Disownership of left hand and objects related to it in a

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Cognitive Neuroscience and Neuropsychology
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NeuroReport 8, 293–296 (1996)
WE describe a woman with right brain damage who
denied the ownership of her left hand and of extracorporeal objects (e.g. rings) which were worn on the left
hand itself. When the same objects were worn on the
right hand or were held by the examiner, the patient
correctly recognized them as her own. Other personal
objects unrelated to the left hand (e.g. pins, earrings,
comb) were always correctly recognized as her own.
Thus, by inference, the mental image of one’s body may
include inanimate objects which had been in contact or
in close proximity with the body itself. These findings
provide, for the first time, experimental support to the
speculative notion of an extended body schema.
Key words: Anosognosia; Extended body schema; Right
brain damage; Somatoparaphrenia
Introduction
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Salvatore Aglioti,CA Nicola Smania,1
Michela Manfredi2
and Giovanni Berlucchi
Dipartimento di Scienze Neurologiche e della
Visione, Sezione Fisiologia Umana, Strada Le
Grazie 8, I-37134, Verona; 1Servizio Recupero e
Rieducazione Funzionale, Policlinico Borgo
Roma, Verona; 2Dipartimento di Scienze
Neurologiche e della Visione, Sezione
Neurologia, Verona, Italy
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Disownership of left hand
and objects related to it
in a patient with right
brain damage
Neurological and psychological evidence suggests
that the spatial representations for mapping the body
and extracorporeal objects are largely independent
from one another.1–5 The construction and maintenance of a body image rely upon the interaction
among visual, labyrinthine, proprioceptive, tactile
and visceral inputs as well as between these inputs
and the mental representation that one has of one’s
own body.4,6 Self-awareness and the conscious
self–non-self distinction are related in various and
complicated ways to bodily sensations. According to
James,7 the nucleus of the ‘me’ is always the bodily
existence felt to be present at the time; however, this
feeling may include non-corporeal items that are
perceived in association with the body, such as
clothes or other material belongings. James also
pointed out that it is difficult, if not impossible, to
draw a precise and permanent boundary between
what a person calls ‘me’ and what he or she calls
‘mine’, a statement which applies to paraphernalia
and bodily parts alike. Thus, at least theoretically, the
mental image of one’s body may include objects that
had been in contact or in close proximity with the
body itself. This body image can be regarded as an
extended body schema. For example, a probe may
become, at least temporarily, part of the body image
of a surgeon as well as a stick may be part of the
body schema of a blind man.8 In line with this
© Rapid Science Publishers
CA
Corresponding Author
hypothesis is the anecdotal evidence from amputee
patients who report the sensation of a tight ring on
their phantom hand.4,9 Although hypotheses about
an extended body schema have been formulated since
the last century, the present study is the first to
provide experimental evidence supporting such
hypotheses.
Materials and Methods
C.B., a 73-year-old, right handed, housewife with
5 years of schooling suffered a right hemisphere
stroke on November 4, 1995 (Fig. 1). On admission,
she presented with motor and sensory deficits to her
left hemisoma. Left extrapersonal and personal
neglect with strong denial of ownership of the left
hand was observed. According to her son, soon after
the stroke his mother asked him to remind doctors
to take away the hand that they had left in her bed.
When first seen by us, 4 days after the stroke, the
patient appeared well orientated as to time and place.
She was able to remember her telephone number and
perform within normal limits in a short-term memory
digit span test. C.B. showed a striking anosognosia10–12 for her left-side sensorimotor defects. She
denied having any problem with her left hemisoma
but complained about an aching right hip-joint which
had been operated several years before. Like other
patients with large lesions to the right side of the
brain13,14 C.B. resolutely denied the ownership of her
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S. Aglioti et al
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Table 1. Description of the objects used in the experimental sessions. The possible effect of dimension, weight
and material of the objects was taken into account. The
golden pin, for example, shared all the above features with
the rings. The key-ring was put on the fourth finger in a
ring-like fashion with the aim of examining the effect of a
relationship with the left hand as close as possible to that
of the rings.
Object
0111
Belonging Related to
to patient disowned
body part
Ring with diamonds/garnet
Gold ring with an R
Watch with brown strap
Small gold pin
Earrings
Blue comb
Holy icon (Santa Rita)
Holy icon (Mother Mary)
Knife with a white handle
Clock
Ring with a lapis lazuli
Ring with a diamond
Watch with a black strap
Brown comb
Brush
Key ring (with key)
Scissors
Padlock
0111
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
N
N
N
N
N
N
N
N
Y
Y
Y
N
N
N
N
N
N
N
Y
Y
Y
N
N
N
N
N
Category
1
1
1
2
2
2
2
2
2
2
3
3
3
4
4
4
4
4
FIG. 1. CT transverse cuts, taken 6 days after the stroke, show a
large area of cortical and subcortical infarction. The white progressive numbers on the left lower corner of each cut indicate a caudal
to rostral progression.
