How do neural changes in subcortical regions (e.g., accumbens and amygdala) associated with reward-seeking and emotion coincide with development of the prefrontal regions and do they relate to impulsivity and risk-taking behaviors? We have developed a neurobiological model of adolescent development within this framework that builds on rodent models (Laviola et al. 1999
; Spear 2000
) and recent imaging studies of children, adolescents, and adults (Ernst et al. 2005
; Galvan et al. 2007
; Galvan et al. 2006
; Hare & Casey, in press
). depicts this model illustrating how bottom-up limbic and prefrontal top-down control regions should be considered together. The graph shows different developmental trajectories for these systems, with limbic systems developing earlier than prefrontal control regions. According to this model, the individual is biased more by functionally mature limbic regions during adolescence (i.e., imbalance of limbic relative to prefrontal control), compared to children, for whom these systems are both still developing, and compared to adults, for whom these systems are fully mature. This perspective provides a basis for nonlinear shifts in behavior across development, due to earlier maturation of this limbic system relative to the less mature top-down prefrontal control region. Furthermore, with development and experience, the functional connectivity between these regions provides a mechanism for top-down control of these regions (Hare & Casey, in press
). Our model reconciles the contradiction between health statistics of risky behavior during adolescence and the astute observation by Reyna and Farley (2006)
that adolescents are able to reason and understand risks of behaviors in which they engage.
FIGURE 3 The traditional explanation of adolescent behavior has been that it is due to the protracted development of the prefrontal cortex. Our model takes into consideration the development of the prefrontal cortex together with subcortical limbic regions (e.g., (more ...)
According to our model, in emotionally salient situations, the more mature limbic system will win over the prefrontal control system. In other words, when a poor decision is made in an emotional context, the adolescent may know better, but the salience of the emotional context biases his or her behavior in opposite direction of the optimal action.
Our neurobiological model proposes that the combination of heightened responsiveness to rewards and immaturity in behavioral control areas may bias adolescents to seek immediate rather than long-term gains, perhaps explaining their increase in risky decision making and emotional reactivity. Tracking subcortical (e.g., accumbens and amygdala) and cortical (e.g., prefrontal) development of decision making and emotional reactivity across childhood and through adulthood provides additional clarification on whether changes reported in adolescence are specific to this period of development or, rather, reflect maturation that is steadily occurring in a somewhat linear pattern from childhood to adulthood.
Our findings were consistent with rodent models (Laviola et al. 2003
) and previous imaging studies during adolescence (Ernst et al. 2005
), which show enhanced accumbens activity to rewards. Adolescents, as compared to children and adults, showed an exaggerated accumbens response in anticipation of reward. However, both children and adolescents showed a less mature response in prefrontal control regions than adults. These findings suggest that there are different developmental trajectories for these regions. The enhancement in accumbens activity during adolescence may relate to the increase in impulsive and risky behaviors observed during this period of development (see ).
FIGURE 4 Magnitude and extent of accumbens and OFC activity to reward. Adolescents (13–17 years) showed greater percent signal change to large rewards than either children (aged 7–11 years) or adults (23–29 years) in the accumbens (A). (more ...)
In the second study, we examined the development of behavioral and neural responses in performance of an emotional go/no-go paradigm (Hare & Casey, in press
; Hare et al. 2005
). During the experiment, participants were presented with two emotional facial expressions (fearful, neutral, or happy) and were asked to respond to one of the emotions (e.g., fear) and suppress their response to the other emotion (e.g., neutral). In the context of negative emotional information (fearful faces), reaction times improved with age but were longer when detecting fearful faces relative to a neutral or happy face. This slowing in reaction time was correlated with greater amygdala activity (Hare & Casey, in press
). Activity in the orbital frontal cortex increased with age, and greater orbital frontal activity relative to amygdala was associated with more efficiency in suppressing emotional reactivity (longer reaction times and greater amygdala activity). These findings are in accordance with animal studies (Baxter et al. 2000
) which show connectivity between the amgydala and orbital frontal cortex are important for assessing changes in emotional value of an object and adapting behavior accordingly.
Differential recruitment of prefrontal and subcortical regions has been reported across a number of developmental fMRI studies (Casey et al. 2002
; Monk et al. 2003
; Thomas et al. 2004
). These findings were typically interpreted in terms of immature prefrontal regions rather than as an imbalance between prefrontal and subcortical regional development. Given evidence of prefrontal regions in guiding appropriate actions in different contexts (Miller & Cohen 2001
), immature prefrontal activity might hinder appropriate estimation of future outcomes, especially when making a decision within an emotional context (i.e., heat of the moment). This interpretation is consistent with previous research showing elevated subcortical, relative to cortical, activity when decisions are biased by immediate versus long-term gains (McClure et al. 2004
). Further, fMRI studies have shown limbic subcortical activity positively correlates with suboptimal choice behaviors (Kuhnen & Knutson 2005
In sum, during adolescence, relative to childhood or adulthood, an immature ventral prefrontal cortex may not provide sufficient top-down control of robustly activated reward and affect processing regions (e.g., accumbens and amygdala). This imbalance in development of these regions and relative top-down control results in less influence of prefrontal systems (orbitofrontal cortex) relative to the accumbens and amygdala in reward valuation and emotional reactivity.