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Emotion
2008, Vol. 8, No. 6, 781–791
Copyright 2008 by the American Psychological Association
1528-3542/08/$12.00 DOI: 10.1037/a0014195
Effects of Oxytocin and Prosocial Behavior on Brain Responses to Direct
and Vicariously Experienced Pain
Tania Singer and Romana Snozzi
Geoffrey Bird
University of Zurich
University College London
Predrag Petrovic
Giorgia Silani and Markus Heinrichs
Karolinska Institute
University of Zurich
Raymond J. Dolan
Wellcome Trust Centre for Neuroimaging, London, England
In this study, we tested the validity of 2 popular assumptions about empathy: (a) empathy can be
enhanced by oxytocin, a neuropeptide known to be crucial in affiliative behavior, and (b) individual
differences in prosocial behavior are positively associated with empathic brain responses. To do so, we
measured brain activity in a double-blind placebo-controlled study of 20 male participants either
receiving painful stimulation to their own hand (self condition) or observing their female partner
receiving painful stimulation to her hand (other condition). Prosocial behavior was measured using a
monetary economic interaction game with which participants classified as prosocial (N ⫽ 12) or selfish (N ⫽
6), depending on whether they cooperated with another player. Empathy-relevant brain activation
(anterior insula) was neither enhanced by oxytocin nor positively associated with prosocial behavior.
However, oxytocin reduced amygdala activation when participants received painful stimulation themselves (in the nonsocial condition). Surprisingly, this effect was driven by “selfish” participants. The
results suggest that selfish individuals may not be as rational and unemotional as usually suggested, their
actions being determined by their feeling anxious rather than by reason.
Keywords: empathy, pain, prosocial behavior, oxytocin, amygdala
Supplemental materials: http://dx.doi.org/10.1037/a0014195.supp
Past endeavors in neuroscientific research on empathy have
focused on the question concerning how we (our brains) know
what it feels like for another person to experience pain in the
absence of any stimulation to our own body. Theoretical conceptualizations of empathy (Decety & Jackson, 2004; Decety &
Lamm, 2006; de Vignemont & Singer, 2006; Gallese, 2003; Preston & de Waal, 2002) suggest that we understand other people’s
affective states via activation of neural networks usually involved
in processing our own affective states. Indeed, several human
fMRI studies have provided evidence for a role of such shared
neural networks that enable one to feel what it feels like for
another person to actually experience pain, touch, or disgust when
one merely observes or imagines the other person experiencing
pain, touch, or disgust— but receives no such stimulation oneself
(Avenanti, Bueti, Galati, & Aglioti, 2005; Avenanti, Paluello,
Bufalari, & Aglioti, 2006; Bufalari, Aprile, Avenanti, Di Russo, &
Aglioti, 2007; Cheng et al., 2007; Gu & Han, 2007; Jabbi, Swart,
& Keysers, 2007; Jackson, Brunet, Meltzoff, & Decety, 2006;
Jackson, Meltzoff, & Decety, 2005; Keysers et al., 2004; Lamm,
Batson, & Decety, 2007; Moriguchi et al., 2007; Morrison &
Downing, 2007; Morrison, Lloyd, di Pellegrino, & Roberts, 2004;
Saarela et al., 2007; Singer et al., 2004, 2006; Wicker et al., 2003).
In an early study, Singer et al. (2004), for example, investigated
empathy for pain when participants received pain themselves or
Social neuroscience has started uncovering the neural mechanisms underlying our capacity for empathy, that is, our capacity to
share and understand the feelings of others (de Vignemont &
Singer, 2006). The present study extends previous research on
empathy in addressing two distinct, currently unresolved questions. It investigates (a) whether empathic brain responses can be
enhanced by oxytocin (OT), a neuropeptide that has been found to
be involved in the modulation of social affiliative and approach
behavior; and (b) whether individual differences in empathic brain
responses differ as a function of the type of prosocial behavior
observed in a standard economic trust game.
Tania Singer, Romana Snozzi, and Giorgia Silani, Center for the Study
of Social and Neural Systems, University of Zurich; Geoffrey Bird, Institute of Cognitive Neuroscience, University College London; Predrag
Petrovic Department of Clinical Neuroscience, Karolinska Institute;
Markus Heinrichs, Clinical Psychology and Psychobiology, Department of
Psychology, University of Zurich; Raymond J. Dolan, Wellcome Trust
Centre for Neuroimaging, London, England.
Correspondence concerning this article should be addressed to Tania
Singer, Center for the Study of Social and Neural Systems, University of
Zurich, Blümlisalpstrasse 10, CH– 8006 Zurich, Switzerland. E-Mail:
singer@iew.uzh.ch
781
782
SINGER ET AL.
witnessed their partners receiving pain. The authors showed that
the affective components of the pain matrix (anterior insula [AI]
and anterior cingulate cortex [ACC ]), activated when participants
received pain, were also activated vicariously for their partner’s
pain. This pattern of results has proven to be robust and was seen
using different pain stimuli and situations as well as when people
empathized with strangers (Botvinick et al., 2005; Jackson et al.,
2005; Lamm et al., 2007; Morrison et al., 2004; Singer et al.,
2006). Some studies have also provided evidence for a positive
correlation between magnitude of empathy-related activation and
individual differences as measured by questionnaires such as
Davis’s (1980) Interpersonal Reactivity Index (Jabbi et al., 2007;
Lamm et al., 2007; Singer et al., 2004, 2006). Empathic brain
responses are not only positively correlated with trait measures of
empathy, but also with online unpleasantness ratings (Cheng et al.,
2007; Jackson et al., 2005; Saarela et al., 2007). Furthermore, these
empathy-related brain activations appear to be modulated by factors such as the intensity of pain applied to the other (Avenanti et
al., 2006), cognitive appraisal (Lamm et al., 2007), previous experience with the empathy-inducing stimulus (Cheng et al., 2007),
and perceived fairness of the other (Hein & Singer, 2008; Singer
et al., 2006). However, to the best of our knowledge, no study has
ever looked at whether such empathic brain responses can also be
modulated by pharmacological interventions, for example, by the
administration of OT.
