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REVIEW ARTICLE
published: 19 November 2013
doi: 10.3389/fnins.2013.00211
The neurobiology of collective action
Paul J. Zak1,2*and Jorge A. Barraza1
1Center for Neuroeconomics Studies, Claremont Graduate University, Claremont, CA, USA
2Department of Neurology, Loma Linda University Medical Center, Loma Linda, CA, USA
Edited by:
Masaki Isoda, Kansai Medical
University, Japan
Steve W. C. Chang, Duke University,
USA
Reviewed by:
Karli K. Watson, Duke University,
USA
Jean-Francois Gariépy, Duke
University, USA
*Correspondence:
Paul J. Zak, Center for
Neuroeconomics Studies,
Claremont Graduate University,
Harper East 208, 150 E. 10th St.,
Claremont, CA 91711, USA
e-mail: paul.zak@cgu.edu
This essay introduces a neurologically-informed mathematical model of collective action
(CA) that reveals the role for empathy and distress in motivating costly helping behaviors.
We report three direct tests of model with a key focus on the neuropeptide oxytocin
as well as a variety of indirect tests. These studies, from our lab and other researchers,
show support for the model. Our findings indicate that empathic concern, via the brain’s
release of oxytocin, is a trigger for CA. We discuss the implications from this model for
our understanding why human beings engage in costly CA.
Keywords: oxytocin, prosocial behavior, neuroscience, economics, empathy
INTRODUCTION
How do people come together to achieve a common goal? This
essay will argue that the physiologic drivers of collective action
(CA) are the same mechanisms that are involved in the experience
of empathy. Specifically, we present a formal model and describe
neuroeconomics studies from our lab that have revealed empa-
thy, and empathic concern in particular, as a crucial component
of CA. Herein we review studies from our lab that demon-
strate the neuroactive hormone oxytocin instantiates empathy
and promotes prosocial behaviors, including CA (for other simi-
lar reviews of the human oxytocin literature see Bartz et al., 2011;
De Dreu, 2012; Feldman, 2012; Guastella and MacLeod, 2012;
Kumsta and Heinrichs, 2012; Van IJzendoorn and Bakermans-
Kranenburg, 2012; Carter, 2013; for similar reviews focusing on
neural activity see Shamay-Tsoory, 2011; Decety et al., 2012). We
begin with the understanding that most CA is not done for purely
altruistic or other-regarding motives. For instance, people may
volunteer for a cause out of concern for others, but may also vol-
unteer out of a felt or social obligation, to build their reputation,
or to feel better about themselves (e.g., Omoto and Snyder, 1995).
This review focuses on the role of one particular motive for CA:
empathy. A biologically based human capacity, empathy has been
found to motivate prosocial behaviors (e.g., Eisenberg and Fabes,
1990; Batson and Oleson, 1991; Penner et al., 2005). Empathy
can promote CA by reducing self-regarding concerns and enhanc-
ing other regarding motives (e.g., Batson, 1991). We propose that
empathy is a motive for CA, an adaptive human behavior with
neurobiological underpinnings (for similar arguments see Brown
and Brown, 2006; de Waal, 2008; Gonzalez-Liencres et al., 2013).
This idea was captured in Adam Smith’s (1759) mas-
terwork The Theory of Moral Sentiments where he wrote,
“Generosity, humanity, kindness, compassion, mutual friendship
and esteem...please the indifferent spectator upon almost every
occasion. His sympathy with the person who feels those passions,
exactly coincides with his concern for the person who is the
object of them” (Vol. 1, ch. iv, para. 313). In discussing sympa-
thy, or “fellow-feeling” as Smith defined it, we will use the word
empathy (a term derived from an 1858 coinage einfühlung or
“feeling into” by German philosopher Rudolf Lotze (1817−1881)
that more closely captures the notion of an innate human capac-
ity for one individual to respond to the experiences of another
(Davis, 1996).
The literatures describing empathy are large and diverse
(Batson, 2010), but our focus is on a narrower notion, empathic
concern. Empathic concern is an emotion that is felt for another
person (also see Barraza and Zak, 2013) and has been called the
“root of all altruism” (McDougall, 1926). Empathic concern has
been used interchangeably with notions of compassion (Batson,
2010), though we prefer the former term as being less generally
used and thus less prone to misuse. Those who become aware of
distress in others and are able to regulate the arousal that arises
from it are more likely to experience empathic concern (Eisenberg
and Fabes, 1990).
We begin by presenting a rationale for CA. Next, we intro-
duce a neurobiologically-based model of prosocial behaviors in
order to identify empathic concern as a proximal mechanism for
CA. We then introduce evidence from recent studies from our
lab suggesting a role for the neuropeptide oxytocin in produc-
ing empathic concern and inducing CA. Figure 1 summarizes the
proposed relationships.
