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Human Brain Mapping 38:4034–4046 (2017)
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Mindfulness Meditation Regulates Anterior Insula
Activity During Empathy for Social Pain
Davide Laneri,1 S€
oren Krach,2 Frieder M Paulus,2 Philipp Kanske,3
Verena Schuster,1 Jens Sommer,1 and Laura M€
uller-Pinzler 2*
1
Department of Psychiatry and Psychotherapy, Philipps-University Marburg, Rudolf-Bultmann Strasse 8, Marburg, 35039, Germany
2
€beck,
Department of Psychiatry and Psychotherapy, Social Neuroscience Lab, University of Lu
€
Ratzeburger Allee 160, Lubeck, 23538, Germany
3
Department of Social Neuroscience, Max Planck Institute for Human Cognitive and Brain
Sciences, Stephanstr. 1a, Leipzig, 04103, Germany
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Abstract: Mindfulness has been shown to reduce stress, promote health, and well-being, as well as to increase
compassionate behavior toward others. It reduces distress to one’s own painful experiences, going along with
altered neural responses, by enhancing self-regulatory processes and decreasing emotional reactivity. In order
to investigate if mindfulness similarly reduces distress and neural activations associated with empathy for
others’ socially painful experiences, which might in the following more strongly motivate prosocial behavior,
the present study compared trait, and state effects of long-term mindfulness meditation (LTM) practice. To do
so we acquired behavioral data and neural activity measures using functional magnetic resonance imaging
(fMRI) during an empathy for social pain task while manipulating the meditation state between two groups of
LTM practitioners that were matched with a control group. The results show increased activations of the anterior insula (AI) and anterior cingulate cortex (ACC) as well as the medial prefrontal cortex and temporal pole
when sharing others’ social suffering, both in LTM practitioners and controls. However, in LTM practitioners,
who practiced mindfulness meditation just prior to observing others’ social pain, left AI activation was lower
and the strength of AI activation following the mindfulness meditation was negatively associated with trait
compassion in LTM practitioners. The findings suggest that current mindfulness meditation could provide an
adaptive mechanism in coping with distress due to the empathic sharing of others’ suffering, thereby possibly
C 2017 Wiley Periodicals, Inc.
V
enabling compassionate behavior. Hum Brain Mapp 38:4034–4046, 2017.
Key words: mindfulness meditation; social pain; vicarious embarrassment; empathy; anterior insula
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During social interactions we attempt to make sense of
others’ states like their sensations, emotions or thoughts in
order to predict and understand their behavior and react
accordingly. One route to understanding others is to
empathically share their states and feelings, be it physical
pain [Singer et al., 2004], social pain, such as social
Additional Supporting Information may be found in the online
version of this article.
L€
ubeck, Ratzeburger Allee 160, D-23538 L€
ubeck, Germany. E-mail:
mueller-pinzler@snl.uni-luebeck.de
Contract grant sponsor: German Research Foundation (DFG);
Contract grant number: KR3803/7-1; Contract grant sponsor: von
Behring-R€
ontgen-Stiftung; Contract grant number: KR 60-0023
Received for publication 8 July 2016; Revised 25 April 2017;
Accepted 28 April 2017.
INTRODUCTION
*Correspondence to: Dr. Laura M€
uller-Pinzler, Department of Psychiatry and Psychotherapy, Social Neuroscience Lab, University of
C 2017 Wiley Periodicals, Inc.
V
DOI: 10.1002/hbm.23646
Published online 15 May 2017 in Wiley Online Library (wileyonlinelibrary.com).
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Empathy for Social Pain and Mindfulness
exclusion [Beeney et al., 2011; Masten et al., 2011; Novembre et al., 2013] and embarrassment [Krach et al., 2011,
2015; M€
uller-Pinzler et al., 2016; Paulus et al., 2015b], or joy
[Mobbs et al., 2009]. Here, negative affective experiences
like social exclusion and embarrassment are considered to
be a form of social pain. This relatively new construct of
social pain has been established to emphasize the conceptual overlap of the distress and affective arousal with physical pain, which is thought to signal a threat for our bodily
integrity. In this line, affective experiences in the domain of
social pain serve a similar function, however signaling
threats to our social integrity, a core aspect of the embarrassment experience [Eisenberger et al., 2003; Keltner, 1995;
Macdonald and Leary, 2005; M€
uller-Pinzler et al., 2015].
Neuroimaging and pharmacological studies support this
conceptual overlap indicating some common pathways
involved in processing both social and physical pain [Dewall et al., 2010; Kross et al., 2011; Paulus et al., 2015b]. It has
been suggested, however, that sharing others’ negative
affective experiences or social pain might also lead to feelings of empathic distress in the observer [Batson, 2009].
Recent studies showed that empathic distress alters social
decision making [Sarlo et al., 2014] and increases the egocentric desire to reduce one’s own distress [Batson, 1991;
Eisenberg et al., 2010]. While empathy is typically positively associated with prosocial behavior and increases the
motivation to help the other person in pain [Eisenberg and
Miller, 1987] the experience of intense negative affect might
also have the opposite consequences and shift the individuals attention toward the own distress [Hoffmann, 2008]. In
contrast to the experience of empathy and sympathy, distress has been shown to evoke egoistic motivations to
reduce one’s own aversive arousal [Batson et al., 1987] and
can reduce prosocial helping behavior [Eisenberg et al.,
1989; Eisenberg and Fabes, 1990]. Hence, empathizing with
others’ negative emotions and especially feeling empathic
distress may not necessarily have prosocial consequences.
