A team of researchers affiliated with several institutions in China has found that people who engage in altruistic behaviors feel less pain than they otherwise would.
In their paper published in Proceedings of the National Academy of Sciences, the group outlines the experiments they carried out with volunteers and what they learned from them.
Prior research has shown that engaging in altruistic behaviors (extending kindness to others without expecting anything in return) can make people feel good – doing so causes the brain to produce chemicals such as dopamine which heighten good feelings.
Now, the researchers have found that engaging in such activities can also dull the sensation of pain.
To learn more about how engaging in altruistic behavior might impact the perception of pain, the researchers carried out four experiments.
In the first experiment, they asked people giving blood after an earthquake to rate how the pain of the needle jab – they also questioned people giving blood when there were no recent disasters.
They found that the people volunteering after the earthquake reported that the needle hurt less than the other group.
In a second experiment, the researchers asked volunteers to help revise a handbook for migrant children while being exposed to cold conditions.
They found that those volunteers reported less cold discomfort than did those who did not volunteer to revise the handbook.
In a third experiment, the researchers compared cancer patients experiencing pain who cooked and cleaned for others with similar patients who only did so for themselves – once again, they found those helping others reported less pain.
In their final experiment, the researchers asked volunteers to donate money to help orphans; those subjects were also asked how much they thought their donation helped the kids. Each of the volunteers then underwent an MRI scan while experiencing electrical shocks.
The researchers report that those who had donated showed less brain response to the shock then did those who refused to donate. They also found that the more a volunteer felt their donation had helped the orphans, the less their brain responded to the shock.
The researchers suggest their experiments, when combined with results from other studies, indicate that altruistic behavior not only makes people feel good, it also reduces the experience of pain.
Empathy represents a core social function that allows individuals to recognize and understand the emotional states of others and respond to them accordingly (Eisenberg and Eggum, 2009).
Empathy has 2 main components: cognitive empathy, which includes cognitive processes of perspective-taking allowing us to infer the mental states of others; and emotional empathy, reflecting a direct affective reaction involving understanding, sharing, and responding appropriately to their feelings (Shamay-Tsoory et al., 2009).
Numerous studies have focused specifically on empathy in response to physical pain (Marsh, 2018) and social pain caused by being rejected or excluded (Wesselmann et al., 2009) and established that both share common neural circuits (Eisenberger et al., 2003).
Empathy for those in suffering leads to distressed feelings and a motivation for altruistic helping behavior (FeldmanHall et al., 2015). Reciprocal altruism is associated with increased activity in the reward system (Rilling et al., 2002), although altruism is often exhibited in the absence of an expected reciprocity and can occur at the cost of self-interest (de Waal, 2008). Such costly altruistic behaviors and associated activity in reward-related regions are driven by other-oriented empathy rather than personal distress (FeldmanHall et al., 2015).
The neuropeptide oxytocin (OXT) can modulate core pain empathy regions, including the anterior cingulate cortex (ACC) and insula, as well as mentalizing and reward-related striato-frontal circuits (see Wigton et al., 2015). Intranasal OXT administration particularly enhances emotional—rather than cognitive—empathy via the amygdala (Hurlemann et al., 2010; Geng et al., 2018a).
On the other hand, insula responses can be either enhanced (Striepens et al., 2012) or decreased in the context of pain empathy (Bos et al., 2015) and embarrassment (Geng et al., 2018b). In line with its emotional empathy-enhancing effects, intranasal OXT has been reported to increase altruistic behavior towards an ostracized individual (Riem et al., 2013). However, in this latter study exhibiting altruistic behavior had no cost to the participants, whereas in real-life situations it often does (Camerer and Fehr, 2006).
Although OXT has often been reported to facilitate prosocial behaviors, it can also promote anti-social ones such as self-serving lying and group-serving dishonesty (Shalvi and De Dreu, 2014; Kendrick et al., 2017; Sindermann, 2018). On the other hand, OXT can also increase altruistic behaviors (Hu et al., 2016; Aydogan et al., 2017a). Thus, although OXT can influence empathy, altruistic, and self-serving behaviors, it is unclear what its functional role may be when these motivations are competing.
The current placebo (PLC)-controlled double-blind functional magnetic resonance imaging (fMRI) study therefore aimed at determining the effects of intranasal OXT on competing behavioral tendencies between empathy-motivated altruism and self-interest. A Cyberball paradigm was employed where subjects initially observed a social exclusion situation and subsequently engaged in the game.
