Brain functional correlates of emotion regulation across adolescence and young adulthood

Few studies have examined the neural correlates of emotion regulation across adolescence and young adulthood. Existing studies of cognitive reappraisal indicate that improvements in regulatory efficiency may develop linearly across this period, in accordance with maturation of prefrontal cortical systems. However, there is also evidence for adolescent differences in reappraisal specific to the activation of “social‐information processing network” regions, including the amygdala and temporal‐occipital cortices. Here, we use fMRI to examine the neural correlates of emotional reactivity and reappraisal in response to aversive social imagery in a group of 78 adolescents and young adults aged 15–25 years. Within the group, younger participants exhibited greater activation of temporal‐occipital brain regions during reappraisal in combination with weaker suppression of amygdala reactivity—the latter being a general correlate of successful reappraisal. Further analyses demonstrated that these age‐related influences on amygdala reactivity were specifically mediated by activation of the fusiform face area. Overall, these findings suggest that enhanced processing of salient social cues (i.e., faces) increases reactivity of the amygdala during reappraisal and that this relationship is stronger in younger adolescents. How these relationships contribute to well‐known vulnerabilities of emotion regulation during this developmental period will be an important topic for ongoing research. Hum Brain Mapp 37:7–19, 2016. © 2015 Wiley Periodicals, Inc.     

Thinning of the lateral prefrontal cortex during adolescence predicts emotion regulation in females

Adolescence is a crucial period for the development of adaptive emotion regulation strategies. Despite the fact that structural maturation of the prefrontal cortex during adolescence is often assumed to underlie the maturation of emotion regulation strategies, no longitudinal studies have directly assessed this relationship. This study examined whether use of cognitive reappraisal strategies during late adolescence was predicted by (i) absolute prefrontal cortical thickness during early adolescence and (ii) structural maturation of the prefrontal cortex between early and mid-adolescence. Ninety-two adolescents underwent baseline and follow-up magnetic resonance imaging scans when they were aged approximately 12 and 16 years, respectively. FreeSurfer software was used to obtain cortical thickness estimates for three prefrontal regions [anterior cingulate cortex; dorsolateral prefrontal cortex (dlPFC); ventrolateral prefrontal cortex (vlPFC)]. The Emotion Regulation Questionnaire was completed when adolescents were aged approximately 19 years. Results showed that greater cortical thinning of the left dlPFC and left vlPFC during adolescence was significantly associated with greater use of cognitive reappraisal in females, though no such relationship was evident in males. Furthermore, baseline left dlPFC thickness predicted cognitive reappraisal at trend level. These findings suggest that cortical maturation may play a role in the development of adaptive emotion regulation strategies during adolescence.     

How grossed out are you? The neural bases of emotion regulation from childhood to adolescence

The ability to regulate one's emotions is critical to mental health and well-being, and is impaired in a wide range of psychopathologies, some of which initially manifest in childhood or adolescence. Cognitive reappraisal is a particular approach to emotion regulation frequently utilized in behavioral psychotherapies. Despite a wealth of research on cognitive reappraisal in adults, little is known about the developmental trajectory of brain mechanisms subserving this form of emotion regulation in children. In this functional magnetic resonance imaging study, we asked children and adolescents to up-and down-regulate their response to disgusting images, as the experience of disgust has been linked to anxiety disorders. We demonstrate distinct patterns of brain activation during successful up- and down-regulation of emotion, as well as an inverse correlation between activity in ventromedial prefrontal cortex (vmPFC) and limbic structures during down-regulation, suggestive of a potential regulatory role for vmPFC. Further, we show age-related effects on activity in PFC and amygdala. These findings have important clinical implications for the understanding of cognitive-based therapies in anxiety disorders in childhood and adolescence.     

Adolescent social cognitive and affective neuroscience: past, present, and future

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.     

