1998), synchronous stroking of a dummy body part together with one's own corresponding body part typically misleads the brain to self-attribute the dummy limb (Botvinick and Cohen, 1998, Ehrsson et al., 2004, Tsakiris and Haggard, 2005) or even a whole body (Ehrsson, 2007, Lenggenhager et al., 2007). The experience of (illusory) body ownership has been linked to activity in frontal brain regions, predominantly the ventral premotor cortex (PMv; Ehrsson et al., 2004, Ehrsson et al., 2005, Petkova et al., 2011), but also posterior regions like the right temporo-parietal junction (rTPJ; Blanke et al., 2002, Blanke et al., 2005, Ionta et al., 2011, Tsakiris et al., 2008), posterior parietal cortex and intraparietal sulcus (PPC/IPS; Brozzoli et al., 2012, Ehrsson et al., 2004, Gentile et al., 2011, Petkova et al., 2011, Shimada et al., 2005; Tsakiris, 2010), and occipito-temporal regions like the body part-selective extrastriate body area (EBA; Arzy et al., 2006, Blanke and Mohr, 2005, Downing et al., 2001, Ionta et al., 2011). Primary somatosensory cortex (SI; Kanayama et al., 2007, Kanayama et al., 2009, Lenggenhager et al., 2011, Tsakiris et al., 2007) and the anterior insula (AI; Ehrsson et al., 2007) have also been associated with body ownership. Activity in these regions has been interpreted as reflecting the degree of illusory self-attribution or “incorporation” of the fake limb or body (Blanke, 2012, Ehrsson et al., 2004, Holmes and Spence, 2004, Petkova et al., 2011, Tsakiris, 2010).
Here, we used a fully automated setup to induce a novel, multi-site version of the RHI inside an fMRI scanner with high spatial resolution, addressing two potential caveats of the procedures typically used to evoke the illusion. First, we matched visual and tactile stimuli of both RHI and control condition in temporal synchrony, in contrast to the typically used asynchronous stroking control condition where observed touch on the dummy hand and felt touch on the own hand are presented serially. In our control condition, observed and felt touch were presented synchronously at spatially incongruent locations (palm and forearm). This synchronous stimulation countered potential problems associated with a serial, isolated presentation of observed and felt touch: For example, premotor cortex has been shown to be engaged in (serial) sensory predictions even in tasks using abstract, nonbiological stimuli (Schubotz and von Cramon, 2002, Schubotz and von Cramon, 2003, Schubotz and von Cramon, 2004), and the presentation of observed touch before felt touch at the same location could potentially be influenced by effects of anticipation of touch (see e.g. Carlsson et al., 2000, Keysers et al., 2010, Kuehn et al., 2012). Moreover, the resulting design enabled us to calculate a joint contrast comparing two RHI and control conditions, in which spatiotemporal differences between stimuli in the conditions were averaged out, and thus the resulting effects were attributable to the experienced illusion only. Second, by fully automating our experimental setup, we eliminated the human experimenter from the procedure. The induction of the RHI by touch from another person may interfere with self-related information processing, as many brain regions associated with body ownership (e.g., EBA, insula, PMv, and SI) also respond to observed human actions and touch, or mere vision of bodies of others (Bernhardt and Singer, 2012, Blanke, 2012, Ebisch et al., 2008, Keysers et al., 2010, Peelen and Downing, 2007, Zaki and Ochsner, 2012). Therefore, we aimed to isolate body ownership mechanisms from effects introduced by social interaction. The RHI has been induced automatically in one PET study (Tsakiris et al., 2007), but to our knowledge no automated MR-compatible RHI setup has been reported to date. We tested for BOLD signal differences between the RHI versus control condition within the ownership-related regions identified in previously published studies, expecting effects in regions whose response to the illusion is not influenced by receiving human touch. Moreover, we tested whether activity in those regions would reflect individual differences in the experienced intensity of the ownership illusion (Ehrsson et al., 2004, Petkova et al., 2011, Tsakiris et al., 2007).
Section snippets
Participants
20 healthy volunteers (22–36 years old; 13 females; 19 right-handed, one classified as “mixed left-handed”, measured with the Edinburgh Handedness Inventory, Oldfield, 1971; normal or corrected-to-normal vision) participated in the experiment; 16 of these participants took part in an additional scanning session for the functional EBA localizer. All participants gave written informed consent before the experiment and the study was approved by the local Ethical Committee of the Charité University
Behavioral results
Participants' mean reported ownership ratings for the RHI condition were significantly higher than those for the control condition (Fig. 1E; Wilcoxon's signed-rank test, n = 20, Z = 3.99, p = 0.00007). Moreover, the RHI condition was the only condition in which all participants affirmed experiencing ownership of the dummy arm (i.e., all ratings were positive; mean ownership rating = 2.30, SD = 0.66). On average, participants reported experiencing the illusion after 5.66 s (SD = 5.87 s), which means that the
Discussion
Illusory ownership of a dummy arm was successfully induced by our novel, fully automated RHI setup, as indicated by the participants' ratings. Moreover, we found significant brain activity differences between the RHI and control condition in several of the expected brain regions. Our results, in particular the correlation of illusion scores and left EBA activity, further demonstrate a correspondence of behavioral and neural measures of illusory ownership. As we excluded the possibility that
Acknowledgments
This research was supported by a grant from the German Federal Ministry of Education and Research (BMBF) to FB. We thank R. Auksztulewicz, and B. Spitzer for comments, and E. Kirilina for technical advice. The authors declare no competing financial interests.
References (97)
- et al.