The Cyberball game is widely used to induce social exclusion leading to painful feelings (Williams, 2009) and can induce social pain empathy when observing others being excluded (Wesselmann et al., 2009) and prosocial behavior towards them (Masten et al., 2011).
This paradigm is also effective in capturing effects of OXT on social behaviors, for example, increasing social interactions with a reciprocal player in high-functioning autism spectrum disorders (Andari et al., 2010) and motivation to restore social connections with negative players in men (Xu et al., 2017).
In the current paradigm, participants were scanned while first observing 3 unknown individuals playing the game and where 1 player (victim) was gradually excluded by the other 2 (excluders), thereby gaining more money than the victim.
Immediately after the observe session, participants played with the victim and one of the excluders as well as another new player. To create a situation of competing empathy and self-interest, participants were told that any player receiving a ball would receive a small additional monetary reward. In this case, the excluder player was manipulated to be the most attractive cooperator to maximize self-interest, while playing with the victim of exclusion would be rather motivated by empathy-induced altruistic behavior.
Considering convergent evidence for OXT-enhanced emotional empathy, we hypothesized that it would increase empathy for the victim of exclusion. We additionally hypothesized that OXT-facilitated empathy would be accompanied by increased activation in (social) pain (dorsal anterior cingulate cortex [dACC] and anterior insula) and mentalizing networks (medial frontal cortex, posterior superior temporal sulcus [pSTS], posterior cingulate cortex [PCC], and precuneus) (Eisenberger et al., 2003; Masten et al., 2011).
In the second stage of the experiment when the subjects played, we hypothesized that if OXT promotes costly altruistic behavior subjects should increase their proportion of throws to the victim and throw less to the excluder, whereas if it promotes increased self-serving behavior then they would throw more to the excluder player, indicating an increased interest in personal financial gain. Given the engagement of striato-orbitofrontal reward-processing circuits in both monetary reward-anticipation (O’Doherty et al., 2001) and altruistic behavior (FeldmanHall et al., 2015) we hypothesized that the OXT-induced behavioral preference for a player would be mirrored by increased activity in this circuit.
Since cultural orientation, that is, horizontal independence (HI), has been shown to modulate the effect of OXT following social exclusion (Xu et al., 2017), and higher trait altruism is associated with stronger empathic brain responses (Haas et al., 2015), these traits were additionally assessed. Finally, in view of our previous study demonstrating long-term effects on memory and preference for replaying with specific players (Xu et al., 2017), we also investigated these same factors 1 week later.
Discussion
The current study aimed firstly to establish whether OXT enhanced empathic behavior and neural responses towards observing someone being socially excluded, and secondly promoted altruistic or self-serving behaviors and associated neural responses when these 2 behaviors are in competition. Overall, following observation of a modified Cyberball game, both groups showed strong empathic responses towards the victim players and greater likeability and trustworthiness ratings for them compared with excluder players, but OXT did not potentiate this.
Observation of social exclusion was accompanied by increased activity in the mentalizing network, including the PCC, pSTS, IPL, and precuneus; however, activity patterns were also not influenced by OXT. During the subsequent play phase of the paradigm, subjects in both groups threw more balls to the victim player, but this was not enhanced by OXT, suggesting that it did not promote greater altruistic behavior.
However, the OXT group threw significantly more balls to the excluder players, suggesting that OXT promoted self-serving decisions since playing with the excluder should potentially lead to a higher monetary pay-off. In line with our hypothesis, increased self-serving behavior following OXT was associated with stronger activation in the mOFC reward system when subjects were playing with the excluder player. Furthermore, OXT established a negative relationship between mOFC activity and trait altruism, an association that was absent following PLC.
One week after the Cyberball game while the PLC group expressed a greater preference to play again with the victim and novel players compared with the excluder, in the OXT group there was no such difference, indicating that they maintained their greater interest in playing with individuals who might potentially help them gain larger rewards. Thus, overall, our results demonstrate that when altruistic and self-serving motivations are in competition, OXT rather than promoting altruism actually enhances selfish decision-making.
Our hypothesis that OXT would enhance empathic responses towards the victims of social exclusion was not supported. Previous research showed that OXT enhanced emotional but not cognitive empathy, associated with suppressed amygdala responses (Hurlemann et al., 2010; Geng et al., 2018a).
Oxytocin also increased empathic embarrassment in male and female subjects, and this was associated with decreased amygdala and insula cortex responses but with no effect on mentalizing networks (Geng et al., 2018b). Empathic embarrassment can be considered as an example of social pain, and another study has also reported that OXT decreased insula responses to viewing people in pain (Bos et al., 2015).
