Age-related changes in ventrolateral prefrontal cortex activation are associated with daily prosocial behaviors two years later.

As adolescents acquire agency and become contributing members of society, it is necessary to understand how they help their community. Yet, it is unknown how prosocial behavior develops in the context of community-based prosocial behaviors that are relevant to adolescents, such as donating time to charities. In this longitudinal functional magnetic resonance imaging study, adolescents (N=172; mean age at wave 1=12.8) completed a prosocial task annually for three years (N=422 and 375 total behavioral and neural data points, respectively), and 14 days of daily diaries reporting on their prosocial behaviors two years later. During the task, adolescents decided how many minutes they would donate to a variety of local charities. We found that adolescents donated less time to charities from early to mid adolescence. Longitudinal whole-brain analyses revealed declines in ventrolateral prefrontal cortex (vlPFC) activation, as well as inverted U-shaped changes in precuneus activation when adolescents donated their time from early to mid adolescence. A less steep decrease in vlPFC activation predicted greater real-life prosocial behaviors in youth's daily lives two years later. Our study elucidates the neurodevelopmental mechanisms of prosocial behavior from early to mid adolescence that have enduring effects on daily prosocial behaviors in late adolescence.

Developmental changes in brain function linked with addiction-like social media use two years later.

Addiction-like social media use (ASMU) is widely reported among adolescents and is associated with depression and other negative health outcomes. We aimed to identify developmental trajectories of neural social feedback processing that are linked to higher levels of ASMU in later adolescence. Within a longitudinal design, 103 adolescents completed a social incentive delay task during 1-3 fMRI scans (6-9th grade), and a 4th self-report assessment of ASMU and depressive symptoms ∼2 years later (10-11th grade). We assessed ASMU effects on brain responsivity to positive social feedback across puberty and relationships between brain responsivity development, ASMU symptoms, and depressive symptoms while considering gender effects. Findings demonstrate decreasing responsivity, across puberty, in the ventral media prefrontal cortex, medial prefrontal cortex, posterior cingulate cortex, and right inferior frontal gyrus associated with higher ASMU symptoms over 2 years later. Significant moderated mediation models suggest that these pubertal decreases in brain responsivity are associated with increased ASMU symptoms which, among adolescent girls (but not boys), is in turn associated with increased depressive symptoms. Results suggest initial hyperresponsivity to positive social feedback, before puberty onset, and decreases in this response across development, may be risk factors for ASMU in later adolescence.

Neurobiological sensitivity to popular peers moderates daily links between social media use and affect.

Social media behaviors increase during adolescence, and quantifiable feedback metrics (e.g., likes, followers) may amplify the value of social status for teens. Social media's impact on adolescents' daily affect may be exacerbated given the neurodevelopmental changes that increase youths' sensitivity to socio-emotional information. This study examines whether neurobiological sensitivity to popularity moderates daily links between social media use and affect. Adolescents (N = 91, Mage=13.6 years, SDage=0.6 years) completed an fMRI task in which they viewed faces of their high (>1 SD above the mean) and low (<1 SD below the mean) popular peers based on peer-nominated sociometric ratings from their school social networks. Two years later, adolescents reported their time spent on social media and affect daily for two weeks. Neural tracking of popularity in the ventromedial and dorsomedial prefrontal cortex moderated the association between time on social media and affect. Specifically, adolescents who tracked high popular peers in the vmPFC reported more positive affect on days when they used social media more. Adolescents who tracked low popular peers in the vmPFC and dmPFC reported more negative affect on days when they used social media more. Results suggest that links between social media and affect depend on individual differences in neural sensitivity to popularity.

Friendship changes differentially predict neural correlates of decision-making for friends across adolescence.

