Interactive Effects Between Extraversion and Oxytocin Administration

Abstract

Intranasal administration of the neuropeptide oxytocin (OT) appears to have positive social consequences, but these effects are often highly context- and person-specific. The present research examined whether the core personality trait of extraversion may be one important person-specific factor that plays a role in these associations. Across two double-blind randomized placebo-controlled studies (total ns: Study 1 = 121; Study 2 = 112), we observed significant interactions between OT administration and extraversion predicting prosocial outcomes. For individuals low in extraversion, OT administration relative to placebo led to greater perceived social connection and prosocial tendencies (Study 1) and more positive behavioral responses to help and greater trust of an interaction partner (Study 2). In contrast, OT administration was not beneficial for individuals high in extraversion. Overall, these findings contribute to growing evidence that OT administration has complex, person-specific effects on social behavior, indicating that extraversion plays an important role in these associations.

Keywords

oxytocin administration extraversion social outcomes prosocial behavior

The hypothalamic neuropeptide oxytocin (OT) is argued to play an important role in social bonding and affiliation (Bartz & Hollander, 2006; Taylor et al., 2000), in turn facilitating positive social behavior. For example, OT administration has been linked to greater trust (Kosfeld, Heinrichs, Zak, Fischbacher, & Fehr, 2005; Mikolajczak, Gross, et al., 2010; Mikolajczak, Pinon, Lane, de Timary, & Luminet, 2010), generosity (Riem, Bakermans-Kranenburg, Huffmeijer, & van Ijzendoorn, 2013; van Ijzendoorn, Huffmeijer, Alink, & Bakermans-Kranenburg, 2011; Zak, Stanton, & Ahmadi, 2007), and positive social perceptions (Cardoso, Orlando, Brown, & Ellenbogen, 2014; Di Simplicio, Massey-Chase, Cowen, & Harmer, 2009; Marsh, Yu, Pine, & Blair, 2010; Unkelbach, Guastella, & Forgas, 2008). Yet, the relationship between OT and social behavior is rarely straightforward, with OT administration sometimes demonstrating no effect on prosocial behavior (e.g., Baumgartner, Heinrichs, Vonlanthen, Fischbacher, & Fehr, 2008; Conlisk, 2011; Klackl, Pfundmair, Agroskin, & Jonas, 2013; see Nave, Camerer, & McCullough, 2015, for critical review) or even having negative effects (e.g., Bartz, Simeon, et al., 2011; De Dreu et al., 2010; Shamay-Tsoory et al., 2009). This may be due in part to the highly context-specific and person-specific effects of OT administration (Bakermans-Kranenburg & van Ijzendoorn, 2013; Bartz, Zaki, Bolger, & Ochsner, 2011; Guastella & MacLeod, 2012; van Ijzendoorn & Bakermans-Kranenburg, 2012).

One factor that may help to explain the apparently inconsistent effects of OT administration is affiliative motivation, a tendency to desire, approach, and foster social bonds and attachments. Specifically, OT administration may be selectively beneficial for those who are lower in social engagement or affiliative tendencies (see Bartz & Hollander, 2006; Bartz, Zaki, et al., 2011, for reviews). For example, OT administration has social benefits for those higher in avoidant attachment (Bartz et al., 2015; De Dreu, 2012) and on the autism spectrum (Bartz et al., 2010; Domes, Heinrichs, Michel, Berger, & Herpertz, 2007; Guastella et al., 2010). Thus, underlying levels of affiliative motivations may play a key role in determining whether OT administration is beneficial for social processes. One central trait that is linked to affiliative motivations and that has not yet been explored in the context of OT administration is the personality trait extraversion.

Extraversion involves greater sociability, dominance, excitement seeking, and positive affect. Underlying these somewhat distinct features of extraversion appears to be a heightened reward sensitivity and motivation toward pleasant stimuli (Lucas, Diener, Grob, Suh, & Shao, 2000), which may engender greater social engagement and affiliative motivations (Costa & MacCrae, 1992; Depue & Collins, 1999; Watson & Clark, 1997). In turn, extraversion relates to positive social behavior and outcomes (see Ozer & Benet-Martinez, 2006, for review). For example, high levels of extraversion predict greater prosocial behavior, such as helpfulness (Penner, 2002) and volunteerism (Carlo, Okun, Knight, & de Guzman, 2005), and positive social outcomes, such as social support (Berkman, Glass, Brissette, & Seeman, 2000), acceptance (Anderson, John, Keltner, & Kring, 2001), and relationship satisfaction (Watson, Hubbard, & Wiese, 2000).

Given links with affiliative motivations and positive social outcomes, extraversion is therefore a key person-specific characteristic that may influence the associations between OT administration and social processes. In particular, if lower extraversion is related to lower affiliative motivations, then OT administration is likely to be more beneficial for individuals low in extraversion. Indeed, OT administration can enhance self-perceptions of extraversion and affiliation-relevant traits, such as warmth, trust, altruism (Cardoso, Ellenbogen, & Linnen, 2012), and communion (Bartz et al., 2015). Increases in affiliative motivations are in turn likely to carry positive social consequences for those lower in extraversion—even though individuals lower in extraversion tend to experience fewer social interactions, they benefit from them to a similar extent as those high in extraversion (Lucas, Le, & Dyrenforth, 2008). In contrast, if individuals high in extraversion already experience high affiliative motivations, then OT administration is less likely to be socially beneficial.

