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Abstract
& Whether observation of distress in others leads to empathic ness instructions affected participants’ affective responses to
concern and altruistic motivation, or to personal distress and the observed pain. Hemodynamic changes were detected in
egoistic motivation, seems to depend upon the capacity for the insular cortices, anterior medial cingulate cortex (aMCC),
self–other differentiation and cognitive appraisal. In this experi- amygdala, and in visual areas including the fusiform gyrus.
ment, behavioral measures and event-related functional mag- Graded responses related to the perspective-taking instructions
netic resonance imaging were used to investigate the effects were observed in middle insula, aMCC, medial and lateral pre-
of perspective-taking and cognitive appraisal while participants motor areas, and selectively in left and right parietal cortices.
observed the facial expression of pain resulting from medical Treatment effectiveness resulted in signal changes in the peri-
treatment. Video clips showing the faces of patients were pre- genual anterior cingulate cortex, in the ventromedial orbito-
sented either with the instruction to imagine the feelings of frontal cortex, in the right lateral middle frontal gyrus, and in
the patient (‘‘imagine other’’) or to imagine oneself to be in the cerebellum. These findings support the view that humans’
the patient’s situation (‘‘imagine self’’). Cognitive appraisal was responses to the pain of others can be modulated by cognitive
manipulated by providing information that the medical treat- and motivational processes, which influence whether observ-
ment had or had not been successful. Behavioral measures ing a conspecific in need of help will result in empathic con-
demonstrated that perspective-taking and treatment effective- cern, an important instigator for helping behavior. &
INTRODUCTION
that are involved when the self experiences emotion. It
Empathy refers to the capacity to understand and re- is not plausible, however, that this sharedness is abso-
spond to the unique affective experiences of another lute. A complete overlap between self and other repre-
person (Decety & Jackson, 2004; Batson, Fultz, & sentations would produce distress and hamper the
Schoenrade, 1987). This psychological construct de- ability to toggle between self and other perspectives.
notes, at a phenomenological level of description, a In recent years, there has been a growing interest in
sense of similarity between the feelings one experiences research on the neural mechanisms that mediate empa-
and those expressed by others. Despite the various thy, particularly following the target article by Preston
definitions of empathy among psychologists, there is and de Waal (2002), in which they reviewed an impres-
broad agreement on three primary components: (1) an sive array of evidence in support of the perception–action
affective response to another person, which some be- model and its fundamental role in social interaction. This
lieve entails sharing that person’s emotional state; (2) a model posits that perception of emotion activates the
cognitive capacity to take the perspective of the other neural mechanisms that are responsible for the genera-
person; and (3) some monitoring mechanisms that keep tion of emotions. Such a system prompts the observer to
track of the origins (self vs. other) of the experienced resonate with the emotional state of another individual,
feelings. Depending on how empathy is triggered, the with the observer activating the motor representations
automatic tendency to mimic the expressions of others and associated autonomic and somatic responses that
(bottom-up processing) and the capacity for the im- stem from the observed target (i.e., a sort of inverse
aginative transposing of oneself into the feeling and mapping). For instance, a handful of functional magnetic
thinking of another (top-down processing) may be resonance imaging (fMRI) studies have shown that the
differentially involved. It also seems likely that both observation of pain in others is mediated by several brain
processes rely upon, to some extent, neural mechanisms areas that are implicated in processing the affective and
motivational aspects of pain (see Jackson, Rainville, &
Decety, 2006, for a review). In one study, participants
1
INSERM Unit 280, France, 2University of Kansas, 3University received painful stimuli in some trials and, in other trials,
of Chicago observed a signal that their partner, who was present in
D 2007 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 19:1, pp. 42–58
the same room, would receive the same stimuli (Singer tations account of social interaction (Decety & Grèzes,
et al., 2004). The anterior medial cingulate cortex (aMCC; 2006; Decety & Sommerville, 2003). In addition, the
Vogt, 2005), the anterior insula, and the cerebellum were self-perspective yielded higher pain ratings and involved
activated during both conditions. Similar results were re- the pain matrix (Derbyshire, 2000) more extensively in
ported by Morrison, Lloyd, di Pellegrino, and Roberts the secondary somatosensory cortex, the posterior part
(2004), who applied a moderately painful pinprick stim- of the anterior cingulate cortex (ACC), and the middle
ulus to the fingertips of their participants, and—in a insula. These results highlight important differences be-
second condition—showed them a video clip showing tween the self- and other-perspectives. For instance,
another person undergoing similar stimulation. Both con- although the anterior insula is activated both when par-
ditions resulted in common hemodynamic activity in ticipants imagine their own and when they imagine
pain-related areas of the right cingulate cortex. In con- another’s pain, nonoverlapping clusters can be identi-
trast, the primary somatosensory cortex showed signifi- fied within the middle insula. Likewise, both self- and
cant activations in response to tactile stimuli only, but not other-perspectives are associated with a common sub-
to visual stimuli. The different response patterns in the area in the aMCC, but the self-perspective selectively
two areas are consistent with the role of the aMCC activated another part of this region.