Adolescents' peer world is highly dynamic with constant dissolution of old friendships and formation of new ones. Though many of adolescents' risky decisions involve their peers, little is known about how adolescents' ever-changing friendships shape their ability to make these peer-involving risky decisions, particularly adaptive ones, and whether this association shifts over time. In a 5-wave longitudinal fMRI study, 173 adolescents (at wave 1: Mage = 12.8, SDage = 0.52; range = 11.9-14.5) made risky choices to win money for their best friend. We assessed whether participants nominated the same or different best friend as their previous participation year (a total of 340 data points of friendship maintenance / change). In early adolescence, adolescents with the same best friend took more adaptive risks for that best friend than those with a different best friend. In late adolescence, however, adolescents with a different best friend took more adaptive risks for the new best friend than those with the same best friend. Further, the amygdala was differentially sensitive to friendship maintenance / change during these peer-involving adaptive risks across time. This study has implications for how stable and flexible peer landscapes differentially modulate social motivation and social decision-making over the course of adolescence.

Neural tracking of social hierarchies in adolescents' real-world social networks.

In the current study, we combined sociometric nominations and neuroimaging techniques to examine adolescents' neural tracking of peers from their real-world social network that varied in social preferences and popularity. Adolescent participants from an entire school district (N = 873) completed peer sociometric nominations of their grade at school, and a subset of participants (N = 117, Mage = 13.59 years) completed a neuroimaging task in which they viewed peer faces from their social networks. We revealed two neural processes by which adolescents track social preference: (1) the fusiform face area, an important region for early visual perception and social categorization, simultaneously represented both peers high in social preference and low in social preference; (2) the dorsolateral prefrontal cortex (DLPFC), which was differentially engaged in tracking peers high and low in social preference. No regions specifically tracked peers high in popularity and only the inferior parietal lobe, temporoparietal junction, midcingulate cortex and insula were involved in tracking unpopular peers. This is the first study to examine the neural circuits that support adolescents' perception of peer-based social networks. These findings identify the neural processes that allow youths to spontaneously keep track of peers' social value within their social network.

Neural Representation of Donating Time and Money.

Volunteering and charitable donations are two common forms of prosocial behavior, yet it is unclear whether these other-benefitting behaviors are supported by the same or different neurobiological mechanisms. During an fMRI task, 40 participants (20 female-identifying; age: mean = 18.92 years, range = 18.32-19.92 years) contributed their time (in minutes) and money (in dollars) to a variety of local charities. With the maximum amount of time and money that participants could spend on these charities, they did not differentially donate their time and money. At the neural level, donating time and money both showed activations in brain regions involved in cognitive control (e.g., dorsolateral PFC) and affective processing (e.g., dorsal anterior cingulate cortex), but donating time recruited regions involved in reward valuation (e.g., ventral striatum) and mentalizing (e.g., temporal pole) to a greater extent than donating money. Further, the precuneus, which is also a region involved in mentalizing, more strongly tracked the varying amount of money than time donated, suggesting that the precuneus may be more sensitive to the increasing magnitude of a nonsocial exchange (e.g., donating money is a financial exchange) than a social exchange (e.g., donating time is an interpersonal exchange). Our findings elucidate shared as well as distinct neurobiological properties of two prosocial behaviors, which have implications for how humans share different resources to positively impact their community.SIGNIFICANCE STATEMENT Prosocial behaviors broadly characterize how humans act to benefit others. Various prosocial behaviors, such as volunteering and charitable donations, share the goal of positively contributing to community. Our study identifies brain regions that may serve as ubiquitous neurobiological markers of community-based prosocial behaviors. Despite this shared goal, our study also shows that the human brain responds to donating time and money in diverging ways, such that brain regions associated with processing emotional reward and thinking about others are more strongly recruited for donating time than for money. Therefore, our study sheds light on how different personal resources, such as one's time and money, within a prosocial context are represented in the brain.

Adolescents' neural sensitivity to high and low popularity: Longitudinal links to risk-taking and prosocial behavior.

Adolescents are particularly attuned to popularity within peer groups, which impacts behaviors such as risk-taking and prosocial behavior. Neurodevelopmental changes orient adolescents toward salient social cues in their environment. We examined whether neural regions that track popularity are associated with longitudinal changes in risk-taking and prosocial behavior. During an fMRI scan, adolescents (n = 109, Mage=13.59, SD=0.59) viewed pictures of their popular and unpopular classmates based on sociometric nominations from their social networks. Neural tracking of high popularity in the dorsomedial prefrontal cortex was associated with increases in risk-taking behavior, whereas tracking of low popularity in the right insula was associated with increases in prosocial behavior. Results suggest that individual differences in neural tracking of popularity relate to longitudinal changes in adolescents' social behaviors.