In the current study in both the PLC and OXT groups, there was evidence at the whole brain level for increased activation in core mentalizing regions (for convergent findings, see also Masten et al., 2011) but no responses in the pain network (notably the insula).
In general, empathic ratings by subjects for the victim were not that high and altered activation was only observed in the mentalizing network which we have shown in the context of empathic embarrassment is not influenced by OXT (Geng et al., 2018b).
The empathy experienced in the current context may therefore have been more cognitive than emotional. Indeed, since participants could not directly observe the other players and static neutral faces were used, social pain had to be inferred by mentalizing how the victim may emotionally experience exclusion.
Since the mentalizing system is a core component of the cognitive empathy (Shamay-Tsoory et al., 2009), this may explain why OXT failed to have any impact on empathic ratings or associated likeability and trustworthiness ratings for the victim due to its greater influence on emotional rather than cognitive empathy.
Our original hypothesis that where altruistic and self-serving motivations were in competition OXT would enhance altruistic responses was also not supported. Overall, while participants in both groups threw more balls to the victim player, indicative of an altruistic response and validating the experimental manipulation, OXT had no effect on this.
Similarly, both groups rated the likeability and trustworthiness of excluder players lower than that of victims after observing the game and also 1 week later after playing it, but again this was not influenced by OXT. This finding agrees with previous studies showing that subjects exhibit greater prosocial behavior towards individuals observed to be socially excluded (Masten et al., 2011; Van Der Meulen et al., 2016).
On the other hand, subjects in the OXT group threw a significantly greater proportion of balls to the excluder player, indicative of an enhanced self-serving motivation since the latter would have been perceived as being more likely to reciprocate, leading to greater financial gain. A previous study has reported that OXT can enhance strategic reasoning in decision-making (Aydogan et al., 2018), and it is possible that our current results could also reflect an OXT effect on strategic decision-making. However, in the current paradigm the obvious strategy for subjects to gain more money had already been clearly demonstrated to them by the excluder players during the observation session.
Furthermore, after the observation session all subjects revealed awareness of this strategy since they identified the differences in the relative gains obtained by excluders as opposed to the victim. Thus, during the Play session it would seem more likely that OXT was only influencing whether subjects decided to use this prior-demonstrated strategy to gain their additional personal monetary reward.
While a number of previous studies have demonstrated that OXT can facilitate altruistic behaviors in terms of cooperation, generosity, trait judgements and valuing other’s possessions, these have mainly involved contexts where personal costs to individuals were absent or low (Andari et al., 2010; Declerck et al., 2010; Zhao et al., 2016, 2017).
The finding that under circumstances where there is perceived to be a potential cost of altruism in terms of reduced personal gain argues for the primary function of OXT as enhancing the motivation for resource acquisition. Where individuals do exhibit costly altruistic behavior, this is paralleled by increased empathic concern and altered activation in the ventral tegmental area, caudate, and subgenual anterior cingulate, which are important for promoting social attachment and caregiving (FeldmanHall et al., 2015).
Although OXT has been shown to modulate neural processing in these regions in social and nonsocial contexts (e.g., Mickey et al., 2016; Zhao et al., 2019), it did not affect activity in this circuitry during the present paradigm, further indicating its lack of effect on promoting altruism.
Previous studies have reported that OXT can promote lying to benefit in-group members, although not purely for self-gain (Shalvi and De Dreu, 2014), and reduce honesty for personal gain in a competitive environment (Aydogan et al., 2017b). However, OXT can also promote pure self-serving lying to increase personal gain when there is no risk of discovery (Sindermann et al., 2018) and increase acceptance of self-benefit, but not other types of moral dilemmas (Scheele et al., 2014).
Interestingly, OXT effects on self-serving lying for financial gain are modulated by OXT receptor genotype (Sindermann et al., 2018). Taken together and in line with our current results, accumulating evidence therefore suggests that OXT can promote personal self-interest in some contexts.
On the neural level, increased self-serving behavior following OXT was associated with increased mOFC activation when subjects interacted with excluder players. The mOFC is involved in monitoring associations between previous stimuli with reward and tracking response-outcome probabilities during changing reward contingencies (Elliott et al., 2000; Kringelbach and Rolls, 2004).
Moreover, the mOFC codes the value of different behavioral options including that of expected monetary gains (Breiter et al., 2001) and its activity increases with monetary reward magnitude (O’Doherty et al., 2001). Thus, increased mOFC responses in the OXT group may reflect an enhanced value of the expected greater monetary reward when cooperating with the excluder player.
