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Reducing aggressive responses to social exclusion using
transcranial direct current stimulation
Paolo Riva,
1
Leonor J. Romero Lauro,
1
C. Nathan DeWall,
2
David S. Chester,
2
and Brad J. Bushman
3,4
1
Department of Psychology, University of Milano-Bicocca, Milano, Italy,
2
Department of Psychology, University of Kentucky, Lexington, KY, USA,
3
Department of Psychology, The Ohio State University, OH, USA, and
4
Department of Communication Science, VU University Amsterdam,
Amsterdam, The Netherlands
A vast body of research showed that social exclusion can trigger aggression. However, the neural mechanisms involved in regulating aggressive
responses to social exclusion are still largely unknown. Transcranial direct current stimulation (tDCS) modulates the excitability of a target region.
Building on studies suggesting that activity in the right ventrolateral pre-frontal cortex (rVLPFC) might aid the regulation or inhibition of social exclusion-
related distress, we hypothesized that non-invasive brain polarization through tDCS over the rVLPFC would reduce behavioral aggression following social
exclusion. Participants were socially excluded or included while they received tDCS or sham stimulation to the rVLPFC. Next, they received an oppor-
tunity to aggress. Excluded participants demonstrated cognitive awareness of their inclusionary status, yet tDCS (but not sham stimulation) reduced
their behavioral aggression. Excluded participants who received tDCS stimulation were no more aggressive than included participants. tDCS stimulation
did not influence socially included participants aggression. Our findings provide the first causal test for the role of rVLPFC in modulating aggressive
responses to social exclusion. Our findings suggest that modulating activity in a brain area (i.e. the rVLPFC) implicated in self-control and emotion
regulation can break the link between social exclusion and aggression.
Keywords: aggression; social exclusion; emotion regulation; social pain; transcranial direct current stimulation (tDCS)
INTRODUCTION
Malloy didn’t speak to them as they went by the boiler. They drew
into themselves and no one could foresee how they would come out
of the cloud. For there are two possible reactions to social
ostracismeither a man emerges determined to be better, purer,
and kindlier or he goes bad, challenges the world and does even
worse things.
John Steinbeck, Cannery Row (1945)
As Steinbeck quote suggests, when people are socially ostracized,
excluded or rejected by others, they can either try to gain acceptance
by behaving prosocially or lash out at others by behaving aggressively.
Lashing out at others seems paradoxical, because it would invite
further social rejection (Twenge et al., 2001; Buckley et al., 2004).
Yet, rejected people often choose this course of action (Twenge
et al., 2001; Buckley et al., 2004; MacDonald and Leary, 2005; Leary
et al., 2006; DeWall et al., 2009; Riva et al., 2011; for a review, see
DeWall and Bushman, 2011).
Social rejection increases aggression both inside and outside
the laboratory. In one laboratory experiment (Twenge et al., 2001),
for example, participants were informed after a group interaction
that nobody wanted to work with them (i.e. excluded) or that
everybody wanted to work with them (i.e. included). Excluded
participants behaved more aggressively against members of
their group, which took the form of blasting them with
unpleasant and prolonged noise. In an analysis of news reports
involving 15 US school shooters (Leary et al., 2003), all but two of
the shooters had been socially excluded, such as by a girlfriend or by
peers. Social exclusion was a better predictor of school shootings than
several other risk factors (e.g. evidence of a psychological disorder,
interest in guns, bombs or explosives, fascination with death).
The potential for exclusion to elicit such violence necessitates
the understanding of neural mechanisms that are involved in
regulating (or suppressing) aggressive responses that typically follow
social rejection. What might suppress aggressive responses to
social exclusion? The next section explores one possibility, namely
activation in a brain region associated with regulation of negative
emotions.
The regulatory function of right ventrolateral pre-frontal cortex
The right ventrolateral pre-frontal cortex (rVLPFC) is a potential
candidate for a neural mechanism that may weaken the link between
social exclusion and aggression. According to recent theories (Cohen
et al., 2012), rVLPFC is the neural region commonly recruited across
different forms of self-control. For example, the rVLPFC is involved in
motor control (Chikazoe et al., 2009), risk-taking behavior (Ernst
et al., 2002), control over immediate temptations (McClure et al.,
2004) and emotional control (Kim and Hamann, 2007; see also
Wager et al., 2008). More specifically, several brain imaging studies
suggest that the rVLPFC might be directly involved in the regulation or
suppression of negative emotions elicited by a wide array of stimuli
(Lieberman et al., 2004; Ochsner and Gross, 2005; Wager et al., 2008;
Berkman and Lieberman, 2009; Cohen et al., 2012). One study found
that rVLPFC activity correlated with reduced negative emotional
experience during reappraisal of aversive images (Wager et al., 2008).
