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Neuroscience and Biobehavioral Reviews 36 (2012) 34–46
Contents lists available at ScienceDirect
Neuroscience and Biobehavioral Reviews
journal homepage: www.elsevier.com/locate/neubiorev
Review
Bodily illusions in health and disease: Physiological and clinical
perspectives and the concept of a cortical ‘body matrix’
G. Lorimer Moseley a,b,∗ , Alberto Gallace c , Charles Spence d
a
The Sansom Institute for Health Research, University of South Australia, Adelaide, Australia
Neuroscience Research Australia, Sydney, Australia
University of Milano-Biccoca, Milano, Italy
d
University of Oxford, Oxford, UK
b
c
a r t i c l e
i n f o
Article history:
Received 8 November 2010
Received in revised form 22 March 2011
Accepted 25 March 2011
Keywords:
Rubber hand illusion
Body ownership
Cortical representation
Somatotopic representation
Spatial representation
Tactile function
Complex regional pain syndrome
Chronic pain
Spatial neglect
Phantom limb pain
Mirror therapy
a b s t r a c t
Illusions that induce a feeling of ownership over an artificial body or body-part have been used to explore
the complex relationships that exist between the brain’s representation of the body and the integrity of
the body itself. Here we discuss recent findings in both healthy volunteers and clinical populations that
highlight the robust relationship that exists between a person’s sense of ownership over a body part, cortical processing of tactile input from that body part, and its physiological regulation. We propose that a
network of multisensory and homeostatic brain areas may be responsible for maintaining a ‘body-matrix’.
That is, a dynamic neural representation that not only extends beyond the body surface to integrate both
somatotopic and peripersonal sensory data, but also integrates body-centred spatial sensory data. The
existence of such a ‘body-matrix’ allows our brain to adapt to even profound anatomical and configurational changes to our body. It also plays an important role in maintaining homeostatic control over
the body. Its alteration can be seen to have both deleterious and beneficial effects in various clinical
populations.
© 2011 Elsevier Ltd. All rights reserved.
Contents
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Behavioural and perceptual aspects of the RHI . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Representations of peripersonal space and body ownership . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Neural mechanisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Body-centred spatial representations and bodily illusions – lessons from the clinic . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Spatial representation and autonomic control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
The ‘body matrix’ . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
What happens to the disowned/replaced part? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Other distortions of bodily perception induced by misleading visual cues . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Other bodily illusions in patients – can it all be done with mirrors? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Appendix A.
Supplementary data . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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1. Introduction
∗ Corresponding author at: University of South Australia GPO Box 2471 Adelaide
5001 Australia. Tel.: +61 8 83021416; fax: +61 8 83022853.
E-mail address: [email protected] (G.L. Moseley).
0149-7634/$ – see front matter © 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.neubiorev.2011.03.013
It is over a decade now since Botvinick and Cohen (1998)
reignited contemporary research interest in the class of out-ofbody illusions of which the rubber hand illusion (RHI) constitutes
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G.L. Moseley et al. / Neuroscience and Biobehavioral Reviews 36 (2012) 34–46
Fig. 1. Typical experimental setup used to induce the RHI. The participant’s hand is
placed out of view and the artificial, rubber hand is placed in view. The experimenter
strokes both hands synchronously. In less than a minute, most participants report
that they can actually feel the touch on the rubber hand, and begin to feel a sense of
ownership over the rubber hand. Asynchronous stroking rarely elicits the illusion.
but one example. These phenomena are not new (Binet, 1888; Janet,
1898) – Tastevin (1937) published what is commonly acknowledged to be the first study of an out-of-body sensation elicited by
an artificial finger. However, the last few years has seen a seemingly exponential growth of research on the phenomenon (see
Makin et al., 2008, for a recent review). This burgeoning of research
interest can be attributed, at least in part, to scientists’ increased
appreciation of disorders of body representation in a number of
psychopathologies. In addition, the rapid development of immersive virtual reality environments (e.g., Slater et al., 2009), where the
possibility of ‘projecting’ (and controlling) the body into external
(or virtual) space is becoming a reality (Gallace et al., in press), have
given a far broader context to our understanding of body ownership
and awareness than ever before.
The RHI is both subjectively powerful and, at the same time,
simple to induce in the majority of participants – it can be elicited
in a matter of seconds using nothing more that a joke-shop rubber
hand, or even a pair of stuffed washing-up gloves (Ehrsson et al.,
2004; Pavani et al., 2000). In the basic RHI (see Fig. 1), a participant is seated at a table with their right hand resting, out-of-sight
behind an occluding screen, on the table. The rubber hand is placed
directly in front of the participant in their direct view and in an
anatomically plausible posture. The participant adopts the same
hand posture as that of the rubber hand. The experimenter, sitting
on the other side of the table, then starts to stroke both the rubber hand and the participant’s own occluded hand in synchrony.
Remarkably, after a few seconds of stroking (approximately 11 s
on average; see Ehrsson et al. (2004) and Kammers et al. (2009),
although the timing of onset has been shown to be variable both
within and between individuals (Zopf et al., 2010)), the majority of
participants start to agree with statements such as ‘It seemed as if
I were feeling the touch of the paintbrush in the location where I
saw the rubber hand touched’, ‘I felt as if the rubber hand were my
hand’, and ‘I found myself looking at the dummy hand thinking it
was actually my own’ (Botvinick and Cohen, 1998).
2. Behavioural and perceptual aspects of the RHI
The strength of the RHI depends on the crossmodal congruence between what a person feels via the somatosensory pathways
and what they see (Tsakiris, 2010). Although some researchers
have emphasised the role of visual input in the RHI, describing
35
it as an example of vision ‘overuling’ touch and proprioception
(Honma et al., 2009), or ‘visual capture’ of touch and proprioception (Capelari et al., 2009), it is important to note that visual input
is not critical either to inducing (Ehrsson et al., 2005a; Giummarra
et al., 2010a,b; Petkova and Ehrsson, 2009), or to maintaining, the
illusion (Moseley et al., 2008b). Undoubtedly, however, the illusion
is dependent on multisensory input: It works best when proprioception and touch are involved, when the rubber hand is placed in
an anatomically plausible posture (Lloyd, 2007; Pavani et al., 2000;
Tsakiris and Haggard, 2005; Zopf et al., 2010); when the same stimulation (visual and tactile) is provided to both the real and rubber
hand (although seeing a laser pointer cast on the real or rubber
hand can also induce an illusion of touch; see Durgin et al., 2007).
That said, the illusion of ownership can still be induced to some
extent when various of these criteria are not met. So, for example, when the rubber hand is stroked with a piece of soft cotton
and the real hand with rough sponge, the difference in texture is
detected, but the RHI is still induced (Schutz-Bosbach et al., 2009).
