A Neurodevelopmental Shift in Reward Circuitry from Mother's to Nonfamilial Voices in Adolescence.

The social worlds of young children primarily revolve around parents and caregivers, who play a key role in guiding children's social and cognitive development. However, a hallmark of adolescence is a shift in orientation toward nonfamilial social targets, an adaptive process that prepares adolescents for their independence. Little is known regarding neurobiological signatures underlying changes in adolescents' social orientation. Using functional brain imaging of human voice processing in children and adolescents (ages 7-16), we demonstrate distinct neural signatures for mother's voice and nonfamilial voices across child and adolescent development in reward and social valuation systems, instantiated in nucleus accumbens and ventromedial prefrontal cortex. While younger children showed greater activity in these brain systems for mother's voice compared with nonfamilial voices, older adolescents showed the opposite effect with increased activity for nonfamilial compared with mother's voice. Findings uncover a critical role for reward and social valuative brain systems in the pronounced changes in adolescents' orientation toward nonfamilial social targets. Our approach provides a template for examining developmental shifts in social reward and motivation in individuals with pronounced social impairments, including adolescents with autism.SIGNIFICANCE STATEMENT Children's social worlds undergo a transformation during adolescence. While socialization in young children revolves around parents and caregivers, adolescence is characterized by a shift in social orientation toward nonfamilial social partners. Here we show that this shift is reflected in neural activity measured from reward processing regions in response to brief vocal samples. When younger children hear their mother's voice, reward processing regions show greater activity compared with when they hear nonfamilial, unfamiliar voices. Strikingly, older adolescents show the opposite effect, with increased activity for nonfamilial compared with mother's voice. Findings identify the brain basis of adolescents' switch in social orientation toward nonfamilial social partners and provides a template for understanding neurodevelopment in clinical populations with social and communication difficulties.

Characterizing trajectories of anxiety, depression, and criminal offending in male adolescents over the 5 years following their first arrest.

Youth in the juvenile justice system evince high rates of mental health symptoms, including anxiety and depression. How these symptom profiles change after first contact with the justice system and - importantly - how they are related to re-offending remains unclear. Here, we use latent growth curve modeling to characterize univariate and multivariate growth of anxiety, depression, and re-offending in 1216 male adolescents over 5 years following their first arrest. Overall, the group showed significant linear and quadratic growth in internalizing symptoms and offending behaviors over time such that levels decreased initially after first arrest followed by a small but significant upturn occurring a few years later. Crucially, multivariate growth models revealed strong positive relationships between the rates of growth in internalizing symptoms and offending behaviors such that improvements in mental health related to greater decreases in offending, and vice versa. These results highlight the reciprocal nature of internalizing and externalizing problems in adolescence, underscoring the importance of considering mental health alongside offending in the juvenile justice system.

Exploring Disproportionate Minority Contact in the Juvenile Justice System Over the Year Following First Arrest.

Minority youth are disproportionately represented in the juvenile justice system. Examining how racial disparities relate to biased entry into and continued involvement with the system, while accounting for past and current offending, can provide context about the mechanisms behind overrepresentation. 1,216 adolescents were examined after first arrest to explore associations between race and history of self-reported offending, likelihood of formal processing, and likelihood of rearrest. Black youth committed fewer offenses prior to arrest than White youth, Black and Latino youth were more likely to be formally processed, and Black youth were most likely to be rearrested (even controlling for postbaseline offending), highlighting that minority youth are overrepresented in the juvenile justice system despite similar or lower levels of criminal behavior.

Neural circuits underlying mother's voice perception predict social communication abilities in children.

The human voice is a critical social cue, and listeners are extremely sensitive to the voices in their environment. One of the most salient voices in a child's life is mother's voice: Infants discriminate their mother's voice from the first days of life, and this stimulus is associated with guiding emotional and social function during development. Little is known regarding the functional circuits that are selectively engaged in children by biologically salient voices such as mother's voice or whether this brain activity is related to children's social communication abilities. We used functional MRI to measure brain activity in 24 healthy children (mean age, 10.2 y) while they attended to brief (<1 s) nonsense words produced by their biological mother and two female control voices and explored relationships between speech-evoked neural activity and social function. Compared to female control voices, mother's voice elicited greater activity in primary auditory regions in the midbrain and cortex; voice-selective superior temporal sulcus (STS); the amygdala, which is crucial for processing of affect; nucleus accumbens and orbitofrontal cortex of the reward circuit; anterior insula and cingulate of the salience network; and a subregion of fusiform gyrus associated with face perception. The strength of brain connectivity between voice-selective STS and reward, affective, salience, memory, and face-processing regions during mother's voice perception predicted social communication skills. Our findings provide a novel neurobiological template for investigation of typical social development as well as clinical disorders, such as autism, in which perception of biologically and socially salient voices may be impaired.

Anxiety may alter the role of fronto-striatal circuitry in adolescent risky decision-making.

