Perception, 2010, volume 39, pages 1396 ^ 1407
doi:10.1068/p6582
Ouch! My phantom leg jumps/hurts when you stab
``my'' virtual hand
Melita J Giummarra, Bernadette M Fitzgibbonô, Nellie Georgiou-Karistianis,
Michael E R Nicholls½, Stephen J Gibson#, John L Bradshaw
Experimental Neuropsychology Research Unit, School of Psychology and Psychiatry,
Monash University, Wellington Road, Clayton, VIC 3800, Australia (ô also Monash Alfred Psychiatry
Research Centre, School of Psychology and Psychiatry, Monash University and the Alfred Hospital,
Melbourne, VIC, Australia); ½ School of Psychology, Flinders University, Bedford Park, South Australia;
# National Ageing Research Institute, Parkville, VIC, Australia; and Caulfield General Medical Centre,
Caulfield, VIC, Australia; e-mail: [email protected]
Received 23 September 2009, in revised form 3 September 2010
Abstract. Pain synaesthetes experience pain in a presensitised region when observing or imagining
another person in pain. We conducted an upper-limb embodiment study using a modified rubberhand illusion in which lower-limb amputees originally participated as control subjects for the
upper-limb amputees. While we found all subjects experienced topographic illusory sensations,
we also serendipitously found that lower-limb amputee pain synaesthetes experienced pain or a
motor response in their phantom leg when the embodied hand was threatened (eg with a retractable knife, mousetrap, or syringe) or submitted to high-frequency stimulation (eg vibration).
Embodiment illusions were brought about by touching, manipulating, or threatening a rubber or
real hand which was observed through a mirror so that it was superimposed upon the target
hand (phantom hand for upper-limb amputees, or real hand in others). Participants included
eight pain synaesthetes (six lower-limb amputees, one upper-limb amputee, and one nonamputee),
and thirty-one controls (eight lower-limb amputees, twelve upper-limb amputees, and eleven nonamputees). We documented participant's subjective reports, together with quantitative measures
including the Questionnaire Measure of Emotional Empathy. We found no association between
pain synaesthesia and empathy scores. On the basis of related literature we suggest that pain
synaesthetes likely experienced phantom-leg pain because (a) the motor system was already engaged
during visual capture; (b) threatening stimuli, to which they are hyper-vigilant, triggered avoidance
or `escape' motor schemata; and (c) there could be no feedback confirming that initiated motor
schemata for the phantom limb were successfully performed. Ultimately, we have further defined
this new condition, synaesthesia for pain, as not only having a sensory pain component, but also
a key motor component, manifesting itself in avoidance, contraction, and withdrawal `actions'.
1 Introduction
Synaesthesia for pain is a recently defined condition in which patients perceive pain
in one part of their bodies that is triggered when pain is observed or imagined in
another person (Fitzgibbon et al 2010; Giummarra and Bradshaw 2008). When observing another in pain, we not only consciously comprehend that they are in pain, but
we also interpret their experience throughout some of the same regions of the pain
matrix that mediate personal experience of pain (Jackson et al 2006; Singer et al
2004). The pain matrix is a network of cortical regions involved in processing pain in
oneself comprising both sensory and motor regions of the cortex (Jackson et al 2005).
Pain synaesthetes typically experience pain in a presensitised regionöeg phantom leg
or pelvisöwhen observing or thinking about another being injured or in pain, but
not when they directly experience such an injury. Pain synaesthesia likely corresponds
to a heightened sensitivity in pain networks in the brain.
While all current published cases of synaesthesia for pain have presented it as
acquired sensory disturbances (Bradshaw and Mattingley 2001; Giummarra and Bradshaw
2008), typically following trauma or injury (eg amputation or childbirth), other sensory
synaesthetes report the congenital variant of touch synaesthesia (Banissy et al 2009;
Threatened hands evoke phantom leg responses in pain synaesthetes
1397
Blakemore et al 2005). More recently, Osborn and Derbyshire (2010) observed that
pain synaesthesia could be induced in `normals', indicating that pain synaesthesia may
also be present, along a sensory/threshold continuum, in healthy individuals, similar
to touch synaesthesia (Banissy et al 2009). Little is known of the contribution of
various aspects of the traumatic experience involved in evoking pain synaesthesia.
That is, we do not know whether it is the physical or psychological components, a
combination of them both, and/or some pre-existing trait such as heightened empathy;
eg touch synaesthetes have been found to have heightened empathy compared with
non-synaesthetes (Banissy and Ward 2007).
Congenital or ideopathic synaesthesia typically involves the blending of unrelated
sensory information (eg grapheme ^ colour synaesthesia) (Rich et al 2005) with quite
vivid perceptions (eg specific colours for letters or words). Acquired types of synaesthesia, on the other hand, tend to comprise converging representations from different
modalitiesöeg sound ^ touch synaesthesia (Ro et al 2007), touch ^ vision (Armel and
Ramachandran 1999; Ramachandran and Brang 2009) and vision/imagery ^ pain
(Giummarra and Bradshaw 2008)öand result in triggered sensations that are less
specific, varying from tingling through to touch or pain.
In the present study we report the perception of pain or a motor response in a
phantom leg when an embodied fake or real hand was threatened (eg with a retractable
knife, mousetrap, or syringe) or submitted to high-frequency stimulation (eg vibration).
