Edited by: Peter G. Enticott, Monash University, Australia
Reviewed by: Dean S. Carson, Stanford University, USA; Hidenori Yamasue, University of Tokyo, Japan
*Correspondence: Angeliki Theodoridou, School of Experimental Psychology, University of Bristol, 12a Priory Road, Clifton, Bristol BS8 1TU, UK. e-mail:
This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in other forums, provided the original authors and source are credited and subject to any copyright notices concerning any third-party graphics etc.
Oxytocin (OT) is thought to play an important role in human interpersonal information processing and behavior. By inference, OT should facilitate empathic responding, i.e., the ability to feel for others and to take their perspective. In two independent double-blind, placebo-controlled between-subjects studies, we assessed the effect of intranasally administered OT on affective empathy and perspective taking, whilst also examining potential sex differences (e.g., women being more empathic than men). In study 1, we provided 96 participants (48 men) with an empathy scenario and recorded self-reports of empathic reactions to the scenario, while in study 2, a sample of 120 individuals (60 men) performed a computerized implicit perspective taking task. Whilst results from Study 1 showed no influence of OT on affective empathy, we found in Study 2 that OT exerted an effect on perspective taking ability in men. More specifically, men responded faster than women in the placebo group but they responded as slowly as women in the OT group. We conjecture that men in the OT group adopted a social perspective taking strategy, such as did women in both groups, but not men in the placebo group. On the basis of results across both studies, we suggest that self-report measures (such as used in Study 1) might be less sensitive to OT effects than more implicit measures of empathy such as that used in Study 2. If these assumptions are confirmed, one could infer that OT effects on empathic responses are more pronounced in men than women, and that any such effect is best studied using more implicit measures of empathy rather than explicit self-report measures.
Oxytocin (OT) is a highly conserved neuropeptide and an accumulation of its receptors are found in the amygdala (Loup et al.,
In line with its anatomical and functional properties, OT is involved in human interpersonal information processing and behavior such as in enhancing prosocial judgments and behavior. For example, OT as compared to placebo administration (1) yielded higher trust in others (Kosfeld et al.,
Given OT's role in interpersonal information processing and behavior, it can be assumed that it also plays a role in empathy, that is, the ability to understand another's emotional perspective and to be personally affected by it in a way that mirrors the feelings of the individual (Eisenberg and Miller,
To date, examination of OT's role in empathy has been associated with two main pitfalls. Firstly, most studies have used self-report questionnaires, which lack accuracy and are prone to socially desirable responding Tierney and McCabe,
In two independent studies, we used comparable double-blind placebo-controlled between-subject designs to assess healthy individuals' empathy as a function of nasal OT administration. In study 1, we provided participants with a vignette in which a person's unfortunate plight was described. Participants rated their empathic feelings toward the individual (see e.g., Coke et al.,
In addition to these hypotheses, we considered the role of participant sex. Some studies of OT effects support an enhancing role of OT for interpersonal behavioral responses in both sexes (for evidence of absence of sex-dimorphic effects of OT see Ditzen et al.,
In both studies, we conducted two sessions: a baseline session performed by participants at home and a laboratory session for which participants came to the University. Before participation in either session we obtained written informed consent from each participant. We only tested participants who met our inclusion criteria: being a fluent English speaker, not having consumed any medication, or having any other medical reason why they should not receive OT. In the case of female participants, they could not be pregnant, or if post-birth, should not be breastfeeding. The research protocol in both studies was approved by the Faculty of Science Human Research Ethics Committee at the University of Bristol. We recruited participants through poster advertisement in and around university buildings and sent emails to various departments and posted on the university's jobs website. In the baseline session, participants provided demographic information (e.g., age, sex) and filled in self-report questionnaires such as the Major Depression Inventory (MDI; Bech,
