Executive Function The Search for an Integrated Account Marie T. Banich

Executive Function The Search for an Integrated Account Marie T. Banich

Executive Function The Search for an Integrated Account Marie T. Banich

Department of Psychology & Neuroscience, and Institute of Cognitive Science, University of Colorado at Boulder;

Department of Psychiatry, University of Colorado Denver

ABSTRACT—In general, executive function can be thought

of as the set of abilities required to effortfully guide be-

havior toward a goal, especially in nonroutine situations.

Psychologists are interested in expanding the under-

standing of executive function because it is thought to be a

key process in intelligent behavior, it is compromised in a

variety of psychiatric and neurological disorders, it varies

across the life span, and it affects performance in compli-

cated environments, such as the cockpits of advanced

aircraft. This article provides a brief introduction to the

concept of executive function and discusses how it is

assessed and the conditions underwhich it is compromised.

A short overview of the diverse theoretical viewpoints re-

garding its psychological and biological underpinnings is

also provided. The article concludes with a consideration

of how a multilevel approach may provide a more inte-

grated account of executive function than has been previ-

ously available.

KEYWORDS—executive function; frontal lobe; prefrontal

cortex; inhibition; task switching; workingmemory; atten-

tion; top-down control

Like other psychological constructs, such as memory, executive

function is multidimensional. As such, there exists a variety of

models that provide varying viewpoints as to its basic component

processes. Nonetheless, common across most of them is the idea

that executive function is a process used to effortfully guide

behavior toward a goal, especially in nonroutine situations.

Various functions or abilities are thought to fall under the rubric

of executive function. These include prioritizing and sequencing

behavior, inhibiting familiar or stereotyped behaviors, creating

and maintaining an idea of what task or information is most

relevant for current purposes (often referred to as an attentional

or mental set), providing resistance to information that is dis-

tracting or task irrelevant, switching between task goals, uti-

lizing relevant information in support of decision making,

categorizing or otherwise abstracting common elements across

items, and handling novel information or situations. As can be

seen from this list, the functions that fall under the category of

executive function are indeed wide ranging.

ASSESSING EXECUTIVE FUNCTION

The very nature of executive function makes it difficult to

measure in the clinic or the laboratory; it involves an individual

guiding his or her behavior, especially in novel, unstructured,

and nonroutine situations that require some degree of judgment.

In contrast, standard testing situations are structured—partic-

ipants are explicitly told what the task is, given rules for per-

forming the task, and provided with information on task

constraints (e.g., time limits). Since executive function covers

a wide domain of skills, there is no single agreed-upon ‘‘gold

standard’’ test of executive function. Rather, different tasks are

typically used to assess its different facets.

One classic test often used to assess the compromise of ex-

ecutive function after brain injury is theWisconsin Card Sorting

Test. This task is thought to measure a variety of executive

subprocesses, including the ability to infer the categories that

should guide behavior, the ability to create an attentional set

based on those abstract categories, and the ability to switch one’s

attentional set as task demands change. Briefly, individualsmust

deduce from the experimenter’s response the rule by which the

cards should be sorted (rather than being told the rule explicitly;

see Fig. 1a). After the initial rule is learned successfully, the

examiner changes the rule without informing the individual. At

this point the old rule must be rejected, the new rule discovered,

and a switch made from the old rule to the new. The ability to

exhibit such flexible readjustment of behavior is a cardinal

characteristic of executive function. Individuals with frontal

lobe damage and children younger than 4 years (who are typi-

cally tested on a two-dimensional version of the sorting task)

tend to persist in sorting items according to the previous and now

inappropriate rule.

Address correspondence to Marie Banich, Director, Institute of Cognitive Science, University of Colorado at Boulder, UCB 0344, Boulder, CO 80305; e-mail: marie.banich@colorado.edu.

