Assessment of Executive Function in Infants And.11
Assessment of Executive Function in Infants And.11
ABSTRACT: Objective: The development of executive function (EF) in infants and toddlers has received in-
creased interest by clinicians and researchers. Higher rates of deficits in EF have been reported in at-risk
groups of infants such as those born extremely preterm. These deficits play an important role in the etiology
of early neurodevelopmental problems and are predictive of subsequent nonoptimal educational outcomes.
In this study, the Bayley-4 is used to follow the developmental course of EF and to determine whether EF is a
unitary concept or can be parsed into discrete components over the first 42 months. Method: All 81 cognitive
items from the Bayley-4 normative sample of 1700 infants and toddlers were classified a priori into 6 EFs, and
then, 5 age groups derived from Bayley-4 start points were factor analyzed to determine at what age EFs
emerge and to address the controversy of whether the factor structure of the cognitive items for each of 5 age
groups reflect a single factor or multiple factors. Results: Bayley-4 items form 1 to 5 EF factors for each age
group, accounting for 59% to 74% of the variance. There is a developmental progression in EF as well. The
results indicate EF constructs can be identified early. Conclusion: Executive function tasks in infants and
toddlers are interrelated with task content either remaining the same or changing with advancing age
(i.e., content that is homotypic or heterotypic, respectively). EFs measured by Bayley-4 items are useful
clinically and become more complex with increasing age, corresponding to more advanced brain de-
velopment and integration. The findings have the potential of providing additional information in the as-
sessment of infants at risk such as those born preterm.
(J Dev Behav Pediatr 43:e431–e441, 2022) Index terms: Bayley-4, executive function, infants.
Copyright © 2022 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
development,11 the tasks that assess EF have been distin- to increasing age. There was no consideration given re-
guished based on their purported demands. It is difficult garding which EFs might be involved in the execution of
to identify a single EF as the sole contributor to perfor- an item. One of the aims in designing the Bayley-4 Cogni-
mance on a task in infancy because of “task impurity” tive subscale was to include tasks that impose varying EF
(meaning most tasks involve several EFs), although it may demands on the infant or toddler. Some of these tasks can
be possible to identify the primary EF. Theories of EF be considered “homotypic,” meaning that an early skill or
development in infancy2,7,11 postulate transitions begin- acquisition has an obvious connection with a later behavior
ning with early reactive attention to environmental stimuli and it seems to measure the same concept (e.g., attention)
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in the newborn period. This is followed over the first 6 across multiple ages. Other tasks are more heterotypic,
months of life by development of more voluntary control with the links between early manifestations and later abil-
of attention through an orienting system subserved by ities being less obvious and seeming unrelated or in-
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posterior brain systems that allow selective attention and congruent. In such cases, it is assumed that the relevant
attentional disengagement. Beginning at approximately brain region has functional circuitry allowing for at least
age 6 months, infants begin to develop “executive atten- rudimentary function and continuity with later behaviors.10
tion” mediated by anterior brain regions that entails im- Heterotypic tasks are common because of the limited be-
provements in the ability to inhibit distractions and havioral repertoires and the immaturity of the relevant
sustain attention over longer periods and in response task brain regions in very young children. Stated differently,
demands. WM, or the ability to retain mental representa- there is often apparent discontinuity between the early
tions of experienced events or task demands, develops in manifestations of a skill and its later appearance because of
concert with attentional control and response inhibition the developmental status and later refinement of the un-
during the latter half of the first year, with improved co- derlying brain substrate as seen in performance of infant
ordination of these systems in the second year that per- tests such as the Bayley-4.
mits infants to better regulate their behavior by inhibiting Examination of cross-age performances of infants and
prepotent response tendencies in favor of achieving a toddlers on cognitive items from the Bayley-4 normative
nonimmediate goal or following a rule. A final stage in sample would provide an opportunity to explore the
development of EF in young children is the ability to shift developmental unfolding of EF and also the issue of
attention between mental sets.12,14 whether to conceptualize the EF domain as a unitary
construct or a multicomponent ability domain.14
Neuroanatomic Underpinnings Knowledge gained from such investigations could then
Executive functions are mediated by a neuroanatomic be used in comparing infants and toddlers at risk, such as
network that primarily involves the prefrontal cortex those with preterm birth to normative data to better
(PFC) but also includes other brain areas: the frontos- understand the early developmental consequences of
triatal and temporal regions, the right caudate nucleus, prematurity.
