Wouter van den Bos

Changing Brains, Changing Perspectives The Neurocognitive Development of Reciprocity

Adolescence is characterized by the emergence of advanced forms of social perspective taking and significant changes in social behavior. Yet little is known about how changes in social cognition are related to changes in brain function during adolescence. In this study, we investigated the neural correlates of social behavior during three phases of adolescence, carrying out functional magnetic resonance imaging of participants’ brains while they were Player 2 in the Trust Game. We found that with age, adolescents were increasingly sensitive to the perspective of the other player, as indicated by their reciprocal behavior. These advanced forms of social perspective-taking behavior were associated with increased involvement of the left temporo-parietal junction and the right dorsolateral prefrontal cortex. In contrast, young adolescents showed more activity in the anterior medial prefrontal cortex, a region previously associated with self-oriented processing and mentalizing. These findings suggest that the asynchronous development of these neural systems may underlie the shift from thinking about self to thinking about the other.

Striatum–Medial Prefrontal Cortex Connectivity Predicts Developmental Changes in Reinforcement Learning

During development, children improve in learning from feedback to adapt their behavior. However, it is still unclear which neural mechanisms might underlie these developmental changes. In the current study, we used a reinforcement learning model to investigate neurodevelopmental changes in the representation and processing of learning signals. Sixty-seven healthy volunteers between ages 8 and 22 (children: 8-11 years, adolescents: 13-16 years, and adults: 18-22 years) performed a probabilistic learning task while in a magnetic resonance imaging scanner. The behavioral data demonstrated age differences in learning parameters with a stronger impact of negative feedback on expected value in children. Imaging data revealed that the neural representation of prediction errors was similar across age groups, but functional connectivity between the ventral striatum and the medial prefrontal cortex changed as a function of age. Furthermore, the connectivity strength predicted the tendency to alter expectations after receiving negative feedback. These findings suggest that the underlying mechanisms of developmental changes in learning are not related to differences in the neural representation of learning signals per se but rather in how learning signals are used to guide behavior and expectations.

Unfair? It depends: Neural correlates of fairness in social context

Fairness is a key concept in social interactions and is influenced by intentionality considerations. In this functional magnetic resonance imaging study, we investigated the neural correlates of fairness by focusing on responder behavior to unfair offers in an Ultimatum Game paradigm with conditions that differed in their intentionality constraints. Brain activity underlying rejection vs acceptance of unfair offers appeared highly dependent on intentionality. Rejection of unfair offers when the proposer had no-alternative as well as acceptance of offers when the proposer had a fair- or hyperfair-alternative was associated with activation in a network of regions including the insula and the dorsal medial prefrontal cortex. These activations were interpreted as neural responses to norm violations because they were mostly involved when behavior was inconsistent with socially accepted behavior patterns. Rejection of unfair offers in the no-alternative condition further resulted in activity in the anterior medial prefrontal cortex and the temporoparietal junction, which was interpreted in terms of higher moral mentalizing demands required in social decision-making when rejection could not be readily justified. Together, results highlight the significance of intentionality considerations in fairness-related social decision-making processes.

Dissociable brain networks involved in development of fairness considerations: Understanding intentionality behind unfairness

In this functional magnetic resonance imaging study, we examined developmental changes in the brain regions involved in reactions to unfair allocations. Previous studies on adults suggested that reactions to unfairness are not only affected by the distribution itself but also by the ascribed intentionality of the proposer. In the current study, we employed the mini Ultimatum Game (Falk, Fehr, & Fischbacher, 2003) to examine responder behavior to unfair offers of varying degrees of intentionality. Sixty-eight participants from four age groups (10-, 13-, 15-, and 20-year-olds) carried out the task while fMRI data were acquired. Participants of all ages showed activation in the bilateral insula and dorsal anterior cingulate cortex (dACC) during rejection of unintentional but acceptance of intentional unfair offers. Rejection of unintentional unfair offers further involved increasing activation with age in the temporoparietal junction and the dorsolateral prefrontal cortex. These findings provide evidence for an early developing insula-dACC network involved in detecting personal norm-violations and gradually increasing involvement of temporal and prefrontal brain regions related to intentionality considerations in social reasoning. The results are discussed in light of recent findings on the development of the adolescent social brain network.

What motivates repayment? Neural correlates of reciprocity in the Trust Game

Reciprocity of trust is important for social interaction and depends on individual differences in social value orientation (SVO). Here, we examined the neural correlates of reciprocity by manipulating two factors that influence reciprocal behavior: (1) the risk that the trustor took when trusting and (2) the benefit for the trustee when being trusted. FMRI results showed that anterior Medial Prefrontal Frontal Cortex (aMPFC) was more active when participants defected relative to when participants reciprocated, but was not sensitive to manipulations of risk and benefit or individual differences in SVO. However, activation in the temporal-parietal-junction (rTPJ), bilateral anterior insula and anterior cingulate cortex (ACC) was modulated by individual differences in SVO. In addition, these regions were differentially sensitive to manipulations of risk for the trustor when reciprocating. In contrast, the ACC and the right dorsolateral prefrontal cortex were sensitive to the benefit for the trustee when reciprocating. Together, the results of this study provide more insight in how several brain regions work together when individuals reciprocate trust, by showing how these regions are differentially sensitive to reciprocity motives and perspective-taking.