In that study, the degree of activity in rVLPFC and correlated
with self-reported negative emotions, indicating not only that this
region is active when people try to regulate their negative emotions
but also that rVLPFC activity relates directly with the amount of
negative emotions an individual is able to regulate (see also Cohen
et al., 2012).
Focusing on neural responses to social exclusion, past research has
shown that the rVLPFC is often activated when people experience
threats to social belongingness, and serves also to inhibit the emotional
distress of such a threatening event. Specifically, studies have found an
inverse association between activation of rVLPFC and (i) activation of
Received 16 August 2013; Revised 27 February 2014; Accepted 16 April 2014
Advance Access publication 18 April 2014
Correspondence should be addressed to Paolo Riva, Department of Psychology, University of Milano-Bicocca,
Piazza Ateneo Nuovo, 1, 20126–Milano, Italy. E-mail: paolo.riva1@unimib.it.
doi:10.1093/scan/nsu053 SCAN (2015) 10, 352 ^35 6
ßThe Aut hor (2014). Published by Oxford University Pre ss. For Permissions, ple ase email: journals. permissio ns@ oup.c om
at Università degli studi di Milano Bicocca-Biblioteca di Ateneo on May 10, 2016http://scan.oxfordjournals.org/Downloaded from
brain regions associated with distress elicited by social rejection [e.g.
dorsal anterior cingulate cortex (dACC)] and (ii) self-reported social
distress. These findings suggest that the rVLPFC might be involved in
down-regulating the emotional distress caused by threats to social
belongingness (Eisenberger et al., 2003, 2007; Onoda et al., 2009).
Similarly, other studies have shown increased activation of the
rVLPFC when social exclusion is accompanied by social support
(Onoda et al., 2010). In addition, studies investigating individual
differences in social pain perception have found that people low in
rejection sensitivity display higher levels of rVLPFC activation when
excluded than do people high in rejection sensitivity (Kross et al., 2007;
Onoda et al., 2009). Therefore, in addition to being broadly involved in
emotion regulation, the rVLPFC plays a key role in regulating the pain
of social rejection.
What implications might these findings have for behaviors that
often accompany social exclusion? One possibility is that the regulation
of social pain by the rVLPFC may reduce subsequent aggression.
Indeed, activation of the dACC during social rejection, a likely indi-
cator of social pain, was associated with subsequent aggression but
only when participants did not possess the executive ability to regulate
the pain (Chester et al., 2013). Conversely, participants with greater
regulatory abilities showed a negative association between dACC
activation and aggression. These findings suggest that top-down,
inhibitory functions may be able to break the link between social
exclusion and aggression by negating the ability of social pain to
translate into aggression. The rVLPFC might serve just such a
regulatory or inhibitory role.
Neuromodulation via transcranial direct current stimulation
Transcranial direct current stimulation (tDCS) is a top-down modu-
latory approach that involves attaching two electrodes to the scalp and
applying a weak electrical current from the positively charged cathode
to the negatively charged anode. Although the neurophysiological
mechanisms underlying the modulation effects of tDCS are not fully
understood (Utz et al., 2010), there is evidence that anodal stimulation
increases the excitability of cortical neurons beneath the electrode,
whereas cathodal stimulation has an opposite effect (Nitsche and
Paulus, 2000). This technique therefore allows researchers to modulate
the pattern of brain responses instead of simply observing them, which
allows for causal inferences to be made.
Using tDCS, we recently found a causal relationship between
rVLPFC activity and pain regulation (Riva et al., 2012). We argue
that given the regulatory function of rVLPFC during social exclusion,
increasing the cortical excitability of this region might also reduce the
typical aggressive response that often follows social exclusion. We
hypothesized that if rVLPFC stimulation buffers against the hurt feel-
ings associated with social rejection, then rVLPFC stimulation could
also buffer against the aggressive behavior associated with social
rejection.
Overview
In this study, we tested whether non-invasive brain polarization
through anodal tDCS over the rVLPFC could decrease aggression
resulting from social exclusion. Our hypothesis is based on prior
research suggesting that the rVLPFC is involved in regulation of several
domains, includingbroadlyregulation of negative emotions
(Lieberman et al., 2004; Ochsner and Gross, 2005; Wager et al.,
2008; Berkman and Lieberman, 2009; Cohen et al., 2012) andmore
specificallyregulation of negative emotions resulting from social ex-
clusion (Eisenberger et al., 2003; Onoda et al., 2010, Riva et al., 2012).
