I have written about this in some previous posts (here, here, and here), in which I agreed with much of what Zak argues, but I also pointed out the weaknesses in the empirical evidence that he claims to support his position. I had to think more about this at the Liberty Fund conference on Sapolsky's Behave, because Zak was one of the discussants, and he criticized Sapolsky for saying that oxytocin has a "dark side"--"Oxytocin, the luv hormone, makes us more prosocial to Us and worse to everyone else. That's not generic prosociality. That's ethnocentrism and xenophobia" (Behave, 117). No, Zak insisted, there is no such "dark side" to oxytocin.
In the context of Zak's general argument, this debate over the neurophysiological influence of oxytocin on behavior raises a question about Smith's moral and economic philosophy: Does the Smithian liberalism of morals and markets require that human beings cooperate with one another indiscriminately and unconditionally as based on a universal humanitarian sympathy, or does in-group bonding and cooperation tend to promote aggressive protection of the in-group from perceived out-group threat?
Oxytocin (OT) is a nine-amino acid neuropeptide and peptide hormone that evolved among mammals to support the birth of offspring, maternal bonding and care of offspring, and sometimes monogamous mating of parents who jointly care for their offspring. In humans and some other animals, OT seems to be associated generally with emotional bonding, empathy, and trust. But the interaction of the OT system with other neurophysiological systems and with environmental circumstances is so complicated that it is hard to study, and there is no agreement among scientists as to exactly how and where it works in the brain. The Wikipedia article on OT is a good summary of the research and the controversies.
Zak was a coauthor of an influential paper published in 2005 in Nature entitled "Oxytocin Increases Trust in Humans." Their experiment was to have people play the "Trust Game." Two people are each given some amount of money, say $12. One person, designated the "investor," can either keep his money or transfer some of it to the person designated the "trustee." The money transferred is tripled. So if the trustee has received $8 from the investor, the trustee would then have $36. The trustee can then either keep all of his money or transfer some of it to the investor. The trustee who transfers some of his money shows trust in the trustee--trusting that the trustee will not selfishly refuse to share some of his gain. The trustee who does share some of his money shows his trustworthiness. Of course, this is designed to mimic the economic gains from trade in market exchanges. Zak and his colleagues showed that if some players of this game have OT sprayed into their noses before playing the game, and others have a placebo sprayed into their noses, those investors who have received OT will show more trusting behavior in transferring money, although trustees who have received OT do not show a statistically significant higher rate of back transfer than those in the placebo group.
Here's the abstract for their article:
"Trust pervades human societies. Trust is indispensable in friendship, love, families, and organizations, and plays a key role in economic exchange and politics. In the absence of trust among trading partners, market transactions break down. In the absence of trust in a country's institutions and leaders, political legitimacy breaks down. Much recent evidence indicates that trust contributes to economic, political, and social success. Little is known, however, about the biological basis of trust among humans. Here we show that intranasal administration of oxytocin, a neuropeptide that plays a key role in social attachment and affiliation in non-human animals, causes a substantial increase in trust among humans, thereby greatly increasing the benefits from social interactions. We also show that the effect of oxytocin on trust is not due to a general increase in the readiness to bear risks. On the contrary, oxytocin specifically affects an individual's willingness to accept social risks arising through interpersonal interactions. These results concur with animal research suggesting an essential role for oxytocin as a biological basis of prosocial approach behavior" (Kosfeld et al. 2005).Notice the extraordinary claim here--that the pervasive basis of all social bonding is the trust that can be elicited by oxytocin. The international publicity about this and later articles about the power of oxytocin for fostering trust, empathy, and affection stirred world-wide excitement about oxytocin as the "love hormone." People started buying spray bottles of oxytocin to intensify their love lives--oxytocin was linked to orgasms--to help close a business deal, or perhaps to spray up the noses of world leaders to secure world peace. It was said that when people hug, this creates a surge of oxytocin. So Zak gave popular lectures and interviews advising people to hug one another at least eight times a day to enjoy the benefits of oxytocin. He was soon called "Dr. Love." Zak's charming style is on display in a widely-viewed TED talk.
