Berna Güroğlu

Social exclusion and punishment of excluders: neural correlates and developmental trajectories

Social exclusion is a distressing experience and can result in a reduction of prosocial behavior. In this fMRI study we examined the neural networks involved in social exclusion and subsequent fairness considerations across adolescent development. Participants from 3 age groups (10-12, 14-16 and 19-21 year olds) participated in the study and performed two tasks; first, participants played Cyberball to induce feelings of social inclusion and exclusion, followed by a Dictator game in which participants were asked to divide coins between themselves and the players who previously included or excluded them. Results revealed a network of regions associated with social exclusion, which involve the medial prefrontal cortex (mPFC)/ventral anterior cingulate cortex (vACC), subgenual ACC and the lateral PFC, as well as the insula and the dorsal ACC. Although social exclusion generated strong distress for all age groups, 10-12 year olds showed increased activity in the subgenual ACC in the exclusion game, which has been associated in previous studies with negative affective processing. Results of the Dictator game revealed that all age groups selectively punished the excluders by making lower offers. These offers were associated with activation in the temporoparietal junction (TPJ), superior temporal sulcus (STS) and the lateral PFC. Age comparisons revealed that adults showed additional activity in the insula and dorsal ACC when making offers to the excluders. The results are discussed in the light of recent findings on neural networks involved in social exclusion and the development of social brain regions.

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.

Testosterone levels correspond with increased ventral striatum activation in response to monetary rewards in adolescents.

Risk taking is an integral part of learning and development, particularly during adolescence the prevalence of risky behaviors peak. It is hypothesized that the tendency to take risks is related to pubertal maturation, where there is interplay between gonadal hormones, the neural mechanisms that underlie affective (e.g., reward) processing, and risky behavior. To test this hypothesis, fifty healthy adolescents (aged 10-16 years; 33 girls, 17 boys) at different stages of puberty performed a gambling task while lying in the MRI scanner, and provided saliva samples for hormone assessment. Gonadal hormone levels were correlated with the neural response to receiving a monetary reward. Results showed that testosterone level correlated positively with activation in the striatum for both boys and girls, suggesting that individual differences in hormones at puberty are related to the way adolescents respond to reward, which can ultimately affect risk-taking behavior.

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.

Structural brain development between childhood and adulthood: Convergence across four longitudinal samples

Longitudinal studies including brain measures acquired through magnetic resonance imaging (MRI) have enabled population models of human brain development, crucial for our understanding of typical development as well as neurodevelopmental disorders. Brain development in the first two decades generally involves early cortical grey matter volume (CGMV) increases followed by decreases, and monotonic increases in cerebral white matter volume (CWMV). However, inconsistencies regarding the precise developmental trajectories call into question the comparability of samples. This issue can be addressed by conducting a comprehensive study across multiple datasets from diverse populations. Here, we present replicable models for gross structural brain development between childhood and adulthood (ages 8–30 years) by repeating analyses in four separate longitudinal samples (391 participants; 852 scans). In addition, we address how accounting for global measures of cranial/brain size affect these developmental trajectories. First, we found evidence for continued development of both intracranial volume (ICV) and whole brain volume (WBV) through adolescence, albeit following distinct trajectories. Second, our results indicate that CGMV is at its highest in childhood, decreasing steadily through the second decade with deceleration in the third decade, while CWMV increases until mid-to-late adolescence before decelerating. Importantly, we show that accounting for cranial/brain size affects models of regional brain development, particularly with respect to sex differences. Our results increase confidence in our knowledge of the pattern of brain changes during adolescence, reduce concerns about discrepancies across samples, and suggest some best practices for statistical control of cranial volume and brain size in future studies.

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.

