Accounting for Taste: A Multi-Attribute Neurocomputational Model Explains the Neural Dynamics of Choices for Self and Others.

How do we make choices for others with different preferences from our own? Although neuroimaging studies implicate similar circuits in representing preferences for oneself and others, some models propose that additional corrective mechanisms come online when choices for others diverge from one's own preferences. Here we used event-related potentials (ERPs) in humans, in combination with computational modeling, to examine how social information is integrated in the time leading up to choices for oneself and others. Hungry male and female participants with unrestricted diets selected foods for themselves, a similar unrestricted eater, and a dissimilar, self-identified healthy eater. Across choices for both oneself and others, ERP value signals emerged within the same time window but differentially reflected taste and health attributes based on the recipient's preferences. Choices for the dissimilar recipient were associated with earlier activity localized to brain regions implicated in social cognition, including temporoparietal junction. Finally, response-locked analysis revealed a late ERP component specific to choices for the similar recipient, localized to the parietal lobe, that appeared to reflect differences in the response threshold based on uncertainty. A multi-attribute computational model supported the link between specific ERP components and distinct model parameters, and was not significantly improved by adding time-dependent dual processes. Model simulations suggested that longer response times previously associated with effortful correction may alternatively arise from higher choice uncertainty. Together, these results provide a parsimonious neurocomputational mechanism for social decision-making, additionally explaining divergent patterns of choice and response time data in decisions for oneself and others.SIGNIFICANCE STATEMENT How do we choose for others, particularly when they have different preferences? Whereas some studies suggest that similar neural circuits underlie decision-making for oneself and others, others argue for additional, slower perspective-taking mechanisms. Combining event-related potentials with computational modeling, we found that integration of others' preferences occurs over the same timescale as for oneself while differentially tracking recipient-relevant attributes. Although choosing for others took longer and produced differences in late-emerging neural responses, computational modeling attributed these patterns to greater response caution rather than egocentric bias correction. Computational simulations also correctly predicted when and why choosing differently for others takes longer, suggesting that a model incorporating value integration and evidence accumulation can parsimoniously account for complex patterns in social decision-making.

Reason's Enemy Is Not Emotion: Engagement of Cognitive Control Networks Explains Biases in Gain/Loss Framing.

In the classic gain/loss framing effect, describing a gamble as a potential gain or loss biases people to make risk-averse or risk-seeking decisions, respectively. The canonical explanation for this effect is that frames differentially modulate emotional processes, which in turn leads to irrational choice behavior. Here, we evaluate the source of framing biases by integrating functional magnetic resonance imaging data from 143 human participants performing a gain/loss framing task with meta-analytic data from >8000 neuroimaging studies. We found that activation during choices consistent with the framing effect were most correlated with activation associated with the resting or default brain, while activation during choices inconsistent with the framing effect was most correlated with the task-engaged brain. Our findings argue against the common interpretation of gain/loss framing as a competition between emotion and control. Instead, our study indicates that this effect results from differential cognitive engagement across decision frames.SIGNIFICANCE STATEMENT The biases frequently exhibited by human decision makers have often been attributed to the presence of emotion. Using a large fMRI sample and analysis of whole-brain networks defined with the meta-analytic tool Neurosynth, we find that neural activity during frame-biased decisions was more significantly associated with default behaviors (and the absence of executive control) than with emotion. These findings point to a role for neuroscience in shaping long-standing psychological theories in decision science.

Translating upwards: linking the neural and social sciences via neuroeconomics.

The social and neural sciences share a common interest in understanding the mechanisms that underlie human behaviour. However, interactions between neuroscience and social science disciplines remain strikingly narrow and tenuous. We illustrate the scope and challenges for such interactions using the paradigmatic example of neuroeconomics. Using quantitative analyses of both its scientific literature and the social networks in its intellectual community, we show that neuroeconomics now reflects a true disciplinary integration, such that research topics and scientific communities with interdisciplinary span exert greater influence on the field. However, our analyses also reveal key structural and intellectual challenges in balancing the goals of neuroscience with those of the social sciences. To address these challenges, we offer a set of prescriptive recommendations for directing future research in neuroeconomics.

Decoding the anatomical network of spatial attention.