Adolescent impatience decreases with increased frontostriatal connectivity

Significance Compared with children and adults, teens and young adults often exhibit greater impulsivity and corresponding increases in emergency room visits, accidents from drug or alcohol use, and increased mortality risk. However, it remains poorly understood how increased impulsivity during adolescence may be explained in terms of brain and cognitive development. We focused on impatience, a central component of impulsiveness. We relate impatient behavior on a decision-making task to changes in connectivity within the brain’s frontostriatal circuitry. Our results suggest that relative future orientation, not sensitivity to immediate rewards, determines adolescent impatience. These findings may help to design interventions to prevent the detrimental effects of adolescent impulsiveness and serve as a template for understanding neurodevelopmental disorders. Adolescence is a developmental period associated with an increase in impulsivity. Impulsivity is a multidimensional construct, and in this study we focus on one of the underlying components: impatience. Impatience can result from (i) disregard of future outcomes and/or (ii) oversensitivity to immediate rewards, but it is not known which of these evaluative processes underlie developmental changes. To distinguish between these two causes, we investigated developmental changes in the structural and functional connectivity of different frontostriatal tracts. We report that adolescents were more impatient on an intertemporal choice task and reported less future orientation, but not more present hedonism, than young adults. Developmental increases in structural connectivity strength in the right dorsolateral prefrontal tract were related to increased negative functional coupling with the striatum and an age-related decrease in discount rates. Our results suggest that mainly increased control, and the integration of future-oriented thought, drives the reduction in impatience across adolescence.

Regions of the MPFC differentially tuned to social and nonsocial affective evaluation

The medial prefrontal cortex (MPFC) reliably activates in social cognition and reward tasks. This study locates distinct areas for each. Participants made evaluative (positive/negative) or social (person/not a person) judgments of pictured positive or negative people and objects in a slow event-related design. Activity in an anterior rostral region (arMPFC) was significantly greater for positive than for negative persons but did not show a valence effect for objects, and this was true regardless of the judgment task. This suggests that the arMPFC is tuned to social valence. Interestingly, however, no regions of the MPFC were found to be responsive to social information independently of valence. A region-of-interest analysis of the paraanterior cingulate cortex (pACC), previously implicated in reward processing, demonstrated sensitivity to the valence of all stimuli, whether persons or objects, across tasks. Affective evaluation may be a general function of the MPFC, with some regions being tuned to more specific domains of information (e.g., social) than are others.

Connectivity Strength of Dissociable Striatal Tracts Predict Individual Differences in Temporal Discounting

Large individual differences exist in the ability to delay gratification for the sake of satisfying longer-term goals. These individual differences are commonly assayed by studying intertemporal preferences, as revealed by choices between immediate and delayed rewards. In the brain, reward-based and goal-oriented decisions are believed to rely on the striatum and its interactions with other cortical and subcortical networks. However, it remains unknown which specific cortical-striatal tracts are involved in intertemporal decision making. We use connectivity analyses in both structural and functional MRI to further our understanding of the relationship between distinct corticostriatal networks and intertemporal preferences in humans. Our results revealed distinct striatal pathways that are differentially related to delay discounting. Structural and functional connectivity between striatum and lateral prefrontal cortex was associated with increased patience, whereas connectivity between subcortical areas and striatum was associated with increased impulsivity. These findings provide novel insights into how the anatomy and functioning of striatal circuits mediate individual differences in intertemporal choice.

Better than expected or as bad as you thought? The neurocognitive development of probabilistic feedback processing

Learning from feedback lies at the foundation of adaptive behavior. Two prior neuroimaging studies have suggested that there are qualitative differences in how children and adults use feedback by demonstrating that dorsolateral prefrontal cortex (DLPFC) and parietal cortex were more active after negative feedback for adults, but after positive feedback for children. In the current study we used functional magnetic resonance imaging (fMRI) to test whether this difference is related to valence or informative value of the feedback by examining neural responses to negative and positive feedback while applying probabilistic rules. In total, 67 healthy volunteers between ages 8 and 22 participated in the study (8–11 years, n = 18; 13–16 years, n = 27; 18–22 years, n = 22). Behavioral comparisons showed that all participants were able to learn probabilistic rules equally well. DLPFC and dorsal anterior cingulate cortex were more active in younger children following positive feedback and in adults following negative feedback, but only when exploring alternative rules, not when applying the most advantageous rules. These findings suggest that developmental differences in neural responses to feedback are not related to valence per se, but that there is an age-related change in processing learning signals with different informative value.

Towards a general model of temporal discounting.

Psychological models of temporal discounting have now successfully displaced classical economic theory due to the simple fact that many common behavior patterns, such as impulsivity, were unexplainable with classic models. However, the now dominant hyperbolic model of discounting is itself becoming increasingly strained. Numerous factors have arisen that alter discount rates with no means to incorporate the different influences into standard hyperbolic models. Furthermore, disparate literatures are emerging that propose theoretical constructs that are seemingly independent of hyperbolic discounting. We argue that, although hyperbolic discounting provides an eminently useful quantitative measure of discounting, it fails as a descriptive psychological model of the cognitive processes that produce intertemporal preferences. Instead, we propose that recent contributions from cognitive neuroscience indicate a path for developing a general model of time discounting. New data suggest a means by which neuroscience-based theory may both integrate the diverse empirical data on time preferences and merge seemingly disparate theoretical models that impinge on time preferences.