To test these possibilities, we examined data from two randomized, double-blind, placebo-controlled studies where participants reported their levels of extraversion and received a single dose of intranasal OT (40 IU) or a placebo, prior to the assessment of several positive social outcomes. In Study 1, positive social outcomes included perceived social connection to others in general and prosocial tendencies toward several charitable organizations. Study 2 examined actual social behavior toward an interaction partner, including positive behavior in response to receiving help and interpersonal trust. We predicted that while OT administration may promote positive social consequences for those lower in extraversion, it would be less socially beneficial for those higher in extraversion.

Method

Participants and Design

The data for the current studies come from two larger studies that involved additional manipulations and measures; details and additional analyses are provided in the Supplemental Online Materials (SOM) and other manuscripts (Human, Thorson, Woolley, & Mendes, 2015; Human, Woolley, & Mendes, 2015). Both studies share a similar general paradigm, and therefore, the methods and results are presented together. In both studies, participants between the ages of 18 and 35 who spoke English as their first language were recruited from the San Francisco/Bay Area community. Prior to scheduling a lab appointment, participants were prescreened and excluded if they were pregnant, lactating, or self-reported poor mental or physical health. Once scheduled, participants were sent a personality questionnaire to complete online prior to their lab visit. Sample size was determined a priori based on published between-subjects studies examining interactive effects of OT and individual differences, which typically report between 60–80 participants (e.g., De Dreu, 2012). Because there is reason to believe that past studies were underpowered (Cohen, 1962; Vankov, Bowers, & Munafo, 2014), we aimed to collect larger samples of roughly 120 participants per study, in an effort to balance power and cost/feasibility concerns (studies were run sequentially over 2 years each). For Study 1, a total of 121 participants completed the online questionnaire as well as the lab visit (64 female, 57 male; M_age = 25.01, SD_age = 4.01); for Study 2, a total of 112 participants completed the online questionnaire as well as the lab visit (67 female, 45 male; M_age = 24.27, SD_age = 3.62). No cases with full data were excluded, but there were additional missing data on the individual social outcome measures; sample sizes for each analysis are reported below.

Procedure

Personality assessment

Prior to arrival at the lab, participants rated their personality traits in an online survey. Extraversion was assessed on the extraversion subscale of the Big Five Mini Markers (Saucier, 1994), which includes the following items: bashful (reversed), bold, energetic, extraverted, quiet (reversed), shy (reversed), talkative, and withdrawn (reversed; Study 1: M = 5.67, SD = 1.35, α = .83; Study 2: M = 5.82, SD = 1.46, α = .89). Each item was rated on a 1 (extremely inaccurate)–9 (extremely accurate) scale.¹

Arrival and nasal spray administration

Upon arrival at the lab, participants were given a brief overview of the procedure, and a trained experimenter obtained informed consent. The experimenter then confirmed a negative test for pregnancy for all female participants via a urine sample. Participants were randomly assigned to the placebo versus OT administration condition and were instructed how to administer the nasal spray. The spray bottles were indistinguishable other than a colored dot on the bottom of the bottle; no one who interacted with the participants knew which color indicated OT/placebo. The spray contained either 40 IU of OT (Syntocinon spray, Novartis, Switzerland) or a placebo (same compounds as Syntocinon minus OT). In line with recommendations by Guastella et al. (2013), participants utilized a metered multidose pump spray bottle, with each spray containing no more than 100 μL and alternated nostrils until the bottle was empty (approximately 3 puffs per nostril). Participants self-administered the spray in the presence of an MD-trained research assistant.

Intranasal administration has been shown to lead to significant increases in cerebrospinal fluid OT levels in humans as measured by lumbar puncture (Striepens et al., 2013), although it was only detectable 75 min after administration, and there is controversy surrounding the nature and the mechanisms of the effects of OT administration on the brain (Leng & Ludwig, 2016). Other experimental work with intranasal OT in humans has consistently utilized an absorption period ranging between 40 and 50 min (Heinrichs, Baumgartner, Kirschbaum, & Ehlert, 2003; Kosfeld et al., 2005; Shamay-Tsoory et al., 2009); we therefore assessed social outcomes at least 40 min postadministration. During the waiting period, participants watched a neutral video about hiking the Appalachian Trail.

Social Outcomes: Study 1

Social connection

A total of 117 participants (placebo = 57; OT = 60) completed a measure assessing how close participants felt to others with the Inclusion of Other in Self scale (Aron, Aron, & Smollan, 1992). In this version, participants selected a single picture that best described the closeness of two groups, “me” and “other people,” on a 1 (complete separation)–7 (almost complete overlap) scale (M = 4.12; SD = 1.45).

Prosocial tendencies

A total of 114 participants (placebo = 56; OT = 58) completed a measure assessing prosocial tendencies with a questionnaire we developed and pilot tested prior to the study, which assessed participants’ support for a variety of organizations seeking help. Participants were told:

As part of the UC system, many research labs at UCSF partner with local charities. Every week, UCSF receives information about charities interested in finding volunteers. On the computer screen, you’ll be able to learn about organizations currently seeking help, and then UCSF would like you to indicate your interest in helping them by clicking your answer choice.

Participants were told their contact information would not be shared with the organizations but that their responses would be useful to nonprofit groups as they try to gauge the public’s interest in their missions.