The precise physical characteristics of the two limbs need not be
identical either. In fact, there are even anecdotal reports of volunteers reporting the illusion of ownership over a block of wood, or,
remarkably, over a table-top, using the same experimental method
(Armel and Ramachandran, 2003). Other researchers though have
published contrasting results: The illusion of ownership over a stick
(Tsakiris and Haggard, 2005) or a box (Hohwy and Paton, 2010)
cannot readily be induced in healthy participants, but it appears
relatively easy to transfer the illusion once it is induced, from the
rubber hand to another object placed in the same spatial location
as the artificial hand (Hohwy and Paton, 2010). What is more, once
the illusion has been induced, participants tend to provide irrational and supernatural explanations for sensory phenomena that
do not ‘fit’. For example, if the seen stimulus approaches the rubber hand without touching it – and given that the tactile stimulus
to the actual hand still occurs in synchrony with the expected touch
of the rubber hand – participants’ reports include statements such
as: ‘there is an invisible extension of the (stimulating) finger to my
arm’ and ‘there is a magnetic forcefield between the finger and the
arm’ (Hohwy and Paton, 2010; Nielsen, 1963). Although most participants do not cognitively endorse the reality of the rubber hand,
for example stating “. . .it feels like the rubber hand’s my hand. . .so I
wouldn’t have another hand. Logically, I only have one (right) hand”
(Lewis and Lloyd, 2010), the illusion may be sufficient to disrupt
what the rubber hand looks like: “(the rubber hand) looks like my
own hand!” (Lewis and Lloyd, 2010).
Once the RHI has been established, stimuli presented on, or near
to, the artificial hand, elicit behavioural and neural responses that
would normally occur if they had been delivered on, or nearby,
the participant’s own hand (e.g., Armel and Ramachandran, 2003;
Ehrsson et al., 2007). For example, we normally respond more
quickly to visual stimuli presented on our own hand than we do
to visual stimuli presented in the peripersonal space near the hand
(Whiteley et al., 2008; see also Whiteley et al., 2004). Short and
Ward (2009) recently used a ‘virtual hand’ paradigm, in which participants viewed 3D images of two hands, through a head-mounted
visual display. Once a sense of ownership over the virtual hands
had been established, the temporal advantage of responding to
visual stimuli on the hand over visual stimuli occurring near the
hand was replicated (see Hartcher-O’Brien et al., 2010). Thus, the
neural mechanisms that subserve the facilitation of processing of
body-related stimuli endorse the virtual hand.
Just as stimuli that evoke the desire to interact using the rubber hand increase the strength of the illusion (Giummara et al.,
2010), stimuli that threaten the artificial hand can engage protective responses. Moving a knife or needle toward the artificial hand
often induces withdrawal of the actual hand (which, in turn, breaks
the illusion). Nevertheless, the perceived threat to the hand is suffi-
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G.L. Moseley et al. / Neuroscience and Biobehavioral Reviews 36 (2012) 34–46
cient to result in the activation of brain regions consistent with the
preservation of the body (Ehrsson et al., 2007) (see below). That
stimuli approaching the rubber hand evoke protective responses
demonstrates that the spatial attributes of the stimuli, as well as
their somatotopic attributes, contribute to the sense of ownership
over the hand (although, notably, ‘image’ attributes do not (Holmes
et al., 2006). In fact, Makin et al.’s (2008) recent account of the RHI,
emphasiszes the dependence of the RHI on multisensory representations of space that appear to be hand-centred (see also Lloyd,
2007). That is, it seems as though we not only own our body parts,
but we also in some sense ‘own’ the space around them as well.
These observations in-and-of-themselves raise the interesting
question as to whether the body can survive without the mind –
certainly the mind-body link is more complex and bidirectional
than previously thought, as demonstrated by recent applications of
the RHI (see below). As for responses that serve to preserve a rubber hand embodied via the RHI, one might suggest that whether or
not such protective responses are dependent on the illusion itself is
open to question. Relevant in this regard are the results of a study by
Avenanti et al. (2005) in which they reported a modulation of cortically evoked responses of the hand muscles when the participants
watched another person’s hand being injured. In that experiment,
there was no attempt to induce a sense of ownership over the seen
hand. The authors attributed the effect to a kind of ‘motor empathy’,
rather than to a sense of ownership over the other’s hand. Similar
mechanisms in the sensory domain may underpin synaesthesia for
pain, in which seeing someone else being injured evokes pain in
one’s own body (see Fitzgibbon et al., 2010, for a review).
The RHI can also induce complex perceptual states that cannot be evoked simply by watching another person. For example,
we have recently discovered that feelings that are characteristic of
successful acupuncture, collectively called ‘Deqi’, are experienced
when acupuncture is given to the rubber hand that is being viewed
by the participant, and not to the real hand. This works just as
long as the illusion is established beforehand (Bulley et al., 2011).
Moreover, in healthy volunteers conditioned to the feeling of transcutaneous electrical nerve stimulation (TENS), subsequent TENS to
the rubber hand can evoke tingling sensations and increased pressure pain thresholds on the actual arm (Bulley et al., 2011). These
remarkable observations concur with the work of Hohwy and Paton
(2010) in that the perceptual responses were logically impossible
– that is, participants knew the acupuncture and TENS were only
applied to an artificial hand – yet they nonetheless still felt the
effects.
Perhaps counterintuitively, the RHI appears to be more vivid
when there is no actual hand at all. Giummarra et al. (2010a,b)
recently induced a variant of the RHI in amputees, by using a mirror and a rubber hand placed on the opposite side of the mirror
to the amputated limb. They compared the feelings and proprioceptive drift induced by stroking the rubber hand or the intact
limb. Amputees were more likely than healthy controls to report
illusory sensations, regardless of whether the rubber hand or the
intact hand was stimulated. This finding adds to previous reports of
synchiria in amputees (Sathian, 2000). Synchiria is the perception of
touch on the phantom at seeing touch on the reflected intact limb.
Both amputees and controls were more likely to report illusory sensations when the rubber hand was stroked than when the intact
hand was stroked. Moreover, amputees who had sustained an avulsion of the brachial plexus prior to amputation, an injury that leaves
the arm paralysed and insensate, were less likely to report illusory
sensations but no less likely to endorse embodiment of the rubber
hand. This finding strongly suggests that the illusory sensations
that can be evoked by the RHI depend on one’s sensory experience.
Consistent with this idea is the finding of dysynchiria (Acerra and
Moseley, 2005). Dysynchiria is the perception of pain, or tingling,
when on one hand at seeing touch on the reflected intact hand.
Importantly, pain is evoked when the stimulated area corresponds
to an area on the affected limb that would be sensitive to touch (socalled ‘allodynia’) and tingling or paraesthesia is evoked when the
stimulated area corresponds to an area on the affected limb that is
paraesthetic. The occurrence of dysynchiria is reasonably common
in people with CRPS (see below), but is uncommon in non-CRPS
neuropathic pain states (Kramer et al., 2008). Other accounts of pain
being evoked, or indeed relieved, by cross-modal stimuli abound,
for example the man who experienced pain when his wife was
injured (Bradshaw and Mattingley, 2001) or the amputee who gains
pain relief by stimulating the prosthesis at a location corresponding
to his pain (Moseley, 2007b; Weeks and Tsao, 2010).