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left hand and insisted that it had been left in her bed
by the doctors. On verbal command, she could touch
her left ear, eye, shoulder, elbow, and knee, but only
with great effort could she touch her left hand.
Moreover, after touching the hand she typically
stated that it was not her own. The ownership of
other body parts was correctly acknowledged. Her
knowledge about prototypical human figures was
preserved because she had no problems in reporting
that human bodies typically consist of one head, one
trunk, two eyes, two ears, one nose, two hands, two
arms, two legs, two feet.
When we first saw the patient, she wore two rings
on her left ring finger, namely her wedding ring and
a ring with two lateral, small diamonds and one
central big garnet. She also wore on her right fourth
finger a large golden ring with an R on its plate
surface. C.B. not only denied the ownership of her
left hand, but she also denied ever having seen the
rings worn on her left hand; by contrast, she recognized the ring on her right hand and reported many
details about it (e.g. ‘this ring was made from a necklace, about 10 years ago’). We took the wedding ring
away and moved the garnet ring from the left to the
right hand. Surprising as it may seem, now the patient
was not only able to recognize the ring as her own,
294 Vol 8 No 1 20 December 1996
but was also able to retrieve much autobiographical
information related to it (e.g. ‘I remember quite
clearly that this ring had been given to me by my
late husband’). A few seconds later we replaced the
garnet ring on the disowned left hand and asked C.B.
to describe the ring and report its owner. The patient
described the ring adequately and also admitted that
it looked similar to the one which was on her right
hand one minute before; however, she appeared
genuinely convinced that both the hand and the ring
belonged to the doctor. Moreover, the gold ring
(which was correctly recognized as her own when
worn on the right hand), was no longer labelled
as her own when put on the disowned left hand.
Both the rings were correctly recognized as her
own when held by the examiner in front of her. To
assess the phenomenon systematically, we used
objects with combinations of the two attributes relevant to the task, namely ownership and perceptuorepresentational relationships with the disowned
body part (Table 1).
C.B. was tested in three experimental sessions, 4,
5, and 6 days after the stroke. Each session, lasting
about 2 h, began with specific questions about the
ownership of different body segments. On each
experimental trial, one object was put in the right or
Body image and brain damage
1
the left hand. The patient’s left hand was positioned
in the right space or along the bodily midline by
the examiner. All testing sessions were videorecorded
and results were scored with the help of the film
sequences.
Results
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A standard neurological examination revealed a left
somatosensory deficit, mild for the lower limb and
severe for the upper limb. There was a left hemianopia on a confrontation test. The patient showed
perfect recognition of objects by active and passive
touch with the right hand. Because of her sensorimotor deficits she was unable to manipulate objects
with the left hand. In a condition of passive tactile
exploration where the left hand was guided by the
examiner, the patient was unable to recognize any
objects. Visual recognition of objects or familiar faces
was perfect. Extreme left hemispatial neglect was
evident from line- and letter cancellation tasks and
from a task of copying complex line drawings.
Moreover, C.B. showed a marked head deviation
towards the right hemispace and her eyes were
magnetically captured by visual stimuli presented in
the right hemispace. In spite of this rightward bias
the patient could be instructed to align her head and
eyes with the bodily midline. Paradoxical visual
extinction15 was assessed by presenting two simultaneous stimuli, at about 10 and 20° to the right of a
central fixation point. In spite of its retinal advantage, the 10° stimulus went unnoticed. Detection of
tactile stimuli was assessed by delivering to the
dorsum of each hand (lying in its homonymous hemispace) a sequence of unilateral or bilateral light
touches.16 All left side stimuli in the bilateral stimulation condition were extinguished and only two of
five left unilateral stimuli were detected, suggesting
a severe somatosensory deficit. However, positioning
the left hand in the right space was accompanied by
a dramatic improvement in left hand accuracy under
both unilateral and bilateral conditions, confirming
that apparent somatosensory deficits may be caused
by neglect.17 It is remarkable that when the left hand
was in its heteronymous hemispace C.B. reported
feeling stimuli on a hand that, in her opinion, did not
belong to her. All objects were named and described
correctly, but there was a selective impairment in
attributing ownership of objects related to the
disowned left hand (Table 2). On the first two testing
sessions C.B. obstinately refused to admit that her
left hand belonged to her. Instead, she maintained
that the hand belonged to the examiner. On the third
testing session the delusional symptom had partially
faded. When, at the beginning of the session, the
examiner touched C.B.’s left hand and inquired about
the ownership of the hand she hesitated before saying
that it was not her hand. Moreover, in three of four
correct trials with objects in category 1, the patient
recognized the hand as her own.