in coding the motivational-affective dimension of pain, Finally, being aware of one’s own emotions and feel-
which is associated with the preparation of behavioral ings enables us to reflect on them. Among various
responses to aversive events (Vogt, 2005; Paus, 2001). In emotion regulation strategies when observing a target in
another study, participants were shown photographs de- pain, reappraisal by denial of relevance (i.e., taking a de-
picting right hands and feet in painful or neutral everyday- tached observer position), by implicitly or explicitly gen-
life situations, and were asked to imagine the level of pain erating an image of the observing self which is unaffected
that these situations would produce ( Jackson, Meltzoff, by the target, is known to reduce the subjective experi-
& Decety, 2005). Significant activation in regions in- ence of anxiety, sympathetic arousal, and pain reactivity
volved in the network processing the affective aspect of (Kalisch et al., 2005). Such a strategy is likely to play an
pain, notably the aMCC and the anterior insula, was de- important role in preventing empathic overarousal (think
tected. Moreover, the level of activity within the aMCC about a psychotherapist and his/her client). fMRI studies
was strongly correlated with participants’ mean ratings of have identified a limited number of regions in the antero-
pain attributed to the different situations. These results lateral prefrontal and medial prefrontal/orbito-frontal
lend support to the idea that common neural circuits are cortices that mediate such function (Kalisch et al., 2005;
involved in representing one’s own and others’ affective Ochsner, Bunge, Gross & Gabrieli, 2002).
pain-related states. Recently, Singer and colleagues (2006) The goal of the present experiment was to assess the
demonstrated that the hemodynamic response in this respective contribution of the processes that mediate
circuit is modulated by learned social preferences, espe- empathy: affective sharing, perspective-taking, and cog-
cially in male participants. nitive appraisal. We exposed participants to video clips
Imagining how another person feels and how one showing the faces of persons who were described as
would feel in a particular situation requires distinct patients suffering a neurological disease affecting their
forms of perspective-taking that likely carry different audition. As a cover story, participants were told that
emotional consequences (Batson, Early, & Salvarini, patients underwent a sound therapy supposed to im-
1997). Research in social psychology (e.g., Batson et al., prove their medical status; however, as this therapy
2003; Underwood & Moore, 1982) has documented this involved being stimulated with sounds of a certain
distinction by showing that the former may evoke em- frequency, patients had to suffer great pain during
pathic concern (defined as an other-oriented response treatment. Participants were requested to watch the
congruent with the perceived distress of the person in videos adopting two different perspectives, that is, ei-
need), whereas the latter induces both empathic con- ther imagining how they themselves would feel if they
cern and personal distress (i.e., a self-oriented aversive were in the place of the other (imagine self ), or
emotional response). In a recent fMRI study, partici- imagining how the other feels (imagine other). In
pants were shown pictures of people with their hands or addition, participants were told that the video clips
feet in painful or nonpainful situations with the instruc- had been shot from two groups of individuals. In one
tion to imagine themselves or to imagine another in- group, patients got better after treatment, whereas
dividual experiencing these situations ( Jackson, Brunet, patients from the other group did not benefit from that
Meltzoff, & Decety, 2006). Both the self-perspective and treatment. This manipulation was performed to elicit
the other-perspective were associated with activation in different cognitive appraisals by observers watching
the neural network involved in pain processing, includ- identical stimuli, but with knowledge of different impli-
ing the parietal operculum, the aMCC, and the anterior cations. It was anticipated that witnessing another per-
insula. These results reveal the similarities in neural son suffering and knowing that the treatment had not
networks representing first-person and third-person in- been effective would increase emotional distress in the
formation, which is consistent with the shared represen- observer (and vice versa). During scanning, participants
(4.44b/4.72c)
[main effect of perspective taking, F(1,15) = 4.623, p =
14.56b/12.56c
Suppression
13.59 (6.26)
.048, partial h2 = 0.236; M(Self ) = 34.375, SD = 15.478;
M(Other) = 27.083, SD = 13.088]. Treatment effec-
Normative data derived and transformed to sum scores from: IRI (Bellini, Baime, & Shea, 2002); EQ (Baron-Cohen & Wheelwright, 2004); ECS (Doherty, 1997); ERS (Gross & John, 2003).
