Executive Function and the Frontal Lobes: A Meta-Analytic Review

Currently, there is debate among scholars regarding how to operationalize and measure executive functions. These functions generally are referred to as “supervisory” cognitive processes because they involve higher level organization and execution of complex thoughts and behavior. Although conceptualizations vary regarding what mental processes actually constitute the “executive function” construct, there has been a historical linkage of these “higher-level” processes with the frontal lobes. In fact, many investigators have used the term “frontal functions” synonymously with “executive functions” despite evidence that contradicts this synonymous usage. The current review provides a critical analysis of lesion and neuroimaging studies using three popular executive function measures (Wisconsin Card Sorting Test, Phonemic Verbal Fluency, and Stroop Color Word Interference Test) in order to examine the validity of the executive function construct in terms of its relation to activation and damage to the frontal lobes. Empirical lesion data are examined via meta-analysis procedures along with formula derivatives. Results reveal mixed evidence that does not support a one-to-one relationship between executive functions and frontal lobe activity. The paper concludes with a discussion of the implications of construing the validity of these neuropsychological tests in anatomical, rather than cognitive and behavioral, terms.     

Biological and psychological development of executive functions.

The purpose of this overview is to provide a background for understanding the relation between the biological maturation of the frontal lobes and the development of the psychological concept of executive functions. In the first section, an interactive hierarchical feedback model is presented as a heuristic way of conceptualizing the relationship of the frontal lobes and executive functions to other brain regions and abilities. The following two sections present a synopsis of research on biological maturation and the psychological development of executive functions.     

Patterns of cognitive ageing

Neuroanatomical evidence suggests that normal ageing affects some brain areas, and the “local” functions they support, earlier and more severely than others. Changes appear to be especially marked in the hippocampus, temporal association and prefrontal cortex. Evidence from classical neuropsychological studies suggests that these brain areas are associated with memory and “executive” functions, respectively. We may, therefore, expect that tests purported to measure these functions may be disproportionately affected in old age and that there may be evidence for some separation of these functions even within neurologically normal populations. What we also know, however, is that measures reflecting general fluid ability also decline with increasing age, so any hypothesis relating to specific “local” deficits must acknowledge and account for any “globar” changes in performance. Volunteers (n=162) aged between 60–80 years who had completed the Cattell and Cattell Culture Fair Intelligence Test (CCF) completed the Cambridge Automated Neuropsychological Test Battery (CANTAB). The CANTAB has been administered to several patient populations and tests from the battery have been shown to be sensitive to damage in both temporal and prefrontal areas (Owen et al., 1996). Results from the test battery showed that both the Paired Associate Learning and Spatial Recognition tests were the most sensitive to normal ageing even when CCF is accounted for. In contrast, this performance on the “executive” tests, shown to be sensitive to frontal lobe damage, was not related to age, and CCF scores predicted performance on these tests. These results are discussed in relation to theories of cognitive ageing and patterns of change and in relation to several important methodological and theoretical considerations for the study of executive function. Received: 31 March 1999 / Accepted: 23 July 1999     

The neural basis of updating: Distinguishing substitution processes from other concurrent processes

Sörqvist, P. & Sætrevik, B. (2010). The neural basis of updating: Distinguishing substitution processes from other concurrent processes. Scandinavian Journal of Psychology, 51, 357–362. Most previous studies of updating processes have not been able to contrast processes of substituting items in memory with other concurrent processes. In the present investigation, we used a new task called “number updating” and an fMRI protocol to contrast the activation of trials that require item substitution (adding a new item to the working memory representation and suppressing an old item) with trials that involve no substitution (discarding the new item). Trials that require item substitution activated the dorsolateral prefrontal cortex, the posterior medial frontal cortex and the parietal lobes, areas typically seen activated for working memory tasks in general. Trials that do not require substitution activated the anterior medial frontal cortex. Studies examining executive functions have associated this area with cognitive conflict, and may represent suppression of the substitution processes.     