In nonhuman mammals, the neuropeptide OT has been shown to
play a central role in social behavior. More specific, research has
shown that it is associated with the ability to form social attachments and with affiliation, including parental care, pair bonding,
sexual behavior, and social memory (Carter, 1998; Insel & Young,
2001; Lim & Young, 2006; Young & Wang, 2004). In addition,
OT has been found to also decrease stress responses and anxiety in
social interactions (Bale, Davis, Auger, Dorsa, & McCarthy, 2001;
Neumann, Kromer, Toschi, & Ebner, 2000; Parker, Buckmaster,
Schatzberg, & Lyons, 2005). Receptors for the neuropeptide OT
are distributed in various brain regions (Landgraf & Neumann,
2004), including limbic regions such as the amygdala (Huber,
Veinante, & Stoop, 2005).
Recent research has shown that neuropeptides cross the blood–
brain barrier after intranasal administration (Born et al., 2002),
thus providing a useful method for studying the central nervous
system effects of OT in humans as well (Heinrichs & Domes,
2008). Recent studies using this method have suggested that OT is
also a potent modulator in the processing of social behavior in
humans (for a review, see Heinrichs & Domes, 2008). Specifically,
OT has been found to reduce endocrine and psychological responses to social stress (Heinrichs, Baumgartner, Kirschbaum, &
Ehlert, 2003), to modulate social memory (Heinrichs,
Meinlschmidt, Wippich, Ehlert, & Hellhammer, 2004), and to
increase trust, generosity, and the ability to infer the mental states
of another person (“mind reading”) (Domes, Heinrichs, Michel,
Berger, & Herpertz, 2007; Kosfeld, Heinrichs, Zak, Fischbacher,
& Fehr, 2005; Zak, Stanton, & Ahmadi, 2007). In general OT has
been assumed to play a crucial role in overcoming natural avoidance of proximity and facilitate approach behavior (e.g., Kosfeld et
al., 2005). Even though empathy is generally believed to be closely
related to prosocial, affiliation, and bonding behavior (for a discussion, see, e.g., Preston & de Waal, 2002) and has been suggested to be enhanced by OT in the literature (e.g., Zak et al.,
2007), this assumption has never explicitly been tested within the
context of an empathy paradigm. Thus, to examine the effects of
OT on empathy, we used the empathy-for-pain paradigm previously described by Singer et al. (2004).
We hypothesized that if OT really enhances empathy, its effect
should be revealed in an increase in subjective ratings of empathic
feelings as well as in increased activity in empathic brain responses in AI and ACC when participants are exposed to another
person’s suffering (other condition). If, however, as accumulating
new evidence suggests, OT effects are mostly mediated via the
amygdala, effects of OT should be observed in the nonempathy
condition when people receive pain (self condition), but not in the
empathy condition. Thus, previous studies examining empathy for
pain (Singer et al., 2004, 2006; see also, Lamm et al., 2007) have
shown enhanced activation of amygdala in the self but not in the
other condition. This prediction would not be in line with the
suggested social effects of OT but would be in line with recent
fMRI studies testing the effect of exogenously administered OT on
brain activation in humans exposed to emotional stimuli that
showed attenuated activation in amygdala after OT administration
(Baumgartner, Heinrichs, Vonlanthen, Fischbacher, & Fehr, 2008;
Domes, Heinrichs, Glascher, et al., 2007; Kirsch et al., 2005;
Petrovic, Kalisch, Singer, & Dolan, 2008). Note, however, that
these studies chose paradigms using mostly social stimuli known
to activate the amygdala such as fearful facial expressions. Using
the present paradigm, we compare for the first time a social
condition not involving amygdala responses and a nonsocial condition activating amygdala.
In addition to the investigation of modulatory effects on empathic brain responses induced by OT, we investigated a second
distinct but also unresolved question regarding the empathic brain:
Can we find evidence for the proposed association between individual differences in empathic brain responses and prosocial behavior? Prosocial behavior is a broad construct that includes helping behavior, cooperation, and altruism (Penner, Dovidio, Piliavin,
& Schroeder, 2005). Behavioral studies in the context of developmental psychology indeed have suggested that empathic concern
is, albeit weakly, correlated with helping behavior (Eisenberg,
Miller, et al., 1989). However, when empathy motivates helping
behavior and when it leads to distress and withdrawal remains
unclear (Batson & Shaw, 1991; de Vignemont & Singer, 2006;
Eisenberg, Fabes, et al., 1989). One problem related to psychological research on prosocial behavior is often the lack of experimentally controlled laboratory tasks for the quantitative assessment of
prosocial behavior. In the context of economics research, by contrast, prosocial behavior is operationalized in terms of choices
people make in interactive games with monetary incentives.
Prosocial behavior, or altruism, is then defined as costly acts that
increase another person’s benefits (Fehr & Fischbacher, 2003). In
this study, we used a well-known economic game, the trust game
(Ashraf, Bohnet, & Piankov, 2006; Berg, Dickhaut, & McCabe,
1995), to assess differences in prosocial behavior. In the trust
game, Player 1 has the opportunity to send money to Player 2,
knowing that every unit sent will be doubled by the experimenter
and in the hope that Player 2 will send more money back. Player
2 then decides how much money to send back to Player 1, knowing
that he can maximize his own profit by not sending any at all. On
the basis of this decision, Player 2 can be classified as prosocial
(conditional cooperators) or selfish (personal income maximizers).
SPECIAL SECTION: EMPATHY, PROSOCIAL BEHAVIOR, AND OXYTOCIN
We expected that these individual differences in trust game behavior predicted individual differences in empathic brain responses expected to be observed in AI and ACC.
