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.

Neurobiological correlates of antisociality across adolescence and young adulthood: a multi-sample, multi-method study.

BACKGROUND: Antisociality across adolescence and young adulthood puts individuals at high risk of developing a variety of problems. Prior research has linked antisociality to autonomic nervous system and endocrinological functioning. However, there is large heterogeneity in antisocial behaviors, and these neurobiological measures are rarely studied conjointly, limited to small specific studies with narrow age ranges, and yield mixed findings due to the type of behavior examined. METHODS: We harmonized data from 1489 participants (9-27 years, 67% male), from six heterogeneous samples. In the resulting dataset, we tested relations between distinct dimensions of antisociality and heart rate, pre-ejection period (PEP), respiratory sinus arrhythmia, respiration rate, skin conductance levels, testosterone, basal cortisol, and the cortisol awakening response (CAR), and test the role of age throughout adolescence and young adulthood. RESULTS: Three dimensions of antisociality were uncovered: 'callous-unemotional (CU)/manipulative traits', 'intentional aggression/conduct', and 'reactivity/impulsivity/irritability'. Shorter PEPs and higher testosterone were related to CU/manipulative traits, and a higher CAR is related to both CU/manipulative traits and intentional aggression/conduct. These effects were stable across age. CONCLUSIONS: Across a heterogeneous sample and consistent across development, the CAR may be a valuable measure to link to CU/manipulative traits and intentional aggression, while sympathetic arousal and testosterone are additionally valuable to understand CU/manipulative traits. Together, these findings deepen our understanding of the fundamental mechanisms underlying different components of antisociality. Finally, we illustrate the potential of using current statistical techniques for combining multiple datasets to draw robust conclusions about biobehavioral associations.

Behavioral and Neural Pathways Supporting the Development of Prosocial and Risk-Taking Behavior Across Adolescence.

This study tested the pathways supporting adolescent development of prosocial and rebellious behavior. Self-report and structural brain development data were obtained in a three-wave, longitudinal neuroimaging study (8-29 years, N = 210 at Wave 3). First, prosocial and rebellious behavior assessed at Wave 3 were positively correlated. Perspective taking and intention to comfort uniquely predicted prosocial behavior, whereas fun seeking (current levels and longitudinal changes) predicted both prosocial and rebellious behaviors. These changes were accompanied by developmental declines in nucleus accumbens and medial prefrontal cortex (MPFC) volumes, but only faster decline of MPFC (faster maturity) related to less rebellious behavior. These findings point toward a possible differential susceptibility marker, fun seeking, as a predictor of both prosocial and rebellious developmental outcomes.

Are individual differences quantitative or qualitative? An integrated behavioral and fMRI MIMIC approach.

In cognitive neuroscience there is a growing interest in individual differences. We propose the Multiple Indicators Multiple Causes (MIMIC) model of combined behavioral and fMRI data to determine whether such differences are quantitative or qualitative in nature. A simulation study revealed the MIMIC model to have adequate power for this goal, and parameter recovery to be satisfactory. The MIMIC model was illustrated with a re-analysis of Van Duijvenvoorde et al. (2016) and Blankenstein et al. (2018) decision making data. This showed individual differences in Van Duijvenvoorde et al. (2016) to originate in qualitative differences in decision strategies. Parameters indicated some individuals to use an expected value decision strategy, while others used a loss minimizing strategy, distinguished by individual differences in vmPFC activity. Individual differences in Blankenstein et al. (2018) were explained by quantitative differences in risk aversion. Parameters showed that more risk averse individuals preferred safe over risky choices, as predicted by heightened vmPFC activity. We advocate using the MIMIC model to empirically determine, rather than assume, the nature of individual differences in combined behavioral and fMRI datasets.

Neural tracking of subjective value under riskand ambiguity in adolescence.

Although many neuroimaging studies on adolescent risk taking have focused on brain activation during outcome valuation, less attention has been paid to the neural correlates of choice valuation. Subjective choice valuation may be particularly influenced by whether a choice presents risk (known probabilities) or ambiguity (unknown probabilities), which has rarely been studied in developmental samples. Therefore, we examined the neural tracking of subjective value during choice under risk and ambiguity in a large sample of adolescents (N = 188, 12-22 years). Specifically, we investigated which brain regions tracked subjective value coding under risk and ambiguity. A model-based approach to estimate individuals' risk and ambiguity attitudes showed prominent variation in individuals' aversions to risk and ambiguity. Furthermore, participants subjectively experienced the ambiguous options as being riskier than the risky options. Subjective value tracking under risk was coded by activation in ventral striatum and superior parietal cortex. Subjective value tracking under ambiguity was coded by dorsolateral prefrontal cortex (PFC) and superior temporal gyrus activation. Finally, overlapping activation in the dorsomedial PFC was observed for subjective value under both conditions. Overall, this is the first study to chart brain activation patterns for subjective choice valuation under risk and ambiguity in an adolescent sample, which shows that the building blocks for risk and ambiguity processing are already present in early adolescence. Finally, we highlight the potential of combining behavioral modeling with fMRI for investigating choice valuation in adolescence, which may ultimately aid in understanding who takes risks and why.