Neural similarity in nucleus accumbens during decision-making for the self and a best friend: Links to adolescents' self-reported susceptibility to peer influence and risk taking.

Adolescence is marked by increased peer influence on risk taking; however, recent literature suggests enormous individual variation in peer influence susceptibility to risk-taking behaviors. The current study uses representation similarity analysis to test whether neural similarity between decision-making for self and peers (i.e., best friends) in a risky context is associated with individual differences in self-reported peer influence susceptibility and risky behaviors in adolescents. Adolescent participants (N = 166, Mage = 12.89) completed a neuroimaging task in which they made risky decisions to receive rewards for themselves, their best friend, and their parents. Adolescent participants self-reported peer influence susceptibility and engagement in risk-taking behaviors. We found that adolescents with greater similarity in nucleus accumbens (NACC) response patterns between the self and their best friend reported greater susceptibility to peer influence and increased risk-taking behaviors. However, neural similarity in ventromedial prefrontal cortex (vmPFC) was not significantly associated with adolescents' peer influence susceptibility and risk-taking behaviors. Further, when examining neural similarity between adolescents' self and their parent in the NACC and vmPFC, we did not find links to peer influence susceptibility and risk-taking behaviors. Together, our results suggest that greater similarity for self and friend in the NACC is associated with individual differences in adolescents' peer influence susceptibility and risk-taking behaviors.

Developmental Changes in Habenular and Striatal Social Reinforcement Responsivity Across Adolescence Linked With Substance Use.

BACKGROUND: Habenula (HB) function is implicated in substance use disorders and is involved in inhibiting dopamine release in the ventral striatum (VS). While blunted VS reward responsivity is implicated in risk for later substance use, links between HB reinforcement processing and progression of use have not, to our knowledge, been examined among adolescents. In the present study, we longitudinally assessed HB and VS responsivity to social rewards and punishments across adolescence and examined associations with substance use. METHODS: Within a longitudinal design, 170 adolescents (53.5% female) completed 1 to 3 functional magnetic resonance imaging scans across 6th to 9th grade and reported yearly substance use across 6th to 11th grade. We examined VS and HB responsivity to social reinforcement during a social incentive delay task in which adolescents received social rewards (smiling faces) and punishments (scowling faces). RESULTS: We observed increased VS responsivity to social rewards (vs. reward omissions) and increased VS, but decreased HB, responsivity to social punishment avoidance versus receipt. However, contrary to hypotheses, the HB displayed increased responsivity to social rewards (vs. reward omissions). Further, adolescents reporting regular substance use displayed longitudinally declining HB responsivity to social rewards (vs. reward omissions), whereas adolescents reporting no substance use displayed longitudinally increasing HB responsivity. In contrast, whereas VS responsivity to punishment avoidance versus receipt increased longitudinally among regular substance users, it stayed relatively stable among nonusers. CONCLUSIONS: These results suggest that differential HB and VS social reinforcement processing trajectories across adolescence are associated with substance use.

Behavioral and Neural Trajectories of Risk Taking for Peer and Parent in Adolescence.

One feature of adolescence is a rise in risk-taking behaviors, whereby the consequences of adolescents' risky action often impact their immediate surrounding such as their peers and parents (vicarious risk taking). Yet, little is known about how vicarious risk taking develops, particularly depending on who the risk affects and the type of risky behavior. In a 3-wave longitudinal fMRI study, 173 adolescents completed 1-3 years of a risky decision-making task where they took risks to win money for their best friend and parent (n with behavioral and fMRI data ranges from 139-144 and 100-116 participants, respectively, per wave). Results of this preregistered study suggest that adolescents did not differentially take adaptive (sensitivity to the expected value of reward during risk taking) and general (decision-making when the expected values of risk taking and staying safe are equivalent) risks for their best friend and parent from sixth to ninth grade. At the neural level, preregistered ROI analyses revealed no differences in the ventral striatum and ventromedial pFC during general nor adaptive risk taking for best friend versus parent over time. Furthermore, exploratory longitudinal whole-brain analyses revealed subthreshold differences between best friend and parent trajectories within regulatory regions during general vicarious risk taking and social-cognitive regions during adaptive vicarious risk taking. Our findings demonstrate that brain regions implicated in cognitive control and social-cognitive processes may distinguish behaviors involving peers and parents over time.