Method
Participants
We scanned 21 healthy, right-handed, male participants who
were asked to come to the scanning sessions with their romantic
partner. One participant was excluded from the analysis due to data
loss. The participants ranged in age from 20 to 31 with a mean age
of 24.6 years (SD ⫽ 3.2). All participants gave informed consent
and the study was approved by the local research ethics committee.
Procedure
Participants came for two sessions scheduled, on average, 10
days apart (M ⫽ 10.4 days, SD ⫽ 4.33, minimum [min.] ⫽ 2,
maximum [max.] ⫽ 14). In a first step, OT or a placebo was
administered with a nasal spray. It has been shown that neuropeptides pass the blood– brain barrier reliably after intranasal application (Born et al., 2002). Several studies using this method have
reported OT-dependent effects on either behavior or brain function
(Baumgartner et al., 2008; Domes, Heinrichs, Michel et al., 2007;
Heinrichs et al., 2003, 2004; Kirsch et al., 2005; Kosfeld et al.,
2005; Petrovic et al., 2008; Pitman, Orr, Lasko, 1993). The spray
was administered to participants four times with a delay of 45 s
between administrations, each administration consisting of one
inhalation of the spray into each nostril. Each inhalation contained
approximately 4 IU; participants thus received a total of 32-IU OT
in the OT condition. Session (OT, placebo) order was randomized using a double-blind procedure. Scanning began roughly
45 min after spray administration (M ⫽ 45.8, SD ⫽ 2.7, min. ⫽
42, max. ⫽ 55).
The empathy-for-pain paradigm was similar to the one used in
Singer et al. (2004). In brief, by means of a system of mirrors,
participants saw their own and their partner’s hand lying on a tilted
board. Pain electrodes were attached to the dorsum of their hands.
On a screen they saw an arrow pointing to one of the hands,
indicating whether the participant or his partner would be stimulated next. The color of the arrow indicated whether the stimulation would be painful or nonpainful. In contrast to Singer et al., the
self and other conditions were blocked. In the self condition, to
prevent the participants’ experience of the effect of OT on pain
processing from altering their empathic response, participants
started with the empathy condition. Also, after each trial of painful
or nonpainful stimulation to self or other, participants indicated
how they felt about the stimulation by rating the degree of unpleasantness/pleasantness on an analogue rating scale ranging
from ⫺10 (very unpleasant) to ⫹10 (very pleasant).
Behavioral and Questionnaire Measures
All participants filled out the Interpersonal Reactivity Index
(IRI; Davis, 1980), a questionnaire used to assess empathy, and the
State–Trait Anxiety Inventory (STAI; Spielberger, Gorsuch, Lushene, Vagg, & Jacobs, 1983), which is used to assess anxiety level.
Prosocial behavior was assessed using a trust game, for which the
participants were randomly paired with an anonymous player from
783
the University of Nottingham, who had played the game several
weeks before at the School of Economics. The Nottingham players’ decisions were kept in anonymous envelopes and used as the
Player 1 decisions. The participants in London (who were the ones
being scanned) were Player 2s. (For more details, see Supplementary Material A). Both players received an endowment of £5.
Player 1s decided whether they wanted to keep their money or
transfer it to Player 2. The experimenter then doubled the amount
of money transferred. Player 2s decided whether they wanted to
transfer their money given that (a) Player 1 had transferred his or
her money or that (b) Player 1 had not transferred his or her
money. After this decision, each Player 2 was paired at random
with a Player 1 and paid according to the two players’ decisions.
Later, Player 2s were classified as “prosocial” if they had decided
to cooperate if Player 1 had cooperated. They were classified as
“selfish” if they had decided to keep the money even if Player 1
had sent their money. Thus, “selfish participants” had chosen to
optimize their own reward at Player 1’s expense and to keep their
£5 even though they had received £10 from Player 1 (who consequently was left with no money at all).
Image Acquisition and Analysis
The imaging data (T2ⴱ-weighted echo planar images, EPI) measuring blood oxygen level dependent (BOLD) contrast were acquired using a 1.5-Tesla Siemens Sonata system. To reduce inhomogeneities in amygdala and orbitofrontal cortex, we used a
sequence with axial slices tilted by 30° and a flip angle of 90° that
reduces signal dropout due to susceptibility-induced field inhomogeneities in amygdala and orbitofrontal cortex (O’Doherty, Deichmann, Critchley, & Dolan, 2002). Our field of view covered the
whole brain in 44 planes. We had a TR of 3.96 s (90 ms per slice).
Each run began with six “dummy” volumes discarded for analyses.
At the end of each scanning session, a T1-weighted structural
image was acquired.
The data were preprocessed and analyzed with SPM5 (Wellcome Department of Imaging Neuroscience, London; www.fil
.ion.ucl.ac.uk/spm). Scans were first realigned, normalized, and
spatially smoothed by a 10 mm full-width half-maximum Gaussian
kernel (6 mm at the first level, 8 mm at the second level). A
high-pass filter (with a cut-off at 128 s) was applied to the time
series. The data was then analyzed in an event-related fashion. The
experiment constituted a 2 ⫻ 2 ⫻ 2 factorial design with the first
factor representing the drug condition (OT vs. placebo), the second
factor the pain condition (pain vs. no pain), and the third factor the
target condition (self vs. other). The conditions for each participant
were modeled within a fixed effects general linear model. The
resulting beta estimate maps were then taken to a second-level
group analysis and the significance of contrasts of interest assessed
within a random effects framework to allow statistical inference
across the population. On the second level, one-sample t tests were
used to assess the main effects of pain, drug, and target and the
interaction between the three factors. Unpaired two-sample t tests
were used to assess the difference in activation between the selfish
and prosocial participants. In addition, linear contrasts between
pain and no pain for self and other in the placebo condition were
computed to assess both the pain matrix and empathic brain
responses. Shared pain-related networks in self and other were
assessed by computing a conjunction analysis on (pain vs. no pain)
SINGER ET AL.
