Adolescence is often described as a period of heightened reactivity to emotions paired with reduced regulatory capacities, a combination suggested to contribute to risk-taking and susceptibility to peer influence during puberty. However, no longitudinal research has definitively linked these behavioral changes to underlying neural development. Here, 38 neurotypical participants underwent two fMRI sessions across the transition from late childhood (10 years) to early adolescence (13 years). Responses to affective facial displays exhibited a combination of general and emotion-specific changes in ventral striatum (VS), ventromedial PFC, amygdala, and temporal pole. Furthermore, VS activity increases correlated with decreases in susceptibility to peer influence and risky behavior. VS and amygdala responses were also significantly more negatively coupled in early adolescence than in late childhood while processing sad and happy versus neutral faces. Together, these results suggest that VS responses to viewing emotions may play a regulatory role that is critical to adolescent interpersonal functioning.
The mirror neuron system (MNS) has been proposed to play an important role in social cognition by providing a neural mechanism by which others’ actions, intentions, and emotions can be understood. Here functional magnetic resonance imaging was used to directly examine the relationship between MNS activity and two distinct indicators of social functioning in typically-developing children (aged 10.1 years±7 months): empathy and interpersonal competence. Reliable activity in pars opercularis, the frontal component of the MNS, was elicited by observation and imitation of emotional expressions. Importantly, activity in this region (as well as in the anterior insula and amygdala) was significantly and positively correlated with established behavioral measures indexing children’s empathic behavior (during both imitation and observation) and interpersonal skills (during imitation only). These findings suggest that simulation mechanisms and the MNS may indeed be relevant to social functioning in everyday life during typical human development.
Self-evaluations undergo significant transformation during early adolescence, developing in parallel with the heightened complexity of teenagers’ social worlds. Intuitive theories of adolescent development, based in part on animal work, suggest that puberty is associated with neural-level changes that facilitate a “social reorientation” (Nelson, Leibenluft, McClure, and Pine, 2005). However, direct tests of this hypothesis using neuroimaging are limited in humans. This longitudinal fMRI study examined neurodevelopmental trajectories associated with puberty, self-evaluations, and the presumed social reorientation during the transition from childhood to adolescence. Participants (N = 27, M age = 10.1 and 13.1 years at timepoints one and two, respectively) engaged in trait evaluations of two targets (the self and a familiar fictional other), across two domains of competence (social and academic). Responses in ventromedial PFC increased with both age and pubertal development during self-evaluations in the social domain, but not in the academic domain. These results suggest changes in social self-evaluations are intimately connected with biology, not just peer contexts, and provide important empirical support for the relationship between neurodevelopment, puberty, and social functioning.
Adolescence is marked by profound psychosocial and physiological changes. Although investigations into the interactions between these forces have begun to shed light on the neural correlates of affective processing during the transition to adolescence, relatively little is known about the relationship between pubertal development and emotion perception at the neural level. In the current longitudinal study, 45 neurotypical participants were shown affective facial displays while undergoing fMRI, at ages 10 and 13. Neural responses to emotional expressions at both time points were then correlated with a self-report measure of pubertal development, revealing positive associations with activity in amygdala, thalamus and visual cortical areas at age 10 that increased in magnitude and extent by age 13. At the latter time point, pubertal development was additionally correlated with enhanced responses to faces in temporal pole, ventrolateral prefrontal cortex (PFC) and dorsomedial PFC. Longitudinal comparisons revealed that the relationships between pubertal development and activity in the amygdala, hippocampus and temporal pole were significantly stronger during early adolescence than late childhood. These results suggest that pubertal development per se is linked to neural processing of socioemotional stimuli, particularly with respect to the integration of complex perceptual input and higher order cortical processing of affective content.
adolescence; puberty; emotion; fMRI; amygdala; longitudinal
In this article, we review three areas of research within adolescent social cognitive and affective neuroscience: (i) emotion reactivity and regulation, (ii) mentalizing and (iii) peer relations, including social rejection or acceptance as well as peer influence. The review provides a context for current contributions to the special issue of Social Cognitive and Affective Neuroscience on Adolescence, and highlights three important themes that emerge from the special issue, which are relevant to future research. First, the age of participants studied (and labels for these age groups) is a critical design consideration. We suggest that it might be logical to reduce the reliance on convenience samples of undergraduates to represent adults in psychology and cognitive neuroscience studies, since there is substantial evidence that the brain is still developing within this age range. Second, developmental researchers are broadening their scope of inquiry by testing for non-linear effects, via increased use of longitudinal strategies or much wider age ranges and larger samples. Third, there is increasing appreciation for the interrelatedness of the three areas of focus in this special issue (emotion reactivity and regulation, mentalizing, and peer relations), as well as with other areas of interest in adolescent development.
