One anecdotal observation to have emerged over the last decade or so has been that the RHI appears to work better (i.e., it is established more robustly) when the limbs (both artificial and real) are stroked (e.g., with a paintbrush) rather than when tapped (only the former likely activating the C-tactile afferents; [104]). The latest research by Crucianelli et al. [58] has now highlighted the importance of engaging the participant’s emotional system in inducing a strong illusion. In particular, these researchers demonstrated that slow touch (i.e., stroking), a kind of tactile stimulation that is known to selectively activate the C-tactile (CT) afferents (the affective touch system; see [113, 114]), gives rise to a stronger sense of ownership over the rubber hand than fast stroking (at a non-preferred speed for the C-tactile afferents). That said, other research has shown that even the presentation of painful tactile stimuli (pinpricks) can be used to induce the RHI [103].
9.3.2 Interim Summary
The existence of the RHI has been taken by many researchers to provide evidence of the mind’s ability to incorporate a variety of NBOs into its body representation. The results of the research that has been published to date clearly demonstrate that the magnitude of the RHI is reduced or decreased with asynchronous (as compared to synchronous) stroking, when an object (rather than a hand-like object) is stroked (at least when ownership is assessed by means of questionnaire responses) and when the fake body part is not aligned with, or else is too far removed from the participant’s own hand and arm (e.g., [54, 77, 99, 115]; see [20, 116], for reviews; though see also [84]).
9.4 Movement and the RHI
One problem with the use of joke shop and prosthetic limbs is that the seen (and hence the actual) limb typically has to remain static during the course of the trial/study. Obviously, feeling that one has control over the movement of a dynamic limb would be expected to increase the strength of any ‘feelings of ownership’ over a seen limb or NBO (see [117–119], for support). Perhaps for this very reason, the last few years have seen an increasing use of (manipulable) video images of a participant’s own hand (e.g., [120–123]) and/or the use of VR technologies in order to induce the RHI (or better said out-of-body effect—OBE—or the virtual body illusion—VBI; see [124, 125]). Others, meanwhile, have used a mirror to look at the incorporation of a moving limb (see [28, 66, 126, 127]). Such approaches typically allow the participant to move the seen (and actual) limb in a fairly natural manner, thus presumably increasing the likelihood that an observer will take ownership of the seen limb or body part (e.g., see [120, 124, 125]). Indeed, when Dummer et al. explicitly assessed the impact of movement on the strength of the RHI, they observed a more robust illusion under those conditions where the arms (both rubber and real) moved together than when they did not.
Furthermore, in a fascinating early study, Nielsen [118] demonstrated that once an illusion of ownership had been established over a seen arm, then some degree of inconsistency in terms of the dynamics of the seen and felt arm movements could be tolerated by participants. The participants in his study looked through a slit in order to see their limb. They were given the task of trying to draw a straight line on a piece of paper. After a number of trials, it was a stooge’s hand that they saw rather than their own. The participants did not realize even when, after a few trials of the stooge’s hand drawing a straight line, it started to draw lines that were curved instead. Interestingly, the participants in this study did not immediately disown the seen limb. Rather, they tended to account for the discrepancy between seen and felt movement by suggesting that they had been distracted or lost control of their own arm. In other words, once a person takes ownership over a seen limb or NBO, certain discrepancies (or incongruities) can be accepted (cf. [98]).
Now, the observant reader may have been wondering what exactly the difference is between inducing a RHI in the missing limb of an amputee and the mirror box technique popularized by Ramachandran and Rogers-Ramachandran ([128, 129]; see also [130, 131]; though see also [132]). In fact, more generally, it is legitimate to consider what exactly the relationship is between the RHI in normal participants and those early studies of recalibration involving participants pointing to objects while wearing prismatic glasses that deviated their gaze by some number of degrees to either the left or right [133–135]. Is there, perhaps, more similarity than many people give credit between these two paradigms? Perhaps. But one noticeable difference that has gone along with the growing interest in the RHI is the utilization of subjective report (at least from questionnaire measures) rather than relying on more objective performance measures, such as pointing or measures of proprioceptive drift.
9.5 Physiological and Neural Consequences of Inducing Out-of-Body Illusions
What is becoming increasingly clear is that perceptual illusions such as the RHI can have physiological consequences, consequences that would simply not have been thought possible even a decade ago. So, for example, Moseley et al. [136] were the first to report that inducing the RHI leads to a slight but significant drop in the body temperature of the affected limb (see also [76, 137]).13 Taking ownership of another limb (or NBO) increases histamine reactivity in a participant’s arm as well [139]. That is, the size of the skin wheal response elicited by the application of histamine correlates with the vividness of the RHI, as assessed by the questionnaire method. It would really seem, then, as though the disowned limb in the classic RHI is in some sense being rejected by the body [140].