3. Representations of peripersonal space and body
ownership
One might speculate that in addition to an anatomically accurate representation of our body (as supported, for example, by
the somatosensory homunculus; Narici et al., 1991; Penfield and
Boldrey, 1937) our brains also support other, coarser, neural representations that are responsible for mapping not only the body
surface but the space around it as well. In the extant literature on
spatial information processing, the term ‘peripersonal space’ has
been used to define the visual space around the body (Rizzolatti
et al., 1997). It is widely agreed that one of the main functions of
such a representation is to provide information about the position of objects in the surrounding environment with respect to
the body (Holmes and Spence, 2004; Ladavas et al., 1998a). For
some researchers, this occurs with the ultimate aim of planning
and executing movements whose purpose is to protect the body
from physical threat (Cooke and Graziano, 2004). Neurophysiological studies suggest that this representation of the space around
the body is body part-centred (i.e., it is supported by neurons having their receptive fields centred on the head, face, neck, torso, or
shoulder; Holmes and Spence, 2004; Ladavas et al., 1998b).
Recently, Makin et al. (2008) suggested that multisensory representations of ‘peri-hand’ space are critical for attributing an
artificial hand to the self, which is in line with the finding that the
spatial constraints of the RHI are about 30 cm from the participant’s
real hand (Lloyd, 2007). Makin et al. (2008) put forward a putative
neurocognitive model to explain the RHI in terms of multisensory
integration in peri-hand space. They suggested that once the space
around a rubber hand is represented as peri-hand space, the seen
stroke of the brush on the dummy hand is then represented in reference frames centred on, and defined with respect to, the rubber
hand (a process they argue to involve the activation of the intraparietal sulcus). Similarly, the felt touch of the brush stroking the
real hand will also activate the same crossmodal mechanisms. This
conjunction of visual and tactile sensory events in hand-centred
coordinates signals the occurrence of a single bimodal stimulus. As
a consequence, the sensation of touch is referred from the hidden
real hand to the seen rubber hand (possibly involving the activation
in the premotor cortex). While this elegant model appears able to
explain the RHI, it cannot explain a number of other more recently
reported phenomena related to the representation of the body. In
particular, how can this representation of the peri-hand space be
involved in the temperature drop observed by Moseley et al. (2009)
after the induction of the RHI, or with the effects of crossing the
hands in CRPS patients (Moseley et al., 2009)? It is difficult to reconcile the fact that a representation centred on a certain body part
(and which is not affected by the position of that body part in space)
can be involved in a number of effects that depend on where the
body part is actually placed in external space. Certainly, one possibility is that all of these various phenomena are simply not related,
and that different mechanisms are needed in order to explain them
all. However, that said, a synthesis may still be possible.
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37
This ever-increasing body of literature provides compelling evidence of the behavioural embodiment of artificial body parts and
objects, and the pervasive nature of perceptual experiences that are
evoked when multisensory inputs are manipulated experimentally.
Clearly, somatotopic representations of the inputs are fundamental,
as are spatial representations centred on the body part concerned
– peripersonal space. One would expect, then, that uncovering the
neurological mechanisms involved in bodily illusions such as the
RHI might cast light on the relations between our sense of body
ownership and other bodily functions, in health and disease.
4. Neural mechanisms
Neuroimaging studies have started to uncover the neural underpinnings of the RHI. In the first study to be published on this topic,
Ehrsson et al. (2004) highlighted the importance of the parietal
cortex and the premotor cortex in the initiation of the illusion
in a functional magnetic resonance imaging (fMRI) study. Subsequent research by Tsakiris et al. (2007) using positron emission
tomography (PET) highlighted the importance of the right insula to
the maintenance of the illusion. Tsakiris and his colleagues argued
that cortical multisensory areas – the premotor cortex, the superior parietal lobule, and the operculum – seem to be critical to
the induction of the RHI, while the right insula, and perhaps the
frontal operculum, appear to be important in evoking the sense
of ownership that follows. It is notable then that damage to the
right posterior insula is implicated in post-stroke patients with
anosognosia – a disorder in which individuals deny the existence
of a disability such as paralysis or sensory impairment (Karnath
et al., 2005). Interestingly, although anosognosia has been often
considered a disorder in a patient’s awareness of his/her deficits
rather than a proper body-ownership disorder, it has been recently
suggested that pathological beliefs regarding the functioning of
one’s own limbs and disturbed feelings of limb ownership are clinically and anatomically linked (Karnath and Baier, 2010a; see also
Karnath and Baier, 2010b; Karnath et al., 2005, for the involvement
of the right insula in both the sense of limb ownership and of its
functioning).
Schaefer et al. (2007) used an artificial hand and arm that
appeared visually to be connected to the participant’s own body
in order to give their participants the impression that they had a
supernumerary third arm (positioned in a central location between
their actual hands; see also Newport et al., 2010). The behavioural
data, obtained by means of questionnaire responses, demonstrated
that six out of the eight participants tested felt as if they had three
arms (yet another impossible notion!). Even more interesting is
that the activation of primary somatosensory cortex (SI), as measured by magneto-encephalography (MEG), was modulated by the
perceived presence of the supernumerary limb (i.e., the cortical
representation of the thumb shifted to a more medial and superior
position). This modulation was found to be positively related to the
strength of the feeling that the third arm actually belonged to the
participant. That is, the modulation of bodily awareness seems to
correlate with changes in activity at the level of the somatosensory
cortex – a finding consistent with earlier work in which artificially
induced referred sensations occurred with concomitant changes
in S1 responses (Schaefer et al., 2006). That sensory input can be
used to induce impossible configurations of the perceptual representation of one’s body is not new. In older experiments using
tendon vibration (e.g., Craske, 1977), participants were reported
to experience their hand moving through their head, or their nose
growing to an unnatural length (the so-called ‘Pinocchio illusion’),
or their waist shrinking (Ehrsson et al., 2005b). However, recent
work has also established that entirely novel bodily schema can also
be generated without the need to manipulate the sensory input: For
instance, in one recent study, Moseley and Brugger (2009) encour-
Fig. 2. The perceived form of the phantom limb in an amputee who had learnt to
perform a movement of their phantom limb that would be impossible to perform
with an intact limb. Remarkably, the formation of the new phantom also reduced
his capacity to perform sideways movements of his phantom wrist, movements
that would be made more difficult by the new structure of the wrist (Moseley and
Brugger, 2009).
aged upper limb amputees to learn a movement of their phantom
limb that would be impossible to perform in a real limb because
of anatomical constraints. Remarkably, those who reported success also reported fundamental changes in the structure of their
phantom limb – for example, the wrist joint was transformed
into a wheel and axle type joint (see Fig. 2). Crucially, all of the
participants’ reports (which, of course, might be subject to experimenter expectancy effects) were corroborated by performance on
an implicit motor imagery task.