A MATHEMATICAL MODEL OF COLLECTIVE ACTION
CA refers to a set of behaviors that are performed with others to
meet a goal or strive to make progress on a desired outcome. CA
includes both cooperative behaviors (where two or more people
work toward a mutually beneficial outcome) and collective help-
ing behaviors (where two or more people work for the benefit of
others not involved in the action). CA can be a single event (e.g.,
assisting someone who is drowning, pitching in money or time
for a group picnic) or can extend over a long period of time (e.g.,
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Zak and Barraza The neurobiology of collective action
FIGURE 1 | A physiologic model of collective action. Oxytocin induces
empathic concern that increases the likelihood of collective action.
volunteering weekends at a retirement home, or the provision of
public goods). Thus, CA includes a wide array of actions that
are done for the benefit of others at some cost to the individual,
whether or not these benefits extend to the self.
Why do people intentionally engage in behavior where the self
bears a direct or opportunity cost? Game theoretic models derived
from the prisoner’s dilemma show that conditional cooperation
is typically a better long-term strategy than consistent defection
(Axelrod, 1984). These models, however, generally focus on why
people would engage in behaviors that, although benefiting oth-
ers, eventually benefit the actor. Tellingly, some forms of CA may
provide little or no direct, immediate, or guaranteed benefit to the
actor (Melis and Semmann, 2010).
Empathic concern for another’s welfare may be a proxi-
mate mechanism motivating individuals to engage in costly CA.
Empathic concern is a candidate mechanism for CA because it
allows individuals to focus on the state of others, even in situa-
tions where there may be no direct benefit for the actor (de Waal,
2008). For example, empathic concern after a signal of distress or
request for help, resolves the problem of reciprocal motives for
CA where the actor benefits at a later time by placing weight on
the well-being of others.
Behavioral scientists have found that empathic concern tips
the scale in favor for prosocial engagement (e.g., Batson, 1991;
Davis, 1996; Sober and Wilson, 1998; Preston and de Waal,
2002). The arousal: Cost-reward model of helping behavior
(Dovidio, 1984; Dovidio et al., 1991) states that in order for peo-
ple to be motivated to help others, they have to first become
aware of the need of others for help. Aversive arousal elicited
through emotional contagion makes the need for intervention
salient. Aversive arousal then motivates a cognitive weighing of
the costs and benefits for acting prosocially. Empathic concern
is assumed to increase the costs for not engaging, for exam-
ple, producing guilt, shame, and further distress if the observer
does not help or cooperate. An explicit model of prosocial
emotions such as guilt and shame prompting costly prosocial
behavior was proposed by Bowles and Gintis (2003). Empathic
concern may reward those who help others, for example, pro-
ducing a so-called warm glow utility flow (positive affect for
engaging in helping others; Andreoni, 1990) or other internal
reward (Harbaugh et al., 2007) as we will propose in the model
below.
The empathy-altruism hypothesis (e.g., Batson, 1991; Batson
and Oleson, 1991), suggests that an empathic response is a nec-
essary component in human prosocial behaviors. The arousal
experienced from witnessing another’s aversive state leads to
divergent affective reactions, especially distress and empathic con-
cern. Whereas distress (self-focused aversive feelings) motivates
a desire to reduce aversive arousal, empathic concern causes one
to attend to the other’s aversive state. Those who are distressed
may seek to escape the arousing situation (either psychologically
or physically) when it is less costly than staying involved (Batson,
1987). On the other hand, empathizing with those requiring help
makes it difficult to disengage without seeking to relieve the
other’s distress.
A large number of psychological studies have supported
the link between empathic concern and prosocial engagement.
Instead of reviewing this extensive literature (e.g., see Davis, 1996;
de Waal, 2008; Batson, 2010), we use volunteerism to illustrate
the role of empathic concern in CA. Volunteerism is a form
of CA that occurs in the context of groups and organizations,
where people give of their time for the benefit of a person,
group, or cause (e.g., Penner et al., 2005). Volunteerism is inter-
esting because it is long-term planned behavior (Penner, 2002).