Development of the Cerebral Cortex across Adolescence: A Multisample Study of Inter-Related Longitudinal Changes in Cortical Volume, Surface Area, and Thickness

Before we can assess and interpret how developmental changes in human brain structure relate to cognition, affect, and motivation, and how these processes are perturbed in clinical or at-risk populations, we must first precisely understand typical brain development and how changes in different structural components relate to each other. We conducted a multisample magnetic resonance imaging study to investigate the development of cortical volume, surface area, and thickness, as well as their inter-relationships, from late childhood to early adulthood (7–29 years) using four separate longitudinal samples including 388 participants and 854 total scans. These independent datasets were processed and quality-controlled using the same methods, but analyzed separately to study the replicability of the results across sample and image-acquisition characteristics. The results consistently showed widespread and regionally variable nonlinear decreases in cortical volume and thickness and comparably smaller steady decreases in surface area. Further, the dominant contributor to cortical volume reductions during adolescence was thinning. Finally, complex regional and topological patterns of associations between changes in surface area and thickness were observed. Positive relationships were seen in sulcal regions in prefrontal and temporal cortices, while negative relationships were seen mainly in gyral regions in more posterior cortices. Collectively, these results help resolve previous inconsistencies regarding the structural development of the cerebral cortex from childhood to adulthood, and provide novel insight into how changes in the different dimensions of the cortex in this period of life are inter-related. SIGNIFICANCE STATEMENT Different measures of brain anatomy develop differently across adolescence. Their precise trajectories and how they relate to each other throughout development are important to know if we are to fully understand both typical development and disorders involving aberrant brain development. However, our understanding of such trajectories and relationships is still incomplete. To provide accurate characterizations of how different measures of cortical structure develop, we performed an MRI investigation across four independent datasets. The most profound anatomical change in the cortex during adolescence was thinning, with the largest decreases observed in the parietal lobe. There were complex regional patterns of associations between changes in surface area and thickness, with positive relationships seen in sulcal regions in prefrontal and temporal cortices, and negative relationships seen mainly in gyral regions in more posterior cortices.

Chronic childhood peer rejection is associated with heightened neural responses to social exclusion during adolescence

This functional Magnetic Resonance Imaging (fMRI) study examined subjective and neural responses to social exclusion in adolescents (age 12–15) who either had a stable accepted (n = 27; 14 males) or a chronic rejected (n = 19; 12 males) status among peers from age 6 to 12. Both groups of adolescents reported similar increases in distress after being excluded in a virtual ball-tossing game (Cyberball), but adolescents with a history of chronic peer rejection showed higher activity in brain regions previously linked to the detection of, and the distress caused by, social exclusion. Specifically, compared with stably accepted adolescents, chronically rejected adolescents displayed: 1) higher activity in the dorsal anterior cingulate cortex (dACC) during social exclusion and 2) higher activity in the dACC and anterior prefrontal cortex when they were incidentally excluded in a social interaction in which they were overall included. These findings demonstrate that chronic childhood peer rejection is associated with heightened neural responses to social exclusion during adolescence, which has implications for understanding the processes through which peer rejection may lead to adverse effects on mental health over time.

Sharing and giving across adolescence: an experimental study examining the development of prosocial behavior

In this study we use economic exchange games to examine the development of prosocial behavior in the form of sharing and giving in social interactions with peers across adolescence. Participants from four age groups (9-, 12-, 15-, and 18-year-olds, total N = 119) played three types of distribution games and the Trust game with four different interaction partners: friends, antagonists, neutral classmates, and anonymous peers. Nine- and 12-year-olds showed similar levels of prosocial behavior to all interaction partners, whereas older adolescents showed increasing differentiation in prosocial behavior depending on the relation with peers, with most prosocial behavior toward friends. The age related increase in non-costly prosocial behavior toward friends was mediated by self-reported perspective-taking skills. Current findings extend existing evidence on the developmental patterns of fairness considerations from childhood into late adolescence. Together, we show that adolescents are increasingly better at incorporating social context into decision-making. Our findings further highlight the role of friendships as a significant social context for the development of prosocial behavior in early adolescence.

Neural correlates of social decision making and relationships: a developmental perspective.

Social competence, e.g., effective functioning in interpersonal relationships, plays an important role in well being during ones lifetime. Social skills, such as perspective taking and understanding intentionality, develop during childhood and adolescence. We hypothesize that these behavioral changes result from protracted development of brain regions involved in social interactions. We give a brief outline of behavioral and neuroimaging studies on fairness, trust, and reciprocity considerations in social decision making and the development of these considerations. We propose that a better understanding of the mechanisms underlying the developing brain and sociocognitive skills is important for understanding the development of social relationships.