Summary: Best, J.R., Miller, P.H., & Jones, L.L. (2009). Executive functions after age 5: Changes and correlates, Developmental Review, 29(3), 180-200.

Abstract

Research on executive functioning (EF) has been predominantly focused on preschool children. This paper outlines why it is important to examine EF throughout childhood and across the lifespan:

  1. examining EF in older children can address the question of whether EF is a unitary construct. 
  2. much of the development of EF, especially working memory, shifting, and planning, occurs after age 5.
  3. important applications of EF research concern the role of school-age children’s EF in various aspects of school performance, as well as social functioning and emotional control. 

Intro

The prefrontal cortex (PFC) is critical to the planning, organization, and regulation of cognition and behavior. Executive function (EF) serves as an umbrella term to encompass the goal-oriented control functions of the PFC. Relatively complex neuropsychological instruments such as the Wisconsin Card Sorting Test (WCST) were first employed to evaluate frontal lobe functioning and later to assess EF. Research with a focus on preschoolers is great, because such work identifies the very beginnings of each component of EF. Also, as it is needed to work with simplified tasks, suitable for young children, it is possible to assess a single EF component, thus avoiding the problem of task impurity. Finally the focus on preschoolers has revealed important relations between EF and theory of mind. However, assessing EF in school-age children allows us to ask questions that cannot be answered in research with preschoolers. Research on further changes in the development of each EF component and in the relations among the components during later childhood and adolescence would not only clarify EF as a construct but also provide insight into processes underlying the development of EF. Furthermore, significant improvements in EF tasks occur during the school years. It is, therefore, important to examine EF in school-age children in order to get a developmental picture of EF. As with studying the developmental trajectories of EF components in childhood and adolescence, the course of typical EF decline should clarify the interaction of EF components to produce goal-oriented behavior and the nature of brain processes supporting EF.

Like brain development in general, PFC development involves both progressive (e.g., neuron proliferation, synaptogenesis, myelination) and regressive (e.g., cell death, synaptic pruning) changes. The general finding that EF (behavioural development) develops throughout adolescence is affirmed by the protracted development of the PFC (neural development).

EF as a construct

In order to explore EF as a construct, it is necessary to involve older children and adolescents as well as preschoolers in research. Two questions arise:

  1. Is EF best thought of as a unitary process or as a set of multiple, distinct component processes?
  2. If EF does refer to distinct component processes, how are these processes related and how does this relationship change as the child develops?

Concerning the first question: Most studies support the view that EF consists of related but separable components (which is also called the unity-but-diversity view) and purport that a common mechanism (or mechanisms) underlies all EF processes. Other evidence supports the unity-but diversity view through, first, showing that the different developmental trajectories over childhood and adolescence undermine the notion of a completely unified EF. Second, through neuroimaging research that indicates that multiple EF tasks that span different EF domains recruit slightly different regions of the PFC. Third, through research at multiple time points and finally, through the fact that a particular deficit, such as poor academic performance in a specific area (see below) is associated with a greater impairment for some EF components than others, which suggests some independence. A remaining methodological challenge is to create EF tasks that isolate and assess one or the other EF component.

Concerning the second question: Structural equation modeling (SEM) is used as a method that allows the researcher to examine what (and how) EF domains are recruited during complex problem solving. Research shows, that the relations among EF components change with age. Knowledge of what EF skills are recruited during successful completion of complex problem solving is important not only for theoretical reasons, but also for practical ones, such as developing interventions for school children with poor EF. This knowledge can only be gained through including older children and adolescents, as well as preschoolers in research.

The developmental trajectories of EFs

Inhibition

Inhibition commonly refers to the ability to suppress a dominant, automatic or prepotent response, but inhibition also entails interference control, directed forgetting, emotional control, and motor control. Research documents rapid improvements in early childhood on tasks such as the Day/Night task, Luria’s fist and finger game, and the A-not-B task. In the preschool years children significantly reduce their inhibition errors. Although improved inhibition during the preschool years is striking, significant improvements also occur later, particularly between ages 5 and 8. Unlike the fundamental changes during preschool, changes during adolescence mainly consist of refinements in speed and accuracy. Behavioral improvements in inhibition appear to be paralleled by refinements in the underlying brain activity in the PFC and in networks that include the PFC. Neuroimaging (fMRI), EEG and Diffusion Tensor Imaging (DTI) suggest that in addition to the focalization and migration of activity, perhaps increasing connectivity of frontal brain regions serves to enhance inhibition in later childhood.

Working Memory (WM)

Generally speaking, WM involves the ability to maintain and manipulate information over brief periods of time. Research shows a linear increase in performance from age 4 to 15 for a battery of WM tasks of varying complexity. The age-related changes in performance depended on the complexity of the particular task. Thus, it is important to consider the complexity of the task when extrapolating a general trajectory of WM development. Research shows that WM development apparently continues through adolescence, and easier WM tasks are mastered before more complex ones. Neuroimaging studies also point to continued changes in brain activity associated with WM through childhood and adolescence. Results of the studies suggest further refinement of WM through adolescence as the prefrontal regions become more specialized for WM. Paralleling the behavioral findings on inhibition, these results suggest that the large improvements in WM in early childhood, along with qualitative changes in brain recruitment, are followed by more subtle refinements consisting of quantitative changes in activation and focalization of brain regions related to WM.

