How we engage in mutual cooperation: the neuroscience of trust

By Luciano Marinelli

Throughout life, many decisions are made within the context of social interactions, hence will affect both us and other people. Difficult social decisions often involve an internal conflict between following our own interests and that of others. These decisions require a good amount of trust, especially when engaging in reciprocal exchange, in which a positive action towards another is reciprocated by the other party. Because this often involves a time delay between giving and receiving, it is possible for people to accept favours but not reciprocate in favour of short-term self-interests, and both parties will also fear such behaviour in the other (Rilling JK et al., 2011). Because of this, we have to decide whether to trust the other and vice-versa. How do these trust assessments occur and how do most people overcome the temptation to not reciprocate? This review will outline the neuroscience behind building and reciprocating trust and how different brain regions interact to encourage mutual collaboration. 

Several studies have found that the neuropeptide oxytocin (OT) increases trust among humans by interacting with the amygdala. Baumgartner et al. (Baumgartner T. et al., 2008) demonstrated that injecting oxytocin into subjects is associated with a reduction in the activation of neural systems mediating fear, including the amygdala. This same study also showed that amygdala activation was attenuated by oxytocin when the participants decided to trust opponents despite receiving feedback that half of the trust behaviour was betrayed from the same opponents in previous rounds (Baumgartner T. et al., 2008). Therefore OT-mediated inhibition of the amygdala facilitates trust by reducing the fear of betrayal (not reciprocating favours) (Rilling JK et al., 2011). Such inhibition is mediated by the ventromedial prefrontal cortex (VMPFC), as shown by patients with VMPFC lesions exhibiting potentiated amygdala activity (Motzkin JC et al., 2014). However, this was only seen in men, suggesting that trust in men is affected by fear of social risk mediated by the amygdala, whereas in women other factors play a role (Nishina K. et al., 2018).  

Moreover, we are far more likely to trust someone who we know has reciprocated in the past rather than someone who has often cheated. Thus, reward learning shapes our decision. Regions involved in reward processing such as the caudate nucleus and the orbitofrontal cortex mediate such behaviour. These regions are less activated when stimuli are less novel or expected, hence during cooperative interactions with trustworthy individuals, in which the outcome matches our expectations, they are less activated (Fett AJ et al., 2014). As a demonstration of this, an fMRI study by Wardle M et al (Wardle MC et al., 2013) showed greater activation of the caudate nucleus during trust decisions with partners who reciprocated only 25% or 50% of the time in the past compared to with partners who reciprocated 75% of the time (Wardle MC et al., 2013). It can therefore be hypothesized that the caudate nucleus and the orbitofrontal cortex are responsible for assessing the trustworthiness of another individual based on their reputation.

On the other side, there is obvious temptation by the other party to not reciprocate in order to attain a higher personal benefit, but this is often overcome. The anterior medial prefrontal cortex (AMPFC) and the right temporo-parietal junction (rTPJ) regulate such behaviour. The AMPFC is more active when participants defect compared to when they reciprocate, suggesting this region is important for valuing personal outcome over the outcome of reciprocating trust. Hence, it can be inferred that the AMPFC is responsible for the temptation to break the promise to reciprocate because of greater personal outcome. However, the rTPJ usually helps resist this temptation and instead value the other party and the benefit from reciprocating by aiding in the understanding of other people’s intentions (Fett AJ et al., 2014). This region, as a result, is involved in shifting attention from the self to others, motivating individuals to value the outcomes for the other party (van den Bos W. et al., 2009).  

Reciprocating behaviour is also dependent on the social value orientation of the individual. Individuals with a prosocial orientation, who have goals more aligned with those of the other, exhibit greater rTPJ activation when defecting whereas pro-self individuals show greater rTPJ activation when reciprocating. This would mean that prosocial individuals have to shift their attention less when reciprocating (it’s more “normal” for them) than when defecting, and the opposite is true for pro-selves. Thus, defecting may be aversive to pro-socials, whereas reciprocating may be aversive to pro-selves, who would therefore be less willing to reciprocate. Furthermore, pro-socials exhibit greater ventral striatum activity when reciprocating compared to pro-self individuals, suggesting pro-socials also find more reward value when collaborating (van den Bos W. et al., 2009; Rilling K. et al., 2011) 