CURRENT DIRECTIONS IN PSYCHOLOGICAL SCIENCE

Volume 18—Number 2 89Copyright r 2009 Association for Psychological Science

Cognitive psychologists have attempted to disentangle the

different executive subprocesses that underlie performance on

the Wisconsin Card Sorting Test, as well as to identify other

executive subprocesses. For example, the ability to switch

mental sets has been studied by presenting individuals with

multidimensional stimuli (e.g., a colored numeral) along with a

cue that indicates the attribute on which a response should be

based (e.g., color, or whether the number is odd or even). Indi-

viduals are slower to respond and make more errors on trials

requiring a task switch (e.g., categorize by color preceded by

categorize by odd/even) than they do on those that do not (e.g.,

categorize by color preceded by categorize by color), indicating

that task switching requires executive control (Monsell, 2003).

In other executive tasks, decisions must be based on task-

relevant information in the face of distracting information. One

such measure of this ability is the Stroop task, in which a word’s

color must be identified while ignoring the word itself. Since

word reading is more automatic than color naming, executive

control is required to override the tendency to read or to respond

on the basis of the word rather than the ink color. The need for

such control is reflected in slower responses when the word

names a competing ink color (e.g., the word ‘‘red’’ printed in blue

ink) than when it does not (e.g., the word ‘‘sum’’ in red ink or the

word ‘‘red’’ in red ink).

Other tasks, such as the Tower of London task, examine the

ability to plan and sequence behavior towards a goal. In this task,

a start state and a goal state are shown, and the individual must

determine the shortest number of moves required to get the balls

from the starting state to the goal state (see Fig. 1b). An inability

to solve the problems, taking more steps than necessary, and/or

impulsively starting to move the balls before planning are all

symptoms of executive dysfunction on this task.

THE COMPROMISE OF EXECUTIVE FUNCTION

Psychologists are interested in executive function because it is

critical for self-directed behavior, so much so that the greater the

decrement in executive function after brain damage, the poorer

the ability to live independently (Hanks, Rapport, Millis, &

Deshpande, 1999). Normal children, adolescents, and older

adults also show decrements in executive function. Most notable

in children is their perseveration when required to switch tasks.

Although they can correctly answer questions about what they

should do, they nonetheless are often unable to produce the

correct motor response (Zelazo, Fyre, &Rapus, 1996). Similarly,

parents often wonder why teenagers take risks and make im-

prudent decisions even though they seem to ‘‘know’’ better. This

demonstrated knowledge about abstract rules coupled with an

inability to implement them, especially in the face of distracting

or conflicting information, is reminiscent of that observed in

children. The ability to plan ahead in multistep processes, to

learn about contingences between reward and punishment in

multifaceted decision-making tasks, and to exert inhibitory

control and reduce impulsive behavior continues to increase

during the teenage years and, in fact, well into the early 20s

(Steinberg, 2007). Executive function is also the cognitive

ability most affected by aging (e.g., Treitz, Heyder, & Daum,

2007), with even more severe decline associated with mild

cognitive impairment and Alzheimer’s disease. Finally, execu-

tive function is compromised across a large number of psychi-

atric illnesses, including schizophrenia, bipolar disorder,

??

First Move

Second Move

FinishStart

Fourth Move

Third Move

a

b

Fig. 1. Examples of tasks often used to assess executive function. In the Wisconsin Card Sorting Test (a), individuals must sort cards into one of four piles; each card has items on it that vary along three dimensions— color, number, and shape—with each dimension having one of four values (e.g., Color: red, blue, green, or yellow; Number: 1, 2, 3, or 4; Shape: circle, square, triangle, or cross). Individualsmust deduce the correct rule (i.e., dimension) on which to sort the cards based on feedback provided by the examiner about whether each choice made was correct or incorrect. When the rule is changed, individualswith prefrontal damage andchildren younger than 4 often perseverate on this type of task. They are either unable to learn the new rule or return to the old rule even after they have successfully sorted a number of trials by that new rule. In the Tower of London task (b), an individual is showna series of itemswith an initial state and a goal state; on every trial, there are three pegs, which can hold one, two, and three balls, respectively. The individual must determine the shortest number of moves required to get from the initial state to the final goal state. In some cases, suchas in the sequence shownhere, the individual may have to backtrack—that is, move a ball to a temporary position (the first move) before moving it back to its final position.

