The dopaminergic reward system underpins gender differences in social preferences

Soutschek, A., Burke, C. J., Beharelle, A. R., Schreiber, R., Weber, S. C., Karipidis, I. I., Ten Velden, J., Weber, B., Haker, H., Kalenscher, T., & Tobler, P. N. (2017). The dopaminergic reward system underpins gender differences in social preferences. Nature Human Behaviour, 1, 819-827. doi:10.1038/s41562-017-0226-y.
Women are known to have stronger prosocial preferences than men, but it remains an open question as to how these behavioural differences arise from differences in brain functioning. Here, we provide a neurobiological account for the hypothesized gender difference. In a pharmacological study and an independent neuroimaging study, we tested the hypothesis that the neural reward system encodes the value of sharing money with others more strongly in women than in men. In the pharmacological study, we reduced receptor type-specific actions of dopamine, a neurotransmitter related to reward processing, which resulted in more selfish decisions in women and more prosocial decisions in men. Converging findings from an independent neuroimaging study revealed gender-related activity in neural reward circuits during prosocial decisions. Thus, the neural reward system appears to be more sensitive to prosocial rewards in women than in men, providing a neurobiological account for why women often behave more prosocially than men. A large body of evidence suggests that women are often more prosocial (for example, generous, altruistic and inequality averse) than men, at least when other factors such as reputation and strategic considerations are excluded1,2,3. This dissociation could result from cultural expectations and gender stereotypes, because in Western societies women are more strongly expected to be prosocial4,5,6 and sensitive to variations in social context than men1. It remains an open question, however, whether and how on a neurobiological level the social preferences of women and men arise from differences in brain functioning. The assumption of gender differences in social preferences predicts that the neural reward system’s sensitivity to prosocial and selfish rewards should differ between women and men. Specifically, the hypothesis would be that the neural reward system is more sensitive to prosocial than selfish rewards in women and more sensitive to selfish than prosocial rewards in men. The goal of the current study was to test in two independent experiments for the hypothesized gender differences on both a pharmacological and a haemodynamic level. In particular, we examined the functions of the neurotransmitter dopamine using a dopamine receptor antagonist, and the role of the striatum (a brain region strongly innervated by dopamine neurons) during social decision-making in women and men using neuroimaging. The neurotransmitter dopamine is thought to play a key role in neural reward processing7,8. Recent evidence suggests that dopaminergic activity is sensitive not only to rewards for oneself but to rewards for others as well9. The assumption that dopamine is sensitive to both self- and other-related outcomes is consistent with the finding that the striatum shows activation for both selfish and shared rewards10,11,12,13,14,15. The dopaminergic response may represent a net signal encoding the difference between the value of preferred and unpreferred rewards8. Regarding the hypothesized gender differences in social preferences, this account makes the following predictions. If women prefer shared (prosocial) outcomes2, women’s dopaminergic signals to shared rewards will be stronger than to non-shared (selfish) rewards, so reducing dopaminergic activity should bias women to make more selfish decisions. In line with this hypothesis, a functional imaging study reported enhanced striatal activation in female participants during charitable donations11. In contrast, if men prefer selfish over prosocial rewards, dopaminergic activity should be enhanced to selfish compared to prosocial rewards. In line with this view, upregulating dopaminergic activity in a sample of exclusively male participants increased selfish behaviour in a bargaining game16. Thus, contrary to the hypothesized effect in women, reducing dopaminergic neurotransmission should render men more prosocial. Taken together, the current study tested the following three predictions: we expected the dopaminergic reward system (1) to be more sensitive to prosocial than selfish rewards in women and (2) to be more sensitive to selfish than prosocial rewards in men. As a consequence of these two predictions, we also predicted (3) dopaminoceptive regions such as the striatum to show stronger activation to prosocial relative to selfish rewards in women than in men. To test these predictions, we conducted a pharmacological study in which we reduced dopaminergic neurotransmission with amisulpride. Amisulpride is a dopamine antagonist that is highly specific for dopaminergic D2/D3 receptors17. After receiving amisulpride or placebo, participants performed an interpersonal decision task18,19,20, in which they made choices between a monetary reward only for themselves (selfish reward option) and sharing money with others (prosocial reward option). We expected that blocking dopaminergic neurotransmission with amisulpride, relative to placebo, would result in fewer prosocial choices in women and more prosocial choices in men. To investigate whether potential gender-related effects of dopamine are selective for social decision-making, we also tested the effects of amisulpride on time preferences in a non-social control task that was matched to the interpersonal decision task in terms of choice structure. In addition, because dopaminergic neurotransmission plays a crucial role in brain regions involved in value processing, such as the striatum21, a gender-related role of dopaminergic activity for social decision-making should also be reflected by dissociable activity patterns in the striatum. Therefore, to further test our hypothesis, we investigated the neural correlates of social decision-making in a functional imaging study. In line with our predictions for the pharmacological study, we expected to find stronger striatum activity during prosocial relative to selfish decisions in women, whereas men should show enhanced activity in the striatum for selfish relative to prosocial choices.
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