We predicted that the increased cortical excitability resulting from
anodal tDCS stimulation over rVLPFC could potentiate the regulatory
function of this cortical region (Nitsche and Paulus, 2000), thus redu-
cing people’s tendency to react aggressively after being socially
excluded.
METHOD
Participants
Participants were 80 healthy university students (79% female;
M
age
¼23.06, s.d. ¼4.36) who received 10E($13). Participants with
a prior or existing history of neurological disease, psychiatric disorder,
epilepsy, head injury or any communication impairment were
excluded.
Procedure
A few weeks before the experiment proper, participants completed a
measure of individual differences in trait anger on the internet (i.e.
State-Trait Anger Scale; Spielberger and Sydeman, 1994). We included
this measure to control for individual differences in aggressiveness.
In the experiment proper, participants were tested individually.
They were told the researchers were studying the effect of brain stimu-
lation on the relationship between mental visualization and taste
testing. After informed consent was obtained, participants rated how
much they liked five tastes (i.e. salty, sweet, bitter, hot and spicy and
sour; 1 ¼not at all to 10 ¼extremely).
Next, participants were randomly assigned to receive either anodal
tDCS or sham stimulation over the rVLPFC. Stimulation was
applied using a constant current regulator via sponge-soaked
electrodes (DC-STIMULATOR, NeuroConn GmbH, Germany). The
25 cm
2
anodal electrode was placed over F6 (MNI coordinates: 58,
30, 8; Onoda et al., 2010), consistent with the international 10–20
system for electroencephalogram (EEG) electrode placement. The
35 cm
2
reference (cathodal) electrode was placed over the contralateral
supraorbital area. We used these electrode sizes and placements for
three reasons. First, using two differently sized electrodes is the stand-
ard procedure to increase the current underneath the target electrode
(Nitsche et al., 2008). Second, the small distance between the two
electrodes should cause a large amount of current to be shunted
through the scalp, thus further increasing the focality of the stimula-
tion (Datta et al., 2008; Bikson et al., 2010). Third, the placement of the
cathode over the supraorbital area should reduce the amount of elec-
trical stimulation because the distance between the cortical surface and
the scalp is increased, and because air is present in the sinus cavities.
A constant current of 1.5 mA intensity was applied for 20 min, lead-
ing to a current density of 0.06 mA/cm
2
for the stimulation electrode
and 0.04 mA/cm
2
for the reference electrode. For sham stimulation, the
electrodes were placed in the same position, but the stimulator was
turned on for 30 s only (Gandiga et al., 2006) and the current intensity
was gradually increased at the beginning of the session (8 s of ‘ramp
up’) and decreased at the end of the session (5 s of ‘ramp down’) to
mimic the itching sensation of the real stimulation. In the following
1157 s the stimulation was off but the monitor of the device kept
showing the impedence control. Thus, all participants believed they
received stimulation for 20 min.
Five minutes before the end of the tDCS or sham stimulation, par-
ticipants played a virtual online ball-tossing game called ‘Cyberball’
(Williams et al., 2000). Participants were told that they would
engage in a ball-throwing game with two other players, ostensibly
real participants, for the purposes of exercising their mental visualiza-
tion abilities. Participants were told that they should visualize all
aspects of the game, the players and the location. In actuality, the
two computer characters were pre-programmed agents randomly
assigned to either include or exclude the real participant from the
game. In the social exclusion condition, after a few throws, the two
tDCS, social exclusion, and aggression SCAN (2015) 353
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computer players stopped throwing the ball to the participant for the
remainder of the game. In the inclusion condition, the computer
players threw the ball to the actual participant for 10 of the 30
total tosses (Williams et al., 2000). As a manipulation check, partici-
pants were asked how often (0–100%) they received the ball.
Aggression was measured using the well-validated hot-sauce para-
digm (Lieberman et al., 1999). The experimenter gave the participants
a copy of the taste-test questionnaire with the taste preferences of one
of the other Cyberball players, which contained the value ‘2’ for ‘Hot
and Spicy’ foods. Participants were told that a random generator in the
computer would assign them to allocate vs taste one of the foods listed.