Adolescents' Perceptions of Social Risk and Prosocial Tendencies: Developmental Change and Individual Differences.

Many prosocial behaviors involve social risks such as speaking out against a popular opinion, bias, group norm, or authority. However, little is known about whether adolescents' prosocial tendencies develop over time with their perceptions of social risks. This accelerated longitudinal study used within-subject growth-curve analyses to test the link between prosocial tendencies and social risk perceptions, in a sample of adolescents who completed self-reports annually for three years (N = 893; M age = 12.30 years, 10 - 14 years at Wave 1, and 10 - 17 years across the full study period; 50% Girls, 33% White non-Latinx, 27% Latinx, 20% African American, 20% Mixed/Other Race). The association between social risk tolerance and prosocial tendencies changed significantly across adolescence, such that at for younger adolescents, more prosocial tendencies were associated with less social risk tolerance, whereas for relatively older adolescents, more prosocial tendencies were associated marginally with more social risk tolerance. Additional individual differences by empathy (but not sensation seeking) emerged. These findings suggest that prosocial development across adolescence may be associated with an underlying ability to tolerate social risks.

Association of Habitual Checking Behaviors on Social Media With Longitudinal Functional Brain Development.

Importance: Social media platforms provide adolescents with unprecedented opportunities for social interactions during a critical developmental period when the brain is especially sensitive to social feedback. Objective: To explore how adolescents' frequency of checking behaviors on social media platforms is associated with longitudinal changes in functional brain development across adolescence. Design, Setting, and Participants: A 3-year longitudinal cohort study of functional magnetic resonance imaging (fMRI) among sixth- and seventh-grade students recruited from 3 public middle schools in rural North Carolina. Exposures: At wave 1, participants reported the frequency at which they checked Facebook, Instagram, and Snapchat. Main Outcome or Measure: Neural responses to the Social Incentive Delay task when anticipating receiving social feedback, measured annually using fMRI for 3 years. Participants saw a cue that indicated whether the social feedback (adolescent faces with emotional expressions) would be a reward, punishment, or neutral; after a delay, a target appeared and students responded by pressing a button as quickly as possible; a display of social feedback depended on trial type and reaction time. Results: Of 178 participants recruited at age 12 years, 169 participants (mean [SD] age, 12.89 [0.58] years; range, 11.93-14.52 years; 91 [53.8%] female; 38 [22.5%] Black, 60 [35.5%] Latinx, 50 [29.6%] White, 15 [8.9%] multiracial) met the inclusion criteria. Participants with habitual social media checking behaviors showed lower neural sensitivity to social anticipation at age 12 years compared with those with nonhabitual checking behaviors in the left amygdala, posterior insula (PI), and ventral striatum (VS; ß, -0.22; 95% CI, -0.33 to -0.11), right amygdala (ß, -0.19; 95% CI, -0.30 to -0.08), right anterior insula (AI; ß, -0.23; 95% CI, -0.37 to -0.09), and left dorsolateral prefrontal cortex (DLPFC; ß, -0.29; 95% CI, -0.44 to -0.14). Among those with habitual checking behaviors, there were longitudinal increases in the left amygdala/PI/VS (ß, 0.11; 95% CI, 0.04 to 0.18), right amygdala (ß, 0.09; 95% CI, 0.02 to 0.16), right AI (ß, 0.15; 95% CI, 0.02 to 0.20), and left DLPFC (ß, 0.19; 95% CI, 0.05 to 0.25) during social anticipation, whereas among those with nonhabitual checking behaviors, longitudinal decreases were seen in the left amygdala/PI/VS (ß, -0.12; 95% CI, -0.19 to -0.06), right amygdala (ß, -0.10; 95% CI, -0.17 to -0.03), right AI (ß, -0.13; 95% CI, -0.22 to -0.04), and left DLPFC (ß, -0.10, 95% CI, -0.22 to -0.03). Conclusions and Relevance: The results of this cohort study suggest that social media checking behaviors in early adolescence may be associated with changes in the brain's sensitivity to social rewards and punishments. Further research examining long-term associations between social media use, adolescent neural development, and psychological adjustment is needed to understand the effects of a ubiquitous influence on development for today's adolescents.