tiveness did not have a significant effect on recogni-
tion rates ( p = .485), nor was the interaction term
significant ( p = .736). In addition, patients displaying
(5.64b/6.12c)
stronger pain were more likely to be recognized (as indi-
Reappraisal
31.35 (4.23)
c
27.6 /27.66
cated by a significant correlation between the perceived
b
intensity of pain determined in the pretests and the
percentage of correct hits, r = .429, p = .004).
The forced-choice memory test showed that the self-
perspective led to a higher percentage of correct classi-
fications [main effect of perspective taking, F(1,14) =
Contagion Scale
The table provides results for the sample investigated in our study, and published normative values.
Suppression = 28.
a
Normative Data
Female sample.
the videos, with reports of mimicry being stronger in the and caudate nucleus), and bilateral periamygdalar re-
self-perspective in eight of these subjects. gion reveals the affective response to the observation
of pain. Additional significant clusters were detected in
motor control-related regions, such as the cingulate and
Network of Areas Involved in the Observation
supplementary motor area (CMA/SMA) and the lateral
of Pain
precentral gyrus, as well as in temporo-parietal and
Observation of pain expressed by the patients activated lateral prefrontal areas (Brodmann’s areas 8 and 9).
a widely distributed network of brain regions, reflecting Analysis of the localizer task resulted in bilateral
the sensory, cognitive–motor, and affective processing hemodynamic changes in the posterior superior tempo-
of the stimuli (Figure 3). Clusters comprising (bilater- ral gyrus, comprising the Heschl gyrus and overlapping
ally) medial and lateral occipital cortex, including the with the probabilistic cytoarchitectonic maps of the
fusiform gyrus, indicate the visual processing of the primary auditory cortices provided in the Anatomy
stimuli. Activity in bilateral anterior and in the left Toolbox (Morosan et al., 2001). Also, activity was de-
middle insula, aMCC, thalamus, basal ganglia (pallidum tected bilaterally in the anterior insula, in the left middle
Figure 3. Significant
hemodynamic response to
the observation of patients
expressing pain (Watching
Pain > Baseline). Activation
was detected in the neural
network involved in the
sensory (FFG = fusiform
gyrus, MOG = middle
occipital gyrus) and the
affective processing of pain
(insula, aMCC). Results are
superimposed on axial (z =
16, z = 6), coronal ( y =
70), and sagittal sections
(x = 0) of the single-subject
structural MNI MRI template
(used in all figures and
displayed in neurological
convention). Threshold p =
.00001 (uncorrected), k = 20.
reflects a difference in relative deactivation that was more cated stronger hemodynamic responses with higher
pronounced with the other-perspective [mean param- Emotional Contagion scores in these regions.
eter estimates: M(Other Effective) = 4.15, M(Other
Not-effective) = 0.4, M(Self Effective) = 0.48, M(Self
DISCUSSION
Not-effective) = 3.4].
The ROI analysis of amygdala activity revealed a There are good reasons to posit that witnessed pain in
stronger response in the amygdala with the self-perspec- others may result in anxiety, promoting at least cautious
tive [trend-like main effect for the perspective factor, approach behavior or general threat-defense mecha-
F(1,16) = 4.38, p = .053, partial h2 = 0.215], with this nisms (MacDonald & Leary, 2005). The affective experi-
difference being slightly more pronounced in the left ence of pain signals an aversive state and motivates
hemisphere [trend-like interaction Perspective Hemi- behavior to terminate, reduce, or escape exposure to
sphere, F(1,16) = 3.077, p = .099, partial h2 = 0.161; the source of the noxious stimulation (Price, 1999).
