B RA I N RE SE A R CH RE V I EW S 54 ( 20 0 7 ) 2 1 9–2 3 2

a v a i l a b l e a t w w w. s c i e n c e d i r e c t . c o m

w w w. e l s e v i e r. c o m / l o c a t e / b r a i n r e s r e v

Review

Central mechanisms in phantom limb perception: The past,

present and future

Melita J. Giummarra a,b,⁎, Stephen J. Gibson b,c ,

Nellie Georgiou-Karistianis a , John L. Bradshaw a
a
Experimental Neuropsychology Research Unit, School of Psychology, Psychiatry and Psychological Medicine, Monash University,
Clayton VIC 3800, Australia
b
National Ageing Research Institute, Parkville, VIC, Australia
c
Caulfield Pain Management and Research Centre, Caulfield, VIC, Australia

A R T I C LE I N FO AB S T R A C T

Article history: Phantom limbs provide valuable insight into the mechanisms underlying bodily awareness
Accepted 28 January 2007 and ownership. This paper reviews the complexity of phantom limb phenomena
Available online 1 February 2007 (proprioception, form, position, posture and telescoping), and the various contributions of
internal constructs of the body, or body schema, and neuromatrix theory in explaining these
Keywords: phenomena. Specific systems and processes that have received little attention in phantom
Phantom sensation limb research are also reviewed and highlighted as important future directions. These
Phantom pain neuromatrix include prosthesis embodiment and extended physiological proprioception (i.e., the
Mirror neuron extension of the body's “area of influence” that thereby extends one's innate sense of
Body schema proprioception), mirror neurons and cross-referencing of the phantom limb with the intact
limb (and the related phenomena of perceiving referred sensations and mirrored
movements in the phantom from the intact limb). The likely involvements of the body
schema and the body–self neuromatrix, mirror neurons, and cross-callosal and ipsilateral
mechanisms in phantom limb phenomena all suggest that the perception of a “normal”
phantom limb (that is, a non-painful phantom that has the sensory qualities of an intact
limb) is more than likely an epiphenomenon of normal functioning, action understanding
and empathy, and potentially may even be evolutionarily adaptive and perhaps necessary.
Phantom pain, however, may be a maladaptive failure of the neuromatrix to maintain global
bodily constructs.
© 2007 Elsevier B.V. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 220
2. Proprioception of the phantom limb . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 220
2.1. Distorted perception of the phantom limb . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 221
2.2. Telescoping of the phantom limb . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 221

⁎ Corresponding author. Experimental Neuropsychology Research Unit, School of Psychology, Psychiatry and Psychological Medicine,
Monash University, Clayton VIC 3800, Australia. Fax: +61 3 9905 3948.
E-mail address: melita.giummarra@med.monash.edu.au (M.J. Giummarra).

0165-0173/$ – see front matter © 2007 Elsevier B.V. All rights reserved.
doi:10.1016/j.brainresrev.2007.01.009
220 B RA I N R E SE A R CH RE V I EW S 54 ( 20 0 7 ) 2 1 9–2 3 2

3. Prosthesis use and embodiment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 222

4. The cortical origins of phantom limb phenomena . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 223
4.1. The body schema . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 223
4.2. The neuromatrix. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 224
4.3. Phantom phenomena problematic for current theory . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 224
4.4. Mirror neurons. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 225
4.4.1. Mirror neurons and action understanding . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 225
4.4.2. Mirror neurons and empathy for pain in amputees . . . . . . . . . . . . . . . . . . . . . . . . . . . . 225
4.5. Cross referencing between the intact limb and the phantom limb . . . . . . . . . . . . . . . . . . . . . . . . 226
4.5.1. Mirrored sensation and movement from the intact limb to the phantom limb . . . . . . . . . . . . . 226
4.5.2. Experimentally induced sensory and motor coupling between the phantom and real limb . . . . . . 227
5. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 228
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 228
References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 228