Neural Reactivity to Social Punishment Predicts Future Engagement in Nonsuicidal Self-injury Among Peer-Rejected Adolescents.

BACKGROUND: Rates of nonsuicidal self-injury (NSSI) increase dramatically in adolescence. Affective reactivity and adverse social experiences have been linked to NSSI, but less is known about whether these factors may separately or interactively predict NSSI, especially longitudinally. This study combined functional magnetic resonance imaging and a sociometric measure to test whether a combination of neural (e.g., amygdala) reactivity to social punishment and peer-nominated peer acceptance/rejection predicts NSSI longitudinally in adolescence. Amygdala reactivity was examined as a potential neural marker of affective reactivity to social punishment, which may heighten NSSI risk in contexts of social adversity. METHODS: One hundred twenty-five adolescents (63 female) completed a social incentive delay task during neuroimaging and school-based peer nominations to measure peer acceptance/rejection. NSSI engagement was assessed at baseline and 1-year follow-up. RESULTS: Greater amygdala reactivity to social punishment predicted greater NSSI engagement 1 year later among adolescents with high peer rejection. This effect for the amygdala was specific to social punishment (vs. reward) and held when controlling for biological sex and pubertal development. Exploratory analyses found that ventral striatum reactivity to social reward and punishment similarly interacted with peer rejection to predict NSSI but that amygdala connectivity with salience network regions did not. CONCLUSIONS: Amygdala reactivity to social punishment, in combination with high peer rejection, may increase NSSI risk in adolescence, possibly via heightened affective reactivity to adverse social experiences. Objective measures of neurobiological and social risk factors may improve prediction of NSSI, while therapeutic approaches that target affective reactivity and increase prosocial skills may protect against NSSI in adolescence.

Positive risk taking and neural sensitivity to risky decision making in adolescence.

This study examines associations between adolescents' positive risk taking and neural activation during risky decision-making. Participants included 144 adolescents ages 13-16 years (Mage = 14.23; SDage = 0.7) from diverse racial and ethnic groups. Participants self-reported their engagement in positive and negative risk taking. Additionally, participants played the Cups task during fMRI, where they chose between a safe choice (guaranteed earning of 15 cents) and a risky choice (varying probabilities of earning more than 15 cents). Using a risk-return framework, we examined adolescents' sensitivity to both risks (safe versus risky) and returns (expected value, or potential reward as a function of its probability of occurring) at the behavioral and neural levels. All participants took more risks when the expected value of the choice was high. However, high positive risk taking was uniquely associated with dampened dmPFC tracking of expected value. Together, results show that adolescents' positive risk taking is associated with neural activity during risky decision-making. Findings are among the first to identify brain-behavior correlations associated with positive risk taking during adolescence.

Self-oriented neural circuitry predicts other-oriented adaptive risks in adolescence: a longitudinal study.

Adolescence is marked by changes in decision-making and perspective-taking abilities. Although adolescents make more adaptive decisions with age, little is understood about how adolescents take adaptive risks that impact others and how this behavior changes developmentally. Functional coupling between reward [e.g., ventral striatum (VS)] and 'social brain' [e.g. temporal parietal junction (TPJ)/ posterior superior temporal sulcus (pSTS), medial prefrontal cortex (mPFC)] systems may be differentially shape adaptive risks for the self and other. A total of 173 participants completed between one and three sessions across three waves [a total of 433 behavioral and 403 functional magnetic resonance imaging (fMRI) data points]. During an fMRI scan, adolescents completed a risky decision-making task where they made risky decisions to win money for themselves and their parent. The risky decisions varied in their expected value (EV) of potential reward. Results show that from the 6th through 9th grades, adolescents took increasingly more adaptive risks for themselves than for their parent. Additionally, greater VS-TPJ/pSTS and VS-mPFC connectivity that tracks EV when making risky decisions for themselves in 6th grade, but a lower VS-mPFC connectivity in 9th grade, predicted greater adaptive risk-taking for their parent. This study contributes to our understanding of the self as a neural proxy for promoting adaptive social behaviors in youth.

