Neural mechanisms of information seeking.

We ubiquitously seek information to make better decisions. Particularly in the modern age, when more information is available at our fingertips than ever, the information we choose to collect determines the quality of our decisions. Decision neuroscience has long adopted empirical approaches where the information available to decision-makers is fully controlled by the researchers, leaving neural mechanisms of information seeking less understood. Although information seeking has long been studied in the context of the exploration-exploitation trade-off, recent studies have widened the scope to investigate more overt information seeking in a way distinct from other decision processes. Insights gained from these studies, accumulated over the last few years, raise the possibility that information seeking is driven by the reward system signaling the subjective value of information. In this piece, we review findings from the recent studies, highlighting the conceptual and empirical relationships between distinct literatures, and discuss future research directions necessary to establish a more comprehensive understanding of how individuals seek information as a part of value-based decision-making.

Dissociable Contributions of the Medial Parietal Cortex to Recognition Memory.

Human neuroimaging studies of episodic memory retrieval routinely observe the engagement of specific cortical regions beyond the medial temporal lobe. Of these, medial parietal cortex (MPC) is of particular interest given its distinct functional characteristics during different retrieval tasks. Specifically, while recognition and autobiographical recall tasks are both used to probe episodic retrieval, these paradigms consistently drive distinct spatial patterns of response within MPC. However, other studies have emphasized alternate MPC functional dissociations in terms of brain network connectivity profiles or stimulus category selectivity. As the unique contributions of MPC to episodic memory remain unclear, adjudicating between these different accounts can provide better consensus regarding MPC function. Therefore, we used a precision-neuroimaging dataset (7T functional magnetic resonance imaging) to examine how MPC regions are differentially engaged during recognition memory and how these task-related dissociations may also reflect distinct connectivity and stimulus category functional profiles. We observed interleaved, though spatially distinct, subregions of MPC where responses were sensitive to either recognition decisions or the semantic representation of stimuli. In addition, this dissociation was further accentuated by functional subregions displaying distinct profiles of connectivity with the hippocampus during task and rest. Finally, we show that recent observations of dissociable person and place selectivity within the MPC reflect category-specific responses from within identified semantic regions that are sensitive to mnemonic demands. Together, by examining precision functional mapping within individuals, these data suggest that previously distinct observations of functional dissociation within MPC conform to a common principle of organization throughout hippocampal-neocortical memory systems.

Lesions to different regions of frontal cortex have dissociable effects on voluntary persistence.

Deciding how long to keep waiting for uncertain future rewards is a complex problem. Previous research has shown that choosing to stop waiting results from an evaluative process that weighs the subjective value of the awaited reward against the opportunity cost of waiting. In functional neuroimaging data, activity in ventromedial prefrontal cortex (vmPFC) tracks the dynamics of this evaluation, while activation in the dorsomedial prefrontal cortex (dmPFC) and anterior insula (AI) ramps up before a decision to quit is made. Here, we provide causal evidence of the necessity of these brain regions for successful performance in a willingness-to-wait task. 28 participants with frontal lobe lesions were tested on their ability to adaptively calibrate how long they waited for monetary rewards. We grouped the participants based on the location of their lesions, which were primarily in ventromedial, dorsomedial, or lateral parts of their prefrontal cortex (vmPFC, dmPFC, and lPFC, respectively), or in the anterior insula. We compared the performance of each subset of lesion participants to behavior in a control group without lesions (n=18). Finally, we fit a newly developed computational model to the data to glean a more mechanistic understanding of how lesions affect the cognitive processes underlying choice. We found that participants with lesions to the vmPFC waited less overall, while participants with lesions to the dmPFC and anterior insula were specifically impaired at calibrating their level of persistence to the environment. These behavioral effects were accounted for by systematic differences in parameter estimates from a computational model of task performance: while the vmPFC group showed reduced initial willingness to wait, lesions to the dmPFC/anterior insula were associated with slower learning from negative feedback. These findings corroborate the notion that failures of persistence can be driven by sophisticated cost-benefit analyses rather than lapses in self-control. They also support the functional specialization of different parts of the prefrontal cortex in service of voluntary persistence.