Strategy application disorder: the role of the frontal lobes in human multitasking

Strategy application disorder is a term used to describe a pattern of deficits, usually associated with frontal lobe dysfunction, where people show disorganisation, absentmindedness and problems with planning and decision making in everyday life despite normal performance on traditional neuropsychological tests. It is argued that the prototypical situation which presents problems for these cases are those which require multitasking, and although good cases are rare in the literature, those that do exist show a characteristic neuropsychological pattern. Moreover, this pattern is confirmed in recent group studies of multitasking and of the relationship between multitasking tests (such as the Six Element Test), failures in everyday life and other neuropsychological measures. At present the evidence suggests that the potential frontal brain regions most implicated in multitasking are the anterior cingulate; B.A. 10 and immediately adjacent areas; and the right dorsolateral prefrontal cortex, with each making a unique contribution to different aspects of performance. Furthermore, recent studies show striking dissociations between performances on multitasking tests and two of the most commonly administered measures of executive function: the verbal fluency test and the Wisconsin Card Sorting Test, which sets a minimum level for a fractionation of the executive syndrome in humans. Received: 31 March 1999 / Accepted: 23 July 1999     

Les capacités d'inhibition : une fonction « frontale » ?

It has been strongly suggested that one important function related to frontal lobes is inhibition. However, a review of the literature on classical tests of inhibition (Stroop test, WCST, and AB-AC learning) suggests that this hypothesis is not well established. We further examined this hypothesis using short-term and long-term directed forgetting tasks (Reed, 1970, Zacks et al., 1996), the Stroop test and the Hayling test (Burgess and Shallice, 1996) in 13 patients with focal frontal lesions. The results revealed short-term and long-term memory deficits and a slowing down, but no inhibition deficit compared with control subjects. These results question the relevance of the hypothesis of the frontal lobe as the unique substrate of inhibitory mechanisms. More generally, they address the issue of executive functions: are these sustained by the frontal cortex or by a cortical and subcortical diffuse neural network?     

Rehabilitation of executive deficits in closed head injury and anterior communicating artery aneurysm patients

This paper reports a study that was aimed to rehabilitate executive functions in closed head injury (CHI) and anterior communicating artery (ACoA) aneurysm patients. The groups tested comprised 10 CHI patients, 9 ACoA aneurysm patients and 19 controls. We employed a dual-task paradigm that is known to tap the ability to co-ordinate two actions. The treatment consisted of five experimental sessions, in which the dual-task paradigm was used. In the CHI study, the dual-task cost was measured before the treatment (assessment), immediately after the treatment (retest), and 3 months after the treatment (follow-up). In the ACoA aneurysm study, the dual-task cost was also assessed 12 months after the treatment. A significant reduction of the dual-task cost from assessment to retest was found. This reduction remained stable in the follow-up sessions. The results are discussed with reference to the absence of spontaneous recovery of this specific executive function and to the possibility that the beneficial effect of the treatment generalises to other executive functions and/or daily living activities. Received: 31 March 1999 / Accepted: 23 July 1999     

Frontal-Striatal Circuits in Cognitive Aging: Evidence for Caudate Involvement

Changes in cognition with aging have been claimed to be due in large part to a decline in frontal lobe function. However, at our present state of knowledge, the emphasis on the frontal lobes to the exclusion of the rest of the frontal-striatal circuits of which they are a part is unwarranted. To argue this point, I consider another anatomical candidate within these circuits, the caudate. Evidence is presented that the caudate decreases in size with age as much as the frontal lobes and that damage to either the frontal lobes or the caudate is accompanied by declines in inhibitory processes, executive control, and cognitive speed similar to those seen in normal aging. Separating the unique contributions of the frontal lobes and the caudate to these circuits is difficult but should be the focus of future studies of the biological basis of cognitive aging.     

Effects of Hormone Replacement Therapy and Aging on Cognition: Evidence for Executive Dysfunction

ABSTRACT

The present study was designed to explore whether the frontal lobe hypothesis of cognitive aging may be extended to describe the cognitive effects associated with estrogen use in postmenopausal women. Postmenopausal estrogen-only users, estrogen + progesterone users, and non-users (60–80 years old), as well as young, regularly cycling women (18–30 years old) completed an item and source memory task. Since source memory is thought to rely more on executive processes than item memory, we hypothesized that aging and estrogen effects would be greater for source memory than for item memory. Neuropsychological tests explored whether the effects of aging and estrogen use were revealed on other tests of frontal lobe function. Results from the experimental task revealed greater aging and estrogen effects for source memory than for item memory, and neuropsychological results revealed aging and estrogen effects on a subset of tests of executive function. Women on estrogen + progesterone therapy did not outperform non-users, suggesting that the addition of progesterone to hormone therapy may mitigate the benefits induced by estrogen use alone. Overall, findings support the hypothesis that estrogen use may temper age-related cognitive decline by helping to maintain functions subserved by the frontal lobes.     

