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Scientific Commentaries

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Masel BE, DeWitt DS. Traumatic brain injury: a disease process, not an
event. J Neurotrauma 2010; 27: 152940.
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This limb is mine but I do not want it: from


anatomy to body ownership
The experience that the body is part of the self, and in particular
that my body belongs to me in all its parts, in a coherent and
continuous way, is a fundamental aspect of consciousness.
Moreover, a normal sense of body ownership is critical for our
daily interaction with the objects of the outside world. The different processes that are involved in the building up of normal body
awareness are far from being clear. A classical distinction, introduced by Head and Holmes (1911), is that between body schema
and body image. Body schema is generally regarded as an unconscious, bottom-up, dynamic representation, relying on proprioceptive information and involved in enabling and monitoring motor
actions. Body image is considered to be a more conscious,
top-down, cognitive representation, mostly used to make perceptual judgements. More recently, the unified concept of body
matrix has been introduced that captures functional features like
multisensory processes that are relevant for the construction of
body awareness (Moseley et al., 2012).

At first glance, the sensation that I have a body, and that I am


that body, is so self-evident and immediate that it seems there is
nothing to explain about it. The feeling of the same old body
always there (James, 1890) is part of our identity from the beginning of our conscious life, and appears to be a sensation so
intimately tied to all aspects of our mental processes that even
when parts of the body are severely affected by either brain
damage, as in hemiplegia after a stroke, or by peripheral traumatic
injuries, as in limb amputation, patients can still have the experience of a normal functioning of their body. In anosognosia for
hemiplegia, patients are convinced that their paretic limb can still
move, and it has been proved that their altered body awareness is
based on normal neural signals that affect the motor behaviour of
the good side of the body (Garbarini et al., 2012). Similarly, in
amputees, phantom sensation (rephrasing James, the feeling that
the same old body is still there) are often observed, indicating the
persistence of normal body sensorymotor maps despite the

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Amor S, Puentes F, Baker D, van der Valk P. Inflammation in neurodegenerative diseases. Immunology 2010; 129: 15469.
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et al. MR-based brain and cerebrospinal fluid measurement after
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injury revisited. Acta Neurochir (Wien) 2006; 148: 18193; discussion
934.
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Sunaert S, et al. Graph analysis of functional brain networks for
cognitive control of action in traumatic brain injury. Brain 2012; 135:
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biomarkers of pathological mechanisms. J Cereb Blood Flow Metab
2012, in press.
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for use with traumatic brain injury research. J Neurotrauma 2012; 29:
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Stewart W. Inflammation and white matter degeneration persist for
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2011; 164: 120729.

Brain 2013: 136; 913

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| Brain 2013: 136; 913

that the disorder is rare, 13 xenomelic patients constitute an


important database) that makes the observations reliable and an
important starting point for future research. The results show that,
compared with normal subjects, xenomelic patients have alterations in the cortical architecture and, in particular, a reduced
cortical thickness and volume in the superior parietal lobule and
reduced cortical surface area in the inferior parietal lobule, in the
somatosensory areas SI and SII and in the anterior insular cortex
and frontal operculum. These observations are enlightening because the areas involved in the disorder are often indicated as
crucial in the construction of the feeling of owning a body, therefore suggesting a tight link between xenomelia and an impairment
of complex circuits responsible for the integration of fundamental
information for the establishment and maintenance of the sense of
body ownership.
It is of greatest interest, in this respect, that some of the areas
that Hilti et al. (2013) associate to the xenomelic disturbance partially overlap with brain areas found to be damaged in a neuropsychological disorder, known as somatoparaphrenia, which
strikingly parallels xenomelia. In its classic form, patients, after
right hemisphere lesions, deny the ownership of their left limbs,
a behaviour that can be seen as the extreme consequence of the
feeling of strangeness that some xenomelic subjects declare having
towards their left limbs. The lesional pattern recently associated
with somatoparaphrenia involves a complex and distributed right
frontotemporoparietal network extending to subcortical structures (Gandola et al., 2012), and to the insula (Karnath et al.,
2010). Therefore, the behavioural/anatomical similarities between
the two disturbances suggest that impairments in one or more
regions identified in the studies reported above and now by Hilti
et al. (2013) may affect the construction of a coherent body
image, possibly destroying a specific part of it, to an extent that
patients either deny the ownership of the affected limbs (as in
somatoparaphrenia) or they want to get rid of them because of
the stress caused by the distorted representation (as in xenomelia).
We are still far from fully understanding the kind of distortion
experienced by the patients in these syndromes, but their analogical aspects would suggest a specific and localized alteration of
body image so that body representation is somehow missing the
area of the affected limb (Brang et al., 2008). This might be congenital in xenomelia, and the abnormalities found by Hilti et al.
(2013) would, therefore, be the cause, or a facilitating factor, of
subjects feeling of left limb strangeness (and not the effect, as
might be argued), whereas in somatoparaphrenic patients, the
firm belief of dis-ownership is acquired as a consequence of a
complex, and more severe, lesional pattern (Gandola et al.,
2012) that would lead to the misidentification of the affected limb.
For xenomelic patients, one question we can ask is how do they
feel after the amputation? There are not many reports on that,
and it is not clear whether they experience phantom limb sensations. The hypothesis of the existence of an analogically impaired
body image before surgery would actually predict that after amputation, being the body aspect coherent with the body image,
patients should not have any phantom limb sensation. This might
be a question to be addressed in future research. Another point
that may deserve further investigation is related to the motor
aspect of the limb affected by the amputation desire. Hilti et al.