1. Introduction Brugger et al., 2000), and “pain matrix” mirror system

Phantom limbs are a seemingly curious phenomenon, never-
theless perceived by up to 98% of amputees following
amputation (Ramachandran and Hirstein, 1998), nerve avul-
sion (Melzack, 1992), or spinal cord injury (Bors, 1951; Braun et
al., 2001; Le Chapelain et al., 2001; Mikulis et al., 2002; Moore et
al., 2000), and by about 20% of children with congenital limb
aplasia (Melzack et al., 1997). Phantom pain is experienced by
up to 80% of amputees (Kooijman et al., 2000; Sherman, 1994),
with pain usually characterised as either (a) burning, tingling,
or throbbing; (b) cramping or squeezing; and (c) shocking or
shooting (Sherman, 1994). Phantom sensations are perceived
immediately after limb loss by most amputees (Ramachan-
dran and Hirstein, 1998); however for some, they may emerge
years or even decades after limb loss. The duration of
phantom limb perception also varies between individuals,
and phantom sensations may be perceived for anything from
a few days to weeks, months, years or even decades after limb
loss before they fade completely, if at all (Kooijman et al., 2000;
Machin and Williams, 1998).
Phantom sensations are reported most commonly follow-
ing the amputation of an arm or leg, or some part thereof
(Ramachandran and Hirstein, 1998), although they have also
been reported following removal of the breast (Aglioti et al.,
1994; Bressler et al., 1955; Jamison et al., 1979), penis (Fisher,
1999), eye (Sörös et al., 2003), teeth (Marbach, 1993), bladder
(Arcadi, 1977; Biley, 2001; Brena and Sammons, 1979) and
rectum (Cherng et al., 2001; Farley and Smith, 1968; Ovesen et
al., 1991). Phantom sensations following removal of visceral
organs may be painful in nature (for example, menstrual pain
following hysterectomy or phantom pain that resembles pre-
surgical pain) and tend to be characterised by functional
sensations; for example, sensations of urination or erection
following penis removal (Fisher, 1999; Weinstein, 1998).
The present paper reviews the literature on the perceived
“body space” of phantom limbs, their interaction with
prosthetic devices, and the evidence that the body schema
(Section 4.1, below) plays an integral role in phantom limb
perception. Current theories of phantom limb perception are
also reviewed, including Melzack’s (1990) neuromatrix theory
(Section 4.2, below), and the more recently proposed roles of
the fronto-parietal mirror neuron system (Brugger, 2006;
(Giummarra et al., 2006a) (Section 4.4, below). The pain matrix
refers to the pain-related network that primarily includes the
secondary somatosensory cortex (SII), insular regions, the
anterior cingulate cortex (ACC), and the movement-related
areas such as the cerebellum and supplementary motor area
(Singer et al., 2004). Through the mirror neuron system,
amputees with phantom sensations may have a greater
“postural empathy” for others such that they are better able
to match their own body schema against the observed bodies
of others, and are thus potentially more likely to have a bodily
experience that resembles that observed in others. The
mechanisms of cross-referencing the phantom limb with the
opposite limb are also considered (Section 4.5, below). This
review proposes that – with the likely involvement of the body
schema, mirror systems, and cross-callosal and ipsilateral
projections in phantom limb phenomena – the perception of a
“normal”, non-painful phantom limb is very likely to be an
epiphenomenon of normal functioning, action understanding
and empathy, and potentially even evolutionarily adaptive and
perhaps necessary.
2. Proprioception of the phantom limb
Phantom limbs are generally perceived to occupy veridical
body space – being of a particular size, shape and posture – and
may be perceived to be completely paralysed, or under the
amputee's volitional control (Roux et al., 2001), or to move
spontaneously or reflexively (Ramachandran and Hirstein,
1998). The phantom limb is generally described as adopting a
“habitual” position and posture (e.g., partially flexed at the
elbow with the forearm pronated), resting at the side of the
body, or in a posture that resembles the posture of the limb
prior to amputation (Ramachandran and Hirstein, 1998).
Spontaneous changes in posture of the phantom limb are
also common in amputees (Ramachandran and Hirstein, 1998)
and in (normal) patients who are under anaesthesia (Bromage
and Melzack, 1974; Melzack and Bromage, 1973). Henderson
and Smyth (1948) reported that the phantom tends to be
“correctly aligned to the stump with which it moves” (p. 90).
Often, however, the phantom limb may be perceived to be
stuck in a fixed position (Devor, 1997) and sometimes to
 B RA I N RE SE A R CH RE V I EW S 54 ( 20 0 7 ) 2 1 9–2 3 2
dissociate from the stump, particularly when the latter is out
of view (Fraser, 2002; Halligan, 1999; Wright et al., 1997). In one
of the few studies to address phantom limb proprioception
specifically, Fraser (2002) found that 63% of her sample felt
that their limb remained in a fixed position when they moved
other body parts. The perceived position of a limb in non-
amputees (Gross and Melzack, 1978), and phantom limbs in
paraplegics (Bors, 1951; Conomy, 1973; Hill, 1999) and (normal)
patients under anaesthesia (Bromage and Melzack, 1974;
Melzack and Bromage, 1973), may also become dissociated
from the real position of that limb when it is occluded from
sight.
While memories of the limb immediately prior to amputa-
tion may endure in the phantom (Katz and Melzack, 1990;
Ramachandran and Hirstein, 1998; Riddoch, 1941), these
memories do not determine the constant or continuing
posture of the phantom (Henderson and Smyth, 1948). For
example, while patients are under brachial plexus nerve block
for upper limb surgery (Melzack and Bromage, 1973), or
epidural block for lower limb surgery (Bromage and Melzack,
1974), they experience phantom limbs that do not remain in
the same position as that occupied by the limb at the time of
anaesthesia. Rather, the limb was more likely to occupy one of
a common repertoire of positions, in slight flexion, that would
have been assumed by the limb outside of anaesthesia, and
was unlikely to occupy random or unusual positions. Simi-
larly, Fraser (2002) found that the majority of amputees in her
study indicated that their phantom limb took the general
shape or form of the limb prior to amputation, and many
reported that parts of the amputated limb were missing (61%),
had shrunken or were shortened (28%), or had become
magnified (8%). Some amputees report the experience of a
general awareness of the presence of a phantom limb that is
without positional or sensory qualities (André et al., 2001;
Fraser, 2002; Hunter et al., 2003). Phantom limb posture in
some patients with spinal cord injury also mirrors the position
in which the limb was last seen during the spinal cord trauma
(Bors, 1951; Conomy, 1973; Ettlin et al., 1980). Furthermore,
Ettlin et al. (1980) reported that phantom limb illusions were
only perceived by patients who retained consciousness during
the spinal cord injury.
2.1. Distorted perception of the phantom limb
In rare instances, the phantom limb takes on a posture that is
abnormal, distorted or disfigured. Generally, amputees report
that they can move their phantom limb through normal, but
usually limited, ranges; however, a small percentage report
that they can move the phantom limb through anatomically
impossible ranges or amplitudes (Price, 1976). Melzack (1992)
described two cases of phantom limbs in abnormal postures;
one where the phantom arm was extended from the
shoulder at a 90° angle and the individual felt that he must
walk through doorways sideways, and another where the
phantom arm was stuck behind the individual's back
preventing him from sleeping on his back. Henderson and
Smyth (1948) also described a patient's anatomically unrea-
listic perception of phantom fingers that were “grossly
twisted and interwoven”. Patients with spinal cord injury
may also perceive their phantom sensations, particularly in
221
the lower limbs, as occupying anatomically unrealistic and
unnatural postures; for example, feeling “like the toes are all
turned down under the bottom of the foot”, that each digit was
somehow twisted so that “each toe pointed in a different way”
(Conomy, 1973), or that the legs were “twisted”, “crossed”, or
“blown up” (Bors, 1951). In normals, the perception of
anatomically impossible limb positions can be induced
using muscle and tendon vibration; for example, when
Craske (1977) vibrated and passively stretched the biceps
brachii of his subjects, some reported varying degrees of
hyperextension or hyperflexion of the joint, including the
(non-painful) perception that the “the arm is being broken”,
“it is being bent backwards”, or that “my hand is going
through my shoulder”. Other studies have described illusory
limb displacement, including the hand being bent back
towards the dorsal surface of the forearm (Craske, 1977), or
protruding down through a solid surface (Romani et al.,
2005); the forearm remaining stationary while the hand
continues to move downwards (Lackner and Taublieb, 1983);
or extending the nose with the Pinocchio effect (Lackner, 1988).
Romani et al. (2005) found that the mirror neuron system
(see 4.4, below) reacts to both biomechanically possible and
impossible movements, and that it is able to detect which
muscle would be involved in the actual execution of the
observed movement. These findings suggest that while
central representations of the body are indeed able to code
for anatomically impossible limb positions, the actual
perception of such limb positions rarely occurs, even in a
phantom limb, and is likely to be associated with the
experience or anticipation of pain (Willoch et al., 2000); for
example, see Armel and Ramachandran's (2003) study in
which the movement of a rubber finger (using the rubber
limb paradigm1) into “painful” positions, when the subjects
own hidden finger was moved slightly, induced responses
associated with pain. With respect to phantom limbs, Hill
(1999) noted that distorted posture in a phantom limb may
be more common following traumatic limb loss in which the
limb had been distorted by the accident. Alternatively, André
et al. (2001) suggest that phantom limbs may become
seemingly deformed or dysmorphic as a result of ectopic
activity in the stump (neuromas, ephapses, sprouting), or of
remapping in the somatosensory cortex, the thalamus or the
dorsal column nuclei. Empirical research on the mechanisms
underlying distorted or disfigured phantom limbs is, how-
ever, lacking.
2.2. Telescoping of the phantom limb
Phantom limbs may be perceived to be continuous and intact
resembling a normal limb, or telescoped so that the proximal
1
In the rubber limb paradigm, the subject's arm is hidden from
view – either behind a screen or under the table – and a life-sized
rubber model of the same arm is placed on the table in front of
them. The subject is instructed to fixate on the rubber limb, while
two small paint brushes are used to simultaneously stroke the
rubber hand and the subject's hidden hand. Within minutes,
subjects report that they feel the touch on the rubber hand, not
their hidden hand, as if their arm has embodied the fake rubber
limb (Botvinick and Cohen, 1998; Ehrsson et al., 2004).
222 B RA I N R E SE A R CH RE V I EW S 54 ( 20 0 7 ) 2 1 9–2 3 2
portion of the limb is missing or has shrunken with just the
more distal portion floating near, attached to, or “within” the
stump (Flor et al., 2006; Solonen, 1962; Weiss and Fishman,
1963). While telescoping is commonly reported in the litera-
ture, the definition of this phenomenon is lacking and it is
ambiguous whether telescoping refers to the displacement of
relative position of the components of the phantom limb over