thalamus, globus pallidus, and cerebellum, as well as Given the wide use of the Bayley Scales in research
regulation of neurotransmitters.13 Developmental im- studies and in clinical settings, measures of EF derived
provements in EF may be due to advances in functional from its administration could also serve as a standard
integration of different areas of the brain versus the against which to assess the utility of other, more experi-
simple development and maturation of one region such mental EF measures. In this way, measures of EF based on
as the PFC alone. However, the extent of abnormal de- the Bayley-4 could contribute to the validation of more
velopment of the prefrontal lobes may be an important robust and age-specific assessments of EF in infants.
determinant of deficits in cognitive functioning.11
Brain injury at earlier gestational ages can cause gross METHODS
failure of thalamocortical innervation; by contrast, later
Subjects
injury (i.e., closer to term) interferes with the refinement
As part of the test standardization process, 1700 typ-
of thalamocortical connections into mature circuits.13
ically developing children who received the Bayley-4
Axons, neurons, and dendrites are affected, as is overall
were stratified based on US Census data for sex, race/
brain organization. The subplate neuronal layer is the
ethnicity, parent education level, and region of the
structure through which the lower and upper brain
centers are connected and is highly susceptible to dis- country and divided into 17 age groups of 100 children
each.15 Informed consent was obtained originally by
ruption and/or injury in children born preterm and may
Pearson. The data used in this study were deidentified,
be a prime cause of EF deficits in this group.
and hence, no further review was necessary. Essentially,
The Bayley-4 this is a secondary analysis of the data set gathered in the
Bayley-4 standardization.
The Bayley Scales of Infant and Toddler Development-49
is the reference standard for assessing developmental delay
in cognitive, language, and motor domains. Items on the Procedure
Bayley were included based on a modified power format All 81 Bayley-4 cognitive items were grouped a priori
with items becoming increasingly difficult corresponding into 6 executive function (EF) categories based on face
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validity and consensus of the authors as to what EF was the more complex tasks, these processes become in-
assumed to be primarily necessary for item completion. creasingly influential. It is assumed that many of these
Because of the assumed inter-relatedness of EFs, it is Bayley-4 items involve more than 1 executive function.
acknowledged that there is the possibility of overlap in For factor analysis, to prevent items being entered twice
functions. Language and motor domains were not in- in the analyses, items C37 and C42 were placed in
cluded in these analyses. Performance on the 6 EF cate- working memory (WM), although they also involved in-
gories was evaluated in the normative sample divided hibition. Similarly, items C48 and C51 were considered
into 5 age groupings. These age groupings were based representative of higher-order cognitive processes and
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on the Bayley-4 start points that specify where the child flexibility/shift, respectively. When cross-loading oc-
should begin the cognitive subtest based on age. The curred, the highest loading of the item warranted in-
start points afforded basal pass rates of 95%9 for the clusion on that factor.
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Table 1. Bayley-4 Cognitive Items and Hypothesized Underlying groups (see Weibe et. al.)14. Three attention items had
Executive Functions SDs of 0, these being too easy (Table 4).
