Social closeness and feedback modulate susceptibility to the framing effect

Although we often seek social feedback (SFB) from others to help us make decisions, little is known about how SFB affects decisions under risk, particularly from a close peer. We conducted two experiments using an established framing task to probe how decision-making is modulated by SFB valence (positive, negative) and the level of closeness with feedback provider (friend, confederate). Participants faced mathematically equivalent decisions framed as either an opportunity to keep (gain frame) or lose (loss frame) part of an initial endowment. Periodically, participants were provided with positive (e.g., “Nice!”) or negative (e.g., “Lame!”) feedback about their choices. Such feedback was provided by either a confederate (Experiment 1) or a gender-matched close friend (Experiment 2). As expected, the framing effect was observed in both experiments. Critically, an individual's susceptibility to the framing effect was modulated by the valence of the SFB, but only when the feedback provider was a close friend. This effect was reflected in the activation patterns of ventromedial prefrontal cortex and posterior cingulate cortex, regions involved in complex decision-making. Taken together, these results highlight social closeness as an important factor in understanding the impact of SFB on neural mechanisms of decision-making.     

Distinct neural activation patterns underlie economic decisions in high and low psychopathy scorers

Psychopathic traits affect social functioning and the ability to make adaptive decisions in social interactions. This study investigated how psychopathy affects the neural mechanisms that are recruited to make decisions in the ultimatum game. Thirty-five adult participants recruited from the community underwent functional magnetic resonance imaging scanning while they performed the ultimatum game under high and low cognitive load. Across load conditions, high psychopathy scorers rejected unfair offers in the same proportion as low scorers, but perceived them as less unfair. Among low scorers, the perceived fairness of offers predicted acceptance rates, whereas in high scorers no association was found. Imaging results revealed that responses in each group were associated with distinct patterns of brain activation, indicating divergent decision mechanisms. Acceptance of unfair offers was associated with dorsolateral prefrontal cortex activity in low scorers and ventromedial prefrontal cortex activity in high scorers. Overall, our findings point to distinct motivations for rejecting unfair offers in individuals who vary in psychopathic traits, with rejections in high psychopathy scorers being probably induced by frustration. Implications of these results for models of ventromedial prefrontal cortex dysfunction in psychopathy are discussed.     

The amygdala and decision-making

Decision-making is a complex process that requires the orchestration of multiple neural systems. For example, decision-making is believed to involve areas of the brain involved in emotion (e.g., amygdala, ventromedial prefrontal cortex) and memory (e.g., hippocampus, dorsolateral prefrontal cortex). In this article, we will present findings related to the amygdala's role in decision-making, and differentiate the contributions of the amygdala from those of other structurally and functionally connected neural regions. Decades of research have shown that the amygdala is involved in associating a stimulus with its emotional value. This tradition has been extended in newer work, which has shown that the amygdala is especially important for decision-making, by triggering autonomic responses to emotional stimuli, including monetary reward and punishment. Patients with amygdala damage lack these autonomic responses to reward and punishment, and consequently, cannot utilize “somatic marker” type cues to guide future decision-making. Studies using laboratory decision-making tests have found deficient decision-making in patients with bilateral amygdala damage, which resembles their real-world difficulties with decision-making. Additionally, we have found evidence for an interaction between sex and laterality of amygdala functioning, such that unilateral damage to the right amygdala results in greater deficits in decision-making and social behavior in men, while left amygdala damage seems to be more detrimental for women. We have posited that the amygdala is part of an “impulsive,” habit type system that triggers emotional responses to immediate outcomes.     

Reward and social valuation deficits following ventromedial prefrontal damage

Lesion and imaging studies have implicated the ventromedial prefrontal cortex (vmPFC) in economic decisions and social interactions, yet its exact functions remain unclear. Here, we investigated the hypothesis that the vmPFC represents the subjective value or desirability of future outcomes during social decision-making. Both vmPFC-damaged patients and control participants acted as the responder in a single-round ultimatum game. To test outcome valuation, we contrasted concrete, immediately available gains with abstract, future ones. To test social valuation, we contrasted interactions with a human partner and those involving a computer. We found that, compared to controls, vmPFC patients substantially reduced their acceptance rate of unfair offers from a human partner, but only when financial gains were presented as abstract amounts to be received later. When the gains were visible and readily available, the vmPFC patients' acceptance of unfair offers was normal. Furthermore, unlike controls, vmPFC patients did not distinguish between unfair offers from a human agent and those from a computerized opponent. We conclude that the vmPFC encodes the expected value of abstract, future goals in a common neural currency that takes into account both reward and social signals in order to optimize economic decision-making.     