These observations emerged serendipitously while carrying out a larger study of upperlimb embodiment (Giummarra et al 2010). The original embodiment study induced
phantom-hand illusions in both amputees and nonamputees when using a modified
rubber-hand illusion: participants observed a hand being stimulated in a mirror as if
`superimposed' upon the target hand, without the simultaneous stroking or stimulation of the target hand as done in the traditional rubber-hand illusion (Botvinick and
Cohen 1998). Five of the six lower-limb amputee pain synaesthetes who participated
in the present study reported synaesthetic responses to at least one stimulus warranting
further investigation.
We do not report here general findings from the original study (Giummarra et al
2010). Rather, the aim of the current study was to describe and investigate the perception of synaesthetic phantom-leg pain in response to perception of threat to an
embodied hand. First, we hypothesised that phantom-leg reactions when the embodied
hand was threatened may have been due to heightened embodiment of the threatened
hand in pain synaesthetes. Second, we expected that pain synaesthetes would exhibit
heightened empathyöusing the Questionnaire Measure of Emotional Empathy (QMEE)
(Mehrabian and Epstein 1972)öcompared with non-synaesthetes, as has been previously found for touch synaesthetes (Banissy and Ward 2007). We ultimately discuss
the present observations within the context of our current model of synaesthesia for
pain; that is, that synaesthesia for pain stems from disinhibited activation, or central
sensitisation, of a fundamentally adaptive system for the empathic perception of pain
in another (Giummarra and Bradshaw 2008).
2 Method
2.1 Participants
Two groups participated in the present study: pain synaesthetes and those without pain
synaesthesia. Both groups included upper- and lower-limb amputees, and nonamputees.
The criterion for inclusion in the pain synaesthesia group was to have reported that
phantom (or other) pain was triggered by observing or imagining another person in pain.
All of the amputees had previously participated in a questionnaire study in which the
pain synaesthetes had been identified as such (Giummarra et al, in press). In the present
study, all amputees were asked what triggered their phantom pain prior to commencing
1398
M J Giummarra, B M Fitzgibbon, N Georgiou-Karistianis, and coauthors
the embodiment paradigm, and all pain synaesthetes again described their experience
of pain triggered by either observing or thinking about another in pain. After asking
open questions about pain triggers, we then clarified with all participants who had not
disclosed pain synaesthesia whether they had these triggers, and no further pain synaesthetes were identified.
2.1.1 Pain synaesthetes. Eight pain synaesthetes participated, including six lower-limb
amputees, one upper-limb amputee, and one nonamputee. All acquired pain synaesthesia
following amputation trauma, or traumatic childbirth in the last case. There were five
males (63%) aged 40 ^ 88 years (M ˆ 64 years, SD ˆ 15 years). Most of these pain
synaesthetes had been identified in an earlier study (Giummarra et al, in press), and
have also been described elsewhere (Giummarra and Bradshaw 2008). Pain synaesthesia
was defined by the perception of `empathic' pain, typically in a presensitised region,
when observing or thinking about another in pain (Fitzgibbon et al 2010; Giummarra
and Bradshaw 2008). All of these individuals satisfied these criteria. See table 1 for the
pain synaesthete characteristics.
Table 1. Pain synaesthete characteristics: (a) amputation/trauma details, (b) phantom sensation/pain
and embodiment.
Subject
(gender;
age, years)
Years
since
amputation
Side and level of
amputation/
synaesthetic pain
Cause
(a)
1 (F, 59)
2 (M, 82)
3 (M, 88)
4 (M, 68)
5 (F, 59)
6 (M, 53)
7 (M, 60)
8 (F, 40)
26
6
13
27
37
9
3.5
4
right below elbow
bilateral above knee
left above knee
right below knee
right above knee
right above knee
right above knee
pelvic region
cancer
vascular disease
trauma
trauma
trauma
trauma
vascular disease
traumatic childbirth
Phantom
sensation
frequency
Phantom
pain
frequency
Questionnaire
Measure of
emotional
empathy
Embodiment strength
real-hand
condition
rubber-hand
condition
infrequent
never
never
always
always
always
daily
n/a
infrequent
infrequent
annual
always
monthly
infrequent
daily
n/a
26
30
13
22
ÿ1
21
missing
ÿ3
high
none
low
moderate
moderate
high
moderate
low
high
moderate
moderate
high
low
low
moderate
none
(b)
1
2
3
4
5
6
7
8
(F, 59)
(M, 82)
(M, 88)
(M, 68)
(F, 59)
(M, 53)
(M, 60)
(F, 40)
Lower-limb amputees, who had normal and intact upper limbs, were invited to
participate within the control sample in the original study to control for the potential
confound of trauma on embodiment. The reason for this was that, when piloting the
paradigm in undergraduate psychology students, it appeared, qualitatively, that the few
participants who had experienced prior trauma experienced heightened embodiment
and perceptual illusions compared with other participants.
Threatened hands evoke phantom leg responses in pain synaesthetes
1399
2.1.2 Non-synaesthetes. The non-synaesthete sample comprised eleven nonamputees,
twelve upper-limb amputees, and eight lower-limb amputees. The non-synaesthetes
included twenty-two men (71%) aged 22 ^ 79 years (M ˆ 48 years, SD ˆ 14 years).