Recently, researchers have been using event-related potentials
(ERPs) in order to investigate the role of early and late neural
processing in the integration of seen and felt tactile stimulation,
thought to be at the core of the RHI. Watching someone else being
touched activates secondary somatosensory cortex in the same
manner as being touched – a kind of tactile empathy (Keysers et al.,
2004). Press et al. (2008) extended this to the RHI. They demonstrated increased N140 amplitudes, which are thought to reflect
the early sensory processing of the stimuli, after a training period
in which participants were exposed to synchronous tactile and
visual stimuli presented on a rubber hand or a non-corporeal rubber object. Surprisingly, this effect did not change as a function of
whether the participants were viewing a rubber hand or another
object. This would seem consistent with Armel and Ramachandran’s observation that they were able to induce the illusion
of ownership over a table-top (Armel and Ramachandran, 2003;
though see Tsakiris and Haggard, 2005; Hohwy and Paton, 2010,
for contradictory findings). Press et al. (2008) also reported that
later ERP components (i.e., those occurring more than 200 ms poststimulus) were modulated by the ‘spatial’ compatibility between
the real hand and the visible rubber hand/object. That is, an
enhanced sustained negativity was found following stimulation
of the left hand when participants viewed a left rubber hand or
object. These findings can be taken to suggest that: (1) Early levels
of sensory information processing (e.g., the secondary somatosensory cortex, SII) are modulated by the synchronous presentation of
visual and tactile stimuli, but not by the anatomical compatibility
between higher order representation(s) of the body and the position (or nature) of the objects in external space; (2) Later levels of
information processing are affected both by the spatial compatibil-
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ity between the position of the stimuli in external space and by the
actual position of the body in space; and (3) These later changes in
neural activity seem to be related to the physical similarity between
the object placed in that part of space (i.e., a neutral object or rubber hand) and the participant’s own body. Press and her colleagues
went on to conclude that higher order body representations affect
later but not early stages of tactile information processing. It is relevant to note here that disrupting activity in higher order areas such
as the right temporo-parietal junction (rTPJ) by using TMS impairs
the process that compares the compatibility between the visual
aspect of a stimulus and a mental representation of the body. That
is, TMS over rTPJ reduced the extent to which an artificial rubber
hand was incorporated into the mental representation of a person’s
own body, while it increased the incorporation of a neutral object
(Tsakiris et al., 2008; see also Tsakiris, 2010).
5. Body-centred spatial representations and bodily
illusions – lessons from the clinic
On the basis of the large body of empirical evidence that is
now available, it has been suggested that spatial rather than solely
anatomical representations might play a major role in the awareness of tactile stimuli presented on the body surface (Gallace and
Spence, 2008, 2010; Kitazawa, 2002). One source of evidence in
support of such a claim comes from the study of those patients
affected by spatial neglect. In fact, neurological damage to those
areas of the brain involved in the processing and selection of the
spatial aspects of stimulation, such as in neglect or extinction, is
often associated with disorders of body ownership. So, for example, neglect patients may show the presence of somatoparaphrenia,
a form of delusion whereby the patient denies ownership of a limb
or an entire side of their body. That is, patients with this condition might affirm (even if no evidence of psychiatric disorders is
present) that their contralesional arm belongs to the doctor or to
another patient who they believe may have left it behind (Vallar
and Ronchi, 2009). It is worth noting here that this deficit has
also been reported in patients with spared somatosensory processing (e.g., Berthier and Starkstein, 1987). This suggests that
peripheral mechanisms are unlikely to constitute the main cause
of disrupted body disownership disorders such as somatoparaphrenia.
Emerging data suggest that tactile neglect-like pathologies, disrupted bodily awareness and body ownership can also result from
neurological disease triggered by musculoskeletal injury. Anecdotal accounts exist, for example Sacks’ (1991) reflections of limb
disownership after a fracture. One condition in which disrupted
bodily awareness is common is complex regional pain syndrome
(CRPS), which is most common after wrist fracture (occurring
in about 2% of cases). CRPS is characterised by severe pain and
sensitivity, swelling, and motor disturbance. Disrupted thermal
regulation, with the affected arm most often cooler than the healthy
one, is a cardinal sign of the disorder. Signs and symptoms are usually confined to a single limb or occasionally to one side of the
body (see Janig and Baron, 2002, and Moseley, 2007a, for reviews).
Although usually triggered by minor tissue injury, CRPS has also
been reported after stroke (Petchkrua et al., 2000) and psychogenic
cases have also been reported too (Grande et al., 2004). Acute
CRPS is sometimes still considered a peripheral disorder (Oaklander
and Fields, 2009), but chronic CRPS is now widely established
to be a central nervous system disease (Janig and Baron, 2002).
Behavioural evidence of neglect and disruption of bodily awareness, including disownership of the limb, were first reported in
people with CRPS almost 150 years ago in seminal work by Mitchell
(1864). However, only recently have these phenemona been formally investigated using more robust empirical/psychophysical
methods.
Fig. 3. Mean (circles) and standard deviation (error bars) of the perceived size of
the thumb (filled circles) and index finger (open circles) during control, after full
anaesthesia of the thumb induced by local anaesthestic injection into the digital
nerves of the thumb, after innocuous stimulation of the intact thumb, and after
painful cooling of the thumb. Asterisk denotes significantly different to control.
Modified from Gandevia and Phegan (1999), with permission from the author.
We now know that in those suffering from CRPS of one limb,
the limb is perceived to be bigger than it actually is (Moseley,
2005), a phenomenon known as ‘macrosomatognosia’ (Podoll and
Robinson, 2000). As might be predicted, CRPS is also associated
with increased two-point discrimination threshold on the affected
limb (Moseley et al., 2008e; Moseley and Wiech, 2009). This perceived enlargement of a specific body part occurs clinically with the
use of local anaesthesia – think of the feeling of a fat lip after the
anaesthetic wears off following a dental procedure – and has been
induced experimentally by topical anaesthetic applied to a single
digit, non-noxious electrical stimulation of one digit, and painful
cooling of one digit (Gandevia and Phegan, 1999, see Fig. 3).
Amputees often report that their phantom limb is very large,
twisted, heavy, or floating above them (Melzack, 1989). The wide
range of perceptual distortions that are reported by amputees has
been comprehensively studied (Giummarra et al., 2010a,b) and
such distortions are usually attributed to bottom-up mechanisms,
namely disrupted somatosensory input from the body-part concerned. The common observation that people with CRPS often
report feeling as though the affected limb no longer belongs to
them, has also been attributed to bottom-up mechanisms (Lewis
et al., 2007).
