Age-related differences in ventral striatal and default mode network function during reciprocated trust.

Social relationships change across the lifespan as social networks narrow and motivational priorities shift to the present. Interestingly, aging is also associated with changes in executive function, including decision-making abilities, but it remains unclear how age-related changes in both domains interact to impact financial decisions involving other people. To study this problem, we recruited 50 human participants (Nyounger = 26, ages 18-34; Nolder = 24, ages 63-80) to play an economic trust game as the investor with three partners (friend, stranger, and computer) who played the role of investee. Investors underwent functional magnetic resonance imaging (fMRI) during the trust game while investees were seated outside of the scanner. Building on our previous work with younger adults showing both enhanced striatal responses and altered default-mode network (DMN) connectivity as a function of social closeness during reciprocated trust, we predicted that these relations would exhibit age-related differences. We found that striatal responses to reciprocated trust from friends relative to strangers and computers were blunted in older adults relative to younger adults, thus supporting our primary pre-registered hypothesis regarding social closeness. We also found that older adults exhibited enhanced DMN connectivity with the temporoparietal junction (TPJ) during reciprocated trust from friends compared to computers while younger adults exhibited the opposite pattern. Taken together, these results advance our understanding of age-related differences in sensitivity to social closeness in the context of trusting others.

Age-related change in task-evoked amygdala-prefrontal circuitry: A multiverse approach with an accelerated longitudinal cohort aged 4-22 years.

The amygdala and its connections with medial prefrontal cortex (mPFC) play central roles in the development of emotional processes. While several studies have suggested that this circuitry exhibits functional changes across the first two decades of life, findings have been mixed - perhaps resulting from differences in analytic choices across studies. Here we used multiverse analyses to examine the robustness of task-based amygdala-mPFC function findings to analytic choices within the context of an accelerated longitudinal design (4-22 years-old; N = 98; 183 scans; 1-3 scans/participant). Participants recruited from the greater Los Angeles area completed an event-related emotional face (fear, neutral) task. Parallel analyses varying in preprocessing and modeling choices found that age-related change estimates for amygdala reactivity were more robust than task-evoked amygdala-mPFC functional connectivity to varied analytical choices. Specification curves indicated evidence for age-related decreases in amygdala reactivity to faces, though within-participant changes in amygdala reactivity could not be differentiated from between-participant differences. In contrast, amygdala-mPFC functional connectivity results varied across methods much more, and evidence for age-related change in amygdala-mPFC connectivity was not consistent. Generalized psychophysiological interaction (gPPI) measurements of connectivity were especially sensitive to whether a deconvolution step was applied. Our findings demonstrate the importance of assessing the robustness of findings to analysis choices, although the age-related changes in our current work cannot be overinterpreted given low test-retest reliability. Together, these findings highlight both the challenges in estimating developmental change in longitudinal cohorts and the value of multiverse approaches in developmental neuroimaging for assessing robustness of results.

Experimental evidence for a child-to-adolescent switch in human amygdala-prefrontal cortex communication: A cross-sectional pilot study.

Interactions between the amygdala and prefrontal cortex are fundamental to human emotion. Despite the central role of frontoamygdala communication in adult emotional learning and regulation, little is known about how top-down control emerges during human development. In the present cross-sectional pilot study, we experimentally manipulated prefrontal engagement to test its effects on the amygdala during development. Inducing dorsal anterior cingulate cortex (dACC) activation resulted in developmentally-opposite effects on amygdala reactivity during childhood versus adolescence, such that dACC activation was followed by increased amygdala reactivity in childhood but reduced amygdala reactivity in adolescence. Bayesian network analyses revealed an age-related switch between childhood and adolescence in the nature of amygdala connectivity with the dACC and ventromedial PFC (vmPFC). Whereas adolescence was marked by information flow from dACC and vmPFC to amygdala (consistent with that observed in adults), the reverse information flow, from the amygdala to dACC and vmPFC, was dominant in childhood. The age-related switch in information flow suggests a potential shift from bottom-up co-excitatory to top-down regulatory frontoamygdala connectivity and may indicate a profound change in the circuitry supporting maturation of emotional behavior. These findings provide novel insight into the developmental construction of amygdala-cortical connections and implications for the ways in which childhood experiences may influence subsequent prefrontal function.