In the laboratory session at the local university, approximately one week later, participants were tested individually. They were instructed to abstain from alcohol, caffeine, and nicotine for 24 h before testing and from food and drink (except water) for 2 h before testing. When they arrived in the laboratory, each participant signed an informed consent form. The session lasted up to 2 h, with the actual task battery being assessed in the first 60 min after the waiting period, and the remaining time being used to guard for potential side effects. At the very beginning, participants were told that they would first receive a small dose of OT or a near identical looking and smelling placebo before being tested in various tasks. Information was also given about possible side effects associated with OT administration and participants were informed that they had the right to withdraw from the study at any time. In a double-blind procedure, participants were randomly assigned to self-administer a small intranasal dose of either 24 IU OT (Syntocinon Spray, Novartis, 3 puffs per nostril, each puff containing 4 IU OT), or placebo (containing the same ingredients, but OT, to the OT nasal spray). After a waiting period of 25–30 min, participants completed the task battery including the empathy vignette task (Study 1) and the 3PP-task (Study 2). Tasks were presented in two blocks, randomized in order. In study 1, the empathy scenario task was administered either 35 or 55 min after drug administration. In study 2, the 3PP-task was completed either 35 or 60 min after drug administration (see Theodoridou et al.,
In the laboratory sessions, we also assessed current mood, wakefulness, and calmness with the short form of the Multidimensional Mood State Questionnaire (Steyer et al.,
Of the 96 participants (mainly students, mean age: 21.4 years, age range: 18–40 years), 51 (25 males) received OT, and 45 received placebo (23 males). As reported in our previous study (Theodoridou et al.,
Emotional reactions to another person's plight were assessed using a procedure similar to that employed previously (e.g., Coke et al.,
Half of the adjectives tap on empathic concern (i.e., other-oriented emotional empathy at the plight of others):
Of the 120 participants (mainly students, mean age: 22.4 years, age range: 18–44 years), 60 (30 males) received OT, and 60 received placebo (30 males). As in study 1 (Theodoridou et al.,
In Study 1, data from one participant was excluded because this person responded especially slowly (average response time: 18 s). We also excluded scores (ratings) that were two standard deviations above or below the mean (1.51% of the data). A MANOVA test was carried out on mean empathic concern ratings and mean personal distress ratings, with drug (OT, Placebo) and participant sex (male, female) as between-subjects variables. One-sample
In Study 2, reaction times shorter than 200 ms and longer than 5000 ms were considered to be outliers and were dropped (Harris et al.,
The ANOVA on age showed no significant main effects [drug:
The MANOVA showed that OT (vs. placebo) had no effect on empathic concern,
When comparing the two adjective rating scores against chance level (3.5), the one-sample
OT | M | 4.93 (0.64) | 10.93 (<0.001) | 3.80 (1.01) | 1.47 (0.15) |
F | 5.23 (0.89) | 9.82 (<0.001) | 3.86 (1.46) | 1.24 (0.23) | |
P | M | 4.93 (0.91) | 7.39 (<0.001) | 3.49 (1.18) | −0.04 (0.97) |
F | 5.39 (1.10) | 8.03 (<0.001) | 4.16 (1.35) | 2.30 (0.03) |
The ANOVA on age showed no significant main effects [drug:
The ANOVA on mean reaction times for correct decisions showed a significant main effect of figure position,
We found significant 2-way interactions between figure position and participant sex,
Finally, to further elucidate the significant drug, target sex, and participant sex interaction, we performed 2-way ANOVAs, for the OT and the placebo group separately, with figure sex as a repeated measure and sex as a between subject-factor. The ANOVA for the OT group only showed the significant main effect on figure sex,
In two independent double-blind, placebo-controlled between-subject design studies we investigated whether the consumption of a single dose of OT affected the ability to empathize with another individual's unfortunate plight (Study 1) and the ability to mentally take the perspective of another person (Study 2). In study 1, we provided participants with a scenario designed to elicit empathy [modified version used by Coke et al. (
In study 1, the OT and placebo group provided comparable adjective ratings after hearing about an unknown person's plight. By inference the two groups reported comparable empathic reactions and personal distress when rating these adjectives. Contrary to previous findings supporting the role of OT in prosocial and affiliative behavior (Kosfeld et al.,