But then, this orgasmic excitement over oxytocin was deflated in two ways. First, beginning in 2010, Carsten de Dreu of the University of Amsterdam and his colleagues published a series of papers on oxytocin as promoting xenophobic--in/group versus out/group--behavior (de Dreu et al. 2010, 2011, 2012). Popular journalists reported this as the "dark side" of oxytocin that Zak and his colleagues had ignored.
The second deflating development in the study of OT, beginning around 2015, was a series of articles by scientists who pointed out that the scientific study of OT was so empirically and theoretically dubious that there was no scientific consensus on exactly when, where, and how OT acted in the brain; nor was their any agreement on the behavioral effects of OT (Nave, Camerer, and McCullough 2015; Shen 2015). There is very little evidence that intranasal OT crosses the blood-brain barrier and reaches its target tissues in the brain. Alternatively, researchers have shown correlations between OT-related brain processes and peripheral measures of OT in body fluids (blood plasma, saliva, or urine). Zak has relied on drawing blood and measuring levels of OT in the blood. But it is not clear that peripheral OT measures are reliable indicators of what OT is doing in the brain. Furthermore, the attempts to replicate the finding that OT is connected to trust have largely failed.
I asked Zak about whether there was any research to support his denial of de Dreu's showing of OT being associated with xenophobic Us/Them bias, or what has been called "parochial altruism"--being cooperative with members of one's own group but defensively competitive with those outside one's group. (I have written about the coevolution of parochial altruism and war here and here.) Zak responded by citing a recent article that he coauthored with his colleagues (Terris et al. 2018) with the title "Endogenous Oxytocin Release Eliminates In-Group Bias in Monetary Transfers with Perspective Taking."
Here's the abstract for the article:
"Oxytocin (OT) has been shown to facilitate trust, empathy, and other prosocial behaviors. At the same time, there is evidence that exogenous OT infusion may not result in prosocial behaviors in all contexts, increasing in-group biases in a number of studies. The current investigation seeks to resolve this inconsistency by examining if endogenous OT release is associated with in-group bias. We studied a large group of participants (N = 399) in existing groups and randomly formed groups. Participants provided two blood samples to measure the change in OT after a group salience task and then made computer-mediated monetary transfer decisions to in-group and out-group members. Our results show that participants with an increase in endogenous OT showed no bias in monetary offers in the ultimatum game (UG) to out-group members compared to in-groups. There was also no bias in accepting UG offers, though in-group bias persisted for a unilateral monetary transfer [in the dictator game (DG)]. Our analysis shows that the strength of identification with one's group diminished the effects that an increase in OT had on reducing bias, but bias only recurred when group identification reached 87% of its maximum value. Our results indicate that the endogenous OT system appears to reduce in-group bias in some contexts, particularly those that require perspective-taking [that is, in the UG but not in the DG]" (Terris et al. 2018, 1).Notice that while the title says that endogenous OT release "eliminates" in-group bias, this is not quite true, because the authors concede that strong group identification supports in-group bias even with an increase in OT. Notice also that they concede de Dreu's finding by saying that exogenous OT infusion can increase in-group biases in some contexts. In the article, they say that "studies using exogenous OT often pit an in-group against an out-group by asking people to make decisions that explicitly benefit their group," which shows "that exogenous OT increases the effect of primed group competition by intensifying a situational feature in the experiment" (Terris et al. 2018, 2).
One theory of how OT acts is that it increases the "social salience" of phenomena in the circumstances of action; and if an experiment creates "primed group competition," then increased OT can shine a spotlight on that context of group competition so as to stimulate an in-group bias. "Social salience is the likely cause of the so-called 'dark side' of OT, namely bias of one's preferences toward in-group members" (Terris et al. 2018, 2). So, they suggest, there really is a "dark side" to OT, at least in those circumstances where group-against-group competition is prominent.