784
in self and (pain vs. no pain) in other in the placebo condition
alone. Regression analyses were computed to assess correlations
between empathic brain responses and subjective unpleasantness
ratings. Inclusive masking procedures (set on a threshold of p ⬍
.05, uncorrected) were used in the regression analysis to restrict
activation to the brain areas observed in the simple contrast of:
other ⫻ (pain versus no pain). Effects of OT were assessed by
computing the contrasts: OT ⫻ (pain versus no pain) – placebo ⫻
(pain versus no pain) and placebo ⫻ (pain versus no pain) – OT ⫻
(pain versus no pain).
We report results in a priori regions of interest at p ⬍ .001
uncorrected for multiple comparisons with an extent threshold of
minimally eight contiguous voxels, except for the pain matrix
(pain vs. no pain in self in the placebo condition) in which a
slightly higher threshold was used ( p ⬍ .0001, uncorrected). Small
volume corrections (SVC) were applied for an anatomically defined mask around bilateral amygdala, defined according to the
Wake Forest University (WFU) PickAtlas software (http://
fmri.wfubmc.edu/cms/software).
Results
Behavioral Results
Table 1 provides descriptive statistics for the full sample as well
as for subsamples of prosocial participants and selfish participants
for age, education, and IRI and STAI scores. Subjective unpleas-
Table 1
Descriptive Characteristics of the Total and the Two Subsamples
Age
M
SD
Education
M
SD
IRI, total score
M
SD
IRI, perspective taking
M
SD
IRI, fantasy scale
M
SD
IRI, empathic concern
M
SD
IRI, personal distress
M
SD
State anxiety
M
SD
Trait anxiety
M
SD
Prosocial
versus selfishd
Alla
Prosocialb
Selfishc
24.60
3.22
25.33
3.28
22.67
2.94
p ⫽ .11
5.60
2.34
5.75
2.73
5.67
1.97
p ⫽ .95
62.60
7.50
61.63
8.89
64.92
2.87
p ⫽ .26
16.10
4.17
16.08
3.99
17.17
4.71
p ⫽ .62
15.50
3.59
14.88
3.34
15.92
4.54
p ⫽ .59
19.25
2.69
18.83
2.86
19.50
2.74
p ⫽ .64
11.75
3.46
11.83
3.76
12.33
2.66
p ⫽ .78
33.00
7.86
31.58
6.67
36.67
10.07
p ⫽ .22
35.83
7.31
36.38
7.95
34.17
4.79
p ⫽ .54
Note. Education ⫽ years of education after age 16; IRI ⫽ Interpersonal
Reactivity Scale.
a
N ⫽ 20. b n ⫽ 12. c n ⫽ 6. d Unpaired t tests, two-tailed.
antness ratings were computed as the difference between average
ratings in the pain minus the no-pain condition. The unpleasantness ratings of one of the participants were not used for the
analysis due to a lack of reliable ratings. The average unpleasantness ratings are depicted in Figure 1. They were significantly
higher in the self than in the other condition, placebo: t(19) ⫽ 4.20,
p ⬍ .01; OT: t(19) ⫽ 3.32, p ⬍ .01. There was no significant
difference between the average unpleasantness ratings in the placebo and the OT condition, self: t(19) ⫽ .20, p ⫽ .85; other:
t(19) ⫽ .85, p ⫽ .41. Individual differences in empathy (IRI) and
anxiety (STAI) were not correlated with unpleasantness in any
condition.
Next, we classified participants based on their behavior in the
trust game. Of the 20 participants in our study, we observed 12
prosocial participants who reciprocated the other’s trust and 6
selfish participants who maximized their income regardless of
their partner’s behavior. Two participants were not classifiable
according to this distinction, as they decided to send their money
to Player 1 even though Player 1 had not sent any money to them.
To test whether the two types differed with respect to their behavioral unpleasantness ratings, we performed a 2 ⫻ 2 ⫻ 2 analysis of
variance (ANOVA) with prosociality (prosocial/selfish) as a
between-subjects factor and drug (OT/placebo) and target (self/
other) as within-subject factors. This ANOVA did not show any
differences for the prosociality and drug factors, but did show a
significant difference for the target factor, F(1, 16) ⫽ 21.7, p ⬍
.001, with higher pain ratings when the participants received pain
as compared to empathizing with the pain of others. None of the
interaction terms were significant. Unpaired t comparisons revealed that the two types neither differed on scores for the different
subscales of the IRI nor on scores of the STAI (see Table 1). In
sum, prosocial and selfish participants did not show any major
behavioral differences.
Brain Imaging Results
Empathy. To identify the pain matrix, we computed a contrast
between painful and nonpainful stimulation trials for the self in the
placebo condition (placebo: self [pain–no pain]). We observed a
typical pattern, shown in previous pain studies (e.g., Singer et al.,
2004, 2006), involving activation in SI and SII; posterior, mid, and
anterior insula; operculum; dorsal and rostral parts of ACC; preSMA; cerebellum; amygdala; and the ventral striatum (see Supplementary Material, Table 1). Also in line with previous findings,
the comparison of brain activation in participants observing their
partner receiving painful versus nonpainful stimulation (placebo:
other (pain–no pain]) revealed activation in right AI extending into
the operculum as well as activation foci in thalamus and left
lingual gyrus (see also Table 2). A conjunction analysis testing for
shared activation between the self and the other condition (placebo: self [pain–no pain] ⫹ other [pain–no pain]) showed activation
in the right thalamus and the right AI (see Table 2 and Figure 2)
confirming previous findings of a critical role for AI in empathy
for pain.