time, or whether it refers to active movement of the
components of the phantom limb in accordance with the
concept of actively retracting a telescope. The term appears to
have been used more often to refer to the former definition;
however, some authors have used the term either with the
latter meaning or without clarifying the intended meaning; for
example, see Poeck's (1964) case description of a child whose
phantoms “gradually withdrew within the stump” when she
approached the wall with her arms, which were congenitally
missing both forearms and hands. Also, comments such as
Melzack's (1990) report that “sometimes the limb is slowly
telescoped into the stump” are ambiguous and could be
interpreted either way. In this paper, discussion about
telescoping of a phantom limb will refer to a phantom limb
that has shortened over time with the distal portion gradually
perceived to be closer to the stump.
When a phantom limb becomes telescoped it usually does
so in a “diffuse process, affecting most of the limb simulta-
neously, and not progressively, from the stump towards the
periphery” (Henderson and Smyth, 1948, p. 91). Consequently,
the remaining parts of the limb appear to become magnified
because they maintain their original size. In some amputees
telescoping may take place over a number of years, or may
change from moment to moment or day to day. The phantom
limb is perceived to be telescoped in between 49 and 63% of
cases, and this process generally begins within the first few
weeks post-amputation (Carlen et al., 1978). The distal portion
of the phantom limb may subsequently disappear (Shukla et
al., 1982), or remain “dangling” from the stump in about 50% of
cases (Ramachandran and Hirstein, 1998). Phantom limbs
apparently do not telescope in patients with spinal cord
transection, brachial plexus avulsion or in cases with pre-
existing peripheral nerve injury (Katz, 1992; Ramachandran
and Hirstein, 1998), perhaps because there are conflicting
representations of the deafferented body part according to
visual and somatosensory afferents.
It is widely accepted that phantom limbs become tele-
scoped because the distal portion of any limb is more strongly
represented in the cortex relative to the more proximal
regions of the limb (Ramachandran and Hirstein, 1998). The
upper limbs, compared with the lower limbs, are more
diffusely represented throughout the cortex as they are
integral in fine unimanual and bimanual motor schemata,
and this disparity manifests in more rapid telescoping of the
lower compared with upper limbs (Henderson and Smyth,
1948; Jones, 1988; Ramachandran and Hirstein, 1998). Over
time, the more weakly represented regions of the limb may
“fade from consciousness” while the distal portion of the limb
becomes attached to the stump, perhaps as a result of
changes in receptive fields, cortical reorganisation or changes
in stump sensitivity (Hill, 1999). Katz (1992) suggested that the
perceived distance between the phantom and the stump may
be a function of the distance separating their respective
representations in the somatosensory homunculus. While
telescoping was originally thought to be a sign of adaptive
plasticity, it tends to be related to increased levels of phantom
pain (Flor et al., 2006). Telescoping of the phantom appears to
be associated with remapping of the distal portion of the
phantom limb onto nearby regions of the cortex; for example,
movement of a completely telescoped phantom arm corre-
sponds to activity in the cortical region that represents the
shoulder, partially telescoped phantoms to activity in the
region of the arm and non-telescoped phantoms to activity in
the hand region (Flor et al., 2006). Flor et al. (2006) proposes
that the continued perception of an extended (i.e., non-
telescoped) phantom limb might reverse maladaptive cortical
changes, as the phantom continues to provide sensory
feedback to the area that previously represented the ampu-
tated limb. Telescoped phantoms, on the other hand, activate
areas remote from the limb representation (Flor et al., 2006),
and such cortical reorganisation is strongly correlated with
phantom pain.
3. Prosthesis use and embodiment
Amputees commonly feel that their phantom limb embodies
and thus becomes one with the prosthesis, and they often
confound their phantom limb with the prosthesis (André et
al., 2001). Such embodiment may be associated with a two-
way interaction between prosthesis use and phantom limb
perception. Initially, the pre-existing representation of the
amputated limb in the body schema – which also likely
provides the template for phantom limb perception – may
come to provide a valuable neural template for prosthesis use.
Repeated use of the prosthetic limb may, in turn, reinforce the
representation of the missing limb and thus reinforce the
perception of phantom limb sensations.
This hypothesis is supported by Lotze et al. (1999) who
found that upper limb amputees who use myoelectric pros-
theses do not show cortical reorganisation, or phantom limb
pain, compared with those who use either a cosmetic
prosthesis or no prosthesis. Amputees who use a prosthesis
extensively retain a different functional representation of the
amputated limb compared to non-prosthesis users, and the
endpoint of the amputated limb is perceived to be more distal
than it actually is (McDonnell et al., 1989). These findings
suggest that prostheses become embodied in the same way
that a habitually employed tool does (Lewis, 2006; Yamamoto
and Kitazawa, 2001), and preserve the biological representa-
tion of the amputated limb; that is, the bimodal neurons in the
posterior parietal cortex that code peripersonal space appear
to be recoded to represent space accessible to a handheld tool –
e.g., rake or screwdriver – in monkeys (Iriki et al., 1996) and
neurologically intact humans (Maravita et al., 2003; Yamamoto
and Kitazawa, 2001; Yamamoto et al., 2005). Essentially, it
appears that the prosthesis is incorporated into the body
schema and becomes part of a coherent internal model of the
body (Murray and Fox, 2002), and this contributes to the
relative facility and rapidity with which amputees can learn to
control a prosthesis (André et al., 2001; Murray, 2004).
While using a prosthesis, the amputee's bodily experience
is generally one of being whole, such that the prosthesis is felt
 B RA I N RE SE A R CH RE V I EW S 54 ( 20 0 7 ) 2 1 9–2 3 2
to be a “part of them” (Murray, 2004), and they phenomen-
ologically have a normal and intact body (André et al., 2001;
Giummarra et al., 2006b). The prosthesis may be described as
being embodied by, or fused with, the phantom limb (Gow et
al., 2004). The perceived convergence between phantom limb
and prosthesis helps to coordinate movement and maintain
fluid and natural motor control over the prosthesis (MacLa-
chlan et al., 2004a). For some amputees, when the phantom
limb is itchy, scratching the corresponding locus on the
embodied prosthesis can relieve the itch (Giummarra et al.,
2006b; Gow et al., 2004), suggesting that the prosthesis is
represented in the contralateral somatosensory cortex in the
same region as the phantom limb, and that the visual
feedback that parts of the prosthesis are being stimulated is
centrally processed and thus perceived as if the phantom limb
is being stimulated.
Future research. The relationship between phantom limb
sensations, prosthesis use and embodiment is still not well
understood. There is limited research to inform us of whether
and how phantom sensations and phantom pain differ
according to the use of a prosthesis, or the type of prosthesis
used. Our understanding of tool embodiment and extended
physiological proprioception – that is, the extension of the
body's “area of influence” that also extends one's innate sense
of proprioception (Gow et al., 2004) – could benefit greatly
from research on prosthesis embodiment. Experimental
research could adopt the rubber limb paradigm (Botvinick
and Cohen, 1998) to explore prosthesis embodiment. Studies
should examine prosthesis embodiment within a body
schema framework, and determine whether amputees with
phantom sensations (particularly those with complex sensa-
tions) differ in adaptation to prosthesis use compared with
other amputees without phantom sensations. Additionally, it
is unknown whether prosthesis embodiment varies between
upper limb and lower limb amputees, whose missing limbs
biologically do (upper limb) and do not (lower limb) habitually
use tools. These studies could also investigate whether
amputees' perceptions of prosthesis embodiment vary
according to voluntary versus passive movement of the
prosthesis. Investigation of the interaction between phantom
sensations and a prosthesis may provide valuable insight into
the interaction between internal constructs of the body and
the embodiment of a tool as a functional extension of the
body.
4. The cortical origins of phantom limb
phenomena
4.1. The body schema
Many authors have highlighted the distinction between the
concepts of body image and the body schema (Gallagher, 1986;
Maravita, 2006). Recently, Schwoebel and Coslett (2005) high-
lighted that there are at least three distinct types of body
representations. First, the body image is the lexical–semantic
representation of the body including the names and functions
of body parts and relations between body parts and external
objects. Second, the body structural description is a topological
map of body part locations. These body part locations are
223
monitored by visual input and defined by the boundaries of
body parts and their proximity to other body parts and objects.
Finally, the body schema, in brief, is the internal, dynamic
representation of the spatial and biomechanical properties of
one's body, and is derived from multiple sensory and motor
inputs that interact with motor systems in the generation of
actions. It is the body schema that is implicated in providing a
template for the perception of phantom limbs following
amputation or deafferentation.
Ongoing bodily experience is brought about by the “body
schema”, the plastic and dynamic representation of the body
that is constantly being modified and updated. Head and
Holmes (1911–1912) are often credited for coining the term
“body schema”; however, Maravita (2006), and Holmes and
Spence (2006) highlighted that Münk, in 1890, had previously
considered the concept of an organised spatial representation
of the body with respect to the world, and Bonnier, in 1905, had
introduced the term schema to this concept. The main
systems that contribute to the properties of the body schema
include: (a) proprioceptive and somatosensory systems, (b)
vestibular system, (c) visual system, and (d) movement
systems and efference copy—that is, the neural copy of a
movement command that is sent to the parietal cortex to be
mapped onto the body schema to generate expected sensory
outcomes (McGonigle et al., 2002), and to the premotor cortex
in preparation for rapid corrective adjustment of movements
when errors between the expected and actual sensory out-
comes are detected (Helmholtz, 1995; Lewis, 2006; Rinehart et
al., in press). The body schema is fundamentally generated in
the parietal cortex – particularly the multimodal cells in the
superior parietal lobule (Lewis, 2006), parieto-insular region
(Ventre-Dominey et al., 2003) and the temporo-parietal junc-
tion (Blanke and Arzy, 2005) – together with inputs and
outputs to various other cortical and subcortical regions.
Neurons in the parietal cortex are involved in mapping “real
space” relative to the body – that is, coding egocentric frames
of reference – based on the convergence of retinal, somaes-
thetic, proprioceptive, vestibular, and auditory signals relating
to the self and space, together with information about
movements of the eyes, neck, trunk and limbs (Stein, 1992).
Damage within the various sensory systems that contribute to