As such, volunteering is less influenced by situational factors
than other prosocial actions. Further, volunteering is typically
focused on aiding strangers to whom there is no social obliga-
tion (Omoto and Snyder, 1995). In general, volunteers have been
found to be more dispositionally empathic than non-volunteers
(e.g., Rushton, 1984; Bekkers, 2005). Those who score high in
dispositional empathy anticipate feelings of empathy and satis-
faction during volunteering and are more willing to volunteer
because of those feelings (Davis et al., 1999). Individuals who
report empathy-driven prosocial motives for volunteering, for
example expressing values and concern for their community, are
found to persist longer as volunteers than those who endorse
self-oriented motives like enhancing their employability or to feel
better about themselves (e.g., Clary and Orenstein, 1991; Penner
and Finkelstein, 1998). These findings indicate that empathic con-
cern is a key factor in motivating and sustaining one form of
CA—volunteerism. In the model of CA that follows, we seek
to clarify the mechanisms through which empathic concern and
distress affect other-regarding behaviors.
The model we propose is a neurologically-informed extension
of the model in Zak et al. (2007) that is based on a decade’s
worth of experiments using an inductive approach (Park and Zak,
2004; Vercoe and Zak, 2010) in which experimental treatments
are systematically varied before a model is proposed. The goal in
presenting this model is not to replace traditional game theoretic
models of CA, but to extend these models to include the role of
empathic concern during social interactions.
The model takes as its foundation a model introduced in a
footnote by the prominent Irish social philosopher Edgeworth
(1881/2012) in his book Mathematical Psychics: An Essay on the
Application of Mathematics to the Moral Sciences where utility
is obtained from one’s own consumption and a weighted util-
ity of another’s consumption (Edgeworth, 1881/1967). Andreoni
(1990); Sally (2001, 2002),andLevitt and List (2007) have pro-
posed similar models without drawing on neural findings, while
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Zak and Barraza The neurobiology of collective action
Morishima et al. (2012), develop a neurally-informed mathemati-
cal model based on theory of mind. Similar to Morishima et al. we
propose a model steeped in experimental findings that can shed
new insights into CA. The model differs from Edgeworth and the
existing literature by including responses that are conditional on
one’s own, and the other’s, physiologic states.
The decision-maker, who we will identify as person 1, faces the
following decision problem
Maxb1b2E{U(b1)+α(τ)U(b2)}
s.t.b1+b2=M
where U(b1) is the utility person 1 receives from consuming ben-
efits b1,b2is the benefit that person 2 receives from person 1,
U(b2) is the utility person 2 obtains from b2, and total resources,
M, are finite. Assume U(b) is increasing, continuous and strictly
concave. Person 1 chooses b1and b2through this constrained
optimization problem. We will call this the Empathy-Collective
Action model.
Edgeworth called the weight αon the other’s utility “effec-
tive sympathy” (1881/1967, p. 53) and considered it a constant;
using Lotze’s definition of emotional contagion, we will call α
“empathic concern.” Our Empathy-Collective Action model gen-
eralizes Edgeworth by identifying CA as an individually costly
behavior and by taking into account the motivation for proso-
cial action by letting empathic concern depend on the situation
the decision-maker faces. Specifically, let α(τ): [0,1]→+be
a continuous hyperbolic function where empathic concern, α,
depends on the observed distress of person 2, τ.Theparame-
ter τcaptures the distress that motivates the decision-maker to
pay attention to the needs of the other person. As previously dis-
cussed, “distress” should be understood as any situation in which
the behavior or emotional state of another (or group of others)
suggests that they may need assistance. The function αhas the fol-
lowing properties, α(0)≥0, limτ→∞ α(τ)=0, and τ∗=argmax
α(τ),withα(τ∗)>α(0),andτ∗finite. That is, α(τ)has the shape
of a parabola.
The empathic concern function α(τ)is hyperbolic because
moderate distress motivates action, but high degrees of distress
are aversive causing one to want to escape rather than help (e.g.,
Batson et al., 1987). For example, if one sees someone sprain an
ankle and fall to the ground, most people are motivated to help.
Seeing someone with a bloody compound fracture of the ankle
may be so distressing that many bystanders will flee and avoid
helping. Alternatively, distress may arise from social pressures of
inaction.
In the Empathy-Collective Action model, when α(τ)=0, per-
son 1 is completely self-interested, and when α(τ)=1 s/he is
other-regarding, sharing benefits equally with person 2. Values of
α(τ)>1 cause person 1, at an optimum, to offer more resources
to person 2 than she keeps herself. It is straightforward to prove
that as αrises, the benefits to person 2, b2, increase. Different
values of αwould account individual variations in empathic con-
cern and resulting differences in individually-costly CA. Indeed,
CA, where an individual bears a direct or opportunity cost dur-
ing CA, requires a positive value of α(τ). The model’s value is that
is shows how individual variations in empathic concern (α)and
the social environment (τ) can be included in a game-theoretic
model of CA. If one exhibits low CA in a given situation, the
model predicts that either empathic concern or one’s perception
of the needs of others (or both) is low. For example, an adult wait-
ing to cross a busy street may not elicit costly CA by those nearby,
but a small child alone seeking to cross such a street is likely to
produce greater CA, especially among parents who may be more
sensitized to children.