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absence of a body part (Franz and Ramachandran, 1998). These


two pathological conditions paradoxically show normal functioning
of some body representations despite modified body conditions.
We may speculate that the construction of body awareness is
reached by the contribution of so many different neural networks,
implementing both body schema and body image process, to be
resistant, within certain limits, to different pathological assaults.
The idea of an enduring sense of coherent body awareness is
evolutionary plausible and may be the base of the feeling of
unity and ownership experienced when we think to ourself.
In this context, the disorder studied by Hilti et al. (2013) in the
current issue of Brain is completely counterintuitive. Indeed, xenomelia, previously called apotemnophilia or body integrity identity
disorder, is a dramatic condition in which sufferers, who apparently do not have history of brain damage, desire the amputation
of healthy limbs. Often the desire for the amputation dates back
to childhood, and sometimes it started after exposure to an amputee. It can also be accompanied by a sexual attraction for amputation of own or others limbs.
The interpretation of such an astonishing mental status has been
controversial. The sexual component, the analogy with gender
disorders and the frequent co-occurrence of psychiatric symptoms
have favoured for a long time a pure psychological/psychodynamic interpretation (De Preester, 2011). However, many subjects have been reported to be sane and rational, without any
other psychological problems, with the exception of the emotional
strain related to the desire for a different body. On the other
hand, some features of the disorder have pointed to the possibility
of a neurological origin of xenomelia (Brang et al., 2008). For
instance, the limbs most frequently involved are the lower limbs
and in particular the ones on the left side, suggesting some sort of
hemispheric asymmetry for the anomalous desire. More importantly, both subjective and objective sensory abnormalities have
been reported: when asked if the limb felt different in some
way, subjects may say that the limb felt like it was not their
own and may also report experienced sensations in the limb
they want to be amputated less intensely as compared with
their other limbs (First, 2004). Moreover, in some cases, xenomelic
subjects want the operation because they feel incomplete (De
Presteer, 2011) or over-complete (McGeoch et al., 2011) with
four limbs, but would feel more complete with three, suggesting a
distortion of body image. The subjective experience reported by
these subjects is associated with alteration of objective parameters.
Brang et al. (2008) found heightened skin conductance response
to pinprick, in two subjects, below the desired line of amputation,
while McGeoch et al. (2011) found a selective reduced activation
in the right superior parietal lobe in magnetoencephalography
scans during tactile stimulation of the affected leg when compared
with both subjects unaffected legs and that of control subjects.
Therefore, different observations point to the possibility that the
disorder may be interpreted within a theoretical framework that
takes into account possible impairment in body representation. In
this respect, the article by Hilti et al. (2013) is a fundamental step
for clarifying the nature of the disorder. The principal aim of the
study was to investigate whether there are structural abnormalities
that may explain xenomelic subjects behaviour. The study was
carried out in a relatively large sample of subjects (considering

Scientific Commentaries

Scientific Commentaries

Funding
This paper was funded by a Compagnia di San Paolo grant and a
MIUR-PRIN grant to AB.
Anna Berti
Department of Psychology, University of Turin, Via Po 14,
Turin, Italy
Correspondence to: Anna Berti,
Department of Psychology,
University of Turin, Via Po 14,
Turin, Italy
E-mail: annamaria.berti@unito.it

doi:10.1093/brain/aws346

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(2013) note that despite the feeling of strangeness they experience for the affected limb, xenomelic subjects are well aware that
they are the agent of the action they perform with that limb, that
is they do not show any sign of anarchic hand syndrome (Schaefer
et al., 2010). However, although agency might be intact, motor
intentionality and motor awareness for the affected limbs might be
affected by the sense of dis-ownership. Body schema and body
image interact and one might predict reduced motor intentionality
and, consequently, reduced motor activation for the limb that
might not be represented (or under-represented) in the body
image of xenomelic patients. Such findings would further
strengthen the interpretation of xenomelia as a disorder imprinted
in body representation and especially would be in keeping with
the concept of body as source or power to action, i.e. as the
variety of motor potentialities that define the horizon of the
world in which we live (Gallese and Sinigaliga, 2010). In any
case, the article by Hilti et al. (2013) demonstrates the hardwired
nature of xenomelia, or at least of its main features, and, supporting the validity of using an anatomo-clinical correlation model,
represents an important contribution to understanding how an
apparent self-evident sensation, like body ownership, is built up
in a complex and multidimensional way.

Brain 2013: 136; 913

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