Mindfulness meditation, typically described as a state of
“non-judgmental attention to experiences in the present
moment,” is often applied with the purpose to counteract
these tendencies, reduce stress and promote health and
well-being [Holzel et al., 2011; Kabat-Zinn, 1982]. As a
psychotherapeutic intervention mindfulness has been
shown to produce beneficial effects on mental and physical health [Grossman et al., 2004] as well as on clinical
measures and stress-related symptoms in healthy subjects
[Khoury et al., 2015]. Mechanisms involved during mindfulness are assumed to enhance self-regulatory processes
and cognitive reappraisal, as well as decrease emotional
reactivity, as shown in depression [Teasdale et al., 1995] or
as discussed for physiological reactivity [Holzel et al.,
2011; Khoury et al., 2015], thereby reducing distress in
response to one’s own painful experiences and expectedly
also in response to others’ suffering. Although compassion
meditation has a more specific focus on feelings of positivity and happiness, while mindfulness meditation focuses
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on non-judgmentally becoming fully aware of the present
moment, recent research has provided evidence that mindfulness meditation in itself enhanced compassion [Wallmark et al., 2013] and compassionate responses to
suffering [Condon et al., 2013; Lim et al., 2015]. Other
studies also suggest that the practice of mindfulness
encourages the development of compassionate emotions
[Birnie et al., 2010]. In addition, some Buddhist traditions
support the idea that compassion emerges from or is a
synonym of pure awareness, which is the goal of the practice of mindfulness [Nakagawa, 2009]. Therefore, mindfulness meditation might inherently impact affective and
empathic reactions via processes comprising compassionate responding, which has been found to be a strong predictor of prosocial behavior [Sprecher, 2005].
In this line, studies showed that mindfulness based trainings lead to more engagement in empathy [Lamothe et al.,
2016; Shapiro et al., 1998], but less experience of personal distress when confronted with other’s suffering [Dekeyser et al.,
2008]. Similar effects were found for short term meditation
trainings specifically involving exercises and ideas from compassion meditation with enhanced sympathetic concern for,
and reduced aversion to the suffering of others on the level of
emotion expressions [Rosenberg et al., 2015]. Here, we ask,
what the effect of mindfulness meditative practice is on the
empathic sharing of a specific form of social pain, namely the
experience of embarrassment on behalf of others.
To date, there is a large body of literature which specifically focuses on the neural correlates of empathy for
others’ physical and social pain. Understanding the threat
to another’s social integrity is a rather complex process
and it is assumed that mainly two distinct but interacting
routes are involved enabling humans to understand another’s condition [Keysers and Gazzola, 2007; Paulus et al.,
2013b; Waytz and Mitchell, 2011]. One of them is referred
to as “mentalizing” and involves mental projections of
oneself into another person’s perspective, reflections about
their behavior, and it typically engages brain regions in
the temporal lobe and temporo-parietal junction, the
medial prefrontal cortex (mPFC), and the precuneus [Frith
and Frith, 2003]. Previous studies showed that these mentalizing areas were recruited when making sense of others’
socially painful situations [M€
uller-Pinzler et al., 2016; Paulus et al., 2017; Paulus et al., 2015b]. The second route
involves so-called “mirroring” or “sharing” and is
assumed to be a direct mapping of others’ sensory or
affective states and actions on one’s own neural system
predominantly through sensory and motor streams. When
we share others’ experiences, the same regions, which are
involved in the first-hand experience, show increased activation [among others the anterior insula (AI) and anterior
cingulate cortex (ACC)], leading to the so-called “shared
circuits” hypothesis [Eisenberger et al., 2003; Engen and
Singer, 2013; Krach et al., 2011; Kross et al., 2011; Singer
et al., 2004]. Activations within these regions are supposed
to map the conscious negative affective experience and
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Laneri et al.
interoceptive awareness of physiological arousal [Craig,
2003] regardless of it being caused by one’s own or another’s suffering. The empathic responses of these circuits
show strong modulations not only by intra-individual variation in empathic resonance [Kanske et al., 2015], but also
inter-individual differences in trait empathy [Krach et al.,
2011; Singer et al., 2004] with individuals scoring higher in
trait empathy showing increased activation in AI and
ACC. Interoceptive deficits related to alexithymia are also
associated with decreased responses of empathy related
brain regions [Bird et al., 2010]. Other studies showed that
empathy related neural activations can be modulated by
appraisal processes and assumptions about the observer’s
state of mind [Lamm et al., 2007a, 2007b], suggesting that
empathic responses and behavioral reactions to others’
suffering are highly variable and can be willfully influenced by cognitive and motivational processes.
Along these lines, a few studies investigated the impact
of meditation training on responses to others’ suffering
and the related neural correlates [Klimecki et al., 2013,
2014]. Although these studies implemented short-term
meditation training that focused on compassion rather
than mindfulness, they might provide an important reference for our understanding of empathic responding. This
is supported by studies showing that both, mindfulness as
well as compassion, are assumed to go along with
increased empathy as well as decreased personal distress
responses to others’ suffering [Dekeyser et al., 2008;
Lamothe et al., 2016]. These studies showed that shortterm compassion meditation training increased positive
affect in response to others’ suffering along with activation
of the medial orbitofrontal cortex and ventral striatum,
regions typically associated with reward processing [Knutson et al., 2000]. Activations in AI and ACC, potentially
mapping shared negative affect and physiological arousal,
were reduced while observing others’ suffering [Klimecki
et al., 2014]. Mindfulness training has been shown to
decrease the experience of one’s own bodily pain [Haase
et al., 2016; Zeidan et al., 2011]. Similarly, subsequent to
mindfulness training higher non-reactivity to own inner
(affective) experiences as one aspect of mindfulness was
associated with decreased responding of the AI, potentially mapping a mechanism of reduced vulnerability to
negative affect [Paul et al., 2013]. However, while some
studies found decreased activations of AI and ACC during
mindfulness meditation [Ives-Deliperi et al., 2011], others
support the notion that heightened awareness of interoceptive and bodily signals during a state of mindfulness is
accompanied by increased activations of the AI [Holzel
et al., 2011]. Therefore, the role of the AI especially in
response to others’ suffering as a consequence of mindfulness training does not seem to be thoroughly clear. Effects
of short-term trainings might also be of limited duration.
Therefore, studies on experienced meditators, who are
used to practice mindfulness meditation throughout their
lives, might provide additional and valuable insights.