Given the themes of the present volume, it is of interest to consider the neural substrates of illusions of body ownership/representation.14 Relevant in this regard, a number of researchers have studied the neural substrates underlying the elicitation and maintenance of the RHI (e.g., [54, 141]). Using functional magnetic resonance imaging (fMRI), Ehrsson and his colleagues were able to highlight an increase of activity in the bilateral ventral premotor cortex, the left intraparietal cortex, and the cerebellum bilaterally linked to the induction of the RHI. Interestingly, the level of activity in the premotor cortex (bilaterally) turned out to be correlated with the strength of the illusion (see also [106]). The suggestion was that the premotor cortex may be responsible for the feeling of ownership over the rubber hand (see also [79, 82]).
Meanwhile, Tsakiris et al. ([123]; see also [142]) observed activation in the temporo-parietal junction (TPJ) and in the right insula (in their positron-emission tomography, PET) study. The different neural substrates highlighted by these various studies may well reflect differences in the substrates involved in the initial elicitation of ownership of an NBO [54] and those involved in the maintenance of the sense of ownership, once established ([123, 141]; see also [19, 142]). Tsakiris and his colleagues have argued that while multisensory brain areas such as the premotor cortex, the superior parietal lobule, and the operculum may be critical for inducing the RHI, other areas, such as the right insula and perhaps also the frontal operculum, may be important in terms of evoking the sense of ownership that follows. Interestingly, research using transcranial magnetic stimulation (TMS) over the inferior parietal lobule has shown that temporarily interfering with activity in certain cortical areas (a kind of temporary lesion if you will) reduces the magnitude of the RHI [142, 143]. What is more, damage to the fibres that connect the ventral premotor cortex with other cortical sites has been reported to interfere with the RHI [144].
In their review, Makin et al. [116] put forward the suggestion that the illusory ownership of a fake hand might involve trimodal neurons in the premotor cortex and intraparietal sulcus. Extrastriate areas are also likely to be relevant to certain out-of-body illusions (see [16]).15 Finally, the results on an electroencephalography (EEG) study reported by Kanayama et al. [64, 86] suggested that changes in gamma band activity may also be correlated with the strength of the RHI. Specifically, interelectrode synchrony was significantly correlated with questionnaire measures of the strength of the RHI. In summary, the last decade has seen a rapid advance in our understanding of the neural substrates supporting incorporation in the human brain.
Conclusions: On the Incorporation of Prostheses into the Body Representation
As mentioned earlier in this chapter, the hope for many of those working in the field of prosthetics research is that the insights gained from studying the role of bottom-up multisensory integration and top-down factors (such as attention and the assumption of unity) over body representation in neurologically normal adult human participants may eventually serve to provide insights with regard to the best way in which to ensure that those who have lost a limb, and who are using (or may simply be thinking about using) some sort of prosthesis (or neuroprosthesis), can be helped. On the basis of the research that has been published to date, it would seem plausible to believe that the field of brain-computer interface (BCI) design might well benefit from the findings of RHI research on the malleability and limitations of incorporation in the body representation. There has undoubtedly been an increase of interest in trying to apply the insights of a number of those paradigms developed on the basis of studying neurologically normal participants to understanding the distortions experienced by a variety of patient groups (e.g., [140]; though see also [62]).
A major goal in applied neuroscience is to create artificial limb devices that feel and act just like real limbs. This work is associated with great technical challenges and raises fundamental questions related to how the brain distinguishes between parts of one’s body and objects in the external world. [60, p. 3443]
In conclusion, I would like to argue that great progress has been made over the last 15 years or so in terms of furthering our understanding of the malleability of the body representation in both health and disease. It turns out that the human brain exhibits a surprising ability to incorporate a variety of NBOs into the body representation. A number of factors (such as synchronous sensory input) have been shown to modulate the likelihood that incorporation will occur—others (such as the visual similarity in colour and texture between the participant’s body and the prosthesis), surprisingly, have been shown to be of little importance. While tentative steps have been made in terms of studying the incorporation of prosthetic limbs in amputees [60, 62], much further research is undoubtedly still needed. So, for example, it is noticeable how much of the research that has been conducted to date has been focused on upper limb amputees. It would seem at least plausible to suggest that visual factors may end up playing a more important role for upper limb prostheses, given that we see much more of our arms than we do of our lower limbs [146, 147]. Hence, in the future, it would be nice to see more research looking at the incorporation of lower limbs into the brain’s representation of the body (see [148, 149]). Furthermore, the question of whether individual differences in interoceptive sensitivity may predict the likelihood that a given prosthesis will be successfully incorporated into an amputee’s body representation also seems worthy of further consideration.
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