Item Description Modality
GRP 4 (23 Months 0 Days to 28 Months 30 Days)
Attention
This group has 4 factors accounting for 66% of the
C2 Looks at object 7–10 s Visual
variance. As evident from PCA of the younger age
C3 Habituates to rattle Auditory groups, items loading on factor 1 placed demands on
C8 Visually shifts attention to bell/rattle Visual/auditory WM, flexibility/shift, and planning (21%). However,
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C9 Visual preference—more complex item Visual some of the items loading on this factor also involved
C10 Visual habituation Visual attention to the environment and to pictures, possibly
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Table 2. Principal Component Analysis for Group 1: Age #6 Months 30 Days
Factor 1 Factor 2 Factor 3 Factor 4
Attention
C2 looks at object 0.64
C3 habituates to rattle 0.65
C8 visually shifts attention 0.76
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levels of internal attentional regulation versus atten- Regarding attention, Bayley18 suggested age 1.3
tion being reactive to the environment. Based on these months is when 50% of infants visually inspect the en-
data, attention seems homotypic, while cognitive skils vironment. Control of attention is evident as early as 4
are more heterotypic. Content analysis of items load- months, with a significant transition at 9 months. For
ing on other factors reflects more specific aspects of example, high novelty preference in early visual tasks is
EF. Hence, the assertion of Miyake et al.5 that there is replaced at 18 to 24 months by the ability to focus on a
both “unity and diversity” in EF is supported. central stimulus. Other cognitive skills such as
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Table 3. Principal Component Analysis for Group 2: Ages 7 Months to 13 Months 30 Days
Factor 1 Factor 2 Factor 3 Factor 4
Attention
C8 visually shifts attention 0.51
C9 visual—more complex 0.95
C10 visual habituation 0.85
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Table 4. Principal Component Analysis for Group 3: Ages 14 Months 0 Days to 22 Months 30 Days
Factor 1 Factor 2 Factor 3 Factor 4 Factor 5
Attention
C9 visual preference 0.90
C10 visual habituation 0.80
C11 preference for novel (0.44) 0.80
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WM
C21 searches for object (0.53) 0.63
C24 anticipatory gaze (0.47) (0.41)
C28 missing objects 0.72
C32 hidden object 0.53
C37 hidden object reversed 0.56
C42 visual displacement (0.43) 0.51
C56 spatial memory (3) 0.61 (0.50)
C76 spatial memory (6) 0.96
C60 children’s names 0.64
C64 repeats words 0.88
C67 discriminates pictures 0.85
C80 number sequence 0.95
Goal-directed problem-solving
C14 object to mouth 0.91
C22 pulls string to get ring (0.62) (0.62)
C57 2-step action 0.54
Flexibility/shift
C34 removes pellet (0.30) (0.32)
C35 clear box obstacle 0.63
C53 puzzle: cone (0.44) 0.58
C73 puzzle: dog 0.97
C74 puzzle: cat 0.95
C40 form board: pink 0.79
C43 blue form board: 1 piece 0.64
C47 blue board: 3 pieces 0.76
C49 form board: 4 pieces 0.77
C51 rotated pink board 0.75
Higher-order processes
C48 pencil to obtain object 0.52
C62 grouping by size 0.88
C63 grouping by color 0.95
C68 simple patterns 0.95
C81 completes patterns 0.95
Variance 35% 14% 9% 5% 4%
Variance after rotation 28% 15% 9% 9% 6%
( ) 5 cross-loading on factor. WM, working memory.
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habituation and visual discrimination are related to at- months) and the ability to imitate a 2-step action are also
tention.12,16 Items tapping this skill become more com- examples of Bayley-4 items that require planning and
plex with increasing age. The earlier skills are heavily problem-solving. These skills improved gradually with
dependent on visual sensory abilities, while later items each age group, and all Bayley-4 goal-directed planning
also involve auditory attention. From approximately 14 items were successfully completed by most of the oldest
months onward, the tasks primarily involving attention toddlers. Rudimentary planning skills emerge at 7 to 8
were consistently mastered. months, and these are essential for goal-directed behav-
Infants are able to show early WM skills on tasks at 7.5 ior. Infants born preterm perform more poorly than full-
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to 8 months. By 9 to 12 months, infants are capable of term counterparts at 8 months corrected age and 10 to
holding 1 or 2 items in WM for longer periods of time.17 11 months chronological age on multistep planning tasks
Object permanency is perhaps the first manifestation of (e.g., removing a barrier and pulling a cloth and then
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WM. Anticipatory gaze or recalls names of children pulling a string to retrieve a toy).25
demonstrates the inter-relatedness of attention and WM The capacity to be flexible and shift when
in the process of learning and the fact that these func- approaching a problem is necessary for successful com-
tions provide a base for further EF development. At pletion of various items such as to remove a pellet, cir-
young ages, the distinction between short-term memory cumvent a barrier, or assemble puzzles. Observing the
and WM is not as clear as in older children. infant’s unsuccessful attempts during tasks such as form
Inhibition is involved in memory tasks such as finding boards or puzzle assembly also enables determination of
a hidden object reversed or finding a hidden object after the presence or absence of flexibility/shift. Infants who
a visible displacement. It is difficult to separate inhibition approach the task in a trial-and-error fashion or who
and WM items on the Bayley-4, and it is quite likely that persist in repeating the same unsuccessful response
inhibition is not distinct but is rather a basic function demonstrate less well-developed EF to change, as well as
encompassed in many tasks that use other EFs. Inhibition limitations in their ability to learn from experience.
