Transitioning from childhood into adolescence: A comprehensive longitudinal behavioral and neuroimaging study on prosocial behavior and social inclusion.

Acting prosocially and feeling socially included are important factors for developing social relations. However, little is known about the development of neural trajectories of prosocial behavior and social inclusion in the transition from middle childhood to early adolescence. In this pre-registered study, we investigated the development of prosocial behavior, social inclusion, and their neural mechanisms in a three-wave longitudinal design (ages 7-13 years; NT1 = 512; NT2 = 456; NT3 = 336). We used the Prosocial Cyberball Game, a ball tossing game in which one player is excluded, to measure prosocial compensating behavior. Prosocial compensating behavior showed a linear developmental increase, similar to parent-reported prosocial behavior, whereas parent-reported empathy showed a quadratic trajectory with highest levels in late childhood. On a neural level we found a peak in ventral striatum activity during prosocial compensating behavior. Neural activity during social inclusion showed quadratic age effects in anterior cingulate cortex, insula, striatum, and precuneus, and a linear increase in temporo-parietal junction. Finally, changes in prosocial compensating behavior were negatively associated with changes in ventral striatum and mPFC activity during social inclusion, indicating an important co-occurrence between development in brain and social behavior. Together these findings shed a light on the mechanisms underlying social development from childhood into adolescence.

Longitudinal associations between prosocial behavior and behavioral problems across childhood: A robust random-intercept cross-lagged panel model.

Prior studies have indicated that prosocial behavior might be a protective factor for developing internalizing and externalizing behavioral problems. However, little research has been conducted on within-person changes of prosocial behavior and behavioral problems over time. With random-intercept cross-lagged panel models (RI-CLPMs), the current study analyzed longitudinal associations between prosocial behavior and behavioral problems in two twin cohorts (98% Western European): in early childhood (age M = 4.77, SD = .58, 52% girls, N = 440) and middle childhood (age M = 7.94, SD = .67, 51% girls, N = 512). To obtain robust results, two parental reported questionnaires and an observational task were used as prosocial behavior assessments. In line with the literature, we found a significant between-person association between externalizing behavior and parent reported prosocial behavior in middle childhood, but not in early childhood. Some evidence indicated that changes in externalizing problems affect later prosocial behavior in middle childhood. Overall, however, the RI-CLPMs provided most support for the hypothesis that within-person changes in prosocial behavior are not related to within-person changes in behavioral problems. Thus, our findings did not support the hypothesis that increased prosocial behavior directly results in decreased behavioral problems, but emphasizes the need to take into account the multifaceted nature of prosocial behavior. (PsycInfo Database Record (c) 2022 APA, all rights reserved).

The nature of the self: Neural analyses and heritability estimates of self-evaluations in middle childhood.

How neural correlates of self-concept are influenced by environmental versus genetic factors is currently not fully understood. We investigated heritability estimates of behavioral and neural correlates of self-concept in middle childhood since this phase is an important time window for taking on new social roles in academic and social contexts. To do so, a validated self-concept fMRI task was applied in a twin sample of 345 participants aged between 7 and 9 years. In the self-concept condition, participants were asked to indicate whether academic and social traits applied to them whereas the control condition required trait categorization. The self-processing activation analyses (n = 234) revealed stronger medial prefrontal cortex (mPFC) activation for self than for control conditions. This effect was more pronounced for social-self than academic self-traits, whereas stronger dorsolateral prefrontal cortex (DLPFC) activation was observed for academic versus social self-evaluations. Behavioral genetic modeling (166 complete twin pairs) revealed that 25-52% of the variation in academic self-evaluations was explained by genetic factors, whereas 16-49% of the variation in social self-evaluations was explained by shared environmental factors. Neural genetic modeling (91 complete twin pairs) for variation in mPFC and anterior prefrontal cortex (PFC) activation for academic self-evaluations confirmed genetic and unique environmental influences, whereas anterior PFC activation for social self-evaluations was additionally influenced by shared environmental influences. This indicates that environmental context possibly has a larger impact on the behavioral and neural correlates of social self-concept at a young age. This is the first study demonstrating in a young twin sample that self-concept depends on both genetic and environmental factors, depending on the specific domain.

Genetic and environmental influences on structure of the social brain in childhood.

