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Development of Metacognitive and Emotional Executive

Functions in Children
a
Alfredo Ardila
a
Department of Communication Sciences and Disorders, Florida International University,
Miami, Florida
Version of record first published: 28 Jan 2013.

To cite this article: Alfredo Ardila (2013): Development of Metacognitive and Emotional Executive Functions in Children,
Applied Neuropsychology: Child, DOI:10.1080/21622965.2013.748388

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 APPLIED NEUROPSYCHOLOGY: CHILD, 0: 1–6, 2013
Copyright © Taylor & Francis Group, LLC
ISSN: 2162-2965 print/2162-2973 online
DOI: 10.1080/21622965.2013.748388

Development of Metacognitive and Emotional

Executive Functions in Children
Alfredo Ardila
Department of Communication Sciences and Disorders, Florida International University, Miami, Florida

It has been proposed that two major components of executive functions can be
distinguished: (1) one related to complex cognition (metacognition, such as planning,
problem solving, etc.); (2) the other related to coordinating and controlling emotional
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behavior. Contemporary neuroimaging techniques have demonstrated that there are two
distinct functional-anatomical networks within the prefrontal cortex: one associated with
cognitive control and the other associated with value based decision making—each
related to specific frontal-lobe areas. Metacognitive (but not emotional) executive
functions have been demonstrated to be correlated with general intellectual level
(intelligence). Research has shown that emotional executive functions (such as attention
control) develop earlier in life (during the 1st year), before the development of
metacognitive executive functions (such as planning and verbal fluency), which develop
around the age of 3 and are correlated with the development of a grammatical language.

Key words: development in children, executive functions, metacognition

INTRODUCTION 2006; Blair, 2004; Lezak, Howieson, Loring, & Hannay,

2004).
Although it is assumed that the prefrontal cortex plays a Consequently, two major components of executive
major controlling and monitoring role, executive func- functions could be distinguished: (1) those classically
tions depend on extended networks involving different related to complex cognition (such as planning, problem
brain areas. Most importantly, the prefrontal cortex does solving, etc.), and (2) those related to coordinating and
not only participate in those classically recognized execu- controlling emotional behavior. This idea has been sug-
tive operations (sequencing, alternating, inhibiting, etc.), gested by different authors; for instance, a distinction has
but also plays a core role in coordinating cognition and been proposed between the “cool” cognitive aspects of
emotion (Mitchell & Phillips, 2007). The prefrontal lobe executive functions, which are more associated with dor-
has extensive connections to subcortical and limbic solateral regions of the prefrontal cortex, and the “hot”
system areas (Barbas, 2006; Damasio & Anderson, 1993; affective aspects, which are more associated with the ven-
Koziol & Budding, 2009), and even its orbital portion tral and medial regions (Zelazo & Müller, 2002). This
could be regarded as an extension of the limbic system. hot/cool distinction has been applied to the development
By coordinating cognition and emotion, the prefrontal of executive functions in children (Hongwanishkul,
lobe plays a major function by controlling the limbic Happaney, Lee, & Zelazo, 2005).
system impulses—that is, making limbic impulses
“socially acceptable” (e.g., Beer, John, Scabini, & Knight,
TWO EXECUTIVE FUNCTION SYSTEMS
Address correspondence to Alfredo Ardila, Department of
Since the first systematic report of a frontal-lobe lesion
Communication Sciences and Disorders, Florida International
University, 11200 SW 8th Street, AHC3-431B, Miami, FL 33199. (the Phineas Gage case; Harlow, 1848, 1868), it has been
E-mail: [email protected] noted that executive/frontal-lobe function includes two
 2 ARDILA