The role of early attachment and parental presence in adolescent behavioral and neurobiological regulation.

Early attachment shapes brain development underlying emotion regulation. Given that sensitivity to affective cues is heightened during adolescence and effective emotion regulation strategies continue to develop, it is imperative to examine the role of early attachment and parental influence on adolescent regulation. Fifty-one children (M age=32.61 months) participated in a modified Strange Situation with their mother and approximately 10 years later (M age =13.2 years) completed an fMRI scan during which they were presented with appetitive and aversive affective cues (images of adolescent interactions) during a Go-Nogo task. They completed the task alone and in the presence of a parent. Behavioral multilevel models and whole-brain analyses showed attachment-related patterns, such that affective cues elicited greater behavioral and neural dysregulation in insecure (versus secure) adolescents.Furthermore, parental presence buffered behavioral and neural dysregulation toward socially aversive cues for adolescents with early insecure attachment, underscoring the salience of caregivers across development in promoting regulation in their offspring.

Neural Correlates of Conflicting Social Influence on Adolescent Risk Taking.

Adolescence is often characterized by heightened risk-taking behaviors, which are shaped by social influence from parents and peers. However, little is understood about how adolescents make risky decisions under conflicting influence. The valuation system in the brain may elucidate how adolescents differentially integrate conflicting social information. Twenty-eight adolescents (Mage  = 12.7 years) completed a social influence task during a functional magnetic resonance imaging scan. Behaviorally, adolescents took more risks only when their parent endorsed risky decisions but not when their peers endorsed risky decisions. At the neural level, adolescents showed enhanced vmPFC-striatum functional connectivity when they made risky decisions that followed their parents' risky decisions. Results suggest that parents' decisions may guide youths' risk-taking behavior under conflicting influence.

Neural Underpinnings of Social Contextual Influences on Adolescent Risk-Taking.

Purpose of review: Adolescence is a developmental period often characterized by heightened risk taking and increased sensitivity to socially salient stimuli. In this report, we discuss how the developing brain serves as both a link between, and a susceptibility factor for, social contextual factors and risk taking in adolescence. Recent findings: Neural activity in regions related to affective processing, cognitive control, and social cognition, which continue to develop across the adolescent years, shape the relationship between adolescents' social environment and their risk taking. Summary: Examining neural patterns of adolescent brain development enriches our understanding of how adolescents' complex social environment modulates their risk-taking behavior, which may have implications for adolescents' current and future substance use.

Behavioral and Neural Dysregulation to Social Rewards and Links to Internalizing Symptoms in Adolescents.

Adolescence is a time of unique sensitivity to socially salient stimuli such as social rewards. This period overlaps with the onset of psychopathology such as internalizing and externalizing symptoms. In the current studies, we examined behavioral and neural patterns of dysregulation to social rewards and threats, and links to internalizing and externalizing symptoms in youths. In study 1, we used a social Go/NoGo cognitive control task using peer faces to test for age-related behavioral differences in inhibitory failures in adolescents (N = 53, Mage = 13.37 years), and adults (N = 51, Mage = 43.71 years). In study 2, an independent adolescent sample (N = 51, Mage = 13.98 years) completed a similar social Go/NoGo cognitive control task during fMRI. Results show that adolescents had greater inhibitory failures - as measured by false alarm rate - to both social reward and threat cues than adults, and more so to social reward than threat cues. Greater inhibitory failures to social reward than threat cues were associated with greater internalizing symptoms, but were not significantly related to externalizing symptoms. At the neural level, greater inhibitory failures to social reward than threat cues as well as greater internalizing symptoms were both associated with heightened amygdala-ventral striatum connectivity. Our findings indicate that subcortico-subcortical connectivity, which is deemed to occur chronologically earlier and thus necessary for subcortico-cortical circuits, may serve as an early biomarker for emotion dysregulation and a risk factor for internalizing symptoms.