The study of stroke patients with modern lesion-symptom analysis techniques has yielded valuable insights into the representation of spatial attention in the human brain. Here we introduce an approach--multivariate pattern analysis--that no longer assumes independent contributions of brain regions but rather quantifies the joint contribution of multiple brain regions in determining behavior. In a large sample of stroke patients, we found patterns of damage more predictive of spatial neglect than the best-performing single voxel. In addition, modeling multiple brain regions--those that are frequently damaged and, importantly, spared--provided more predictive information than modeling single regions. Interestingly, we also found that the superior temporal gyrus demonstrated a consistent ability to improve classifier performance when added to other regions, implying uniquely predictive information. In sharp contrast, classifier performance for both the angular gyrus and insular cortex was reliably enhanced by the addition of other brain regions, suggesting these regions lack independent predictive information for spatial neglect. Our findings highlight the utility of multivariate pattern analysis in lesion mapping, furnishing neuroscience with a modern approach for using lesion data to study human brain function.

Ventromedial prefrontal cortex encodes emotional value.

The ventromedial prefrontal cortex (vmPFC) plays a critical role in processing appetitive stimuli. Recent investigations have shown that reward value signals in the vmPFC can be altered by emotion regulation processes; however, to what extent the processing of positive emotion relies on neural regions implicated in reward processing is unclear. Here, we investigated the effects of emotion regulation on the valuation of emotionally evocative images. Two independent experimental samples of human participants performed a cognitive reappraisal task while undergoing fMRI. The experience of positive emotions activated the vmPFC, whereas the regulation of positive emotions led to relative decreases in vmPFC activation. During the experience of positive emotions, vmPFC activation tracked participants' own subjective ratings of the valence of stimuli. Furthermore, vmPFC activation also tracked normative valence ratings of the stimuli when participants were asked to experience their emotions, but not when asked to regulate them. A separate analysis of the predictive power of vmPFC on behavior indicated that even after accounting for normative stimulus ratings and condition, increased signal in the vmPFC was associated with more positive valence ratings. These results suggest that the vmPFC encodes a domain-general value signal that tracks the value of not only external rewards, but also emotional stimuli.

Characterizing individual differences in functional connectivity using dual-regression and seed-based approaches.

A central challenge for neuroscience lies in relating inter-individual variability to the functional properties of specific brain regions. Yet, considerable variability exists in the connectivity patterns between different brain areas, potentially producing reliable group differences. Using sex differences as a motivating example, we examined two separate resting-state datasets comprising a total of 188 human participants. Both datasets were decomposed into resting-state networks (RSNs) using a probabilistic spatial independent component analysis (ICA). We estimated voxel-wise functional connectivity with these networks using a dual-regression analysis, which characterizes the participant-level spatiotemporal dynamics of each network while controlling for (via multiple regression) the influence of other networks and sources of variability. We found that males and females exhibit distinct patterns of connectivity with multiple RSNs, including both visual and auditory networks and the right frontal-parietal network. These results replicated across both datasets and were not explained by differences in head motion, data quality, brain volume, cortisol levels, or testosterone levels. Importantly, we also demonstrate that dual-regression functional connectivity is better at detecting inter-individual variability than traditional seed-based functional connectivity approaches. Our findings characterize robust-yet frequently ignored-neural differences between males and females, pointing to the necessity of controlling for sex in neuroscience studies of individual differences. Moreover, our results highlight the importance of employing network-based models to study variability in functional connectivity.

A computational account of how individuals resolve the dilemma of dirty money.

Money can be tainted when it is associated with direct or indirect harm to others. Deciding whether to accept "dirty money" poses a dilemma because money can be used to help others, but accepting dirty money has moral costs. How people resolve the dilemma of dirty money remains unknown. One theory casts the dilemma as a valuation conflict that can be resolved by integrating the costs and benefits of accepting dirty money. Here, we use behavioral experiments and computational modeling to test the valuation conflict account and unveil the cognitive computations employed when deciding whether to accept or reject morally tainted cash. In Study 1, British participants decided whether to accept "dirty" money obtained by inflicting electric shocks on another person (versus "clean" money obtained by shocking oneself). Computational models showed that the source of the money (dirty versus clean) impacted decisions by shifting the relative valuation of the money's positive and negative attributes, rather than imposing a uniform bias on decision-making. Studies 2 and 3 replicate this finding and show that participants were more willing to accept dirty money when the money was directed towards a good cause, and observers judged such decisions to be more praiseworthy than accepting dirty money for one's own profit. Our findings suggest that dirty money can be psychologically "laundered" through charitable activities and have implications for understanding and preventing the social norms that can justify corrupt behavior.

Within- and cross-participant classifiers reveal different neural coding of information.

