Belief updating during social interactions: neural dynamics and causal role of dorsomedial prefrontal cortex.

In competitive interactions, humans have to flexibly update their beliefs about another person's intentions in order to adjust their own choice strategy, such as when believing that the other may exploit their cooperativeness. Here we investigate both the neural dynamics and the causal neural substrate of belief updating processes in humans. We used an adapted prisoner's dilemma task in which participants explicitly predicted the co-player's actions, which allowed us to quantify the prediction error between expected and actual behaviour. First, in a EEG experiment we found a stronger medial frontal negativity (MFN) for negative than positive prediction errors, suggesting that this medial-frontal ERP component may encode unexpected defection of the co-player. The MFN also predicted subsequent belief updating after negative prediction errors. In a second experiment we used transcranial magnetic stimulation (TMS) to investigate whether the dorsomedial prefrontal cortex (dmPFC) causally implements belief updating after unexpected outcomes. Our results show that dmPFC TMS impaired belief updating and strategic behavioural adjustments after negative prediction errors. Taken together, our findings reveal the time-course of the use of prediction errors in social decisions, and suggest that the dmPFC plays a crucial role in updating mental representations of others' intentions.Significance statement For successful social interactions, humans must be able to reliably predict their interaction partners' actions. Previous research has linked this capacity mainly to posterior regions involved in mentalizing. Here, we show that the prefrontal cortex also plays a crucial role for adjusting our beliefs about others' cooperativeness as well: Inhibiting the dorsomedial prefrontal cortex with brain stimulation impaired the ability to modify expectations about the interaction partner's willingness to cooperate. Our findings highlight the role of belief updating for strategic social interactions, and identify the dorsomedial prefrontal cortex and its underlying neural dynamics as neural substrate of the ability to successfully learn others' strategies.

Neural reward representations enable utilitarian welfare maximization.

From deciding which meal to prepare for our guests to trading-off the pro-environmental effects of climate protection measures against their economic costs, we often must consider the consequences of our actions for the well-being of others (welfare). Vexingly, the tastes and views of others can vary widely. To maximize welfare according to the utilitarian philosophical tradition, decision makers facing conflicting preferences of others should choose the option that maximizes the sum of subjective value (utility) of the entire group. This notion requires comparing intensities of preferences across individuals. However, it remains unclear whether such comparisons are possible at all, and (if they are possible) how they might be implemented in the brain. Here, we show that female and male participants can both learn the preferences of others by observing their choices, and represent these preferences on a common scale to make utilitarian welfare decisions. On the neural level, multivariate support vector regressions revealed that a distributed activity pattern in the ventromedial prefrontal cortex (VMPFC), a brain region previously associated with reward processing, represented preference strength of others. Strikingly, also the utilitarian welfare of others was represented in the VMPFC and relied on the same neural code as the estimated preferences of others. Together, our findings reveal that humans can behave as if they maximized utilitarian welfare using a specific utility representation and that the brain enables such choices by repurposing neural machinery processing the reward others receive.Significance statement In many situations politicians and civilians strive to maximize the welfare of social groups. If the preferences of group members are in conflict, identifying the utilitarian welfare-maximizing option requires that decision makers can compare the strengths of conflicting preferences on a common scale. Yet, there is a fundamental lack of understanding which brain mechanisms enable such comparisons of conflicting utilities. Here, we show that brain regions involved in reward processing compute welfare comparisons by representing the preferences of others with a common neural code. This provides a neurobiological mechanism to compute utilitarian welfare maximization as desired by moral philosophy in the Humean tradition.

Causal roles of prefrontal and temporo-parietal theta oscillations for inequity aversion.