Our next task is to present neurobiological evidence showing
that empathy affects CA.
NEUROBIOLOGICAL MECHANISMS
Knowing the neurobiology of empathic concern not only pro-
vides additional information on mechanism, but may also
produce additional testable implications and applications (see
Neurobiological Mechanisms). A large body of work now exists
on the neural basis for empathy using functional MRI which
have been reviewed in detail elsewhere (see Lamm et al., 2011;
Shamay-Tsoory, 2011; Bernhardt and Singer, 2012). These studies
generally locate empathy within the brain’s pain matrix, specif-
ically in the anterior cingulate cortex and the anterior insula
(Singer et al., 2004, 2006; Hein and Singer, 2008). However, these
studies focus on the distress aspect of social engagement by study-
ing responses to pain rather than the possible rewards of empathic
concern.
The Empathy-Collective Action model of prosocial behavior
that posits a utility flow or “warm glow” is consistent with find-
ings from two studies using fMRI by examining donations to
charities. Moll et al. (2006) found that brain regions differentially
more active during donations to preferred charities compared
to unpreferred charities included striatal regions associated with
rewarding stimuli. These researchers also found that contrast-
ing brain activity during charitable donations and individual
reward revealed activation in the subgenual cortex, a brain region
that modulates rewards associated with affiliative behaviors. In
a related study of charitable donations, Harbaugh et al. (2007)
found that donating to a charity, relative to keeping money for
oneself, also produced activation in striatal regions of the brain.
They further showed that voluntary donations to charity were
associated with a greater subjective experience of satisfaction and
larger striatal activation than mandatory donations.
THE ROLE OF OXYTOCIN
The best evidence for the role of empathic concern affecting CA
would be to discover a manipulable neural mechanism that would
raise or lower αin the Empathy-Collective Action model. The
word “manipulable” is important here to demonstrate that such
a mechanism directly causes CA.Ifwepushonthismechanism
(somehow), we would expect to see less self-focused benefits b1,
andmoreother-focusedbenefitsb2.
Oxytocin (OT) is an evolutionarily ancient molecule that is a
key part of the mammalian attachment system supporting costly
care for offspring. In socially monogamous mammals, OT and
a closely related hormone, arginine vasopressin, facilitate attach-
ment to and protection of mates (see Carter, 1998). Maternal (and
in some species paternal) care for offspring is a template for more
general other-regarding behaviors (Sober and Wilson, 1998; de
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Zak and Barraza The neurobiology of collective action
Waal, 2008). In the human brain, high densities of OT receptors
are primarily found in the amygdala, hypothalamus, and subgen-
ual cortex (Tribollet et al., 1992; Barberis and Tribollet, 1996),
brain regions associated with emotions and social behaviors.
OT can be measured in blood and cerebral spinal fluid, and
synthetic OT can be infused into human beings intravenously or
intranasally to gauge its effects on behaviors (Churchland and
Winkielman, 2012). A key issue for studying OT in humans is that
under physiologic stress, central (brain) and peripheral (body)
OT co-release (Wotjak et al., 1998; Neumann, 2008). This means
that a change in blood levels in OT after a stimulus is likely to be
positively correlated with changes in OT in the brain. In addi-
tion, peripheral OT binds to receptors in the heart and vagus
nerve, reducing anxiety and cardiovascular tone (see Porges, 2001,
2007) and thereby signaling approachability. OT binding in ani-
mals is associated with the modulation of midbrain dopamine
and serotonin (Pfister and Muir, 1989; Liu and Wang, 2003).
Studies using OT infusion in humans have shown that it
enhances the ability to infer others’ emotions and intentions from
facial expressions (Domes et al., 2007). OT also increases the
time spent gazing toward the eye region of the face (Guastella
et al., 2008), and the recognition of faces (Savaskan et al., 2008).
Mice with the gene for the OT receptor knocked out have social
amnesia—they do not appear to remember animals they have
previously encountered (Ferguson et al., 2000).
Situations that motivate CA often involve a request for help.
Such requests may provoke both empathic distress and concern
as in the Empathy-Collective Action model. OT infusion has been
shown to reduce activity in the amygdala in response to socially
fearful stimuli (Kirsch et al., 2005) and fear conditioned stim-
uli (Petrovic et al., 2008). By reducing anxiety, OT may help
people sustain CA over extended periods of time. Social psychol-
ogist Shelley Taylor calls this the “tend and befriend” role of OT
(Taylor et al., 2000; Taylor, 2006), where OT reduces anxiety and
promotes affiliative behaviors in response to stress.