Shifting

Shifting regards the ability to shift between mental states, operations, or tasks. The WCST is the classic shifting task, whereby the participant is asked to sort cards based on a specific dimension (e.g., shape). Then,  the sorting rule changes and the participant must determine the new sorting rule (e.g., color) and sort accordingly. Successful task switching involves inhibition of previously activated mental sets. The ability to shift between more complex task sets, each with more numerous and complex rules improves with age, typically until early adolescence. Shifting ability may be measured in terms of shift cost, which is the difference either in response time or accuracy between shift trials and non-shift trials. Results show an increasing awareness of the relationship between speed and accuracy in childhood. This suggests the emerging presence of metacognition and its contributions to developmental differences in task performance. Mature task shifting is related to inferior frontal and parietal regions as well as superior temporal regions in adults. 

Planning

Planning is a critical part of goal-oriented behavior; it embodies the ability to formulate actions in advance and to approach a task in an organized, strategic and efficient manner. Tasks that evaluate planning ability require the child to prepare multiple steps of action in advance, to evaluate those actions, and to change course if necessary. The most frequently used tasks are the Tower of Hanoi (TOH) and the Tower of London (TOL). The particular age at which mastery is reached depends on the difficulty of the TOL or TOH task condition. The ability to effectively plan up to three moves is present by middle childhood, but the ability to effectively create more complex plans of 4 or 5 moves seems to develop at some point in late childhood or adolescence. Thus, planning ability seems to follow a protracted developmental course such that performance improves at least into late childhood and often adolescence. Little is known about the brain changes related to the development of planning skills.

Aging and executive function

EF seems to be particularly vulnerable to age-related cognitive declines. In contrast, non-executive abilities such as procedural memory, vocabulary, and numeric abilities are relatively spared by the aging process. In accord with the specific vulnerability of EF, normal aging is not characterized by widespread neural changes but instead by selective cell loss, dendritic deterioration, and chemical dysregulation in the PFC and hippocampus. Research suggest that with age dopamine (DA) projections to the dorsolateral preforantal cortex (DL-PFC) are disrupted, causing impairments to the gating mechanism. Such disruptions equally impair WM and inhibition, which supports the finding that performance on a variety of executive tasks deteriorates with age. Multiple executive processes begin to show impairment by the 7th decade of life. Functional neuroimaging studies point to the complexity of the neural correlates of EF. 

Conclusions

Inhibition shows prominent improvement during the preschool years and less change later on. WM and shifting, on the other hand, appear to emerge in the preschool years but really improve the most afterwards in a more linear fashion. Planning ability, which typically is measured by more complex tasks, seems to make the largest gains in later childhood or adolescence. EF is particularly vulnerable to the aging process as multiple executive processes (e.g., resistance to interference, WM) begin to show impairment by the 7th decade of life.

Uses of executive function in daily life

After age 5, children enter more social settings and go to school.

Social functioning and emotional control

The same general brain structures appear to underlie both cognitive and emotional processing. EF appears to be related to social and emotional self regulation. The link between one aspect of self-regulation, effortful control (which includes attention control, inhibitory control and low-intensity pleasure and is assessed by the Children’s Behavior Questionnaire), and EF is likely due to the development of the anterior attention network. Attention training may improve children’s cognitive and emotional regulation. The link between EF and social functioning continues during aging. 

School performance

EF might affect school performance (e.g. through not being able to remember instructions, performing mental calculations, poor writing, unmoral behaviours or language impairment, which is associated with WM). In turn, by providing situations that encourage EF practice, EF development may be facilitated, too. By expanding EF research to school-age children, the relations to an important aspect of childhood—schooling—can be examined. Different academic activities (e.g., mathematics, reading, and writing) appear to involve different combinations of EF components. Attempts to uncover causality between EF and school functioning have been inconclusive. Likewise, more research is needed to reveal the contextual factors (e.g., type of classroom environment) that enhance EF. Once these relations are clarified, interventions can be developed to bolster the specific EF domains underlying each academic skill.

Conclusions and directions for future research

EF as a construct

We know that the specific relations among the various EF components change across development, which suggests that the components are somewhat separate, even though related. Future research could employ a training study design in order to address whether EF consists of largely independent components or a single, unified ability.

Developmental trajectories of each EF component

The review of subsequent developments shows continued improvement of all components, probably even into adolescence, as well as somewhat different developmental trajectories for each component. Particular sorts of studies with school-age children and elderly adults would be especially useful for examining key questions
about development. These may for example clarify why children of different ages differ in the particular components of EF they find difficult to recruit.

Uses of EF in daily life

Research has shown a possible link of EF to social problems. Although peer relationships are known to become increasingly important during middle childhood and adolescence, we know little about the connections between EF and peer interaction. The work on older children expands the domains for which EF might be important, in particular, formal schooling. The EF components appear to be related differentially to various academic subjects. In both children and adults, inhibition and updating of WM, but not shifting, are related to monitoring performance in a time-based prospective memory task. More research and theorizing on EF in children older than 5 would provide a more complete picture of the development of EF. Such work would shift the research focus from the early emergence of EF to its refinement and application to daily life.

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