Dissociable contributions of the medial parietal cortex to recognition memory.

Human neuroimaging studies of episodic memory retrieval routinely observe the engagement of specific cortical regions beyond the medial temporal lobe. Of these, medial parietal cortex (MPC) is of particular interest given its ubiquitous, and yet distinct, functional characteristics during different types of retrieval tasks. Specifically, while recognition memory and autobiographical recall tasks are both used to probe episodic retrieval, these paradigms consistently drive distinct patterns of response within MPC. This dissociation adds to growing evidence suggesting a common principle of functional organization across memory related brain structures, specifically regarding the control or content demands of memory-based decisions. To carefully examine this putative organization, we used a high-resolution fMRI dataset collected at ultra-high field (7T) while subjects performed thousands of recognition-memory trials to identify MPC regions responsive to recognition-decisions or semantic content of stimuli within and across individuals. We observed interleaving, though distinct, functional subregions of MPC where responses were sensitive to either recognition decisions or the semantic representation of stimuli, but rarely both. In addition, this functional dissociation within MPC was further accentuated by distinct profiles of connectivity bias with the hippocampus during task and rest. Finally, we show that recent observations of person and place selectivity within MPC reflect category specific responses from within identified semantic regions that are sensitive to mnemonic demands. Together, these data better account for how distinct patterns of MPC responses can occur as a result of task demands during episodic retrieval and may reflect a common principle of organization throughout hippocampal-neocortical memory systems.

Less cortical complexity in ventromedial prefrontal cortex is associated with a greater preference for risky and immediate rewards.

In our everyday lives, we are often faced with situations in which we have to make choices that involve risky or delayed rewards. However, the extent to which we are willing to accept larger risky (over smaller certain) or larger delayed (over smaller immediate) rewards vary across individuals. Here we investigated the relationship between cortical surface complexity in medial prefrontal cortex and individual differences in risky and intertemporal preferences. We found that lower cortical complexity in ventromedial prefrontal cortex (vmPFC) was associated with a greater preference for risky and immediate rewards. In addition to these common structural associations in mPFC, we also found associations between lower cortical complexity and a greater preference for immediate rewards that extended into left dorsomedial prefrontal cortex and right vmPFC. Taken together, the shared association suggests that lower cortical complexity in vmPFC may be a structural marker for individual differences in impulsive behavior.

Individual differences in delay discounting are associated with dorsal prefrontal cortex connectivity in children, adolescents, and adults.

Delay discounting is a measure of impulsive choice relevant in adolescence as it predicts many real-life outcomes, including obesity and academic achievement. However, resting-state functional networks underlying individual differences in delay discounting during youth remain incompletely described. Here we investigate the association between multivariate patterns of functional connectivity and individual differences in impulsive choice in a large sample of children, adolescents, and adults. A total of 293 participants (9-23 years) completed a delay discounting task and underwent 3T resting-state fMRI. A connectome-wide analysis using multivariate distance-based matrix regression was used to examine whole-brain relationships between delay discounting and functional connectivity. These analyses revealed that individual differences in delay discounting were associated with patterns of connectivity emanating from the left dorsal prefrontal cortex, a default mode network hub. Greater delay discounting was associated with greater functional connectivity between the dorsal prefrontal cortex and other default mode network regions, but reduced connectivity with regions in the dorsal and ventral attention networks. These results suggest delay discounting in children, adolescents, and adults is associated with individual differences in relationships both within the default mode network and between the default mode and networks involved in attentional and cognitive control.

Statistical information about reward timing is insufficient for promoting optimal persistence decisions.