The right temporo-parietal junction (rTPJ) and the right lateral prefrontal cortex (rLPFC) are known to play prominent roles in human social behaviour. However, it remains unknown which brain rhythms in these regions contribute to trading-off fairness norms against selfish interests as well as whether the influence of these oscillations depends on whether fairness violations are advantageous or disadvantageous for a decision maker. To answer these questions, we used non-invasive transcranial alternating current stimulation (tACS) to determine which brain rhythms in rTPJ and rLPFC are causally involved in moderating aversion to advantageous and disadvantageous inequity. Our results show that theta oscillations in rTPJ strengthen the aversion to unequal splits, which is statistically mediated by the rTPJ's role for perspective taking. In contrast, theta tACS over rLPFC enhanced the preference for outcome-maximizing unequal choices more strongly for disadvantageous compared to advantageous outcome distributions. Taken together, we provide evidence that neural oscillations in rTPJ and rLPFC have distinct causal roles in implementing inequity aversion, which can be explained by their involvement in distinct psychological processes.

Toward a Unifying Account of Dopamine's Role in Cost-Benefit Decision Making.

Dopamine is thought to play a crucial role in cost-benefit decision making, but so far there is no consensus on the precise role of dopamine in decision making. Here, we review the literature on dopaminergic manipulations of cost-benefit decision making in humans and evaluate how well different theoretical accounts explain the existing body of evidence. Reduced D2 stimulation tends to increase the willingness to bear delay and risk costs (i.e., wait for later rewards, take riskier options), while increased D1 and D2 receptor stimulation increases willingness to bear effort costs. We argue that the empirical findings can best be explained by combining the strengths of two theoretical accounts: in cost-benefit decision making, dopamine may play a dual role both in promoting the pursuit of psychologically close options (e.g., sooner and safer rewards) and in computing which costs are acceptable for a reward at stake. Moreover, we identify several limiting factors in the study designs of previous investigations that prevented a fuller understanding of dopamine's role in value-based choice. Together, the proposed theoretical framework and the methodological suggestions for future studies may bring us closer to a unifying account of dopamine in healthy and impaired cost-benefit decision making.

Social metacognition drives willingness to commit.

Showing or telling others that we are committed to cooperate with them can boost social cooperation. But what makes us willing to signal our cooperativeness, when it is costly to do so? In two experiments, we tested the hypothesis that agents engage in social commitments if their subjective confidence in predicting the interaction partner's behavior is low. In Experiment 1 (preregistered), 48 participants played a prisoner's dilemma game where they could signal their intentions to their co-player by enduring a monetary cost. As hypothesized, low confidence in one's prediction of the co-player's intentions was associated with a higher willingness to engage in costly commitment. In Experiment 2 (31 participants), we replicate these findings and moreover provide causal evidence that experimentally lowering the predictability of others' actions (and thereby confidence in these predictions) motivates commitment decisions. Finally, across both experiments, we show that participants possess and demonstrate metacognitive access to the accuracy of their mentalizing processes. Taken together, our findings shed light on the importance of confidence representations and metacognitive processes in social interactions. (PsycInfo Database Record (c) 2023 APA, all rights reserved).

A process model account of the role of dopamine in intertemporal choice.

Theoretical accounts disagree on the role of dopamine in intertemporal choice and assume that dopamine either promotes delay of gratification by increasing the preference for larger rewards or that dopamine reduces patience by enhancing the sensitivity to waiting costs. Here, we reconcile these conflicting accounts by providing empirical support for a novel process model according to which dopamine contributes to two dissociable components of the decision process, evidence accumulation and starting bias. We re-analyzed a previously published data set where intertemporal decisions were made either under the D2 antagonist amisulpride or under placebo by fitting a hierarchical drift diffusion model that distinguishes between dopaminergic effects on the speed of evidence accumulation and the starting point of the accumulation process. Blocking dopaminergic neurotransmission not only strengthened the sensitivity to whether a reward is perceived as worth the delay costs during evidence accumulation (drift rate) but also attenuated the impact of waiting costs on the starting point of the evidence accumulation process (bias). In contrast, re-analyzing data from a D1 agonist study provided no evidence for a causal involvement of D1R activation in intertemporal choices. Taken together, our findings support a novel, process-based account of the role of dopamine for cost-benefit decision making, highlight the potential benefits of process-informed analyses, and advance our understanding of dopaminergic contributions to decision making.