No participants had neurological or psychiatric diagnoses. There were no significant
differences between synaesthetes and non-synaesthetes in the perception of `emotional'
triggers of phantom pain (eg pain that is triggered by extreme negative emotions such
as anger, frustration, or sadness). Of the non-synaesthetes three (25%) upper-limb
amputees, and three (38%) lower-limb amputees reported general emotional triggers of
their phantom pain. Three (50%) of the lower-limb amputee pain synaesthetes reported
more general emotional triggers for their phantom pain.
2.2 Materials and apparatus
2.2.1 Mirror box. The mirror box was 66 cm wide, 54 cm deep, and 40 cm high and
had sliding tracks in the centre through which a mirror was placed to face either
towards the left or right, depending on the target hand (which was hidden behind the
mirror). A cover was placed over the target-(phantom)-limb side of the box so that
the space behind the mirror could not be seen. See figure 1 for the mirror box when
(a) the participant's real hand and (b) the rubber hand was used.
(a)
(b)
Figure 1. Experimental setup for left-sided embodiment in which (a) the participant's real right
hand, and (b) the right rubber-hand was used, with the participant's own right hand on his/her
lap. The grey-shaded region represents the arm that is covered and hidden behind the mirror.
2.2.2 Rubber limbs. The rubber hands were cosmetic glove prostheses developed by
Regal prosthetics, Hong Kong, and were highly realistic in colour, skin texture, size,
shape, and attention to detail with respect to veins and fingernails. In this study
we only used hands (that is, there was no equivalent apparatus to test lower-limb
embodiment in the lower-limb amputees), as the overall study focused exclusively on
upper-limb embodiment.
2.2.3 Stimuli. Five categories of stimuli were used to investigate the perception of common kinaesthetic and proprioceptive sensations. Within each category, the qualities of
sensation varied from low-threshold, non-threatening stimuli (eg cotton-bud or finger
movement of 108) through to potentially threatening or painful stimuli (eg syringe,
knife that apparently pierces the hand while in fact retracting into the handle, or finger
movement of 908).
There were 17 trials in total: 7 trials for touch (cotton bud, spatula, skewer, syringe,
blunt knife, hand holding knife, and knife stabbing hand); 3 for pressure (mousetrap
not set, set, and set off on the index finger); 3 for movement (of the fingers to 108,
458, and 908); 2 for vibration (low frequency and high frequency); and 2 for temperature (ice cube and boiling/warm water). A kettle was boiled in the participant's
presence so that they knew boiling water was used. There were 8 threatening trials per
participant in the rubber-hand condition (including the syringe, blunt and stabbing
knives, mousetrap set and set off, high-frequency vibration, and boiling water); there
were 4 threatening and high-frequency trials (including the syringe, mousetrap not set,
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M J Giummarra, B M Fitzgibbon, N Georgiou-Karistianis, and coauthors
knife stabbing hand, and high-frequency vibration) per participant in the real-hand
condition. The mousetrap set and set-off, movement to 908, and boiling water stimuli
were excluded from the real-hand condition.
2.3 Questionnaires and ratings
Participants reported and rated illusions of embodiment and other sensations perceived
in the hidden/target hand after each trial. Participants rated (a) the intensity of any
sensation perceived in the target limb from 0 to 10 and (b) the degree to which the
limb observed in the mirror represented the target limb, rated from 0 (no illusion) to
10 (complete illusion: ``the mirror reflection represents my limb''). For the `potentially
threatening' stimuli, participants also rated whether they had an urge to withdraw their
target limb from the stimulus from ÿ10 (urge to approach the stimulus) to 0 (no urge
to approach or withdraw from the stimulus) to ‡10 (strongest urge or actual withdrawal from the stimulus). Participants also rated any change in phantom-limb pain on
a scale of 0 (no change) to 10 (greatest change in pain).
After each category of stimuli was applied to the rubber limb (that is, in the
rubber-limb condition only), participants completed a modified version of Botvinick
and Cohen's (1998) Rubber Hand Embodiment Scale (RHES); see original study for
description (Giummarra et al 2010). Originally we found that stimulus-specific ratings
of embodimentöthat is, from aboveöwere most robust and were therefore used exclusively in the present study.
Participants completed the Questionnaire Measure of Emotional Empathy (QMEE)
(Mehrabian and Epstein 1972). The QMEE is a 33-item test in which the respondent
answers each item on a scale from very strong disagreement (ÿ4) to very strong agreement (‡4). Each item on the scoring key is designated as either a positive or a negative
item. Typical items from the QMEE scale are: ``The people around me have a great
influence on my mood'', ``Lonely people are probably unfriendly'', and ``Seeing people
cry upsets me''. The scale was selected as it was designed to measure emotional rather
than cognitive aspects of empathy, and has high internal consistency (Chlopan et al
1985; Mehrabian and Epstein 1972). It has also been referred to as the Balanced
Emotional Empathy Scale (BEES) (Hein and Singer 2008; Singer et al 2004). Self-rated
empathy with this scale has been found to correlate with (a) activation in the left
anterior insula and inferior frontal gyrus when observing pain from the faces of people
in pain (Saarela et al 2007; Singer et al 2004); and (b) reaction time to noxious stimuli
(Morrison et al 2007), suggesting empathic processing of pain in others that is measurable
by this scale. However, not all studies find a consistent relationship between the BEES
and pain processing (Danziger et al 2006), and there is some controversy over the finding
of high correlations in some empathy for pain-imaging studies (Vul et al 2009).