90 Volume 18—Number 2

Executive Function

depression, substance use disorders, and attention deficit

hyperactivity disorder (e.g., Willcutt, Doyle, Nigg, Faraone, &

Pennington, 2005).

PSYCHOLOGICAL AND NEUROBIOLOGICAL MODELS

OF EXECUTIVE FUNCTION

Even though there is agreement that damage to the frontal lobe is

associated with compromised executive function, there is little

accord on much else—with regard either to the cognitive com-

ponents of executive function or to the manner in which the

frontal lobe supports executive function. This lack of consensus

seriously inhibits our understanding of the psychological and

neural mechanisms underlying executive function, as well as the

development of treatments to prevent or ameliorate deficits in

this area.

To somewhat oversimplify a complicated literature, one class

of models argues that executive function is an emergent function

of a more basic, largely monolithic psychological construct like

general intelligence (g), fluid intelligence, reasoning and pro-

cessing speed, or the ability to actively maintain information

online to meet task demands (often conceptualized as working

memory; e.g., Salthouse & Davis, 2006). Studies examining in-

dividual differences in task performance across neurologically

intact individuals suggest that there may actually be distinct

subcomponents to executive function, including the ability to

inhibit a prepotent response, the ability to shift the task set

guiding behavior, and the ability to update the contents of

working memory. Of note, studies of twins suggest that at least

some of these subcomponents, notably response inhibition and

set shifting, appear to be separable from g (Friedman et al.,

2006).

Equally contentious are theories regarding the neural mech-

anisms of executive function. Some researchers have argued that

lateral regions of the prefrontal cortex (PFC) are engaged across

a diverse set of demands that engage executive function (Duncan

& Owen, 2000). Such theories are consistent with findings that

the performance of patients with frontal lobe lesions across

distinct tasks can be explained by a single factor. Other theories

hold, however, that distinct regions of the prefrontal cortex are

involved in different aspects of executive functions. For exam-

ple, Petrides (2005) has argued that inferior lateral regions of the

prefrontal cortex (Brodmann Areas [BA] 45, 47) maintain in-

formation in working memory while others, notably mid-dorso-

lateral prefrontal regions (BA 9, 46), perform executive-control

operations on that information. Another theory is that control

mechanisms in the prefrontal cortex are organized in a hierar-

chical manner, with more anterior regions using internally

generated information to guide behavior and more posterior

regions using information from the environment (Christoff &

Gabrieli, 2000). Another idea, based on the pattern of decrement

found across a battery of tests in patients with focal frontal le-

sions, is that there are three main types of executive function,

each associated with a different part of the frontal cortex. In this

view, initiating and sustaining a response rely on medial frontal

regions, task setting relies on left lateral regions, and monitoring

involved in checking and adjusting task performance over time

relies on right lateral regions (Stuss & Alexander, 2007).