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Similar to the effects found after mindfulness training,
neuroimaging studies on long-term meditation (LTM) practitioners showed behavioral effects of reduced pain experiences and increased activations of the AI and ACC during the
experience of own bodily pain [Gard et al., 2012; Lutz et al.,
2013] and merely while being in a state of mindfulness [Fox
et al., 2016]. Thereby, altered functioning of the AI was speculated to be based on structural changes of the insula cortex
[Fox et al., 2014]. However, study designs varied in several
aspects, for example, in how (visual vs. auditory) and if
stimuli were presented and when (during vs. after meditation) brain activation was measured. Moreover, many studies assessed effects of mindfulness meditation training on
the experience of one’s own bodily pain [Gard et al., 2012;
Haase et al., 2016; Lutz et al., 2013; Zeidan et al., 2011]. Concentrating on one’s own (inner) sensations in a state of
mindfulness in contrast to focusing on a social target in pain
and experiencing (reduced) personal distress might elicit
greatly differential neural activation patterns. We, therefore,
assume that comparisons across studies and general conclusions are still limited. Thus, the questions remain how, first,
mindfulness meditation affects the experience of socially
painful situations and second how empathizing with others’
painful states is affected by meditation. Since many traditional meditation practices aim to counteract self-centered
tendencies, decrease egocentric attitudes toward our external
world, and increase other-oriented thinking [see Lutz et al.,
2008], it is of great interest to further unravel effects on
empathic sharing of others’ socially painful experiences.
The aim of this study is therefore to characterize how
long-term mindfulness meditation, which is associated
with increased self-regulation and decreased distress [Holzel et al., 2011], modulates empathy for others’ social pain
including the related neural activity in the AI. Specifically,
we wanted to test if a change in AI activation, which has
been shown after short-term compassion meditation trainings [Klimecki et al., 2014], might be evident in LTM practitioners of mindfulness meditation when confronted with
others’ social suffering. To this end, we applied a validated empathy for social pain paradigm, during which
stimuli are presented that depict social targets in a wide
variety of potentially embarrassing and unpleasant social
situations [Krach et al., 2011; M€
uller-Pinzler et al., 2012;
Paulus et al., 2013a, 2015a, 2015b]. Furthermore, it is an
open question if LTM induces outlasting dispositional
changes, which affect the perception of social situations in
general, or if current meditation practice activates a distinctive state, which only affects social perceptions
momentarily. We therefore specifically compared state versus trait effects of mindfulness meditation practice while
maintaining the subjects’ focus on the suffering individual.
MATERIALS AND METHODS
Ethics Statement
We confirm that the research has been conducted in
compliance with the ethical guidelines of the American
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Empathy for Social Pain and Mindfulness
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TABLE I. Means and standard deviations for sample characteristics and empathy for embarrassment ratings
CON
M
Age
50.37
IQ
126.11
CLS
4.17
IRI Fantasy
3.36
IRI Perspective
3.61
IRI Empathy
3.54
IRI Distress
2.86
Years of Meditation
Meditation per day (min)
EE
4.01
NEUT
1.05
MED_OFF
MED_ON
SD
M
SD
M
SD
F
P
g2
5.44
14.20
0.82
0.42
0.51
0.52
0.44
52.69
128.75
5.05
3.39
3.72
3.48
2.56
17.69
38.26
3.71
1.06
6.61
11.14
0.65
0.43
0.36
0.39
0.54
11.32
30.23
0.57
0.09
49.69
123.50
4.95
3.42
3.63
3.63
2.56
15.31
25.94
3.79
1.12
8.90
12.31
0.59
0.33
0.48
0.38
0.59
7.76
14.02
0.60
0.22
0.81
0.68
8.39
0.12
0.29
0.42
1.88
0.48
2.19
1.36
1.17
0.452
0.511
0.001
0.884
0.749
0.660
0.164
0.494
0.150
0.266
0.318
0.03
0.03
0.26
0.01
0.01
0.02
0.07
0.02
0.07
0.05
0.05
0.48
0.10
Note. M 5 mean. SD 5 standard deviation. CON 5 control group (10 m/9 f). MED_OFF 5 group resting before the social pain task (9 m/
7 f). MED_ON 5 group meditating before the social pain task (11 m/5 f). CLS 5 Compassionate Love Scale. IRI 5 Interpersonal Reactivity Index, split into four subscales. EE 5 empathic embarrassment rating during scanning. NEUT 5 empathic embarrassment rating during scanning. F-values, P-values, and g2-values refer to one-way ANOVAs comparing variables across the three or two groups,
respectively.
Psychological Association (APA). The study protocol was
approved by the Marburg ethics committee at the local
faculty of medicine and all subjects gave written informed
consent.
Participants
Overall, the study included N 5 51 participants. None of
them were diagnosed with neurological or psychiatric disorders (present and past), current alcohol or drug abuse,
use of psychiatric medications (present and past), anatomical brain abnormalities (e.g., lesions, strokes, etc.). All participants were fluent in German, and had normal or
corrected-to-normal vision. N 5 32 of the participants were
experienced LTM practitioners, the others were control
subjects (CON), who reported no meditation experience
(n 5 19, 10 male, aged 42–63 years; M 5 50.37; SD 5 5.44;
see Table I for all participant characteristics). LTM practitioners were recruited from Buddhist and Zen centers
across Germany and were regularly practicing meditation
(M 5 32.10 min/day, SD 5 23.63). LTM practitioners were
randomly assigned to two groups and were either
instructed to actively meditate prior to the task (MED_ON,
n 5 16, 11 male, aged 36–64 years; M 5 49.69; SD 5 8.90) or
rest in the scanner for the same amount of time (MED_OFF,
n 5 16, 9 male, aged 40–60 years; M 5 52.69; SD 5 6.61).