Metacognitive deficits are associated with lower sensitivity to preference reversals in nicotine dependence.

Deficits in impulse control belong to the core profile of nicotine dependence. Smokers might thus benefit from voluntarily self-restricting their access to the immediate temptation of nicotine products (precommitment) in order to avoid impulse control failures. However, little is known about how smokers' willingness to engage in voluntary self-restrictions is determined by metacognitive insight into their general preferences for immediate over delayed rewards. Here, with a series of monetary intertemporal choice tasks, we provide empirical evidence for reduced metacognitive accuracy in smokers relative to non-smokers and show that smokers overestimate the subjective value of delayed rewards relative to their revealed preferences. In line with the metacognitive deficits, smokers were also less sensitive to the risk of preference reversals when deciding whether or not to restrict their access to short-term financial rewards. Taken together, the current findings suggest that deficits not only in impulse control but also in metacognition may hamper smokers' resistance to immediate rewards and capacity to pursue long-term goals.

Causal role of right dorsolateral prefrontal cortex for norm-guided social decision making: A meta-analysis of TMS studies.

Theoretical accounts ascribe the right dorsolateral prefrontal cortex (rDLPFC) a crucial role in social decision making, but previous studies assessing the rDLPFC's function with transcranial magnetic stimulation (TMS) provided inconsistent evidence. While some studies suggest that the rDLPFC promotes norm-guided behavior, others report the rDLPFC to implement selfish choices. To decide between these conflicting accounts, we conducted a meta-analysis of studies that investigated the impact of rDLPFC TMS on social decision making. While we observed no significant effect of rDLPFC TMS across all studies, moderator analyses revealed that the rDLPFC's role in social decision making crucially depends on the social context: in particular, we found that rDLPFC promotes norm-guided behavior predominantly when decision makers have to trade-off their interaction partners' intentions and fairness expectations against their selfish interests (reactive fairness). In contrast, there was no evidence that rDLPFC TMS affects prosocial giving (proactive fairness). Our results thus inform theoretical accounts by showing that brain stimulation over rDLPFC does not increase or decrease norm-guided behavior per se; instead, contextual factors determine the role of the rDLPFC in social interactions.

Learning from Ingroup Experiences Changes Intergroup Impressions.

Humans form impressions toward individuals of their own social groups (ingroup members) and of different social groups (outgroup members). Outgroup-focused theories predict that intergroup impressions are mainly shaped by experiences with outgroup individuals, while ingroup-focused theories predict that ingroup experiences play a dominant role. Here we test predictions from these two psychological theories by estimating how intergroup impressions are dynamically shaped when people learn from both ingroup and outgroup experiences. While undergoing fMRI, male participants had identical experiences with different ingroup or outgroup members and rated their social closeness and impressions toward the ingroup and the outgroup. Behavioral results showed an initial ingroup bias in impression ratings which was significantly reduced over the course of learning, with larger effects in individuals with stronger ingroup identification. Computational learning models revealed that these changes in intergroup impressions were predicted by the weight given to ingroup prediction errors. Neurally, the individual weight for ingroup prediction errors was related to the coupling between the left inferior parietal lobule and the left anterior insula, which, in turn, predicted learning-related changes in intergroup impressions. Our findings provide computational and neural evidence for ingroup-focused theories, highlighting the importance of ingroup experiences in shaping social impressions in intergroup settings.Significance Statement:Living in multicultural societies, humans interact with individuals of their own social groups (ingroup members) and of different social groups (outgroup members). However, little is known about how people learn from the mixture of ingroup and outgroup interactions, the most natural experiences in current societies. Here, participants had identical, intermixed experiences with different ingroup and outgroup individuals and rated their closeness and impressions toward the ingroup and the outgroup. Combining computational models and fMRI, we find that the weight given to ingroup experiences (ingroup prediction errors) is the main source of intergroup impression change, captured by changes in connectivity between the parietal lobe and insula. These findings highlight the importance of ingroup experiences in shaping intergroup impressions in complex social environments.

