Elsevier

Brain and Cognition

Volume 72, Issue 1, February 2010, Pages 124-133
Brain and Cognition

Review Article
A time of change: Behavioral and neural correlates of adolescent sensitivity to appetitive and aversive environmental cues

https://doi.org/10.1016/j.bandc.2009.07.003Get rights and content

Abstract

Adolescence is a developmental period that entails substantial changes in affective and incentive-seeking behavior relative to both childhood and adulthood, including a heightened propensity to engage in risky behaviors and experience persistent negative and labile mood states. This review discusses the emotional and incentive-driven behavioral changes in adolescents and their associated neural mechanisms, focusing on the dynamic interactions between the amygdala, ventral striatum, and prefrontal cortex. Common behavioral changes during adolescence may be associated with a heightened responsiveness to incentives and emotional cues while the capacity to effectively engage in cognitive and emotion regulation is still relatively immature. We highlight empirical work in humans and animals that addresses the interactions between these neural systems in adolescents relative to children and adults, and propose a neurobiological model that may account for the nonlinear changes in adolescent behavior. Finally, we discuss other influences that may contribute to exaggerated reward and emotion processing associated with adolescence, including hormonal fluctuations and the role of the social environment.

Introduction

The description of adolescence as “a developmental period rife with change” may be an understatement for those of us who think back to our own experiences during this time of life, or who observe teens today (Hall, 1904). Adolescence can be defined as the phase of gradual transition between childhood and adulthood, which is overlapping yet conceptually distinct from the physical changes marking puberty and physical maturation (Ernst et al., 2006, Spear, 2000). In recent years, researchers from a broad spectrum of scientific disciplines have shown significant interest in this period of the lifespan due to its intense physical, behavioral, social, and neurological changes, and the alarming health statistics associated with this time of life.

Beyond the intellectual interest in this period as a psychological snapshot in time, research examining adolescent behavior and its associated neural changes is particularly relevant to adolescent health. In adolescence, there is a heightened propensity to engage in risky behaviors that can lead to negative outcomes, including substance abuse, unprotected sex, inflicting harm on others, injuries, and death. According to the 2007 Youth Risk Behavior Survey (YRBS, Eaton et al., 2008) the four leading causes of death that account for 72% of adolescent mortality – motor vehicle accidents, unintentional injuries, homicide, and suicide – are preventable. Such statistics suggest that these fatalities may be attributed, in part, to poor choices or risky actions (e.g., accidents, injuries) and/or heightened emotionality (e.g., suicide) underscoring the importance of understanding the biological basis of emotional and incentive-seeking behavior of adolescents, the focus of the present review.

Section snippets

Storm and stress? Affective changes during adolescence

Adolescence has been considered, almost by definition, as a period of heightened stress (Spear, 2000) due to the array of transitions being experienced concomitantly, including physical maturation, drive for independence, increased salience of social and peer interaction, and brain development (Blakemore, 2008, Casey et al., 2008a, Casey et al., 2008b). Although new-found independence and social engagement can be stimulating and challenging in a positive way, it may also lead to feelings of

Adolescent incentive-driven behavior

In the previous section, we have asserted that adolescents frequently experience negative and volatile emotions. However, the period of adolescence is also marked by a nonlinear enhancement in risk-taking behavior, characterized by approaching pleasurable experiences without appropriate reverence to their associated potentially negative consequences. Several classes of epidemiological data support this conceptualization of adolescent behavior. In particular, adolescents engage in significantly

Synthesizing a model of adolescent behavior change

Based on the behavioral work just described, we have observed three main themes characterizing unique aspects of adolescent behavior, relative to behavior of children and adults. First, adolescents appear to show heightened sensitivity to salient environmental cues. Behaviorally, this idea is supported by epidemiological reports of adolescent risk-taking behavior, and empirical work showing exaggerated responses to both positive and negative environmental cues in adolescents relative to