When deciding how long to keep waiting for delayed rewards that will arrive at an uncertain time, different distributions of possible reward times dictate different optimal strategies for maximizing reward. When reward timing distributions are heavy-tailed (e.g., waiting on hold) there is a point at which waiting is no longer advantageous because the opportunity cost of waiting is too high. Alternatively, when reward timing distributions have more predictable timing (e.g., uniform), it is advantageous to wait as long as necessary for the reward. Although people learn to approximate optimal strategies, little is known about how this learning occurs. One possibility is that people learn a general cognitive representation of the probability distribution that governs reward timing and then infer a strategy from that model of the environment. Another possibility is that they learn an action policy in a way that depends more narrowly on direct task experience, such that general knowledge of the reward timing distribution is insufficient for expressing the optimal strategy. Here, in a series of studies in which participants decided how long to persist for delayed rewards before quitting, we provided participants with information about the reward timing distribution in several ways. Whether the information was provided through counterfactual feedback (Study 1), previous exposure (Studies 2a and 2b), or description (Studies 3a and 3b), it did not obviate the need for direct, feedback-driven learning in a decision context. Therefore, learning when to quit waiting for delayed rewards might depend on task-specific experience, not solely on probabilistic reasoning.

Pupillometric evidence for a temporal expectations-based account of persistence under temporal uncertainty.

People often quit waiting for delayed rewards when the exact timing of those rewards is uncertain. This behavior often has been attributed to self-control failure. Another possibility is that quitting is the result of a rational decision-making process in the face of uncertainty, based on the decision-maker's expectations about the possible arrival times of the awaited reward. There are forms of temporal expectations (e.g., heavy-tailed) under which the expected time remaining until a reward arrives actually increases as time elapses. In those cases, the rational strategy is to quit waiting when the expected reward is no longer worth the expected time remaining. To arbitrate between the "limited self-control" and "temporal expectations" accounts of persistence, we measured pupil diameter during a persistence task, as a physiological marker of surprise (phasic responses) and effort (pre-decision diameter). Phasic pupil responses were elevated in response to reward receipt. Critically, the extent to which pupils dilated following rewards depended on the delay: people showed larger pupillary surprise responses the more delayed the reward was. This result suggests that people expect the reward less the longer they wait for it-a form of temporal expectations under which limiting persistence is rational. Moreover, predecision pupil diameter before quit events was not associated with how long the participant had been waiting, but rather, depended on how atypical the quit decision was compared with the participant's usual behavior. These data provide physiological evidence for a temporal expectations account of persistence under temporal uncertainty.

Individual Differences in Delay Discounting are Associated with Dorsal Prefrontal Cortex Connectivity in Youth.

Delay discounting is a measure of impulsive choice relevant in adolescence as it predicts many real-life outcomes, including substance use disorders, obesity, and academic achievement. However, the functional networks underlying individual differences in delay discounting during youth remain incompletely described. Here we investigate the association between multivariate patterns of functional connectivity and individual differences in impulsive choice in a large sample of youth. A total of 293 youth (9-23 years) completed a delay discounting task and underwent resting-state fMRI at 3T. A connectome-wide analysis using multivariate distance-based matrix regression was used to examine whole-brain relationships between delay discounting and functional connectivity was then performed. These analyses revealed that individual differences in delay discounting were associated with patterns of connectivity emanating from the left dorsal prefrontal cortex, a hub of the default mode network. Delay discounting was associated with greater functional connectivity between the dorsal prefrontal cortex and other parts of the default mode network, and reduced connectivity with regions in the dorsal and ventral attention networks. These results suggest that delay discounting in youth is associated with individual differences in relationships both within the default mode network and between the default mode and networks involved in attentional and cognitive control.

An fMRI-Based Brain Marker of Individual Differences in Delay Discounting.