Analyzing distributed patterns of brain activation using multivariate pattern analysis (MVPA) has become a popular approach for using functional magnetic resonance imaging (fMRI) data to predict mental states. While the majority of studies currently build separate classifiers for each participant in the sample, in principle a single classifier can be derived from and tested on data from all participants. These two approaches, within- and cross-participant classification, rely on potentially different sources of variability and thus may provide distinct information about brain function. Here, we used both approaches to identify brain regions that contain information about passively received monetary rewards (i.e., images of currency that influenced participant payment) and social rewards (i.e., images of human faces). Our within-participant analyses implicated regions in the ventral visual processing stream-including fusiform gyrus and primary visual cortex-and ventromedial prefrontal cortex (VMPFC). Two key results indicate these regions may contain statistically discriminable patterns that contain different informational representations. First, cross-participant analyses implicated additional brain regions, including striatum and anterior insula. The cross-participant analyses also revealed systematic changes in predictive power across brain regions, with the pattern of change consistent with the functional properties of regions. Second, individual differences in classifier performance in VMPFC were related to individual differences in preferences between our two reward modalities. We interpret these results as reflecting a distinction between patterns showing participant-specific functional organization and those indicating aspects of brain organization that generalize across individuals.

How peer influence shapes value computation in moral decision-making.

Moral behavior is susceptible to peer influence. How does information from peers influence moral preferences? We used drift-diffusion modeling to show that peer influence changes the value of moral behavior by prioritizing the choice attributes that align with peers' goals. Study 1 (N = 100; preregistered) showed that participants accurately inferred the goals of prosocial and antisocial peers when observing their moral decisions. In Study 2 (N = 68), participants made moral decisions before and after observing the decisions of a prosocial or antisocial peer. Peer observation caused participants' own preferences to resemble those of their peers. This peer influence effect on value computation manifested as an increased weight on choice attributes promoting the peers' goals that occurred independently from peer influence on initial choice bias. Participants' self-reported awareness of influence tracked more closely with computational measures of prosocial than antisocial influence. Our findings have implications for bolstering and blocking the effects of prosocial and antisocial influence on moral behavior.

Local pattern classification differentiates processes of economic valuation.

For effective decision making, individuals must be able to form subjective values from many types of information. Yet, the neural mechanisms that underlie potential differences in value computation across different decision scenarios are incompletely understood. Here, we used functional magnetic resonance imaging (fMRI), in conjunction with the machine learning technique of support vector machines (SVM), to identify brain regions that contain unique local information associated with different types of valuation. We used a combinatoric approach that evaluated the unique contributions of different brain regions to model generalization strength. Local voxel patterns in left posterior parietal cortex contained unique information differentiating probabilistic and intertemporal valuation, a result that was not accessible using standard fMRI analyses. We conclude that the early valuation phases for these reward types differ on a fine spatial scale, suggesting the existence of computational topographies along the value construction pathway.

Neuroeconomics, health psychology, and the interdisciplinary study of preventative health behavior.

The goal of this article is to introduce readers to theories, tools, and evidence from the field of neuroeconomics and to describe how health psychology and neuroeconomics can be mutually informative in the study of preventative health behaviors. Preventative health behavior here refers to both individual actions that impact one's health (e.g., exercise) and broader behavioral patterns, such as those captured in personality constructs. Although neuroeconomic researchers have begun to incorporate health-relevant behaviors into their studies, the full potential of this research to inform preventative health models is as yet unrealized. What is needed to "translate up" is the unification of rich theoretical content from health psychology with investigations by neuroeconomic researchers of the decision-making process during health-relevant choices. We identify choice as a central, shared feature across models of preventative health behavior that can serve as an inroad for neuroeconomics to contribute to existing models and highlight commonalities that might not otherwise be apparent. A central premise of our argument is that, because health decisions are nearly always multiply determined, a more precise and mechanistic understanding of how choices are made is an important but understudied topic in health psychology. A partnership between health psychologists and neuroeconomic researchers can yield valuable insights into how preventative health choice is made and to identify targets and methods for intervention.

Loss Aversion Reflects Information Accumulation, Not Bias: A Drift-Diffusion Model Study.

Defined as increased sensitivity to losses, loss aversion is often conceptualized as a cognitive bias. However, findings that loss aversion has an attentional or emotional regulation component suggest that it may instead reflect differences in information processing. To distinguish these alternatives, we applied the drift-diffusion model (DDM) to choice and response time (RT) data in a card gambling task with unknown risk distributions. Loss aversion was measured separately for each participant. Dividing the participants into terciles based on loss aversion estimates, we found that the most loss-averse group showed a significantly lower drift rate than the other two groups, indicating overall slower uptake of information. In contrast, neither the starting bias nor the threshold separation (barrier) varied by group, suggesting that decision thresholds are not affected by loss aversion. These results shed new light on the cognitive mechanisms underlying loss aversion, consistent with an account based on information accumulation.

Informatic parcellation of the network involved in the computation of subjective value.