Effects of social and emotional context on neural activation and synchrony during movie viewing

Sharing emotional experiences impacts how we perceive and interact with the world, but the neural mechanisms that support this sharing are not well characterized. In this study, participants (N = 52) watched videos in an MRI scanner in the presence of an unfamiliar peer. Videos varied in valence and social context (i.e., participants believed their partner was viewing the same (joint condition) or a different (solo condition) video). Reported togetherness increased during positive videos regardless of social condition, indicating that positive contexts may lessen the experience of being alone. Two analysis approaches were used to examine both sustained neural activity averaged over time and dynamic synchrony throughout the videos. Both approaches revealed clusters in the medial prefrontal cortex that were more responsive to the joint condition. We observed a time‐averaged social‐emotion interaction in the ventromedial prefrontal cortex, although this region did not demonstrate synchrony effects. Alternatively, social‐emotion interactions in the amygdala and superior temporal sulcus showed greater neural synchrony in the joint compared to solo conditions during positive videos, but the opposite pattern for negative videos. These findings suggest that positive stimuli may be more salient when experienced together, suggesting a mechanism for forming social bonds.     

Contributions of the prefrontal cortex to the neural basis of human decision making

The neural basis of decision making has been an elusive concept largely due to the many subprocesses associated with it. Recent efforts involving neuroimaging, neuropsychological studies, and animal work indicate that the prefrontal cortex plays a central role in several of these subprocesses. The frontal lobes are involved in tasks ranging from making binary choices to making multi-attribute decisions that require explicit deliberation and integration of diverse sources of information. In categorizing different aspects of decision making, a division of the prefrontal cortex into three primary regions is proposed. (1) The orbitofrontal and ventromedial areas are most relevant to deciding based on reward values and contribute affective information regarding decision attributes and options. (2) Dorsolateral prefrontal cortex is critical in making decisions that call for the consideration of multiple sources of information, and may recruit separable areas when making well defined versus poorly defined decisions. (3) The anterior and ventral cingulate cortex appear especially relevant in sorting among conflicting options, as well as signaling outcome-relevant information. This topic is broadly relevant to cognitive neuroscience as a discipline, as it generally comprises several aspects of cognition and may involve numerous brain regions depending on the situation. The review concludes with a summary of how these regions may interact in deciding and possible future research directions for the field.     

Frontotemporal Regulation of Subjective Value to Suppress Impulsivity in Intertemporal Choices

Impulsive decisions arise from preferring smaller but sooner rewards compared with larger but later rewards. How neural activity and attention to choice alternatives contribute to reward decisions during temporal discounting is not clear. Here we probed (1) attention to and (2) neural representation of delay and reward information in humans (both sexes) engaged in choices. We studied behavioral and frequency-specific dynamics supporting impulsive decisions on a fine-grained temporal scale using eye tracking and MEG recordings. In one condition, participants had to decide for themselves but pretended to decide for their best friend in a second prosocial condition, which required perspective taking. Hence, conditions varied in the value for themselves versus that pretending to choose for another person. Stronger impulsivity was reliably found across three independent groups for prosocial decisions. Eye tracking revealed a systematic shift of attention from the delay to the reward information and differences in eye tracking between conditions predicted differences in discounting. High-frequency activity (175-250 Hz) distributed over right frontotemporal sensors correlated with delay and reward information in consecutive temporal intervals for high value decisions for oneself but not the friend. Collectively, the results imply that the high-frequency activity recorded over frontotemporal MEG sensors plays a critical role in choice option integration.SIGNIFICANCE STATEMENT Humans face decisions between sooner smaller rewards and larger later rewards daily. An objective benefit of losing weight over a longer time might be devalued in face of ice cream because they prefer currently available options because of insufficiently considering long-term alternatives. The degree of contribution of neural representation and attention to choice alternatives is not clear. We investigated correlates of such decisions in participants deciding for themselves or pretending to choose for a friend. Behaviorally participants discounted less in self-choices compared with the prosocial condition. Eye movement and MEG recordings revealed how participants represent choice options most evident for options with high subjective value. These results advance our understanding of neural mechanisms underlying decision-making in humans.     