Cognitive reappraisal of peer rejection in depressed versus non-depressed adolescents: Functional connectivity differences

BackgroundDepression is the most common psychiatric disorder in adolescence, and is characterised by an inability to down-regulate negative emotional responses to stress. Adult studies suggest this may be associated with reduced functional connectivity between prefrontal and subcortical regions, yet the neurological mechanisms in adolescence remain unclear.MethodsWe developed a novel, age-appropriate, reappraisal paradigm to investigate functional connectivity during reappraisal of a real-life source of stress in 15 depressed and 15 non-depressed adolescents. During fMRI, participants i) attended to, and ii) implemented reappraisal techniques (learnt prior to fMRI) in response to, rejection.ResultsReappraisal reduced negative mood and belief in negative thoughts in both groups alike, however during reappraisal (versus attend) trials, depressed adolescents showed greater connectivity between the right frontal pole and numerous subcortical and cortical regions than non-depressed adolescents.ConclusionsThese findings tentatively suggest that, when instructed, depressed adolescents do have the ability to engage neural networks involved in emotion regulation, possibly because adolescence reflects a period of heightened plasticity. These data support the value of cognitive reappraisal as a treatment tool, identify neural markers that could be used to optimise current therapies, and lay the foundations for developing novel neuroscientific techniques for the treatment of adolescent depression.     

The development of social cognition in adolescence: An integrated perspective

Social cognitive processes are critical in navigating complex social interactions and are associated with a network of brain areas termed the ‘social brain’. Here, we describe the development of social cognition, and the structural and functional changes in the social brain during adolescence, a period of life characterised by extensive changes in social behaviour and environments. Neuroimaging and behavioural studies have demonstrated that the social brain and social cognition undergo significant development in human adolescence. Development of social cognition and the social brain are discussed in the context of developments in other neural systems, such as those implicated in motivational-affective and cognitive control processes. Successful transition to adulthood requires the rapid refinement and integration of these processes and many adolescent-typical behaviours, such as peer influence and sensitivity to social exclusion, involve dynamic interactions between these systems. Considering these interactions, and how they vary between individuals and across development, could increase our understanding of adolescent brain and behavioural development.     

Neurodevelopmental changes across adolescence in viewing and labeling dynamic peer emotions

Adolescence is a sensitive period of social-affective development, characterized by biological, neurological, and social changes. The field currently conceptualizes these changes in terms of an imbalance between systems supporting reactivity and regulation, specifically nonlinear changes in reactivity networks and linear changes in regulatory networks. Previous research suggests that the labeling or reappraisal of emotion increases activity in lateral prefrontal cortex (LPFC), and decreases activity in amygdala relative to passive viewing of affective stimuli. However, past work in this area has relied heavily on paradigms using static, adult faces, as well as explicit regulation. In the current study, we assessed cross-sectional trends in neural responses to viewing and labeling dynamic peer emotional expressions in adolescent girls 10–23 years old. Our dynamic adolescent stimuli set reliably and robustly recruited key brain regions involved in emotion reactivity (medial orbital frontal cortex/ventral medial prefrontal cortex; MOFC/vMPFC, bilateral amygdala) and regulation (bilateral dorsal and ventral LPFC). However, contrary to the age-trends predicted by the dominant models in studies of risk/reward, the LPFC showed a nonlinear age trend across adolescence to labeling dynamic peer faces, whereas the MOFC/vMPFC showed a linear decrease with age to viewing dynamic peer faces. There were no significant age trends observed in the amygdala.     

The social brain in adolescence: evidence from functional magnetic resonance imaging and behavioural studies

Social cognition is the collection of cognitive processes required to understand and interact with others. The term ‘social brain’ refers to the network of brain regions that underlies these processes. Recent evidence suggests that a number of social cognitive functions continue to develop during adolescence, resulting in age differences in tasks that assess cognitive domains including face processing, mental state inference and responding to peer influence and social evaluation. Concurrently, functional and structural magnetic resonance imaging (MRI) studies show differences between adolescent and adult groups within parts of the social brain. Understanding the relationship between these neural and behavioural observations is a challenge. This review discusses current research findings on adolescent social cognitive development and its functional MRI correlates, then integrates and interprets these findings in the context of hypothesised developmental neurocognitive and neurophysiological mechanisms.     

