The neurobiology of the emotional adolescent: From the inside out

https://doi.org/10.1016/j.neubiorev.2016.07.037Get rights and content

Highlights

  • Emotionality and affect-related psychopathology increase in adolescence.

  • Managing emotions is a key task of adolescence related to brain and pubertal changes.

  • Neural changes in social-cognitive processes relate to affective behavior.

  • Many features of social experiences shape neural bases of cognition and affect.

  • Ecologically-valid fMRI tasks probe neural substrates of social-emotional experience.

Abstract

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.

Introduction

The emotional life of an adolescent is complex both inside and out. From the “inside”, adolescents experience vast hormonal changes and fine tuning of the neural networks that both produce and manage emotions. From the “outside”, they experience dramatic and dynamic shifts in the structure and significance of key social relationships, such as those with parents, peers, and romantic partners as well as a variety of novel experiences and increasing societal demands. The convergence of these internal and external changes can result in affective experiences and behaviors that are sometimes overwhelming, confusing, and difficult to manage.

Although adolescence has long been hailed as a period of emotional challenge (for both adolescents and their parents) (Hall, 1931), it is only in the past 15 years that we have really begun to understand the “inside” of the adolescent from the perspective of the brain. Tapping into the emotional lives of adolescents is not a straightforward endeavor because adolescents can be reluctant to share their emotions, and, particularly during adolescence, emotional reactions vary tremendously by context. Fortunately, recent methodological advances in neuroscience with particular applications for developmental and clinical populations has led to considerable improvement in our understanding of neurobiological mechanisms of adolescents’ emotional lives. Moreover, recent conceptual models of neurodevelopment in adolescence (Crone and Dahl, 2012) suggest that we can use what has been learned about brain growth and plasticity in adolescence to leverage adolescents’ heightened emotionality in productive ways (e.g., civic engagement) and to discover new strategies to ameliorate forms of emotional dysregulation (e.g., anxiety and depression) that often emerge during adolescence.

In this review, we discuss evidence of three primary connections between neurobiological and affective development in adolescence. First, adolescence is marked by a high level of emotionality and a substantial increase in psychopathological levels of dysfunctional affect. Although individual differences exist in levels of adolescent emotionality, they also correspond broadly with the ordering of changes instantiated by pubertal and brain development. Second, learning to manage one’s emotional reactions is a principal task of adolescence that relates to social-cognitive development. These social-cognitive processes are supported by changes in the connections among brain structures implicated in functions such as such as mentalizing, self-appraisal, social learning, and emotion regulation. Third, in addition to the influence of brain maturation, adolescents’ affective behavior is intertwined with a number of other psychological factors that modify emotional experience. The valence and novelty of certain contexts (particularly in the social domain) and the latent effects of past social experiences interact with neural bases of cognition and emotion to further modify the salience of current experiences. We conclude our review by describing implications of the findings reviewed and recommending future directions for research on the brain’s role in affective behavior during adolescence.

Of note, we orient this review on research that emphasizes social context and social affect; uses neuroimaging; and focuses on a set of specific brain regions for three main reasons. First, we have argued that social interactions and relationships are among the most critical contexts to interact with neurobiological development in adolescence (Nelson and Guyer, 2011, Nelson et al., 2016, Nelson et al., 2014, Nelson et al., 2005). Given the importance of social relationships to well-being and optimal functioning, the human brain must be designed to promote social learning and affiliation with others across development. However, adolescence is a particularly dynamic, context-dependent phase of development for social-affiliative behavior. While most individuals experience an increase in the intensity and frequency of emotions during adolescence, heightened emotionality is mostly and most strongly experienced in social settings. Affective behavior and social demands interact and, with experience and time, typically facilitate adaptive behavior. Nonetheless, although we focus on social affect and social context, we do recognize that several constructs including emotional intensity, emotion regulation, and context dependence may have broader application than just the social domain.