Re-evaluating the role of the orbitofrontal cortex in reward and reinforcement

The orbitofrontal cortex and adjacent ventromedial prefrontal cortex carry reward representations and mediate flexible behaviour when circumstances change. Here we review how recent experiments in humans and macaques have confirmed the existence of a major difference between the functions of the ventromedial prefrontal cortex and adjacent medial orbitofrontal cortex (mOFC) on the one hand and the lateral orbitofrontal cortex (lOFC) on the other. These differences, however, may not be best accounted for in terms of specializations for reward and error/punishment processing as is commonly assumed. Instead we argue that both lesion and functional magnetic resonance imaging studies reveal that the lOFC is concerned with the assignment of credit for both reward and error outcomes to the choice of specific stimuli and with the linking of specific stimulus representations to representations of specific types of reward outcome. By contrast, we argue that the ventromedial prefrontal cortex/mOFC is concerned with evaluation, value-guided decision-making and maintenance of a choice over successive decisions. Despite the popular view that they cause perseveration of behaviour and inability to inhibit repetition of a previously made choice, we found that lesions in neither orbitofrontal subdivision caused perseveration. On the contrary, lesions in the lOFC made animals switch more rapidly between choices when they were finding it difficult to assign reward values to choices. Lesions in the mOFC caused animals to lose their normal predisposition to repeat previously successful choices, suggesting that the mOFC does not just mediate value comparison in choice but also facilitates maintenance of the same choice if it has been successful.     

Impairments in an early stage of the decision-making process in patients with ventromedial prefrontal damage: preliminary results

Lesions of the ventromedial prefrontal cortex can result in a deficient decision-making behavior. So far, most experimental results in the neuropsychological decision-making research have been obtained with gambling tasks. Due to their high complexity, it is difficult to evaluate the underlying processes of the decision-making deficits. The aim of this study was to assess if patients with ventromedial prefrontal damage compared to patients with dorsolateral prefrontal damage and controls show a deficit in an early stage of the decision-making process. Nine patients with ventromedial prefrontal damage, three with dorsolateral prefrontal damage, and eleven healthy controls were tested with a newly developed decision task in which they had to search actively for the information they needed for their decisions. Our results show that patients with ventromedial prefrontal damage compared to the brain-lesioned dorsolateral prefrontal control group and healthy controls searched less for information with regard to risk defusing operators or consequences of their decisions indicating impairment already in the early stage of the decision-making process.     

Self-oriented neural circuitry predicts other-oriented adaptive risks in adolescence: a longitudinal study

Adolescence is marked by changes in decision-making and perspective-taking abilities. Although adolescents make more adaptive decisions with age, little is understood about how adolescents take adaptive risks that impact others and how this behavior changes developmentally. Functional coupling between reward [e.g., ventral striatum (VS)] and ‘social brain’ [e.g. temporal parietal junction (TPJ)/ posterior superior temporal sulcus (pSTS), medial prefrontal cortex (mPFC)] systems may be differentially shape adaptive risks for the self and other. A total of 173 participants completed between one and three sessions across three waves [a total of 433 behavioral and 403 functional magnetic resonance imaging (fMRI) data points]. During an fMRI scan, adolescents completed a risky decision-making task where they made risky decisions to win money for themselves and their parent. The risky decisions varied in their expected value (EV) of potential reward. Results show that from the 6th through 9th grades, adolescents took increasingly more adaptive risks for themselves than for their parent. Additionally, greater VS–TPJ/pSTS and VS–mPFC connectivity that tracks EV when making risky decisions for themselves in 6th grade, but a lower VS–mPFC connectivity in 9th grade, predicted greater adaptive risk-taking for their parent. This study contributes to our understanding of the self as a neural proxy for promoting adaptive social behaviors in youth.     

Neurobiology of decision-making: risk and reward.

