Common and distinct brain regions processing multisensory bodily signals for peripersonal space and body ownership
Introduction
The sense that our body belongs to us, body ownership (BO), is argued to be one of the cardinal features of subjective experience (Blanke and Metzinger, 2009, Gallagher, 2000). Recently, multisensory bodily illusion paradigms have been developed to study BO in the laboratory, describing the detailed behavioral mechanisms underlying the sensation of ownership for the hand (Botvinick and Cohen, 1998), the face (Sforza et al., 2010, Tsakiris, 2008) and the entire body (Ehrsson, 2007, Lenggenhager et al., 2007, Petkova and Ehrsson, 2008). These illusions have demonstrated that by manipulating multisensory cues it is possible to induce ownership over fake or virtual body parts or whole bodies. For example, to induce the rubber hand illusion, Botvinick and Cohen (1998) stroked with a brush both a realistic-looking rubber hand (in view of the participant) and the real hand of the participant (occluded from view) using stroking patterns in spatio-temporal synchrony. Participants felt stronger illusory ownership over the rubber hand in the synchronous (illusion) than the asynchronous (control) visuo-tactile stroking condition. Similar paradigms applied synchronous visuo-tactile stimuli between the trunk of a participant and a virtual body to achieve ownership over a body (full-body illusion, out-of-body illusion or body-swap illusion; Ehrsson, 2007; Lenggenhager et al., 2007; Petkova and Ehrsson, 2008), or between the participant's and another person's face to manipulate face ownership (enfacement illusion; Sforza et al., 2010; Tsakiris, 2008). These results, as well as converging evidence from subsequent variations of these experiments, have led to a growing consensus that ownership over hands, faces, and bodies crucially relies on the integration of multiple bodily signals in the brain (Blanke, 2012, Blanke et al., 2015, Ehrsson, 2012, Ehrsson et al., 2004; Makin et al., 2008; Serino et al., 2013; Tsakiris, 2010).
Research in non-human primates has shown that multisensory cues, in particular those involving the body, are processed and integrated by a specialized neural system mapping the space around the body, i.e. the peripersonal space (PPS) (Cléry et al., 2015, di Pellegrino and Làdavas, 2015, Graziano and Cooke, 2006, Ladavas and Serino, 2008, Rizzolatti et al., 1997). Specific populations of multisensory neurons, originally described in a fronto-parietal network of the macaque brain, integrate tactile information on the body with visual (or auditory) stimuli occurring close to the body, i.e. within the PPS (Graziano and Cooke, 2006; Rizzolatti et al., 1981a, Rizzolatti et al., 1981b; Duhamel et al., 1998; Fogassi et al., 1996; Graziano et al., 1994). Similar multisensory integration mechanisms have been also described in the human brain, in frontal and parietal areas, homologous to those macaque regions where PPS neurons have been identified (Bremmer et al., 2001, Serino et al., 2011, for reviews, see Cléry et al., 2015; di Pellegrino and Làdavas, 2015).
Importantly, recent accounts have proposed a direct link between the neural mechanism underlying BO and multisensory PPS processing (Blanke, 2012, Blanke et al., 2015, Ehrsson, 2012; T. R. Makin et al., 2008). Under normal circumstances, the extent of PPS is defined by the size of the multisensory receptive fields of PPS neurons. Synchronous visuo-tactile stimulation implemented to induce the different bodily illusions (altering BO) may lead to changes in the spatial characteristics of multisensory receptive fields of PPS neurons in such a way that the boundaries of PPS extend to include the virtual body part or whole body for which participants experience ownership (for a discussion, see Blanke et al., 2015). Behavioral support of this prediction has been provided in both the context of the rubber hand illusion (Guterstam et al., 2016, Pavani et al., 2000, Zopf et al., 2010), the enfacement illusion (Maister et al., 2015) and the full body illusion (Aspell et al., 2009; Noel et al., 2015). These studies showed that after synchronous visuo-tactile stimulation, visual or auditory stimuli presented close to the artificial body for which participants experience ownership were integrated with tactile information on their body, as normally only occurred for stimuli presented close to their physical body (i.e. within PPS; see Serino et al., 2015).
Neuroimaging experiments have recently started unraveling the brain mechanisms associated with encoding of sensory events within the hand, face and trunk PPS (e.g., Makin et al., 2007, Bremmer et al., 2001; Huang et al., 2012). Although activations have most often been reported in premotor and posterior parietal areas (e.g. Makin et al., 2007), they also encompassed a larger network of regions, including the parietal operculum (e.g. Tyll et al., 2013), the insula (e.g. Schaefer et al., 2012), the cingulate cortex (e.g. Holt et al., 2014), the lateral occipital cortex (e.g. Gentile et al., 2013), the putamen (e.g. Gentile et al., 2011) and the cerebellar cortex (e.g. Brozzoli et al., 2011).