In fact, disruption of body-related representations is widespread
in painful disorders. For example, in phantom limb pain, to the
extent of S1 reorganisation, as measured by the shift in the peak
S1 response to stimulation of the lip, is positively related the
magnitude of usual phantom limb pain (Flor et al., 1995). S1 reorganisation has also been documented in people with chronic low
back pain (Flor et al., 1997) and CRPS (Maihofner et al., 2003). In
CRPS, the somatotopic representation of the affected limb in primary sensory cortex is altered such that the peak cortical evoked
response to stimulation of the 5th digit is about 1 cm closer to
the peak cortical evoked response to 1st digit stimulation than in
healthy controls (Maihofner et al., 2003); tactile stimuli are often
mislocalised and proprioceptive acuity is reduced (Frettloh et al.,
2006; Maihofner et al., 2006). When asked to judge whether a picture represents a left or right hand, a task that has been thoroughly
investigated in healthy controls (see Parsons, 2001, for review),
people with CRPS of one hand take longer to make this judgment if the pictured hand corresponds to their own affected limb
(Moseley, 2004a,b). Previously, this effect has been attributed to
pain (Schwoebel et al., 2001), However, experiments in healthy
controls suggest that it probably reflects an information processing
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39
and Jensen, 2001) – perhaps they too have a cold side of space.
One is inclined to ask then, to what extent are higher order spatial
representations responsible for these phenomena? The answers to
such questions might have implications that extend well beyond
our understanding of those individuals with chronic pain – indeed,
many psychiatric and neurological conditions are also characterised by both distortions of bodily awareness or ownership and
disrupted thermal regulation (see Supplementary Table S1).
Fig. 4. Individual data showing the stimulus onset asynchrony (SOA) at which participants were equally likely to judge either stimulus as occurring first. That is, the
point of subjective simultaneity, PSS, with the hands uncrossed (filled circles) or
crossed over the midline (open circles). Data shown with affected hand to the right.
Note that when the arms were not crossed, tactile stimuli from the healthy hand
were prioritised over those from the affected side, but when the arms were crossed,
this relationship was reversed, showing prioritisation of tactile stimuli from the
healthy side of the midline over those form the affected side of the midline.
Adapted from Moseley et al. (2009).
bias instead, such that visual stimuli relevant to the healthy hand
are prioritised over those relevant to the painful hand (Hudson
et al., 2006; Moseley et al., 2005). A similar effect has also been
observed in spatial neglect (Coslett, 1998). Thus, it is clear that the
body-related cortical maps of the affected body-part are disrupted
in patients suffering from CRPS. What is more, the response profile
of S1 neurons is altered as well. However, some of these findings
may equally relate to disruption of higher level representations,
such as those responsible for the functional engagement of body
parts (e.g. Blasing et al., 2010) or for the mapping of external space.
Relevant to this possibility is the recent finding that CRPS is
associated with spatially defined deficits in sensory processing.
For example, in one recent study, individuals with unilateral CRPS
resulting from tissue trauma to one arm made temporal order judgments (TOJs) concerning pairs of tactile stimuli, one delivered to
either hand (Moseley et al., 2009). When the arms were positioned
to either side of the body midline (i.e., in their normal space), the
vibrotactile stimulus delivered to the affected hand had to be presented before the stimulus to the other hand in order for them to be
perceived as simultaneous. However, when the participant’s arms
were crossed over, such that the affected hand was now situated
on the opposite side of the body midline and the healthy hand was
placed on the affected side of space, the order of the stimuli had to
be reversed in order for them to appear simultaneous (see Fig. 4).
This pattern of results is also characteristic of post-stroke neglect
(Aglioti et al., 1999; Berberovic et al., 2004; Rorden et al., 1997).
6. Spatial representation and autonomic control
The link between these higher order representations and signs
and symptoms of CRPS seems to be even closer than was previously thought. Hard though it might be to believe, patients with
CRPS involving autonomic dysfunction of one hand have a cold side
of external space (Moseley et al., unpublished data). That is, when
these patients hold their affected, cool, hand on the opposite side
of the midline, it becomes warmer. Even more remarkably, when
the participants held their unaffected, healthy hand on the opposite side of the midline, it became somewhat cooler and slightly
less painful, although the extent of pain relief was too small to be
clinically meaningful. The extent of the temperature change was
positively related to how far across the midline the hand was positioned. These observations clearly beg further investigation in order
to address questions such as: How are the disruption of body ownership, tactile processing, and thermal regulation related to one
another and to pain? Relevant to this is the finding that phantom
limb pain is negatively related to stump temperature (Nikolajsen
7. The ‘body matrix’
Here, we suggest that a multisensory representation of peripersonal space, and, in particular, of the space directly around the body
– what we call a ‘body matrix’ – might be involved in some aspects
of the phenomena described in this review (see Fig. 5). This representation is likely to receive inputs from areas of the brain that code
for visual, tactile, and proprioceptive input. An important difference
between the body matrix and other representations of peripersonal space is that the body matrix is aligned with a body-centred
rather than hand-centred frame of reference. That is, stimuli arising from the left side of external space and within the body-matrix
are always mapped as ‘left’, regardless of the fact that they arise
from the left hand, or from the right hand being placed in the left
space (and regardless of their sensory modality). Note, however,
that under those conditions in which the hands are crossed over
the midline, the strength of the connections from somatotopically
organized areas might change (Gallace et al., in press). Given that a
body-centred frame of reference does not depend on the position
of the body parts in space (e.g., whether the arms are crossed or
uncrossed over the body midline), results such as those obtained
with CRPS patients become more easily explained. Of course, it
remains to be established whether this midline effect is centred on
the head or the torso, that this representation is rather coarse, and
extends beyond the boundaries of the body surface, allows external objects, such as rubber hands (or indeed two rubber hands, see
Petkova and Ehrsson, 2009), to be perceived as part of the body (but
perhaps it is also responsible for phenomena such as tactile completion; Gallace and Spence, in press; Kitagawa et al., 2009). Given the
multisensory nature of such representations, synchronous crossmodal stimulation of the external object would seem most likely
to modulate ownership. Of course, any ‘assumption of unity’ that
the participant has (i.e. a top-down belief that what the participant
sees genuinely belongs together with what they feel), may help to
facilitate the illusion (see Helbig and Ernst, 2007; Spence, 2007).
We propose that this body-centred representation might be
altered (or the amount of neural activation involved in the representation be decreased; Maihofner et al., 2003) by abnormal
feedback from other areas of the brain, just as is seen following
direct neurological damage. A malfunctioning in the part of this representation responsible for mapping one side of the space around
the body might, for example, be caused by altered input from the
side of the body that more often occupies that part of space. In the
case of CRPS, this altered input might result from musculoskeletal injury, while, in the neglect syndrome, this might be caused
by direct damage or lack of feedback from other higher order spatial representations. The presence of an alteration that is spatially,
rather than somatotopically driven, would then help to explain why
it is that tactile processing in both neglect and CRPS patients varies
whenever their hands are crossed over the body midline.