Understanding how the brain computes value is a basic question in neuroscience. Although individual studies have driven this progress, meta-analyses provide an opportunity to test hypotheses that require large collections of data. We carry out a meta-analysis of a large set of functional magnetic resonance imaging studies of value computation to address several key questions. First, what is the full set of brain areas that reliably correlate with stimulus values when they need to be computed? Second, is this set of areas organized into dissociable functional networks? Third, is a distinct network of regions involved in the computation of stimulus values at decision and outcome? Finally, are different brain areas involved in the computation of stimulus values for different reward modalities? Our results demonstrate the centrality of ventromedial prefrontal cortex (VMPFC), ventral striatum and posterior cingulate cortex (PCC) in the computation of value across tasks, reward modalities and stages of the decision-making process. We also find evidence of distinct subnetworks of co-activation within VMPFC, one involving central VMPFC and dorsal PCC and another involving more anterior VMPFC, left angular gyrus and ventral PCC. Finally, we identify a posterior-to-anterior gradient of value representations corresponding to concrete-to-abstract rewards.

Functional connectivity with ventromedial prefrontal cortex reflects subjective value for social rewards.

According to many studies, the ventromedial prefrontal cortex (VMPFC) encodes the subjective value of disparate rewards on a common scale. Yet, a host of other reward factors-likely represented outside of VMPFC-must be integrated to construct such signals for valuation. Using functional magnetic resonance imaging (fMRI), we tested whether the interactions between posterior VMPFC and functionally connected brain regions predict subjective value. During fMRI scanning, participants rated the attractiveness of unfamiliar faces. We found that activation in dorsal anterior cingulate cortex, anterior VMPFC and caudate increased with higher attractiveness ratings. Using data from a post-scan task in which participants spent money to view attractive faces, we quantified each individual's subjective value for attractiveness. We found that connectivity between posterior VMPFC and regions frequently modulated by social information-including the temporal-parietal junction (TPJ) and middle temporal gyrus-was correlated with individual differences in subjective value. Crucially, these additional regions explained unique variation in subjective value beyond that extracted from value regions alone. These findings indicate not only that posterior VMPFC interacts with additional brain regions during valuation, but also that these additional regions carry information employed to construct the subjective value for social reward.

Value normalization in decision making: theory and evidence.

A sizable body of evidence has shown that the brain computes several types of value-related signals to guide decision making, such as stimulus values, outcome values, and prediction errors. A critical question for understanding decision-making mechanisms is whether these value signals are computed using an absolute or a normalized code. Under an absolute code, the neural response used to represent the value of a given stimulus does not depend on what other values might have been encountered. By contrast, under a normalized code, the neural response associated with a given value depends on its relative position in the distribution of values. This review provides a simple framework for thinking about value normalization, and uses it to evaluate the existing experimental evidence.

Contributions of frontopolar cortex to judgments about self, others and relations.

Activation in frontopolar cortex (FPC; BA 10) has been associated both with attending to mental states and with integrating multiple mental relations. However, few previous studies have manipulated both of these cognitive processes, precluding a clear functional distinction among regions within FPC. To address this issue, we developed an fMRI task that combined mentalizing and relational integration processes. Participants saw blocks of single words and performed one of three judgments: how pleasant or unpleasant they found each word (Self condition), how a specific friend would evaluate the pleasantness of the word (Other condition), or the difference between their own pleasantness judgment and that of their friend (Relational condition). We found that medial FPC was modulated by Other relative to Self judgments, consistent with a role in mentalizing. Lateral FPC was significantly activated during Relational compared to Self judgements, suggesting that this region is particularly involved in relational integration. The results point to a strong functional dissociation between medial and lateral FPC. In addition, the data demonstrate a role for lateral FPC in the social domain, provided that the task requires the integration of one's preferences with those of others.

Nucleus accumbens mediates relative motivation for rewards in the absence of choice.

To dissociate a choice from its antecedent neural states, motivation associated with the expected outcome must be captured in the absence of choice. Yet, the neural mechanisms that mediate behavioral idiosyncrasies in motivation, particularly with regard to complex economic preferences, are rarely examined in situations without overt decisions. We employed functional magnetic resonance imaging in a large sample of participants while they anticipated earning rewards from two different modalities: monetary and candy rewards. An index for relative motivation toward different reward types was constructed using reaction times to the target for earning rewards. Activation in the nucleus accumbens (NAcc) and anterior insula (aINS) predicted individual variation in relative motivation between our reward modalities. NAcc activation, however, mediated the effects of aINS, indicating the NAcc is the likely source of this relative weighting. These results demonstrate that neural idiosyncrasies in reward efficacy exist even in the absence of explicit choices, and extend the role of NAcc as a critical brain region for such choice-free motivation.