Importantly, our results show no effect of drug administration on personal distress or empathic concern. Therefore, our findings fail to provide evidence for an anxiolytic and prosocial effect of OT, respectively, in the context of affective responses to an individual's plight. It is worth noting that in line with previous relevant studies (Batson et al.,
To further understand the influence of sex on the link between OT effects on empathic abilities we tested an equal number of women and men. Studies in which individuals were provided with audio tapes narrating the plight of a needy person showed that women reported higher levels of empathy than men for the needy person (Batson et al.,
In study 2, we found that speed of response in the drug groups interacted with figure sex and participant sex. We observed that sex differences in the placebo group were absent in the OT group. More precisely, in both drug groups, we found that people responded faster to female than male figures. In the placebo group, we additionally observed that men responded faster than women, and that this sex difference was statistically significant for male figures and a statistical trend for female figures. Given that these sex differences are absent in the OT group, we infer that OT might have sex-dimorphic effects on this measure of perspective taking ability, an inference that is in line with a recent review by MacDonald (
If OT fosters social perspective taking in men, we could expect in future studies that a higher than normal OT availability may facilitate men's tendency to step into another person's shoes, a fundamental component of empathy (e.g., see Kaiser et al.,
We suggest that the above findings on OT effects in men are not an artifact of overall or aberrant performance in our study population, because we replicated previous behavioral findings using slightly modified versions of the current 3PP-task. Firstly, reaction times were faster for back-facing than front-facing pictures (see also e.g., Arzy et al.,
Two studies examined the differential effects of OT on empathic responses, once using self-report ratings after having heard the story of an unknown person's unfortunate plight (study 1) and once using reaction times in a computerized 3PP-task (study 2). The major findings were that while OT as compared to placebo administration did not enhance self-reported empathic concern toward others (study 1), it showed that a male over female advantage in the 3PP-task that was evident in the placebo group was absent in the OT group (study 2). This finding is suggestive of a potential strategy change (purportedly more social than spatial performance strategy, see rationale in more detail above) in men after consuming OT as compared to placebo. Such a facilitation of social perspective taking might already be present in women, regardless of which of the two drugs were consumed. Thus, additional OT availability might affect men but not women in the 3PP-task. This conjecture, if supported in the future, might be relevant to sub-populations low in appropriate social abilities, such as individuals with alexithymia, social anxiety disorder, and schizophrenia (Caldwell et al.,
Given the conjectural nature of our conclusions, future studies should verify the strategy participants employ in the 3PP-task, e.g., examine whether women are slower because they use a social perspective strategy while men (at least without pharmacologically enhanced OT availabilities) use a spatial perspective taking strategy (Gardner et al.,
Another potential explanation of the above finding is that OT administration generally slows men down. It should be noted that whilst OT administration has been shown to slow men down in contexts other than spatial processing, such as during approach-avoidance motor responses to emotional faces (Theodoridou et al.,
Importantly, the sex differences and the interaction with drug group were observed in a task that was introduced as a task that assesses empathy. Future research could introduce the task as one that assesses mental rotation (see also Massa et al.,
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
We wish to thank the ESRC for funding this study in way of a studentship to the lead author, Angeliki Theodoridou. We also thank Professor Stafford Lightman and Professor Peter Rogers for offering protocol advice, and Professor Markus Heinrichs and Dr. Bernadette von Dawans for helping us source study materials. We are also grateful to Sophie and Ken for posing as models for our perspective taking task.
1As reported in previous studies on results obtained from this population, participants could not predict the treatment they received (see Theodoridou et al.,
2No effect of task order (task administered 35 min vs. 55 min after drug intake) was found when it was added as a covariate to the MANOVA (
3When task order (task administered 35 min after drug intake, task administered 60 min after drug intake) was added to the above ANOVA as a covariate no effects involving task order were found (all