Parent-Child Attachment Security and Depressive Symptoms in Early Adolescence: The Mediating Roles of Gratitude and Forgiveness.

Although greater parent-child attachment security is linked with children's lower levels of depressive symptoms, little research has evaluated potential explanatory mechanisms. We investigated whether dispositional gratitude and interpersonal forgiveness explain the relation between attachment security with parents and early adolescents' depressive symptoms. Early adolescents (N = 105; M age = 12.3 years; 51% girls) completed questionnaires assessing their attachment security to mother and father figures, depressive symptoms, and dispositional gratitude, and an interview assessing interpersonal forgiveness. Results revealed that greater attachment security to mothers and fathers was associated with fewer depressive symptoms and greater levels of dispositional gratitude and interpersonal forgiveness. Further, dispositional gratitude and interpersonal forgiveness were negatively associated with depressive symptoms. Dispositional gratitude emerged as a mediator between attachment security with each parent and depressive symptoms. Our findings suggest that greater parent-child security may promote early adolescents' appreciation of positive events, which in turn may relate to fewer depressive symptoms.

Previous Institutionalization Is Followed by Broader Amygdala-Hippocampal-PFC Network Connectivity during Aversive Learning in Human Development.

UNLABELLED: Early institutional care can be profoundly stressful for the human infant, and, as such, can lead to significant alterations in brain development. In animal models, similar variants of early adversity have been shown to modify amygdala-hippocampal-prefrontal cortex development and associated aversive learning. The current study examined this rearing aberration in human development. Eighty-nine children and adolescents who were either previously institutionalized (PI youth; N = 46; 33 females and 13 males; age range, 7-16 years) or were raised by their biological parents from birth (N = 43; 22 females and 21 males; age range, 7-16 years) completed an aversive-learning paradigm while undergoing functional neuroimaging, wherein visual cues were paired with either an aversive sound (CS+) or no sound (CS-). For the PI youth, better aversive learning was associated with higher concurrent trait anxiety. Both groups showed robust learning and amygdala activation for CS+ versus CS- trials. However, PI youth also exhibited broader recruitment of several regions and increased hippocampal connectivity with prefrontal cortex. Stronger connectivity between the hippocampus and ventromedial PFC predicted significant improvements in future anxiety (measured 2 years later), and this was particularly true within the PI group. These results suggest that for humans as well as for other species, early adversity alters the neurobiology of aversive learning by engaging a broader prefrontal-subcortical circuit than same-aged peers. These differences are interpreted as ontogenetic adaptations and potential sources of resilience. SIGNIFICANCE STATEMENT: Prior institutionalization is a significant form of early adversity. While nonhuman animal research suggests that early adversity alters aversive learning and associated neurocircuitry, no prior work has examined this in humans. Here, we show that youth who experienced prior institutionalization, but not comparison youth, recruit the hippocampus during aversive learning. Among youth who experienced prior institutionalization, individual differences in aversive learning were associated with worse current anxiety. However, connectivity between the hippocampus and prefrontal cortex prospectively predicted significant improvements in anxiety 2 years following scanning for previously institutionalized youth. Among youth who experienced prior institutionalization, age-atypical engagement of a distributed set of brain regions during aversive learning may serve a protective function.

Altered ventral striatal-medial prefrontal cortex resting-state connectivity mediates adolescent social problems after early institutional care.