Years of meditation experience ranged between 5 and 38
years and there was no difference between the two LTM
groups (F(1,30) 5 0.48, P 5 0.494). The three groups did also
not differ in terms of sex (Chi2 5 0.995, P 5 0.608), age, and
IQ (see Table I). In order to control for differences in the
exact meditation styles that meditators were practicing on a
regularly basis, we asked participants to indicate the meditation style that they had expertise in. In the following, a
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meditation expert categorized these meditation styles in
Zen meditation, Vipassana meditation, and other types of
mindfulness meditation (see Supporting Information Table
S1). While about half of the meditators indicated that they
practiced one specific mindfulness meditation style (n 5 17)
the others were practicing two or more different types of
mindfulness meditation (n 5 15) and distributions did not
differ between the two groups in this regard (Chi2 5 0.15,
P 5 0.928). Frequencies of Zen, Vipassana, and mindfulness
practice of other styles did not differ significantly between
groups (Zen: Chi2 5 2.03, P 5 0.154; Vipassana: Chi2 5 0.00,
P > 0.999; other: Chi2 5 2.33, P 5 0.127).
General Procedure
In order to distinguish effects of enduring trait characteristics of LTM practitioners from effects of temporary
state changes elicited by the preceding meditation practice
on empathy for others’ social pain, we manipulated the
meditation state in a between-subjects design. Half of the
LTM practitioners were randomly assigned to actively
meditate for eight minutes before the task (MED_ON
group) while the other half had a rest period of equal
length prior to the task (MED_OFF group). The meditation
and resting period was conducted in the MRI just prior to
the empathy for embarrassment experiment. The
MED_ON group had the instruction to perform a mindfulness meditation, which typically involves paying “nonjudgmental attention to experiences in the present
moment” [Kabat-Zinn, 1982] and the MED_OFF group
was explicitly instructed not to meditate but rest. The
CON group was instructed to rest for the same time as the
MED_OFF group did.
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Figure 1.
A. Stimuli used in the fMRI experiment. EE situations depicted
social targets in embarrassing situations, potentially eliciting
empathic embarrassment in the observer. Ten sketches displayed
non-norm-violating control situations (NEUT). Stimuli were presented together with two sentences describing the situation
below the sketches [e.g., You are at a post-office: you observe a
women’s trouser ripping while she bends down to lift a package. . . (EE)]. B. Sequence of the experimental paradigm. Red
arrows indicate that subjective ratings of the protagonist‘s experience of embarrassment correspond to the preceding embarrassment situation. [Color figure can be viewed at
wileyonlinelibrary.com]
After providing written informed consent participants
were carefully instructed about the experimental procedure. Participants received two example trials of the
empathy for embarrassment paradigm for practice that
were not displayed during the fMRI session and were
asked to mentally visualize the displayed situations as vividly as possible (for the description of the paradigm and
stimuli see fMRI paradigm and stimuli). After completion
of the fMRI paradigm, participants were asked to fill out
the Interpersonal Reactivity Scale [IRI; Davis, 1980] and
the Compassionate Love Scale [CLS; Sprecher, 2005] in
order to assess their trait levels of empathy as well as
compassion.
transgression, thus experiencing embarrassment him- or
herself (EE). From the observers’ perspective these situations conform to the definition of empathy, as the social
target and the observer share a similar affective state, that
is, the embarrassment in response to the norm transgression. These trials were thus included for the purpose of
the present analysis of empathic embarrassment. The other
ten situations depicted protagonists in embarrassing situation, who were unaware about the norm violation during
the situation, thus not experiencing embarrassment themselves. These situations were excluded from the present
analyses, since they are conceptually different from true
empathic experience as we have previously argued [Paulus et al., 2013b]. Neutral control stimuli displayed the
social target in a similar public context, however, without
violating socially normative standards. For clarification
each sketch was accompanied by a two-sentence description of the current situation (e.g., “You are at the grocery
store: You observe a woman at the cashier who is realizing
that she cannot pay her purchase. . .,” see Fig. 1).
In the MRI, stimuli were presented on an LCD screen
with Presentation 12.1 software package (Neurobehavioral
Systems, Albany, CA) and the participants were able to
see them via a mirror placed on the head coil. All sketches
fMRI Paradigm and Stimuli
During the empathy for embarrassment paradigm all
groups viewed the same set of 20 previously validated
hand-drawn sketches depicting embarrassing situations
and 10 neutral sketches (NEUT) serving as control situations. The embarrassment situations displayed a social target while he or she was violating a social norm in public
and threatened his or her social integrity. Importantly, in
10 of these situations the target was aware about the norm
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Empathy for Social Pain and Mindfulness
were presented for 12 seconds together with the description of the situation. The text was presented in a black 24point non-serif font (Arial) on a white background in two
to three rows below the sketches. The stimulus presentation was followed by a blank screen for 1 second and a
subsequent rating period of 3 seconds. In order to focus
the participants’ attention on the social target’s state not
on their own feelings, participants were asked to evaluate
the intensity of the social target’s experience of embarrassment during the preceding situation after each stimulus
presentation (“How strongly did the person you were
observing experience embarrassment?”). Responses were
made on a scale ranging from 1 (“not at all”) to 5 (“very
strong”) using a button press of the right hand. A jittered
low-level baseline showing a fixation cross for an average
of 8 seconds was interleaved between the rating period
and the following trial. Stimuli were presented in a
pseudo-randomized order, ensuring that no type of situation was immediately repeated and there were no accumulations of one specific type of situations during the fMRI
measurement. The total experiment lasted 12.14 minutes.
Data Acquisition
Participants were scanned at 3T (Siemens Trio, Erlangen).
A BOLD sensitive echo planar imaging (EPI) sequence was
used for acquisition of functional volumes during the experiment (TR 5 2.2 s, TE 5 30 ms, flip angle 5 908, 36 ascending
slices, slice thickness 5 3 mm, 10% gap, FoV 5 192 mm,
matrix 64 3 64).
Data Analysis
Behavioral data
Data were analyzed with IBM SPSS Statistics for Windows, Version 22.0 (IBM Corp., 2013, Armonk, NY). Overall, 0.39% of the participants’ ratings of the social target’s
embarrassment were missing and missing values were
replaced by the subject and condition specific average.