The experimenter pressed a button on the computer and the role that
was ostensibly randomly assigned to the participant appeared on the
screen. In reality, all the participants were assigned to allocate hot
sauce to their ostensible partner by putting the amount they wanted
their partner to taste in a plastic cup. They were told their partner had
to eat the entire amount in the cup and they would not know who gave
him or her the hot sauce. The amount of hot sauce allocated was
weighed using a digital scale that was accurate to 0.10 g. Giving hot
sauce to someone who does not like to eat spicy food is a face-valid
measure of aggression that is easily quantifiable and ecologically valid
(Lieberman et al., 1999). A debriefing followed. During the debriefing,
participants were asked whether they perceived any physical sensation
from the electrodes.
RESULTS
Preliminary analysis
Age and gender differences
A 2 (social inclusion vs exclusion) 2 (anodal vs sham stimulation)
between-subjects ANOVA found that excluded vs included participants
did not differ in terms of age, F(1,74) ¼1.23, P¼0.27. Similarly, the
mean age of those who received anodal stimulation was not different
from that of those who received sham stimulation, F(1,74) ¼0.23,
P¼0.64. Moreover, the number of males and females did not differ
across experimental conditions,
2
(3) ¼4.20, P¼0.24. Thus, the data
from males and females were combined for subsequent analyses.
Trait anger
A 2 (social inclusion vs exclusion) 2 (anodal vs sham stimulation)
between-subjects ANOVA found that trait anger scores did not differ
between excluded and included participants, F(1,74) ¼1.29, P¼0.26.
Similarly, trait anger scores did not differ between those who received
anodal stimulation and sham stimulation, F(1,74) ¼0.66, P¼0.42.
Physical sensation from electrodes
In line with previous research (Nitsche et al., 2008), we found that very
few participants (i.e. 5 of 80, or 6%) reported experiencing physical
sensation from the electrodes. Crucially, a Pearson chi-square test
showed that self-reported physical sensation did not vary across ex-
perimental conditions,
2
(3) ¼2.28, P¼0.51.
Exclusion manipulation check
A 2 (social inclusion vs exclusion) 2 (anodal vs sham stimulation)
between-subjects ANOVA found that excluded participants reported
receiving fewer tosses (11.20%) than did included participants
(28.82%), F(1,76) ¼61.99, P< 0.001, d¼1.73. Crucially, percentage
of throws was not affected by the tDCS manipulation [Interaction:
F(1,75) ¼0.23, P> 0.63,
p2
¼0.00], suggesting that participants in
the tDCS and sham stimulation groups were equally cognitively
aware of their inclusionary status during the game.
Primary analyses
A22 ANOVA found that excluded participants behaved more
aggressively (M¼10.84, s.d. ¼8.41) than did included participants
(M¼6.53, s.d. ¼3.52), F(1,76) ¼9.87, P< 0.002, d¼0.72. This finding
replicates numerous studies showing that social exclusion can increase
aggression. Although it was in the predicted direction and not trivial in
size, the main effect for stimulation type was not significant,
F(1,76) ¼2.30, P< 0.14, d¼0.35. Most important, the predicted inter-
action effect was significant, F(1,76) ¼5.26, P< 0.025,
p2
¼0.065.
As can be seen in Figure 1, socially excluded participants given
anodal stimulation over the rVLPFC were less aggressive than those
given sham stimulation, F(1,76) ¼7.28, P< 0.009, d¼0.62. Among
socially included participants, no aggression differences emerged be-
tween the anodal and sham stimulation, F(1,76) ¼0.30, P< .59,
d¼0.12. Crucially, excluded participants who received anodal stimu-
lation were no more aggressive than included participants,
F(1,76) ¼1.22, P< 0.28, d¼0.41 (see Figure 1).
DISCUSSION
Domestic violence, school shootings and workers’ disruptive reactions
following their discharge represent a few examples of the strong link
between social rejection and aggressive behavior. Past research has
shown that when people are rejected, ostracized or humiliated (e.g.
when they are unable to fulfill the ‘need to belong,’; see Baumeister and
Leary, 1995), they often behave aggressively against those who exclude
them (Twenge et al., 2001; Buckley et al., 2004; MacDonald and Leary,
2005; Leary et al., 2006; DeWall et al., 2009; Riva et al., 2011), and they
sometimes even aggress against innocent targets (e.g. Twenge et al.,
2001; DeWall et al., 2010).
Previous research has also identified the rVLPFC as a critical region
involved in emotion regulation (Lieberman et al., 2004; Ochsner and
Gross, 2005; Wager et al., 2008; Berkman and Lieberman, 2009; Cohen
et al., 2012). Furthermore, previous research has shown that anodal
tDCS over the rVLPFC can decrease pain following social exclusion
(Riva et al., 2012).