Our findings are in line with previous studies demonstrating that OXT enhances activity in brain reward regions in social contexts, such as when viewing a romantic partner’s face (Scheele et al., 2013; nucleus accumbens and ventral tegmentum), receiving affective touch (Scheele et al., 2014; orbitofrontal cortex); and receiving social feedback to promote learning (Hu et al., 2015; putamen). One study has also reported that OXT increases activity in the putamen during monetary reward and loss anticipation (Nawijn et al., 2016), and oxytocin receptors are known to be strongly expressed in the human brain reward system (Quintana et al., 2019).
Additionally, OXT produced a negative association between PTM trait altruism and mOFC activation that was absent following PLC. This suggests that at the neural level OXT particularly increased the value of the potential monetary gain in subjects with low baseline altruistic tendencies. Possibly individuals with high trait altruism are less likely to experience a greater anticipation of gaining a greater monetary reward by playing with the excluder under OXT, as a result of greater feelings of guilt evoked by having to exclude other players, and notably the victim.
While both behavioral and neural effects of OXT observed in the current paradigm indicate a shift towards a self-serving rather than altruistic motivation it is notable that the pattern of altered bias is quite subtle. Under OXT, subjects do not actually play more with excluders than with either victim or novel players and effectively exhibit an egalitarian playing pattern that is unlikely to generate feelings of exclusion in any of the other players.
This contrasts with the PLC group who show a clear pattern of excluding the excluders compared with both victim and novel players. Thus, OXT may only promote self-benefit behavior if it does not damage others and cause feelings of guilt.
Indeed, this is supported by findings that OXT increases lying for self-gain when individuals know that there is no chance their lies will be discovered or will reduce the financial gain of others (Sinderman et al., 2018). Alternatively, it might be argued that subjects in the PLC group are exhibiting altruistic punishment towards the excluders and OXT is reducing the desire to inflict such punishment.
However, altruistic punishment is strongly associated with altered amygdala function (Scheele et al., 2012), and there was no evidence for differential amygdala responses in the PLC and OXT groups. While OXT can promote altruistic punishment of defectors, and feelings of anger and disappointment towards them in the Prisoner’s dilemma game, it also increases cooperation with them thereby increasing self-gain (Aydogan et al., 2017a).
Thus, in the current context OXT may primarily bias individuals towards an optimal self-gain strategy, although without simultaneously doing so by overtly damaging others emotionally. Clearly, to further establish this it would be necessary to investigate the effects of OXT under circumstances where increasing self-gain would also significantly damage others emotionally.
There are several limitations to the present study. Firstly, the victim observed being excluded in the game was a stranger to the participant and if they had been a partner, relative, or other in-group member then OXT may have had the opposite effect by enhancing empathic and altruistic behaviors rather than self-serving ones. Secondly, only male participants were included and a number of studies have reported opposite neural and behavioral effects of OXT in males and females (Scheele et al., 2014; Gao et al., 2016; Luo et al., 2017).
Thus, in a similar situation OXT may have facilitated altruistic rather than self-serving behavior in women. Thirdly, the Cyberball game is an online dynamic virtual game intended to simulate real social interactions and subjects may not be completely convinced that they are interacting with others.
Importantly though, only 3 subjects questioned afterwards if the other players involved were in fact real, whereas the majority involved in the study did not do so, suggesting that they did believe they were real. Nevertheless, it remains possible that if interactions with other players were direct face to face results might have been different. Lastly, the Cyberball paradigm can incorporate additional factors, such as deception and anxiety about being ostracized by others.
As such, it may not exclusively examine altruistic and selfish behaviors, although we showed no differential effects of treatment on subjects’ mood during the course of the experiment. Future studies may consider employing additional paradigms to elicit altruistic and selfish behaviors.
In summary, our current findings demonstrate that when self-serving and altruistic behaviors are in competition OXT promotes increased self-benefit behavior associated with increased activation in the mOFC, indicative of greater reward anticipation. Furthermore, the effects of OXT on mOFC are strongest in individuals with lower trait altruism. Thus, OXT tends to bias individuals towards acquisition of resources for self-benefit rather than altruistic behavior, although this may not extend to the point where it generates strong negative feelings in others or feelings of guilt and risk of punishment for social norm violations.
More information: Yilu Wang et al. Altruistic behaviors relieve physical pain, Proceedings of the National Academy of Sciences (2019). DOI: 10.1073/pnas.1911861117