Longitudinal structural brain development and externalizing behavior in adolescence.

BACKGROUND: Cross-sectional studies report relations between externalizing behavior and structural abnormalities in cortical thickness of prefrontal regions and volume reductions in subcortical regions. To understand how these associations emerge and develop, longitudinal designs are pivotal. METHOD: In the current longitudinal study, a community sample of children, adolescents and young adults (N = 271) underwent magnetic resonance imaging (MRI) in three biennial waves (680 scans). At each wave, aspects of externalizing behavior were assessed with parent-reported aggression and rule-breaking scores (Child Behavior Checklist), and self-reported aggression scores (Buss-Perry Aggression Questionnaire). Regions of interest (ROIs) were selected based on prior research: dorsolateral prefrontal (dlPFC), orbitofrontal (OFC), anterior cingulate cortex (ACC), insula, and parahippocampal cortex, as well as subcortical regions. Linear mixed models were used to assess the longitudinal relation between externalizing behavior and structural brain development. Structural covariance analyses were employed to identify whether longitudinal relations between ROIs (maturational coupling) were associated with externalizing behavior. RESULTS: Linear mixed model analyses showed a negative relation between parent-reported aggression and right hippocampal volume. Moreover, this longitudinal relation was driven by change in hippocampal volume and not initial volume of hippocampus at time point 1. Exploratory analyses showed that stronger maturational coupling between prefrontal regions, the limbic system, and striatum was associated with both low and high externalizing behavior. CONCLUSIONS: Together, these findings reinforce the hypothesis that altered structural brain development coincides with development of more externalizing behavior. These findings may guide future research on normative and deviant development of externalizing behavior.

Contributions of Reward Sensitivity to Ventral Striatum Activity Across Adolescence and Early Adulthood.

It was examined how ventral striatum responses to rewards develop across adolescence and early adulthood and how individual differences in state- and trait-level reward sensitivity are related to these changes. Participants (aged 8-29 years) were tested across three waves separated by 2 years (693 functional MRI scans) in an accelerated longitudinal design. The results confirmed an adolescent peak in reward-related ventral striatum, specifically nucleus accumbens, activity. In early to mid-adolescence, increases in reward activation were related to trait-level reward drive. In mid-adolescence to early adulthood decreases in reward activation were related to decreases in state-level hedonic reward pleasure. This study demonstrates that state- and trait-level reward sensitivity account for reward-related ventral striatum activity in different phases of adolescence and early adulthood.

Development of Multifaceted Risk Taking and the Relations to Sex Steroid Hormones: A Longitudinal Study.

Risk taking is a multidimensional construct. It is currently unclear which aspects of risk-taking change most during adolescence and if/how sex hormones contribute to risk-taking tendencies. This study applied a longitudinal design with three time-points, separated by 2 years, in participants aged 8-29 years (670 observations). The Balloon Analogue Risk Task, a delay discounting task, and various self-report questionnaires were administered, to measure aspects of risk taking. Longitudinal analyses demonstrated mostly nonlinear age-related patterns in risk-taking behavior and approach-related personality characteristics (peaking in late adolescence). Increased testosterone and estradiol were found to increase risk-taking behavior and impulsive personality, but decrease avoidance-like personality. This study demonstrates that risk taking is most pronounced in mid-to-late adolescence and suggests that sex hormones accelerate this maturational process.

Neural Mechanisms Underlying Risk and Ambiguity Attitudes.