Early caregiving adversity is associated with increased risk for social difficulties. The ventral striatum and associated corticostriatal circuitry, which have demonstrated vulnerability to early exposures to adversity, are implicated in many aspects of social behavior, including social play, aggression, and valuation of social stimuli across development. Here, we used resting-state functional magnetic resonance imaging to assess the degree to which early caregiving adversity was associated with altered coritocostriatal resting connectivity in previously institutionalized youth (n = 41) relative to youth who were raised with their biological families from birth (n = 47), and the degree to which this connectivity was associated with parent-reported social problems. Using a seed-based approach, we observed increased positive coupling between the ventral striatum and anterior regions of medial prefrontal cortex (mPFC) in previously institutionalized youth. Stronger ventral striatum-mPFC coupling was associated with parent reports of social problems. A moderated-mediation analysis showed that ventral striatal-mPFC connectivity mediated group differences in social problems, and more so with increasing age. These findings show that early institutional care is associated with differences in resting-state connectivity between the ventral striatum and the mPFC, and this connectivity seems to play an increasingly important role in social behaviors as youth enter adolescence.

Computational substrates of social value in interpersonal collaboration.

Decisions to engage in collaborative interactions require enduring considerable risk, yet provide the foundation for building and maintaining relationships. Here, we investigate the mechanisms underlying this process and test a computational model of social value to predict collaborative decision making. Twenty-six participants played an iterated trust game and chose to invest more frequently with their friends compared with a confederate or computer despite equal reinforcement rates. This behavior was predicted by our model, which posits that people receive a social value reward signal from reciprocation of collaborative decisions conditional on the closeness of the relationship. This social value signal was associated with increased activity in the ventral striatum and medial prefrontal cortex, which significantly predicted the reward parameters from the social value model. Therefore, we demonstrate that the computation of social value drives collaborative behavior in repeated interactions and provide a mechanistic account of reward circuit function instantiating this process.

Normative development of ventral striatal resting state connectivity in humans.

Incentives play a crucial role in guiding behavior throughout our lives, but perhaps no more so than during the early years of life. The ventral striatum is a critical piece of an incentive-based learning circuit, sharing robust anatomical connections with subcortical (e.g., amygdala, hippocampus) and cortical structures (e.g., medial prefrontal cortex (mPFC), insula) that collectively support incentive valuation and learning. Resting-state functional connectivity (rsFC) is a powerful method that provides insight into the development of the functional architecture of these connections involved in incentive-based learning. We employed a seed-based correlation approach to investigate ventral striatal rsFC in a cross-sectional sample of typically developing individuals between the ages of 4.5 and 23-years old (n=66). Ventral striatal rsFC with the mPFC showed regionally specific linear age-related changes in connectivity that were associated with age-related increases in circulating testosterone levels. Further, ventral striatal connectivity with the posterior hippocampus and posterior insula demonstrated quadratic age-related changes characterized by negative connectivity in adolescence. Finally, across this age range, the ventral striatum demonstrated positive coupling with the amygdala beginning during childhood and remaining consistently positive across age. In sum, our findings suggest that normative ventral striatal rsFC development is dynamic and characterized by early establishment of connectivity with medial prefrontal and limbic structures supporting incentive-based learning, as well as substantial functional reorganization with later developing regions during transitions into and out of adolescence.

Maternal buffering of human amygdala-prefrontal circuitry during childhood but not during adolescence.

Mature amygdala-prefrontal circuitry regulates affect in adulthood but shows protracted development. In altricial and semialtricial species, caregivers provide potent affect regulation when mature neurocircuitry is absent. The present investigation examined a potential mechanism through which caregivers provide regulatory influences in childhood. Children, but not adolescents, showed evidence of maternal buffering, such that maternal stimuli suppressed amygdala reactivity. In the absence of maternal stimuli, children exhibited immature amygdala-prefrontal connectivity. However, in the presence of maternal stimuli, children's connectivity was more mature, resembling adolescents' connectivity. Children showed improved affect-related regulation in the presence of their mothers. Individual differences emerged, with greater maternal influence on amygdala-prefrontal circuitry associated with stronger mother-child relationships and maternal modulation of behavioral regulation. These findings suggest a neural mechanism through which caregivers modulate children's regulatory behavior by inducing more mature connectivity and buffering against heightened reactivity. Maternal buffering in childhood, but not adolescence, suggests that childhood may be a sensitive period for amygdala-prefrontal development.