2.4 Procedure
Participants gave informed consent prior to inclusion in the study. The study was
approved by local university and hospital ethics boards, and met the ethical standards
laid down in the 1964 Declaration of Helsinki. Participants sat in front of the mirror
box, with the midline of the box (and thus the central mirror) directly in front of their
body midline. They placed their target or `phantom' hand behind the mirror, and a
cover was placed over that side of the box. There were two conditions in the study:
the rubber-hand condition and the real-hand condition. In the rubber-hand condition,
a rubber limb was placed so that it was `superimposed' upon the target or phantom hand,
via the mirror (eg if the participant had a left-sided amputation, a right-sided rubber limb
was placed in the box). When the rubber hand was in the box, the participant rested
his/her other arm out of sight. In the real-hand condition the participant placed both
arms in the box and viewed the reflection of the real arm as if superimposed upon the
target or phantom hand.
Threatened hands evoke phantom leg responses in pain synaesthetes
1401
The participant fixated upon the mirror reflection of the rubber hand in each trial.
Participants were asked to comment freely upon any change in sensation that they
perceived in their target or phantom hand only, and were told that there were no right
or wrong sensations to perceive or report. If participants reported a change in sensation, they were asked to further describe it, in their own words. The above procedure
was performed for all 17 stimuli involving the fake rubber hand, and was then repeated
with the participant's own intact/real hand in the box (in the real-hand condition).
Four trials were not conducted in the real-hand condition: the set mousetrap, mousetrap snapped onto the index finger, movement of fingers to 908, and boiling water
(warm water was used instead). Lower-limb amputees were also asked to report any
other sensations evoked (eg in the phantom leg); however, we did not explicitly indicate
that we expected synaesthetic sensations in the pain synaethetes.
3 Results
3.1 Embodiment and illusory sensations for the mirror-reflected hand
There were no differences in embodiment illusions between pain synaesthetes and
non-synaesthetes (ratings for ``the degree to which the limb observed in the mirror
represented the target limb'') in the rubber-limb condition (F17, 20 ˆ 0:86, p ˆ ns; Wilks'
l ˆ 0:58; Zp2 ˆ 0:42) or the real-limb condition (F13, 23 ˆ 0:54, p ˆ ns; Wilks' l ˆ 0:77;
Zp2 ˆ 0:24). Furthermore, both groups were equally likely to experience illusory
sensations in the embodied hand. See table 2 for means and standard deviations for
embodiment ratings, and perception of illusory sensations for pain synaesthetes and
non-synaesthetes. Equal numbers of pain synaesthetes and controls reported pain in
the embodied hand in the syringe trials (one synaesthete and one non-synaesthete), and
when the mousetrap was set off on the index finger of the rubber hand (two synaesthetes
and two non-synaesthetes).
3.2 Perceptual responses in other body parts during illusory hand stimulation
Six (75%) pain synaesthetes and no controls reported synaesthetic responses in a region
previously identified as prone to pain synaesthesia (the phantom leg). The nonamputee
pain synaesthete reported no synaesthetic perceptions in the pelvis where she typically
experiences pain synaesthesia.
The upper-limb pain synaesthete did report vivid embodiment illusions and topographically consistent `synaesthetic' sensations in the embodied hand; however, many
pain synaesthetes (n ˆ 5; 63%) and non-synaesthetesöincluding upper-limb (n ˆ 8, 67%)
and lower-limb (n ˆ 6; 75%) amputees and nonamputees (n ˆ 5, 45%)öalso reported
phantom `synaesthetic' sensations in the embodied hand. Thus, it was difficult to
distinguish synaesthetic responses in the upper-limb pain synaesthete from general illusions induced during embodiment. We therefore focus our discussion on lower-limb
pain synaesthetes whose non-topographic synaesthetic sensations were unexpected.
Among the pain synaesthetes, synaesthetic responses occurred in 20% (10 of
48 trials) of threatening/high-frequency trials in the rubber-hand condition, and 36%
(13 of 36 trials) of trials in the real-hand condition. This was not initially expected
as lower-limb amputees were recruited simply to control for the potential confound
of trauma on illusory-hand embodiment. While all lower-limb amputees were asked
to report any changes in sensations in the hidden phantom leg as well as the hand,
only the pain synaesthetes reported that some stimuli triggered synaesthetic responses
in the phantom leg. These sensations were not always painful, but included sensations
such as tingling, buzzing, burning, contraction, `withdrawal', or sharp pain. See table 3
for descriptions of synaesthetic responses.
1402
Table 2. Embodiment illusions (M, SD) and perceptual illusions (w2 with Fisher's Exact Test) between pain synaesthetes and non-synaesthetes.