maintaining, updating or evoking templates of the body
schema can result in various perceptual aberrations, including
denial of limb ownership in somatoparaphrenia (Aglioti et al.,
1996; Halligan et al., 1995b; Ramachandran, 1996), perceived
absence of body parts in asomatognosia (Arzy et al., 2006;
Schiff and Pulver, 1999), supernumerary phantom limbs
(Brugger, 2003; Mazzoni et al., 1997; Miyazawa et al., 2004;
Sakagami et al., 2002), disembodiment and autoscopic phe-
nomena in out-of-body experiences (Blanke, 2004; Blanke and
Arzy, 2005; Brugger et al., 1997), and magnification and
shrinking of various body parts, or Alice in Wonderland
illusions, in somaesthetic aura (Kew et al., 1998).
The body schema consists of innate representations of the
biological, evolutionary design and function of the human
body and a repertoire of motor templates (e.g., hand–mouth
coordination) designed to promote survival in infancy (Galla-
gher et al., 1998). It also provides a neural platform for
understanding and interacting with others throughout life
(Brugger et al., 2000; Melzack, 1989). Phantom limb perception
224 B RA I N R E SE A R CH RE V I EW S 54 ( 20 0 7 ) 2 1 9–2 3 2
following congenital limb deficiency suggests that the brain
may be genetically predisposed to represent a prototypical
human body, regardless of the correspondence or lack thereof
between the ideal model and the actual body (Berlucchi and
Aglioti, 1997). The innate body schema is then retained and
modified throughout life experience (Melzack et al., 1997;
Weinstein and Sersen, 1961; Weinstein et al., 1964). The range
of triggers that evoke or modify phantom sensations and pain
provide evidence for the complex involvement of the various
systems likely involved in bodily awareness and perception in
phantom limb phenomena, including stimulation of the
vestibular system (André et al., 2001; Le Chapelain et al.,
2001), visual illusions of phantom limb embodiment using the
mirror box [also see 4.5.2, below] (Ramachandran et al., 1995)
and tactile or somatosensory inputs from the stump and/or
remaining portion of the amputated limb (Melzack et al., 1997;
Saadah and Melzack, 1994; Wilkins et al., 2004). Additionally,
“forgetting” the limb loss and the performance of automatic
motor schemas with the phantom limb (e.g., attempts to
answer the telephone or fend off a blow with the missing limb)
can trigger phantom sensations and pain (Giummarra et al.,
2006a; Hill, 1999; Price, 1976; Ramachandran and Hirstein,
1998). The complex nature of phantom limbs suggests that the
same systems responsible for maintaining, updating and
evoking internal representations of the body are responsible
for maintaining templates of the phantom limb. These
sensory systems are further accounted for in Melzack's
(1989, 1990, 1992, 1996) neuromatrix theory of phantom limb
perception.
4.2. The neuromatrix
Melzack's (1989, 1990, 1992, 1996) neuromatrix theory of
phantom limb perception extends theories of the body
schema, and proposes that conscious awareness and percep-
tion of the body and self are primarily generated within the
brain via patterns of activity (or neurosignatures) that can be
triggered or modulated by various perceptual inputs. These
inputs primarily include (a) somatosensory inputs (cutaneous,
visceral and other somatic receptors), (b) visual and other
sensory inputs that influence the cognitive interpretation of
the situation, (c) phasic and tonic cognitive and emotional
inputs from other areas of the brain, (d) intrinsic neural
inhibitory modulation inherent in all brain function, and (e)
the activity of the body's stress regulation systems, including
cytokines as well as the endocrine, autonomic, immune and
opioid systems (Melzack, 1999). These inputs thus generate
the body–self neuromatrix primarily through the somatosen-
sory, limbic and thalamocortical systems.
While multiple sensory inputs are integrated to create the
body–self neuromatrix, amputation and deafferentation are
commonly associated with cortical reorganisation, and spon-
taneous bursts of activity that produce output patterns that
resemble activity associated with pain and thus lead to the
conscious experience of phantom pain (Melzack, 1999). For
example, according to Melzack (1996) high-frequency bursts of
activity associated with deafferentation may be interpreted as
hot or burning pain, although there is evidence that burning
pain is associated with vascular mechanisms (i.e., a reduction
in blood flow in the stump) (Sherman, 1994). Melzack (1996)
further proposes that cramping pain and shooting phantom
pain may arise from similar origins from spontaneous activity
associated with intention to move muscles; however, there is
also evidence that cramping phantom pain is related to
muscle tension in the residual limb (Sherman, 1994). Con-
tinued sensory input through stimulation and functional
sensitivity of the residual limb and stump, however, may
preserve a “normal”, non-painful representation of the
amputated limb in the body schema (Bittar et al., 2005; Lotze
et al., 1999); for example, by providing continued sensory input
via sensory discrimination training (the discrimination
between the frequency and/or location of sensory inputs,
such as electrical impulses (Flor et al., 2001)), myoelectric
prosthesis use, Transcutaneous Electrical Nerve Stimulation
(TENS), or vibration.
The neuromatrix theory provides a valuable model for the
perception of phantom phenomena, and particularly phan-
tom pain, which, unlike sources of pain triggered by injury or
lesion, is often triggered by supraspinal (e.g., affective,
emotional, and cognitive factors), peripheral (e.g., from the
residual limb/stump, or other sites) and environmental (e.g.,
changes in barometric pressure) experiences, as well as by
spontaneous ectopic activity at central, spinal or peripheral
levels. A major limitation of the neuromatrix theory, however,
is that while it can broadly account for the various aspects of
phantom phenomena, it is possibly too broad and difficult to
be tested empirically, particularly with respect to painless
phantom sensations.
4.3. Phantom phenomena problematic for current theory
There are many aspects of phantom limb experience that
current theory of phantom limb phenomena do not explain,
or which cannot be tested under current models. First, why
do some amputees with similar circumstances of limb loss
experience no phantom sensations, some only painless
phantom sensations, and some only phantom pain (as
amputees in our studies have reported)? Second, how do
internal representations of the self (that is, templates of the
body schema) interact with specific sensory afferents (e.g.,
visual, proprioceptive, motor, vestibular) in relation to
phantom limb sensations? Third, how and why do phan-
tom limbs telescope actively? Fourth, why do phantom
sensations continue to be perceived by some amputees,
while for others phantom sensations diminish, telescope or
disappear over time? Fifth, why do some congenital and
childhood amputees feel phantom sensations as adults,
even when they have never experienced a limb (e.g.,
absence of all four limbs as reported by Brugger et al.,
2000)? Sixth, why do people who desire amputation of a
healthy body part (Body Integrity Identity Disorder; BIID
(Bayne and Levy, 2005; First, 2005)) perceive a conflict in the
body–self neuromatrix such that their physical body does
not converge with their phenomenological experience?
Would people with BIID perceive a phantom limb following
amputation and if so, would this differ from other
amputees without BIID? Seventh, why do some amputees
experience phantom pain when they observe another
person in pain (i.e., “empathic pain”), and does this relate
to how empathic one is? Finally, why do some amputees
 B RA I N RE SE A R CH RE V I EW S 54 ( 20 0 7 ) 2 1 9–2 3 2
perceive sensations in the phantom limb that mirrors those in
the intact limb? While the neuromatrix theory may be a very
adequate model for the complexity of phantom limb pain,
non-painful phantom sensations are likely to also be related
to other complex central processes involved in bodily percep-
tion, beyond the body schema. The latter include mirror
neuron systems – particularly those involving movement
(fronto-parietal mirror system), pain (anterior cingulate cortex
and anterior insula), and touch (somatosensory and posterior
parietal cortices) – and mechanisms of cross-referencing
between the phantom limb and intact limb (Giummarra et al.,
2006a).
4.4. Mirror neurons
4.4.1. Mirror neurons and action understanding
Mirror neurons have an integral role in the observation and
understanding of goal-directed actions between an agent and
an object (Gallese, 2001; Rizzolatti et al., 1988). Mirror neurons
were initially identified by Rizzolatti et al. (1988) in the ventral
premotor cortex in the macaque monkey. These neurons fired
not only while the monkey executed a goal-directed action,
but also when it observed another monkey, or the human
experimenter, perform the same goal-directed motor action.
Essentially, in order to understand the actions of others one
must match the action against one's own motor system,
simulating cortical activity in the same neurons that are
responsible for performing that action (Buccino et al., 2004;
Fadiga et al., 2005; Rizzolatti et al., 2002). Following the
discovery of mirror neurons in monkeys, similar mirror
neuron systems were identified in humans and were found
to result not only in action simulation in the motor cortex, but
also sub-threshold activity in muscles engaged in the
observed action (Fadiga et al., 2005). Essentially, activity in
mirror neuron systems enables the observer to embody the
other's motivational system.
Amputees with phantom sensations may provide evidence
that efficient action understanding requires a mirror neuron
system that retains a representation of an intact and
functioning body. Amputees may experience “somatic” or
“postural” empathy during mirror neuron activity when
observing others using their limbs (Price, 2006). This process
may evoke phantom limb perception, or even the perceived
embodiment of another's movements without apparent
phantom limb perception (Frank, 1986). Mirror neuron activity
may thus both require and reinforce the representation of the
body and its functions within the body schema—even if a limb
has been amputated, in which case activation of mirror
neurons may reinforce the representation of the phantom
limb. Phantom limb perception in cases of congenital limb loss
supports the possible role of mirror neurons in the retention of
a representation of the missing limb within the body schema
(Brugger, 2006; Brugger et al., 2000; Funk et al., 2006; Price,
2006). For example, the case of a 44-year-old amputee who was
born missing all four limbs, but who perceived vivid phantom
limbs (Brugger et al., 2000), suggests that phantom limb
perception may have evolved, at least in part, from the
habitual observation of other people moving their limbs, and
the continued activation of the innate body schema. While
these mechanisms may explain phantom limb perception
225
following congenital limb absence (Brugger, 2006; Brugger
et al., 2000; Price, 2006), we propose that they are also likely
to be central to the perception of phantom limbs following
acquired limb loss.
Future research. The role of mirror neurons in phantom limb
perception is only just beginning to receive attention, and
much work is required to clarify its role in congenital and
acquired limb loss. In particular, research should examine the
relationship between action understanding and phantom
limb perception and movement. For example, do amputees
differ with respect to action perception and embodiment of
another's motor system (i.e., mirror system activity) according
to (a) whether they perceive phantom pain, phantom sensa-
tions, or neither phantom pain or sensations; (b) whether they