An important role in deciding to reciprocate is played by the feeling of guilt in the case we don’t return the favour. van den Bos et al. showed that patients with VMPFC lesions exhibit less feelings of guilt associated with lower levels of prosocial behaviour, as demonstrated by patients offering less money and keeping more to themselves in the dictator game (van den Bos W. et al., 2009). Thus, in addition to reducing the fear of betrayal when assessing an individual’s trustworthiness, the VMPFC also encourages reciprocation by minimizing the potential arousal of negative emotions, particularly guilt, in the event of cheating. In addition to this, the frontal pole present in this region has also been shown to protect long-term plans from immediate demands as well as in valuing future rewards (Koechlin E et al., 2007). Being so highly involved in trust, the VMPFC is, in fact, considered one of the main mediators of trust behaviour.

Ultimately, trust is regulated by multiple brain regions working together, particularly involving the prefrontal cortex. In fact, because of its much greater size in humans compared to animals, the prefrontal cortex is believed to be the main region responsible for the ability of humans to cooperate with non-relatives, unlike animals (Rilling K. et al., 2011). The prefrontal cortex can therefore be used as a potential therapeutic target region for conditions in which trust is affected, as in autistic children (Yi L. et al., 2013). Further research into how this area, as well as other regions, mediate trust could thus provide novel meaningful knowledge on the neuroscience behind this behaviour, and it would also be of high interest to further explore how trust levels vary with factors such as age in the future. 

References:

Baumgartner, T., Heinrichs, M., Vonlanthen, A., Fischbacher, U., & Fehr, E. (2008). Oxytocin shapes the neural circuitry of trust and trust adaptation in humans. Neuron, [online] 58(4), 639-650. Available at: doi:10.1016/j.neuron.2008.04.009

Fett, A. J., Gromann, P. M., Giampietro, V., Shergill, S. S., & Krabbendam, L. (2014). Default distrust? An fmri investigation of the neural development of trust and cooperation. Social Cognitive and Affective Neuroscience, [online] 9(4), 395-402. doi:10.1093/scan/nss144

Koechlin, E., & Hyafil, A. (2007). Anterior prefrontal function and the limits of human decision-making. Science, [online] 318(5850), 594-598. doi:10.1126/science.1142995

Motzkin, J. C., Philippi, C. L., Wolf, R. C., Baskaya, M. K., & Koenigs, M. (2014). Ventromedial prefrontal cortex is critical for the regulation of Amygdala activity in humans. Biological Psychiatry, [online] 77(3), 276-284. doi:10.1016/j.biopsych.2014.02.014

Nishina, K., Takagishi, H., Fermin, A. S., Inoue-Murayama, M., Takahashi, H., Sakagami, M., & Yamagishi, T. (2018). Association of the oxytocin receptor gene with attitudinal trust: Role of amygdala volume. Social Cognitive and Affective Neuroscience. [online] 13(10), 1091-1097. Available from: doi:10.1093/scan/nsy075

Rilling, J. K., & Sanfey, A. G. (2011). The neuroscience of social decision-making. Annual Review of Psychology, [online] 62(1), 23-48. Available from: doi:10.1146/annurev.psych.121208.131647

Van den Bos, W., & Guroglu, B. (2009). The role of the Ventral medial prefrontal cortex in social decision making. Journal of Neuroscience, [online] 29(24), 7631-7632. Available from: doi:10.1523/jneurosci.1821-09.2009

Van den Bos, W., Van Dijk, E., Westenberg, M., Rombouts, S. A., & Crone, E. A. (2009). What motivates Repayment? Neural correlates of reciprocity in the trust game. Social Cognitive and Affective Neuroscience, [online] 4(3), 294-304. Available from: doi:10.1093/scan/nsp009

Wardle, M. C., Fitzgerald, D. A., Angstadt, M., Sripada, C. S., McCabe, K., & Luan Phan, K. (2013). The caudate signals bad reputation during trust decisions. PLoS ONE, [online] 8(6). Available from: doi:10.1371/journal.pone.0068884

Yi, L., Pan, J., Fan, Y., Zou, X., Wang, X., & Lee, K. (2013). Children with autism spectrum disorder are more trusting than typically developing children. Journal of Experimental Child Psychology, [online] 116(3), 755-761. Available from: doi:10.1016/j.jecp.2013.05.005

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