Another important change in brain structure occurs within tracts of white matter, bundles of myelinated axons that transport neural signals between brain regions (Cascio, et al., 2007
). In contrast to gray matter, white matter pathways appear to increase in size, density, and organization throughout adolescence and well into adulthood (Schmithorst, Wilke, Dardzinski, & Holland, 2002
; Snook, Paulson, Roy, Phillips, & Beaulieu, 2005
). Of particular interest is the structural integrity of white matter tracts between subcortical brain regions and the prefrontal cortex, as these pathways may mediate cross-communication between subcortical emotion- and incentive-driven regions and prefrontal control regions (Hare & Casey, 2005
; O#x00027;Doherty, 2004
; Pessoa, 2008
; Phelps, 2006
A growing body of work is accumulating to suggest that the structural integrity of subcortical-cortical white matter pathways regardless of age is related to behavior and personality characteristics pertinent to reward and emotion processing. Kim and Whalen (2008)
have recently shown that the strength of connectivity between the amygdala and the ventromedial prefrontal cortex predicts fewer symptoms of anxiety in healthy adult subjects, consistent with previous reports identifying a similar amygdala-PFC pathway (Johansen-Berg et al., 2008
). Perhaps the link between structure and personality would explain individual differences in these behaviors during adolescence, where white matter maturity appears to be intermediate and variable across individuals.
Using a developmental sample, Liston and colleagues (2006)
reported that several white matter tracts showed continued maturation across adolescence, including tracts between the ventral prefrontal cortex and striatum. Of the tracts examined, only the maturity of a ventral frontostriatal pathway predicted better impulse control, measured by effort in performance on a go-no-go task (Liston, et al., 2006
). Taken together, these studies offer intriguing evidence that subcortical-cortical white matter pathways continue to undergo structural change throughout adolescence and that the efficiency of cognitive control is, in part, dependent on the maturity of frontostriatal connections. This may be consequential to the ability to control impulses in the face of potential rewards. Future studies relating properties of white matter tracts to personality traits and cognitive abilities within developmental samples may allow greater understanding of the role of top-down and bottom-up connections in emotional and incentive-driven behavior.
The studies discussed in the previous section suggest that adolescents may show a “hyper-reactivity” to salient environmental cues. A more comprehensive picture of adolescent emotional development takes into account the interaction between affective and control systems in the brain when required to suppress, ignore, or inhibit responses to emotional cues. Cognitive control can be defined as the ability to sustain goal-directed cognition in the face of extraneous information, and its development and neural substrates are discussed at length in another article in this volume (Luna et al, this issue). However, cognitive control is also relevant to emotional and incentive processing, because it is particularly difficult for youth to maintain cognitive control in the face of emotionally charged or incentive-laden distractors (Eigsti et al., 2006
). When healthy adult participants are asked to consciously suppress their affective responses to salient environmental cues, enhanced activity is often observed in ventrolateral and medial prefrontal cortices (Ochsner & Gross, 2005
; Urry et al., 2006
). Counterproductive recruitment of the ventromedial prefrontal cortex may serve as a neural predictor for psychiatric illnesses such as clinical depression (Johnstone et al., 2007), the incidence of which is elevated during adolescence. The interplay between emotional and cognitive systems is at the crux of our model, and we assert that adolescents display a functionally imbalanced pattern of neural activity that may be related to behavioral deficits in successfully inhibiting emotional responses.
More functional neuroimaging studies are needed to elucidate the interaction between emotional and controlled processing in adolescence, but initial studies have provided important insight into these interactions. A study by Monk and colleagues (2003)
compared neural activity of adolescent and adult participants while they viewed fearful and neutral facial expressions of emotion. While viewing the faces, participants engaged in passive viewing or were asked to shift focus away from the face stimuli and instead rate their own emotional state. The emotional state rating was thought to necessitate shift in focus away from the facial stimuli, calling for an enhancement in controlled processes in the presence of emotion cues. Adults recruited the ventrolateral prefrontal cortex, localized to the inferior frontal gyrus to a greater extent than adolescents during trials requiring this attentional shift, when fearful faces were presented. The authors interpreted this finding as reflecting adults’ ability to recruit lateral prefrontal regions to disengage from external emotional cues in order to focus on internal goals, while adolescents recruited this system less efficiently. The observation of a lateral prefrontal locus of activation is interesting and may reflect important differences between this paradigm and those presented in latter sections. For example, in this experiment, activity was not correlated with any behavioral index of disengagement, implying that adolescents may be making use of different psychological strategies to complete the task at hand relative to adults. It will be important for future work to include behaviorally matched samples as well as those with modified performance across ages (presumably indexing the psychological process at hand) to further enable the interpretation of cross-developmental effects (as in Schlaggar et al., 2002
Hare and colleagues (2008)
additionally tested for associations between subcortical limbic and frontal regions implicated in cognitive control. Functional connectivity analyses identified a region of the ventral prefrontal cortex whose recruitment predicted the downregulation of the amygdala and less slowing of reaction times over the course of the experiment. When examining this relationship across development, adolescents under-recruited the ventral prefrontal cortex relative to adults. In other words, this study drew a linkage between under-recruitment of the ventral prefrontal cortex, exaggeration of the amygdala and slowed performance – and this pattern was characteristic of adolescents. In sum, these findings suggest that a limbic-cortical functional network mediates the ability to exert control in the face of emotion, with adolescents showing relatively greater limbic and differential prefrontal recruitment. This functional imbalance results in less efficiency in performing a goal-directed action in the presence of emotional cues.
Paralleling these results in the domain of incentive processing, Galvan also reported differential recruitment of the orbitofrontal cortex (OFC) in a sample including children, adolescent, and adult participants. The OFC is a subregion of the prefrontal cortex that has been shown in adults to represent reward contingencies and exert inhibitory control over risky reward-related impulses (Daw, O#x00027;Doherty, Dayan, Seymour, & Dolan, 2006
; Galvan, et al., 2005
; see Rolls, 2000
for a review). Galvan and colleagues reported that in adolescents, the OFC increased in response to the receipt of monetary reward (Galvan et al., 2006
), similar to that observed in prior reports (May et al., 2004
). In addition, adolescents showed spatially diffuse patterns of OFC activity that were more similar to children than adults, in contrast to the extent of activity in the NAcc, that in adolescents was comparable to that of adults. The spatially diffuse activity in the OFC reported by Galvan and colleagues relative to the NAcc serves as a functional marker of brain immaturity (Durston, et al., 2006
), providing additional evidence to a functional immaturity of the prefrontal cortex during the adolescent years relative to the earlier and more focal pattern of NAcc activity observed during this age.
In conclusion, subcortical systems critical to reward processing, including the ventral striatum and amygdala, show hyperactive responses to emotion and reward eliciting cues relative to both children and adults. The exaggerated neural responses in these regions lend support to the model proposed earlier, whereby limbic and striatal signals are disproportionately large during the adolescent years. In contrast with the peaking of subcortical emotional and incentive-relevant brain responses, activity in the prefrontal cortex shows a very different trajectory of development. Our model theorizes that the prefrontal cortex undergoes a late-onset linear maturation with age, which is supported by structural and functional data just described. Work to date largely supports the notion that the prefrontal cortex continues to function at immature levels during the adolescent years, and exerts less regulatory control over subcortical regions relative to adults. The hyper-active upregulation of subcortical responses to salient environmental cues, paired with an immature regulatory system, may be responsible for changes in adolescent behavior, and can account for the nonlinear peak in incentive-seeking and emotional behavior often observed in adolescents.