Prosocial behavior and empathy are important aspects of developing social relations in childhood. Prior studies showed protracted structural development of social brain regions associated with prosocial behavior. However, it remains unknown how structure of the social brain is influenced by genetic or environmental factors, and whether overlapping heritability factors explain covariance in structure of the social brain and behavior. The current study examined this hypothesis in a twin sample (aged 7-9-year; N = 512). Bilateral measures of surface area and cortical thickness of the medial prefrontal cortex (mPFC), temporo-parietal junction (TPJ), posterior superior temporal sulcus (pSTS), and precuneus were analyzed. Results showed genetic contributions to surface area and cortical thickness for all brain regions. We found additional shared environmental influences for TPJ, suggesting that this region might be relatively more sensitive to social experiences. Genetic factors also influenced parent-reported prosocial behavior (A = 45%) and empathy (A = 59%). We provided initial evidence that the precuneus shares genetically determined variance with empathy, suggesting a possible small genetic overlap (9%) in brain structure and empathy. These findings show that structure of the social brain and empathy are driven by a combination of genetic and environmental factors, with some factors overlapping for brain structure and behavior.

A Bi-Dimensional Taxonomy of Social Responsivity in Middle Childhood: Prosociality and Reactive Aggression Predict Externalizing Behavior Over Time.

Developing social skills is essential to succeed in social relations. Two important social constructs in middle childhood, prosocial behavior and reactive aggression, are often regarded as separate behaviors with opposing developmental outcomes. However, there is increasing evidence for the co-occurrence of prosociality and aggression, as both might indicate responsivity to the social environment. Here, we tested whether a bi-dimensional taxonomy of prosociality and reactive aggression could predict internalizing and externalizing problems over time. We re-analyzed data of two well-validated experimental tasks for prosociality (the Prosocial Cyberball Game) and reactive aggression (the Social Network Aggression Task) in a developmental population sample (n = 496, 7-9 years old). Results revealed no associations between prosociality and reactive aggression, confirming the independence of those constructs. Interestingly, although prosociality and reactive aggression independently did not predict problem behavior, the interaction of both was negatively predictive of changes in externalizing problems over time. Specifically, only children who scored low on both prosociality and reactive aggression showed an increase in externalizing problems 1 year later, whereas levels of externalizing problems did not change for children who scored high on both types of behavior. Thus, our results suggest that at an individual level, reactive aggression in middle childhood might not always be maladaptive when combined with prosocial behavior, thereby confirming the importance of studying social competence across multiple dimensions.

Genetic and environmental influences on MRI scan quantity and quality.

The current study provides an overview of quantity and quality of MRI data in a large developmental twin sample (N = 512, aged 7-9), and investigated to what extent scan quantity and quality were influenced by genetic and environmental factors. This was examined in a fixed scan protocol consisting of two functional MRI tasks, high resolution structural anatomy (3DT1) and connectivity (DTI) scans, and a resting state scan. Overall, scan quantity was high (88% of participants completed all runs), while scan quality decreased with increasing session length. Scanner related distress was negatively associated with scan quantity (i.e., completed runs), but not with scan quality (i.e., included runs). In line with previous studies, behavioral genetic analyses showed that genetics explained part of the variation in head motion, with heritability estimates of 29% for framewise displacement and 65% for absolute displacement. Additionally, our results revealed that subtle head motion (after exclusion of excessive head motion) showed lower heritability estimates (0-14%), indicating that findings of motion-corrected and quality-controlled MRI data may be less confounded by genetic factors. These findings provide insights in factors contributing to scan quality in children, an issue that is highly relevant for the field of developmental neuroscience.

Qoala-T: A supervised-learning tool for quality control of FreeSurfer segmented MRI data.

Performing quality control to detect image artifacts and data-processing errors is crucial in structural magnetic resonance imaging, especially in developmental studies. Currently, many studies rely on visual inspection by trained raters for quality control. The subjectivity of these manual procedures lessens comparability between studies, and with growing study sizes quality control is increasingly time consuming. In addition, both inter-rater as well as intra-rater variability of manual quality control is high and may lead to inclusion of poor quality scans and exclusion of scans of usable quality. In the current study we present the Qoala-T tool, which is an easy and free to use supervised-learning model to reduce rater bias and misclassification in manual quality control procedures using FreeSurfer-processed scans. First, we manually rated quality of N = 784 FreeSurfer-processed T1-weighted scans acquired in three different waves in a longitudinal study. Different supervised-learning models were then compared to predict manual quality ratings using FreeSurfer segmented output data. Results show that the Qoala-T tool using random forests is able to predict scan quality with both high sensitivity and specificity (mean area under the curve (AUC) = 0.98). In addition, the Qoala-T tool was also able to adequately predict the quality of two novel unseen datasets (total N = 872). Finally, analyses of age effects showed that younger participants were more likely to have lower scan quality, underlining that scan quality might confound findings attributed to age effects. These outcomes indicate that this procedure could further help to reduce variability related to manual quality control, thereby benefiting the comparability of data quality between studies.

Heritability of neural reactions to social exclusion and prosocial compensation in middle childhood.