Neuroimaging studies of working memory:

We performed meta-analyses on 60 neuroimaging (PET and fMRI) studies of working memory (WM), considering three types of storage material (spatial, verbal, and object), three types of executive function (continuous updating of WM, memory for temporal order, and manipulation of information in WM), and interactions between material and executive function. Analyses of material type showed the expected dorsal-ventral dissociation between spatial and nonspatial storage in the posterior cortex, but not in the frontal cortex. Some support was found for left frontal dominance in verbal WM, but only for tasks with low executive demand. Executive demand increased right lateralization in the frontal cortex for spatial WM. Tasks requiring executive processing generally produce more dorsal frontal activations than do storage-only tasks, but not all executive processes show this pattern. Brodmann’s areas (BAs) 6, 8, and 9, in the superior frontal cortex, respond most when WM must be continuously updated and when memory for temporal order must be maintained. Right BAs 10 and 47, in the ventral frontal cortex, respond more frequently with demand for manipulation (including dual-task requirements or mental operations). BA 7, in the posterior parietal cortex, is involved in all types of executive function. Finally, we consider a potential fourth executive function: selective attention to features of a stimulus to be stored in WM, which leads to increased probability of activating the medial prefrontal cortex (BA 32) in storage tasks.     

Contributions of Studies on Alcohol Use Disorders to Understanding Cerebellar Function

Neuropathological, neuropsychological, and neuroimaging studies of human alcoholism provide evidence for degradation of frontal, pontine, thalamic, and cerebellar brain sites and disturbed associated functions. Current studies using neuroimaging combined with examination of executive functions, traditionally considered the sole purview of the frontal lobes, have identified a role for the cerebellum serving as a compensatory processing adjunct to enable normal performance on challenging tasks tapping executive functions. This overview proposes that disruption of an executive frontocerebellar network is a major contributor to characteristic behaviors of alcoholism that, on the one hand, enable alcohol use disorders, and on the other hand, lead to compensation for dysfunctions in alcoholism traditionally considered frontally-based.     

A developmental perspective on decision making in young soccer players: The role of executive functions

Lately, interest in both domain-specific and domain-general cognitive processes has increased as a means to explain soccer player expertise. While the two types of processes have mostly been studied separately, we sought to connect these lines of research by investigating the role of executive functions in soccer players’ decision making from a developmental perspective. As these cognitive processes as well as their relation might differ between age groups, we took a developmental perspective to better understand this link in a sample of N = 128 soccer players (M_age = 10.69 years, SD = 1.44). Two age groups (younger vs. older players) performed a video-based option-generation and decision-making task that used temporal occlusion. Additionally, executive functions were assessed with standardized computer-based tests. Results show a link between executive functions and sport-specific decision making, most prominent for working memory. Further, older players generated better options and showed better inhibition and cognitive flexibility than younger players. We suggest there is a crucial turning point in cognitive development around the age of 11 years.     

Mapping numerical processing, reading, and executive functions in the developing brain: an fMRI meta-analysis of 52 studies including 842 children

Tracing the connections from brain functions to children's cognitive development and education is a major goal of modern neuroscience. We performed the first meta-analysis of functional magnetic resonance imaging (fMRI) data obtained over the past decade (1999-2008) on more than 800 children and adolescents in three core systems of cognitive development and school learning: numerical abilities, reading, and executive functions (i.e. cognitive control). We ran Activation Likelihood Estimation (ALE) meta-analyses to obtain regions of reliable activity across all the studies. The results indicate that, unlike results usually reported for adults, children primarily engage the frontal cortex when solving numerical tasks. With age, there may be a shift from reliance on the frontal cortex to reliance on the parietal cortex. In contrast, the frontal, temporo-parietal and occipito-temporal regions at work during reading in children are very similar to those reported in adults. The executive frontal regions are also consistent with the imaging literature on cognitive control in adults, but the developmental comparison between children and adolescents demonstrates a key role of the anterior insular cortex (AIC) with an additional right AIC involvement in adolescents.     