To test whether individual differences in subjectively perceived
unpleasantness correlated with empathic brain responses, we performed a regression analysis with the subjective ratings using the
contrast (placebo: other (pain–no pain]). This revealed a correlation with the right AI/operculum and the ACC (see Table 2 and
SPECIAL SECTION: EMPATHY, PROSOCIAL BEHAVIOR, AND OXYTOCIN
Figure 1. Subjective unpleasantness ratings: Average unpleasantness ratings for the conditions self (green) and other (red), placebo (filled), and
oxytocin (shaded) with error bars (SEM), ⴱ p ⬍ .01.
Figure 3). A comparable regression analysis with the IRI did not
reveal any significant correlation in empathy-relevant brain areas,
neither for the IRI total nor for any of the subscales. Overall,
however, these results replicate previous findings of an important
role of AI and ACC in empathic brain responses elicited when
observing another person suffering pain (de Vignemont & Singer,
2006; Singer et al., 2004, 2006).
OT. To test the effects of OT on both pain-related processing
in the self as well as on empathic brain responses, we compared
pain-related activation (pain–no pain) in self and other in the
placebo compared to the OT condition. Table 3 provides an overview of the results. For the self condition, higher activation for the
OT compared to placebo condition (self: OT [pain–no pain] –
placebo [pain–no pain]) were found mainly in orbitofrontal regions. In line with previous findings showing a reduction of
amygdala response due to the administration of OT, the reverse
contrast (self: placebo [pain–no pain] – OT [pain–no pain]) revealed higher activation in the right amygdala extending into
ventral striatum and the midbrain in the placebo compared to the
OT condition. With respect to the other condition, right OFC
activation was observed for the contrast (other: OT [pain–no pain)
– placebo [pain–no pain]). However, contrary to our hypothesis of
OT-induced enhancement of activation in empathy-relevant brain
networks, no significant activation was observed when testing for
significantly higher activation in the placebo compared to the OT
condition for others (other: placebo [pain–no pain] – OT [pain–no
pain]). To ensure we were not missing OT-related modulation in
empathy-relevant brain regions due to insufficient power, we lowered the threshold to p ⬍ .01, but still no difference in the
785
magnitude of activation in the right AI or ACC was observed
between the two drug conditions.
Prosociality. The second goal of this study was to investigate
whether there is a predictive link between prosocial behavior and
empathic brain responses. To this end, we first focused only on the
placebo condition and compared brain responses in the self and
other condition for the prosocial and selfish participants (see Table 4).
In the self condition, prosocial participants showed higher activation in medial PFC (placebo, self: prosocial [pain–no pain] –
selfish [pain–no pain]). Selfish participants, on the other hand,
showed higher activation in right TPJ, SFG, and cerebellum (placebo, self: selfish [pain–no pain] – prosocial [pain–no pain]). In
contrast to the hypothesis that prosocial as compared to selfish
participants show higher activation in empathy-relevant brain areas, the contrast (placebo, other: prosocial [pain–no pain] – selfish
[pain–no pain]) did not show significant activation, neither in right
AI nor in ACC nor in any other brain regions. To assure again that
this lack of differential findings was not based on a lack of power,
we lowered the threshold to p ⬍ .01, but could not detect any
significant differences in empathy-relevant brain areas between
prosocial and selfish participants.
Based on our two independent observations of OT effects on
amygdala responses in the self condition and effects of prosocial
types on amygdala responsivity to impending pain in self, we
finally also tested whether the effects of OT in the self condition
were different for prosocial and selfish participants (see Table 5).
This three-way interaction of pain versus no pain, OT versus
placebo, and prosocial versus selfish participants indeed revealed
significant activation in amygdala and mPFC. These activations
and associated contrast estimates for the peak in the triple interaction within the amygdala are depicted in Figure 4. As Figures 4
illustrates, the three-way interaction is attributable to high activations in the amygdala for selfish participants in the placebo con-
Table 2
Empathic Brain Responses and Regression Analysis
Region
Pain minus no pain in other,
placebo
R AI
R operculum
R AIa
R thalamus
L lingual gyrus
Conjunction of pain minus
no pain in self and
other, placebo
R AI
R AIa
R thalamus
Regression of
unpleasantness ratings
on pain minus no pain
in other, placebo
Operculum/AI
Operculum/AIa
ACC
Cluster size
x
y
z
Z scores
15
30
30
54
45
6
–18
27
24
21
–12
–57
6
6
0
3
–6
3.51
3.61
3.36
4.15
3.56
33
42
6
27
21
–12
6
–3
3
3.59
3.22
4.13
57
48
–9
24
24
12
3
12
39
4.69
3.25
4.07
26
8
19
26
28
11
Note. p ⬍ .001, uncorrected; cluster size ⬎ 7 voxels. R ⫽ right; L ⫽ left;
AI ⫽ anterior insula; ACC ⫽ anterior cingulate cortex.
a
Sub-maxima within a cluster.
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SINGER ET AL.
Figure 2. Empathic brain responses: Activation in the right anterior insula (AI) revealed by conjunction
analyses depicting shared activation in painful versus nonpainful trials in the self and other placebo condition.
Threshold is set at p ⬍ .001, uncorrected.
dition which are suppressed in the OT condition. Based on these
findings, we tested the hypothesis that activation in the amygdala
is higher for selfish than prosocial participants using a lowered
threshold for the contrast (placebo, self: selfish [pain–no pain] –
prosocial participants [pain–no pain]). Indeed, we found a significantly higher activation in the right amygdala for the selfish
participants on a threshold of p ⬍ .002. An inspection of the betas
in mPFC revealed that this three-way interaction was due to selfish
participants showing decreased activation in the self placebo condition and an increased activation in the self OT condition, which
is the opposite of the previously described amygdala pattern (see
Supplementary Material, Figure 1).