Experiencing and observing social exclusion and inclusion, as well as prosocial behavior, are important aspects of social relationships in childhood. However, it is currently unknown to what extent these processes and their neural correlates differ in heritability. We investigated influences of genetics and environment on experiencing social exclusion and compensating for social exclusion of others with the Prosocial Cyberball Game using fMRI in a twin sample (aged 7-9; N = 500). Neuroimaging analyses (N = 283) revealed that experiencing possible self-exclusion resulted in activity in inferior frontal gyrus and medial prefrontal cortex, which was influenced by genetics and unique environment. Experiencing self-inclusion was associated with activity in anterior cingulate cortex, insula and striatum, but this was not significantly explained by genetics or shared environment. We found that children show prosocial compensating behavior when observing social exclusion. Prosocial compensating behavior was associated with activity in posterior cingulate cortex/precuneus, and showed unique environmental effects or measurement error at both behavioral and neural level. Together, these findings show that in children neural activation for experiencing possible self-exclusion and self-inclusion, and for displaying prosocial compensating behavior, is accounted for by unique environmental factors and measurement error, with a small genetic effect on possible self-exclusion.

Distinctive heritability patterns of subcortical-prefrontal cortex resting state connectivity in childhood: A twin study.

Connectivity between limbic/subcortical and prefrontal-cortical brain regions develops considerably across childhood, but less is known about the heritability of these networks at this age. We tested the heritability of limbic/subcortical-cortical and limbic/subcortical-subcortical functional brain connectivity in 7- to 9-year-old twins (N = 220), focusing on two key limbic/subcortical structures: the ventral striatum and the amygdala, given their combined influence on changing incentivised behavior during childhood and adolescence. Whole brain analyses with ventral striatum (VS) and amygdala as seeds in genetically independent groups showed replicable functional connectivity patterns. The behavioral genetic analyses revealed that in general VS and amygdala connectivity showed distinct influences of genetics and environment. VS-prefrontal cortex connections were best described by genetic and unique environmental factors (the latter including measurement error), whereas amygdala-prefrontal cortex connectivity was mainly explained by environmental influences. Similarities were also found: connectivity between both the VS and amygdala and ventral anterior cingulate cortex (vACC) showed influences of shared environment, while connectivity with the orbitofrontal cortex (OFC) showed heritability. These findings may inform future interventions that target behavioral control and emotion regulation, by taking into account genetic dispositions as well as shared and unique environmental factors such as child rearing.

Heritability of aggression following social evaluation in middle childhood: An fMRI study.

Middle childhood marks an important phase for developing and maintaining social relations. At the same time, this phase is marked by a gap in our knowledge of the genetic and environmental influences on brain responses to social feedback and their relation to behavioral aggression. In a large developmental twin sample (509 7- to 9-year-olds), the heritability and neural underpinnings of behavioral aggression following social evaluation were investigated, using the Social Network Aggression Task (SNAT). Participants viewed pictures of peers that gave positive, neutral, or negative feedback to the participant's profile. Next, participants could blast a loud noise toward the peer as an index of aggression. Genetic modeling revealed that aggression following negative feedback was influenced by both genetics and environmental (shared as well as unique environment). On a neural level (n = 385), the anterior insula and anterior cingulate cortex gyrus (ACCg) responded to both positive and negative feedback, suggesting they signal for social salience cues. The medial prefrontal cortex (mPFC) and inferior frontal gyrus (IFG) were specifically activated during negative feedback, whereas positive feedback resulted in increased activation in caudate, supplementary motor cortex (SMA), and dorsolateral prefrontal cortex (DLPFC). Decreased SMA and DLPFC activation during negative feedback was associated with more aggressive behavior after negative feedback. Moreover, genetic modeling showed that 13%-14% of the variance in dorsolateral PFC activity was explained by genetics. Our results suggest that the processing of social feedback is partly explained by genetic factors, whereas shared environmental influences play a role in behavioral aggression following feedback.

The neural correlates of dealing with social exclusion in childhood.

Observing social exclusion can be a distressing experience for children that can be followed by concerns for self-inclusion (self-concerns), as well as prosocial behavior to help others in distress (other-concerns). Indeed, behavioral studies have shown that observed social exclusion elicits prosocial compensating behavior in children, but motivations for the compensation of social exclusion are not well understood. To distinguish between self-concerns and other-concerns when observing social exclusion in childhood, participants (aged 7-10) played a four-player Prosocial Cyberball Game in which they could toss a ball to three other players. When one player was excluded by the two other players, the participant could compensate for this exclusion by tossing the ball more often to the excluded player. Using a three-sample replication (N = 18, N = 27, and N = 26) and meta-analysis design, we demonstrated consistent prosocial compensating behavior in children in response to observing social exclusion. On a neural level, we found activity in reward and salience related areas (striatum and dorsal anterior cingulate cortex (dACC)) when participants experienced inclusion, and activity in social perception related areas (orbitofrontal cortex) when participants experienced exclusion. In contrast, no condition specific neural effects were observed for prosocial compensating behavior. These findings suggest that in childhood observed social exclusion is associated with stronger neural activity for self-concern. This study aims to overcome some of the issues of replicability in developmental psychology and neuroscience by using a replication and meta-analysis design, showing consistent prosocial compensating behavior to the excluded player, and replicable neural correlates of experiencing exclusion and inclusion during middle childhood.