But then, the authors admit that even in their experiment, where there was no "primed group competition," a high degree of group identification produced a bias towards one's in-group after a surge of OT (Terris et al. 2018, 6-7).
Recognizing this natural human propensity to in-group bias is compatible with Adam Smith's account of how the natural human desire for a mutual sympathy of sentiments supports morals and markets. Smith knows that we do not feel sympathy (or empathy or trust) indiscriminately and unconditionally for all of humanity. Rather, our sympathy is stronger for those close to us (our family, our friends, our fellow citizens) than for those far away, those outside our group. And so, whenever there is any competition between groups, we naturally favor our in-group over any out-group. Love of one's own is natural. In The Theory of Moral Sentiments, Smith writes:
"Every independent state is divided into many different orders and societies, each of which has its own particular powers, privileges, and immunities. Every individual is naturally more attached to his own particular order or society, than to any other. His own interest, his own vanity, the interest and vanity of many of his friends and companions, are commonly a good deal connected with it. He is ambitious to extend its privileges and immunities. He is zealous to defend them against the encroachments of ever other order or society" (VI.ii.7).This natural in-group bias is manifest in Smith's Wealth of Nations in his insistence that the first duty of government is military force to defend society against the violence and invasion of other societies (V.i).
Darwinian scientists can now explain this natural propensity to xenophobia and war as arising from the evolution of morality through group selection in war. Darwin himself saw this in The Descent of Man: "an advancement in the standard of morality will certainly give an immense advantage to one tribe over another. A tribe including many members who, from possessing in a high degree the spirit of patriotism, fidelity, obedience, courage, and sympathy, were always ready to aid one another, and to sacrifice themselves for the common good, would be victorious over most other tribes; and this would be natural selection" (2004, 157-58). Despite the continuing controversy over evolutionary group selection, many evolutionary scientists see evidence that Darwin was right about the evolutionary importance of group selection through war (Choi and Bowles 2007; Bowles and Gintis 2011). That's why I have included the natural desire for war as one of the 20 natural desires of our evolved human nature (Arnhart 1998).
If group selection has favored an evolved propensity for cooperating within one's group to compete with out-groups, then, de Dreu has argued, one might explain OT as part of a neurophysiological system to motivate a "tend and defend" response--trust and cooperation within the group and defensive aggression against competing out-groups. One might predict this from the fact that the ancient evolutionary roots of oxytocin are connected to not only the birth of offspring but also to the group-wide care and defense of offspring. Thus, de Dreu observes:
"findings here reveal that oxytocin-motivated non-cooperation is driven by the desire to protect vulnerable in-group members, even when immediate self-interest is not at stake. The male participates in our study behaved as the proverbial Mamma Bear who, while not being immediately in danger herself, lashes out against predators threatening her cubs. As predicted, such protective behavior emerged especially when participants received oxytocin rather than placebo" (De Dreu et al. 2012, 5).Remarkably, as already indicated, Zak and his colleagues don't dispute this claim, although they stress that this in-group biased behavior associated with OT arises only in the context of "primed group competition" or when group identification is strong.
It is also remarkable that Zak and his colleagues don't dispute the claim of Nave et al. (2015) and others that the research on the connection between OT and trust in humans has not been replicated. Ernst Fehr, who led the original Nature study published in 2005, has admitted: "What we're left with is a lack of evidence. I agree that we have no robust replications of our original study, and until then, we have to be cautious about the claim that oxytocin causes trust" (quoted in Yong 2015
The fundamental problem here is that the "neuroeconomics" research of Zak and others is too shallow to reveal exactly when, where, and how oxytocin modulates neural circuits in the brain to promote social cognition and social behavior. Spraying oxytocin into people's noses or measuring oxytocin in blood samples does not tell us what oxytocin is doing in the brain. For deeper research into the neural circuitry of oxytocin, we need to look to the research on oxytocin in the brains of non-human animals, such as Robert Froemke's studies of how oxytocin in the brains of female mice help them to care for and protect their pups (Marlin et al. 2015; Mitre et al. 2016; Valtcheva and Froemke 2019). But then combining this with research on humans to infer how oxytocin acts in human brains will be difficult. One way to do this is through neuroimaging studies of how OT works in live human brains (Ma et al. 2016).