perceive a “moveable” phantom limb compared with those
who perceive a phantom limb that is “paralysed”; and (c)
whether they use a prosthesis, the type of prosthesis used and
the perceived embodiment of the prosthesis.
4.4.2. Mirror neurons and empathy for pain in amputees
In addition to action understanding, mirror neurons are
involved in other domains of perception and perceptual under-
standing, including emotion (Ruby and Decety, 2004), disgust
(Wicker et al., 2003), touch (Keysers et al., 2004), and pain
(Jackson et al., 2005; Morrison et al., 2004; Singer et al., 2004).
For example, mirror neurons are likely to be responsible for
the instinct to cringe or shudder when observing another
person in pain (Miller, 2005). We propose that the mirror
neuron systems for touch and pain may be involved in
maintaining the representation of a phantom limb, and in
some cases triggering phantom pain.
Mirror systems for touch, in the secondary somatosensory
cortex, were identified by Keysers et al. (2004) in people who
were touched or observed another person or non-biological
object being touched. Synaesthesia for touch has also been
described in a single case study (Blakemore et al., 2005): using
functional Magnetic Resonance Imaging (fMRI), Blakemore et
al. (2005) investigated the neural networks involved in the
perception of touch in their synaesthete subject (C), and a
group of control subjects. Activations in the somatosensory
cortex were significantly higher in C, compared with controls,
when she observed touch. An area in the left premotor cortex
was activated in C to a greater extent than in the non-
synaesthetic group and the anterior insula cortex (AIC) was
bilaterally activated in C, but there was no evidence of such
activation in the non-synaesthetic group. The evidence
suggests that in C the mirror system for touch is disinhibited
and involves activity that exceeds the threshold for conscious
tactile perception.
When observing another person in pain, we not only
consciously comprehend that the other is in pain, but we also
automatically interpret the experience throughout the same
cortical networks that mediate personal experience of pain.
There is strong evidence that the AIC and the ACC are involved
in both the personal experience of pain and its empathic
experience (Jackson et al., 2005; Morrison et al., 2004; Singer et
al., 2004). These same areas, associated with processing
physical pain, also process feelings of “emotional pain”, such
as social rejection (Eisenberger et al., 2003) or frustration (Abler
et al., 2005). The level of activity in the ACC is strongly
226 B RA I N R E SE A R CH RE V I EW S 54 ( 20 0 7 ) 2 1 9–2 3 2
correlated with an observer's ratings of the intensity of
another's pain (Jackson et al., 2005). The ACC receives
projections from the superior temporal areas, which play a
role in semantic visual processing, and is probably involved in
the affective components of the “pain matrix” during empathy
for pain. The ACC has extensive outputs to the premotor and
motor areas (Morrison et al., 2004), and there are similar motor
action responses to a painful stimulus when it is either
personally experienced, or observed to be experienced by
another person (Avenanti et al., 2005). These findings suggest
that there is empathic inference of the sensory qualities of
another's pain, automatic embodiment of the observer's
motor system, and empathic activity in the autonomic
nervous system's “flight” mechanism during empathy for
pain.
Bradshaw and Mattingley (2001) reported the first clinical
case of feeling mirrored pain when observing another person
in pain. This hyperalgesic man reported that he felt pain that
was immediate and intense, and appeared to be qualitatively
similar to his own hypersensitivity to touch, when he saw his
wife hurt. Giummarra et al. (2006a) have described eight cases
who reported that their phantom pain is triggered by
observing, thinking about, or inferring that another person is
in pain. The neuromatrix theory may suggest that this is due
to triggering pain memories, or heightened activity in the
limbic system due to emotional distress. However, we propose
that it is also probable that empathically perceived pain in the
phantom limb involves mirror system activity within the “pain
matrix”, which maps the observed pain onto the body schema
(Giummarra et al., 2006a). This is a novel hypothesis and
requires further research; for example, using the methodology
of past studies that have examined mirror system activity for
observed and perceived pain (Singer et al., 2004). Through
mirror system activity, the sensory and affective qualities of
the other's pain would be embodied and mapped onto the
observer's body schema (Schwoebel et al., 2002), leading to an
empathic motivational state of readiness for action (Avenanti
et al., 2005). It is of significance that only lower limb amputees
have reported “mirror pain” (Giummarra et al., 2006a). The
experience of mirror pain only in the lower limb suggests
heightened activity of the autonomic nervous system, as a
result of embodiment of the other's fight or flight dilemma,
which is more likely to involve (a) the lower limbs in readiness
for flight from danger, and (b) the urogenital system through
the increased reflex urge to empty the bladder or bowels for
more efficient evasion of danger. Cortical reorganisation of the
lower limb onto the homuncular-adjacent genitals is also
associated with heightened phantom pain (Flor, 2002; Flor and
Birbaumer, 2000). The genitals are highly involved in emo-
tional perceptual processes (Both et al., 2003; van der Velde and
Everaerd, 2001), while the face – which is localised close to the
upper limbs in the somatosensory homunculus – plays an
emotionally expressive role. In summary, while there may be
mirror neuron activity in the pain matrix of non-amputees
and other healthy people without actual perception of pain, it
appears that the mirror neuron system in some people,
particularly lower limb amputees, may be disinhibited, lead-
ing to empathically perceived pain when another is in pain. In
amputees, mirrored pain may be perceived to be localised in
the stump and/or phantom limb, which has been pre-
sensitised, by trauma, to pain. While the possible mirror
system activity for the lower limbs is not well understood,
there is nevertheless some limited evidence for mirror-
neuron-like activity in the lower limbs (Buccino et al., 2005;
Bach and Tipper, 2007), despite the fact that they do not have a
repertoire of meaningful or operant activities that could be
involved in communicating, or understanding another's
intentions, which seems to be a major role for mirror neurons.
Future research. An important area of research includes
investigating the role of mirror systems for pain in amputees
who empathically feel phantom pain when observing another
person in pain. Experimental research should examine the
factors that predispose amputees towards experiencing
empathically triggered pain; for example (a) aspects of
traumatic experience; (b) whether sensitisation to pain is
generalised or specific to the amputated limb; or (c) whether
the other's pain is generalised or specific to the amputee's past
pain experiences. It is not clear whether amputees who have
observed injuries incurred by another person are more likely
to experience phantom pain in general. Empathically triggered
pain is likely to be present in other populations who have
experienced recent trauma, such as childbirth or third-degree
burn victims. For example, consider the case of a woman who
experienced a long painful childbirth, resulting in emergency
caesarean section delivery, who experiences shooting pain
from the groin that radiates down the legs when she is told of
another person's traumatic experience (unpublished case).
4.5. Cross referencing between the intact limb and the
phantom limb
4.5.1. Mirrored sensation and movement from the intact limb
to the phantom limb
While remapping and cortical reorganisation have received
considerable attention in the phantom pain literature (for
example, see reviews by Flor, 2002; Flor et al., 2006), the role of
transcallosal cross-referencing between the phantom limb
and the intact limb has received somewhat less attention. The
present review will focus on the perception of mirrored
sensation and movement from the intact to the phantom
limb. Giummarra et al. (2006a) reported that 13% of their
patients experienced phantom sensations that mirrored
sensations from the intact limb, including: ache, pain or
injury; neuropathy or disability; posture/form; temperature;
touch and exteroception; itching and the ability to ease itch,
discomfort or pain in the phantom by scratching or rubbing
the contralateral limb; and mirror movements. Mirror move-
ments have been described in an upper limb amputee during
passive and active movement of the intact hand (Halligan et
al., 1995a), and in one patient with a supernumerary “alien”
limb subsequent to callosal lesion during active movement
only (Hari et al., 1998; McGonigle et al., 2002). Haigh et al. (2003)
examined the phantom sensations in amputees who had been
diagnosed with rheumatoid arthritis (RA) prior to amputation.
These patients described sensations in the phantom that
mirrored the RA symptoms perceived in the intact leg,
including stiffness and limited ability to move the joints
freely, clawing of the toes, swelling in the ankle and/or knee,
and a desire to exercise the limb. Franz and Ramachandran
(1998) provide evidence that the phantom hand remains
 B RA I N RE SE A R CH RE V I EW S 54 ( 20 0 7 ) 2 1 9–2 3 2
spatially coupled with the intact hand following amputation,
as long as the amputee can conduct voluntary movements in
the phantom.
Animal studies have shown that deafferentation is fol-
lowed by rapid cortical reorganisation contralateral to the
deafferented limb (Donoghue et al., 1990; Sanes et al., 1988).
These findings have been replicated in human studies (Brasil-
Neto et al., 1993; Ziemann et al., 1998), together with evidence
that the motor cortex ipsilateral to the deafferented limb
undergoes cortical reorganisation (Schwenkreis et al., 2003).
Cortical reorganisation following deafferentation is thought to
be based on various mechanisms, including unmasking of pre-
existing synapses by removal of local inhibition, strengthen-
ing of existing synapses in processes such as long-term
potentiation, changes in neuronal membrane excitability,
and axonal sprouting with the formation of new synapses
(Schwenkreis et al., 2003). Amputees who use a functional
prosthesis (Cruz et al., 2003; Hamzei et al., 2001), particularly a
myoelectric prosthesis (Lotze et al., 2001), exhibit less cortical
reorganisation, highlighting that cortical reorganisation may
be use-dependent.
Cross-referencing mechanisms, either at the spinal or
supraspinal level, clearly continue to function even after
deafferentation, particularly in amputees who can execute
voluntary phantom limb movements. The peripheral path-
ways involved in bimanual motor coupling endure in ampu-
tees, such that movement of a phantom limb corresponds to
the activation of motor neurons that once served the missing
hand, which reinnervate the stump muscles (Mercier et al.,
2006). Centrally, cross-referencing of the phantom limb to the
intact, contralateral limb may be related to the disinhibition
and strengthening of pre-existing commissural connections
between the cortical representation of the two limbs. Ordina-
rily, these neural pathways are recruited to enhance perfor-
mance of bimanual movements, and recruit local inhibitory
interneurons during unimanual or antiphase movements
(Carson, 2005). Unilateral movements – particularly move-
ments that are rapid and repetitive or involve force and effort –
are associated with an increase in the regional cerebral blood