Rubber-hand condition Real-hand condition
perceptual illusions
embodimentb
perceptual illusions
sfpa
M (SD)
controls
M (SD)
sfpa
N (%)
controls
N (%)
difference
sfpa
M (SD)
controls
M (SD)
sfpa
N (%)
controls
N (%)
difference
2.5
3.7
3.3
5.3
3.8
4.4
3.8
2.4
3.4
3.6
(2.7)
(3.1)
(3.0)
(2.8)
(3.7)
(3.4)
(3.6)
(2.6)
(2.9)
(2.9)
5.2
5.4
5.2
5.2
4.3
5.3
4.7
5.1
5.5
5.5
(3.6)
(3.3)
(3.3)
(3.5)
(3.6)
(3.5)
(3.7)
(3.6)
(3.7)
(3.8)
2
4
2
4
4
4
3
0
1
3
(25)
(50)
(25)
(50)
(50)
(50)
(37.5)
(0)
(12.5)
(37.5)
16
16
12
7
7
9
5
4
5
12
(51.5)
(51.6)
(38.7)
(22.58)
(22.58)
(30)
(16.1)
(12.9)
(16.13)
(38.7)
w21
w21
w21
w21
w21
w21
w21
w21
w21
w21
ˆ 1:81, ns
ˆ 0:007, ns
ˆ 0:52, ns
ˆ 2:34, ns
ˆ 2:34, ns
ˆ 1:22, ns
ˆ 1:78, ns
ˆ 1:15, ns
ˆ 0:064, ns
ˆ 0:004, ns
5.6
5.3
5.3
4.4
5.3
4.1
4.2
4.8
±
±
(4.3)
(4.3)
(4.4)
(3.9)
(4.4)
(3.2)
(4.1)
(3.6)
4.4
4.6
4.4
4.5
4.5
5.2
4.4
5.1
±
±
(3.6)
(3.6)
(3.4)
(3.3)
(3.4)
(3.7)
(3.5)
(3.7)
3 (37.5)
3 (37.5)
2 (25)
3 (37.5)
3 (37.5)
1 (14.3)
2 (25)
1 (13)
±
±
5
6
9
7
10
9
7
2
±
±
(16.1)
(19.4)
(29)
(22.6)
(32.3)
(30)
(22.6)
(6)
w21
w21
w21
w21
w21
w21
w21
w21
±
±
ˆ 1:78,
ˆ 1:18,
ˆ 0:05,
ˆ 0:74,
ˆ 0:08,
ˆ 0:71,
ˆ 0:02,
ˆ 0:33,
2.1
2.3
2.3
1.7
1.7
2.50
2.4
(2.0)
(2.1)
(2.1)
(1.8)
(2.2)
(3.1)
(2.6)
4.9
4.9
4.3
4.8
4.6
4.6
4.7
(3.6)
(3.8)
(3.7)
(3.5)
(3.5)
(3.6)
(3.8)
3
2
2
2
2
2
2
(37.5)
(25)
(25)
(25)
(25)
(25)
(25)
10
11
9
15
15
11
7
(32.3)
(35.5)
(29.03)
(48.4)
(48.4)
(35.5)
(22.6)
w21
w21
w21
w21
w21
w21
w21
ˆ 0:079, ns
ˆ 0:32, ns
ˆ 0:051, ns
ˆ 1:4, ns
ˆ 1:4, ns
ˆ 0:32, ns
ˆ 0:021, ns
4.75
5.0
±
4.4
4.4
4.4
4.6
(3.6)
(3.8)
5.2
4.9
±
5.4
5.3
5.1
5.2
(3.8)
(3.8)
3 (37.5)
2 (25)
±
3 (37.5)
4 (50)
2 (25)
2 (25)
7
10
±
4
8
8
11
(22.6)
(32.3)
w21
w21
±
w21
w21
w21
w21
ˆ 0:74, ns
ˆ 0:16, ns
(3.9)
(3.9)
(3.9)
(3.9)
(3.5)
(3.7)
(3.7)
(3.7)
(12.9)
(25.8)
(25.8)
(35.5)
ns
ns
ns
ns
ns
ns
ns
ns
ˆ 2:61, ns
ˆ 1:75, ns
ˆ 0:002; ns
ˆ 0:32, ns
a sfp: Pain synaesthetes; b Ratings for ``the degree to which the limb observed in the mirror represented the target limb'' from zero (no illusion) to 10
(complete illusion that ``the mirror reflection represents my limb'').
M J Giummarra, B M Fitzgibbon, N Georgiou-Karistianis, and coauthors
Cotton swab
Spatula
Skewer
Syringe
Blunt knife
Hand holding knife
Knife stabbing hand
Mousetrap not set
Mousetrap set
Mousetrap set off on
the index finger
Movement to 108
Movement to 458
Movement to 908
Low-frequency vibration
High-frequency vibration
Ice cube
Boiling/warm water
embodimentb
N:/psfiles/per3910w/
Threatened hands evoke phantom leg responses in pain synaesthetes
1403
Table 3. Descriptions of synaesthetic responses to stimuli in the rubber-hand and real-hand conditions
in pain synaesthetes.
Stimulus
Subject 2
Subject 3
Rubber-limb condition
syringe
tingling
mousetrap set
off on index
finger
Subject 5
tingling in
phantom
foot
(ball/toes)
burning
in foot
vibration
(high)
boiling water
^
Real-limb condition
syringe
blunt knife
knife stab
vibration (low)
cold
hot
Subject 7
tingle/sharp
leg went ``bang''
pain in index
(tightened and
finger and
withdrew); stump
tingle in toes
physically jerked
same symptoms in leg
as syringe
non-painful stump
contraction
blunt knife
sharp knife
Subject 4
^
tingling
^
^
slight contraction
of stump
slight contraction
of stump
a minor contraction/
jerk in phantom
strong contractions
in stump being held
rather than
intermittent like
earlier
stump contracting/
tightening; not pain;
cold in stump too!
increased illusion
a little
foot burning/
shooting/
shock; like
it started
in stomach
^
slight burn
in foot
burning
in foot
slight burn
in foot
3.3 Potential empathy differences between pain synaesthetes and non-synaesthetes
The QMEE was used to investigate potential differences in pain empathy. There were
no significant differences between pain synaesthetes (M ˆ 15:4; SD ˆ 13:0; median ˆ 21,
range: ÿ3 to ‡30) and non-synaesthetes (M ˆ 10:7; SD ˆ 17:9; median ˆ 9; range:
ÿ28 to ‡42); Mann ^ Whitney U ˆ 65:0, N1 ˆ 23; N2 ˆ 7, ns, two-tailed.