What is the role of this body matrix? We contend that the
body matrix serves to maintain the integrity of the body at
both the homeostatic and psychological levels, and to adapt to
changes in our body structure and orientation (from both an ontogenetical and phylogenetic point of view; see Bremner et al.,
2008). By incorporating regulatory functions such as tempera-
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G.L. Moseley et al. / Neuroscience and Biobehavioral Reviews 36 (2012) 34–46
Fig. 5. Cortical areas involved in the ‘body matrix’, including those implicated in experimental induction of ownership using the RHI (shaded grey), in somatotopic representation of the body (blue) and in peripersonal and body-centred spatial representation (green). The posterior and superior parietal multisensory areas have known connections
with autonomic centres in the insular and thence the brainstem (orange), which poses a feasible mechanism by which limb ownership and body-centred spatial representations can modulate limb-specific blood flow. The diagonal section removes the left cortical hemisphere to show the medial surface of the right hemisphere. Post. = posterior,
Sup. = superior, S1 = primary somatosensory cortex. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of the article.)
ture control and the prioritisation of tactile inputs, the body
matrix contrasts with previous dichotomous distinctions between
a posturo-sensorimotor body ‘schema’ and a conscious and evaluative ‘body image’ (e.g., Gallagher, 2005). Rather, the body matrix
integrates these constructs by proposing a direct inter-relationship
between cognitive representations such as ownership over a body
part and homeostatic function such as thermoregulation. Not that
such an inter-relationship necessitates a single cortical representation that is, one body in the brain. We instead propose that many
cortical representations contribute to this interrelationship, much
in the manner elegantly proposed by Berlucchi and Aglioti (2010),
that is, many bodies in the brain. The precise mechanisms responsible for these inter-relationships certainly need to be investigated
further, including by means of neuroimaging studies. However, we
believe that an important role might be played here by the connections between the posterior parietal cortex (where spatially based
information is processed and integrated) and the insular cortex (see
Fechir et al., 2010, for the report of inhibitory connections between
the insula and autonomic brain stem structures). In addition to
its apparent role in the sense of ownership imparted by the RHI
(Tsakiris et al., 2007), the insular is also important in interoceptive awareness (Craig, 2002; Critchley et al., 2004) and homeostasis
(Oppenheimer et al., 1992). Interestingly, as a paralimbic cortex,
the insular cortex can be considered a relatively old neural structure (Tucker, 1992). Following on from these considerations, it is
not implausible to think that the body matrix (seen as a coarse
representation of the body and of the space around it) might be
evolved within this structure. In fact, from an evolutionary point of
view, it seems more economical to have a unique structure (a sort
of proto-representation of the body space) that can endorse different body shapes (given a small number of constraints) rather than
having a larger number of more specific structures for more specific body shapes. Moreover, most mammals have a broadly similar
body structure (Darwin, 1859) and a ‘body matrix’ such as that proposed here would accommodate this wider range of broadly similar
structures.
Also relevant to this idea of a body matrix is the rapidly expanding literature on empathy. Empathy usually refers to understanding
the emotional state of another, within the context of oneself
(Decety and Jackson, 2006). Empathy is thought to be critical for
social function, allowing us to interpret and predict the behaviours
of others and to respond to them in a functional manner. Indeed,
empathy may involve the active simulation of another person’s
state, via activation of so-called cortical mirror systems (Fitzgibbon
et al., 2010). A multisensory body matrix as proposed here would
accommodate variability in body dimensions in the capacity to mirror the physical configuration and behaviour of another. Moreover,
theories of embodied cognition (e.g., Damasio, 1996; Seitz, 2000)
would suggest that the homeostatic and regulatory role of the body
matrix might also give it a role in emotional empathy.
8. What happens to the disowned/replaced part?
Myriad studies have focused on how a foreign limb, or indeed
object, can be ‘owned’. Researchers now know a lot about embodiment of artificial or even virtual body parts (and indeed entire
bodies, e.g., Ehrsson, 2007; Lenggenhager et al., 2007), but far less is
currently known about what happens to the limb that is ‘replaced’,
if indeed it is. Even in the absence of the clinical observations outlined above, it would seem a sensible consideration because, with
the exception of a small proportion of upper limb amputees (see
Giummarra et al., in press), neurocognitively normal participants
never report the sensation of having three arms when they experience the RHI (Longo et al., 2008; Schaefer et al., in press). This
observation suggests that either (1) The rubber hand and the actual
hand become unified, that is, there is some sense of disownership of
the intact, actual hand; or else (2) Maybe the dominant hand representation simply extinguishes the other representation as happens
in the Colavita effect (see Hartcher-O’Brien et al., 2008, 2010).
The question related to the destiny of the disowned or replace
body part was recently investigated by Moseley and his colleagues
in a series of six RHI experiments, each conducted on a different
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41
Fig. 7. Infra-red thermographic images taken after 10 min of asynchronous stroking
of the rubber hand and the actual hand, which does not induce the rubber hand
illusion (RHIS) (left image) and after 25 min of a sustained rubber hand illusion
(right image). Time course of the change in temperature at each of two locations on
the hand is shown.
Fig. 6. Mean (bold line) and standard deviation (grey line) vividness of the rubber
hand illusion (RHI) (panel a), foot skin temperature (b) and hand skin temperature
(c) during control (Ctl) and RHI conditions. Scatterplots of the decrease in hand skin
temperature vs the vividness of the RHI (d) and of the point of subjective simultaneity (PSS, >0 = away from experimental hand) vs the vividness of the RHI. Asterisk
denotes significant effect p < .02.
Adapted from Moseley et al. (2008b).
group of healthy volunteers (Moseley et al., 2008b). In their first
experiment, they showed that the RHI was associated with cooling
of the ‘replaced’ hand. Subsequently, it was demonstrated that that
the drop in temperature was limited to the experimental hand – the
opposite hand does not cool, nor for that matter does the ipsilateral
leg. This result demonstrates that the effect is not simply a general
effect of arousal (i.e., a body-wide sympathetic response). The drop
in temperature was clearly dependent on the illusion of ownership
over the rubber hand, not on tactile stimulation of the hand, nor
on simultaneous visual and tactile input, and it was equally apparent no matter whether the RHI was induced in the left or right
hand. Finally, the stronger the illusion of ownership over the rubber hand, the greater the drop in temperature of the intact hand
(see Fig. 6). This cooling effect has since been replicated using a
similar protocol (Kammers et al., in press) and using a protocol that
does not involve the spatial disparity between any artificial and
actual hand (Hohwy and Paton, 2010). We suggest here that this
drop in the temperature of the hand might arise from the dynamic
changes in neural activity across the body matrix. That is, following
synchronous visuo-tactile stimulation, neural activation increases
across the representation of the space that is now occupied by the
rubber hand. As a result, that space starts to be considered more
as an actual part of the body (generating protection, body ownership and homeostatic control). By contrast, the neural activation
of the representation of the space where the real hand is placed
decreases. As a consequence, that degree to which a space or body
part is ‘owned’ is decreased, and thus homeostatic control and sensory processing from these areas decreases. Consistent with this
idea is a recent finding of tactile processing deficits induced by
visual-proprioceptive incongruence using prism glasses (Folegatti
et al., 2009). In that study, participants performed a tactile detection
task under a control condition in which visual and proprioceptive
information were aligned and when prism glasses shifted the visual
perspective so that it was no longer aligned with the proprioceptive input. In that condition, tactile processing was disrupted in
the same manner as that observed during the RHI. That finding
seems consistent with the idea that the perceived spatial coordinates of the limb are important. As such, one might predict, that the
reduction in homeostatic control and sensory processing observed
during the RHI would be reduced or eliminated if the rubber hand
and the real hand were to be located in exactly the same location in
space.