Individual differences in delay discounting-how much we discount future compared to immediate rewards-are associated with general life outcomes, psychopathology, and obesity. Here, we use machine learning on fMRI activity during an intertemporal choice task to develop a functional brain marker of these individual differences in human adults. Training and cross-validating the marker in one dataset (Study 1, N = 110 male adults) resulted in a significant prediction-outcome correlation (r = 0.49), generalized to predict individual differences in a completely independent dataset (Study 2: N = 145 male and female adults, r = 0.45), and predicted discounting several weeks later. Out-of-sample responses of the functional brain marker, but not discounting behavior itself, differed significantly between overweight and lean individuals in both studies, and predicted fasting-state blood levels of insulin, c-peptide, and leptin in Study 1. Significant predictive weights of the marker were found in cingulate, insula, and frontoparietal areas, among others, suggesting an interplay among regions associated with valuation, conflict processing, and cognitive control. This new functional brain marker is a step toward a generalizable brain model of individual differences in delay discounting. Future studies can evaluate it as a potential transdiagnostic marker of altered decision-making in different clinical and developmental populations.SIGNIFICANCE STATEMENT People differ substantially in how much they prefer smaller sooner rewards or larger later rewards such as spending money now versus saving it for retirement. These individual differences are generally stable over time and have been related to differences in mental and bodily health. What is their neurobiological basis? We applied machine learning to brain-imaging data to identify a novel brain activity pattern that accurately predicts how much people prefer sooner versus later rewards, and which can be used as a new brain-based measure of intertemporal decision-making in future studies. The resulting functional brain marker also predicts overweight and metabolism-related blood markers, providing new insight into the possible links between metabolism and the cognitive and brain processes involved in intertemporal decision-making.

A Systematic Review on Common and Distinct Neural Correlates of Risk-taking in Substance-related and Non-substance Related Addictions.

Both substance-related as well as non-substance-related addictions may include recurrent engagement in risky actions despite adverse outcomes. We here apply a unified approach and review task-based neuroimaging studies on substance-related (SRAs) and non-substance related addictions (NSRAs) to examine commonalities and differences in neural correlates of risk-taking in these two addiction types. To this end, we conducted a systematic review adhering to the PRISMA guidelines. Two databases were searched with predefined search terms to identify neuroimaging studies on risk-taking tasks in individuals with addiction disorders. In total, 19 studies on SRAs (comprising a total of 648 individuals with SRAs) and 10 studies on NSRAs (comprising a total of 187 individuals with NSRAs) were included. Risk-related brain activation in SRAs and NSRAs was summarized individually and subsequently compared to each other. Results suggest convergent altered risk-related neural processes, including hyperactivity in the OFC and the striatum. As characteristic for both addiction types, these brain regions may represent an underlying mechanism of suboptimal decision-making. In contrast, decreased DLPFC activity may be specific to SRAs and decreased IFG activity could only be identified for NSRAs. The precuneus and posterior cingulate show elevated activity in SRAs, while findings regarding these areas were mixed in NSRAs. Additional scarce evidence suggests decreased ventral ACC activity and increased dorsal ACC activity in both addiction types. Associations between identified activation patterns with drug use severity underpin the clinical relevance of these findings. However, this exploratory evidence should be interpreted with caution and should be regarded as preliminary. Future research is needed to evaluate the findings gathered by this review.

Aging is associated with maladaptive episodic memory-guided social decision-making.

Older adults are frequent targets and victims of financial fraud. They may be especially susceptible to revictimization because of age-related changes in both episodic memory and social motivation. Here we examined these factors in a context where adaptive social decision-making requires intact associative memory for previous social interactions. Older adults made more maladaptive episodic memory-guided social decisions but not only because of poorer associative memory. Older adults were biased toward remembering people as being fair, while young adults were biased toward remembering people as being unfair. Holding memory constant, older adults engaged more with people that were familiar (regardless of the nature of the previous interaction), whereas young adults were prone to avoiding others that they remembered as being unfair. Finally, older adults were more influenced by facial appearances, choosing to interact with social partners that looked more generous, even though those perceptions were inconsistent with prior experience.

A neural signature of the vividness of prospective thought is modulated by temporal proximity during intertemporal decision making.