Each participant’s ratings were averaged within the empathy for embarrassment and neutral situations. Averaged
ratings of embarrassment were then analyzed using analysis of variance (ANOVA) with Group as a between-subject
factor (CON, MED_ON, and MED_OFF) and Condition as
a within-subject factor [empathy for embarrassment (EE)
and neutral (NEUT)]. Paired t-tests comparing the EE condition with the NEUT for each group separately were
implemented to test for group specific empathy effects.
Additionally, the comparison of the MED_OFF versus
CON group for the empathy effect ([CON_EE-CON_NEUT]
vs. [MED_OFF_EE-MED_OFF_NEUT]) allowed testing for
trait effects of LTM on empathy while controlling for state
effects. The comparison of the MED_ON versus MED_OFF
group tests the state effects of meditation on empathy controlling for the trait effects of LTM that are common to
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both LTM groups ([MED_OFF_EE-MED_OFF_NEUT] vs.
[MED_ON_EE-MED_ON_NEUT]).
Functional MRI data
FMRI data was analyzed using SPM8 (www.fil.ion.ucl.
ac.uk/spm). The first four images were dummy scans and
were discarded from further analyses. The remaining 331
EPI volumes were corrected for timing differences of the
slice acquisitions, motion-corrected, and spatially normalized to the standard template of the Montreal Neurological
Institute (MNI) using the EPI template. The normalized
volumes were resliced with a voxel size of 2 3 2 3 2 mm,
smoothed with an 8 mm full-width half-maximum isotropic Gaussian kernel, and high-pass filtered at 1/256 Hz to
remove drifts.
Empathic embarrassment related activation. Statistical
analysis was performed in a two-level, mixed-effects procedure. The fixed-effects generalized linear model (GLM)
on the first level included four epoch regressors modeling
hemodynamic responses to the empathy for embarrassment situations (1), the vicarious embarrassment situations
not included in the current analyses (1), neutral situations
(1), and the rating phase (1) with the abovementioned
stimulus durations. The embarrassment ratings after each
social pain situation were entered as parametric modulators within both of the embarrassment conditions separately to explain additional variance in neural activation
on the within-subject level. Six additional regressors
modeling head movement parameters were included as
regressors of no interest.
Beta-maps of activation in the empathy for embarrassment and the neutral situations were analyzed on the second level. The second-level analysis of activation
differences was conducted with a random-effects GLM.
The GLM contained one factor for the three levels of
Group (CON, MED_ON, MED_OFF) and a second factor
for the two dependent levels of EE versus NEUT
situations. In order to identify brain regions that are
involved when experiencing empathy for embarrassment
we conducted a conjunction analysis and contrasted the
EE against the NEUT condition across all groups ([CON_
EE–CON_NEUT] \ [MED_ON_EE–MED_ON_NEUT] \
[MED_OFF_EE–MED_OFF_NEUT]). Effects of LTM on the
trait level were tested by contrasting empathy effects (EE
vs. NEUT) for MED_OFF versus CON. Effects of preceding meditation practice on the current state, controlling for
trait effects, were tested by comparing empathy effects for
MED_ON versus MED_OFF. We investigated downregulations of empathy related neural networks (NEUTEE) and additionally contrasted EE-NEUT in order to test
for up-regulations. Both comparisons were first examined
within the whole brain and additionally within a functional left AI ROI, which was derived from a previous
study on vicarious embarrassment [Krach et al., 2011]. In
order to control for differences in meditation style that
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Figure 2.
Results of the conjunction analysis of empathic embarrassment (EE) versus neutral (NEUT) situations
across groups ([CON_EE–CON_NEUT] \ [MED_ON_EE–MED_ON_NEUT] \ [MED_OFF_EE–
MED_OFF_NEUT]) are depicted family-wise-error corrected for the whole brain. For further results
see also Table II. [Color figure can be viewed at wileyonlinelibrary.com]
participants practiced on a regularly basis we set up a
random-effects GLM with one factor containing the difference between levels of EE versus NEUT situations for the
three levels of Group (CON, MED_ON, MED_OFF) and
meditation style as a covariate across groups coded as Zen
experience only, Vipassana experience only and experience
in both meditation styles. By this, all comparisons between
the two meditation groups were repeated while controlling
for meditation style. All analyses were thresholded at
P < 0.05 and corrected for multiple comparisons using the
respective family-wise error correction as implemented in
SPM8.
In order to investigate how differences in trait level
compassion, assessed via the CLS, modulate activations of
the AI, Pearson correlations between measures were calculated within each group separately. AI activations were
extracted from the peak voxel of the contrast comparing
empathy effects for the MED_ON versus MED_OFF group
([MED_ON_EE-MED_ON_NEUT] 2 [MED_OFF_EE-MED_
OFF_NEUT]) within the functional AI ROI (x 5 244, y 5 22,
z 5 2 mm). In order to account for large variability of meditation experience (in daily practice hours and years of meditation experience) within groups Spearman correlations
were calculated to test associations with AI activation.
RESULTS
Behavioral Data
Participants’ self-reports of empathic embarrassment
were significantly stronger for EE situations compared
with NEUT situations across all groups (F(1,48) 5 1215.77,
P < 0.001, g2 5 0.962). This effect was also present within
each group (CON: t(18) 5 25.91, P < 0.001, d 5 10.05; EE:
M 5 4.01; SD 5 0.48; NEUT: M 5 1.05; SD 5 0.10; MOD_OFF:
t(15) 5 18.11, P < 0.001, d 5 7.79; EE: M 5 3.71; SD 5 0.57;
NEUT: M 5 1.06; SD 5 0.09; MED_ON t(15) 5 17.43, P < 0.001,
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d 5 5.72; EE: M 5 3.79; SD 5 0.60; NEUT: M 5 1.12;
SD 5 0.22). There was no Group 3 Condition interaction
(F(2,48) 5 1.65, P 5 0.203, g2 5 0.064), no meditation state effect
(t(30) 5 0.10 P 5 0.925, d 5 0.034), and no meditation trait
effect (t(33) 5 1.67, P 5 0.104, d 5 0.567) on empathic embarrassment ratings during EE compared with NEUT
situations.