The posterior parietal cortex remaps touch into external space
Curr. Biol.
(2010) - et al.
Full-body illusions and minimal phenomenal selfhood
Trends Cogn. Sci.
(2009) - et al.
Out-of-body experience heautoscopy and autoscopic hallucination of neurological origin Implications for neurocognitive mechanisms of corporeal awareness and self-consciousness
Brain Res. Rev.
(2005) - et al.
The Rubber Hand Illusion: sensitivity and reference frame for body ownership
Conscious. Cogn.
(2007) - et al.
Haptic perception and body representation in lateral and medial occipito-temporal cortices
Neuropsychologia
(2011) - et al.
Shared representations between self and other: a social cognitive neuroscience view
Trends Cogn. Sci.
(2003) - et al.
A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data
NeuroImage
(2005) - et al.
Psychophysiological and modulatory interactions in neuroimaging
NeuroImage
(1997) Philosophical conceptions of the self: implications for cognitive science
Trends Cogn. Sci.
(2000)- et al.
Multisensory mechanisms in temporo-parietal cortex support self-location and first-person perspective
Neuron
(2011)
Being oneself
J. Physiol. Paris
Dissociating body representations in healthy individuals: differential effects of a kinaesthetic illusion on perception and action
Neuropsychologia
The role of gamma band oscillations and synchrony on Rubber Hand Illusion and crossmodal integration
Brain Cogn.
Self awareness and the body image
Acta Psychol.
Spatial attention and crossmodal interactions between vision and touch
Neuropsychologia
The representation of space near the body through touch and vision
Neuropsychologia
A method for removal of global effects from fMRI time series
NeuroImage
On the other hand: dummy hands and peripersonal space
Behav. Brain Res.
The assessment and analysis of handedness: the Edinburgh inventory
Neuropsychologia
Topographic representation of the human body in the occipitotemporal cortex
Neuron
From part- to whole-body ownership in the multisensory brain
Curr. Biol.
Triple dissociation of faces bodies and objects in extrastriate cortex
Curr. Biol.
Embodied empathy for tactile events: interindividual differences and vicarious somatosensory responses during touch observation
NeuroImage
A blueprint for target motion: fMRI reveals perceived sequential complexity to modulate premotor cortex
NeuroImage
Functional–anatomical concepts of human premotor cortex: evidence from fMRI and PET studies
NeuroImage
Anatomical and functional parcellation of the human lateral premotor cortex
NeuroImage
The parietal role in the sense of self-ownership with temporal discrepancy between visual and proprioceptive feedbacks
NeuroImage
My body in the brain: a neurocognitive model of body-ownership
Neuropsychologia
The role of the right temporo-parietal junction in maintaining a coherent sense of one's body
Neuropsychologia
Correlations and anticorrelations in resting-state functional connectivity MRI: a quantitative comparison of preprocessing strategies
NeuroImage
The free-energy self: a predictive coding account of self-recognition
Neurosci. Biobehav. Rev
Plasticity in unimodal and multimodal brain areas reflects multisensory changes in self-face identification
Cereb. Cortex
Projecting sensations to external objects: evidence from skin conductance response
Proc. Biol. Sci.
Neural basis of embodiment: distinct contributions of temporoparietal junction and extrastriate body area
J. Neurosci.
Extrastriate body area in human occipital cortex responds to the performance of motor actions
Nat. Neurosci.
The neural basis of empathy
Ann. Rev. Neurosci.
Multisensory brain mechanisms of bodily self-consciousness
Nat. Rev. Neurosci.
Stimulating illusory own-body perceptions
Nature
Linking out-of-body experience and self processing to mental own-body imagery at the temporoparietal junction
J. Neurosci.
Rubber hands “feel” touch that eyes see
Nature
The Psychophysics Toolbox
Spat. Vis.
FMRI adaptation reveals a cortical mechanism for the coding of space near the hand
J. Neurosci.
That's near my hand! Parietal and premotor coding of hand-centered space contributes to localization and self-attribution of the hand
J. Neurosci.
Tickling expectations: neural processing in anticipation of a sensory stimulus
J. Cogn. Neurosci.
How do you feel-now? The anterior insula and human awareness
Nat. Rev. Neurosci.
The sentient self
Brain Struct. Funct.
Significance of the insula for the evolution of human awareness of feelings from the body
Ann. N. Y. Acad. Sci.
Neural systems supporting interoceptive awareness
Nat. Neurosci.
Cited by (69)
Knowing what you feel: Inferior frontal gyrus-based structural and functional neural patterns underpinning adaptive body awareness
2022, Journal of Affective DisordersObjects with motor valence affect the visual processing of human body parts: Evidence from behavioural and ERP studies
2022, CortexCitation Excerpt :In fact, the body (and its parts) is considered a special object for its relevance in many cognitive functions such as self-awareness, motor control and social communication. Critically, it has been argued that EBA is not a purely perceptual area, but it might also provide an interface between perceptual and motor processes (Astafiev et al., 2004; Bracci et al., 2012; David et al., 2007; Gallivan, McLean, Valyear, Pettypiece, & Culham, 2011; Kühn, Keizer, Rombouts, & Hommel., 2011; Limanowski, Lutti, & Blankenburg, 2014; Orgs et al., 2016; Simos et al., 2017; Tomasino, Weiss, & Fink, 2012). Remarkably, in our task, all targets were body parts yet, in the Unrelated condition, the N200 (and P300) amplitude significantly differed from the Related one.
Precision control for a flexible body representation
2022, Neuroscience and Biobehavioral Reviews