flow in the ipsilateral motor cortex (Carson, 2005; Kew et al.,
1994), and enhanced interhemispheric interaction of the non-
dominant hemisphere onto the dominant hemisphere
(Kobayashi et al., 2003). Following amputation or deafferenta-
tion, the perception of “referred” or mirrored sensation from
the intact to the phantom limb may be related to altered
inhibitory mechanisms in these ipsilateral pathways, parti-
cularly during high-threshold somatosensory or motor
afferents.
4.5.2. Experimentally induced sensory and motor coupling
between the phantom and real limb
Illusions of touch and movement can be evoked in a phantom
limb, inducing somatosensory and/or motor coupling between
the phantom and real limb, using the additional sense of
vision with mirror feedback (Ramachandran, 1996; Ramachan-
dran et al., 1995). In the mirror box paradigm, a mirror is
positioned vertically in the centre of a box, the amputated
limb and “phantom” are placed on one side out of view, and
the intact limb is placed so that the amputee can see its
reflection. During mirror therapy, the amputee observes the
227
reflection of his normal limb moving in the mirror in order to
induce the visual illusion that he has two intact limbs and that
the intact limb is superimposed onto the felt position of his
phantom limb (Ramachandran, 1996). Ramachandran et al.
(1995) reported that upper limb amputees who used this
technique feel their phantom arm move when they observe
their own arm, or the arm of the experimenter, move in the
mirror. Four out of five of the amputees tested who had
“clenching” spasms in their phantom limbs found instant
relief upon looking into the mirror and opening “both” hands
simultaneously. Ramachandran and Rogers-Ramachandran
(1996) examined intermanual referral in 10 upper limb
amputees using the mirror box paradigm, and found that (a)
three amputees perceived referred sensation that was topo-
graphically organised such that touching the intact thumb
elicited referred touch in the phantom thumb; (b) the referral
of touch, but not temperature or pain; (c) enhanced effects
when mirror feedback was used to give the illusion of touching
the phantom hand; (d) movements of the real hand – either
passively or actively – were referred to the phantom hand in
six amputees; and (e) referral was reported from the intact
hand and forearm up to a level corresponding to the
amputation of the other arm. Sathian (2000) also reported
the intermanual referral of sensation to a hand rendered
anaesthetic by stroke or surgery using the mirror box
paradigm; however, these patients perceived “referred” sen-
sation as pressure in the hidden, anaesthetic hand, regardless
of the type of stimulation of the good hand, which included
pain, cold, vibration or joint movement. Sathian (2000)
proposed that following decreased somatosensory input
from the anaesthetic hand, the neurons that correspond to
the anaesthetic hand may become disinhibited and respon-
sive to input from the ipsilateral hand, input which, during
moderately intense tactile stimulation, exceeds perceptual
threshold resulting in the perception of referred sensation.
Mirror box therapy has now been successfully used in both
upper (Oakley et al., 2002; Ramachandran, 1996) and lower limb
(Brodie et al., 2003; MacLachlan et al., 2004b) amputees to assist
in voluntary movement of the phantom limb and alleviation of
phantom pain, and in some cases apparently causing the
phantom limb to telescope (Ramachandran et al., 1995).
Perceived illusions in the phantom limb are reported to be so
realistic that amputees claim they can see and feel their
phantom limb moving as if it was under their volitional control
(Ramachandran, 1996). Mirror box therapy has also been used
by patients in the early and intermediate stages of Complex
Regional Pain Syndrome (CRPS, type 1) to reduce pain
associated with movement of the affected limb (McCabe et
al., 2003). Conversely, Acerra and Moseley (2005) found that
pain and paraesthesia could be induced in the affected limb of
patients with CPRS (type 1) when corresponding areas of the
unaffected limb were passively stimulated and observed in the
mirror as if superimposed onto the affected limb. These
findings suggest that pain – at least pain associated with
amputation and CRPS (type 1) – may be related to (a) mapping
observed stimulation onto the body schema, already modified
by disease or pain, and (b) a mismatch or reafference (efference
copy) between intention to move the phantom limb and the
lack of proprioceptive feedback from the deafferented limb.
Creating the illusion of convergence between sensory systems
228 B RA I N R E SE A R CH RE V I EW S 54 ( 20 0 7 ) 2 1 9–2 3 2
and efference copy may restore sensory and motor schemas
of the body (Harris, 1999; McCabe et al., 2003; Ramachandran
and Rogers-Ramachandran, 1996).
Viewing a mirror reflection of one's hand conducting
unilateral finger–thumb opposition movements, in normals,
facilitates activity in the ipsilateral motor cortex (Garry et al.,
2005) and may indicate that commissural pathways are
involved in evoking visual “capture” through mirror reflection,
probably via reduced intracortical inhibition. Illusory “phan-
tom” movements in the paretic arm of right-brain stroke
patients have been reported during mirror feedback of the
normal right limb (Zampini et al., 2004), again suggesting that
the visual capture phenomenon is related to the dominance of
vision over somatic senses such as proprioception. This
technique has important treatment implications not only for
reducing levels of phantom pain in amputees, and movement-
related pain in CRPS (type 1), but also for restoring motor
function following stroke. When stroke patients view the
mirror reflection of the good limb superimposed onto the
paretic limb, they would not only perceive the illusion of
enhanced movement of the impaired limb, but could also
trigger and restore neural activity in the deafferented motor
cortex.
Future research. The investigation of cross-referencing the
phantom limb with other parts of the body is an area of
research that has received little attention to date, but could be
both theoretically and clinically invaluable. Future research
should investigate the relative role of internal global con-
structs of the body (the body schema), cross-callosal and
ipsilateral pathways on the perception of mirrored sensations
and movement in the phantom limb. Research on cross-
referencing of movement execution and perception could
examine (a) motor overflow (Addamo et al., 2007; Hoy et al.,
2004) from the intact limb to the residual portion of the
amputated limb measured by EMG (Dennis, 1976; Green, 1967)
or overflow of force (Armatas and Summers, 2001); (b) motor
overflow from the intact limb to the phantom limb measured
by fMRI; (c) mirror movements perceived in the phantom limb
following movement of the intact limb; or (d) motor overflow
from imagined phantom movement to the intact limb
measured by EMG or force overflow.
5. Conclusions
Research on non-painful phantom limbs provides valuable
insight to the mechanisms underlying bodily awareness and
embodiment. The body schema most likely provides the
template for phantom limb perception, particularly consider-
ing the complexity of phantom limb sensations (notably,
proprioception, kinaesthesia, and kinetics), the nature of the
triggers of phantom sensations and pain (e.g., referred
sensations, vestibular stimulation, and visual capture through
the mirror box paradigm), and the likely role of phantom limb
perception in prosthesis use and embodiment. The neuroma-
trix – which inter-relates sensory-discriminative, affective-
motivational and evaluative-cognitive dimensions of bodily
experience – provides a functional model for phantom limb
perception, and phantom pain. We propose that specific
central processes beyond the body schema and neuromatrix
are also involved in phantom limb perception, and require
further research. First, the activation and disinhibition of
various mirror neuron systems – including systems involved
in action understanding, and empathy for touch and empathy
for pain – may both reinforce and require the representation of
the phantom limb in the body schema. Second, the potential
mechanisms underlying the interaction between the phantom
limb and the intact limb require clarification; in particular, the
relative roles of the global body schema, transcallosal and
ipsilateral projections. With the likely involvement of the body
schema and neuromatrix, mirror neuron systems, and trans-
callosal and ipsilateral cross-referencing in phantom limb
phenomena, the perception of a “normal” (non-painful)
phantom limb is in the very least an epiphenomenon of
normal functioning, action understanding and empathy, and
potentially even evolutionarily adaptive and perhaps necessary.
Phantom pain, on the other hand, may be a maladaptive
failure of the neuromatrix to maintain global bodily
constructs.
Acknowledgments
We would like to acknowledge the two anonymous reviewers
who provided invaluable feedback on an earlier draft of the
manuscript.
REFERENCES
Abler, B., Walter, H., Erk, S., 2005. Neural correlates of frustration.
NeuroReport 16, 669–672.
Acerra, N.E., Moseley, G.L., 2005. Dysynchiria: watching the mirror
image of the unaffected limb elicits pain on the affected side.
Neurology 65, 751–753.
Addamo, P.K., Farrow, M., Hoy, K., Bradshaw, J.L.,
Georgiou-Karistianis, N., 2007. The effects of age and attention
on motor overflow production—a review. Brain Res. Rev. 54,
189–204.
Aglioti, S., Cortese, F., Franchini, C., 1994. Rapid sensory
remapping in the adult human brain as inferred from phantom
breast perception. NeuroReport 5, 473–476.
Aglioti, S., Smania, N., Manfredi, M., Berlucchi, G., 1996.
Disownership of left hand and objects related to it in a patient
with right brain damage. NeuroReport 8, 293–296.
André, J.M., Martinet, N., Paysant, J., Beis, J.M., Le Chapelain, L.,
2001. Temporary phantom limbs evoked by vestibular caloric
stimulation in amputees. Neuropsychiatry Neuropsychol.
Behav. Neurol. 14, 190–196.
Arcadi, J.A., 1977. ‘Phantom bladder’: is this an unusual entity?
J. Urol. 118, 354.
Armatas, C.A., Summers, J.J., 2001. The influence of task
characteristics on the intermanual asymmetry of motor
overflow. J. Clin. Exp. Neuropsychol. 23, 557–567.
Armel, K.C., Ramachandran, V.S., 2003. Projecting sensations to
external objects: evidence from skin conductance response.
Proc. R. Soc. Lond., B Biol. Sci. 270, 1499–1506.
Arzy, S., Overney, L.S., Landis, T., Blanke, O., 2006. Neural
mechanisms of embodiment: asomatognosia due to premotor
cortex damage. Arch. Neurol. 63, 1022–1025.
Avenanti, A., Bueti, D., Galati, G., Aglioti, S.M., 2005. Transcranial
magnetic stimulation highlights the sensorimotor side of
empathy for pain. Nat. Neurosci. 8, 955–960.
 B RA I N RE SE A R CH RE V I EW S 54 ( 20 0 7 ) 2 1 9–2 3 2
Bach, P., Tipper, S.P., 2007. Implicit action encoding influences
personal-train judgements. Cognition 102, 151–178.
Bayne, T., Levy, N., 2005. Amputees by choice: body integrity
identity disorder and the ethics of amputation. J. Appl. Philos.
22, 75–86.
Berlucchi, G., Aglioti, S., 1997. The body in the brain: neural bases
of corporeal awareness. Trends Neurosci. 12, 560–564.
Biley, F.C., 2001. Phantom bladder sensations: a new concern for
stoma care workers. Br. J. Nurs. 10, 1290–1296.
Bittar, R.G., Otero, S., Carter, H., Aziz, T.Z., 2005. Deep brain
stimulation for phantom limb pain. J. Clin. Neurosci. 12,
399–404.
Blakemore, S.-J., Bristow, D., Bird, G., Frith, C., Ward, J., 2005.
Somatosensory activations during the observation of touch
and a case of vision–touch synaesthesia. Brain 128, 1571–1583.
Blanke, O., 2004. Out of body experiences and their neural basis. Br.
Med. J. 329, 1415–1416.
Blanke, O., Arzy, S., 2005. The out-of-body experience: disturbed
self-processing at the temporo-parietal junction.