The LTM groups did not differ in terms of trait compassion as assessed via the CLS (t(30) 5 0.45 P 5 0.657, d 5 0.16)
but showed higher levels compared with the CON group
(t(49) 5 4.11 P < 0.001, d 5 1.19). Groups did not differ in
terms of trait empathy as assessed with the IRI (see Table I).
Neuroimaging Data
Common activations across groups
In accordance with our previous studies, we found
increased activations of the ACC and the left AI across all
groups during EE. Additionally, a region within the mPFC
also typically recruited during mentalizing (see Supporting
Information Fig. S2) showed increased activity. Together
with activations of the caudate nucleus, SMA, as well as a
region within the thalamus/brainstem the findings replicate the typical activation patterns in response to empathic
embarrassment [P < 0.05, FWE corrected for the whole
brain; see Fig. 2 and Table II; Paulus et al., 2015b]. An
additional analysis showed that activation within these
areas was specifically associated with vicarious embarrassment ratings varying between all of the presented social
situations on the within subject level (see Supporting
Information Results and Figures).
Between group comparisons: ROI analyses
Comparisons between the LTM and CON groups
showed that there were no significant effects of LTM on
the trait level corrected within the ROI in the left AI. In
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TABLE II. Activation during empathic embarrassment compared with neutral situations
MNI coordinates
Anatomical region
Conjunction EE>NEUT
Cingulate cortex
Middle cingulate cortex
Middle frontal gyrus
Middle cingulate cortex
Caudate nucleus/putamen
Putamen
Caudate nucleus
Thalamus
Anterior insula/putamen
Putamen
Anterior insula
Thalamus
Inferior parietal
Inferior parietal lobule
Supramarginal gyrus
Postcentral gyrus
Superior frontal
Superior frontal gyrus
Posterior-medial frontal
Cyto area
Side
x
y
z
26
220
6
24
44
24
36
32
34
16
18
14
12
8
22
4
12
6
218
228
210
8
14
22
6
4
6
248
258
240
236
230
230
46
34
54
224
216
26
4
56
64
L/R
Cluster size
T
P
6.95
5.67
5.29
<0.001
0.001
0.004
6.77
5.96
4.83
<0.001
<0.001
0.023
6.70
5.82
5.61
<0.000
0.001
0.001
5.57
5.56
5.06
0.002
0.002
0.010
5.47
5.20
0.002
0.006
1,188
R
281
Th-Prefrontal
L
514
Th-Prefrontal
L
278
PFt (IPL)
PFt (IPL)
Area 3b
L
126
Note. Results for the conjunction analysis of empathic embarrassment (EE) versus neutral (NEUT) situations across groups ([CON_EE–CON_NEUT] \ [MED_ON_EE–MED_ON_NEUT] \ [MED_OFF_EE–MED_OFF_NEUT]). The Cyto area column indicates the
assigned cytoarchitectonical area derived from the SPM ANATOMY toolbox v2.2b if available [Eickhoff et al., 2005]. All P-values are
family wise error corrected for the whole brain. Clusters with less than 10 voxels are not reported.
contrast, we did find specific effects of preceding meditation on the current state. LTM practitioners, who had meditated just prior to being exposed to others’ embarrassing
situations (MED_ON), showed decreased activation of the
left AI (t(96) 5 3.10, P 5 0.020, FWE corrected within left AI
ROI; x 5 244, y 5 22, z 5 2 mm) compared with the
MED_OFF group, indicating a down-regulation of AI
activity during empathic embarrassment (see Fig. 3). Controlling for meditation style did not change the finding of
lower AI activation in the MED_ON versus MED_OFF
group in response to EE versus NEUT situations substantially (t(47) 5 3.10, P 5 0.027, FWE corrected within left AI
ROI; x 5 244, y 5 22, z 5 0 mm).
Between group comparisons: whole brain analyses
Similarly, comparisons between the LTM and CON
groups showed no significant effects of trait LTM in the
whole brain analysis. Neither was there an increase of activation in LTM practitioners (MED_OFF) compared with
the CON group, nor a down-regulation of any brain
region as indicated by a whole-brain analysis (P < 0.05,
FWE corrected) even at more lenient thresholds (P < 0.001,
uncorrected).
There was no additional up-regulation or downregulation associated with the current meditation state corrected on the whole brain level (P < 0.05, FWE corrected).
r
On a more lenient threshold there was an additional
down-regulation for the MED_ON compared with the
MED_OFF group in the middle cingulate cortex in
response to EE versus NEUT situations (t(96) 5 3.98,
P < 0.001, k > 50; x 5 2, y 5 0, z 5 28 mm). When controlling for meditation style we found similar results
(t(47) 5 4.17, P < 0.001, k > 50; x 5 2, y 5 2, z 5 28 mm).
Associations of neural activation and trait measures
Correlation analyses showed a negative correlation of
left AI activation and trait compassion (r(14) 5 20.49,
P 5 0.028) for the MED_ON group (within the region
showing decreased activation in the MED_ON vs. MED_OFF group; x 5 244, y 5 22, z 5 2 mm, see Fig. 3). The
MED_OFF group also showed a negative association with
CLS, which however was not significant (r(14) 5 20.31,
P 5 0.119; pooled partial correlation across LTM groups
controlled for group: r(29) 5 20.36, P 5 0.047). There was
no association of CLS scores and left AI activation in the
CON group (r(17) 5 0.01, P 5 0.484). Further, years of meditation experience did not correlate significantly with AI
activation (MED_ON: r(14) 5 0.06, P 5 0.416; MED_OFF:
r(14) 5 20.13, P 5 0.312). Daily meditation practice showed
no association with left AI activation in the MED_OFF
group (r(14) 5 0.15, P 5 0.295). In comparison there was a
stronger negative association of daily meditation practice
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Laneri et al.
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Figure 3.