Individual differences in attitudes to risk (a taste for risk, known probabilities) and ambiguity (a tolerance for uncertainty, unknown probabilities) differentially influence risky decision-making. However, it is not well understood whether risk and ambiguity are coded differently within individuals. Here, we tested whether individual differences in risk and ambiguity attitudes were reflected in distinct neural correlates during choice and outcome processing of risky and ambiguous gambles. To these ends, we developed a neuroimaging task in which participants ( n = 50) chose between a sure gain and a gamble, which was either risky or ambiguous, and presented decision outcomes (gains, no gains). From a separate task in which the amount, probability, and ambiguity level were varied, we estimated individuals' risk and ambiguity attitudes. Although there was pronounced neural overlap between risky and ambiguous gambling in a network typically related to decision-making under uncertainty, relatively more risk-seeking attitudes were associated with increased activation in valuation regions of the brain (medial and lateral OFC), whereas relatively more ambiguity-seeking attitudes were related to temporal cortex activation. In addition, although striatum activation was observed during reward processing irrespective of a prior risky or ambiguous gamble, reward processing after an ambiguous gamble resulted in enhanced dorsomedial PFC activation, possibly functioning as a general signal of uncertainty coding. These findings suggest that different neural mechanisms reflect individual differences in risk and ambiguity attitudes and that risk and ambiguity may impact overt risk-taking behavior in different ways.

Longitudinal self-concept development in adolescence.

This longitudinal behavioral neuroimaging study tested two hypotheses concerning self-concept development in adolescence: domain-specific self-concept and similarity between own (direct) and perceived peers' (reflected) opinions of the self. Participants (N = 189; 10-24 years) evaluated their traits in academic, physical appearance and prosocial domains from direct and reflected perspectives in an functional magnetic resonance imaging session across three time points (TP1: n = 160; TP2: n = 151; TP3: n = 144). Behaviorally, we observed a mid-adolescent dip in self-concept positivity, which was strongest for the academic domain, showing domain differentiation in mid-adolescence. Self-evaluations were associated with activity in, e.g. medial prefrontal cortex (mPFC) and temporal-parietal junction (TPJ). mPFC showed an adolescent-emerging peak in activation, pronounced more for direct than reflected self-evaluations. TPJ activation was generally stronger for reflected self-evaluations, and activation linearly increased with age for both reflected and direct self-evaluations. Longitudinal prediction analyses showed that positivity of self-evaluations predicted increases in self-concept clarity and less fear of negative evaluation 1 and 2 years later, highlighting the developmental benefits of acquiring a positive self-concept. Together, we show that adolescent self-development is characterized by dissociable neural patterns underlying self-evaluations in different domains, and from reflected and direct perspectives, confirming adolescence as a formative phase for developing a coherent and positive self-concept.

Risks and rewards in adolescent decision-making.

Adolescent decision-making has been characterized as risky, and a heightened reward sensitivity may be one of the aspects contributing to riskier choice-behavior. Previous studies have targeted reward-sensitivity in adolescence and the neurobiological mechanisms of reward processing in the adolescent brain. In recent examples, researchers aim to disentangle the contributions of risk- and reward-sensitivity to adolescent risk-taking. Here, we discuss recent findings of adolescent's risk preferences and the associated neural mechanisms. We highlight potential frameworks that target individual differences in risk preferences in an effort to understand adolescent risk-taking, and with an ultimate goal of leveraging undesirable levels of risk taking.

Increased Ventromedial Prefrontal Cortex Activity in Adolescence Benefits Prosocial Reinforcement Learning.

Learning which of our behaviors benefit others contributes to forming social relationships. An important period for the development of (pro)social behavior is adolescence, which is characterized by transitions in social connections. It is, however, unknown how learning to benefit others develops across adolescence and what the underlying cognitive and neural mechanisms are. In this functional neuroimaging study, we assessed learning for self and others (i.e., prosocial learning) and the concurring neural tracking of prediction errors across adolescence (ages 9-21, N = 74). Participants performed a two-choice probabilistic reinforcement learning task in which outcomes resulted in monetary consequences for themselves, an unknown other, or no one. Participants from all ages were able to learn for themselves and others, but learning for others showed a more protracted developmental trajectory. Prediction errors for self were observed in the ventral striatum and showed no age-related differences. However, prediction error coding for others showed an age-related increase in the ventromedial prefrontal cortex. These results reveal insights into the computational mechanisms of learning for others across adolescence, and highlight that learning for self and others show different age-related patterns.

Dealing With Uncertainty: Testing Risk- and Ambiguity-Attitude Across Adolescence.

Attitudes to risk (known probabilities) and attitudes to ambiguity (unknown probabilities) are separate constructs that influence decision making, but their development across adolescence remains elusive. We administered a choice task to a wide adolescent age-range (N = 157, 10-25 years) to disentangle risk- and ambiguity-attitudes using a model-based approach. Additionally, this task was played in a social context, presenting choices from a high risk-taking peer. We observed age-related changes in ambiguity-attitude, but not risk-attitude. Also, ambiguity-aversion was negatively related to real-life risk taking. Finally, the social context influenced only risk-attitudes. These results highlight the importance of disentangling risk- and ambiguity-attitudes in adolescent risk taking.