Neuroscientist 11, 16–24.
Bors, E., 1951. Phantom limbs in patients with spinal cord injury.
Arch. Neurol. Psychiatry 66, 610–631.
Both, S., Everaerd, W., Laan, E., 2003. Modulation of spinal reflexes
by aversive and sexually appetitive stimuli. Psychophysiology
40, 174–183.
Botvinick, M., Cohen, J., 1998. Rubber hands ‘feel’ touch that eyes
see. Nature 391, 756.
Bradshaw, J.L., Mattingley, J.B., 2001. Allodynia: a sensory
analogue of motor mirror neurons in a hyperaesthetic patient
reporting instantaneous discomfort to another's perceived
sudden minor injury? J. Neurol., Neurosurg. Psychiatry 70,
135–140.
Brasil-Neto, J.P., Valls-Solé, J., Pascul-Leone, A., Cammarota, A.,
Amassian, V.E., Cracco, R., Maccabee, P., Cracco, J., Hallett,
M., Cohen, L., 1993. Rapid modulation of human critical
motor outputs following ischaemic nerve block. Brain 116,
511–525.
Braun, M., Le Chapelain, L., Beis, J.M., Opincariu, J., Andre, J.M.,
2001. Feet dorsal imaginary flexion in paraplegic patients: fMRI
of motor areas before and through vestibular stimulation.
NeuroImage 13, S1135.
Brena, S.F., Sammons, E.E., 1979. Phantom urinary bladder
pain—case report. Pain 7, 197–201.
Bressler, B., Cohen, S.I., Magnussen, F., 1955. Bilateral breast
phantom and breast phantom pain. J. Nerv. Ment. Dis. 122,
315–320.
Brodie, E.E., Whyte, A., Waller, B., 2003. Increased motor control of
a phantom leg in humans results from the visual feedback of a
virtual leg. Neurosci. Lett. 341, 167–169.
Bromage, P.R., Melzack, R., 1974. Phantom limbs and the body
schema. Can. Anaesth. Soc. J. 21, 267–274.
Brugger, P., 2003. Supernumerary phantoms: a comment on
Grossi, et al's (2002) spare thoughts on spare limbs. Percept.
Mot. Skills 97, 3–10.
Brugger, P., 2006. From phantom limb to phantom body: varieties
of extracorporeal awareness. In: Knoblich, G., THornton, I.M.,
Grosjean, M., Shiffrar, M. (Eds.), Human Body Perception from
the Inside Out. Oxford Univ. Press, New York, pp. 171–210.
Brugger, P., Regard, M., Landis, T., 1997. Illusory reduplication of
one's own body: phenomenology and classification of
autoscopic phenomena. Cogn. Neuropsychiatry 2, 19–38.
Brugger, P., Kollias, S.S., Müri, R.M., Crelier, G., Hepp-Reymond,
M.-C., 2000. Beyond re-membering: phantom sensations of
congenitally absent limbs. Proc. Natl. Acad. Sci. U. S. A. 97,
6167–6172.
Buccino, G., Binkofski, F., Riggio, L., 2004. The mirror neuron
system and action recognition. Brain Lang. 89, 370–376.
Buccino, G., Riggio, L., Melli, G., Binkofski, F., Gallese, V., Rizzolatti,
G., 2005. Listening to action-related sentences modulates the
229
activity of the motor system: a combined TMS and behavioural
study. Cogn. Brain Res. 24, 355–363.
Carlen, P.L., Wall, P.D., Nadvorna, H., Steinbach, T., 1978. Phantom
limbs and related phenomena in recent traumatic
amputations. Neurology 28, 211–217.
Carson, R.G., 2005. Neural pathways mediating bilateral
interactions between the upper limbs. Brain Res. Rev. 49,
641–662.
Cherng, C.-H., Wong, C.-S., Ho, S.-H., Chang, C.-J., 2001.
Prevalence and clinical characteristics of phantom rectum
syndrome after rectum resection in Chinese patients. Pain
Clin. 13, 113–117.
Conomy, J.P., 1973. Disorders of body image after spinal cord
injury. Neurology 23, 842–850.
Craske, B., 1977. Perception of impossible limb positions induced
by tendon vibration. Science 196, 71–73.
Cruz, V.T., Nunes, B., Reis, A.M., Pereira, J.R., 2003. Cortical
mapping in amputees and dysmelic patients: a functional MRI
study. NeuroRehabilitation 18, 299–305.
Dennis, M., 1976. Impaired sensory and motor differentiation with
corpus callosum agenesis: a lack of callosal inhibition during
ontogeny. Neuropsychologia 14, 455–469.
Devor, M., 1997. Phantom limb phenomena and their neural
mechanism. In: Myslobodsky, M.S. (Ed.), The Mythomanias:
The Nature of Deception and Self-deception, pp. 237–361.
Donoghue, J.P., Suner, S., Sanes, J.M., 1990. Dynamic organization
of primary motor cortex output to target muscles in adult rats:
II. Rapid reorganization following motor nerve lesions. Exp.
Brain Res. 79, 492–503.
Ehrsson, H.H., Spence, C., Passingham, R.E., 2004. That's my hand!
Activity in premotor cortex reflects feeling of ownership of a
limb. Science 305, 875–877.
Eisenberger, N.I., Lieberman, M.D., Williams, K.D., 2003. Does
rejection hurt? An fMRI study of social exclusion. Science 302,
290–292.
Ettlin, T.M., Seiler, W., Kaeser, H.E., 1980. Phantom and
amputation illusions in paraplegic patients. Eur. Neurol. 19,
12–19.
Fadiga, L., Craighero, L., Olivier, E., 2005. Human motor cortex
excitability during the perception of others' action. Curr. Opin.
Neurobiol. 15, 213–218.
Farley, D., Smith, I., 1968. Phantom rectum after complete rectal
excision. Br. J. Surg. 55, 40.
First, M.B., 2005. Desire for amputation of a limb: paraphilia,
psychosis, or a new type of identity disorder. Psychol. Med. 35,
919–928.
Fisher, C.M., 1999. Phantom erection after amputation of penis.
Case description and review of relevant literature on
phantoms. Can. J. Neurol. Sci. 26, 53–56.
Flor, H., 2002. Phantom limb pain. In: Ramachandran, V.S. (Ed.),
Encyclopedia of the Human Brain, vol. 3. Academic Press,
New York, pp. 831–841.
Flor, H., Birbaumer, N., 2000. Phantom limb pain: cortical plasticity
and novel therapeutic approaches. Curr. Opin. Anaesthesiol.
13, 561–564.
Flor, H., Denke, C., Schaefer, M., Grüsser, S., 2001. Effect of sensory
discrimination training on cortical reorganization and
phantom limb pain. Lancet 357, 1763–1764.
Flor, H., Nikolajsen, L., Jensen, T.S., 2006. Phantom limb pain: a
case of maladaptive CNS plasticity. Nat. Rev., Neurosci. 7,
873–881.
Frank, G., 1986. On embodiment: a case study of congenital limb
deficiency in American culture. Cult. Med. Psychiatry 10,
189–219.
Franz, E.A., Ramachandran, V.S., 1998. Bimanual coupling in
amputees with phantom limbs. Nat. Neurosci. 1, 443–444.
Fraser, C., 2002. Fact and fiction: a clarification of phantom limb
phenomena. Br. J. Occup. Ther. 65, 256–260.
Funk, M., Shiffrar, M., Brugger, P., 2006. Hand movement
230 B RA I N R E SE A R CH RE V I EW S 54 ( 20 0 7 ) 2 1 9–2 3 2
observation by individuals born without hands: phantom limb
experience constrains visual limb perception. Exp. Brain Res.
164, 341–346.
Gallagher, S., 1986. Body image and body schema: a conceptual
clarification. J. Mind Behav. 7, 541–554.
Gallagher, P., Butterworth, G.E., Lew, A., Cole, J., 1998. Hand–mouth
coordination, congenital absence of limb, and evidence for
innate body schemas. Brain Cogn. 38, 53–65.
Gallese, V., 2001. The ‘shared manifold’ hypothesis — from mirror
neurons to empathy. J. Conscious. Stud. 8, 33–50.
Garry, M.I., Loftus, A., Summers, J.J., 2005. Mirror, mirror on the
wall: viewing a mirror reflection of unilateral hand movements
facilitates ipsilateral M1 excitability. Exp. Brain Res. 163,
118–122.
Giummarra, M.J., Georgiou-Karistianis, N., Gibson, S.J., Chou, M.,
Bradshaw, J.L., 2006a. The menacing phantom: what triggers
phantom limb pain and why? Australasian Winter Conference
on Brain Research, Queenstown, New Zealand.
Giummarra, M.J., Georgiou-Karistianis, N., Nicholls, E.R., Gibson,
S.J., Chou, M., Stone, K., Bradshaw, J.L., 2006b. Embodied pain:
the interaction between prosthesis use and phantom pain.
30th Annual Scientific Meeting of the International Society for
Prosthetics and Orthotics, Australian National Member
Society, Fremantle, WA.
Gow, D., MacLachlan, M., Aird, C., 2004. Reaching with electricity:
externally powered prosthetics and embodiment. In:
MacLachlan, M., Gallagher, P. (Eds.), Enabling Technologies:
Body Image and Body Function. Churchill Livingstone,
Edinburgh, pp. 155–168.
Green, J.B., 1967. An electromyographic study of mirror
movements. Neurology 17, 91–94.
Gross, Y., Melzack, R., 1978. Body image: dissociation of real and
perceived limbs by pressure-cuff ischemia. Exp. Neurol. 61,
680–688.
Haigh, R.C., McCabe, C.S., Halligan, P.W., Blake, D.R., 2003. Joint
stiffness in a phantom limb: evidence of central nervous
system involvement in rheumatoid arthritis. Rheumatology 42,
888–892.
Halligan, P.W., 1999. Phantoms in the brain. Br. Med. J. 319,
587–588.
Halligan, P.W., Marshal, J.C., Wade, D.T., 1995a. Sensory
disorganization and perceptual plasticity after limb
amputation: a follow up study. NeuroReport 5, 1341–1345.
Halligan, P.W., Marshal, J.C., Wade, D.T., 1995b. Unilateral
somatoparaphrenia after right hemisphere stroke: a case
description. Cortex 31, 173–182.
Hamzei, F., Liepert, J., Dettmers, C., Adler, T., Kiebel, S., Rijntjes, M.,
Weiller, C., 2001. Structural and functional cortical
abnormalities after upper limb amputation during childhood.
NeuroReport 12, 957–962.
Hari, H., Hänninen, R., Mäkinen, T., Veikko, J., Forss, N., Seppä, M.,
Salonen, O., 1998. Three hands: fragmentation of human bodily
awareness. Neurosci. Lett. 240, 131–134.
Harris, A.J., 1999. Cortical origin of pathological pain. Lancet 354,
1464–1466.
Head, H., Holmes, G., 1911–1912. Sensory disturbances from
cerebral lesions. Brain 34, 102–254.
Helmholtz, H., 1995. Science and Culture: Popular and
Philosophical Essays. University of Chicago Press, Chicago.
Henderson, W.R., Smyth, G.E., 1948. Phantom limbs. J. Neurol.,
Neurosurg. Psychiatry 11, 88–112.
Hill, A., 1999. Phantom limb pain: a review of the literature on
attributes and potential mechanisms. J. Pain Symp. Manag. 17,
125–142.
Holmes, N.P., Spence, C., 2006. Beyond the body: visual, prosthetic,
and technological contributions to bodily perception and
awareness. In: Knoblich, G., THornton, I.M., Grosjean, M.,
Shiffrar, M. (Eds.), Human Body Perception from the Inside Out.
Oxford Univ. Press, New York, pp. 15–64.
Hoy, K.E., Fitzgerald, P.B., Bradshaw, J.L., Armatas, C.A.,
Georgiou-Karistianis, N., 2004. Investigating the cortical origins
of motor overflow. Brain Res. Rev. 46, 315–327.
Hunter, J.P., Katz, J., Davis, K.D., 2003. The effect of tactile and
visual sensory inputs on phantom limb awareness. Brain 126,
579–589.
Iriki, A., Tanaka, M., Iwamura, Y., 1996. Coding modified body
schema during tool use by macaque postcentral neurones.
NeuroReport 7, 2325–2330.
Jackson, P.L., Meltzoff, A.N., Decety, J., 2005. How do we perceive
the pain of others? A window into the neural processes
involved in empathy. NeuroImage 24, 771–779.
Jamison, K., Wellisch, D.K., Katz, R.K., Pasnau, R.O., 1979. Phantom
breast syndrome. Arch. Surg. 114, 93–95.
Jones, L.A., 1988. Motor illusions: what do they reveal about
proprioception? Psychol. Bull. 103, 72–86.
Katz, J., 1992. Psychophysiological contributions to phantom
limbs. Can. J. Psychiatry 37, 282–298.
Katz, J., Melzack, R., 1990. Pain ‘memories’ in phantom limbs:
review and clinical observations. Pain 43, 319–336.
Kew, J.J.M., Ridding, M.C., Rothwell, J.C., Leigh, P., Passingham, R.E.,
Sooriakumaran, S., Frackowiak, R.S.J., Brooks, D.J., 1994.
Reorganization of cortical blood flow and transcranial
magnetic stimulation maps in human subjects after upper
limb amputation. J. Neurophysiol. 72, 2517–2524.
Kew, J., Wright, A., Halligan, P.W., 1998. Somesthetic aura: the
experience of “Alice in Wonderland”. Lancet 351, 1934.
Keysers, C., Wicker, B., Gazzola, V., Anton, J.L., Fogassi, L., Gallese,
V., 2004. A touching sight: SII/PV activation during the
observation and experience of touch. Neuron 42, 335–346.
Kobayashi, M., Hutchinson, S., Schlaug, G., Pascual-Leone, A., 2003.
Ipsilateral motor cortex activation on functional magnetic
resonance imaging during unilateral hand movements is
related to interhemispheric interactions. NeuroImage
2259–2270.
Kooijman, C.M., Dijkstra, P.U., Geertzen, J.H.B., Elzinga, A., van der
Schans, C.P., 2000. Phantom pain and phantom sensations in
upper limb amputees: an epidemiological study. Pain 87, 33–41.
Lackner, J.R., 1988. Some proprioceptive influences on the
perceptual representation of body shape and orientation. Brain
111, 281–297.