Discussion
The aim of this study was twofold: First, using a classical
empathy paradigm, we wanted to test the hypothesis that administration of OT enhances empathy. If OT enhances empathic brain
responses as studies reporting enhancing effects of OT on trust,
approach, bonding, and affiliative behavior in animals and humans
suggest, we should observe an increase in brain activity in
empathy-relevant brain regions, namely ACC and AI. However, if
OT-induced effects are mostly mediated via the amygdala as
recent fMRI studies suggested (Baumgartner et al., 2008; Domes,
Heinrichs, Glascher et al., 2007; Kirsch et al., 2005; Petrovic et al.,
Figure 3. Individual differences in empathic brain responses: (A) Correlation of parameter estimates in the
anterior insula/operculum for (pain vs. no pain) in the placebo other condition and subjective unpleasantness
ratings. (B) Activation revealed in anterior insula/operculum for the contrast (pain vs. no pain) in the placebo
other condition (red) and for the regression analysis of unpleasantness ratings on the contrast (pain vs. no pain)
in the placebo other condition (yellow). Threshold is set at p ⬍ .001, uncorrected.
SPECIAL SECTION: EMPATHY, PROSOCIAL BEHAVIOR, AND OXYTOCIN
Table 3
Effects of Oxytocin for (Pain Versus No Pain) in Self and Other
Self oxytocin ⬎ placebo
R medial OFC
R medial OFC
R medial OFCa
R lateral OFC
Self placebo ⬎ oxytocin
R amygdala/striatum
Midbrain
Other oxytocin ⬎ placebo
No significant activation
Other placebo ⬎ oxytocin
R OFC
Cluster size
x
y
z
Z scores
27
25
8
18
15
6
45
27
66
60
42
–24
–12
–9
–15
4.65
3.42
3.25
3.29
18
27
24
6
0
⫺9
–12
–12
3.92ⴱ
3.88
8
27
27
–18
3.99
Note. p ⬍ .001, uncorrected (except where noted otherwise); family wise
error corrected after small volume correction, cluster size ⬎ 7 voxels. R ⫽
right; OFC ⫽ orbitofrontal cortex.
a
Sub-maxima within a cluster.
ⴱ
p ⬍ .05.
2008), we should observe an effect of OT in the nonsocial self
condition, that is, when participants process nociceptive stimuli
but not in the social empathy condition. This latter hypothesis is
derived from previous studies in which amygdala has been shown
to be activated in the self condition (Singer et al., 2004, 2006), but
not when empathizing with another person.
The second goal of the study was to test another implicit, but
never tested, assumption about the empathic brain, namely that
individual differences in prosocial behavior predict empathic brain
responses. If the hypothesis is true, we should find enhanced
empathy-relevant activation in AI and ACC in prosocial as compared to selfish participants as measured in a standard economic
trust game.
Our results neither revealed that OT enhances empathic responses nor that the prosocial participants showed higher empathic
brain responses. Rather, in line with previous OT studies (Baum-
787
Table 5
Effects of Oxytocin in Prosocial and Selfish Participants
Self placebo ⬎ oxytocin,
prosocial ⬎ selfish
Medial PFC
L fronto-insular PFC
L fronto-insular PFCa
Self placebo ⬎ oxytocin,
selfish ⬎ prosocial
R amygdala
L amygdala
Cluster size
x
y
z
Z scores
21
18
–9
–33
–27
63
42
33
0
–3
–6
4
3.52
3.32
19
8
15
–21
–9
–9
–18
–24
3.57ⴱ
3.59
Note. Table depicts three-way interactions for the factors drug, pain, and
prosociality in the self condition. p ⬍ .001, uncorrected (except where
noted otherwise). Family wise error corrected after small volume correction, cluster size ⬎ 7 voxels. PFC ⫽ prefrontal cortex; L ⫽ left; R ⫽ right.
a
Sub-maxima within a cluster.
ⴱ
p ⬍ .05.
gartner et al., 2008; Domes, Heinrichs, Glascher et al., 2007;
Kirsch et al., 2005), we demonstrated a modulation by OT of
amygdala activation when participants processed nociceptive stimulation in the self condition. Activity in amygdala in the self
condition was lower after OT was administered exogenously compared to the placebo condition. Surprisingly, this effect seems to
have been driven by the selfish participants alone: selfish, but not
prosocial, participants showed enhanced amygdala activation
when confronted with nociceptive stimulation and hence an OTinduced reduction.
Table 4
Effects of Prosociality for (Pain Versus No Pain) in Placebo
for Self
Self prosocial ⬎ selfish
Medial PFC
Medial PFCa
Self selfish ⬎ prosocial
R TPJ
R SFG
R cerebellum
R amygdala
Other prosocial ⬎ selfish
No significant activation
Other selfish ⬎ prosocial
No significant activation
Cluster size
x
y
z
Z scores
14
–6
–12
63
69
0
0
18
8
13
11
54
27
42
21
–36
30
–75
–3
30
57
–27
–15
3.57
3.35
3.87
3.69
3.56
2.85ⴱ
Note. p ⬍ .001, uncorrected (except where noted otherwise); cluster
size ⬎ 7 voxels. PFC ⫽ prefrontal cortex; R ⫽ right; TPJ ⫽ temporoparietal junction; SFG ⫽ superior frontal gyrus.
a
Sub-maxima within a cluster.
ⴱ
p ⬍ .002, uncorrected.
Figure 4. Effects of oxytocin and types on amygdala: The bar diagram
illustrates parameter estimates derived from the right amygdala (21, ⫺3,
18) revealed in the three-way interaction (pain, drug, prosociality) in self.
Contrast estimates on the contrast (pain vs. no pain) are shown for the self
(green) and the other (red) in the placebo (filled), and oxytocin (shaded)
conditions, separately for prosocial and selfish participants. Threshold is
set at p ⬍ .001, uncorrected.
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SINGER ET AL.
Empathic Brain Responses and Prosocial Behavior
The results of the analyses focusing on brain activation elicited
when participants either received nociceptive stimulation (self
condition) or vicariously experienced their partner’s pain (other
condition) largely replicated previous results obtained with a similar paradigm (e.g., Singer et al., 2004, 2006). The pain matrix
encompassed a complex network including primary and secondary
somatosensory cortices; posterior, mid, and anterior parts of the
insular cortices; operculum; dorsal and rostral parts of the ACC;
pre-SMA; cerebellum; amygdala; and the ventral striatum. When
participants empathized with their partners in pain, activation was
observed in right AI extending into operculum and the right
thalamus.