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     

The neurobiology of the emotional adolescent: From the inside out

Adolescents are commonly portrayed as highly emotional, with their behaviors often hijacked by their emotions. Research on the neural substrates of adolescent affective behavior is beginning to paint a more nuanced picture of how neurodevelopmental changes in brain function influence affective behavior, and how these influences are modulated by external factors in the environment. Recent neurodevelopmental models suggest that the brain is designed to promote emotion regulation, learning, and affiliation across development, and that affective behavior reciprocally interacts with age-specific social demands and different social contexts. In this review, we discuss current findings on neurobiological mechanisms of adolescents’ affective behavior and highlight individual differences in and social-contextual influences on adolescents’ emotionality. Neurobiological mechanisms of affective processes related to anxiety and depression are also discussed as examples. As the field progresses, it will be critical to test new hypotheses generated from the foundational empirical and conceptual work and to focus on identifying more precisely how and when neural networks change in ways that promote or thwart adaptive affective behavior during adolescence.     

“Don’t judge me!”: Links between in vivo attention bias toward a potentially critical judge and fronto-amygdala functional connectivity during rejection in adolescent girls

During adolescence, increases in social sensitivity, such as heightened attentional processing of social feedback, may be supported by developmental changes in neural circuitry involved in emotion regulation and cognitive control, including fronto-amygdala circuitry. Less negative fronto-amygdala circuitry during social threat processing may contribute to heightened attention to social threat in the environment. However, “real-world” implications of altered fronto-amygdala circuitry remain largely unknown. In this study, we used multiple novel methods, including an in vivo attention bias task implemented using mobile eye-tracking glasses and socially interactive fMRI task, to examine how functional connectivity between the amygdala and prefrontal cortex (PFC) during rejection and acceptance feedback from peers is associated with heightened attention towards potentially critical social evaluation in a real-world environment. Participants were 77 early adolescent girls (ages 11–13) oversampled for shy/fearful temperament. Results support the reliability of this in vivo attention task. Further, girls with more positive functional connectivity between the right amygdala and anterior PFC during both rejection and acceptance feedback attended more to potentially critical social evaluation during the attention task. Findings could suggest that dysfunction in prefrontal regulation of the amygdala’s response to salient social feedback supports heightened sensitivity to socially evaluative threat during adolescence.     

THE ROLE OF PEER REJECTION IN ADOLESCENT DEPRESSION

Adolescence is a period of major risk for depression, which is associated with negative personal, social, and educational outcomes. Yet, in comparison to adult models of depression, very little is known about the specific psychosocial stressors that contribute to adolescent depression, and whether these can be targeted by interventions. In this review, we consider the role of peer rejection. First, we present a comprehensive review of studies using innovative experimental paradigms to understand the role of peer rejection in adolescent depression. We show how reciprocal relationships between peer rejection and depressive symptoms across adolescence powerfully shape and maintain maladaptive trajectories. Second, we consider how cognitive biases and their neurobiological substrates may explain why some adolescents are more vulnerable to the effects of, and perhaps exposure to, peer rejection compared to others. Finally, we draw attention to emerging cognitive and functional magnetic resonance imaging‐based neurofeedback training, which by modifying aspects of information processing may promote more adaptive responses to peer rejection. A better understanding of the mechanisms underlying adolescent depression may not only alleviate symptoms during a period of substantial developmental challenges, but may also reduce the burden of the disorder across the lifespan.     

Emotion regulation and depressive symptoms: Examining the mediation effects of school connectedness in Chinese late adolescents

This study tested Gross's process model of emotion regulation in a Chinese adolescent sample. It hypothesized that emotion regulation strategies (cognitive reappraisal and expressive suppression) would predict adolescents' perception of school connectedness and depressive symptoms. It also posited that school connectedness may be a possible mediator between emotion regulation and depressive symptoms. Participants were 504 adolescents aged 16–18 from two Chinese public upper secondary schools. Structural equation modeling analyses indicated that reappraisal and suppression significantly associated with school connectedness and depressive symptoms, and school connectedness mediated the link between emotion regulation and depressive symptoms, even when the general emotion experiences were controlled. Although boys unexpectedly reported higher level depressive symptoms, the hypothesized model was invariant across gender except for the link between suppression and depressive symptoms. These findings demonstrate that it is meaningful to involve both emotion regulation processes and school connectedness in explaining adolescent depressive symptoms.     