Toward a neurobiological model of adolescent behavior

We have developed a biological model that characterizes brain changes underlying the patterns of adolescent behavior that takes into account the nonlinearity of emotional and incentive-seeking behaviors that are unique to this period (Casey et al., 2008a, Casey et al., 2008b). This empirically driven model posits an imbalance between the relative structural and functional maturity of brain systems critical to emotional and incentive-based behavior (e.g., subcortical regions including the

Assessing differential relative maturity of subcortical and prefrontal regions

Outside of the functional neuroimaging literature, there is evidence to suggest a differential relative maturity of subcortical brain structures as compared to prefrontal regions, which may be most pronounced during adolescence. Evidence for the continued pruning of prefrontal cortical synapses well into development has been established in both nonhuman primates and humans (Huttenlocher, 1997, Rakic et al., 1986), with greater regional differentiation found in the human brain (Huttenlocher, 1997

Brain mechanisms of enhanced sensitivity to salient environmental cues

Functional neuroimaging techniques allow for the noninvasive measurement of regional brain activity while subjects perform tasks aimed at isolating psychological processes of interest. In affective neuroscience, researchers have used neuroimaging techniques to identify a network of brain regions that appear to be particularly responsive to appetitive and aversive stimuli, including the amygdala, ventral striatum, midbrain nuclei, and medial and lateral prefrontal cortices (Adolphs, 2002, Kober

Brain mechanisms of reduced top–down control over responses to salient cues in adolescents

Another important change in brain structure occurs within tracts of white matter, bundles of myelinated axons that transport neural signals between brain regions (Cascio, Gerig, & Piven, 2007). In contrast to gray matter, white matter pathways appear to increase in size, density, and organization throughout adolescence and well into adulthood (Schmithorst et al., 2002, Snook et al., 2005). Of particular interest is the structural integrity of white matter tracts between subcortical brain

Individual differences bias the responsivity of a subcortical–cortical network

The experiments just described suggest that adolescents tend to show enhanced subcortical responsivity to environmentally salient cues, as well as diminished prefrontal responses in contexts requiring cognitive control. However, simple observation of the raw data points representing the amygdala response in Fig. 2A, and nucleus accumbens response depicted in Fig. 2B, clearly shows there is substantial individual variability in these responses. In our conceptualization, adolescence in and of

The role of gonadal hormones on affective and incentive processing in the adolescent brain

One potential source of influence in ‘imbalanced’ subcortical–cortical responding is individual differences in pubertal hormone levels. During adolescence there is a significant increase in circulating gonadal hormones, which ultimately leads to the process of sexual maturation (Spear, 2000). Gonadal hormone effects on the brain have been conceptualized into either “organizational” mechanisms whereby sex hormones cause permanent changes to neural systems which in turn influence behavior, or

The influence of peers on affective and incentive processing in the adolescent brain

Relations with peers takes on a heightened importance in adolescence (Steinberg, 2005), rendering it a potential source for mediating changes in affective and incentive behavior. On one hand, adolescents as a group may show enhanced sensitivity to social cues, particularly those generated by peers, as compared to adults and children. Additionally, individual differences in sensitivity to peers may be particularly relevant in biasing adolescent behavior.

Recent studies have attempted to

Caveats and limitations

The research just described, primarily conducted in just the past five years, has made remarkable strides in characterizing the nature of emotion and reward responding in the adolescent brain. However, it should be pointed out that the number of experiments on this topic is still relatively few and caution should be taken in drawing unequivocal conclusions from them. More studies with larger samples sizes are called for to fully elucidate the nature of amygdala–striatal–prefrontal interactions

Conclusions

Relative to adults and children, adolescents engage in disproportionately risky behaviors, which can lead to a wide variety of negative outcomes including substance abuse, unprotected sex, injuries, and suicide. Many of these behaviors are at least in part mediated by incentive and emotional responding, be it inappropriate appetitive behavior leading to risky approach of potential rewards, or the outcome of experiencing extreme negative affect such as self-harm and suicide. Emotional and

Acknowledgments

This work was supported by NIH grants DA007274, 50-MH079513, R01 DA018879, R01 MH73175, the Mortimer D. Sackler family, and the Dewitt-Wallace Fund.

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