Review ArticleA time of change: Behavioral and neural correlates of adolescent sensitivity to appetitive and aversive environmental cues
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.
References (110)
- et al.
Functional magnetic resonance imaging of facial affect recognition in children and adolescents
Journal of the American Academy of Child and Adolescent Psychiatry
(1999) - et al.
Emotion and motivation: The role of the amygdala, ventral striatum, and prefrontal cortex
Neuroscience and Biobehavioral Reviews
(2002) - et al.
Diffusion tensor imaging: Application to the study of the developing brain
Journal of the American Academy of Child and Adolescent Psychiatry
(2007) - et al.
Changes in cerebral functional organization during cognitive development
Current Opinion in Neurobiology
(2005) - et al.
The adolescent brain
Developmental Review
(2008) - et al.
Imaging the developing brain: What have we learned about cognitive development?
Trends in Cognitive Science
(2005) - et al.
Adolescent stress and coping: Implications for psychopathology during adolescence
Journal of Adolescence
(1993) - et al.
Sexual differentiation of the vertebrate brain: Principles and mechanisms
Frontiers in Neuroendocrinology
(1998) - et al.
Amygdala and nucleus accumbens in responses to receipt and omission of gains in adults and adolescents
Neuroimage
(2005) - et al.
Individual differences in trait anxiety predict the response of the basolateral amygdala to unconsciously processed fearful faces
Neuron
(2004)