Evidence for dissociable cognitive and neural pathways from poverty versus maltreatment to deficits in emotion regulation

Poverty and threat exposure (TE) predict deficits in emotion regulation (ER). Effective cognitive ER (i.e., reappraisal) may be supported by: (1) cognitive processes implicated in generating and implementing cognitive reappraisal, supported by activation in brain regions involved in cognitive control (e.g., frontal, insular, and parietal cortices) and (2) emotion processing and reactivity, involving identification, encoding, and maintenance of emotional states and related variation in brain activity of regions involved in emotional reactivity (i.e., amygdala). Poverty is associated with deficits in cognitive control, and TE with alterations in emotion processing and reactivity. Our goal was to identify dissociable emotional and cognitive pathways to ER deficits from poverty and TE. Measures of cognitive ability, emotional processing and reactivity, ER, and neural activity during a sadness ER task, were examined from a prospective longitudinal study of youth at risk for depression (n = 139). Both cognitive ability and left anterior insula extending into the frontal operculum activity during a sadness reappraisal task mediated the relationship between poverty and ER. Emotion processing/reactivity didn’t mediate the relationship of TE to ER. Findings support a cognitive pathway from poverty to ER deficits. They also underscore the importance of dissociating mechanisms contributing to ER impairments from adverse early childhood experiences.     

Puberty initiates a unique stage of social learning and development prior to adulthood: Insights from studies of adolescence in wild chimpanzees

In humans, puberty initiates a period of rapid growth, change, and formative neurobehavioral development. Brain and behavior changes during this maturational window contribute to opportunities for social learning. Here we provide new insights into adolescence as a unique period of social learning and development by describing field studies of our closest living relatives, chimpanzees. Like humans, chimpanzees have a multiyear juvenile life stage between weaning and puberty onset followed by a multiyear adolescent life stage after pubertal onset but prior to socially-recognized adulthood. As they develop increasing autonomy from caregivers, adolescent chimpanzees explore and develop many different types of social relationships with a wide range of individuals in a highly flexible social environment. We describe how adolescent social motivations and experiences differ from those of juveniles and adults and expose adolescents to high levels of uncertainty, risk, and vulnerability, as well as opportunities for adaptive social learning. We discuss how these adolescent learning experiences may be shaped by early life and in turn shape varied adult social outcomes. We outline how future chimpanzee field research can contribute in new ways to a more integrative interdisciplinary understanding of adolescence as a developmental window of adaptive social learning and resilience.     

Impact of Sleep and Circadian Rhythms on Addiction Vulnerability in Adolescents

Sleep homeostasis and circadian function are important maintaining factors for optimal health and well-being. Conversely, sleep and circadian disruptions are implicated in a variety of adverse health outcomes, including substance use disorders. These risks are particularly salient during adolescence. Adolescents require 8 to 10 hours of sleep per night, although few consistently achieve these durations. A mismatch between developmental changes and social/environmental demands contributes to inadequate sleep. Homeostatic sleep drive takes longer to build, circadian rhythms naturally become delayed, and sensitivity to the phase-shifting effects of light increases, all of which lead to an evening preference (i.e., chronotype) during adolescence. In addition, school start times are often earlier in adolescence and the use of electronic devices at night increases, leading to disrupted sleep and circadian misalignment (i.e., social jet lag). Social factors (e.g., peer influence) and school demands further impact sleep and circadian rhythms. To cope with sleepiness, many teens regularly consume highly caffeinated energy drinks and other stimulants, creating further disruptions in sleep. Chronic sleep loss and circadian misalignment enhance developmental tendencies toward increased reward sensitivity and impulsivity, increasing the likelihood of engaging in risky behaviors and exacerbating the vulnerability to substance use and substance use disorders. We review the neurobiology of brain reward systems and the impact of sleep and circadian rhythms changes on addiction vulnerability in adolescence and suggest areas that warrant additional research.     