different components. As a matter of fact, most of the such as solving the Tower of Hanoi (Fincham, Carter,
disturbances reported in Phineas Gage (and in many van Veen, Stenger, & Anderson, 2002), the Controlled
cases of prefrontal syndromes) refer to behavioral/emo- Word Association Test (letter fluency; Baldo, Schwartz,
tional disturbances, or more exactly, disturbances in Wilkins, & Dronkers, 2006), working memory (Yoon,
coordinating cognition and emotion/motivation. Harlow Hoffman, & D’Esposito, 2007), and solving the Wisconsin
(1848, 1868) described severe emotional changes in Card-Sorting Test (Lie, Specht, Marshall, & Fink, 2006).
Phineas Gage but emphasized that no intellectual impair-
ments were observed; he clearly pointed out that neither
Emotional/Motivational Executive Functions
his memory nor his intelligence were compromised by the
brain lesion. Harlow (1848) stated that the “equilibrium Emotional/motivational executive functions are responsi-
or balances so to speak, between his intellectual faculties ble for coordinating cognition and emotion, or the ability
and animal propensities seem to have been destroyed. He to fulfill basic impulses following socially acceptable
is fitful, irreverent, indulging in gross profanity (which strategies. The ventromedial areas of the prefrontal
was not previously his custom), manifesting little or no cortex are involved in the expression and control of emo-
deference for his fellows, and impatient of restraint or tional and instinctual behaviors (Fuster, 1997, 2002).
advice when it conflicts with his desires” (p. 389). It should This function is related with so-called “inhibitory con-
be emphasized that the frontal damage in Phineas Gage trol” of behavior (Miller & Wang, 2006). Clinical evi-
involved the orbital and medial aspects, but not the pre- dence (e.g., Luria, 1969; Stuss & Knight, 2002) and
frontal dorsolateral area (Damasio, Grabowski, Frank, experimental research (e.g., Leung & Cai, 2007; Medalla,
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Galaburda, & Damasio, 1994; Ratiu & Talos, 2004; see Lera, Feinberg, & Barbas, 2007) suggest that the neural
Figure 1). substrate for this inhibitory function resides mainly in the
Consequently, it can be assumed that there are two dif- medial and orbital portions of the prefrontal cortex.
ferent, but closely related types of executive function These two types of executive functions (“metacogni-
(e.g., Ardila, 2008; Fuster, 2002; Happaney, Zelazo, & tive” and “emotional/ motivational”) depend on rela-
Stuss, 2004). tively different prefrontal areas, and as a matter of fact,
two major variants in the prefrontal syndrome are fre-
quently distinguished, one mostly impairing cognition
Metacognitive Executive Functions
(or rather cognitive control—that is, “metacognition”)
Metacognitive executive functions include problem solv- and the other mostly impairing behavior.
ing, abstracting, planning, strategy development and
implementation, and working memory—abilities mostly Dorsolateral Syndrome. Cummings (1993) indicated
related to the dorsolateral area of the prefrontal cortex that the dorsolateral circuit is the most important in exec-
(e.g., Stuss & Knight, 2002). The dorsolateral prefrontal utive functioning. Cortical–subcortical connections have
cortex has been observed to participate in diverse plan- been suggested (Koziol & Budding, 2009). The most
ning, abstracting, problem-solving, and working-memory noted deficit is an inability to organize a behavioral
tasks. Using functional magnetic resonance imaging, dor- response to novel or complex stimuli. Symptoms are on a
solateral prefrontal activation has been found in tasks continuum and reflect the capacity to shift cognitive sets,
engage existing strategies, and organize information to
meet changing environmental demands. Various research-
ers, including Luria (1969), have noted perseveration,
stimulus-bound behavior, echopraxia, and echolalia.
Lateralization has been noted in executive dysfunction
(Goldberg, 2001). The ventral and dorsal portions of the
prefrontal cortex are believed to interact in the mainte-
nance of rational and “nonrisky” decision making (Manes
et al., 2002). According to Fuster (1997, 2002), the most
general executive function of the lateral prefrontal cortex
is the temporal organization of goal-directed actions in
the domains of behavior, cognition, and language.