TRUST, RECIPROCITY, AND COOPERATION
Our lab was the first to demonstrate that OT promotes proso-
cial behaviors among human beings (Zak et al., 2004, 2005).
We began this research in 2001 by examining the role of OT in
facilitating trust between strangers. In these studies, we used a
task from experimental economics called the trust game (Berg
et al., 1995). In our trust experiments, participants were endowed
with $10 to compensate them for their time and discomfort (see
below). They were then given the opportunity to increase their
earnings by making a single decision by computer and without
coordinating with others using their $10. For this task, they were
matched randomly in dyads with random assignment to the roles
of decision-maker 1 (DM1) or decision-maker 2 (DM2). All DMs
received extensive and identical instructions informing them that
DM1 could transfer some of his or her endowment to the DM2
in dyad, and this amount would be removed from DM1’s account
and tripled in DM2’s account. DM2 was then notified by com-
puter of the tripled transfer from DM1 and was reminded of
the total in his or her account. After this, the software prompted
DM2 to return to DM1 any amount from zero to the account
total. The return transfer was not tripled and was removed from
DM2’s account on a one-to-one basis. After these two decisions,
the interaction was concluded. The consensus view in economics
is that the DM1 transfer denotes trust, and the DM2 transfer
captures reciprocity or trustworthiness.
So why would DM2 return any money, something partici-
pants do 98% of the time (Zak et al., 2007)? We found that
the more money DM2s received, the greater the increase in OT.
Importantly, the higher the spike of OT for DM2, the more she
or he reciprocated by returning money to the DM1 who showed
trust (Zak et al., 2004, 2005; Zak, 2012). Nine other hormones
(e.g., vasopressin, estradiol) were ruled out for mediation or inter-
active effects, supporting the direct link between endogenous OT
release and trustworthiness.
We next demonstrated the causal effect of OT on trust by
administering 24IU of synthetic OT intranasally, a method uti-
lized to enhance OT levels in the brain. After allowing for an hour
for the OT to enter the brain, participants played the trust game.
Not only did the average level of trust rise for those given OT,
more than twice as many people on OT showed maximal trust
by sending all of their money to a stranger (45 vs. 22% for those
on placebo; Kosfeld et al., 2005). There was no effect of OT on
an objective risk-taking task, providing evidence for its uniquely
social effects. Moreover, the results were not due to changes in
mood or cognitive blunting. These studies provide evidence that
OT helps us determine who to trust and when to reciprocate, two
key ingredients for CA.
Certainly trust can promote CA, but our trust research left
open two important questions: are there non-pharmacologic
ways to raise OT? and, is OT directly associated with empathic
concern? In our trust experiments, the receipt of money denoting
trust resulted in a substantial spike in endogenous OT relative to
baseline. Prior to our work, the only known ways to raise OT in
humans were to go into labor, to breastfeed a child, or to engage
in sexual activity. These methods of raising OT are impractical
for laboratory experiments, so we began to search for other ways
endogenous OT might be manipulated. Research in rodents pro-
vided equivocal data that belly stroking might induce OT release.
To test this in humans, we used licensed massage therapists to give
participants a 15-min moderate pressure back massage. A con-
trol group simply rested quietly for 15 min on different days.
Participants had their blood drawn and played the trust game one
time. We found that massage raised OT (Morhenn et al., 2008,
2012), and for DM2s in the trust game, massage primed the brain
to release 16% more OT than DM2 controls. Amazingly, recipro-
cation was 243% higher by DM2s in the massage group relative
toDM2controls(Morhenn et al., 2008).ThechangeinOT
strongly predicted the amount of money DM2s would sacrifice
to reciprocate to DM1s.
We next undertook direct tests of the zero-sum Empathy-
Collective Action model using a task called the Ultimatum Game
(UG Güth et al., 1982). In this game, participants were again
put into dyads and randomly assigned to the roles of DM1 and
DM2. DM1 began the experiment with $10 while DM2 began
with nothing. After extensive and identical instructions, DM1 was
prompted by computer to propose a split of the $10 to DM2. If
DM2 accepted the proposal, the money was paid. The catch was
that if DM2 rejected the proposal, both DMs received nothing. In
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Zak and Barraza The neurobiology of collective action
Western countries, offers less than $3 are nearly always rejected.
We hypothesized that raising OT would increase empathy, α,and
generate more generosity (generosity was defined as the amount a
DM1 proposal exceeded the minimum acceptable offer by DM2s).