Neurological patients with bilateral ventromedial (VM) lesions of the prefrontal cortex often deny, or they are not aware that they have a problem. Furthermore, they often pursue actions that bring some reward in the immediate run, despite severe long-term consequences such as the loss of job, home, and family. The somatic marker hypothesis, which provides an account of this defect in decision-making, posits that the impairment is the result of defective activation of somatic markers that normally function as covert or overt signposts for helping with the process of making choices that are advantageous to the organism. Failure to enact somatic states results from dysfunction in a neural system in which the VM cortex is one critical region. However, other neural regions, including the amygdala, and somatosensory cortices (SI, SII, and insula) are also hypothesized to be components of that same neural system. Recent evidence reveals that substance abusers suffer from decision-making deficit akin to that seen with patients with VM lesions. Thus, the strategies used to study decision-making in neurological patients have direct implications for understanding several neuropsychiatric disorders including addiction and pathological gambling.     

Neural mechanisms of social influence in adolescence

During the transformative period of adolescence, social influence plays a prominent role in shaping young people’s emerging social identities, and can impact their propensity to engage in prosocial or risky behaviors. In this study, we examine the neural correlates of social influence from both parents and peers, two important sources of influence. Nineteen adolescents (age 16–18 years) completed a social influence task during a functional magnetic resonance imaging (fMRI) scan. Social influence from both sources evoked activity in brain regions implicated in mentalizing (medial prefrontal cortex, left temporoparietal junction, right temporoparietal junction), reward (ventromedial prefrontal cortex), and self-control (right ventrolateral prefrontal cortex). These results suggest that mental state reasoning, social reward and self-control processes may help adolescents to evaluate others’ perspectives and overcome the prepotent force of their own antecedent attitudes to shift their attitudes toward those of others. Findings suggest common neural networks involved in social influence from both parents and peers.     

The ability to decide advantageously declines prematurely in some normal older persons

The prefrontal region of the brain, including the ventromedial sector which supports reasoning and decision-making, may undergo disproportionate aging in some older persons, but the empirical evidence is decidedly mixed. To help resolve this, we tested 80 neurologically and psychiatrically healthy Younger (aged 26-55) and Older (aged 56-85) adults on a "Gambling Task", which provides a close analog to real-world decision-making by factoring in reward, punishment, and unpredictability, yielding a sensitive index of ventromedial prefrontal function. A subset of the Older group manifested a decision-making impairment on the Gambling Task, in spite of otherwise intact cognitive functioning. This finding raises the possibility of disproportionate aging of the ventromedial prefrontal cortex in these individuals. Our finding has important societal and public policy implications (e.g., choosing medical care, allocating personal wealth), and may also help explain why many older individuals are targeted by and susceptible to fraudulent advertising.     

Being liked activates primary reward and midline self‐related brain regions

The experience of being liked is a key social event and fundamental to motivating human behavior, though little is known about its neural underpinnings. In this study, we examined the experience of being liked in a group of 15‐ to 24‐year‐old: a cohort for whom forming friendships has a great degree of salience, and for whom the explicit representation of relationships is familiar from their frequent use of social networking technologies. Study participants (n = 19) were led to believe that other participants had formed an opinion on their likability based on their appearance in a photograph, and during fMRI scanning viewed the photographs of people who had purportedly responded favorably to them (alongside photographs of control participants). Results indicated that being liked activated primary reward‐ and self‐related regions, including the nucleus accumbens, midbrain (in an area corresponding to the ventral tegmentum), ventromedial prefrontal cortex, posterior cingulate cortex (including retrosplenial cortex), amygdala, and insula/opercular cortex. Participants showed greater activation of ventromedial prefrontal cortex and amygdala in response to being liked by people that they regarded highly compared to those they regarded less so. Finally, being liked by the opposite compared to the same gender activated the right caudal orbitofrontal cortex and right anterior insula: areas important for the representation of primary somatic rewards. This study demonstrates that neural response to being liked has features that are consistent with response to other rewarding events, but it has additional features that reflect its intrinsically interpersonal character. Hum Brain Mapp, 2010. © 2009 Wiley‐Liss, Inc.     