Social experience calibrates neural sensitivity to social feedback during adolescence: A functional connectivity approach

The adaptive calibration model suggests exposure to highly stressful or highly supportive early environments sensitizes the brain to later environmental input. We examined whether family and peer experiences predict neural sensitivity to social cues in 85 adolescent girls who completed a social feedback task during a functional brain scan and an interview assessing adversity. Whole-brain functional connectivity (FC) analyses revealed curvilinear associations between social experiences and FC between the ventral striatum and regions involved in emotion valuation, social cognition, and salience detection (e.g., insula, MPFC, dACC, dlPFC) during social reward processing, such that stronger FC was found at both very high and very low levels of adversity. Moreover, exposure to adversity predicted stronger FC between the amygdala and regions involved in salience detection, social cognition, and emotional memory (e.g., sgACC, precuneus, lingual gyrus, parahippocampal gyrus) during social threat processing. Analyses also revealed some evidence for blunted FC (VS-PCC for reward; amygdala-parahippocampal gyrus for threat) at very high and low levels of adversity. Overall, results suggest social experiences may play a critical role in shaping neural sensitivity to social feedback during adolescence. Future work will need to elucidate the implications of these patterns of neural function for the development of psychopathology.     

Longitudinal associations among family environment,neural cognitive control,and social competence among adolescents

During adolescence, prefrontal cortex regions, important in cognitive control, undergo maturation to adapt to changing environmental demands. Ways through which social-ecological factors contribute to adolescent neural cognitive control have not been thoroughly examined. We hypothesize that household chaos is a context that may modulate the associations among parental control, adolescent neural cognitive control, and developmental changes in social competence. The sample involved 167 adolescents (ages 13–14 at Time 1, 53% male). Parental control and household chaos were measured using adolescents’ questionnaire data, and cognitive control was assessed via behavioral performance and brain imaging at Time 1. Adolescent social competence was reported by adolescents at Time 1 and at Time 2 (one year later). Structural equation modeling analyses indicated that higher parental control predicted better neural cognitive control only among adolescents living in low-chaos households. The association between poor neural cognitive control at Time 1 and social competence at Time 2 (after controlling for social competence at Time 1) was significant only among adolescents living in high-chaos households. Household chaos may undermine the positive association of parental control with adolescent neural cognitive control and exacerbate the detrimental association of poor neural cognitive control with disrupted social competence development.     

Neural representation of emotion regulation goals

The use of top–down cognitive control mechanisms to regulate emotional responses as circumstances change is critical for mental and physical health. Several theoretical models of emotion regulation have been postulated; it remains unclear, however, in which brain regions emotion regulation goals (e.g., the downregulation of fear) are represented. Here, we examined the neural mechanisms of regulating emotion using fMRI and identified brain regions representing reappraisal goals. Using a multimethodological analysis approach, combining standard activation‐based and pattern‐information analyses, we identified a distributed network of lateral frontal, temporal, and parietal regions implicated in reappraisal and within it, a core system that represents reappraisal goals in an abstract, stimulus‐independent fashion. Within this core system, the neural pattern‐separability in a subset of regions including the left inferior frontal gyrus, middle temporal gyrus, and inferior parietal lobe was related to the success in emotion regulation. Those brain regions might link the prefrontal control regions with the subcortical affective regions. Given the strong association of this subsystem with inner speech functions and semantic memory, we conclude that those cognitive mechanisms may be used for orchestrating emotion regulation. Hum Brain Mapp 37:600–620, 2016. © 2015 Wiley Periodicals, Inc.     

Affective flexibility as a developmental building block of cognitive reappraisal: An fMRI study

Cognitive reappraisal is a form of emotion regulation that involves reinterpreting the meaning of a stimulus, often to downregulate one’s negative affect. Reappraisal typically recruits distributed regions of prefrontal and parietal cortex to generate new appraisals and downregulate the emotional response in the amygdala. In the current study, we compared reappraisal ability in an fMRI task with affective flexibility in a sample of children and adolescents (ages 6–17, N = 76). Affective flexibility was defined as variability in valence interpretations of ambiguous (surprised) facial expressions from a second behavioral task. Results demonstrated that age and affective flexibility predicted reappraisal ability, with an interaction indicating that flexibility in children (but not adolescents) supports reappraisal success. Using a region of interest-based analysis of participants’ BOLD time courses, we also found dissociable reappraisal-related brain mechanisms that support reappraisal success and affective flexibility. Specifically, late increases in middle prefrontal cortex activity supported reappraisal success and late decreases in amygdala activity supported flexibility. Together, these results suggest that our novel measure of affective flexibility – the ability to see multiple interpretations of an ambiguous emotional cue – may represent part of the developmental building blocks of cognitive reappraisal ability.