The present experiment sought to test the possible modulatory role
of the rVLPFC on the link between social exclusion and aggression. We
replicated the well-documented finding that social exclusion triggers
Fig. 1 Hot sauce allocation (in grams) for excluded and included participants given anodal or sham
stimulation. Capped vertical bars denote 1 SE.
354 SCAN (2015) P. R iv a et al.
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behavioral aggression. Specifically, excluded participants gave a greater
amount of hot sauce to an interaction partner who hated spicy foods
than did included participants. More important, we found that
increasing the cortical excitability of the rVLPFC reduced the relation-
ship between social exclusion and aggression. Specifically, we found
that those who were excluded but received tDCS stimulation over the
rVLPFC were no more aggressive than included participants. Thus,
aggression decreased when brain stimulation (vs sham stimulation)
was applied over the rVLPFC following social exclusion.
The results of the present study thus provide evidence for the causal
role of rVLPFC in emotion regulation. The type of montage used in the
present study aimed at obtaining a stronger current underneath our
target electrode. However ‘target’ and ‘reference’ are conventional
terms for the electrodes, and we cannot rule out that a weaker neuro-
modulatory effect was present underneath the cathode. It is therefore
possible that a cathodal-inhibitory effect over the left pre-frontal re-
gions (lPFC) affected the observed results. Thus, future research should
test whether decreasing the cortical excitability (through cathodal
stimulation) of the lPFC is necessary to produce the behavioral effect
we found.
To our knowledge, this is the first research to show that neural
stimulation can disrupt the link between social exclusion and aggres-
sion. Our study supports and extends previous correlational research
suggesting the modulatory role of rVLPFC in a variety of domains,
including control over immediate temptations (McClure et al., 2004)
and emotional control (Kim and Hamann, 2007; Wager et al., 2008).
More generally, we showed how brain stimulation techniques (i.e.
tDCS) have the potential to make a unique contribution to the field
of social neuroscience applied to aggression research. Indeed, these
techniques (e.g. tDCS, TMS) have an exclusive capacitycompared
with brain imaging techniquesto modulate distinct components of
the neural system and allow the measurement of observable behavioral
changes.
Providing evidence for the causal role of the rVLPFC activity in
modulating aggressive responses to social exclusion, our experiment
contributes to the growing literature focused on understanding the
neural and psychological underpinnings of the rejection–aggression
link (Chester et al., 2013).
Limitations and future research
A possible limitation of tDCS is its low spatial resolution. However,
tDCS effects largely come from the cortical area beneath the electrode
(see Zaghi et al., 2010). Computer-based modeling studies show that
the direct functional effects of tDCS are restricted to the area under the
active electrode (Miranda et al., 2006). Nevertheless, future research
should test for the feasibility of adopting other stimulation techniques,
such as repetitive transcranial magnetic stimulation (rTMS) over the
rVLPFC, thus providing more detailed information of the effect we
found.
As to the underlying mechanism, rVLPFC stimulation is known to
numb the pain of social rejection (Riva et al., 2012), and this might
make rejected people less likely to aggressively lash out against others
(see MacDonald and Leary, 2005). Another possibility is that stimulat-
ing the rVLPFC reduces the negative emotions people experience
during social exclusion (see Riva et al., 2011). Therefore, future studies
should test the possibility that the perception of social distress and/or
negative emotions mediate the effect of tDCS on the link between
social rejection and aggression.
We recognize that other mechanisms may play a role in the effect of
tDCS stimulation on aggression. For instance, previous research has
linked greater right than left frontal cortical activity to avoidance mo-
tivation or inhibition, whereas greater left than right frontal cortical
activity has been linked to approach motivation (such as aggression;
see Harmon-Jones et al., 2010). Accordingly, a recent study found that
anodal stimulation over lPFC increased the anger–aggression link
(Hortensius et al., 2012). It is thus possible that increasing the cortical
excitability through anodal tDCS stimulation over right PFC counter-
acts the approach motivation that precipitates aggressive behavior.
Therefore, we recognize that a challenge for future research is to
identify potential mediating variables of the modulatory effect of
tDCS on aggression.
CONCLUSION
The present research provides critical knowledge in understanding the
role of a neural structure (i.e. the rVLPFC) that seems to be critically
involved in regulating aggressive responses that typically follow social
rejection. As Steinbeck insightfully observed in 1945, ‘there are two
possible reactions to social ostracismeither a man emerges deter-
mined to be better, purer, and kindlier or he goes bad, challenges
the world and does even worse things’. The present research shows
that people are less likely go bad or do even worse things, such as
aggress against others, following stimulation to the portion of the
brain that regulates negative emotions and the pain of social rejection.
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