A. Decreased activation of the left AI in the MED_ON versus
MED_OFF group during empathic embarrassment (EE) versus
neutral situations (NEUT) indicating a down-regulation of shared
circuits activation in response prior meditation ([MED_ON_EE–
MED_ON_NEUT]<[MED_OFF_EE–MED_OFF_NEUT]). Results
are depicted uncorrected for displaying purposes within the left
AI ROI. B. Correlation plots for Compassionate Love (CLS)
scores and activation of the left anterior insula for control group
(CON; r(17) 5 0.01, P 5 0.484), the meditation group (MED_ON;
r(14) 5 20.49, P 5 0.028), and the rest group (MED_OFF;
r(14) 5 20.31, P 5 0.119). Parameter estimates of the left AI are
derived from the peak voxel for the contrast [MED_ON_EE–
MED_ON_NEUT]<[MED_OFF_EE–MED_OFF_NEUT] (x 5
244, y 5 22, z 5 2 mm). [Color figure can be viewed at
wileyonlinelibrary.com]
and left AI activation in the MED_ON group (trend-wise
effects; r(14) 5 20.42, P 5 0.053; MED_ON vs. MED_OFF:
z 5 1.51, P 5 0.065). The negative association of daily meditation practice and left AI activation was also stronger
compared with the correlation of the years of meditation
practice and AI activation in the MED_ON group (trend:
z 5 1.29, P 5 0.099).
practitioners and controls that could be related to trait differences. LTM practitioners, however, who meditated just
prior to the task, showed decreased activations of the left
AI in response to empathic embarrassment. This finding
rather argues for state-related changes in empathic
responding. Additionally, left AI activation was correlated
negatively with trait compassion and meditation experience specifically in the group of LTM practitioners, who
meditated before the task.
Noteworthy, the activation decrease in the left AI when
LTM practitioners engaged in a meditative state just before
completing the empathic embarrassment paradigm is in
line with earlier studies showing a down-regulation of AI
activation after mindfulness training in response to own
painful experiences [Haase et al., 2016] and negative affective stimuli [Paul et al., 2013] and also after short-term
compassion meditation training more specifically in
response to another’s suffering [Klimecki et al., 2014]. The
AI is a brain region that is assumed to be implicated in
processing of physiological arousal and the conscious
experience of one’s internal bodily and affective states
[Craig, 2003; Critchley et al., 2004]. Earlier studies on
empathic embarrassment showed that the intensity of subjective experiences of vicarious embarrassment on behalf
of another person is significantly associated with AI activations [Paulus et al., 2015b]. This points to the AI’s role
in generating an interoceptive representation while affectively and empathically sharing another’s embarrassing
DISCUSSION
In the present study we examined how LTM modulates
the experience of empathic embarrassment on behalf of
others’ flaws, failures or norm violations and its processing on the neural systems level. We therefore tested a sample of LTM practitioners, who had been practicing various
mindfulness meditation techniques for many years prior to
our study, and have compassionate characteristics, as indicated by higher trait compassion levels. As previous studies already showed [Krach et al., 2011; Paulus et al., 2015b]
empathic embarrassment triggered activity within areas of
the mentalizing network, that have been related to the
evaluation of the social target’s mental state and image
threats during the embarrassing incident [M€
uller-Pinzler
et al., 2016; Paulus et al., 2015b], in control subjects as well
as LTM practitioners. Similarly, activations of the AI and
ACC were increased as a measure for an empathic sharing
of others’ embarrassing moments. There were no differences in the neural response between the groups of LTM
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Empathy for Social Pain and Mindfulness
moments. Previous studies investigated structural changes
in LTM practitioners and have suggested increased thickness [Lazar et al., 2005], increased cortical folding complexity [Luders et al., 2012], as well as increased
connectivity of white matter within the insula cortex in
meditators [Laneri et al., 2016]. These structural changes
might constitute the architecture that underlies altered
functioning of the AI cortex in LTM practitioners.
With this study we could show that LTM practitioners
show reduced empathic sharing of the another’s suffering
on the neural systems level when engaged in a meditative
state prior to observing others’ socially painful situations.
Enduring trait changes and specifically increases in compassionate responding are an explicit goal of most meditation traditions and mindfulness meditation is associated
with increased self-compassion, and kindness [Holzel
et al., 2011] as well as compassionate behavior toward
others [Condon et al., 2013; Lim et al., 2015]. The aim is to
keep one’s negative feelings and thoughts in a “balanced
awareness instead of over-identifying with them” [Neff,
2003], which might be a mechanism to reduce distress in
response to one’s own but also another’s negative feeling
states [Holzel et al., 2011]. Improving the regulation of
painful thoughts, emotions, and body sensations, no matter if they are one’s own or shared experiences of another,
and developing compassionate feelings instead might be a
mechanism associated with altered insula functioning [Fox
et al., 2016; Holzel et al., 2011]. This is supported by the
negative correlation of trait compassion and left AI activation in the LTM group, which meditated just prior to the
experiment. Our finding suggests that a more compassionate mindset during meditation might reduce the experience of empathic distress and interoceptive sharing of the
other’s suffering.
However, LTM practitioners are still able to recognize
the target’s social pain as indicated by the ratings for the
affective experience of the social target, which did not differ from the control participants’ ratings. In response to a
meditative state LTM practitioners might be relying on
mentally projecting themselves in the social target’s position and simulating the other’s mental state in order to
make sense of his or her emotions [see Paulus et al.,
2013b; Waytz and Mitchell, 2011]. While there are typically
two streams of information processing, namely mentalizing and sharing [Keysers and Gazzola, 2007; Waytz and
Mitchell, 2011], which according to our results might be
recruited by all of the participants, the potential downregulation of AI activation in the MED_ON group suggests
that meditators might less strongly rely on interoceptively
sharing the other person‘s negative affect following a meditative state. However, while down-regulating shared
arousal, mentalizing about the other person’s state of
mind might still provide the information to make sense of
the social situation and to understand the social integrity
threat [see also Paulus et al., 2015b]. In doing so, meditators might be able to cultivate positive feelings of
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r
compassion for the social target [Klimecki et al., 2013]
instead of strongly interoceptively sharing the other’s distress. Mental projection hereby is assumed to recruit mentalizing areas like the mPFC [Frith and Frith, 2003; Waytz
and Mitchell, 2011], which showed similarly enhanced
activations in controls and LTM practitioners when
observing others’ social pain. Fully perceiving and
immersing themselves into the social situation while they
do not engage in an intense interoceptive sharing of the
other’s painful experience might enable LTM practitioners
to more strongly engage in prosocial behaviors in response
to a meditative state [Leiberg et al., 2011]. However, we
did not assess the participants’ own affective states and
positive emotions during the embarrassment paradigm
because we aimed to maintain a non-egocentric focus on
the social target’s suffering. Hence, further studies are
needed to assess the LTM’s affective state and its direct
associations with AI and ACC activity as well as to investigate behavioral consequences during social situations.