Why do people discount future rewards? Multiple theories in psychology argue that one reason is that future events are imagined less vividly than immediate events, thereby diminishing their perceived value. Here we provide neuroscientific evidence for this proposal. First, we construct a neural signature of the vividness of prospective thought, using an fMRI dataset where the vividness of imagined future events is orthogonal to their valence by design. Then, we apply this neural signature in two additional fMRI datasets, each using a different delay-discounting task, to show that neural measures of vividness decline as rewards are delayed farther into the future.

Decision value signals in the ventromedial prefrontal cortex and motivational and hedonic symptoms across mood and psychotic disorders.

Deficits in motivation and pleasure are common across many psychiatric disorders, and manifest as symptoms of amotivation and anhedonia, which are prominent features of both mood and psychotic disorders. Here we provide evidence for an association between neural value signals and symptoms of amotivation and anhedonia across adults with major depression, bipolar disorder, schizophrenia, or no psychiatric diagnosis. We found that value signals in the ventromedial prefrontal cortex (vmPFC) during intertemporal decision-making were dampened in individuals with greater motivational and hedonic deficits, after accounting for primary diagnosis. This relationship remained significant while controlling for diagnosis-specific symptoms of mood and psychosis, such as depression as well as positive and negative symptoms. Our results demonstrate that dysfunction in the vmPFC during value-based decision-making is specifically linked to motivational and hedonic impairments. These findings provide a quantitative neural target for the potential development of novel treatments for amotivation and anhedonia.

Individuals with ventromedial frontal damage display unstable but transitive preferences during decision making.

The ventromedial frontal lobe (VMF) is important for decision-making, but the precise causal role of the VMF in the decision process has not been fully established. Previous studies have suggested that individuals with VMF damage violate transitivity, a hallmark axiom of rational decisions. However, these prior studies cannot properly distinguish whether individuals with VMF damage are truly prone to choosing irrationally from whether their preferences are simply more variable. We had individuals with focal VMF damage, individuals with other frontal damage, and healthy controls make repeated choices across three categories-artworks, chocolate bar brands, and gambles. Using proper tests of transitivity, we find that, in our study, individuals with VMF damage make rational decisions consistent with transitive preferences, even though they exhibit greater variability in their preferences. That is, the VMF is necessary for having strong and reliable preferences, but not for being a rational decision maker. VMF damage affects the variability with which value is assessed, but not the consistency with which value is sought.

Fast construction of interpretable whole-brain decoders.

Researchers often seek to decode mental states from brain activity measured with functional MRI. Rigorous decoding requires the use of formal neural prediction models, which are likely to be the most accurate if they use the whole brain. However, the computational burden and lack of interpretability of off-the-shelf statistical methods can make whole-brain decoding challenging. Here, we propose a method to build whole-brain neural decoders that are both interpretable and computationally efficient. We extend the partial least squares algorithm to build a regularized model with variable selection that offers a unique "fit once, tune later" approach: users need to fit the model only once and can choose the best tuning parameters post hoc. We show in real data that our method scales well with increasing data size and yields interpretable predictors. The algorithm is publicly available in multiple languages in the hope that interpretable whole-brain predictors can be implemented more widely in neuroimaging research.

Neural representations of others' traits predict social decisions.

To guide social interaction, people often rely on expectations about the traits of other people, based on markers of social group membership (i.e., stereotypes). Although the influence of stereotypes on social behavior is widespread, key questions remain about how traits inferred from social-group membership are instantiated in the brain and incorporated into neural computations that guide social behavior. Here, we show that the human lateral orbitofrontal cortex (OFC) represents the content of stereotypes about members of different social groups in the service of social decision-making. During functional MRI scanning, participants decided how to distribute resources across themselves and members of a variety of social groups in a modified Dictator Game. Behaviorally, we replicated our recent finding that inferences about others' traits, captured by a two-dimensional framework of stereotype content (warmth and competence), had dissociable effects on participants' monetary-allocation choices: recipients' warmth increased participants' aversion to advantageous inequity (i.e., earning more than recipients), and recipients' competence increased participants' aversion to disadvantageous inequity (i.e., earning less than recipients). Neurally, representational similarity analysis revealed that others' traits in the two-dimensional space were represented in the temporoparietal junction and superior temporal sulcus, two regions associated with mentalizing, and in the lateral OFC, known to represent inferred features of a decision context outside the social domain. Critically, only the latter predicted individual choices, suggesting that the effect of stereotypes on behavior is mediated by inference-based decision-making processes in the OFC.