Participants then viewed one of two sets of three organizations (versions were equated in pilot testing). In each set, one organization was depicted as helping the environment (e.g., help in picking up trash or coordinating recycling drives), one as helping animals (e.g., assistance for care with abandoned animals or ending animal testing), and, the key category of interest, one as helping people (e.g., seeking tutors or mentors for young children). Each description was paired with a relevant image (see Supplemental Appendix online). All effects held controlling for version.

For each organization, participants responded to the following questions on a 1 (not at all)–9 (very) scale: “How interested are you in helping this organization,” “How important is it to you that this organization is funded by state and federal taxes,” and “How important is this organization to you?” Responses were combined together to assess overall support for each organization (environment: M = 6.49, SD = 1.85, α = .86; animals: M = 6.18, SD = 2.20, α = .89; children: M = 7.02, SD = 1.78, α = .87). Given that OT administration and extraversion are arguably most relevant to prosociality, our primary outcome was support for the organization involving children, which was most directly social in nature, while support for animals and the environment was examined to determine the specificity of effects.

Support for each organization type was highly correlated (rs = .54–.60, all ps < .001). Perceived social connection was not significantly correlated with prosocial tendencies toward children (r = .11, p = .23) or animals (r = .10, p = .30) but was with support for environmental causes (r = .20, p = .04).

Social Outcomes: Study 2

Positive behavior

Study 2 extended Study 1 by examining actual social behaviors with another person. Specifically, participants were exposed to a help manipulation, derived from DeSteno and colleagues (Bartlett & DeSteno, 2006; DeSteno, Bartlett, Baumann, Williams, & Dickens, 2010). In our version of this paradigm, participants engaged in three trials of a tedious computer task. Right at the end of the third trial, the computer ostensibly crashed. Participants were led to believe that they would therefore have to redo the task from the start. However, the computer was then “fixed” (in one condition by a technician who gives instructions to the experimenter and in another by a confederate—a research assistant that the participant believed was another participant, who was of the same gender and roughly the same age and ethnicity), providing the opportunity to assess participant social behavior in response to receiving help from another person. The provider of help (technician/experimenter vs. confederate) did not impact the results presented here (see SOM for additional information on this manipulation and other aspects of this study); as such, we examined social behavior in response to help on average across help provider conditions.

Specifically, the computer crash and subsequent fix were video-recorded, and three observers (trained research assistants), unaware of OT condition and not involved in data collection, coded participants’ social behaviors in response to help. Video-recording of this interaction was included partway through data collection (n = 69), and two of these participants did not complete the extraversion measure, resulting in 67 videos available for analyses (placebo = 37; OT = 30). Observers rated participant affective and social behavior on a 1 (not at all)–5 (a great deal) scale on the following items: grateful (M = 2.22; SD = 1.27), happy (M = 2.51; SD = 1.32), amused (M = 1.29; SD = .62), and friendly (M = 3.20; SD = 1.05). Roughly 20% of the video clips were double-coded (n = 20) and intraclass correlation coefficients were acceptable (M = .76). These ratings were combined together to form an overall composite indicator of positive behavioral responses to help (M = 2.30; SD = .86; α = .79).

Trust task

Participants then engaged in two cooperative tasks with the confederate (see SOM for details). These tasks involved the ability to earn money for correct responses. At the end of the tasks, the participant and the confederate were brought into different rooms, and participants were informed that they and the confederate each earned USD$11 for their performance. Participants were then presented with a “common goods” task designed to assess interpersonal trust. Specifically, participants were told that both they and the confederate would separately decide how much of the USD$11 they would like to put in a common pot (they were not able to communicate with one another about this task). They were told that the total amount placed in the pot by the participant and partner would be multiplied by 1.5 and the total pot would be divided equally between the participant and the confederate. Participants were provided with a list of all possible payouts that could occur based on the participant’s and confederate’s contributions in order to ensure understanding of possible task outcomes. Variations in this task are used extensively to measure trust because the more a participant puts in the pot, the more they can earn, but only if their partner also puts a large amount in the common pot; if not, they stand to earn less than the original amount. Thus, sharing a large amount of money requires trust that one’s partner will do the same.

A total of 110 participants (placebo = 58; OT = 52) provided both extraversion and trust task data. On average, participants tended to place the majority of the money in the shared pot (M = 9.34; SD = 2.78); indeed, 77 (68%) participants shared the full amount, making this variable negatively skewed (skew = −1.44). We therefore log-transformed the reflected variable and then returned it to its original direction of scoring so that higher values represent placing more money in the common pot. Positive behavior in response to help and interpersonal trust were not significantly correlated (r = .10, p = .43).

Results

The effects of extraversion and OT administration were examined with a series of regressions with OT administration (0 = placebo; 1 = OT administration), extraversion (centered), and their interaction as predictors of each social outcome (see Table 1). There were no main effects of OT administration on the social outcomes examined here (all ps > .17), but there were main effects of extraversion on social connection and trust (all ps < .05). However, these main effects were qualified by significant interactions with OT administration, described below.

Table 1.

Full Regression Models With Extraversion, Oxytocin Condition, and Their Interaction Predicting Each Social Outcome.