Aging, Executive Functioning, and Social Control

ABSTRACT— Aging is associated with atrophy of the frontal lobes of the brain, which are the seat of executive functions. Because successful social functioning often requires executive control, aging can lead to unintended social changes via deficits in executive control. In this article I review evidence that, due to losses in executive control, aging leads to increased prejudice and social inappropriateness and, under certain circumstances, increased depression and problem gambling. I then discuss theory and research suggesting possible interventions that might ameliorate unwanted social changes brought about by executive decline.     

The involvement of executive functions in prospective memory performance of adults

The present study examines the relationship between prospective memory performance and executive functioning. The four phases of the prospective memory process—intention formation, intention retention, reinstantiation of the intention, and intention execution—are assumed to require different amounts of executive processing, most of which is demanded in the phases of intention formation and intention execution. At present, though, it is still unclear whether, and to what extent, prefrontal executive systems are involved in different kinds of prospective memory tasks, as some findings suggest that prospective memory might rather rely on nonstrategic processes that are unlikely to depend on prefrontal executive systems. Therefore, this study focuses on the following questions: (1) to what degree does executive functioning predict prospective memory performance in different standard prospective memory tasks and, furthermore, are certain executive measures better predictors than others; (2) are age‐related effects in different prospective memory measures due to individual differences in executive functioning; and (3) do age‐related differences in prospective memory exist that are not explained by individual differences in executive functioning. In a sample of 80 adults (20‐80 years), we applied four instruments to measure prospective memory: a traditional single‐task paradigm, two more complex tasks—one time‐based and one event‐based—and a highly complex multi‐task paradigm. We further assessed a broadly defined construct of executive functioning using several standard neuropsychological tests. Results showed that executive functioning did not predict performance in the simple single‐task paradigm. However, executive functioning, but not age, predicted performance in the two more complex standard tests of prospective remembering, and both executive functioning and age predicted performance in the most complex paradigm. In sum, the obtained data underline the assumption that frontal/ executive functions are related to prospective memory performance across a range of prospective paradigms. It also seems clear that age differences in prospective memory performance partially depend on age‐related individual differences in frontal/executive functions.     

Effects of hormone replacement therapy and aging on cognition: evidence for executive dysfunction

The present study was designed to explore whether the frontal lobe hypothesis of cognitive aging may be extended to describe the cognitive effects associated with estrogen use in postmenopausal women. Postmenopausal estrogen-only users, estrogen + progesterone users, and non-users (60-80 years old), as well as young, regularly cycling women (18-30 years old) completed an item and source memory task. Since source memory is thought to rely more on executive processes than item memory, we hypothesized that aging and estrogen effects would be greater for source memory than for item memory. Neuropsychological tests explored whether the effects of aging and estrogen use were revealed on other tests of frontal lobe function. Results from the experimental task revealed greater aging and estrogen effects for source memory than for item memory, and neuropsychological results revealed aging and estrogen effects on a subset of tests of executive function. Women on estrogen + progesterone therapy did not outperform non-users, suggesting that the addition of progesterone to hormone therapy may mitigate the benefits induced by estrogen use alone. Overall, findings support the hypothesis that estrogen use may temper age-related cognitive decline by helping to maintain functions subserved by the frontal lobes.     