4 Discussion
We report here the experience of pain and/or facilitation of the motor system in the
phantom leg in pain synaesthetes when an embodied rubber or real hand is threatened.
Pain synaesthesia may result from disinhibited mirroring and mimicry of another's
physical, motivational, or emotional state, resulting in actual perception of pain. Pain
synaesthesia has been previously reported in people with lower-limb amputation or
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M J Giummarra, B M Fitzgibbon, N Georgiou-Karistianis, and coauthors
traumatic childbirth (Giummarra and Bradshaw 2008), and typically is not topographically
or qualitatively consistent with the observed pain. However, there are some reports of
high correspondence between the location and intensity of the observed pain and the
induced synaesthetic pain in acquired (Bradshaw and Mattingley 2001) and in likely
congenital cases (Osborn and Derbyshire 2010). Sensory synaesthesia has also been
reported by upper-limb amputees (Ramachandran and Brang 2009) and touch synaesthetes (Banissy and Ward 2007) that is topographically consistent with the observed
touch, and qualitatively comparable to actual touch. Likewise, most participantsö
whether upper-limb amputees, pain synaesthetes, or nonamputeesöin the present
study also reported topographic and perceptually consistent `synaesthetic' sensations
induced in the embodied hand. Both synaesthetic touch and pain have been shown to
be associated with heightened activation in neural regions involved with personal
experience of touch (eg somatosensory cortex, left premotor cortex, and bilateral anterior
insula) (Blakemore et al 2005) or pain (eg anterior cingulate cortex, insula, and primary
and secondary somatosensory cortices) (Osborn and Derbyshire 2010), suggesting the
presence and involvement of sensory mirror systems (Serino et al 2008). On the basis
of our observations, and those previously reported of corticospinal facilitation in the nontargeted hand when observing another receive a painful injection (Avenanti et al 2009b),
we suggest that synaesthetic responses in our subjects relate to facilitation of the motor
system to implement appropriate reactions (to escape) to noxious stimuli.
The synaesthetic sensations we observed may have resulted from the emotional or
arousing nature of the stimuli, or exacerbation of baseline phantom pain. This is unlikely,
however, as three pain synaesthetes and three non-synaesthetes from the lower-limb
sample reported that general emotional distress triggered phantom pain. All other pain
synaesthetes indicated that the only `emotional' trigger is specific to observing or thinking about others in pain, suggesting that emotional distress itself was not the central
trigger of synaesthetic perceptions. That said, affective regions of the pain matrix are
active when observing others in pain (eg anterior cingulate and insular corticesöJackson
et al 2005; Morrison et al 2004), and likely active during pain and touch synaesthesia
(Banissy and Ward 2007).
We were surprised not to find increased empathy in pain synaesthetes. While some
studies report positive correlations between subscales of the IRI, pain ratings (Loggia
et al 2008), and activation within central and corticospinal regions associated with
affective and somatosensory components of the pain matrix when processing pain in
another (Avenanti et al 2009a; Cheng et al 2008; Danziger et al 2006; Singer et al
2004), these findings have been questioned (Vul et al 2009), and others have failed to
show a significant relationship (Avenanti et al 2005; Danziger et al 2006; Jackson et al
2005; Lamm et al 2007). Ultimately, self-measures of empathy, such as the QMEE,
appear to be poor predictors of actual empathic behaviour (Davis and Kraus 1997)
and, correspondingly, may not be sensitive or objective enough to reveal differences
in emotional processing in pain synaesthetes. Furthermore, absence of a significant
relationship may be due to the small number of pain synaesthetes.
It is noteworthy that we have now demonstrated, for the first time, synaesthetic
responses in the phantom leg when threat is directed towards an embodied hand. Our
participants report that pain synaesthesia is typically induced only when viewing images
depicting or threatening pain in another (eg medical programs on television, or trauma
in the newspaper), but not when the same injury or pain is directly experienced in
oneself (eg seeing a child graze his elbow evokes synaesthetic pain in the phantom
foot, but falling and grazing one's own elbow does not) (Giummarra and Bradshaw
2008). The present study created the illusion of self-directed pain by threatening the
pain synaesthete's embodied hand, without actual sensory input, and thus induced
synaesthetic responses in the phantom leg. Because there is no local neuronal activity
Threatened hands evoke phantom leg responses in pain synaesthetes
1405
to either confirm or contra-indicate pain or injury in our pain synaesthetes, motor
components of the pain matrix are activated, triggering associated motivational
avoidance, and sensory responses. This is somewhat reminiscent of our inability to
tickle ourselves as neuronal activity in the somatosensory cortex is attenuated by selfgenerated movement, likely via the cerebellum (Blakemore et al 1998); however, you
can easily be tickled by another person because of absence of efference copy updating
the somatosensory cortex of the upcoming intensity, location, and frequency of sensations to expect. However, this is unlikely as the non-synaesthete lower-limb amputees
also did not have local sensory input relating to the embodiment illusion, and did not
report synaesthetic responses in their phantom legs.