Phineas gauged: decision-making and the human prefrontal cortex

Poor social judgment and decision-making abilities have often been attributed to people who have suffered injury to the ventromedial prefrontal cortex (VMPFC). However, few laboratory tests of decision-making have been conducted on these patients. The exception to this is the Iowa Gambling Task which has often, but not always, demonstrated differential performance between patients and controls. Results from patients with prefrontal cortex lesions on a novel test of decision-making are presented. Participants explored and chose from pairs of gambles that differed in their underlying distributions, primarily in the variance of their respective outcomes. In accordance with many findings from the behavioral decision-making literature, both young normal participants and older patient controls demonstrated a marked avoidance of risk and selected largely from secure, low variance gambles. In contrast, patients with ventromedial lesions were divided into two clear sub-groups. One group behaved similarly to normals, showing a risk-averse strategy. The other group displayed a distinctive risk-seeking behavior pattern, choosing predominantly from the high-variance, high-risk decks. This research demonstrates some of the advantages of using methods and theories from traditional decision-making research to study the behavior of patients, as well as the benefits of examining individual participants, and provides new insights into the nature of the decision-making deficit in patients with ventromedial prefrontal cortex lesions.     

Impulsive personality and the ability to resist immediate reward: An fMRI study examining interindividual differences in the neural mechanisms underlying self-control

The ability to resist immediate rewards is crucial for lifetime success and individual well‐being. Using functional magnetic resonance imaging, we assessed the association between trait impulsivity and the neural underpinnings of the ability to control immediate reward desiring. Low and high extreme impulsivity groups were compared with regard to their behavioral performance and brain activation in situations, in which they had to forego immediate rewards with varying value to achieve a superordinate long‐term goal. We found that highly impulsive (HI) individuals, who successfully compensated for their lack in behavioral self‐control, engaged two complementary brain mechanisms when choosing actions in favor of a long‐term goal, but at the expense of an immediate reward. First, self‐controlled decisions led to a general attenuation of reward‐related activation in the nucleus accumbens, which was accompanied by an increased inverse connectivity with the anteroventral prefrontal cortex. Second, HI subjects controlled their desire for increasingly valuable, but suboptimal rewards through a linear reduction of activation in the ventromedial prefrontal cortex (VMPFC). This was achieved by an increased inverse coupling between the VMPFC and the ventral striatum. Importantly, the neural mechanisms observed in the HI group differed from those in extremely controlled individuals, despite similar behavioral performance. Collectively, these results suggest trait‐specific neural mechanisms that allow HI individuals to control their desire for immediate reward. Hum Brain Mapp, 2012. © 2011 Wiley Periodicals, Inc.     

The effects of intranasal oxytocin on reward circuitry responses in children with autism spectrum disorder

Background

Intranasal oxytocin (OT) has been shown to improve social communication functioning of individuals with autism spectrum disorder (ASD) and, thus, has received considerable interest as a potential ASD therapeutic agent. Although preclinical research indicates that OT modulates the functional output of the mesocorticolimbic dopamine system that processes rewards, no clinical brain imaging study to date has examined the effects of OT on this system using a reward processing paradigm. To address this, we used an incentive delay task to examine the effects of a single dose of intranasal OT, versus placebo (PLC), on neural responses to social and nonsocial rewards in children with ASD.

Methods

In this placebo-controlled double-blind study, 28 children and adolescents with ASD (age: M?=?13.43 years, SD?=?2.36) completed two fMRI scans, one after intranasal OT administration and one after PLC administration. During both scanning sessions, participants completed social and nonsocial incentive delay tasks. Task-based neural activation and connectivity were examined to assess the impact of OT relative to PLC on mesocorticolimbic brain responses to social and nonsocial reward anticipation and outcomes.

Results

Central analyses compared the OT and PLC conditions. During nonsocial reward anticipation, there was greater activation in the right nucleus accumbens (NAcc), left anterior cingulate cortex (ACC), bilateral orbital frontal cortex (OFC), left superior frontal cortex, and right frontal pole (FP) during the OT condition relative to PLC. Alternatively, during social reward anticipation and outcomes, there were no significant increases in brain activation during the OT condition relative to PLC. A Treatment Group × Reward Condition interaction revealed relatively greater activation in the right NAcc, right caudate nucleus, left ACC, and right OFC during nonsocial relative to social reward anticipation during the OT condition relative to PLC. Additionally, these analyses revealed greater activation during nonsocial reward outcomes during the OT condition relative to PLC in the right OFC and left FP. Finally, functional connectivity analyses generally revealed changes in frontostriatal connections during the OT condition relative to PLC in response to nonsocial, but not social, rewards.