Orbitofrontal and Medial Frontal Syndrome. Orbito-

frontal damage has been associated with disinhibition,
inappropriate behaviors, personality changes, irritability,
FIGURE 1 Trajectory of the bar in Phineas Gage’s skull, according to
Harlow (1848) (retrieved from https://neurophilosophy.files.wordpress. mood liability, tactlessness, distractibility, and disregard
com/2006/12/phineas_gage.JPG?w=600). of important events (Stuss & Knight, 2002). These
 DEVELOPMENT OF EXECUTIVE FUNCTIONS 3

patients are unable to respond to social cues. Of note, it of age. This means that the brain maturation and the
was observed by Laiacona and colleagues (1989) that associated cognitive abilities do not grow in a steady and
these patients have no difficulty with card-sorting tasks. continuous way, but there are certain periods when prog-
Eslinger and Damasio (1985) coined the term “acquired ress is more notorious.
sociopathy” to describe deregulation that couples both Regardless of the difficulties in measuring executive
lack of insight and remorse regarding these behaviors. functions in children (Hughes & Graham, 2002), several
The orbitofrontal cortex appears to be linked studies have analyzed the early development of executive
predominantly to limbic and basal forebrain sites. Medial functions. Some executive functions that have been ana-
frontal-lobe damage causes apathy or abulia (a severe lyzed through ontogeny are: attentional control, plan-
form of apathy). Acute bilateral lesions in the medial- ning, set shifting, and verbal fluency (see Jurado &
frontal area can cause akinetic mutism, in which the Rosselli, 2007, for a review). Jurado and Rosselli empha-
individual is awake and has self-awareness but does not size that the first executive function to emerge, by the
initiate behaviors (Ross & Stewart, 1981). According to child’s 1st year, is the ability to inhibit overlearned behav-
Fuster (1997, 2002), the ventromedial areas of the ior, resulting in increased attentional control; however, its
prefrontal cortex are involved in expression and control greatest development is some time later (around 6 to 10
of emotional and instinctual behaviors. years of age). Other executive abilities, for instance plan-
It is evident that the two prefrontal syndromes can ning and set shifting, develop later, around age 3 with sig-
have rather different clinical expressions (metacognitive nificant improvement after age 7. Verbal fluency (a lan-
and emotional/motivational) depending upon the specific guage-mediated executive function) is the last to emerge
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location of the damage. For Phineas Gage, the distur- and is significantly influenced by environmental factors.
bance was observed in controlling emotions and instinc- All executive functions, nonetheless, continue to improve
tual behaviors; it was associated with damage at the orbi- until adolescence.
tofrontal and medial-frontal areas. The dorsolateral Hongwanishkul et al. (2005) assessed different execu-
prefrontal cortex was not damaged, and cognition was tive functions in 3- to 5-year-old children using two puta-
unimpaired. tive measures of cool (metacognitive) executive functions
There is robust evidence to assume that two different (Self-Ordered Pointing and Dimensional Change Card
prefrontal systems support these two executive function Sort) and two putative measures of hot (emotional) exec-
subtypes. For instance, Gläscher et al. (2012) used voxel- utive functions (Children’s Gambling Task and Delay of
based lesion symptom mapping (i.e., method and soft- Gratification). Findings confirmed that performance on
ware for analyzing relationships between behavioral defi- both types of tasks develops during the preschool period.
cits in neurological populations and lesion sites associated However, the measures of hot (emotional) and cool
with those deficits) in 344 individuals with focal brain (metacognitive) executive functions showed different pat-
lesions, including 165 involving prefrontal pathology; a terns of relations to each other and to measures of gen-
comprehensive neuropsychological test battery was eral intellectual function and temperament: Whereas cool
administered to all participants. It was demonstrated that (metacognitive) executive functions significantly corre-
there are two distinct functional-anatomical networks lated with general intellectual ability (“intelligence”), hot
within the prefrontal cortex: (1) one associated with cog- (emotional) executive functions were not related to gen-
nitive control (that is, “metacognitive executive func- eral intellectual functioning (verbal mental age and per-
tions,” including response inhibition, conflict monitor- formance mental age).
ing, and switching), and supported by the dorsolateral Matute et al. (2008) analyzed the influence of age on
prefrontal cortex and anterior cingulate cortex; and (2) a the performance of a planning and organization task
second functional-anatomical network associated with (two skills included in the metacognitive executive func-
value-based decision making (“emotional/motivational tions), using the so-called “Mexican pyramid” (a test
executive functions”), which included the orbitofrontal, similar in principle to the Tower of London Test; Shallice,
ventromedial, and frontopolar cortex. 1982). Its purpose was to measure problem-solving abil-
ity, and it was taken from the Evaluación Neuropsicológica
Infantil (Child Neuropsychological Assessment [ENI];
EXECUTIVE FUNCTIONS IN CHILDREN Matute, Rosselli, Ardila, & Ostrosky-Solís, 2007); 239
school-age children from México and Colombia, distrib-
Executive functions rapidly develop through childhood; uted into six age groups, were selected. Five measures
this development is clearly correlated with the maturation were analyzed: number of correct designs, number of
of the frontal lobes (Anderson, Anderson, Northam, movements per design, execution time in the correct
Jacobs, & Catroppa, 2001). Different growth periods have designs, number of correct designs built with the mini-
been proposed: the period from birth to 2 years of age; mum of movements, and its execution time. A significant
from 7 to 9 years of age; and a finally, from 16 to 19 years effect of age on the five measures was found. Comparison
 4 ARDILA
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FIGURE 2 Scores in four selected executive tests (1 = 5 to 6 years; 2 = 7 to 8 years; 3 = 9 to 10 years; 4 = 11 to 12 years; 5 = 13 to 14 years; adapted
from Ardila et al., 2005).