An fMRI Dataset on Social Reward Processing and Decision Making in Younger and Older Adults.

Behavioural and neuroimaging research has shown that older adults are less sensitive to financial losses compared to younger adults. Yet relatively less is known about age-related differences in social decisions and social reward processing. As part of a pilot study, we collected behavioural and functional magnetic resonance imaging (fMRI) data from 50 participants (Younger: N = 26, ages 18-34 years; Older: N = 24, ages 63-80 years) who completed three tasks in the scanner: an economic trust game as the investor with three partners (computer, stranger, friend) as the investee; a card-guessing task with monetary gains and losses shared with three partners (computer, stranger, friend); and an ultimatum game as responder to three anonymous proposers (computer, age-similar adults, age-dissimilar adults). We also collected B0 field maps and high-resolution structural images (T1-weighted and T2-weighted images). These data could be reused to answer questions about moment-to-moment variability in fMRI signal, representational similarity between tasks, and brain structure.

Social network modulation of reward-related signals.

Everyday goals and experiences are often shared with others who may hold different places within our social networks. We investigated whether the experience of sharing a reward differs with respect to social network. Twenty human participants played a card guessing game for shared monetary outcomes with three partners: a computer, a confederate (out of network), and a friend (in network). Participants subjectively rated the experience of sharing a reward more positively with their friends than the other partners. Neuroimaging results support participants' subjective reports, as ventral striatal BOLD responses were more robust when sharing monetary gains with a friend as compared to the confederate or computer, suggesting a higher value for sharing with an in-network partner. Interestingly, ratings of social closeness covaried with this activity, resulting in a significant partner × closeness interaction; exploratory analysis showed that only participants reporting higher levels of closeness demonstrated partner-related differences in striatal BOLD response. These results suggest that reward valuation in social contexts is sensitive to distinctions of social network, such that sharing positive experiences with in-network others may carry higher value.

Characterizing the mechanisms of social connection.

Understanding how individuals form and maintain strong social networks has emerged as a significant public health priority as a result of the increased focus on the epidemic of loneliness and the myriad protective benefits conferred by social connection. In this review, we highlight the psychological and neural mechanisms that enable us to connect with others, which in turn help buffer against the consequences of stress and isolation. Central to this process is the experience of rewards derived from positive social interactions, which encourage the sharing of perspectives and preferences that unite individuals. Sharing affective states with others helps us to align our understanding of the world with another's, thereby continuing to reinforce bonds and strengthen relationships. These psychological processes depend on neural systems supporting reward and social cognitive function. Lastly, we also consider limitations associated with pursuing healthy social connections and outline potential avenues of future research.

Social feedback promotes positive social sharing, trust, and closeness.

Positive social sharing is an interpersonal emotion regulation strategy that enhances positive affect and social belonging, particularly when met with positive social feedback. Despite the ubiquity of positive social sharing both in person and online, what drives this behavior is not well understood. We hypothesized that positive social feedback serves as a reward that reinforces sharing behavior and strengthens social bonds. Participants made trial-by-trial choices about whether to share social media photos with peers who returned positive ("likes") or negative ("dislikes") feedback. Unbeknownst to participants, peer conditions were manipulated to yield varying amounts of positive and negative feedback. Social bonding was subsequently measured using a trust game and subjective closeness ratings. Participants shared more with peers who provided greater rates of positive feedback. This effect generalized to trust decisions and subjective feelings of closeness and varied individually as a function of interpersonal emotion regulation in daily life. (PsycInfo Database Record (c) 2023 APA, all rights reserved).

Social Context and Reward Sensitivity Enhance Corticostriatal Function during Experiences of Shared Rewards.