Figure 8]. Indeed, negative feelings triggered by pain usually mo-
tivate organisms to avoid dangerous stimuli and move
away from danger. However, the observation of pain in
Correlation of Brain Activity with Behavioral
others may also instigate an altruistic motivation to help
Data and Dispositional Measures
the other, which is quite different from the egoistic
Analysis of the EQ scores revealed significant correla- motivation to reduce personal distress.
tions in the right putamen, the left posterior/middle The aim of our study was to investigate the effects of
insula, the aMCC, and the left cerebellum. Scores of the perspective-taking and cognitive appraisal on the behav-
empathic concern index correlated with a similar cluster ioral and neural correlates of pain observation. To this
in the aMCC. No significant correlation was observed for end, participants watched video clips of patients display-
the Empathic Concern scale of the IRI, the personal ing an aversive emotional response due to painful
distress index, and the Personal Distress scale of the IRI. auditory stimulation under different conditions. Using
Scores of the Emotional Contagion scale correlated with a number of both state and trait behavioral measures
activity in brain regions involved in affective pain pro- and event-related fMRI, we were able to demonstrate
cessing (insula and aMCC) and movement control (SMA, distinct behavioral and neural responses that are in
lateral premotor area; Table 4, Figure 9). In addition, good agreement with both empirical findings and theo-
two clusters in the left and right parietal cortex close retical concepts concerning the promotion of empathic
to the ones revealed by the Self–Other contrasts indi- emotion and, ultimately, altruistic motivation (Batson
Figure 8. Stronger
hemodynamic responses in
left and right amygdala when
subjects adopted the self-
perspective (contrast Self >
Other). Left: t values from the
contrast Self > Other, overlaid
on a coronal section of the
single-subject structural MNI
MRI template. Right: mean
(±SE ) parameter estimates
for signal changes in the
whole amygdala.
et al., 2003; Batson, Early, et al., 1997; Batson, Sager, nipulations were effective. As predicted by previous
et al., 1997). social psychology experiments (Batson et al., 2003;
Batson, Early, et al., 1997), adopting the perspective of
the other evoked stronger empathic concern, whereas
Behavioral Data
personal distress was higher when imagining oneself to
Data of the emotional response indices clearly confirm be in the painful situation. In addition, ineffective treat-
that perspective-taking and treatment-effectiveness ma- ment triggered higher personal distress when patients
were watched with the other-perspective. This might
indicate that participants did not focus on the sensory
Table 4. Areas Showing Significant ( p < .001) Correlations aspects of the observed pain, but rather its ultimate
between Hemodynamic Response, Behavioral Data, and unpleasantness or ‘‘badness’’ by taking into account the
Dispositional Measures
long-term consequences for the patient. Pain ratings
MNI Coordinates support this interpretation, as they were also modulated
Analysis and by treatment effectiveness—although no difference in
Brain Region L/R/M r x y z
patients’ actual expression of pain existed because pa-
Empathy Quotient—Other tients were naı̈ve to the treatment effectiveness. Further,
memory tests demonstrated significant effects of per-
Putamen R .837 26 0 10
spective-taking, as participants showed better recogni-
Insula L .795 36 2 12 tion and classification rates for patients watched using
aMCC M .826 0 4 42 the self-perspective. This finding is in line with studies
indicating that events that are more relevant for the self
Cerebellum L .833 22 46 24 are more likely to be remembered (‘‘self-referential
bias’’; Rogers et al., 1977).
Empathic Concern Index—Other
aMCC R .802 14 16 28
Shared Neural Circuits during Observation
and First-hand Experience of Pain
Emotional Contagion—Watching Pain
Insula R .867 30 16 12
Watching the video clips was associated with hemody-
namic changes in the medial and lateral occipital cortex
x IFG/Operculum R .847 44 18 8 (BA 18) and in the fusiform gyrus. These changes reflect
Insula L .848 32 10 10 the sensory processing of stimuli, as already reported in
previous neuroimaging studies using static and dynamic
aMCC/CCMA R .737 16 26 42
face stimuli (e.g., Botvinick et al., 2005; Grosbras & Paus,
SMA M .789 6 4 52 2006; Haxby, Hoffman & Gobbini, 2000). In addition, as
Precentral Gyrus R .740 50 14 44 predicted, the video clips elicited increased activity in a
number of areas associated with the first-hand experi-
Supramarginal Gyrus R .752 64 38 34 ence of pain, such as the insular cortex, dorsal and ven-
Inferior Parietal Lobe L .749 50 42 36 tral areas of the cingulate cortex, the thalamus, and areas
Inferior Parietal Lobe L .742 56 44 56
involved in motor control (basal ganglia, medial and
lateral premotor areas). The existence of shared neural
r = Pearson’s correlation coefficient, other abbreviations as in Table 2. circuits between the experience and the observation