between groups showed that younger children (5 to 6 children were requested to find commonalities between
years old) had a smaller number of correct designs, while pairs of words (concept formation). Eight pairs of
children aged 5 to 8 years old needed more movements. words were presented, one at a time. Abstract general-
Execution time showed a greater number of differences izations or categorizations (i.e., “A dog and a cat are
between groups. According to the authors, the results animals”) were scored with 2 points; specific and
supported the notion that the development of planning descriptive answers (i.e., “A dog and the cat have four
and organization is fast in the 1st years of school age and legs”) were scored with 1 point, and incorrect answers
slows down in adolescence. received a 0. The maximum score was 16. (4) Matrices
Ardila, Rosselli, Matute, and Guajardo (2005) was a multiple-choice subtest consisting of a series of
reported the developmental pattern of different execu- visual pattern- matching and analogy problems pictured
tive functions between the ages of 5 to 6 years old and in nonrepresentational designs. It required the child to
13 to 14 years old, using 315 participants taken from conceptualize spatial and design relations such as in
public schools (156 boys and 159 girls) and divided into Raven’s Progressive Matrices (Raven, Court, & Raven,
five age ranges (5 to 6 years old, 7 to 8 years old, 9 to 10 1976). One point is given to each option correctly
years old, 11 to 12 years old, and 13 to 14 years old). selected by the child. The maximum score is 8. Figure 2
The scores in several executive function subtests taken presents the development of the scores in these four
for the ENI (Matute et al., 2007) were analyzed. The selected executive function tests.
results in four selected metacognitive executive func- Improvement between the first (5 to 6 years old) and
tions are presented here: (1) For Semantic Verbal the last age range (13 to 14 years old) was observed in the
Fluency, children were instructed to name all animals four tests, but it was highest for the Phonemic Verbal
they could in 1 minute. The score was the total number Fluency Test (the score among the oldest children was
of animals named correctly. (2) For Phonemic Verbal about 7 times greater than among the younger children),
Fluency, children were instructed to say as many words whereas in the other three tests, the score in the oldest
starting with M as they could in 1 minute. The score was group was only about 3 times greater than in the younger
the total number of correct words. (3) For Similarities, group.
 DEVELOPMENT OF EXECUTIVE FUNCTIONS 5

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