Although prior research has demonstrated enhanced striatal response when sharing rewards with close social connections, less is known about how individual differences affect ventral striatal (VS) activation and connectivity when experiencing rewards within social contexts. Given that self-reported reward sensitivity and level of substance use have been associated with differences in VS activation, we set out to investigate whether these factors would be independently associated with enhancements to neural reward responses within social contexts. In this pre-registered study, participants (N=45) underwent fMRI while playing a card guessing game in which correct or incorrect guesses resulted in monetary gains and losses that were shared evenly with either a close friend, stranger (confederate), or non-human partner. Consistent with our prior work, we found increased VS activation when sharing rewards with a socially close peer as opposed to an out-of-network stranger. As self-reported reward sensitivity increased, the difference in VS response to rewards shared with friends and strangers decreased. We also found enhanced connectivity between the VS and temporoparietal junction when sharing rewards with close friends as opposed to strangers. Finally, exploratory analyses revealed that as reward sensitivity and sub-clinical substance use increase, the difference in VS connectivity with the right fusiform face area increases as a function of social context. These findings demonstrate that responsivity to the context of close friends may be tied to individual reward sensitivity or sub-clinical substance use habits; together these factors may inform predictions of risk for future mental health disorders.

Choosing for others changes dissociable computational mechanisms underpinning risky decision-making.

Choices under risk often have consequences for ourselves and others. Yet, it is unclear how the other's identity (stranger, close friend, etc.) influences risky choices made on their behalf. In a mixed within and between subjects design, two participant groups made three series of risky economic decisions: for themselves, another person, or for both themselves and another person (i.e., shared outcomes). One group made choices involving a same-sex stranger (n = 29), the other made choices involving a same-sex close friend (n = 28). Hierarchical Bayesian estimation of computations underlying risky decision-making revealed that relative to choosing for themselves, people were more risk averse, loss averse, and consistent when choices involved another person. Partner identity was additionally crucial: people became risk neutral and more consistent when choosing for friends relative to strangers. These findings establish that the complexity of the social world is mirrored in its nuanced consequences for our choices.

Longitudinal changes in amygdala, hippocampus and cortisol development following early caregiving adversity.

Although decades of research have shown associations between early caregiving adversity, stress physiology and limbic brain volume (e.g., amygdala, hippocampus), the developmental trajectories of these phenotypes are not well characterized. In the current study, we used an accelerated longitudinal design to assess the development of stress physiology, amygdala, and hippocampal volume following early institutional care. Previously Institutionalized (PI; N = 93) and comparison (COMP; N = 161) youth (ages 4-20 years old) completed 1-3 waves of data collection, each spaced approximately 2 years apart, for diurnal cortisol (N = 239) and structural MRI (N = 156). We observed a developmental shift in morning cortisol in the PI group, with blunted levels in childhood and heightened levels in late adolescence. PI history was associated with reduced hippocampal volume and reduced growth rate of the amygdala, resulting in smaller volumes by adolescence. Amygdala and hippocampal volumes were also prospectively associated with future morning cortisol in both groups. These results indicate that adversity-related physiological and neural phenotypes are not stationary during development but instead exhibit dynamic and interdependent changes from early childhood to early adulthood.

The influence of relationship closeness on default-mode network connectivity during social interactions.

Reciprocated trust plays a critical role in forming and maintaining relationships, and has consistently been shown to implicate neural circuits involved in reward-related processing and social cognition. Less is known about neural network connectivity during social interactions involving trust, however, particularly as a function of closeness between an investor and a trustee. We examined network reactivity and connectivity in participants who played an economic trust game with close friends, strangers and a computer. Network reactivity analyses showed enhanced activation of the default-mode network (DMN) to social relative to non-social outcomes. A novel network psychophysiological interaction (nPPI) analysis revealed enhanced connectivity between the DMN and the superior frontal gyrus and superior parietal lobule when experiencing reciprocated vs violated trust from friends relative to strangers. Such connectivity tracked with differences in self-reported social closeness with these partners. Interestingly, reactivity of the executive control network (ECN), involved in decision processes, demonstrated no social vs non-social preference, and ECN-ventral striatum connectivity did not track social closeness. Taken together, these novel findings suggest that DMN interacts with components of attention and control networks to signal the relative importance of positive experiences with close others vs strangers.