That the strength of the illusion and limb-specific cooling are
positively related might lead one to wonder if the effect is in
some way linked to Damasio’s (1996) somatic marker hypothesis; According to Damasio’s oft-cited theory, our reasoning and
decision-making is influenced by our body’s internal state. That
theory would predict that cooling of the limb would occur before
the illusion. In contrast, the illusion clearly occurs before the limb
begins to cool (see Figs. 6 and 7). Of further interest, with regards
to the effects of the RHI on the replaced or disowned hand, were
the results of a series of TOJ experiments performed by healthy
volunteers who either were, or were not, experiencing the illusion
(Moseley et al., 2008b). During the RHI, a vibrotactile stimulus had
to be delivered to the ‘disowned’ hand before an identical stimulus
was delivered to the opposite hand, for the two stimuli to be perceived as simultaneous (see Fig. 6). One might wonder if this effect
could have resulted from the drop in skin temperature, but the magnitude of the cooling effect was too small to induce such a change
(see von Bekesy, 1963). Thus, the simplest interpretation is that
inducing the illusion of ownership over a rubber hand also induced
a type of tactile neglect of the real hand, similar in magnitude to that
observed in people suffering from CRPS of one hand (Moseley et al.,
2009). Moreover, the sense of ownership over the rubber hand was
positively correlated with the extent of the tactile processing bias
as measured by stimulus onset asynchrony at which stimuli were
perceived as simultaneous. A similar relation between the extent
of the tactile processing bias away from the affected hand, and the
reported sense of disownership of the arm, has been observed in
people with CRPS of one arm (Moseley et al., unpublished data).
The integration of ownership and regulatory loops was recently
highlighted by Kammers et al. (in press), who demonstrated that
cooling the experimental arm during the RHI increased the vividness of the illusion and warming it decreased the vividness of the
illusion.
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9. Other distortions of bodily perception induced by
misleading visual cues
While the majority of studies have utilized an artificial (rubber) hand in order to induce intersensory conflict and distortions
of body image, one might ask what happens if such an intersensory conflict is introduced by distorting the veridical visual input
of one’s own limb? Moseley et al. (2008c) recently investigated the
effect on pain of viewing one’s body through a minifying or magnifying lens (see also Kennett et al., 2001; Rock and Victor, 1964).
In that study, participants with chronic pain in their arm made a
set of ten stereotypical movements while viewing their affected
limb. They simply watched their affected arm, or viewed it through
(i) a pair of binoculars that had had their lenses removed (control condition), (ii) through binoculars (magnification condition),
or (iii) through reversed binoculars (minification condition). The
results showed that the increase in pain caused by movement was
lower when the patients looked at their limb through a minifying lens than during any of the other conditions. By contrast, the
increase in pain was greater when patients looked at their limb
through a magnifying lens than in any of the other conditions
(see Fig. 8). Crucially, because motion analysis demonstrated that
the movements themselves were very similar during each condition, it can be concluded that the psychological illusion itself led
to physiological consequences, namely more swelling of the fingers on the affected limb during magnification and less during
minification.
That distorting the visual appearance of a limb can affect
swelling demonstrates the bidirectional nature of the link between
the body matrix and the body itself. However, one might ask how
this effect could occur? There are at least three possibilities here:
First, the representational state of the body probably has direct
projections to descending modulatory neurons within the nociceptive system. In chronic pain patients, sensory cues that imply that
the limb is more swollen than it actually is, likely activate these
modulatory neurons. This possibility would be predicted by our
modern understanding of pain as a protective output of the brain
that depends on the implicit perception of threat to body tissue, not
on the actual threat to body tissue (see Butler and Moseley, 2003,
and Moseley, 2007a, for reviews).
The neural hardware that would be capable of mediating a topdown effect on swelling, should the brain seek to protect a specific
body part, is also well-established – descending projections work
both to facilitate and inhibit activity of spinal nociceptive neurons
(Pertovaara, 2000; Vanegas and Schaible, 2004) and antidromic
activation of C fibres has been shown to induce peptidergic inflammation and thus swelling (e.g., Wang et al., 1997). It is also possible
that the effect is less about protection of the painful arm and,
instead, just a legacy of the visual enhancment of touch, which
is thought to be mediated by visuotactile cells in the parietal
cortex (Kennett et al., 2001; Schaefer et al., 2005a,b, in press). Perhaps magnifying the visual image of the limb increases activity of
these cells sufficiently to induce activation in sensitive neural networks subserving pain, and upregulating descending facilitation
and subsequent peptidergic inflammation in a manner similar to
that described above (Butler and Moseley, 2003).
Perhaps magnifying the image simply introduces conflict
between vision and proprioception. Such incongruence has been
proposed to cause phantom limb pain (Harris, 1999; Ramachandran
et al., 1995), although it should be noted that this explanation would
predict similar effects during both minification and magnification.
There are also anecdotal reports that viewing oneself through a
minifying lens reduces one’s sense of ownership over a body part
(Ramachandran and Rogers Ramachandran, 2007), which would
seem, in part, consistent with the idea that decreasing ownership
over a limb serves to reduce provocation of pain in that limb. In
any case, the remarkable observation that bodily illusions in which
higher order representations of the body are cognitively distorted,
modulates swelling at a tissue level, clearly implicates a top-down
mechanism that extends to the bodily tissues.
In neurologically normal individuals, merely seeing a body part
reduces pain evoked by a noxious stimulus (Longo et al., 2009) and
seeing a magnified view of the body has a larger analgesic effect
(Mancini et al., 2011). That a magnified visual image is algesic in
patients with CRPS but analgesic in healthy controls is consistent
with findings from somatosensory stimuli – proprioceptive when
the central nervous system is in a sensitised state and antinociceptive when it is in a normal state (Fields et al., 2006). Indeed, it is well
established that neural mechanisms that subserve nociception and
pain undergo profound changes in sensitivity as pain persists (see
Butler and Moseley, 2003), so much so that visual input of touch can
evoke pain without any sensory input from the body part (Acerra
and Moseley, 2005). This result would seem similar at first glance
to recent reports that the RHI can be induced using noxious stimuli
such that pain is felt in the rubber hand (Capelari et al., 2009).