Conclusions

The effects of intranasal OT administration on mesocorticolimbic brain systems that process rewards in ASD were observable primarily during the processing of nonsocial incentive salience stimuli. These findings have implications for understanding the effects of OT on neural systems that process rewards, as well as for experimental trials of novel ASD treatments developed to ameliorate social communication impairments in ASD.

     

Responses to Heartbeats in Ventromedial Prefrontal Cortex Contribute to Subjective Preference-Based Decisions

Forrest Gump or The Matrix? Preference-based decisions are subjective and entail self-reflection. However, these self-related features are unaccounted for by known neural mechanisms of valuation and choice. Self-related processes have been linked to a basic interoceptive biological mechanism, the neural monitoring of heartbeats, in particular in ventromedial prefrontal cortex (vmPFC), a region also involved in value encoding. We thus hypothesized a functional coupling between the neural monitoring of heartbeats and the precision of value encoding in vmPFC. Human participants of both sexes were presented with pairs of movie titles. They indicated either which movie they preferred or performed a control objective visual discrimination that did not require self-reflection. Using magnetoencephalography, we measured heartbeat-evoked responses (HERs) before option presentation and confirmed that HERs in vmPFC were larger when preparing for the subjective, self-related task. We retrieved the expected cortical value network during choice with time-resolved statistical modeling. Crucially, we show that larger HERs before option presentation are followed by stronger value encoding during choice in vmPFC. This effect is independent of overall vmPFC baseline activity. The neural interaction between HERs and value encoding predicted preference-based choice consistency over time, accounting for both interindividual differences and trial-to-trial fluctuations within individuals. Neither cardiac activity nor arousal fluctuations could account for any of the effects. HERs did not interact with the encoding of perceptual evidence in the discrimination task. Our results show that the self-reflection underlying preference-based decisions involves HERs, and that HER integration to subjective value encoding in vmPFC contributes to preference stability.SIGNIFICANCE STATEMENT Deciding whether you prefer Forrest Gump or The Matrix is based on subjective values, which only you, the decision-maker, can estimate and compare, by asking yourself. Yet, how self-reflection is biologically implemented and its contribution to subjective valuation are not known. We show that in ventromedial prefrontal cortex, the neural response to heartbeats, an interoceptive self-related process, influences the cortical representation of subjective value. The neural interaction between the cortical monitoring of heartbeats and value encoding predicts choice consistency (i.e., whether you consistently prefer Forrest Gump over Matrix over time. Our results pave the way for the quantification of self-related processes in decision-making and may shed new light on the relationship between maladaptive decisions and impaired interoception.     

The neural substrates of person perception: spontaneous use of financial and moral status knowledge

The current study examines the effect of status information on the neural substrates of person perception. In an event-related fMRI experiment, participants were presented with photographs of faces preceded with information denoting either: low or high financial status (e.g., "earns $25,000" or "earns $350,000"), or low or high moral status (e.g., "is a tobacco executive" or "does cancer research"). Participants were asked to form an impression of the targets, but were not instructed to explicitly evaluate their social status. Building on previous brain-imaging investigations, regions of interest analyses were performed for brain regions expected to support either cognitive (i.e., intraparietal sulcus) or emotional (i.e., ventromedial prefrontal cortex) components of social status perception. Activation of the intraparietal sulcus was found to be sensitive to the financial status of individuals while activation of the ventromedial prefrontal cortex was sensitive to the moral status of individuals. The implications of these results towards uncovering the neural substrates of status perception and, more broadly, the extended network of brain regions involved in person perception are discussed.     

Behavioral inhibition and prefrontal cortex in decision-making.

Every day we make innumerable decisions; some require no effort at all whereas others require considerable deliberation and weighing of various options. Despite the importance of decision-making in our lives and increased research interest, the specific neural mechanisms underlying decision-making remain unclear. We propose that the brain has at least two cortical pathways that independently generate a decision about appropriate behavior in given circumstances. These two pathways are extensions of the dorsal and ventral streams of the visual processing pathways. The parieto-premotor (extended dorsal) pathway makes decisions about motor actions in a largely autonomous and automatic fashion whereas the temporo-ventrolateral prefrontal (extended ventral) pathway is involved primarily in deliberate decisions and inhibitory control over behavior through the inhibitory function of the ventrolateral prefrontal cortex.