The Role of Social Reward and Corticostriatal Connectivity in Substance Use.

This report describes an ongoing R03 grant that explores the links between trait reward sensitivity, substance use, and neural responses to social and nonsocial reward. Although previous research has shown that trait reward sensitivity and neural responses to reward are linked to substance use, whether this relationship is impacted by how people process social stimuli remains unclear. We are investigating these questions via a neuroimaging study with college-aged participants, using individual difference measures that examine the relation between substance use, social context, and trait reward sensitivity with tasks that measure reward anticipation, strategic behavior, social reward consumption, and the influence of social context on reward processing. We predict that substance use will be tied to distinct patterns of striatal dysfunction. Specifically, reward hyposensitive individuals will exhibit blunted striatal responses to social and non-social reward and enhanced connectivity with the orbitofrontal cortex; in contrast, reward hypersensitive individuals will exhibit enhanced striatal responses to social and non-social reward and blunted connectivity with the orbitofrontal cortex. We also will examine the relation between self-reported reward sensitivity, substance use, and striatal responses to social reward and social context. We predict that individuals reporting the highest levels of substance use will show exaggerated striatal responses to social reward and social context, independent of self-reported reward sensitivity. Examining corticostriatal responses to reward processing will help characterize the relation between reward sensitivity, social context and substance use while providing a foundation for understanding risk factors and isolating neurocognitive mechanisms that may be targeted to increase the efficacy of interventions.

Neurobehavioral Mechanisms Supporting Trust and Reciprocity.

Trust and reciprocity are cornerstones of human nature, both at the levels of close interpersonal relationships and economic/societal structures. Being able to both place trust in others and decide whether to reciprocate trust placed in us is rooted in implicit and explicit processes that guide expectations of others, help reduce social uncertainty, and build relationships. This review will highlight neurobehavioral mechanisms supporting trust and reciprocity, through the lens of implicit and explicit social appraisal and learning processes. Significant consideration will be given to the neural underpinnings of these implicit and explicit processes, and special focus will center on the underlying neurocomputational mechanisms facilitating the integration of implicit and explicit signals supporting trust and reciprocity. Finally, this review will conclude with a discussion of how we can leverage findings regarding the neurobehavioral mechanisms supporting trust and reciprocity to better inform our understanding of mental health disorders characterized by social dysfunction.

Decreased Amygdala Reactivity to Parent Cues Protects Against Anxiety Following Early Adversity: An Examination Across 3 Years.

BACKGROUND: The human brain remains highly plastic for a protracted developmental period. Thus, although early caregiving adversities that alter amygdala development can result in enduring emotion regulation difficulties, these trajectories should respond to subsequent enriched caregiving. Exposure to high-quality parenting can regulate (i.e., decrease) children's amygdala reactivity, a process that, over the long term, is hypothesized to enhance emotion regulation. We tested the hypothesis that even following adversity, the parent-child relationship would be associated with decreases in amygdala reactivity to parent cues, which would in turn predict lower future anxiety. METHODS: Participants were 102 children (6-10 years of age) and adolescents (11-17 years of age), for whom data were collected at one or two time points and who either had experienced institutional care before adoption (n = 45) or had lived always with their biological parents (comparison; n = 57). We examined how amygdala reactivity to visual cues of the parent at time 1 predicted longitudinal change (from time 1 to time 2) in parent-reported child anxiety across 3 years. RESULTS: At time 1, on average, amygdala reactivity decrements to parent cues were not seen in children who had received institutional care but were seen in children in the comparison group. However, some children who previously experienced institutional care did show decreased amygdala reactivity to parent cues (∼40%), which was associated with greater child-reported feelings of security with their parent. Amygdala decreases at time 1 were followed by steeper anxiety reductions from time 1 to time 2 (i.e., 3 years). CONCLUSIONS: These data provide a neurobiological mechanism by which the parent-child relationship can increase resilience, even in children at significant risk for anxiety symptoms.