BACKGROUND: Anxiety disorders often emerge in adolescence and are associated with risk aversion. Risk aversion conflicts with the typical adolescent approach-motivated phenotype and can interfere with learning and contribute to symptom maintenance. METHODS: We investigated the neural and behavioral correlates of risk avoidance in a diverse sample of adolescents (N = 137; MAge = 11.3; 34.3 % white, 22.1 % Latino, 20 % Asian, 14.3 % Black, 9.3 % Mixed Race) as they completed a task involving risky decision-making and response inhibition during fMRI. Voluntary cautious choice was compared to successful response inhibition to isolate the neural systems underlying the decision to avoid a risk and identify their relation to risk-taking and anxiety in adolescents. RESULTS: Anxious adolescents self-reported more avoidance but demonstrated normative risk-taking on the laboratory task. Interestingly, they responded quickly during response inhibition but took longer to decide in the face of risk. All youth showed widespread recruitment of decision-making and salience network regions when deciding to avoid risk. The neural mechanisms driving avoidance differed based on anxiety such that left inferior frontal gyrus (IFG) activation was linked to risk avoidance in adolescents with low anxiety and risk-taking in anxious adolescents, while striatal connectivity was linked to risk avoidance in anxious adolescents and risk-taking in those with low anxiety. LIMITATIONS: This work is cross-sectional and therefore cannot speak to causality or directionality of effects. CONCLUSIONS: These results suggest that the neural mechanisms contributing to adolescent risk-taking may function to promote avoidance in anxious youth, increasing vulnerability to maladaptive avoidance and further anxiety development.

Sleep variability over a 2-week period is associated with restfulness and intrinsic limbic network connectivity in adolescents.

STUDY OBJECTIVES: Sleep duration and intraindividual variability in sleep duration undergo substantial changes in adolescence and impact brain and behavioral functioning. Although experimental work has linked acute sleep deprivation to heightened limbic responding and reduced regulatory control, there is limited understanding of how variability in sleep patterns might interact with sleep duration to influence adolescent functioning. This is important for optimal balancing of length and consistency of sleep. Here, we investigated how objective indices of sleep duration and variability relate to stress, restfulness, and intrinsic limbic network functioning in adolescents. METHODS: A sample of 101 adolescents ages 14-18 reported their stressors, after which they wore wrist actigraph watches to monitor their sleep and rated their restfulness every morning over a 2-week period. They also completed a resting-state fMRI scan. RESULTS: Adolescents reporting more stress experienced shorter sleep duration and greater sleep variability over the 2-week period. Longer nightly sleep duration was linked to feeling more rested the next morning, but this effect was reduced in adolescents with high cumulative sleep variability. Sleep variability showed both linear and quadratic effects on limbic connectivity: adolescents with high sleep variability exhibited more connectivity within the limbic network and less connectivity between the limbic and frontoparietal networks than their peers, effects which became stronger once variability exceeded an hour. CONCLUSIONS: Results suggest that cumulative sleep variability is related to stress and limbic network connectivity and shows interactive effects with sleep duration, highlighting the importance of balancing length and consistency of sleep for optimal functioning in adolescence.

Threat or thrill? the neural mechanisms underlying the development of anxiety and risk taking in adolescence.

Anxiety is common in adolescence and has been linked to a plethora of negative outcomes across development. While previous studies of anxiety have focused on threat sensitivity, less work has considered the concurrent development of threat- and reward-related neural circuitry and how these circuits interact and compete during puberty to influence typical adolescent behaviors such as increased risk taking and exploration. The current review integrates relevant findings from clinical and developmental neuroimaging studies to paint a multidimensional picture of adolescent-onset anxiety against the backdrop of typical adolescent development. Ultimately, this paper argues that longitudinal neuroimaging studies tracking approach and avoidance motivations across development are needed to fully understand the mechanisms underlying the development of anxiety in adolescence and to identify and provide effective interventions for at-risk youth.

Neural activity moderates the association between sleep and risky driving behaviors in adolescence.

The biological, environmental, and psychosocial changes that occur in adolescence engender an increase in risk taking often linked to the high rates of motor vehicle crashes amongst young drivers. Most U.S. adolescents suffer from poor sleep, which is known to exacerbate the risk of driving crashes; however, research has yet to uncover a neurobiological link between sleep and risky driving in adolescence. Here, we examined potential moderators of the sleep-risk relation in fifty-six adolescents (14-18y/o) as they completed a driving task during fMRI. While poor sleep was associated with increased risky driving (i.e., running more yellow lights), good sleep emerged as a novel buffer against risky driving in lower sensation-seeking adolescents. Neural activity in the ventral striatum (VS), a key node of the risk-taking circuit, also moderated the sleep-risk association: sleep was related to risk-taking in individuals demonstrating high, but not low, VS response during risky decision-making, suggesting that reward-related neural response may underly the connection between sleep and risk-taking in adolescence. This study sheds light on the risk of driving crashes in youth by highlighting sleep as both an exacerbator and a buffer of risky driving in adolescence. Taken together, these results underscore the importance of improving adolescent sleep.

Impaired voice processing in reward and salience circuits predicts social communication in children with autism.

Engaging with vocal sounds is critical for children's social-emotional learning, and children with autism spectrum disorder (ASD) often 'tune out' voices in their environment. Little is known regarding the neurobiological basis of voice processing and its link to social impairments in ASD. Here, we perform the first comprehensive brain network analysis of voice processing in children with ASD. We examined neural responses elicited by unfamiliar voices and mother's voice, a biologically salient voice for social learning, and identified a striking relationship between social communication abilities in children with ASD and activation in key structures of reward and salience processing regions. Functional connectivity between voice-selective and reward regions during voice processing predicted social communication in children with ASD and distinguished them from typically developing children. Results support the Social Motivation Theory of ASD by showing reward system deficits associated with the processing of a critical social stimulus, mother's voice, in children with ASD. Editorial note: This article has been through an editorial process in which the authors decide how to respond to the issues raised during peer review. The Reviewing Editor's assessment is that minor issues remain unresolved (see decision letter).