Previous neuroimaging research with adults suggests that the medial prefrontal cortex (MPFC) and the medial posterior parietal cortex (MPPC) are engaged during self-knowledge retrieval processes. However, this has yet to be assessed in a developmental sample. Twelve children and 12 adults (average age = 10.2 and 26.1 years, respectively) reported whether short phrases described themselves or a highly familiar other (Harry Potter) while undergoing functional magnetic resonance imaging. In both children and adults, the MPFC was relatively more active during self- than social knowledge retrieval, and the MPPC was relatively more active during social than self-knowledge retrieval. Direct comparisons between children and adults indicated that children activated the MPFC during self-knowledge retrieval to a much greater extent than adults. The particular regions of the MPPC involved varied between the two groups, with the posterior precuneus engaged by adults, but the anterior precuneus and posterior cingulate engaged by children. Only children activated the MPFC significantly above baseline during self-knowledge retrieval. Implications for social cognitive development and the processing functions performed by the MPFC are discussed.
To examine mirror neuron abnormalities in autism, high-functioning children with autism and matched controls underwent fMRI while imitating and observing emotional expressions. Although both groups performed the tasks equally well, children with autism showed no mirror neuron activity in the inferior frontal gyrus (pars opercularis). Notably, activity in this area was inversely related to symptom severity in the social domain, suggesting that a dysfunctional ‘mirror neuron system’ may underlie the social deficits observed in autism.
The dual-systems model of a ventral affective system, whose reactivity confers risks and liabilities, and a prefrontal control system, whose regulatory capacities buffer against these vulnerabilities, is an intuitive account that pervades many fields in the cognitive neurosciences – especially in the study of populations that differ from neurotypical adults, such as adolescents or individuals with affective or impulse regulation disorders. However, recent evidence that is inconsistent with dual-systems models illustrates the complexity of developmental and clinical variations in brain function. Building new models to account for this complexity is critical to progress in these fields, and will be facilitated by research that emphasizes network-based approaches and maps relationships between structure and function, as well as brain and behavior, over time.
Experiences of adversity in the early years of life alter the developing brain. However, evidence documenting this relationship often focuses on severe stressors and relies on peripheral measures of neurobiological functioning during infancy. The present study employed functional magnetic resonance imaging (fMRI) during natural sleep to examine associations between a more moderate environmental stressor (non-physical interparental conflict), and 6–12 month-old infants’ neural processing of emotional tone of voice. The primary question was whether interparental conflict experienced by infants is associated with neural responses to emotional tone of voice, particularly very angry speech. Results indicated that maternal report of higher interparental conflict was associated with infants’ heightened neural responses to very angry versus neutral speech across several brain regions implicated in emotion and stress reactivity and regulation (including rostral anterior cingulate cortex, caudate, thalamus and hypothalamus) – suggesting that even moderate environmental stress may be associated with brain functioning during infancy.
Psychological Stress; Neuroimaging; Emotional Development; Infant Development
Classic theories of self-development suggest people define themselves in part through internalized perceptions of other people’s beliefs about them, known as reflected self-appraisals. This study uses functional magnetic resonance imaging to compare the neural correlates of direct and reflected self-appraisals in adolescence (N = 12, ages 11–14 years) and adulthood (N = 12, ages 23–30 years). During direct self-reflection, adolescents demonstrated greater activity than adults in networks relevant to self-perception (medial prefrontal and parietal cortices) and social-cognition (dorsomedial prefrontal cortex, temporal–parietal junction, and posterior superior temporal sulcus), suggesting adolescent self-construals may rely more heavily on others’ perspectives about the self. Activity in the medial fronto-parietal network was also enhanced when adolescents took the perspective of someone more relevant to a given domain.
