The dopaminergic reward system underpins gender differences in social preferences

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

Healthy decisions in the cued-attribute food choice paradigm have high test-retest reliability

Abstract Food choice paradigms are commonly used to study decision mechanisms, individual differences, and intervention efficacy. Here, we measured behavior from twenty-three healthy young adults who completed five repetitions of a cued-attribute food choice paradigm over two weeks. This task includes cues prompting participants to explicitly consider the healthiness of the food items before making a selection, or to choose naturally based on whatever freely comes to mind. We found that the average patterns of food choices following both cue types and ratings about the palatability (i.e. taste) and healthiness of the food items were similar across all five repetitions. At the individual level, the test-retest reliability for choices in both conditions and healthiness ratings was excellent. However, test-retest reliability for taste ratings was only fair, suggesting that estimates about palatability may vary more from day to day for the same individual

Transcranial stimulation over frontopolar cortex elucidates the choice attributes and neural mechanisms used to resolve exploration-exploitation trade-offs

Optimal behavior requires striking a balance between exploiting tried-and-true options or exploring new possibilities. Neuroimaging studies have identified different brain regions in humans where neural activity is correlated with exploratory or exploitative behavior, but it is unclear whether this activity directly implements these choices or simply reflects a byproduct of the behavior. Moreover, it remains unknown whether arbitrating between exploration and exploitation can be influenced with exogenous methods, such as brain stimulation. In our study, we addressed these questions by selectively upregulating and downregulating neuronal excitability with anodal or cathodal transcranial direct current stimulation over right frontopolar cortex during a reward-learning task. This caused participants to make slower, more exploratory or faster, more exploitative decisions, respectively. Bayesian computational modeling revealed that stimulation affected how much participants took both expected and obtained rewards into account when choosing to exploit or explore: Cathodal stimulation resulted in an increased focus on the option expected to yield the highest payout, whereas anodal stimulation led to choices that were less influenced by anticipated payoff magnitudes and were more driven by recent negative reward prediction errors. These findings suggest that exploration is triggered by a neural mechanism that is sensitive to prior less-than-expected choice outcomes and thus pushes people to seek out alternative courses of action. Together, our findings establish a parsimonious neurobiological mechanism that causes exploration and exploitation, and they provide new insights into the choice features used by this mechanism to direct decision-making

Dissociable mechanisms govern when and how strongly reward attributes affect decisions

Rewards usually have multiple attributes that are relevant for behavior. For instance, even apparently simple choices between liquid or food rewards involve comparisons of at least two attributes, flavor and amount. Thus, in order to make the best choice, an organism will need to take multiple attributes into account. Theories and models of decision making usually focus on how strongly different attributes are weighted in choice, e.g., as a function of their importance or salience to the decision-maker. However, when different attributes impact on the decision process is a question that has received far less attention. Although one may intuitively assume a systematic relationship between the weighting strength and the timing with which different attributes impact on the final choice, this relationship is untested. Here, we investigate whether attribute timing has a unique influence on decision making using a time-varying sequential sampling model (tSSM) and data from four separate experiments. Contrary to expectations, we find only a modest correlation between how strongly and how quickly reward attributes impact on choice. Experimental manipulations of attention and neural activity demonstrate that we can dissociate at the cognitive and neural levels the processes that determine the relative weighting strength and timing of attribute consideration. Our findings demonstrate that processes determining either the weighting strengths or the timing of attributes in decision making can adapt independently to changes in the environment or goals. Moreover, they show that a tSSM incorporating separable influences of these two sets of processes on choice improves understanding and predictions of individual differences in basic decision behavior and self-control

Dissociable mechanisms govern when and how strongly reward attributes affect decisions

Rewards usually have multiple attributes that are relevant for behavior. For instance, even apparently simple choices between liquid or food rewards involve comparisons of at least two attributes, flavor and amount. Thus, in order to make the best choice, an organism will need to take multiple attributes into account. Theories and models of decision making usually focus on how strongly different attributes are weighted in choice, e.g., as a function of their importance or salience to the decision-maker. However, when different attributes impact on the decision process is a question that has received far less attention. Although one may intuitively assume a systematic relationship between the weighting strength and the timing with which different attributes impact on the final choice, this relationship is untested. Here, we investigate whether attribute timing has a unique influence on decision making using a time-varying sequential sampling model (tSSM) and data from four separate experiments. Contrary to expectations, we find only a modest correlation between how strongly and how quickly reward attributes impact on choice. Experimental manipulations of attention and neural activity demonstrate that we can dissociate at the cognitive and neural levels the processes that determine the relative weighting strength and timing of attribute consideration. Our findings demonstrate that processes determining either the weighting strengths or the timing of attributes in decision making can adapt independently to changes in the environment or goals. Moreover, they show that a tSSM incorporating separable influences of these two sets of processes on choice improves understanding and predictions of individual differences in basic decision behavior and self-control

Dissociable mechanisms govern when and how strongly reward attributes affect decisions

Theories and computational models of decision-making usually focus on how strongly different attributes are weighted in choice, for example, as a function of their importance or salience to the decision-maker. However, when different attributes affect the decision process is a question that has received far less attention. Here, we investigated whether the timing of attribute consideration has a unique influence on decision-making by using a time-varying drift diffusion model and data from four separate experiments. Experimental manipulations of attention and neural activity demonstrated that we can dissociate the processes that determine the relative weighting strength and timing of attribute consideration. Thus, the processes determining either the weighting strengths or the timing of attributes in decision-making can independently adapt to changes in the environment or goals. Quantifying these separate influences of timing and weighting on choice improves our understanding and predictions of individual differences in decision behaviour

Computational modeling of resting-state activity demonstrates markers of normalcy in children with prenatal or perinatal stroke

Children who sustain a prenatal or perinatal brain injury intheform of a stroke develop remarkably normal cognitivefunctions in certain areas, with a particular strength in language skills. A dominant explanation for this is that brain regions from the contralesional hemisphere “take over” their functions, whereas the damaged areas and other ipsilesional regions play much less of a role. However, it is difficult to tease apart whether changes in neural activity after early brain injury are due to damage caused by the lesion or by processes related to postinjury reorganization. We sought to differentiate between these two causes by investigating the functional connectivity (FC) of brain areas during the resting state in human children with early brain injury using a computational model. We simulated a large-scale network consisting of realistic models of local brain areas coupled through anatomical connectivity information of healthy and injured participants. We then compared the resulting simulated FC values of healthy and injured participants with the empirical ones. We found that the empirical connectivity values, especially of the damaged areas, correlated better with simulated values of a healthy brain than those of an injured brain. This result indicates that the structural damage caused by an early brain injury is unlikely to have an adverse and sustained impact on the functional connections, albeit during the resting state, of damaged areas. Therefore, these areas could continue to play a role in the development of near-normal function in certain domains such as language in these children.M.H.A. and G.D. weresupported bythe European Research Council(Advanced Grant DYSTRUCTURE 295129). The imaging data analyzed in this study were obtained as part of a project at The University of Chicago in language development that was supported by the National Institute of Child Health and Human Development–National Institutes of Health (Grant P01 HD040605). Their support is gratefully acknowledged, as is the help of our coinvestigators on that grant, Susan Goldin-Meadow and Susan Cohen Levine, and our research assistant, Victoria Li. The authors declare no competing financial interest