Brain stimulation over dorsomedial prefrontal cortex modulates effort-based decision making.

Deciding whether to engage in strenuous mental activities requires trading-off the potential benefits against the costs of mental effort, but it is unknown which brain rhythms are causally involved in such cost-benefit calculations. We show that brain stimulation targeting midfrontal theta oscillations increases the engagement in goal-directed mental effort. Participants received transcranial alternating current stimulation over dorsomedial prefrontal cortex while deciding whether they are willing to perform a demanding working memory task for monetary rewards. Midfrontal theta tACS increased the willingness to exert mental effort for rewards while leaving working memory performance unchanged. Computational modelling using a hierarchical Bayesian drift diffusion model suggests that theta tACS shifts the starting bias before evidence accumulation towards high reward-high effort options without affecting the velocity of the evidence accumulation process. Our findings suggest that the motivation to engage in goal-directed mental effort can be increased via midfrontal tACS.

Reconciling psychological and neuroscientific accounts of reduced motivation in aging.

Motivation is a hallmark of healthy aging, but the motivation to engage in effortful behavior diminishes with increasing age. Most neurobiological accounts of altered motivation in older adults assume that these deficits are caused by a gradual decline in brain tissue, while some psychological theories posit a switch from gain orientation to loss avoidance in motivational goals. Here, we contribute to reconcile the psychological and neural perspectives by providing evidence that the frontopolar cortex (FPC), a brain region involved in cost-benefit weighting, increasingly underpins effort avoidance rather than engagement with age. Using anodal transcranial direct current stimulation together with effort-reward trade-offs, we find that the FPC's function in effort-based decisions remains focused on cost-benefit calculations but appears to switch from reward-seeking to cost avoidance with increasing age. This is further evidenced by the exploratory, independent analysis of structural brain changes, showing that the relationship between the density of the frontopolar neural tissue and the willingness to exert effort differs in young vs older adults. Our results inform aging-related models of decision-making by providing preliminary evidence that, in addition to cortical thinning, changes in goal orientation need to be considered in order to understand alterations in decision-making over the life span.

Opioid antagonism modulates wanting-related frontostriatal connectivity.

Theoretical accounts distinguish between motivational ('wanting') and hedonic ('liking') dimensions of rewards. Previous animal and human research linked wanting and liking to anatomically and neurochemically distinct brain mechanisms, but it remains unknown how the different brain regions and neurotransmitter systems interact in processing distinct reward dimensions. Here, we assessed how pharmacological manipulations of opioid and dopamine receptor activation modulate the neural processing of wanting and liking in humans in a randomized, placebo-controlled, double-blind clinical trial. Reducing opioid receptor activation with naltrexone selectively reduced wanting of rewards, which on a neural level was reflected by stronger coupling between dorsolateral prefrontal cortex and the striatum under naltrexone compared with placebo. In contrast, reducing dopaminergic neurotransmission with amisulpride revealed no robust effects on behavior or neural activity. Our findings thus provide insights into how opioid receptors mediate neural connectivity related to specifically motivational, not hedonic, aspects of rewards.

Effects of a virtual gender swap on social and temporal decision-making.

Mounting evidence has demonstrated that embodied virtual reality, during which physical bodies are replaced with virtual surrogates, can strongly alter cognition and behavior even when the virtual body radically differs from one's own. One particular emergent area of interest is the investigation of how virtual gender swaps can influence choice behaviors. Economic decision-making paradigms have repeatedly shown that women tend to display more prosocial sharing choices than men. To examine whether a virtual gender swap can alter gender-specific differences in prosociality, 48 men and 51 women embodied either a same- or different-gender avatar in immersive virtual reality. In a between-subjects design, we differentiated between specifically social and non-social decision-making by means of a virtually administered interpersonal and intertemporal discounting task, respectively. We hypothesized that a virtual gender swap would elicit social behaviors that stereotypically align with the gender of the avatar. To relate potential effects to changes in self-perception, we also measured implicit and explicit identification with gendered (or gender-typical) traits prior to and following the virtual experience, and used questionnaires that assessed the strength of the illusion. Contrary to our hypothesis, our results show that participants made less prosocial decisions (i.e., became more selfish) in different-gender avatars, independent of their own biological sex. Moreover, women embodying a male avatar in particular were more sensitive to temptations of immediate rewards. Lastly, the manipulation had no effects on implicit and explicit identification with gendered traits. To conclude, while we showed that a virtual gender swap indeed alters decision-making, gender-based expectancies cannot account for all the task-specific interpersonal and intertemporal changes following the virtual gender swap.