Seventeen days after the stroke, in a testing session
where the disowning phenomenon had completely
cleared up, C.B. attribution of ownership to objects
from all categories was fully veridical.
Discussion
In classical neurology, after Head and Holmes’18
humorous suggestion that the feather in the hat of
an Edwardian woman could become part of her body
schema, it has been widely held that the mental image
of a person’s body may extend to inanimate objects
which are in contact with or in close proximity to
the body itself.8,18 James7 speculated that extrapersonal objects systematically associated with the
body can be represented in memory either as ‘mine’
or as ‘me’, depending on whether they are considered in isolation or in conjunction with the associated body part. The representation of a body part
would thus include a representation of the paraphernalia constantly associated with that part in
the subjects’ past experience. Although this concept
of an extended body schema has an intuitive appeal,
so far no factual evidence has been provided in
support of these speculations.
In patient C.B., a lesion affecting the anatomical
substrate of the physical self19 induced a resolute
disownership of her paralytic left hand, which was
attributed to other individuals. This pathological
distortion of the body schema also seems to have
affected the mental representation of extracorporeal
objects that, in the patient’s previous experience, were
systematically associated with parts of her own body.
C.B. denied the ownership of her rings only when
they were viewed on her left hand. Furthermore, the
patient’s incorrect denial of ownership did not extend
to other personal belongings not systematically associated with the disowned hand, even though they
Table 2. Number of the hits out of the total number of
trials in each experimental session for each category of
objects.
Hand
Left
Right
Object
category
1
2
3
4
1
2
3
4
Date of testing
8/11/95
9/11/95
10/11/95
0/6
4/4
2/2
4/4
4/4
4/4
2/2
4/4
0/6
4/4
6/6
4/4
6/6
2/2
4/4
4/4
0/6
2/2
5/5
4/4
6/6
2/2
4/4
2/2
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were presented in contact or in close proximity with
that hand. When our patient viewed in her extrapersonal space or on her right hand the rings usually
worn on her left hand, she recognized them as her
own. This correct judgement probably occurred
because the mode of stimulus presentation activated
the ‘mine’ representation of the rings independent of
that of the disowned hand. C.B.’s false judgement
occurred only when the representation of the rings
was activated conjointly with that of the repudiated
hand. Since the left hand was no longer represented
as ‘me’, the associated paraphernalia were also
expunged from the body schema. It is remarkable
that only in a condition in which the extrapersonal
objects would normally be coded as ‘me’, the retrieval
of autobiographical information about objects related
to the disowned parts seemed impossible. This result
would suggest that an object is represented in egocentric or in allocentric coordinates according to the ‘me’
or ‘mine’ labels attributed to it. Thus, in patient C.B.,
disowning or recognizing as her own the hand-rings
complex depended on the dynamic integration of the
appropriate reference frame with somatosensory and
visual information, whether previous or current.6
Conclusion
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The available information on the relation between
denied body parts and paraphernalia related to them
is extremely scanty. It has been anecdotally reported
that a woman with right brain damage was puzzled
by seeing her wedding ring on her disowned left
hand.20 Equally anecdotal is our previous, unpublished observation of a woman with right brain
damage in whom the disowned left hand was recognized as her own only when her wedding ring was
put on the hand itself. Thus, C.B. differs from those
previous cases and is the first known instance
supporting the notion of an extended body schema.
ACKNOWLEDGEMENTS: We wish to thank Dr J.C. Marshall and Dr J. Harris
for their comments on an earlier draft of the manuscript. The financial contribution of MURST and the Consiglio Nazionale delle Ricerche, Italy, is gratefully
acknowledged.
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Received 10 September 1996;
accepted 24 September 1996
General Summary
The present study provides the first experimental support to the speculative notion that objects external to the body may be included
in one’s body image. We describe a woman with right brain damage in whom denial of the ownership of her left hand included
extracorporeal objects (e.g. rings) which had been in close perceptual and representational contact with the left hand itself. When
the same objects were worn on the right hand or were held by the examiner, the patient correctly recognized them as her own.
Judgements of ownership were always correct when concerning objects unrelated to the denied body part (e.g. pins, earrings, comb).
The disownership of left hand and objects related to it recovered with the same time course. This novel finding suggests that the
mental image of one’s body may be extended to include inanimate objects which had been in contact or in close proximity with the
body itself.
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