Predictor	Extraversion				OT condition				Interaction
Predictor	b (SE)	β	95% CI [Upper, Lower]	t	b (SE)	β	95% CI [Upper, Lower]	t	b (SE)	β	95%CI[Upper, Lower]	t
Study 1
Social Connection	.57 (.13)	.52***	[.28, .77]	4.21	.04 (.25)	.03	[−.31, .37]	.17	−.41 (.19)	−.38*	[−.73, −.04]	−2.19
Volunteer
Children	.44 (.18)	.34*	[.07, .61]	2.46	.50 (.32)	.29	[−.07, .65]	1.56	−.76 (.26)	−.59**	[−.97, −.19]	−2.96
Animals	.51 (.23)	.31*	[.04, .59]	2.28	.35 (.41)	.16	[−.21, .53]	1.47	−.43 (.32)	−.26	[−.65, .13]	−1.33
Environment	.20 (.19)	.14	[−.13, .42]	1.03	.51 (.35)	.28	[−.09, .65]	1.48	−.02 (.27)	−.02	[−.41, .38]	−.09
Study 2
Response to help	.13 (.10)	.21	[−.11, .54]	1.31	.21 (.20)	.27	[−.20, .28]	1.06	−.35 (.14)	−.59*	[−1.06, −.11]	−2.45
Trust	.02 (.07)	.03	[−.21, .26]	.23	.15 (.16)	.19	[−.18, .55]	.98	−.30 (.11)	−.51**	[−.88, .14]	−2.75

Note. OT condition scored such that 0 = placebo and 1 = oxytocin. OT = oxytocin.

*p < .05. **p < .01. ***p < .001.

Study 1

Social Connection

We observed a significant interaction between OT administration and extraversion predicting ratings of social connection, b = −.41, t(113) = −2.19, p = .03. Specifically, within the placebo condition, extraversion was associated with significantly greater social connection to other people in general, b = .57, β = .52, 95% CI [.28, .77], t(113) = 4.21, p < .001. However, extraversion and social connection were not significantly related among participants who received OT administration, b = .15, β = .14, 95% CI [−.10, .39], t(113) = 1.18, p = .24 (see Figure 1).

Figure 1.

Relationship between trait levels of extraversion and social connection (inclusion of others in self) as a function of oxytocin versus placebo administration.

To further understand the nature of this interaction, we examined the effect of OT administration for those who reported low (1 SD below the mean) and high (1 SD above the mean) levels of extraversion. For individuals low in extraversion, receiving OT administration was associated with marginally greater levels of perceived social connection relative to those who received placebo, b = .60, d = .41, 95% CI [.04, .77], t(113) = 1.65, p = .10. In contrast, for those high in extraversion, receiving OT administration was not significantly associated with social connection relative to those who received placebo, b = −.51, d = −.35, 95% CI [−.71, .02], t(113) = −1.46, p = .15.

Prosocial Tendencies

We next examined interactive effects on support for charitable organizations, examining each type of organization separately to examine the specificity of the effects.² Looking first at organizations supporting children, we again observed a significant interaction between OT/placebo and extraversion predicting charitable support, b = −.76, t(110) = −2.96, p = .004. Similar to the pattern with social connection, in the placebo condition, greater extraversion was associated with greater support for children organizations, b = .44, β = .34, 95% CI [.07, .61], t(110) = 2.46, p = .02. However, in the OT administration condition, greater extraversion was associated with marginally lower support for children organizations, b = −.32, β = −.25, 95% CI [−.52, .03], t(110) = −1.74, p = .09 (see Figure 2).

Figure 2.

Relationship between trait levels of extraversion and support for organizations involving children as a function of oxytocin versus placebo administration.

Examining the effects at high versus low levels of extraversion revealed that, for those low in extraversion, OT administration was associated with significantly greater support for these organizations, relative to those who received placebo, b = 1.53, d = .87, 95% CI [.48, 1.25], t(110) = 3.12, p = .002. In contrast, for those high in extraversion, OT administration was not significantly associated with support for these organizations relative to placebo, b = −.52, d = –.30, 95% CI [−.66, .07], t(110) = –1.14, p = .26.

Of note, although there was a significant main effect of extraversion predicting greater support for animal organizations, b = .51, β = .69, 95% CI [.09, 1.29], t(110) = 2.28, p = .02, we did not observe significant interactions between extraversion and OT administration predicting support for animal organizations, b = −.43, t(110) = −1.33, p = .19, or environmental organizations, b = −.02, t(110) = −.09, p = .93.

Study 2

Positive Responses to Help

We next examined effects on positive social behavior in response to receiving help. As above, we observed a significant interaction between extraversion and OT administration, b = −.35, t(63) = −2.45, p = .02. In the placebo condition, extraversion was not significantly associated with more positive behavioral responses to help, b = .13, β = .21, 95% CI [−.11, .54], t(63) = 1.31, p = .19. However, in the OT administration condition, extraversion was significantly negatively associated with positive responses to help, b = −.22, β = −.37, 95% CI [−.72, −.02], t(63) = −2.12, p = .04 (see Figure 3).

Figure 3.

Relationship between trait levels of extraversion and positive social behavior as a function of oxytocin versus placebo administration.

Examining the effect for individuals low and high in extraversion demonstrated that OT administration was associated with significantly more positive social behavior in response to receiving help for those low in extraversion, b = .72, d = .83, 95% CI [.32, 1.33], t(63) = 2.50, p = .02, but not for those high in extraversion, b = −.30, d = −.34, 95% CI [−.82, .15], t(63) = −1.01, p = .31.

Trust

Finally, we examined the interactive effects on trust toward a social interaction partner (the confederate), indexed by the amount of money put in the common pot, log-transformed. Once again, we observed a significant interaction, b = −.30, t(106) = −2.75, p = .007. In the placebo condition, extraversion was not significantly associated with greater trust, b = .02, β = .03, 95% CI [−.21, .26], t(106) = .23, p = .82. However, in the OT administration condition, greater extraversion was associated with significantly lower trust, b = −.28, β = −.48, 95% CI [−.77, −.20], t(106) = −3.38, p = .001 (see Figure 4).