Of course, many questions remain unanswered and the use of
minification lenses to treat those in chronic pain, or magnifying
lens to treat acute procedural pain, are not yet warranted. However, that visual distortion can modulate tissue function adds to
a growing body of evidence that illusions of body ownership and
bodily awareness can have clinical applications.
10. Other bodily illusions in patients – can it all be done
with mirrors?
That a minifying lens can reduce pain (at least in the short
term) in patients with arm pain has now also been demonstrated
with regards to phantom limb pain, albeit in a single case report
(Ramachandran et al., 2009). Nonetheless, those familiar with
research in this area cannot help but see the parallel between
the use of minifying lens to reduce pain and swelling utilized
by Moseley et al. (2008c), and the more widespread use of mirrors to reduce the phantom limb pain, an approach popularized
by Ramachandran et al. (1995). Although the peculiar perceptual
effects that can be induced using mirrors have been of interest for
well over a century (Stratton, 1899), Ramachandran’s observations
sparked much interest in its potential clinically. In short, one places
the affected arm or leg behind a mirror and uses the reflected image
of the healthy arm or leg to ‘trick’ the brain to concluding that
the affected limb is ‘magically’ better, or, as in the case of phantom limb pain in amputees – that the phantom has ‘come alive’
(Ramachandran et al., 1995).
With regard to phantom limb pain and CRPS, anecdotal observations are numerous and usually report complete resolution of
pain and of other distressing symptoms during mirror therapy
(Altschuler and Hu, 2008; Giraux and Sirigu, 2003; Karmarkar and
Lieberman, 2006; MacLachlan et al., 2004; Ramachandran et al.,
1995, 2009; Rosen and Lundborg, 2005; Tichelaar et al., 2007). However, case studies of little or no effect are typically unattractive to
journal editors (Hubbard and Armstrong, 1997), and even the most
benign of treatments can seem powerful on a one-off basis, so, to
assess the efficacy of ‘mirror therapy’, we must rely on the usual scientific methods – randomised controlled trials. A full review of the
evidence lies beyond the scope of this paper, but it has been covered
in some detail elsewhere (Moseley et al., 2008a; Ramachandran
and Altschuler, 2009). Perhaps the most parsimonious conclusion
of the robust scientific data published to date would appear to be
that mirror therapy decreases phantom limb pain and CRPS-related
pain (Chan et al., 2007; McCabe et al., 2003), particularly if it constitutes part of a wider graded program of motor imagery (Moseley,
2006).
Author's personal copy
G.L. Moseley et al. / Neuroscience and Biobehavioral Reviews 36 (2012) 34–46
43
Fig. 8. People with CRPS of one hand watched their hand while they made 10 stereotyped movements under four conditions, undertaken in random order. The first two
conditions involved no distortion of the visual input. Note that when the visual image of the moving hand was magnified, the increase in pain and swelling evoked by
movement was increased. When the visual image of the moving hand was made smaller (minified), the increase in pain and swelling evoked by movements was decreased.
Modified from Moseley et al. (2008c).
It remains unclear as to whether the analgesic effect of mirror therapy is greater than that offered by motor imagery alone
(Brodie et al., 2007). Motor imagery paradigms that include visual
feedback of a virtual limb (Mercier and Sirigu, 2009) report similar effects on phantom limb pain to those that do not include
visual feedback (MacIver et al., 2008), although some reports
suggest motor imagery alone can actually exacerbate pain in
some patients (Moseley, 2004a,b; Moseley et al., 2008d). A headto-head comparison remains to be undertaken. Mirror therapy
seems promising in post-stroke rehabilitation, where it is known
as mirror ‘training’, not ‘therapy’. Again, most case studies are
very positive (Beis et al., 2001; Lum et al., 2004; Sathian et al.,
2000; Stevens and Stoykov, 2004; though see Huffman, 1978, and
Stevens and Stoykov, 2003), but in this case randomised controlled trials also seem encouraging, particularly if mirror therapy
is undertaken in the first months after the stroke (Altschuler et al.,
1999; Cacchio et al., 2009; Sutbeyaz et al., 2007; Yavuzer et al.,
2008).
That mirror feedback and motor imagery both seem to have
some beneficial effects in patients with chronic pain, or post stroke,
is consistent with the idea that the body matrix is disrupted in
these conditions. Indeed, it remains possible that a key mechanism of the effect is the higher level of interest and engagement
in therapy that such illusions might entail. Our group introduced
36 patients with arm pain to the mirror box and to motor imagery
and told them that the effect of both was the same. Most (32/36)
said they would prefer to use the mirror box and expected to
do it more often (Moseley, 2010). We contend that, thus far, the
available clinical trials have not clearly demonstrated that it is the
reflected image of the other hand mediates the effect of mirror
therapy, but more research into this possibility certainly seems
warranted.
Regardless of whether mirror therapy offers any benefit over
and above that offered by motor imagery, it is reasonable that
both reinstate aspects of a disrupted body matrix. Motor imagery
might work to reinstate the body matrix by activating previously
established motor and behavioural representations and mirror
therapy might have its effect via visual pathways. That the body
matrix integrates spatial as well as somatotopic representations
lends itself to explaining the beneficial effects of movementbased therapies that rely on across-midline movements rather than
movement alone, such as Tai Chi and Feldenkrais (Lundblad et al.,
1999).
11. Conclusions
That we own our body and can sense it is taken for granted.
Experiments that have utilized bodily illusions, most notoriously
the RHI, have been very important in these developments. The cortical mechanisms that underpin the RHI have now been elucidated,
at least in part, and the utility of bodily illusions for investigating the representation of our body and the space around it, has
been demonstrated. Indeed, psychological illusions revealed complex relationships between our sense of ownership over a body part,
tactile processing, and autonomic control, relationships that seem
to become disrupted in those individuals suffering from chronic
pain and other neurological and psychiatric disorders. In order to
explain these relationships, we have introduced the concept of
‘body matrix’, a body-centred coarse neural representation of our
body and of the space around it. We propose that such a multisensory representation is involved in maintaining the integrity of
the body (at both the homeostatic and psychological levels), and to
adapt to changes in our body structure, and orientation. Damage,
malfunctioning or altered feedback from and toward this structure
might be one of the causes of certain symptoms of neurological syndromes involving body-ownership disorders, such as neglect and
CRPS. Finally this review has highlighted the fact that multisensory
illusions such as the mirror box, can be used to treat people with
phantom limb pain and to aid recovery after stroke, but more work
is still required to clarify the effects and to elucidate the mediating
mechanism underlying them.
Acknowledgements
GLM is supported by the National Health & Medical Research
Council of Australia ID 571090. We would like to thank Dr. Norimichi Kitagawa for drawing Fig. 1.
Appendix A. Supplementary data
Supplementary data associated with this article can be found, in
the online version, at doi:10.1016/j.neubiorev.2011.03.013.
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