We suggest that the perception of physical symptoms in the phantom leg when the
rubber or real hand is threatened is likely associated with increased activation of
sensorimotor regions of the pain matrix (primary motor cortex, premotor cortex,
parietal cortex, and corticospinal excitability), as is also found in pain empathy studies
(Avenanti and Aglioti 2006; Bufalari et al 2007; Lamm et al 2007). When an embodied
rubber limb is threatened, the same feelings, neural activity (particularly in medial motor
wall areas, and insula anterior cingulate cortices), and increased skin conductance
response are evoked as when real limbs are threatened (Armel and Ramachandran 2003;
Ehrsson et al 2007, 2008; Hagni et al 2008; Lloyd et al 2006).
The present nontopographic relationship between a threatened hand eliciting phantom leg pain does not exclude activation of mirror neuron systems, as it is thought
that such mirrored neural activity primarily correlates with general action goals rather
than specific effectors (Aziz-Zadeh et al 2006). While most participants wished to withdraw the embodied hand from perceived threat, only pain synaesthetes perceived pain
or a motor response in the phantom leg, perhaps because perceived threat evoked a
more generalised motor and avoidance response in pain synaesthetes owing to hypervigilance to implements associated with pain, injury, or amputation (Giummarra and
Bradshaw 2008).
It is unlikely that these synaesthetic reports were confabulatory: (1) while participants
had to report sensations in their phantom legs, they were not told to expect them,
and only the pain synaesthetes reported such sensations; (2) participants were genuinely
surprised when their phantom leg reacted to the hand being threatened; (3) most
pain synaesthetes reacted to different stimuli, but all such stimuli were characterised
as threatening or of high frequency. No synaesthetic responses were reported to nonthreatening, low-impact stimuli; and (4) synaesthetic responses were unique in each case,
sometimes being characterised primarily as a motor response (eg withdrawal, contracting), sometimes as a paraesthesia (eg tingling, buzzing), and sometimes as outright
phantom pain.
In summary, the pain and motor responses experienced by pain synaesthetes may
ultimately have occurred because (a) rubber-hand embodiment preactivated the motor
system; (b) threatening stimuli triggered protective, avoidance or `escape' motor schemata;
and (c) this motor response was perceived as painful and/or unpleasant because of the
absence of feedback to confirm that the motor schemata were successfully performed.
Pain synaesthetes present experiences may be explained by altered cortical reorganisation or heightened cortical excitability of the limb representation following amputation,
perhaps owing to coactivations during perceived threat and phantom pain; however,
the present study has produced no data to confirm or refute this. This study has
further contributed to the definition of the recently identified condition of acquired
synaesthesia for pain. While we have not been able to show any differences in empathy
between pain synaesthetes and non-synaesthetes, we have highlighted that this condition
not only involves the sensory perception of pain, but that it also has a strong motor
component.
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M J Giummarra, B M Fitzgibbon, N Georgiou-Karistianis, and coauthors
References
Armel K C, Ramachandran V S, 1999 ``Acquired synesthesia in retinitis pigmentosa'' Neurocase 5
293 ^ 296
Armel K C, Ramachandran V S, 2003 ``Projecting sensations to external objects: Evidence from skin
conductance response'' Proceedings of the Royal Society of London, Series B 270 1499 ^ 1506
Avenanti A, Aglioti S M, 2006 ``The sensorimotor side of empathy for pain'', in Psychoanalysis
and Neuroscience Ed. M Mancia (Milan: Springer) pp 235 ^ 256
Avenanti A, Bueti D, Galati G, Aglioti S M, 2005 ``Transcranial magnetic stimulation highlights
the sensorimotor side of empathy for pain'' Nature Neuroscience 8 955 ^ 960
Avenanti A, Minio-Paluello I, Bufalari I, Aglioti S M, 2009a ``The pain of a model in the
personality of an onlooker: Influence of state-reactivity and personality traits on embodied
empathy for pain'' NeuroImage 44 275 ^ 283
Avenanti A, Minio-Paluello I, Sforza A, Aglioti S M, 2009b ``Freezing or escaping? Opposite
modulations of empathic reactivity to the pain of others'' Cortex 45 1072 ^ 1077
Aziz-Zadeh l, Wilson S M, Rizzolatti G, Iacoboni M, 2006 ``Congruent embodied representations
for visually presented actions and linguistic phrases describing actions'' Current Biology 16
1818 ^ 1823
Banissy M J, Kadosh R C, Maus G W, Walsh V, Ward J, 2009 ``Prevalence, characteristics and a
neurocognitive model of mirror ^ touch synaesthesia'' Experimental Brain Research 198 261 ^ 272
Banissy M J, Ward J, 2007 ``Mirror ^ touch synaesthesia is linked with empathy'' Nature Neuroscience
10 815 ^ 816
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
Blakemore S J, Wolpert D M, Frith C D, 1998 ``Central cancellation of self-produced tickle