The anterior parts of the insular cortices are the most consistently reported areas in studies on empathy for pain (Botvinick et
al., 2005; Jackson et al., 2005; Lamm et al., 2007; Morrison et al.,
2004; Singer et al., 2004, 2006). Previous findings showed correlations of individual differences in empathic brain responses in AI
and ACC with behavioral and questionnaire measures of empathy
(Cheng et al., 2007; Jackson et al., 2005; Saarela et al., 2007;
Singer et al., 2004, 2006). Consistent with these studies, we also
found a positive correlation of activations in right AI/operculum
and ACC with subjective unpleasantness ratings assessed after
each stimulation trial. Thus, participants who felt more unpleasant
about their partners experiencing pain also showed higher activation in these empathy-relevant brain areas. In contrast to the Singer
et al. (2004, 2006) studies, the correlations between individual
differences in empathy questionnaires (IRI) and empathic brain
networks did not reach significance in this study (nonsignificant
correlations between the IRI and empathic brain responses were
also reported in Jackson et al., 2005; Lamm et al., 2007). We also
failed to demonstrate enhanced ACC activation in the empathy
condition in our sample despite the fact that we observed a positive
correlation of activation in ACC and individual differences in
unpleasantness ratings. This lack of increased ACC activation on
a group level during the empathy condition parallels the findings
of the Singer et al. (2006) study, which also only found reliable
activation in ACC for the female participants (see also Singer et
al., 2004), not for the male participants. Taking all empathy-forpain studies into account, the AI seems to be more reliably activated across both genders than the ACC.
Despite the observation of reliable individual differences in
empathic brain responses, we were still not able to find evidence
to support the assumption that prosocial behavior predicts differences in empathic brain responses. Prosocial as compared to selfish participants (as assessed with a sequential trust game) did not
differ in magnitude of brain responses in AI and ACC. As is the
case for null findings, there are multiple interpretations for the lack
of a difference in empathy between prosocial and selfish participants. First, because there were only six selfish participants, an
obvious explanation for the lack of an effect is small sample size.
On the other hand, other performed analyses showed reliable
effects of prosociality (prosocial vs. selfish) in other brain regions
(e.g., amygdala) using the same threshold. Second, a lack of an
association between empathy and prosocial behavior may reflect
the measure used to assess prosociality. Even though we used one
of the most widely applied measures of prosociality in economics,
it may nevertheless be insufficient in differentiating between dif-
ferent facets of prosocial behavior. In fact, we used the strategy
method in the trust game (i.e., participants were to state what they
would in the event of every possible action of the other player),
which is weighted toward what is often referred to as cold reasoning, in which emotional involvement is low (Brosig, Weimann,
& Yang, 2003). Empathy, however, is more related to hot reasoning, in which emotions are integral to decision making. In addition,
the decision to engage in conditional cooperation or defection in
this trust game may reflect what economists call fairness preferences rather than empathic motivation. In other words, participants
may base their decision on social norms (e.g., “if someone offers
me cooperation, I should reciprocate”) rather than on an empathic
feeling driven by an imaginative representation of the other’s
emotions and a felt concern for the other.
Future research might focus usefully on the development of
adequate behavioral measures that are able to differentiate between
different forms of prosociality and their underlying motivation so
that, for example, fairness-based cooperative behavior can be
distinguished from empathy-based helping behavior. This speaks
to the simple fact that prosocial behavior is so far at best a vaguely
defined construct that encompasses many different forms of otherregarding behavior. The development of new laboratory tasks is
needed to differentiate between subcomponents of prosocial behavior and their relation to empathy.
Empathic Brain Responses and Effects of OT
We also failed to find evidence for an OT-induced increase in
subjective empathy ratings or enhanced activation in empathyrelevant brain regions such as AI and ACC. In contrast and in line
with previous findings showing that exogenously administrated
OT in humans primarily affects amygdala activation (Baumgartner
et al., 2008; Domes, Heinrichs, Glascher et al., 2007; Ferguson,
Aldag, Insel, & Young, 2001; Huber et al., 2005; Kirsch et al.,
2005), we observed an OT-induced reduction of amygdala activation elicited by the anticipation and processing of noxious stimuli
in the self condition.
Inspection of previous studies using a similar empathy-for-pain
paradigm (Singer et al., 2004, 2006) confirmed that, on a group
level, enhanced amygdala activation is typically observed when
participants anticipate and experience pain (self condition), but not
when they empathize with the pain of others (other condition).
Furthermore, using their paradigm, Lamm et al. (2007) also reported activation in the amygdala that was stronger when the
participants were asked to imagine the pain from a first-person as
compared to a third-person perspective. As a consequence, amygdala activation would not be expected in the empathy condition. In
the present paradigm, the short prestimulus interval between
flashes indicative of impending pain and the circle indicative of
actual receipt of nociceptive stimulation does not allow us to infer
whether amygdala activation reflects an anticipatory anxiety response or the actual processing of pain itself. The literature on
amygdala function seems to suggest that the amygdala is rather
involved in anticipatory fear processing rather than in pain processing itself (Adolphs, 2002; LeDoux, 2003; Peyron, Laurent, &
Garcia-Larrea, 2000; Rosen & Donley, 2006; but see Zald, 2003).
For example, in a study by Phelps et al. (2001), participants
showed increased amygdala activation in response to the sight of
a symbol indicative of a possible future noxious stimulation, and
SPECIAL SECTION: EMPATHY, PROSOCIAL BEHAVIOR, AND OXYTOCIN
this response was observed even though the painful stimulation
never actually occurred.