Note that using the zero-sum UG, rather than a positive-sum trust
game, sets the bar for the effects of OT substantially higher than
in positive-sum games. In the trust game, we showed that OT
was associated with reciprocity but that on average both DM1s
and DM2s increased their earnings. In the UG OT was hypothe-
sized to affect costly generosity in which more for DM2 meant less
for DM1. This is just what we found. Infusing 40IU intranasally
into participants caused an 80% increase in generosity relative to
subjects who received a placebo (Zak et al., 2007). Generous par-
ticipants left the lab with less money, but were not less happy
on debriefing than those who were not generous. This pro-
vided the first evidence αcould be manipulated by manipulating
central OT.
The second test of the Empathy-Collective Action model used
testosterone infusion to create “alpha males” in a double-blind
cross-over paradigm (Zak et al., 2009). There is some evidence
that testosterone inhibits OT binding to its receptor (Insel et al.,
1993) and thus testosterone was expected to reduce generosity.
This was indeed what we found. We raised total testosterone
an average of 60% above baseline (free testosterone, and dihy-
drotestosterone, which are more active biologically than total
testosterone, were raised 97 and 128% respectively; all changes
were greater than zero at p<1E-6). Men whose testosterone was
artificially raised, compared to themselves on placebo, were 27%
less generous in the UG. Moreover, the reduction in generosity fell
rapidly as a man’s level of total-, free- and dihydro-testosterone
(DHT) rose, revealing a parametric effect of testosterone on gen-
erosity. For example, participants in the lowest decile of DHT had
85% higher average generosity ($3.65 out of $10) compared to
generosity by those in the highest decile of DHT ($0.55 out of
$10). Interestingly, the enhanced “alpha males” also had a 5%
higher threshold (p=0.001) to punish those who were ungen-
erous toward them. This experiment revealed that αcould be
reduced in the Empathy-Collective Action model.
In a third experiment, we examined whether endogenous OT
was associated with the subjective experience of empathic concern
by having participants watch a 100 s highly emotional video of a
father and his son who has terminal brain cancer (Barraza and
Zak, 2009). A control video had the same father and son going
to the zoo but did not mention cancer or death. We found that
watching the emotional video caused a 47% increase in OT rel-
ative to baseline. Importantly, the change in OT was correlated
withsubjectivereportsofempathicconcernoncewecontrolled
for the distress that participants felt. We also found that those who
were more empathically engaged made more generous offers in
the UG, and generosity in the UG was associated with larger dona-
tions of participants’ earnings to charity at the conclusion of the
experiment. Participants who scored high in a measure of dispo-
sitional empathy (using the Interpersonal Reactivity Index, Davis,
1983), experienced greater empathic concern after the emotional
video and had a larger increase in OT after viewing the emotional
video. The participants who were most empathic and released the
most OT were women; women were also more generous and gave
more money to charity than did men. This study is the first to
provide direct evidence that OT is associated with empathic con-
cern, confirming the intuition of Adam Smith and the design of
the Empathy-Collective Action model.
DEFECTORS AND FREE-RIDERS
Defection is the death-knell of CA. When people begin to free-
ride, for example in public goods games, others typically follow
suit (Camerer, 2003). In our studies using the trust game using
college students, we find that 95% of DM2s who have been
trusted reciprocate. The degree of reciprocation for this 95% are
predicted by their OT levels. The other 5% are unconditional
non-reciprocators, they return nothing or very little money no
matter how much they are trusted. We found that OT levels
of non-reciprocators are abnormally high, indicating OT dys-
regulation. Psychologically, these people have traits similar to
psychopaths (Zak, 2005, 2012).
We have recently extended this finding by studying patients
with social anxiety disorder (Hoge et al., 2008).They,too,have
high levels of OT. Because the brain works through contrast, high
OT masks any additional OT release when receiving a signal of
trust, thus inhibiting a behavioral response. Similarly, a study
of those diagnosed with borderline personality disorder (BPD),
which is associated with a compromised ability to interpret social
signals, showed an inability to maintain reciprocity in the trust
game (King-Casas et al., 2008). This inability to cooperate seemed
to be mediated by abnormal activity in the anterior insula, a brain
region previously associated with empathy for pain (Singer et al.,
2004, 2006); whereas psychologically healthy individuals showed
a strong parametric relationship between amount received in the
trust game and anterior insula activation, no such relationship
was found for BPD subjects suggesting a possible empathy deficit
in BPD.