Trait effects of LTM alone did not impact activations of
the AI, when LTM practitioners did not meditate prior to
the paradigm. This lack of significant differences in neural
activation does not necessarily prove the absence of differences between groups and should be considered with caution since the non-finding could be related to statistical
power. Nevertheless, the trend-wise positive correlation of
the daily amount of meditation practice and left AI activation, which was only present when LTM practitioners
meditated prior to the experiment, supports the notion
that activation differences might indeed be more specifically associated with the state of mindfulness meditation.
Noteworthy, the actual plain years of meditation experience were not associated with decreased activations of the
AI; it was the magnitude of daily practice that had a stronger impact on the participants’ neural responding to
others’ social suffering.
Daily practice of LTM might thus not induce outlasting
dispositions or changes of neural functioning related to
empathic responding, which automatically alter the processing and appraisal of social situations. It, however,
seems to enable individuals to willfully engage in meditation practice and by doing so activate a distinctive mental
state that alters their AI activation in response to other
human beings’ social pain. The results might indicate that
interoceptive sharing of others’ social suffering is reduced
only by this state of mindfulness and nonjudgmental
attention to experiences in the present moment, which is
associated with decreased levels of distress [Khoury et al.,
2015], as well as potentially a compassionate mindset.
While there are studies speaking in favor of more persistent effects of meditation like structural changes of the AI
[Laneri et al., 2016; Lazar et al., 2005], and previous longitudinal training studies did find outlasting effects of, for
example, altered amygdala activity in response to affective
stimuli transferring to non-meditative states [Desbordes
et al., 2012], most studies did not directly investigate state
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Laneri et al.
versus trait effects [for further discussion see Fox et al.,
2016]. Nevertheless, there are other findings pointing
toward specific meditation state effects that do not manifest in the absence of any meditative practice at least for
specific tasks or circumstances like effects on somatosensory brain representations of interoceptive states [see Lutz
et al., 2009]. This might indicate that meditation effects do
not necessarily have to be persistent and automatic but
might require willful engagement in meditation practice in
order to manifest in neural activation differences.
The discrepancy between study findings might be task
specific, for example, due to rather subtle effects of LTM
expertise during processing of highly complex social situations as presented in form of pictorial stimuli eliciting
embarrassment compared with tasks involving the experience of own bodily pain, which might induce rather strong
effects. However, outlasting effects that are independent of
the meditation state might also have been facilitated by
the way short-term meditation trainings were implemented in some of the previous studies (e.g., training and
test in the same study context) or by the way participants
were asked to rate their own affect in response to affective
stimuli instead of solely focusing on the social target.
Nevertheless, we did find a negative correlation of trait
compassion and AI activation in the MED_ON group,
which was not present in the CON group, indicating the
importance of trait differences for regulating the AI’s
response. At the same time the higher trait compassion
scores in LTM practitioners compared with controls reflect
that LTM practitioners exhibit a greater propensity to
experience intense feelings of compassion, likely induced
by long-term practice in increasing altruistic attitudes
toward their external world. It has to be considered, however, that differences in trait compassion are not necessarily acquired by meditation training, although the goal of
many meditation traditions is to install permanent trait
changes [Fox et al., 2016]. Nevertheless, both findings
might point to the assumption that the down-regulation of
AI activation is related to the participants’ learned ability
to experience compassion for other human beings and suggest enduring underlying changes in mental functioning in
LTM practitioners. Trait compassion and state meditation
practice might interact in a way that inter-individual differences in trait compassion codetermine the effectiveness
of state meditation practice for the modulation of neural
activation. We did not assess, however, if state meditation
would affect responses in novices in a similar way. In
order to further support our assumptions studies on novices will be needed.
Our results seem to point toward an effect of state meditation, which might alter neural processing when meditators
willfully engage in meditation practice. In addition, trait
characteristics of experienced meditators might gain specific
importance with meditators higher in trait compassion
showing a stronger down-regulation of AI activation during
state meditation. However, the absence of significant
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r
differences in AI activation for the meditation trait condition
(MED_OFF) does not necessarily mean that there are no
such meditation trait effects. The positive but non-significant
correlation of trait compassion and AI activation in the
MED_OFF group might even point toward a potential effect
of meditation specific traits that might not be detected due
to insufficient power. However, this is rather speculative
and future studies are needed in order to draw further
conclusions.
Earlier studies could already show that meditation has
beneficial effects on mood and health [Fredrickson et al.,
2008; Pace et al., 2009], it increases prosocial behavior [Leiberg et al., 2011] and reduces sharing of negative affect in
trained meditation novices [Klimecki et al., 2014]. A willful
down-regulation of shared circuit activations in LTM practitioners might provide a potentially powerful long-term coping mechanism of decreased sharing of others’ socially or
physically painful experiences during social interactions
while remaining fully aware of the situation and its impact
on the social target. This might specifically affect individuals
who are routinely confronted with other human beings that
suffer from physical or mental illnesses, like people working
in caretaking provisions. While the specificity and applicability of meditation practice on a daily basis needs to be further
investigated (e.g., longitudinal studies), mindfulness and cultivating feelings of compassion might provide potential
mechanisms to induce state changes that facilitates coping
with distressing social situations of our daily lives.
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