Second, we concentrate on functional magnetic resonance imaging (fMRI) because it is a widely used, powerful tool with which to link specific neural substrates with cognitive and behavioral responses to representations of emotional information. FMRI can reveal brain-based responses underlying emotion processing that may lack a behavioral corollary or may be undetectable through other methods of analysis (e.g., observation) or informants (e.g., parents). Furthermore, fMRI can help index inter-individual variance in the neural inputs that are recruited to achieve common behavioral outputs and delineate neural circuits that contribute to different affective phenotypes (e.g., irritability, euphoria). Although fMRI has low temporal resolution relative to electroencephalography, another commonly used assessment of the neural bases of emotion, it offers high spatial resolution for measuring neural processing within both the subcortical structures believed to be at the core of emotional responses, as well as the cortical structures implicated in behavioral integration. Finally, fMRI research has expanded recently to include tasks with high ecological validity designed to show cues or situations that represent more realistic aspects of adolescents’ experiences. This shift has been significant because it has revealed nuances about the neurobiology of affective behavior that relate to social context.

Lastly, both conceptual frameworks of adolescent neurodevelopment and empirical work conducted in adult, clinical, and animal samples (Blakemore and Mills, 2014, Bruhl et al., 2014, Casey et al., 2005, Ernst and Fudge, 2009, Jarcho et al., 2013, Nelson et al., 2005, Scherf et al., 2013, Smith et al., 2014, Somerville et al., 2010, Steinberg, 2005) have guided a large number of neuroimaging studies of adolescent affective behavior to focus on the role of a relatively small number of brain regions in mediating social-affective behavior. Specifically, much attention has been given to the amygdala, striatum, insula, and anterior cingulate cortex (ACC), and a number of regions within the prefrontal cortex (PFC). These regions work together to assign salience, promote learning, monitor conflict, compute relative valence of social stimuli, and integrate this information to generate and guide affective behaviors toward wider goals and within the contexts in which they occur. Although early fMRI studies emphasized localized patterns of regional activation, a recent trend is to delineate patterns of functional interconnection both among these regions, and between these regions and brain areas that sub-serve different functional processes (Ernst et al., 2015, Spear, 2013).

Section snippets

Heightened emotionality in adolescence: form and function

Behaviorally, adolescents show high levels of emotionality, with emotions that are more frequent, intense, and volatile, particularly compared with adults and in ways that differ from emotionality in early childhood (Arnett, 1999, Casey et al., 2010, Larson et al., 2002, Steinberg, 2008). For example, systematic sampling of adolescents’ and adults’ moods over the course of a week has shown that adolescents are more euphoric and more depressed in response to events (e.g., talking to friends,

Control and regulation of affective behavior: form and function

One of the primary tasks of adolescence is to refine one’s cognitive control over behavior and emotional reactions. Virtually all contemporary models of emotional changes during adolescence contain some aspect of a gradually emerging modulatory control neural system. A peak of emotionality in early adolescence is followed by a slowly emerging ability to exert greater self-directed control over behaviors and emotions. This is most evident in the dual systems and imbalance conceptual models of

The emotional adolescent brain in context

Affective behavior during adolescence does not occur in a vacuum. In fact, evidence suggests that the neural circuits that support affective responding are highly sensitive to contextual influences, especially during adolescence. Crone and Dahl (2012), for example, argue that the adolescent brain is highly attuned to social inputs, which facilitates flexible responding among a highly salient and changing social context. This is consistent with the Nelson et al. (2005) conceptualization of

Future directions and conclusions

In our review of the literature, we have highlighted recent work illustrative of the substantial progress that has been made in our understanding of the neurobiology of adolescent affective behavior, particularly with regard to the role of social context and social experiences. As the field moves forward, we suggest extending the existing knowledge-base on the emotional adolescent brain by applying new methodological advances, integrating multiple units of analysis sampled in multiple contexts,

Acknowledgments

Financial support for the writing of the article was provided by the National Institutes of Health awards R01MH098370 (A. E. G.), R01MH093605 (A. E. G.), R01MH103241 (J. S.), R01MH091327 (J. S.), and the National Institute of Mental Health, Intramural Research Program (E. E. N.). These sponsors played no role in the preparation or publication of this report.

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