Our discovery of the “five percent rule” for free-riders
(Shermer, 2008; Zak, 2012) in a fixed institutional setting is
important in understanding CA. It suggests that not all people
can be expected to participate in a collective project, even when
the issue is salient and people are highly motivated. When the
social, economic or institutional environments are less than opti-
mal, greater defection from CA will be expected as high levels of
stress inhibit OT release (Carter, 1998). This is reflected in a low
value of αin the Empathy-Generosity model, making the envi-
ronment in which CA problems are solved important (Dietz et al.,
2003). On the upside, our studies indicate that the majority of the
population–including a study of aboriginal people in Papua New
Guinea (Zak, 2012) release OT for a large variety of stimuli.
COLLECTIVE ACTION THROUGH CHARITABLE INSTITUTIONS
We have now conducted several studies examining giving through
charitable institutions. Charitable donations are unique from
other forms of CA as it is typically done without any direct expo-
sure to the beneficiary or direct knowledge of how the individual
contributions will be used. Though performed by individuals,
charitable giving functions through the collective contributions
made to an institution to address an issue of interest to its contrib-
utors. Barraza et al. (2011) examined whether 40IU of OT would
increase donations in a lab donation task. Participant in the OT
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Zak and Barraza The neurobiology of collective action
condition gave 48% more money than those in the placebo condi-
tion. This result was later replicated by others using a smaller dose
(24IU) and a different charity (Van IJzendoorn et al., 2011). In
another study, participants viewed public service announcements
(PSAs) relating to social and health related issues after 40IU of OT
infusion (Lin et al., 2013). Participants were given an opportu-
nity to donate some of their earnings to the charities promoted in
the ads. We found those who received OT donated to 33% of the
causes while participants receiving the placebo donated to 21% of
the featured charities. OT also increased the size of donation by
56% compared to placebo.
Another set of evidence comes from a growing body of
research examining the association between single nucleotide
polymorphisms (SNPs) of the oxytocin receptor (OXTR) gene,
and social behaviors. Work from others indicated an association
between OXTR SNPs and empathy (Rodrigues et al., 2009; Wu
et al., 2012a)aswellasprosocialbehaviors(Poulin et al., 2012;
Wu et al., 2012b). In a recent study (Barraza et al., in preparation)
we explored if OXTR SNPs affected CA done through charita-
ble institutions. Three of the OXTR SNPs examined (rs237887,
rs2268490, rs2254298) were linked with making a charitable
contribution in a laboratory task. Participants were also asked
to report their donations to charitable institutions outside the
lab. Here, an association between OXTR and monetary dona-
tions was found for rs237887 (AA donating more than AG/GG),
and rs53576 (AA/AG donating more than GG). Individuals with
AA/AG genotype of rs53576 were found to be more likely to
donate to religious charities (versus GG). Unexpectedly, we dis-
covered that these same participants (rs53576: AA/AG) were
more religious than their counterparts (rs53576: GG). Mediation
analysis and indicated that the association between rs53576
and donations was a result of the relationship between rs53576
and religiosity. A possible interpretation is that OT may func-
tion by promoting CA through membership in an existing
group.
RITUAL AND INTERGROUP BEHAVIOR
CA involves both coordination with and a preference to affil-
iate with group members. It has been hypothesized that OT
motivates cooperation especially for one’s in-group by promot-
ing (i) in-group favoritism, (ii) in-group cooperation, and (iii)
defense-motivated non-cooperation toward threatening outsiders
(De Dreu, 2012). OT administration increases bias for ones in-
group when groups are formed for the experiment itself (De Dreu
et al., 2010, 2011; Stallen et al., 2012). Although these studies
provide evidence for in-group preference, they do not provide
support for OT promoting antisociality toward an out-group (see
Van IJzendoorn and Bakermans-Kranenburg, 2012)andmaybe
alternatively explained by OT’s social saliency properties (Chen
et al., 2011). Moreover, OT’s in-group-specific effects may only
arise out of zero-sum tasks between groups, where cooperation
can only be performed at a cost to an out-group. Support for
this interpretation was found by Israel et al. (2012) using a task
that allowed for intergroup cooperation. These scholars reported
that OT promoted both in-group and out-group cooperation,
although those who received OT allocated more resources ben-
efiting their in-group compared to placebo recipients. We have
produced results that fall somewhere in between the DeDreu
et al. and Israel et al. studies. In our study of charitable dona-
tions mentioned above, we found OT increased the size of
charitable donations with a trend toward a preference for an
in-group vs. an out-group charity (American Red Cross or the
Palestinian Red Crescent Society; Barraza et al., 2011). It appears
that OT may promote in-group CA, but may also support CA
across groups when there is a collective benefit available for
everyone.