Frontopolar theta oscillations link metacognition with prospective decision making.

Prospective decision making considers the future consequences of actions and therefore requires agents to represent their present subjective preferences reliably across time. Here, we test the link of frontopolar theta oscillations to both metacognitive ability and prospective choice behavior. We target these oscillations with transcranial alternating current stimulation while participants make decisions between smaller-sooner and larger-later monetary rewards and rate their choice confidence after each decision. Stimulation designed to enhance frontopolar theta oscillations increases metacognitive accuracy in reports of subjective uncertainty in intertemporal decisions. Moreover, the stimulation also enhances the willingness of participants to restrict their future access to short-term gratification by strengthening the awareness of potential preference reversals. Our results suggest a mechanistic link between frontopolar theta oscillations and metacognitive knowledge about the stability of subjective value representations, providing a potential explanation for why frontopolar cortex also shields prospective decision making against future temptation.

The role of oxytocin in delay of gratification and flexibility in non-social decision making.

Oxytocin is well-known for its impact on social cognition. This specificity for the social domain, however, has been challenged by findings suggesting a domain-general allostatic function for oxytocin by promoting future-oriented and flexible behavior. In this pre-registered study, we tested the hypothesized domain-general function of oxytocin by assessing the impact of intranasal oxytocin (24 IU) on core aspects of human social (inequity aversion) and non-social decision making (delay of gratification and cognitive flexibility) in 49 healthy volunteers (within-subject design). In intertemporal choice, patience was higher under oxytocin than under placebo, although this difference was evident only when restricting the analysis to the first experimental session (between-group comparison) due to carry-over effects. Further, oxytocin increased cognitive flexibility in reversal learning as well as generosity under conditions of advantageous but not disadvantageous inequity. Our findings show that oxytocin affects both social and non-social decision making, supporting theoretical accounts of domain-general functions of oxytocin.

The right temporoparietal junction enables delay of gratification by allowing decision makers to focus on future events.

Studies of neural processes underlying delay of gratification usually focus on prefrontal networks related to curbing affective impulses. Here, we provide evidence for an alternative mechanism that facilitates delaying gratification by mental orientation towards the future. Combining continuous theta-burst stimulation (cTBS) with functional neuroimaging, we tested how the right temporoparietal junction (rTPJ) facilitates processing of future events and thereby promotes delay of gratification. Participants performed an intertemporal decision task and a mental time-travel task in the MRI scanner before and after receiving cTBS over the rTPJ or the vertex (control site). rTPJ cTBS led to both stronger temporal discounting for longer delays and reduced processing of future relative to past events in the mental time-travel task. This finding suggests that the rTPJ contributes to the ability to delay gratification by facilitating mental representation of outcomes in the future. On the neural level, rTPJ cTBS led to a reduction in the extent to which connectivity of rTPJ with striatum reflected the value of delayed rewards, indicating a role of rTPJ-striatum connectivity in constructing neural representations of future rewards. Together, our findings provide evidence that the rTPJ is an integral part of a brain network that promotes delay of gratification by facilitating mental orientation to future rewards.

Causal role of lateral prefrontal cortex in mental effort and fatigue.

