Review ArticleWhat has fMRI told us about the Development of Cognitive Control through Adolescence?
Introduction
Adolescence is a period when many aspects of decision-making appear adult-like, yet adolescents’ decisions are inconsistent, and this often leads to suboptimal or even dangerous behavior. The ability to voluntarily guide behavior in a goal-directed fashion is essential to mature decision making. Cognitive control and executive function are terms used to describe the processes that allow us to voluntarily guide our behavior. While adolescents can exhibit sophisticated voluntary behavior, the ability to do so consistently continues to improve during adolescence, making cognitive control a particularly useful model for investigating the vulnerabilities of this period. Characterizing the brain circuitry underlying immaturities in cognitive control can elucidate the important aspects of the neural basis of decision making in adolescence. This paper reviews how typical adolescents differ from adults on two fundamental aspects of cognitive control – response inhibition and working memory (Fuster, 1997b). Response inhibition refers to the ability to voluntarily select a task-appropriate, goal-directed response while suppressing a more compelling but task-inappropriate response. Working memory refers to the mental ‘sketch pad’ that allows us to retain relevant information on-line in order to make a planned, goal-directed response. While these processes work together to support goal driven behavior (Miller & Cohen, 2001), they can be considered independently to characterize specific profiles of cognitive development (Demetriou et al., 2002, Luna et al., 2004).
Major psychopathology can often emerge or intensify during adolescence, indicating that there are vulnerabilities inherent to this developmental transition that may contribute to mental disorders. Additionally, cognitive control is usually compromised in major psychopathology (Luna and Sweeney, 2004a, Sweeney et al., 2004). This suggests that investigating neurocognitive development can serve as a way to probe the integrity of complex brain circuitries associated with psychopathology. For example, if the maturation of long-range connectivity in the brain proves to be important for the late developmental improvements in cognitive control, these processes may be compromised in psychopathology. Additionally, normative adolescence is also characterized by a peak in sensation-seeking that can lead to risk-taking behavior that undermines survival (Chambers et al., 2003, Spear, 2000). Delineating the normative processes that underlie the improvement in cognitive control from adolescence to adulthood provides a template for understanding the neurobehavioral basis of both psychopathology and risk-taking behavior.
Given that behavior is the result of both environmental and biological influences, the ability to assess their association is optimal for characterizing developmental change. Neuroimaging methods provide one approach to investigate concurrent changes in brain and behavior. Functional Magnetic Resonance Imaging (fMRI) is particularly appropriate for developmental studies because it is non-invasive and allows the assessment of brain function relevant for a specific behavior. However, the interpretation of developmental neuroimaging results differs from that of adult neuroimaging studies, because results from younger individuals must be considered in the context of brain function in adulthood. That is, we identify immaturities in brain function in young individuals by comparing them to results in mature adult populations. In this paper, we review the literature characterizing age-related changes in brain function underlying cognitive control of behavior through adolescence. We consider studies that have focused on voluntary response inhibition and those that measure changes in response to working memory demands. We end by discussing methodological issues that are specific to interpreting developmental fMRI results.
Section snippets
The development of cognitive control
Voluntary planned behavior requires the ability to retain online the goal of the response (working memory), to plan and prepare the response, and the ability to suppress task irrelevant responses in order to make a task-appropriate response (response inhibition). In this section, we review how basic components of cognitive control (response inhibition and working memory) change during childhood and adolescence, focusing on neuroimaging studies examining changes in brain function.
Response inhibition
Response inhibition is central to the voluntary control of behavior, providing the flexibility needed for behavior to be guided by a task goal (Davidson et al., 2006, Fuster, 1997b, Miller and Cohen, 2001). As in real life, what is being inhibited varies across experimental tasks – it may be extremely prepotent, such as reflexive responses to external stimuli (e.g., antisaccade task), or a learned automatic response (e.g., go-no-go task). The most frequently used tasks include the go-no-go,
Working memory
Voluntary responses require the ability to maintain a representation of the rules that will guide behavior in working memory (Baddeley, 1986). Much like response inhibition, working memory is a central component of executive function (Fuster, 1997b, Miller and Cohen, 2001) and has a protracted developmental trajectory through adolescence (Demetriou et al., 2002, Luna et al., 2004). Studies have shown that at both the behavioral and neural levels, fundamental working memory skills and their
Development of integrated systems level circuitry
Studies delineating age-related changes in both response inhibition and working memory find that there are enhancements in the recruitment of widespread regions outside of PFC, including parietal, temporal, subcortical and cerebellar regions, with age (Bunge et al., 2002, Crone et al., 2006, Luna et al., 2001, O’Hare et al., 2008, Rubia et al., 2006). Indeed, PFC may be engaged only when other circuitries cannot support processing (Hazy, Frank, & O’Reilly, 2007). PFC allows the active
Considerations in interpreting developmental neuroimaging results
While great strides have been made in understanding age-related changes in brain processes underlying cognitive development, there are still important challenges that we need to address regarding methods and the interpretation of data. A crucial feature of developmental neuroimaging studies is that adults are considered the model system. Therefore, any deviation from adult brain activity is interpreted as an immaturity. This particular aspect of interpreting developmental results can be viewed
Direction of developmental differences
When age groups differ in activation, qualitatively different processes may be involved, each with distinct interpretations. One common result is that the younger group demonstrates an increased magnitude of activity compared to adults in an equivalent region. When the same circuitry as adults is being accessed by younger subjects, but the younger subjects show higher activity, this is often interpreted as indicating that greater effort is required for younger subjects to do the task (Luna et
Conclusions
The developmental fMRI literature characterizing age-related differences in cognitive control includes a range of methodological approaches. This work has generated diverse findings that still share some important consistencies. As has been proposed in the literature, prefrontal systems play a primary role in executive processes and have a protracted development (much like other association areas) into adolescence. Studies therefore have used PFC as an a priori region of interest and have shown
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