Cerebellum anatomy predicts individual risk-taking behavior and risk tolerance.

Human risk tolerance is highly idiosyncratic and individuals often show distinctive preferences when faced with similar risky situations. However, the neural underpinnings of individual differences in risk-taking remain unclear. Here we combined structural and perfusion MRI and examined the associations between brain anatomy and individual risk-taking behavior/risk tolerance in a sample of 115 healthy participants during the Balloon Analogue Risk Task, a well-established sequential risky decision paradigm. Both whole brain and region-of-interest analyses showed that the left cerebellum gray matter volume (GMV) has a strong association with individual risk-taking behavior and risk tolerance, outperforming the previously reported associations with the amygdala and right posterior parietal cortex (PPC) GMV. Left cerebellum GMV also accounted for risk tolerance and risk-taking behavior changes with aging. However, regional cerebral blood flow (CBF) provided no additional predictive power. These findings suggest a novel cerebellar anatomical contribution to individual differences in risk tolerance. Further studies are necessary to elucidate the underestimated important role of cerebellum in risk-taking.

Causal role of the right temporoparietal junction in selfishness depends on the social partner.

The right temporoparietal junction (rTPJ) is a hub of the mentalizing network, but its causal role in social decisions remains an area of active investigation. While prior studies using causal neurostimulation methods have confirmed the role of the rTPJ in mentalizing and strategic social interactions, most of the evidence for its role in resource-sharing decisions comes from correlational neuroimaging studies. Further, it remains unclear if the influence of the rTPJ on decisions about sharing resources depends on whether the other person is salient and identifiable. To clarify the causal role of the rTPJ in social decision making, we examined the effects of putatively inhibitory rTPJ transcranial magnetic stimulation (TMS) on Dictator Game behavior with one partner that was physically present and one that was only minimally identified. Under control conditions, participants tended to create more advantageous inequity toward the partner that was only minimally identified, selfishly keeping more resources themselves. rTPJ TMS reduced this differential treatment of the two partners. Clarifying prior mixed findings, results suggest that the rTPJ may play a role in differentiating between others when deciding how equitably to divide resources, but may not play a general role in reducing selfishness by promoting aversion to advantageous inequity.

Relationship of ventral striatum activation during effort discounting to clinical amotivation severity in schizophrenia.

Motivational deficits play a central role in disability due to negative symptoms of schizophrenia (SZ), but limited pathophysiological understanding impedes critically needed therapeutic development. We applied an fMRI Effort Discounting Task (EDT) that quantifies motivation using a neuroeconomic decision-making approach, capturing the degree to which effort requirements produce reductions in the subjective value (SV) of monetary reward. An analyzed sample of 21 individuals with SZ and 23 group-matched controls performed the EDT during fMRI. We hypothesized that ventral striatum (VS) as well as extended brain motivation circuitry would encode SV, integrating reward and effort costs. We also hypothesized that VS hypoactivation during EDT decisions would demonstrate a dimensional relationship with clinical amotivation severity, reflecting greater suppression by effort costs. As hypothesized, VS as well as a broader cortico-limbic network were activated during the EDT and this activation correlated positively with SV. In SZ, activation to task decisions was reduced selectively in VS. Greater VS reductions correlated with more severe clinical amotivation in SZ and across all participants. However, these diagnosis and amotivation effects could not be explained by the response to parametric variation in reward, effort, or model-based SV. Our findings demonstrate that VS hypofunction in schizophrenia is manifested during effort-based decisions and reflects dimensional motivation impairment. Dysfunction of VS impacting effort-based decision-making can provide a target for biomarker development to guide novel efforts to assess and treat disabling amotivation.