Based on functional neuroimaging studies with the Stroop

task, our laboratory has taken yet another view. We suggest that

executive function involves a temporal cascade of selection

processes that are implemented at distinct way stations in the

PFC (see Fig. 2). In this model, posterior regions of the dorso-

lateral PFC (DLPFC) impose an attentional set toward task-

relevant processes. This region activates when it is difficult

to ignore information that engages a task-irrelevant process,

regardless of the type of task-irrelevant process (e.g., word

reading, color identification) or the nature of the process that

is required for the task (e.g., color identification, object identi-

fication; Banich et al., 2000). In contrast, the mid-DLPFC

selects among the specific representations identified as task-

relevant. For example, this region becomes activated for both

incongruent (e.g., ‘‘red’’ in blue ink) and congruent (e.g., ‘‘red’’ in

red ink) trials in the Stroop task, because one must determine

which source of color information (that contained in the ink color

or that contained in the word) is task-relevant (Milham, Banich,

& Barad, 2003). Posterior portions of the dorsal anterior

cingulate cortex (ACC) tend to be involved in late-stage aspects

of selection, being especially sensitive to response-related fac-

tors. This region shows the greatest activity when stimuli lead to

two competing responses and is less sensitive to semantic types

of conflict (Milham et al., 2001). Finally, anterior regions of the

dorsal ACC appear to be involved in processes related to re-

sponse evaluation, as activity in this region increases when the

probability of making an error increases (Miham & Banich,

2005). An important part of our theory is that how much any of

these executive-control mechanisms are invoked depends on

how effectively control was applied at earlier way stations, with

activity in the ACC being affected by how well regions of DLPFC

impose control. For example, with increased practice at a Stroop

task, activity in the DLPFC drops slightly, but that of the pos-

terior dorsal ACC diminishes greatly as control by DLPFC

becomes more effective (Milham, Banich, Claus, & Cohen,

2003). Conversely, relative to younger adults, older adults show

less DLPFC activity but increased cingulate activity (Miham

et al., 2002), which is consistent with the cascade-of-control

model.

TOWARD AN INTEGRATED MODEL

How can all these different conceptions of executive function be

reconciled? This is a major challenge facing the field today. In

pursuit of a more integrated account of executive function, our

laboratory is working collaboratively along with others at the

University of Colorado and the University of Illinois under the

auspices of a National Institute of Mental Health center grant to

Volume 18—Number 2 91

Marie T. Banich

link theories of executive function across different levels of

analysis. We are considering the nature of executive function at

three distinct levels: the neurobiological (at the level of both

neurotransmitters and brain systems), the psychological, and

the computational. Our goal is to consider how information at

each of these levels can be linked, and thereby lead to a theory of

executive function that can better account for themany disparate

pieces of knowledge currently available.

One example of an issue being actively examined within our

center is the nature of executive processes involved in the im-

position and switching of task sets. Our computational models,

as well as empirical studies of neurotransmitter function, suggest

that dopaminergic connections from the basal ganglia to the

frontal cortex act as a gate, signaling whether one should

hold onto the information currently being maintained in

working memory or clear it out to allow new information to enter

(O’Reilly, 2006). These findings raise the possibility that genetic

variation in dopaminergic function influences the maintenance

and switching of task sets, a possibility we are currently inves-

tigating. At the level of brain systems, one major area affected by

this gating would be the posterior portion of the DLPFC, which

according to our cascade-of-control model is involved in creat-

ing and maintaining an attentional set. Moreover, recent work by

colleagues at the University of Illinois suggests that these same

posterior regions of the DLPFC are involved in creating and

maintaining an ‘‘affective’’ set, as activity in this region during

attentionally demanding tasks differs between depressed and

nondepressed individuals (Herrington et al., 2009). Develop-

mental research in our center shows, at the psychological and

computational levels, that a child’s ability to create abstract

representations of categories predicts her or his task-switching

abilities (Kharitonova, Chien, Colunga, & Munakata, in press).