Figure 4.

Relationship between trait levels of extraversion and trust as a function of oxytocin versus placebo administration. Data are slightly jittered (randomly perturbed) to minimize overplotting.

Examining this effect as a function of low versus high extraversion revealed that receiving OT administration versus placebo was associated with exhibiting significantly greater trust for those low in extraversion, b = .59, d = .69, 95% CI [.31, 1.08], z = 2.66, p = .009. In contrast, for those high in extraversion, OT administration versus placebo was not significantly associated with trust, b = −.28, d = −.33, 95% CI [−.71, .05], z = −1.25, p = .21. Thus, for individuals low in extraversion, receiving OT administration enhanced the likelihood of putting more money in the common pot, indicating greater trust that their partner would do the same.

General Discussion

Although OT is argued to have the potential to benefit social behavior, its effects tend to be highly context-specific and person-specific (Bakermans-Kranenburg & van Ijzendoorn, 2013; Bartz, Zaki, et al., 2011; Guastella & MacLeod, 2012; van Ijzendoorn & Bakermans-Kranenburg, 2012). The current studies contribute to this literature by demonstrating that a core personality trait, extraversion, plays a role in these associations. Specifically, across two studies with a total of 233 participants, OT administration relative to placebo had selectively beneficial effects for individuals lower in extraversion. These effects were found across four conceptually related yet distinct social outcomes, including greater social connection, prosocial tendencies, positive behavioral responses to help, and interpersonal trust. In contrast, OT administration had less social benefit for individuals high in extraversion.

The finding that OT administration was related to greater positive social experiences is consistent with a large body of prior work demonstrating social benefits of OT administration for processes such as trust (Kosfield et al., 2005; Mikolajczak, Gross, et al., 2010; Mikolajczak, Pinon, et al., 2010), generosity (Riem et al., 2013; van Ijzendoorn et al., 2011; Zak et al., 2007), and positive social perceptions (Cardoso, Orlando, et al., 2014; Di Simplicio et al., 2009; Marsh et al., 2010; Unkelbach et al., 2008). Yet these findings also contribute to the growing recognition that the effects of OT administration are nuanced and often selectively beneficial, in this case for those lower levels in extraversion. Indeed, we did not observe any significant main effects of OT on social outcomes. Given the benefits of prosocial behavior and positive social experiences for well-being and health (e.g., Deci, La Guardia, Moller, Scheiner, & Ryan, 2006; Hawkley & Cacioppo, 2010; Thomas, 2010), acute increases in OT may therefore be beneficial for individuals who are less extraverted.

One reason that OT administration may selectively benefit social outcomes for those lower in extraversion may be via enhanced affiliative motivations (Bartz & Hollander, 2006; Bartz, Zaki, et al., 2011). That is, OT administration may have boosted affiliative motivations for those lower in extraversion, making them more likely to view the world and behave in ways that would foster social bonds—to generalized others in Study 1 and specific interaction partners in Study 2. This is consistent with findings that those higher in avoidant attachment (Bartz et al., 2015; De Dreu, 2012) or on the autism spectrum (Bartz et al., 2010) demonstrate greater social benefit from OT administration than those lower on these dimensions—effects that also may be driven, at least partly, by affiliative motivations. Although affiliative motivations and attachment style were not directly assessed in the current studies, taken together, these findings lend support to affiliation as a key mechanistic process that underlies a range of person-specific effects of OT administration. Indeed, extraversion and avoidant attachment style are inversely related (Carver, 1997), making it possible these effects are driven by the same underlying mechanism. Additional research directly examining how these broader person-specific characteristics relate to one another and to the proposed mechanistic process of affiliation, ideally within the same studies and with large samples, is needed.

It is also plausible that OT administration enhanced positive social perceptions and behavior for those low in extraversion because of the more general anxiety-reducing effects of OT administration (Churchland & Winkielman, 2012; Neumann, 2008; Uvnäs-Moberg, 1998), which may have dampened anxieties about one’s existing relationships or possible future behaviors in Study 1 and the immediate social interactions in Study 2. However, our finding that OT administration enhanced prosocial tendencies for explicitly social causes, rather than those supporting animals and the environment, suggests a social specificity more consistent with an affiliation explanation. Understanding the mechanisms underlying these effects is critical, as this will shed light both on the complex role of OT administration in social processes and on the psychological and neurobiological underpinnings of extraversion.

In contrast to the positive effects of OT administration for those low in extraversion, OT administration had less benefit for individuals high in extraversion. It is possible, however, that OT administration is socially beneficial for those higher in extraversion but that there were ceiling effects making it difficult to detect increases. However, if any effect of OT administration was detected for those higher in extraversion, it actually appeared to be negative: For three of the four outcomes, the association between extraversion and positive social processes was marginally or significantly negative in the OT administration condition. That is, while in the placebo condition extraversion was either positively or not significantly related to positive social processes, within the OT administration condition, higher extraversion was actually associated with less positive social processes than lower extraversion. These findings are in line with other evidence that OT administration can have negative consequences for individuals who may be higher in affiliative motivations or social engagement. For example, there are indications that OT administration can decrease perceived cooperation and trust for those low in avoidant attachment (De Dreu, 2012). Further, OT administration has been shown to hinder social perception accuracy for normative individuals, arguably by pushing such individuals past beneficial levels of social sensitivity to a more detrimental point (Cardoso, Ellenbogen, & Linnen, 2014). Similarly, then, perhaps OT administration may push individuals who are already high in affiliative tendencies, such as extraverts, past beneficial levels of affiliation, resulting in less positive social responses. Such an argument is in line with other indications that it may be possible for levels of social engagement or affiliation to increase beyond an optimal level, resulting in negative outcomes for relationships and well-being (e.g., Clark & Lemay, 2010; Kogan, Gruber, Shallcross, Ford, & Mauss, 2013; Kogan et al., 2014). It will be important for future research to continue to examine the potential downsides of OT administration for individuals high in affiliation and/or social engagement.