sensation'' Nature Neuroscience 1 635 ^ 640
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?'' Journal of Neurology, Neurosurgery and Psychiatry 70 135 ^ 140
Bufalari I, Aprile T, Avenanti A, Di Russo F, Aglioti S M, 2007 ``Empathy for pain and touch in
the human somatosensory cortex'' Cerebral Cortex 17 2553 ^ 2561
Cheng Y, Yang C, Lin C, Lee P, Decety J, 2008 ``The perception of pain in others suppresses
somatosensory oscillations: A magnetoencephalography study'' NeuroImage 40 1833 ^ 1840
Chlopan B E, McCain M L, Carbonell J L, Hagen R L, 1985 ``Empathy: Review of available
measures'' Journal of Personality and Social Psychology 48 635 ^ 653
Danziger N, Prkachin K M, Willer J-C, 2006 ``Is pain the price of empathy? The perception of
others' pain in patients with congenital insensitivity to pain'' Brain 129 2494 ^ 2507
Davis M H, Kraus L A, 1997 ``Personality and empathic accuracy'', in Empathic Accuracy
Ed. W Ickes (New York: Guilford Press) pp 144 ^ 168
Ehrsson H H, Rosen B, Stockselius A, Ragno C, Kohler P, Lundborg G, 2008 ``Upper limb
amputees can be induced to experience a rubber hand as their own'' Brain 131 3443 ^ 3452
Ehrsson H H, Wiech K, Weiskopf N, Dolan R J, Passingham R E, 2007 ``Threatening a rubber hand
that you feel is yours elicits a cortical anxiety response'' Proceedings of the National Academy
of Sciences of the USA 104 9828 ^ 9833
Fitzgibbon D M, Giummarra M J, Georgiou-Karistianis N, Enticott P G, Bradshaw J L, 2010
``Shared pain: From empathy to synaesthesia'' Neuroscience and Biobehavioural Reviews 34
500 ^ 512
Giummarra M J, Bradshaw J L, 2008 ``Synaesthesia for pain: Feeling pain with another'', in
The Role of Mirroring Processes in Social Cognition Ed. J A Pineda (San Diego, CA: Humana
Press) pp 287 ^ 307
Giummarra M J, Georgiou-Karistianis N, Gibson S J, Nicholls M E R, Bradshaw J L, 2010
``The phantom in the mirror: A modified rubber-hand illusion in amputees and normals''
Perception 39 103 ^ 118
Giummarra M J, Georgiou-Karistianis N, Nicholls M E R, Gibson S J, Chou M, Bradshaw J L,
in press ``Corporeal awareness and proprioceptive sense of the phantom'' British Journal of
Psychology doi:10.1348/000712610X492558
Hagni K, Eng K, Hepp-Reymond M-C, Holper L, Keisker B, Siekierka E, Kiper D C, 2008
``Observing virtual arms that you imagine are yours increases the galvanic skin response to
an unexpected threat'' PLoS ONE 3 August 28, 1 ^ 6
Hein G, Singer T, 2008 ``I feel how you feel but not always: The empathic brain and its modulation''
Current Opinion in Neurobiology 18 153 ^ 158
Threatened hands evoke phantom leg responses in pain synaesthetes
1407
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
Jackson P L, Rainville P, Decety J, 2006 ``To what extent do we share the pain of others? Insight
from the neural bases of pain empathy'' Pain 125 5 ^ 9
Lamm C, Nusbaum H C, Meltzoff A N, Decety J, 2007 ``What are you feeling? Using functional
magnetic resonance imaging to assess the modulation of sensory and affective responses
during empathy for pain'' PLoS ONE 2 el292
Lloyd D, Morrison I, Roberts N, 2006 ``Role for human posterior parietal cortex in visual
processing of aversive objects in peripersonal space'' Journal of Neurophysiology 95 205 ^ 214
Loggia M L, Mogil J S, Bushnell M C, 2008 ``Empathy hurts: Compassion for another increases
both sensory and affective components of pain perception'' Pain 136 168 ^ 176
Mehrabian A, Epstein N, 1972 ``Measure of emotional empathy'' Journal of Personality 40 525 ^ 543
Morrison I, Lloyd D, Di Pellegrino G, 2004 ``Vicarious responses to pain in anterior cingulate
cortex: Is empathy a multisensory issue?'' Cognitive and Affective Behavioural Neuroscience 4
270 ^ 278
Morrison I, Poliakoff E, Gordon L, Downing P, 2007 ``Response-specific effects of pain observation
on motor behavior'' Cognition 104 407 ^ 416
Osborn J, Derbyshire S W G, 2010 ``Pain sensation evoked by observing injury in others'' Pain
148 268 ^ 274
Ramachandran V S, Brang D, 2009 ``Sensations evoked in patients with amputation from watching
an individual whose corresponding intact limb is being touched'' Archives of Neurology 66
1281 ^ 1284
Rich A, Bradshaw J L, Mattingley J B, 2005 ``A large-scale systematic study of synaesthesia: Is fact
stranger than fiction?'' Cognition 98 53 ^ 84
Ro T, Farne A, Johnson R M, Weeden V, Chu Z, Wang Z J, Hunter J V, Beauchamp M S, 2007
``Feeling sounds after a thalamic lesion'' Annals of Neurology 62 433 ^ 441
Saarela M, Hlushchuk Y, Williams A C D C, Schu«rmann M, Kalso E, Hari R, 2007 ``The compassionate brain: Humans detect intensity of pain from another's face'' Cerebral Cortex 17 230 ^ 237
Serino A, Pizzoferrato F, Ladavas E, 2008 ``Viewing a face (especially one's own face) being
touched enhances tactile perception on the face'' Psychological Science 19 434 ^ 438
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
Vul E, Harris C, Winkielman P, Pashler H, 2009 ``Puzzlingly high correlations in fMRI studies
of emotion, personality, and social cognition'' Perspectives on Psychological Science 4 274 ^ 290
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