Reduced amygdala activation due to OT has been shown in
previous fMRI studies using a similar protocol to exogenously
apply OT via a nasal spray (Baumgartner et al., 2008; Domes,
Heinrichs, Glascher et al., 2007; Kirsch et al., 2005; Petrovic et al.,
2008). However, the present study revealed an interesting new
result that throws light on the interpretation of OT effects. Previous
behavioral and imaging results of OT studies mostly have been
discussed in the context of a specific effect of OT for social stimuli
and behavior. Thus, OT in animals has been shown to be associated with attachment and affiliative behavior including pair bonding, maternal care, and sexual bonding (Campbell, 2007; Carter,
1998; Insel & Shapiro, 1992; Insel & Young, 2001; Lim & Young,
2006; Pedersen, 1997). In humans, exogenously administered OT
has been shown to reduce psychosocial stress responses (Heinrichs
et al., 2003), increase trusting behavior (Kosfeld et al., 2005),
enhance generosity in a social interaction task (Zak et al., 2007),
and improve mindreading ability (Domes, Heinrichs, Michel et al.,
2007). The results of the present study demonstrate an effect of OT
on amygdala response elicited by upcoming noxious stimulation
that does not have a social component. Similarly, Kirsch et al.
observed OT-based reduction of amygdala responses both when
participants were presented with fearful faces but also when they
viewed nonsocial but fearful scenes. These results might suggest
that the common denominator is fear-elicited amygdala activation
rather than activation elicited by social stimuli. However, socially
salient stimuli such as facial emotional expressions seem to be
potent drivers of amygdala activation. Carefully designed future
studies will have to further investigate the relationship between the
effects of OT on amygdala activation and social context.
Empathic Brain Responses, Prosocial Participants, and
the Effects of OT
Surprisingly, the three-way interaction between pain/no pain,
OT/placebo, and prosocial/selfish for the self condition also revealed amygdala activation. This effect seems to have been driven
by the selfish participants alone. As compared to prosocial participants, selfish participants showed significantly higher activation
in the amygdala for pain versus no pain in the self placebo
condition. Consistently, when testing painful versus nonpainful
trials in the self placebo condition for prosocial participants only,
no significant amygdala activation was observed. Consequently,
OT was not able to reduce amygdala responses in the group of
prosocial participants.
Even though heightened amygdala reactivity in selfish participants, reduced by OT, was not hypothesized a priori, this finding
could have important implications for economic theory if replicable. In economic game theory, selfish participants are usually
conceived of as rational players who seek to maximize their own
reward and do not care about another player’s reward. The observation that selfish participants show stronger amygdala reactivity
to noxious stimulation points in a completely different direction.
As described above, amygdala responses are known to play an
important role in emotion and fear processing (Adolphs, 2002;
LeDoux, 2003; Rosen & Donley, 2006). A recent meta-analysis
shows that patients with different anxiety disorders have heightened activity in the amygdala (Etkin & Wager, 2007). Moreover,
789
the strength of amygdala activation has been linked to dispositional traits such as neuroticism and negative attributional style
(Fischer, Tillfors, Furmark, & Fredrikson, 2001; Haas, Omura,
Constable, & Canli, 2007). These findings can be interpreted as
indicating that amygdala responsivity reflects a bias toward threatrelated responses (Bishop, 2007). Accordingly, our results of
heightened amygdala responses to noxious stimuli could suggest
that selfish people are actually rather high in anxiety and more
biased toward threat-related responses rather than nonemotional,
rational people.
This interpretation would suggest that selfishness is related to
anxiety and mistrust toward others. Within this frame of reference,
selfish behavior may be the result of a strategy to avoid anticipated
negative outcomes. We acknowledge that such an interpretation
does not preclude the existence of two types of selfish participants,
one being completely rational, coldblooded, reward maximizing
and the other overly vigilant and anxious. In the present small
sample, we could not detect significant differences between scores
in state and trait anxiety for the two types. To validate the plausibility of such a hypothesis and generalize the present findings to
the entire population, future behavioral studies will have to test
different trust and anxiety tasks in a much larger and heterogeneous sample and future fMRI studies will have to replicate the
observation of enhanced amygdale responses in egoistic types in
the context of other fear-related paradigms. If replicable these
findings may help a better understanding of the mechanisms and
motivations underlying trusting and cooperative behavior in human societies and may have also important implication for the
advancement of institutional designs.
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Received January 22, 2008
Revision received July 23, 2008
Accepted July 25, 2008 䡲
Call for Nominations
The Publications and Communications (P&C) Board of the American Psychological Association
has opened nominations for the editorships of Developmental Psychology, Journal of Consulting
and Clinical Psychology, and Psychological Review for the years 2011–2016. Cynthia Garcı́a
Coll, PhD, Annette M. La Greca, PhD, and Keith Rayner, PhD, respectively, are the incumbent
editors.
Candidates should be members of APA and should be available to start receiving manuscripts in
early 2010 to prepare for issues published in 2011. Please note that the P&C Board encourages
participation by members of underrepresented groups in the publication process and would particularly welcome such nominees. Self-nominations are also encouraged.
Search chairs have been appointed as follows:
● Developmental Psychology, Peter A. Ornstein, PhD, and
Valerie Reyna, PhD
● Journal of Consulting and Clinical Psychology, Norman Abeles, PhD
● Psychological Review, David C. Funder, PhD, and Leah L. Light, PhD
Candidates should be nominated by accessing APA’s EditorQuest site on the Web. Using your
Web browser, go to http://editorquest.apa.org. On the Home menu on the left, find “Guests.” Next,
click on the link “Submit a Nomination,” enter your nominee’s information, and click “Submit.”
Prepared statements of one page or less in support of a nominee can also be submitted by e-mail
to Emnet Tesfaye, P&C Board Search Liaison, at etesfaye@apa.org.
Deadline for accepting nominations is January 10, 2009, when reviews will begin.
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