Conclusion

Collectively, these findings contribute to the growing recognition that effects of OT administration on social behavior are highly person-specific, highlighting the importance of a core personality trait: extraversion. Specifically, a single dose of OT helped to increase positive social outcomes for those low in extraversion, whereas there were indications that OT administration may have negative social consequences for those higher in extraversion. This is consistent with emerging evidence that OT administration may be selectively beneficial for those lower in affiliation, indicating that affiliative motivations may be a key mechanism linking the apparently inconsistent effects of OT administration on social outcomes. Additional research is needed to replicate these effects, ideally with larger samples and at different dosages of OT (Cardoso, Ellenbogen, Orlando, Bacon, & Joober, 2013; Cardoso, Orlando et al., 2014) and to directly examine the potential underlying mechanisms. In sum, these findings suggest that OT administration may selectively benefit those lower in extraversion, facilitating more positive social experiences and behaviors.

Footnotes

Acknowledgments

We are grateful to our dedicated research assistants at the University of California, San Francisco (UCSF) for their assistance in collecting these data and to Jennifer Bartz for helpful feedback on an earlier version of this manuscript.

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: The research was supported in part by Lauren J. Human’s Social Sciences and Humanities Research Council Postdoctoral Fellowship and a Greater Good Science Center grant to Wendy Berry Mendes.

Notes

Supplemental Material

The online supplements are available at

References

Anderson

John

O. P.

Keltner

Kring

A. M.

(2001). Who attains social status? Effects of personality and physical attractiveness in social groups. Journal of Personality and Social Psychology, 81, 116–132.

Aron

E. N.

Smollan

(1992). Inclusion of other in the self scale and the structure of interpersonal closeness. Journal of Personality and Social Psychology, 63, 596–612.

Bakermans-Kranenburg

M. J.

van Ijzendoorn

M. H.

(2013). Sniffing around oxytocin: Review and meta-analyses of trials in healthy and clinical groups with implications for pharmacotherapy. Translational Psychiatry, 3, e258.

Bartlett

M. Y.

DeSteno

(2006). Gratitude and prosocial behavior: Helping when it costs you. Psychological Science, 17, 319–325.

Bartz

J. A.

Hollander

(2006). The neuroscience of affiliation: Forging links between basic and clinical research on neuropeptides and social behavior. Hormones and Behavior, 50, 518–528. doi:10.1016/j .yhbeh.2006.06.018

Bartz

J. A.

Lydon

J. E.

Kolevzon

Zaki

Hollander

Ludwig

N. N.

Bolger

(2015). Differential effects of oxytocin on agency and communion for anxiously and avoidantly attached individuals. Psychological Science, 26, 1177–1186.

Bartz

J. A.

Simeon

Hamilton

Kim

Crystal

Braun

… Hollander

(2011). Oxytocin can hinder trust and cooperation in borderline personality disorder. Social Cognitive and Affective Neuroscience, 6, 556–563.

Bartz

J. A.

Zaki

Bolger

Ochsner

K. N.

(2011). Social effects of oxytocin in humans: Context and person matter. Trends in Cognitive Sciences, 15, 301–309.

Bartz

J. A.

Zaki

Bolger

Hollander

Ludwig

N. N.

Kolevzon

Ochsner

K. N.

(2010). Oxytocin selectively improves empathic accuracy. Psychological Science, 21, 1426–1428.

10.

Baumgartner

Heinrichs

Vonlanthen

Fischbacher

Fehr

(2008). Oxytocin shapes the neural circuitry of trust and trust adaptation in humans. Neuron, 58, 639–650. doi:10.1016/j.neuron.2008.04.009

11.

Berkman

L. F.

Glass

Brissette

Seeman

T. E.

(2000). From social integration to health. Social Science and Medicine, 51, 843–857.

12.

Cardoso

Ellenbogen

M. A.

Linnen

A.-M.

(2012). Acute intranasal oxytocin improves positive self-perceptions. Psychopharmacology, 220, 741–749.

13.

Cardoso

Ellenbogen

M. A.

Linnen

A.-M.

(2014). The effect of intranasal oxytocin on perceiving and understanding emotion on the Mayer-Salovey-Caruso Emotional Intelligence Test (MSCEIT). Emotion, 14, 43–50. doi:10.1037/a0034314

14.

Cardoso

Ellenbogen

M. A.

Orlando

M. A.

Bacon

S. L.

Joober

(2013). Intranasal oxytocin attenuates the cortisol response to physical stress: A dose-response study. Psychoneuroendocrinology, 38, 399–407.

15.

Cardoso

Orlando

M. A.

Brown

C. A.

Ellenbogen

M. A.

(2014). Oxytocin and enhancement of the positive valence of social affiliation memories: An autobiographical memory study. Social Neuroscience, 9, 186–195.