Dorsolateral prefrontal cortex (DLPFC) is well-known for its role in exerting mental work, however the contribution of DLPFC for deciding whether or not to engage in effort remains unknown. Here, we assessed the causal role of DLPFC in effort-based decision making. We disrupted functioning of DLPFC with noninvasive brain stimulation before participants repeatedly decided whether to exert mental effort in a working memory task. We found the same DLPFC subregion involved in mental effort exertion to influence also effort-based decisions: First, it enhanced effort discounting, suggesting that DLPFC may signal the capacity to successfully deal with effort demands. Second, a novel computational model integrating the costs of enduring effort into the effort-based decision process revealed that DLPFC disruption reduced fatigue after accumulated effort exertion, linking DLPFC activation with fatigue. Together, our findings indicate that in effort-based decisions DLPFC represents the capacity to exert mental effort and the updating of this information with enduring time-on-task, informing theoretical accounts on the role of DLPFC in the motivation to exert mental effort and the fatigue arising from it.

Know your weaknesses: Sophisticated impulsiveness motivates voluntary self-restrictions.

Restricting one's access to temptations (precommitment) facilitates the achievement of long-term goals. The sophisticated impulsiveness model of precommitment posits that impulsive agents who are aware that they are impulsive should show the strongest preference for precommitment. Empirically however, two central predictions of this theoretical notion remained untested: whether impulsiveness causally drives the demand for precommitment and whether the willingness to precommit depends on metacognitive awareness of one's impulsiveness. Here, we tested these predictions in three independent experiments. Participants performed a delay discounting task in which they could precommit to larger-later rewards. The results of Experiment 1 provide causal evidence that reducing impulse control capacities increases precommitment demand. Moreover, Experiments 2 and 3 support the hypothesis that metacognitive awareness of one's impulsiveness moderates the relationship between impulsiveness and precommitment. Together, our data put the sophisticated impulsiveness model of precommitment on strong empirical foundations. (PsycInfo Database Record (c) 2020 APA, all rights reserved).

Activation of D1 receptors affects human reactivity and flexibility to valued cues.

Reward-predicting cues motivate goal-directed behavior, but in unstable environments humans must also be able to flexibly update cue-reward associations. While the capacity of reward cues to trigger motivation ('reactivity') as well as flexibility in cue-reward associations have been linked to the neurotransmitter dopamine in humans, the specific contribution of the dopamine D1 receptor family to these behaviors remained elusive. To fill this gap, we conducted a randomized, placebo-controlled, double-blind pharmacological study testing the impact of three different doses of a novel D1 agonist (relative to placebo) on reactivity to reward-predicting cues (Pavlovian-to-instrumental transfer) and flexibility of cue-outcome associations (reversal learning). We observed that the impact of the D1 agonist crucially depended on baseline working memory functioning, which has been identified as a proxy for baseline dopamine synthesis capacity. Specifically, increasing D1 receptor stimulation strengthened Pavlovian-to-instrumental transfer in individuals with high baseline working memory capacity. In contrast, higher doses of the D1 agonist improved reversal learning only in individuals with low baseline working memory functioning. Our findings suggest a crucial and baseline-dependent role of D1 receptor activation in controlling both cue reactivity and the flexibility of cue-reward associations.

Dopaminergic D1 Receptor Stimulation Affects Effort and Risk Preferences.

BACKGROUND: Activation of D1 receptors has been related to successful goal-directed behavior, but it remains unclear whether D1 receptor activation causally tips the balance of weighing costs and benefits in humans. Here, we tested the impact of pharmacologically stimulated D1 receptors on sensitivity to risk, delay, and effort costs in economic choice and investigated whether D1 receptor stimulation would bias preferences toward options with increased costs in a cost-specific manner. METHODS: In a randomized, double-blind, placebo-controlled, parallel-group phase 1 study, 120 healthy young volunteers received either placebo or 1 of 3 doses (6 mg, 15 mg, or 30 mg) of a novel, selective D1 agonist (PF-06412562). After drug administration, participants performed decision tasks measuring their preferences for risky, delayed, and effortful outcomes. RESULTS: Higher doses of the D1 agonist increased the willingness to exert physical effort for reward as well as reduced the preference for risky outcomes. We observed no effects on preferences for delayed rewards. CONCLUSIONS: The current results provide evidence that D1 receptor stimulation causally affects core aspects of cost-benefit decision making in humans.