Lackner, J.R., Taublieb, A.B., 1983. Reciprocal interactions between
the position sense representations of the 2 forearms.
J. Neurosci. 3, 2280–2285.
Le Chapelain, L., Beis, J.-M., André, J.-M., 2001. Vestibular caloric
stimulation evokes phantom limb illusions in patients with
paraplegia. Spinal Cord 39, 85–87.
Lewis, J.W., 2006. Cortical networks related to human use of tools.
Neuroscientist 12, 211–231.
Lotze, M., Grodd, W., Birbaumer, N., Erb, M., Huse, E., Flor, H., 1999.
Does use of a myoelectric prosthesis prevent cortical
reorganization and phantom limb pain? Nat. Neurosci. 2,
501–502.
Lotze, M., Flor, H., Grodd, W., Larbig, W., Birbaumer, N., 2001.
Phantom movements and pain: an fMRI study in upper limb
amputees. Brain 124, 2268–2277.
Machin, P., Williams, A., 1998. A stiff upper lip: coping strategies of
World War II veterans with phantom limb pain. Clin. J. Pain 14,
290–294.
MacLachlan, M., Allen, D., Desmond, D., O'Neill, K., de Paor, A.,
McDarby, G., Halligan, P., 2004a. Virtual reality, phantom limb
pain and prosthetic embodiment: the development of
phenomenologically authentic virtual reality technology for
treatment of phantom limb pain and adaptation to a prosthetic
limb. Annual Conference of the American Academy of
Orthotists and Prosthetists, New Orleans.
MacLachlan, M., McDonald, D., Waloch, J., 2004b. Mirror treatment
of lower limb phantom pain: a case study. Disabil. Rehabil. 26,
901–904.
 B RA I N RE SE A R CH RE V I EW S 54 ( 20 0 7 ) 2 1 9–2 3 2
Maravita, A., 2006. From “body in the brain” to “body in space”:
sensory and intentional components of body representation.
In: Knoblich, G., THornton, I.M., Grosjean, M., Shiffrar, M. (Eds.),
Human Body Perception from the Inside Out. Oxford Univ.
Press, New York, pp. 65–88.
Maravita, A., Spence, C., Driver, J., 2003. Multisensory integration
and the body schema: close to hand and within reach. Curr.
Biol. 13, R531–R539.
Marbach, J.J., 1993. Is phantom tooth pain a deafferentation
(neuropathic) syndrome? Oral Surg. Oral Med. Oral Pathol. Oral
Radiol. Endo. 75, 95–105.
Mazzoni, M., Lucchini, C., Meucci, G., Vista, M., Moretti, P., Sartucci,
F., 1997. Supernumerary phantom limb after ischaemic stroke.
Neurocase 3, 223–230.
McCabe, C.S., Haigh, R.C., Ring, E.F.J., Halligan, P., Wall, P.D., Blake,
D.R., 2003. A controlled pilot study of the utility of mirror visual
feedback in the treatment of complex regional pain syndrome
(type 1). Rheumatology 42, 97–101.
McDonnell, P.M., Scott, R.N., Dickison, J., Theriault, R.A., Wood, B.,
1989. Do artificial limbs become part of the user? New
evidence. J. Rehabil. Res. Dev. 26, 17–24.
McGonigle, D.J., Hanninen, R., Salenius, S., Hari, R., Frackowiak,
R.S.J., Frith, C.D., 2002. Whose arm is it anyway? An fMRI case
study of supernumerary phantom limb. Brain 125, 1265–1274.
Melzack, R., 1989. Phantom limbs: the self and the brain (The D.O.
Hebb Memorial Lecture). Can. Psychol. 30, 1–16.
Melzack, R., 1990. Phantom limbs and the concept of a
neuromatrix. Trends Neurosci. 13, 88–92.
Melzack, R., 1992. Phantom limbs. Sci. Am. 266, 120–126.
Melzack, R., 1996. Gate control theory: on the evolution of pain
concepts. Pain Forum 5, 128–138.
Melzack, R., 1999. From the gate to the neuromatrix. Pain, Suppl. 6,
S121–S126.
Melzack, R., Bromage, P.R., 1973. Experimental phantom limbs.
Exp. Neurol. 39, 261–269.
Melzack, R., Isreal, R., Lacroix, R., Schultz, G., 1997. Phantom limbs
in people with congenital limb deficiency or amputation in
early childhood. Brain 120, 1603–1620.
Mercier, C., Reilly, K.T., Vargas, C.D., Aballea, A., Sirigu, A., 2006.
Mapping phantom movement to representations in the motor
cortex of amputees. Brain 129, 2202–2210.
Mikulis, D.J., Jurkiewicz, M.T., McIlroy, W.E., Staines, W.R.,
Rickards, L., Kalsi-Ryan, S., Crawley, A.P., Fehlings, M.G.,
Verrier, M.C., 2002. Adaptation in the motor cortex following
cervical spinal cord injury. Neurology 58, 794–801.
Miller, G., 2005. Reflecting on another's mind. Science 308,
945–947.
Miyazawa, N., Hayashi, M., Komiya, K., Akiyama, I., 2004.
Supernumerary phantom limbs associated with left
hemisphere stroke: case report and review of the literature.
Neurosurgery 54, 228–231.
Moore, C.I., Stern, C.E., Dunbar, C., Kostyk, S.K., Gehi, A., Corkins,
S., 2000. Referred phantom sensations and cortical
reorganization after spinal injury in humans. Proc. Natl. Acad.
Sci. U. S. A. 97, 14703–14708.
Morrison, I., Lloyd, D., Di Pellegrino, G., 2004. Vicarious responses
to pain in anterior cingulate cortex: is empathy a multisensory
issue? Cognitive Affect. Behav. Neurosci. 4, 270–278.
Murray, C.D., 2004. An interpretative phenomenological analysis
of the embodiment of artificial limbs. Disabil. Rehabil. 26,
963–973.
Murray, C.D., Fox, J., 2002. Body image and prosthesis satisfaction
in the lower limb amputee. Disabil. Rehabil. 24, 925–931.
Oakley, D.A., Whitman, L.G., Halligan, P.W., 2002. Hypnotic
imagery as a treatment for phantom limb pain: two case
reports and a review. Clin. Rehabil. 16, 368–377.
Ovesen, P., Kroner, K., Ornsholt, J., Bach, K., 1991. Phantom-related
phenomena after rectal amputation: prevalence and clinical
characteristics. Pain 44, 289–291.
231
Poeck, K., 1964. Phantoms following amputation in early
childhood and in congenital absence of limbs. Cortex 1,
269–275.
Price, D.B., 1976. Phantom limb phenomena in patients with
leprosy. J. Nerv. Ment. Dis. 163, 108–116.
Price, E.H., 2006. A critical review of congenital phantom limb
cases and a developmental theory for the basis of body image.
Conscious. Cogn. 15, 310–322.
Ramachandran, V.S., 1996. Phantom limbs, neglect syndromes,
repressed memory and Freudian psychology. In: Sporns, O.,
Tonini, G. (Eds.), Selectionism and the Brain. International
Review of Neurobiology, vol. 37, pp. 291–333.
Ramachandran, V.S., Hirstein, W., 1998. The perception of
phantom limbs: the D.O. Hebb lecture. Brain 121, 1603–1630.
Ramachandran, V.S., Rogers-Ramachandran, D., 1996.
Synaesthesia in phantom limbs induced with mirrors. Proc. R.
Soc. Lond., B Biol. Sci. 263, 377–386.
Ramachandran, V.S., Rogers-Ramachandran, D., Cobb, S., 1995.
Touching the phantom limb. Nature 377, 489–490.
Riddoch, G., 1941. Phantom limbs and body shape. Brain 64,
197–222.
Rinehart, N., Chua, P., Bradshaw, J.L., in press. Processes and
mechanisms in neuropsychiatry: motor-executive processes.
In: S. Wood, N. Allen, C. Pantelis (Eds.), Handbook of
Neuropsychology of Mental Illness, Cambridge Univ. Press,
Cambridge.
Rizzolatti, G., Camarda, R., Fogassi, L., Gentilucci, M., Luppino, G.,
Matelli, M., 1988. Functional organization of inferior area 6 in
the macaque monkey: II. Area F5 and the control of distal
movements. Exp. Brain Res. 71, 491–507.
Rizzolatti, G., Craighero, L., Fadiga, L., 2002. The mirror system in
humans. In: Stamenov, M.I., Gallese, V. (Eds.), Mirror Neurons
and the Evolution of Brain and Language, vol. 42. John
Benjamins Publishing Company, Amsterdam, pp. 37–59.
Romani, M., Cesari, P., Urgesi, C., Facchini, S., Aglioti, S.M., 2005.
Motor facilitation of the human cortico-spinal system during
observation of bio-mechanically impossible movements.
NeuroImage 26, 755–763.
Roux, F.-E., Ibarrola, D., Lazorthes, Y., Berry, I., 2001. Virtual
movements activate primary sensorimotor areas in amputees:
report of three cases. Neurosurgery 49, 736–742.
Ruby, P., Decety, J., 2004. How would you feel versus how do
you think she would feel? A neuroimaging study of
perspective taking with social emotions. J. Cogn. Neurosci.
16, 988–999.
Saadah, E.S.M., Melzack, R., 1994. Phantom limb experiences in
congenital limb-deficient adults. Cortex 30, 479–485.
Sakagami, Y., Murai, T., Sugiyama, H., 2002. A third arm on the
chest: implications for the cortical reorganisation theory of
phantom limbs. J. Neuropsychiatry Clin. Neurosci. 14, 90.
Sanes, J.N., Suner, S., Lando, J.F., Donoghue, J.P., 1988. Rapid
reorganisation of adult rat motor cortex somatic
representation patterns after motor nerve injury. Proc. Natl.
Acad. Sci. U. S. A. 85, 2003–2007.
Sathian, K., 2000. Intermanual referral of sensation to anesthetic
hands. Neurology 54, 1866–1868.
Schiff, N.D., Pulver, M., 1999. Does vestibular stimulation activate
thalamocortical mechanisms that reintegrate impaired
cortical regions? Proc. R. Soc. Lond., B Biol. Sci. 266, 421–423.
Schwenkreis, P., Pleger, B., Cornelius, B., Weyen, U., Dertwinkel, R.,
Zenz, M., Malin, J.-P., Tegenthoff, M., 2003. Reorganization in
the ipsilateral motor cortex of patients with lower limb
amputation. Neurosci. Lett. 349, 187–190.
Schwoebel, J., Coslett, H.B., 2005. Evidence for multiple, distinct
representations of the human body. J. Cogn. Neurosci. 17,
543–553.
Schwoebel, J., Boronat, C.B., Coslett, H.B., 2002. The man who
executed “imagined” movements: evidence for dissociable
components of the body schema. Brain Cogn. 50, 1–16.
232 B RA I N R E SE A R CH RE V I EW S 54 ( 20 0 7 ) 2 1 9–2 3 2
Sherman, R.A., 1994. What do we really know about phantom limb
pain? Pain Rev. 1, 261–274.
Shukla, G.D., Sahu, S.C., Tripathi, R.P., Gupta, D.K., 1982. Phantom
limb: a phenomenological study. Br. J. Psychiatry 141, 54–58.
Singer, T., Seymour, B., O'Doherty, J., Kaube, H., Dolan, R.J., Frith,
C., 2004. Empathy for pain involves the affective but not
sensory components of pain. Science 303, 1157–1162.
Solonen, K.A., 1962. The phantom phenomenon in amputated
Finnish war veterans. Acta Orthop. Scand., Suppl. 54, 7–37.
Sörös, P., Husstedt, I.-W., Evers, S., Gerding, H., 2003. Phantom eye
syndrome: its prevalence, phenomenology and putative
mechanisms. Neurology 60, 1542–1543.
Stein, J.F., 1992. The representation of egocentric space in the
posterior parietal cortex. Behav. Brain Sci. 15, 691–700.
van der Velde, J., Everaerd, W., 2001. The relationship between
involuntary pelvic floor muscle activity, muscle awareness and
experienced threat in women with and without vaginismus.
Behav. Res. Ther. 39, 395–408.
Ventre-Dominey, J., Nighoghossian, N., Denise, P., 2003. Evidence
for interacting cortical control of vestibular function and
spatial representation in man. Neuropsychologia 41,
1884–1898.
Weinstein, S.M., 1998. Phantom limb pain and related disorders.
Neurol. Clin. 16, 919–935.
Weinstein, S., Sersen, E.A., 1961. Phantoms in cases of congenital
absence of limbs. Neurology 11, 905–911.
Weinstein, S., Sersen, E.A., Vetter, R.J., 1964. Phantoms and
somatic sensation in cases of congenital aplasia. Cortex 1,
276–290.
Weiss, S.A., Fishman, S., 1963. Extended and telescoped phantom
limbs in unilateral amputees. J. Abnorm. Soc. Psychol. 66,
489–497.
Wicker, B., Keysers, C., Plailly, J., Royet, J.P., Gallese, V.,
Rizzolatti, G., 2003. Both of us disgusted in my insula: the
common neural basis of seeing and feeling disgust. Neuron
40, 655–664.
Wilkins, K.L., McGrath, P.J., Finley, G.A., Katz, J., 2004. Prospective
diary study of nonpainful and painful phantom sensations in a
preselected sample of child and adolescent amputees
reporting phantom limbs. Clinical J. Pain 20, 293–301.
Willoch, F., Rosen, G., Tolle, T.R., Oye, I., Wester, H.J., Berner, N.,
Schwaiger, M., Bartenstein, P., 2000. Phantom limb pain in the
human brain: Unravelling neural circuitries of phantom limb
sensations using positon emission tomography. Ann. Neurol.
48, 842–849.
Wright, A., Halligan, P., Kew, J.J., 1997. Wellcome Trust Science Art
Project.
Yamamoto, S., Kitazawa, S., 2001. Sensation at the tips of invisible
tools. Nat. Neurosci. 4, 979–980.
Yamamoto, S., Moizumi, S., Kitazawa, S., 2005. Referral of tactile
sensation to the tips of L-shaped sticks. J. Neurophysiol. 93,
2856–2863.
Zampini, M., Moro, V., Aglioti, S.M., 2004. Illusory movements of
the contralesional hand in patients with body image disorders.
J. Neurol., Neurosurg. Psychiatry 75, 1626–1628.
Ziemann, U., Corwell, B., Cohen, L.G., 1998. Modulation of
plasticity in human motor cortex after forearm ischemic nerve
block. J. Neurosci. 18, 1115–1123.