Our lab has recently examined a different question: why do
naturally existing groups engage coordinated and costly ritualistic
behaviors? Human life is replete with rituals and we hypothe-
sized that rituals may induce the release of OT to reinforce group
attachment. In this project (Terris et al., in preparation) we exam-
ined OT release before and after rituals for several secular and
religious groups. Groups also made decisions in several economic
tasks, [trust game (TG), ultimatum game (UG), and dictator
game (DG)] by computer, with in-group and out-group mem-
bers. We found that OT significantly increased for some groups
after performing ritual (marching in unison, singing religious
songs), but not for others (Christian prayer). We also observed a
positive correlation between positive regard toward the in-group
after the ritual and how much one gave to one’s in-group relative
totheout-groupintheTGandDG,butnottheUG.Noasso-
ciation was observed between OT change induced by ritual and
prosocial behavior toward in- or out-groups. These results indi-
cate that although some rituals increase plasma OT, the increase
does not appear to influence in-group preferences. This work sug-
gests that OT can unite people to act as a group, but does not
necessarily injure out-group collaboration when there are shared
interests at stake.
TRUST IN POLITICAL INSTITUTIONS
Political actions, such as voting and campaigning, are another
form of CA. Our lab has explored how OT administration affected
trust in government officials and institutions during the 2007
Democratic and Republican primaries (Merolla et al., 2013). We
found that participants given 40IU intranasal OT reported more
agreement with the statement that most people can be trusted
than those on placebo, especially when examining those low on
pre-treatment interpersonal trust. Although OT did not directly
impact trust in the government, we found Democrats on OT were
more trusting of both Democrat and Republican politicians, and
the federal government in general, when compared to those on
placebo. When trust in government is higher, civic CA is likely to
follow.
Generalized trust at the national level affects trust between
individuals in the trust game (Holm and Danielson, 2005).
Generalized trust levels strongly predict rates of economic growth
in a cross-section of developed and less developed countries in
part by facilitating CA (Zak and Knack, 2001). Generalized trust
levels are also highly correlated with other forms of social capital
such as paying taxes and other civic norms (Knack and Keefer,
1997), and trust and self-reported rates of happiness are very
highly correlated at the country level (Zak and Fakhar, 2006)as
are happiness levels and some forms of CA (e.g., volunteering;
Post, 2005).
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Zak and Barraza The neurobiology of collective action
CONCLUSION
Most traditional evolutionary and economic models do not
attempt to provide proximate mechanisms to explain the wide
array of behaviors that are called CA. These models have caused
some behavioral scientists to erroneously conclude that costly
prosocial behaviors are “irrational” or manipulative, presuming
that individuals engaging in CA are hiding behind a “veneer”
covering their true selfish instincts (e.g., de Waal, 2006). We pre-
sented a neurobiologically-informed model of individually-costly
behaviors that benefit others. This model, with the hormone oxy-
tocin at its core, accounts for physiologic factors that are not
provided in extant models, particularly for the role of empathic
concern. It is also consistent with experiments we have run that
reveal substantial amounts of costly other-regarding behaviors,
even in blinded one-shot depersonalized settings.
Those unfamiliar with the existing body of research on oxy-
tocin may be left with the impression of OT as a purely prosocial
hormone. This is not the case. OT has been implicated with
behaviors that could be considered antisocial including ethno-
centrism (De Dreu et al., 2011), envy (Shamay-Tsoory et al.,
2009), and less adherence to fairness norms in certain contexts
(Radke and De Bruijn, 2012). Moreover, there are method-
ological concerns about oxytocin administration (Churchland
and Winkielman, 2012; Guastella et al., 2012), and peripheral
oxytocin measurement (McCullough et al., 2013). The state of
oxytocin research is still in it’s infancy. The Empathy-Collective
Action model seeks to take these disparate findings and provide
a game theoretic structure to understand how OT affects human
social behaviors.
The strength of our approach lies in integrating methodologies
and evidence across disciplines (Zak, 2004). More generally, our
research on the neuroeconomics of social behaviors has revealed
that empathic concern serves as an internal compass that can
result in CA (Zak, 2011). Adam Smith was right on target, fellow-
feeling does appear to be the basis for many moral behaviors and
CA. Research from our lab has simply identified a neurochemical
mechanism behind Smith’s intuition.
ACKNOWLEDGMENTS
We would like to thank the late Elinor Ostrom for valuable
comments on an earlier draft. We also like to thank all of our col-
leagues and research assistants who have collaborated with us on
many of the studies highlighted here.
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Conflict of Interest Statement: The authors declare that the research was con-
ducted in the absence of any commercial or financial relationships that could be
construed as a potential conflict of interest.
Received: 21 August 2013; accepted: 21 October 2013; published online: 19 November
2013.
Citation: Zak PJ and Barraza JA (2013) The neurobiology of collective action. Front.
Neuro sci. 7:211. doi: 10.3389/fnins.2013.00211
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