One potential explanation is that actively maintained task-set

representations are relatively weak in children. They only be-

come stronger, as well as more abstract and able to be general-

ized, with practice or experience. Hence, a new task set with

3

Posterior dorsal ACC: Select the information that should guide responding

4

Anterior dorsal ACC: Evaluate the response

W

C

mid-DLPFC: Bias to task-relevant representations

21

WB CG

RB RG

Posterior DLPFC: Bias to task-relevant processes

Fig. 2.The cascade-of-controlmodel of executive function in frontal cortex.Herewe showhow the cascade-of-controlmodel (Banich et al., 2000;Milham&Banich, 2005;Milham,Banich, Claus,& Cohen, 2003; Milham et al., 2002) would explain performance on the Stroop task. The example shown is for the word ‘‘blue’’ printed in green ink. The direction of the cascade is indicated by the dashed arrows. First, posterior regions of the dorsolateral prefrontal cortex (DLPFC; 1) create and impose a top-down attentional set for task-relevant goals. In this case, a top-down attentional set is imposed toward activation of brain regions involved in ink-color identification (C). This bias must be strong (as denoted by the thick line) to counteract the automatic bias (noted by a thin line) towardbrain regions that are involved inwordprocessing (W).However, this top-downattentional set cannot overcome a lifetime of word reading, so selectionmust occur among the representations that are identified as related to color. We argue that mid-DLPFC (2) selects which of the repre- sentations,most likely being activelymaintained, ismost task relevant.Here the selectionwouldbe toward the ink color green (CG) as compared to the word ‘‘blue’’ (WB). Next, posterior regions of the dorsal anterior cingulate cortex (3) must determine what information should be used in de- termining the response (R), in this case selecting the response (either verbal or manual) associated with green (RG) as compared to the response associated with blue (RB). However, if selection by prior regions in the cascade (i.e., those in DLPFC) is poor, the posterior dorsal cingulatemust also deal with any unresolved issues of selection from prior way stations in the cascade before a re- sponse can be emitted. Finally,more anterior regions of the dorsal anterior cingulate cortex (ACC; 4) are involved in response evaluation. If such an evaluation suggests that an incorrect response wasmade, these anterior regions of the dorsal ACC send a signal back to posterior-DLPFC, telling it to assert top-down control more strongly.

92 Volume 18—Number 2

Executive Function

which a child lacks experience will be relatively weak compared

to a prior task set that has been used repeatedly on preceding

trials.

These are some of our first steps at linking neurobiological,

psychological, and computational approaches in an effort to

better understand executive function. How might such an inte-

grated account be helpful? We believe that a more integrated

account may aid in the design of new interventions for executive

dysfunction. For example, our findings suggest the possibility

that training people in building abstract categories may bolster

aspects of executive function such as task switching. One diffi-

culty with training regimens is that sometimes their results are

not immediately apparent but are only seen down the road. Brain

imaging might provide a means to determine whether additional

or different regions come on line during the course of training

even before behavioral changes are manifest. Studies with drug

interventions might provide another way to bolster engagement

of brain regions necessary for executive function. In sum, an

integrated understanding of executive function should open up

new avenues for intervention to aid individuals who have com-

promised executive functioning because of a psychiatric disor-

der, brain damage, aging, or other factors.

Recommended Reading Jurado, M.B., & Rosselli, M. (2007). The elusive nature of executive

function: A review of our current understanding. Neuropsychology Review, 17, 213–233. A longer review of executive function from the perspective of neuropsychology, linking behavior to brain

systems.

Miyake, A., Friedman, N.P., Emerson, M.J., Witzki, A.H., Howerter, A.,

& Wager, T.D. (2000). The unity and diversity of executive func-

tions and their contributions to complex ‘‘frontal lobe’’ tasks: A

latent variable analysis. Cognitive Psychology, 41, 49–100. Out- lines the argument for separable subcomponents of executive

function, drawn from a cognitive and individual-differences

perspective.

Royall, D.R., Lauterbach, E.C., Cummings, J.L., Reeve, A., Rummans,

T.A., Kaufer, D.I., et al. (2002). Executive control function: A re-

view of its promise and challenges for clinical research. A report

from theCommittee onResearch of theAmericanNeuropsychiatric

Association. Journal of Neuropsychiatry & Clinical Neurosciences, 14, 377–405. Discusses the psychiatric andmedical disorders that are associated with compromised executive function, how execu-

tive function is assessed in clinical settings, and the linkage of

executive function with functional outcome; also discusses chal-

lenges in designing treatments for executive dysfunction.

Acknowledgments—The author would like to thank Gregory

Burgess, Wendy Heller, Gregory A. Miller, Yuko Munakata, and

Randy O’Reilly for comments on earlier versions of this manu-

script. The author would also like to thank all the members of

the Interdisciplinary Behavioral Science Center on the

Determinants of Executive Function and Dysfunction (NIMH

P50 MH079485) for their contributions to some of the ideas

presented in this article. Finally the author would like to

acknowledge the support of NIMH Grants P50 MH079485

and R01 MH070037, on which she serves as Principle Investi-

gator, and NIMH Grant R01 MH061358 (Wendy Heller,

Principal Investigator).

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