The human reward system is sensitive to both social (e.g., validation) and non-social rewards (e.g., money) and is likely integral for relationship development and reputation building. However, data is sparse on the question of whether implicit social reward processing meaningfully contributes to explicit social representations such as trust and attachment security in pre-existing relationships. This event-related fMRI experiment examined reward system prediction-error activity in response to a potent social reward—social validation—and this activity's relation to both attachment security and trust in the context of real romantic relationships. During the experiment, participants' expectations for their romantic partners' positive regard of them were confirmed (validated) or violated, in either positive or negative directions. Primary analyses were conducted using predefined regions of interest, the locations of which were taken from previously published research. Results indicate that activity for mid-brain and striatal reward system regions of interest was modulated by social reward expectation violation in ways consistent with prior research on reward prediction-error. Additionally, activity in the striatum during viewing of disconfirmatory information was associated with both increases in post-scan reports of attachment anxiety and decreases in post-scan trust, a finding that follows directly from representational models of attachment and trust.
reward system; prediction-error; social reward; attachment; love; striatum; trust; fMRI
Extensive developmental research has linked peer rejection during adolescence with a host of psychopathological outcomes, including depression. Moreover, recent neuroimaging research has suggested that increased activity in the subgenual region of the anterior cingulate cortex (subACC), which has been consistently linked with depression, is related to heightened sensitivity to peer rejection among adolescents. The goal of the current study was to directly test the hypothesis that adolescents’ subACC responses are predictive of their risk for future depression, by examining the relationship between subACC activity during peer rejection and increases in depressive symptoms during the following year. During a functional magnetic resonance imaging scan, 20 13-year-olds were ostensibly excluded by peers during an online social interaction. Participants’ depressive symptoms were assessed via parental reports at the time of the scan and 1 year later. Region of interest and whole-brain analyses indicated that greater subACC activity during exclusion was associated with increases in parent-reported depressive symptoms during the following year. These findings suggest that subACC responsivity to social exclusion may serve as a neural marker of adolescents’ risk for future depression and have implications for understanding the relationship between sensitivity to peer rejection and the increased risk of depression that occurs during adolescence.
Neuroimaging studies with adults have begun to reveal the neural bases of empathy; however, this research has focused on empathy for physical pain, rather than empathy for negative social experiences. Moreover, this work has not examined adolescents who may frequently witness and empathize with others who experience negative social experiences like peer rejection. Here, we examined neural activity among early adolescents observing social exclusion compared to observing inclusion, and how this activity related to both trait empathy and subsequent prosocial behavior. Participants were scanned while they observed an individual whom they believed was being socially excluded. At least one day prior to the scan they reported their trait empathy, and following the scan they wrote emails to the excluded victim that were rated for prosocial behavior (e.g., helping, comforting). Observing exclusion compared to inclusion activated regions involved in mentalizing (i.e., dorsomedial prefrontal cortex; DMPFC), particularly among highly empathic individuals. Additionally, individuals who displayed more activity in affective, pain-related regions during observed exclusion compared to inclusion subsequently wrote more prosocial emails to excluded victims. Overall findings suggest that when early adolescents witness social exclusion in their daily lives, some may actually ‘feel the pain’ of the victims and act more prosocially toward them as a result.
adolescence; empathy; peer rejection; social exclusion; functional magnetic resonance imaging
Developmental research has demonstrated the harmful effects of peer rejection during adolescence; however, the neural mechanisms responsible for this salience remain unexplored. In this study, 23 adolescents were excluded during a ball-tossing game in which they believed they were playing with two other adolescents during an fMRI scan; in reality, participants played with a preset computer program. Afterwards, participants reported their exclusion-related distress and rejection sensitivity, and parents reported participants’ interpersonal competence. Similar to findings in adults, during social exclusion adolescents displayed insular activity that was positively related to self-reported distress, and right ventrolateral prefrontal activity that was negatively related to self-reported distress. Findings unique to adolescents indicated that activity in the subgenual anterior cingulate cortex (subACC) related to greater distress, and that activity in the ventral striatum related to less distress and appeared to play a role in regulating activity in the subACC and other regions involved in emotional distress. Finally, adolescents with higher rejection sensitivity and interpersonal competence scores displayed greater neural evidence of emotional distress, and adolescents with higher interpersonal competence scores also displayed greater neural evidence of regulation, perhaps suggesting that adolescents who are vigilant regarding peer acceptance may be most sensitive to rejection experiences.
peer rejection; adolescence; functional magnetic resonance imaging