EEG theta phase coupling during executive control of visual working memory investigated in individuals with schizophrenia and in healthy controls

In healthy humans, it has been shown that executive functions are associated with increased frontal-midline EEG theta activity and theta phase coupling between frontal and posterior brain regions. In individuals with schizophrenia, central executive functions are supposed to be heavily impaired. Given that theta phase coupling is causally involved in central executive functions, one would expect that patients with an executive function deficit should display abnormal EEG theta synchronization. We therefore investigated executive functioning in 21 healthy controls and 21 individuals with schizophrenia while they performed a visuospatial delayed match to sample task. The task required either high executive demands (manipulation of content in working memory [WM]) or low executive demands (retention of WM content). In addition, WM load (one vs. three items) was varied. Results indicated higher frontal theta activity for manipulation processes than for retention processes in patients with schizophrenia, as compared with healthy controls, independently of WM load. Furthermore, individuals with schizophrenia revealed a reduction in theta phase coupling during early stages of the delay period for retention, as well as for manipulation processes at high-WM loads. Deviations in theta phase coupling in individuals with schizophrenia were mainly characterized by aberrant fronto-posterior connections, but also by attenuated posterior connections during manipulation of high-WM load. To conclude, fronto-parietal theta coupling seems to be substantially involved in executive control, whereas frontal theta activity seems to reflect general task demands, such as deployment of attentional resources during WM.     

Sequential Memory: A Developmental Perspective on Its Relation to Frontal Lobe Functioning

The multidimensional nature of the frontal lobes serves to organize and coordinate brain functionings playing a central and pervasive role in human cognition. The executive processes implicated in complex cognition such as novel problem solving, modifying behavior as appropriate in response to changes in the environment, inhibiting prepotent or previous responses, and the implementation of schemas that organize behavior over time are believed to be mediated by the frontal regions of the brain. Overall, the functioning of the frontal lobes assists individuals in goal directed and self-regulatory behavior. Additional theories of frontal lobe functioning have focused on its involvement in temporal, or time-related domains. The organizational and strategic nature of frontal lobe functioning affects memory processes by enhancing the organization of to-be-remembered information. Among the specific memory systems presumed to be based on anterior cerebral structures is the temporal organization of memory. An essential component of memory that involves temporal organization is sequential ordering entailing the ability to judge which stimuli were seen most recently and the temporal ordering of events in memory. Focal lesion studies have demonstrated the importance of the frontal lobes on retrieval tasks in which monitoring, verification, and placement of information in temporal and spatial contexts of critical importance. Similarly, frontal lobe damage has been associated with deficits in memory for the temporal ordering, or sequencing, of events. The acquisition of abilities thought to be mediated by the frontal lobes, including sequential memory, unfolds throughout childhood, serving to condition patterns of behavior for the rest of the brain. Development of the frontal regions of the brain is known to continue through late adolescence and into early adulthood, in contrast to the earlier maturation of other cortical regions. The developmental patterns of the frontal lobes are thought to involve a hierarchical, dynamic, and multistage process.     

The role of the episodic buffer in working memory for language processing

A body of work has accumulated to show that the cognitive process of binding information from different mnemonic and sensory sources as well as in different linguistic modalities can be fractionated from general executive functions in working memory both functionally and neurally. This process has been defined in terms of the episodic buffer (Baddeley in Trends Cogn Sci 4(11):417–423, 2000). This paper considers behavioural, neuropsychological and neuroimaging data that elucidate the role of the episodic buffer in language processing. We argue that the episodic buffer seems to be truly multimodal in function and that while formation of unitary multidimensional representations in the episodic buffer seems to engage posterior neural networks, maintenance of such representations is supported by frontal networks. Although, the episodic buffer is not necessarily supported by executive processes and seems to be supported by different neural networks, it may operate in tandem with the central executive during effortful language processing. There is also evidence to suggest engagement of the phonological loop during buffer processing. The hippocampus seems to play a role in formation but not maintenance of representations in the episodic buffer of working memory.     

Frontal theta power linked to neuroticism and avoidance

Approach–avoidance conflict is thought to generate negative affective bias, mediated by theta rhythms. This process is distinct from, and adds to, the effects of simple aversive input. We assessed this distinction by holding gain constant and increasing loss value so that conflict and simple aversion peaked in the conflict (gain equals loss) and loss (net loss) conditions, respectively. Right frontal areas showed increases in both conflict- and loss-induced theta power. However, loss, but not conflict, power was correlated with avoidance and neuroticism, showing a Gender x Hemisphere interaction. We concluded that multiple aversive processes converge in lateral frontal networks and that individual differences in theta response in these networks may reflect differences in behavioural and emotional reactivity to aversive events.