enables the infant to deter prepotent responses and Reasoning, processing speed, persistence and
therefore show early planful behavior.7,19 Bayley18 in- problem-solving, and being able to understand concepts
dicated that the 50th percentile in displaying precursory require that EFs work in unison. This is evident on
object permanency was 5.2 to 6.0 months (i.e., with an Bayley-4 items such as uses pencil to obtain object, ro-
auditory and visual cue) and that 9.0 months was the age tated pink board, grouping by size or color, or un-
at which infants scored at the 50th percentile in at- derstanding patterns. On the Bayley-4, success on tasks
tending to an isolated visual cue. Memory for hidden involving this complex level of function becomes evi-
objects weakens with increased delay between the dent in GRPs 4 and 5, with the skill becoming more
demonstration and the infant’s response. At approxi- evident at age 2 ½ years.
mately 7 to 8 months, the maximum delay is 2 seconds; The EF items of the Bayley-4 have value in providing
at 9 months, it is 5 seconds; and at 12 months, it is a 10- an early assessment of EF that could be related to later
second delay.20,21 No time between observation and re- cognitive, social, and achievement outcomes and in ex-
sponse is specified on the Bayley-4, although anecdotally amining associations of earlier manifestations of EF to the
it seems to be in the 2- to 3-second range. WM and in- more complex forms of EF displayed by preschool and
hibition are necessary for the EF of flexibility/shifting.4 school-age children. Success on higher-order processing
Inhibitory control helps the young child to selectively items requires thinking, reasoning, and synthesizing of
attend and display goal-directed behavior despite dis- information—all of which involve the EFs of attention,
tractions. There are 3 aspects of inhibition: inhibition of inhibition, and WM as basic components.22 The ability to
the prepotent response, interruption of an ongoing re- successfully complete more difficult tasks at older ages is
sponse, and inhibition of interference from external assumed to require the simultaneous coordination of
stimuli. Developmentally, inhibition is first noted at 7 to basic EF components.19 Future research should involve
12 months, and there is continued improvement up to investigation of the relationships between these early
18 to 30 months.13,23 Many infants have difficulty with indicators of EF and later EFs in preschool and school-age
the classic A-not-B task at 8 to 12 months because they children.
fail to resist a “reinforced habit” (prepotent response) A possible limitation of this study is that the Bayley-4
and select the original site, “A.” Garon et al.8 distin- items were administered to typical infants. Conversely,
guished simple from complex inhibition: Simple in- this is the largest sample to date to be subject to such
hibition requires minimal WM, while the complex form analyses, and the data can be considered “normative.”
would involve more WM to maintain the rules of the task Moreover, it would be expected that many infants born
at hand. preterm would demonstrate a similar mastery sequence
The earliest indicator of goal-directed problem-solving based on their corrected age, although brain disruption
is bringing an object to the mouth.24 This is a simple in extremely preterm infants without apparent injury or
canalized behavior, explaining why there was such a older infants sustaining a brain insult would most likely
high success rate for this item in younger children. Using negatively affect EF, particularly if the subplate neuronal
a pencil to obtain an object (50th percentile 5 17 layer is affected. Another limitation is that the data are
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Table 5. Principal Component Analysis for Group 4: Ages 23 Months 0 Days to 28 Months 30 Days
Factor 1 Factor 2 Factor 3 Factor 4
Attention
C8 visually shifts attention (0.40) 0.91
C9 prefers more complex stimulus (0.40) 0.91
C10 habituation (0.40) 0.92
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Table 6. Principal Component Analysis for Group 5: Ages 29 Months to 42 Months 30 Days
Factor 1 Factor 2 Factor 3
Attention
C26 looks at pictures 0.96
C41 listens to story 0.55 (0.48)
WM
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cross-sectional, and longitudinal data are needed to fur- are involved in loadings of other unrelated tasks on the
ther explore developmental progressions of EFs. An in- first factors at each age.
