Oxytocin and cooperation under conditions of uncertainty: The modulating role of incentives and social information

doi:10.1016/j.yhbeh.2010.01.006

Hormones and Behavior

Volume 57, Issue 3, March 2010, Pages 368-374

https://doi.org/10.1016/j.yhbeh.2010.01.006 Get rights and content

Abstract

The neuropeptide Oxytocin (OT) has been implicated in many aspects of mammalian social behavior. This study investigates how OT interacts with two well-studied determinants of cooperative behavior: incentives and social information. Participants received OT or a placebo and played two economic games: a Coordination Game (with strong incentives to cooperate) and a Prisoner's Dilemma (with weak cooperative incentives). OT enhanced cooperation only when social information was present, and this effect was significantly more pronounced in the Coordination Game. When social information was lacking, OT surprisingly decreased cooperation. Consistent with the well-established role of OT in trust-building and in social cognition, social information appears to be crucial for OT to boost cooperative expectations in an interdependent social interaction that provides incentives to cooperate. When these cues are absent, OT appears to instead elicit a risk-averse strategy.

Section snippets

Participants and design

The experiment was conducted at the University of Antwerp during the spring of 2008. Participants consisted of 259 students (119 males, 140 females, average age = 20.2 years, s.d. = 2.4). They were recruited from different departments via e-mail and signed up for one of 8 sessions (with a minimum of 30 and a maximum of 36 participants per session). Exclusion criteria for participating included any medical or psychiatric illness, pregnancy, substance abuse, smoking more than 15 cigarettes per day,

Results

The main effects of the independent variables on cooperative decision-making are as follows. As expected, there is more cooperation in the CG (58.9 %) than in the PD (29.3 %), and this difference is significant (χ² = 45.25, p < 0.001, N = 259). The social condition has a marginally significant effect on cooperative decisions (χ² = 3.34, p < 0.068, N = 518), with 48.0 % cooperation in the prior contact condition, and 40.1 % in the anonymous partner condition. Finally, there is no difference in cooperative

Discussion and conclusion

A major conclusion that can be drawn from this experiment is that the role of OT in regulating social behavior can be extended to the domain of human cooperation. However, the results of this study indicate that OT's role in stimulating cooperative behavior is critically dependent on the presence of social information (here, in the form of prior contact) and extrinsic cooperative incentives. When strong incentives are present (in the CG), people are generally willing to cooperate when they

Acknowledgments

This research was funded by an NOI grant (1044) from the University of Antwerp. We thank the following graduate students of the department of Management at the University of Antwerp for supervising experiments: Liesbeth Adriaenssens, Sandy Bogaert, Tine Buyl, Griet Emonds, Linda Mertens, Jesse Segers, Kim Sluyts, and Johanna Vanderstraeten.

References (41)

BaumgartnerT. et al.
Oxytocin shapes the neural circuitry of trust and trust adaptation in humans
Neuron
(2008)
BooneC. et al.
Subtle social cues, explicit incentives, and cooperation in social dilemmas
Evol. Hum. Behav.
(2008)
CampbellA.
Attachment, aggression and affiliation: the role of oxytocin in female social behavior
Biol. Psychol.
(2008)
DecetyJ. et al.
The neural bases of cooperation and competition: an fMRI investigation
NeuroImage
(2004)
DomesG. et al.
Oxytocin improves “mindreading” in humans
Biol. Psychiatry
(2007)
GuastellaA.J. et al.
Oxytocin increases gaze to the eye region of the human face
Biol. Psychiatry
(2008)
GuastellaA.J. et al.
Oxytocin enhances the encoding of positive social memories in humans
Biol. Psychiatry
(2008)
GuastellaA.J. et al.
Does oxytocin influence the early detection of angry and happy faces?
Psychoneuroendocrinology
(2009)
HaleyK.J. et al.
Nobody's watching? Subtle cues affect generosity in anonymous economic games
Evol. Human Behav.
(2005)
HaxbyJ.V. et al.
The distributed neural system for face perception
Trends Cogn. Sci.
(2000)

HeinrichsM. et al.

Social support and oxytocin interact to suppress cortisol and subjective responses to psychosocial stress

Biol. Psychiatry

(2003)

HeinrichsM. et al.

Selective amnesic effects of oxytocin on human memory

Physiol. Behav.

(2004)

HollanderE. et al.

Oxytocin increases retention of social cognition in autism

Biol. Psychiatry

(2007)

LengG. et al.

Oxytocin and the maternal brain

Curr. Opin. Pharmacol.

(2008)

LiebrandW.B.G. et al.

Might over morality: social values and the perception of other players in experimental games

J. Exp. Soc. Psychol.

(1986)

RillingJ.K. et al.

A neural basis for social cooperation

Neuron

(2002)

RillingJ.K. et al.

The neural correlates of theory of mind within interpersonal interactions

NeuroImage

(2004)

YoungK.A. et al.

The neurobiology of social attachment: a comparative approach to behavioral, neuroanatomical, and neurochemical studies

Comp. Biochem. Physiol., Part C

(2008)

BarrettH.C. et al.

Modularity in cognition: framing the debate

Psychol. Rev.

(2006)

BartzJ.A. et al.

The neuroscience of affiliation: forging links between basic and clinical research on neuropeptides and social behavior

Horm. Behav.

(2006)

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Citation Excerpt :
This points out that the observed laughing behavior merely functioned as an implicit social signal, thereby reducing social distance (Graham, 1995) and promoting interpersonal outcomes such as closeness and attraction (Campbell et al., 2008; Treger et al., 2013). Comparable to findings that OT promotes explicit interpersonal interactions like cooperation when interacting with ingroup members (Declerck et al., 2010; De Dreu et al., 2010), OT thus also facilitates implicit interpersonal interactions under such conditions, as in our study, in the form of humor. Based on our findings, one may wonder why laughing and smiling took two video segments to emerge.
Oxytocin (OT) is known for facilitating interpersonal interactions in favorable conditions. Humor, on the other hand, is an interpersonal phenomenon that reduces social distance. In this study, we investigated whether OT would increase laughing and smiling in a favorable environment. Therefore, participants were asked to view a brief video clip of a comedy television program in the presence of an ingroup member after administration of either OT or a placebo. Results demonstrated that participants in the OT condition exhibited more laughing and smiling behavior over the course of viewing the video compared to participants in the placebo condition. OT, however, neither affected self-reported affect nor perceived funniness of the clip. These findings indicate that OT, a hormone that can bolster attachment, also has the power to facilitate implicit social interactions by promoting visible and audible social signals, but does not affect the socially irrelevant inner cheerfulness.

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Oxytocin and cooperation under conditions of uncertainty: The modulating role of incentives and social information

Abstract

Section snippets

Participants and design

Results

Discussion and conclusion

Acknowledgments

Neuron

Evol. Hum. Behav.

Biol. Psychol.

NeuroImage

Biol. Psychiatry

Biol. Psychiatry

Biol. Psychiatry

Psychoneuroendocrinology

Evol. Human Behav.

Trends Cogn. Sci.

Biol. Psychiatry

Physiol. Behav.

Biol. Psychiatry

Curr. Opin. Pharmacol.

J. Exp. Soc. Psychol.

Neuron

NeuroImage

Comp. Biochem. Physiol., Part C

Modularity in cognition: framing the debate

Psychol. Rev.

The neuroscience of affiliation: forging links between basic and clinical research on neuropeptides and social behavior

Horm. Behav.