16.

Carlo

Okun

M. A.

Knight

G. P.

de Guzman

M. R. T.

(2005). The interplay of traits and motives on volunteering: Agreeableness, extraversion, and prosocial value motivation. Personality and Individual Differences, 38, 1293–1305.

17.

Carver

C. S.

(1997). Adult attachment and personality: Converging evidence and a new measure. Personality and Social Psychology Bulletin, 23, 865–883.

18.

Churchland

P. S.

Winkielman

(2012). Modulating social behavior with oxytocin: How does it work? What does it mean? Hormones and Behavior, 61, 392–399.

19.

Clark

M. S.

Lemay

E. P.

Jr . (2010). Close relationships. In Fiske

S. T.

Gilbert

D. T.

Lindzey

(Eds.), Handbook of social psychology (5th ed., Vol. 2, pp. 898–940). New York, NY: John Wiley.

20.

Cohen

(1962). The statistical power of abnormal-social psychological research: A review. Journal of Abnormal and Social Psychology, 65, 145–153.

21.

Conlisk

(2011). Professor Zak’s empirical studies on trust and oxytocin. Journal of Economic Behaviour and Organisation, 78, 160–166. doi:10.1016/j.jebo.2011.01.002

22.

Costa

P. T.

McCrae

R. R.

(1992). Revised NEO Personality Inventory (NEOPI-R) and Five Factor Inventory (NEO-FFI) professional manual. Odessa, FL: Psychological Assessment Resources.

23.

Deci

E. L.

La Guardia

J. G.

Moller

A. C.

Scheiner

M. J.

Ryan

R. M.

(2006). On the benefits of giving as well as receiving autonomy support: Mutuality in close friendships. Personality and Social Psychology Bulletin, 32, 313–327.

24.

De Dreu

C. K.

(2012). Oxytocin modulates the link between adult attachment and cooperation through reduced betrayal aversion. Psychoneuroendocrinology, 37, 871–880.

25.

De Dreu

C. K.

Greer

L. L.

Handgraaf

M. J.

Shalvi

Van Kleef

G. A.

Baas

… Feith

S. W.

(2010). The neuropeptide oxytocin regulates parochial altruism in intergroup conflict among humans. Science, 328, 1408–1411.

26.

Depue

R. A.

Collins

P. F.

(1999). Neurobiology of the structure of personality: Dopamine facilitation of incentive motivation and extraversion. Behavioral and Brain Sciences, 22, 491–569.

27.

DeSteno

Bartlett

M. Y.

Baumann

Williams

L. A.

Dickens

(2010). Gratitude as moral sentiment: Emotion-guided cooperation in economic exchange. Emotion, 2, 289–293.

28.

Di Simplicio

Massey-Chase

Cowen

Harmer

(2009). Oxytocin enhances processing of positive versus negative emotional information in healthy male volunteers. Journal of Psychopharmacology, 23, 241–248.

29.

Domes

Heinrichs

Michel

Berger

Herpertz

S. C.

(2007). Oxytocin improves “mind-reading” in humans. Biological Psychiatry, 61, 731–733.

30.

Guastella

A. J.

Einfeld

S. L.

Gray

K. M.

Rinehart

N. J.

Tonge

B. J.

Lambert

T. J.

Hickie

I. B.

(2010). Intranasal oxytocin improves emotion recognition for youth with autism spectrum disorders. Biological Psychiatry, 67, 692–694.

31.

Guastella

A. J.

Hickie

I. B.

McGuinness

M. M.

Otis

Woods

E. A.

Disinger

H. M.

… Banati

R. B.

(2013). Recommendations for the standardisation of oxytocin nasal administration and guidelines for its reporting in human research. Psychoneuroendocrinology, 38, 612–625.

32.

Guastella

A. J.

MacLeod

(2012). A critical review of the influence of oxytocin nasal spray on social cognition in humans: Evidence and future directions. Hormones and Behavior, 61, 410–418.

33.

Hawkley

L. C.

Cacioppo

J. T.

(2010). Loneliness matters: A theoretical and empirical review of consequences and mechanisms. Annals of Behavioral Medicine, 40, 218–227.

34.

Heinrichs

Baumgartner

Kirschbaum

Ehlert

(2003). Social support and oxytocin interact to suppress cortisol and subjective responses to psychosocial stress. Biological Psychiatry, 54, 1389–1398.

35.

Human

L. J.

Thorson

K. R.

Woolley

Mendes

W. B.

(2015). When two positives make a negative: Interactions between oxytocin administration and positive emotion inductions predicting analytical performance. Manuscript submitted for publication.

36.

Human

L. J.

Woolley

Mendes

W. B.

(2015). Effects of oxytocin administration on receiving help. Manuscript submitted for publication.

37.

Klackl

Pfundmair

Agroskin

Jonas

(2013). Who is to blame? Oxytocin promotes nonpersonalistic attributions in response to a trust betrayal. Biological Psychology, 92, 387–394. doi:10.1016/j.biopsycho.2012.11.010

38.

Kogan

Gruber

Shallcross

A. J.

Ford

B. Q.

Mauss

I. B.

(2013). Too much of a good thing? Cardiac vagal tone’s nonlinear relationship with well-being. Emotion, 13, 599–604.

39.