PAUL ZAK'S RESPONSE
Paul Zak has sent me an email message about this post. He has allowed me to post this passage from his message:
"Here's the point I wanted to make: I've spent almost 20 years studying oxytocin and developed several protocols to do this that the scientific community uses. If a single paper of mine does not replicate, I am not concerned, because science works on consensus. The vast majority of my work has been replicated and extended by others. For example, as is typical in science (vs. economics), when I give seminars, I present 10 years or more of research showing a confluence of findings. Camerer et al. wrote one paper on oxytocin. This does not concern me."
REFERENCES
Arnhart, Larry. 1998. Darwinian Natural Right: The Biological Ethics of Human Nature. Albany: State University of New York Press.
Bowles, Samuel, and Herbert Gintis. 2011. The Cooperative Species: Human Reciprocity and Its Evolution. Princeton: Princeton University Press.
Choi, Jung-Kyoo, and Samuel Bowles. 2007. "The Coevolution of Parochial Altruism and War." Science 308 (October 26): 636-40.
Darwin, Charles. 2004. The Descent of Man. 2nd ed. New York: Penguin.
De Dreu, Carsten, et al. 2010. "The Neuropeptide Oxytocin Regulates Parochial Altruism in Intergroup Conflict Among Humans." Science 328 (11 June): 1408-1411.
De Dreu, Carsten, et al. 2011. "Oxytocin Promotes Human Ethnocentrism." Proceedings of the National Academy of Sciences 108 (January 25): 1262-1266.
De Dreu, Carsten, et al. 2012. "Oxytocin Motivates Non-Cooperation in Intergroup Conflict to Protect Vulnerable In-Group Members." PLOS ONE 7, issue 11 (November): e46751.
Kosfeld, Michael, et al. 2005. "Oxytocin Increases Trust in Humans." Nature 435 (2 June): 673-76.
Ma, Yina, Simone Shamay-Tsoory, Shihui Han, and Caroline F. Zink. 2016. "Oxytocin and Social Adaptation: Insights from Neuroimaging Studies of Healthy and Clinical Populations." Trends in Cognitive Sciences 20 (2): 133-45.
Marlin, Blanca, et al. 2015. "Oxytocin Enables Maternal Behaviour by Balancing Cortical Inhibition." Nature 520 (23 April): 499-504.
Mitre, Mariela, et al. 2016. "A Distributed Network for Social Cognition Enriched for Oxytocin Receptors." The Journal of Neuroscience 36 (8): 2517-2535.
Nave, Gideon, Colin Camerer, and Michael McCullough. 2015. "Does Oxytocin Increase Trust in Humans? A Critical Review of Research." Perspectives on Psychological Research 10 (6): 772-89.
Shen, Helen. 2015. "The Hard Science of Oxytocin." Nature 522 (25 June): 410-12.
Terris, Elizabeth, et al. 2018. "Endogenous Oxytocin Release Eliminates In-Group Bias in Monetary Transfers With Perspective Taking." Frontiers in Behavioral Neuroscience 12 (March): article 35.
Valtcheva, Silvana, and Robert C. Froemke. 2019. "Neuromodulation of Maternal Circuits by Oxytocin." Cell and Tissue Research 375: 57-68.
Yong, Ed. 2015. "The Weak Science Behind the Wrongly Named Moral Molecule." The Atlantic, November 13.
Zak, Paul. 2012. The Moral Molecule: The Source of Love and Prosperity. New York: Dutton.
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