Concerning BO, neuroimaging studies have recently engaged in assessing the neural correlates of ownership over a hand, a face, or a whole body (e.g. Apps et al., 2013; Ehrsson et al., 2004; Petkova et al., 2011). The vast majority of these studies highlighted again similar fronto-parietal regions, but also involved the parietal operculum (e.g. Gentile et al., 2013), the insula (e.g. Apps et al., 2013), the cingulate cortex (e.g. Tsakiris et al., 2007), the lateral occipital cortex (e.g. Guterstam et al., 2015), the putamen (e.g. Petkova et al., 2011), and the cerebellar cortex (e.g. Ehrsson et al., 2005). Importantly, the clusters reported in the fronto-parietal regions were neither always present (Limanowski et al., 2014), nor were they necessarily always the most prominent (Apps et al., 2013).
Despite numerous qualitative reviews discussing the neural mechanisms of PPS (Blanke et al., 2015, Cléry et al., 2015, di Pellegrino and Làdavas, 2015) or BO in humans (Blanke, 2012, Ehrsson, 2012, Serino et al., 2013, Tsakiris, 2010), no quantitative assessment of the available data from the literature has, to date, been conducted for PPS or BO. However, this will be important to reveal the key neural structures selectively involved in integrating multisensory stimuli in PPS and for BO. Furthermore, despite the above-mentioned behavioral evidence linking PPS and ownership and reviews suggesting a possible overlap of common neural mechanisms (Blanke, 2012, Blanke et al., 2015, Ehrsson, 2012; Makin et al., 2008), it is currently unknown whether or to what extent they exploit the same or distinct brain regions (but see Brozzoli et al., 2012; Gentile et al., 2013). For instance, the premotor cortex, that has been associated with PPS and BO (see e.g., Brozzoli et al., 2011; Ehrsson et al., 2005, respectively), covers a considerable portion of the frontal lobe and its anatomical delineation in humans is still a matter of debate (Mayka et al., 2006). Therefore, activity reported in ventral and dorsal premotor cortex regions by previous studies on BO or PPS could potentially refer to spatially distinct sub-regions within the premotor cortex. Thus, although the behavioral human and the electrophysiological monkey data suggest a close link between multisensory integrative brain mechanisms within PPS and BO, the evidence in humans remains sparse and has involved, in addition, many areas outside the classical fronto-parietal network.
In order to determine the key neural structures for PPS, for BO, and their potential common structures in humans, we carried out a systematic quantitative coordinate-based meta-analysis on human functional neuroimaging studies (Eickhoff et al., 2009, Eickhoff et al., 2012, Turkeltaub et al., 2002). We investigated which brain regions (i) consistently process unisensory and multisensory events occurring within PPS, (ii) are associated with the subjective sensation of BO, and (iii) whether PPS and BO share common neural substrates. Finally, we characterized these regions in terms of functions and co-activation networks against a database of general neuro-imaging experiments.
Section snippets
Selection of studies and inclusion criteria
We investigated common neural correlates of PPS and BO. To do so, we searched for the relevant neuroimaging experiments using the Pubmed (www.pubmed.com) and the Web of Knowledge (www.webofknowledge.com) internet portals using domain-general (“fMRI” or “PET”) and domain-specific (PPS: “peripersonal space” or “multisensory integration”; BO: “ownership” or “self-identification” or “rubber-hand illusion” or “full-body illusion” or “body-swap illusion”) search terms. Further references were
Individual ALE analysis of PPS
The ALE meta-analysis of the 18 PPS studies uncovered a total of 7 clusters, 4 located in the left hemisphere and 3 in the right hemisphere, in parietal (in the postcentral gyrus), temporo-parietal, and frontal (in the precentral gyrus) regions (Table 3, Fig. 2). There were two clusters in the left parietal cortex; the left dorsal parietal cluster included S1 (areas 2, 3b and 1) and the SPL (area 5, only on the left); the more ventral cluster included S1 (areas 2, 3b and 1) and the IPL (area
Discussion
Recent views in cognitive neuroscience propose that a key component of bodily self-consciousness, that is the feeling that the body is one's own, depends on the integration of multisensory bodily inputs in the space around the body, i.e., the PPS (Blanke, 2012, Blanke et al., 2015, Ehrsson, 2012; Makin et al., 2007; Serino et al., 2013; Tsakiris, 2010). In the present study we conducted the first quantitative meta-analysis based on human functional neuroimaging studies in order to assess which
Conclusion
To conclude, the present meta-analysis highlighted a series of bilateral brain regions, related to multisensory processing in PPS, anteriorly and posteriorly to the central sulcus. These were in the PMv, in parietal cortex area 2, IPS, the SPL, and the IPL. These areas were well connected to each other and are usually activated during sensory-motor tasks. On the other hand, areas involved in the sense of BO were also located in the premotor cortex and in the SPL. Those BO regions were in
Disclosures
The authors declare that the research reported in this manuscript has been conducted in absence of financial and commercial relationships that may be considered as a potential conflict of interest.
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These authors equally contributed to the paper.