Kogan

Oveis

Carr

E. W.

Gruber

Mauss

Shallcross

… Keltner

(2014). Vagal activity is quadratically related to prosocial traits, prosocial emotions, and observer perceptions of prosociality. Journal of Personality and Social Psychology, 107, 1051–1063.

40.

Kosfeld

Heinrichs

Zak

P. J.

Fischbacher

Fehr

(2005). Oxytocin increases trust in humans. Nature, 435, 673–676.

41.

Leng

Ludwig

(2016). Intranasal oxytocin: Myths and delusions. Biological Psychiatry, 79, 243–250. doi:10.1016/j.biopsych.2015.05.003

42.

Lucas

R. E.

Diener

Grob

Suh

E. M.

Shao

(2000). Cross-cultural evidence for the fundamental features of extraversion. Journal of Personality and Social Psychology, 79, 452–468.

43.

Lucas

R. E.

Dyrenforth

P. S.

(2008). Explaining the extraversion/positive affect relation: Sociability cannot account for extraverts’ greater happiness. Journal of Personality, 76, 385–414.

44.

Marsh

A. A.

H. H.

Pine

D. S.

Blair

R. J.

(2010). Oxytocin improves specific recognition of positive facial expressions. Psychopharmacology, 209, 225–232. doi:10.1007/s00213-010-1780-4

45.

Mikolajczak

Gross

J. J.

Lane

Corneille

de Timary

Luminet

(2010). Oxytocin makes people trusting, not gullible. Psychological Science, 21, 1072–1074.

46.

Mikolajczak

Pinon

Lane

de Timary

Luminet

(2010). Oxytocin does not only increase trust when money is at stake but also when confidential information is in the balance. Biological Psychology, 85, 182–184.

47.

Nave

Camerer

McCullough

(2015). Does oxytocin increase trust in humans? A critical review of research. Perspectives in Psychological Science, 10, 772–789.

48.

Neumann

I. D.

(2008). Brain oxytocin: A key regulator of emotional and social behaviours in both females and males. Journal of Neuroendocrinology, 20, 858–865.

49.

Ozer

D. J.

Benet-Martínez

(2006). Personality and the prediction of consequential outcomes. Annual Review of Psychology, 57, 401–421.

50.

Penner

L. A.

(2002). Dispositional and organizational influences on sustained volunteerism: An interactionist perspective. Journal of Social Issues, 58, 447–467.

51.

Riem

M. M.

Bakermans-Kranenburg

M. J.

Huffmeijer

van Ijzendoorn

M. H.

(2013). Does intranasal oxytocin promote prosocial behavior to an excluded fellow player? A randomized-controlled trial with Cyberball. Psychoneuroendocrinology, 38, 1418–1425.

52.

Saucier

(1994). Mini-markers: A brief version of Goldberg’s unipolar big-five markers. Journal of Personality Assessment, 63, 506–516.

53.

Shamay-Tsoory

S. G.

Fischer

Dvash

Harari

Perach-Bloom

Levkovitz

(2009). Intranasal administration of oxytocin increases envy and schadenfreude (gloating). Biological Psychiatry, 66, 864–870.

54.

Striepens

Kendrick

K. M.

Hanking

Landgraf

Wüllner

Maier

Hurlemann

(2013). Elevated cerebrospinal fluid and blood concentrations of oxytocin following its intranasal administration in humans. Scientific Reports, 3, 1–5.

55.

Taylor

S. E.

Klein

L. C.

Lewis

B. P.

Gruenewald

T. L.

Gurung

R. A. R.

Updegraff

J. A.

(2000). Biobehavioral responses to stress in females: Tend-and-befriend, not fight-or-flight. Psychological Review, 107, 411–429.

56.

Thomas

P. A.

(2010). Is it better to give or receive? Social support and the well-being of older adults. The Journals of Gerontology Series B: Psychological Sciences and Social Sciences, 65, 351–357.

57.

Unkelbach

Guastella

A. J.

Forgas

J. P.

(2008). Oxytocin selectively facilitates recognition of positive sex and relationship words. Psychological Science, 19, 1092–1094.

58.

Uvnäs-Moberg

(1998). Antistress pattern induced by oxytocin. News in Physiological Sciences, 13, 22–26.

59.

van Ijzendoorn

M. H.

Bakermans-Kranenburg

M. J.

(2012). A sniff of trust: Meta-analysis of the effects of intranasal oxytocin administration on face recognition, trust to in-group, and trust to out-group. Psychoneuroendocrinology, 37, 438–443.

60.

van Ijzendoorn

M. H.

Huffmeijer

Alink

L. R.

Bakermans-Kranenburg

M. J.

Tops

(2011). The impact of oxytocin administration on charitable donating is moderated by experiences of parental love-withdrawal. Frontiers in Psychology, 2, 258.

61.

Vankov

Bowers

Munafò

M. R.

(2014). On the persistence of low power in psychological science. The Quarterly Journal of Experimental Psychology, 67, 1037–1040.

62.

Watson

Clark

L. A.

(1997). Extraversion and its positive emotional core. In Hogan

Johnson

Briggs

(Eds.), Handbook of personality psychology (pp. 767–793). San Diego, CA: Academic Press.

63.

Watson

Hubbard

Wiese

(2000). General traits of personality and affectivity as predictors of satisfaction in intimate relationships: Evidence from self-and partner-ratings. Journal of Personality, 68, 413–449.

64.

Zak

P. J.

Stanton

A. A.

Ahmadi

(2007). Oxytocin increases generosity in humans. PLoS One, 2, e1128.

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