Brain activation upon ideal-body media exposure and peer feedback in late adolescent girls.

Media's prevailing thin-body ideal plays a vital role in adolescent girls' body image development, but the co-occurring impact of peer feedback is understudied. The present study used functional magnetic resonance imaging (fMRI) to test media imagery and peer feedback combinations on neural activity related to thin-body ideals. Twenty-four healthy female late adolescents rated precategorized body sizes of bikini models (too thin or normal), directly followed by ostensible peer feedback (too thin or normal). Consistent with prior studies on social feedback processing, results showed increased brain activity in the dorsal medial prefrontal cortex (dmPFC)/anterior cingulate cortex (ACC) and bilateral insula in incongruent situations: when participants rated media models' body size as normal while peer feedback indicated the models as too thin (or vice versa). This effect was stronger for girls with lower self-esteem. A subsequent behavioral study (N = 34 female late adolescents, separate sample) demonstrated that participants changed behavior in the direction of the peer feedback: precategorized normal sized models were rated as too thin more often after receiving too thin peer feedback. This suggests that the neural responses upon peer feedback may influence subsequent choice. Our results show that media-by-peer interactions have pronounced effects on girls' body ideals.

The neural and behavioral correlates of social evaluation in childhood.

Being accepted or rejected by peers is highly salient for developing social relations in childhood. We investigated the behavioral and neural correlates of social feedback and subsequent aggression in 7-10-year-old children, using the Social Network Aggression Task (SNAT). Participants viewed pictures of peers that gave positive, neutral or negative feedback to the participant's profile. Next, participants could blast a loud noise towards the peer, as an index of aggression. We included three groups (N=19, N=28 and N=27) and combined the results meta-analytically. Negative social feedback resulted in the most behavioral aggression, with large combined effect-sizes. Whole brain condition effects for each separate sample failed to show robust effects, possibly due to the small samples. Exploratory analyses over the combined test and replication samples confirmed heightened activation in the medial prefrontal cortex (mPFC) after negative social feedback. Moreover, meta-analyses of activity in predefined regions of interest showed that negative social feedback resulted in more neural activation in the amygdala, anterior insula and the mPFC/anterior cingulate cortex. Together, the results show that social motivation is already highly salient in middle childhood, and indicate that the SNAT is a valid paradigm for assessing the neural and behavioral correlates of social evaluation in children.

Predicting reading and mathematics from neural activity for feedback learning.

Although many studies use feedback learning paradigms to study the process of learning in laboratory settings, little is known about their relevance for real-world learning settings such as school. In a large developmental sample (N = 228, 8-25 years), we investigated whether performance and neural activity during a feedback learning task predicted reading and mathematics performance 2 years later. The results indicated that feedback learning performance predicted both reading and mathematics performance. Activity during feedback learning in left superior dorsolateral prefrontal cortex (DLPFC) predicted reading performance, whereas activity in presupplementary motor area/anterior cingulate cortex (pre-SMA/ACC) predicted mathematical performance. Moreover, left superior DLPFC and pre-SMA/ACC activity predicted unique variance in reading and mathematics ability over behavioral testing of feedback learning performance alone. These results provide valuable insights into the relationship between laboratory-based learning tasks and learning in school settings, and the value of neural assessments for prediction of school performance over behavioral testing alone. (PsycINFO Database Record

Neural Correlates of Prosocial Behavior: Compensating Social Exclusion in a Four-Player Cyberball Game.

Prior studies demonstrated contributions of the insula and dorsal anterior cingulate cortex (dACC) for both experiencing and observing social exclusion, but it is not yet well understood how the brain processes the compensation of exclusion, as is observed in prosocial helping. Here, we tested if social brain regions, specifically the medial prefrontal cortex (mPFC) and temporal parietal junction (TPJ) are involved when individuals show prosocial behavior towards excluded others. For this purpose, 23 female participants played a four-player Cyberball Game in which participants could toss balls to each other. During the exclusion game, two players excluded one of the other players. When participants observed exclusion by others, they showed elevated activity in the insula, consistent with prior studies. However, when they tossed the ball to the excluded player, they showed increased activation in the TPJ, consistent with the hypothesis that prosocial behavior is associated with social reasoning. In addition, tossing to the excluded player was associated with increased activity in the nucleus accumbens (NAcc). Given that prior studies reported that the NAcc is involved in experiencing rewards, this may suggest a warm glow for showing prosocial compensation behavior when helping excluded others.