teresting but untested assumption is that the structural
development of the infant’s nervous system correlates CONCLUSIONS
with the emergence of specific behaviors, although In summary, the item analysis of Bayley-4 provides
correlations do not explicitly indicate causality.25,26 support for combinations of early forms of executive
The assumption that loadings may be due to similarity function (EF), including attention, working memory
in tasks (e.g., form boards) rather than underlying EFs is (WM) and inhibition, and mental flexibility and set
contradicted by the fact that other cognitive functions shifting, as contributors to higher-level functions such as
Copyright © 2022 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
reasoning, problem-solving, and multistep planning. 7. Sun J, Buys N. Early executive function deficit in preterm children
These early skills can be measured on Bayley-4 tasks and its association with neurodevelopmental disorders in
childhood: a literature review. Inter J Adolesc Med Health. 2012;
beginning in toddlerhood. Although our findings indicate 24:291–299.
that a given test task might not load on the primary factor 8. Garon N, Bryson SE, Smith IM. Executive function in preschoolers:
at one age, it is possible to do so at a different age. The a review using an integrative framework. Psychol Bull. 2008;134:
findings suggest increases in the complexity of EFs 31–60.
contributing to performance on Bayley-4 tasks with in- 9. Bayley N, Aylward GP. The Bayley Scales of Infant and Toddler
Development. 4th ed. Bloomington, MN: NCS Pearson; 2019.
creasing age of the infant and toddler.
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10. Peterson IJ, Choe DE, LeBeau B. Studying a moving target: the
These findings, along with research indicating asso- challenge and opportunity of heterotypic continuity. Dev Rev.
ciations of measures of EF in infancy with later cognitive 20202020;58:100935.
and behavioral outcomes,22,25 support the potential
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11. Willoughby MT, Blair CB, Wirth RJ, et al. The measurement of
utility of EF items from the Bayley-4 in predicting similar executive function at age 3 years: psychometric properties
criterion validity of a new battery of tests. Psychol Assess. 2010;22:
outcomes. We know that many children without early
306–317.
global development delays nonetheless display weak- 12. Cuevas K, Bell MA. Infant attention and early childhood executive
nesses in readiness at the time of school entry. It is function. Child Dev. 2013;85:397–404.
probable that this inter-relatedness of performance 13. Ball G, Pazderova L, Chew A, et al. Thalamocortical connectivity
across tasks may exacerbate deficits in EF skills in infants predicts cognition in children born preterm. Cereb Cortex. 2015:1–9.
who have been subject to brain disruption or injury, 14. Weibe SA, Sheffield T, Nelson JM, et al. The structure of executive
function in 3-year-olds. J Exp Child Psychol. 2011;108:436–452.
such as those born preterm. If different types of EFs or
15. Bayley N, Aylward GP. The Bayley Scales of Infant and Toddler
other cognitive abilities (e.g., those assessing WM, in- Development (4th ed) Technical Manual. Bloomington, MN: NCS
hibition, and visual perception) draw from a common Pearson; 2019.
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tasks. Moreover, because tasks imposing different spe- visual attention during the first two years of life. JAMA Net Open.
2021;4:e213687.
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17. Gordon L, Picciolini O, Marzocchi GM, et al. Emerging executive
from this same reservoir, infants and toddlers are less skills in very preterm children at 2 years corrected age: a composite
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ACKNOWLEDGMENTS preterm infants. Neuropsychol. 2004;18:673–678.
A special thanks is extended to Shelley Hughes, OT, Director 20. Sun J, Buys N. Planning and its relationship with frontal lobe
Portfolio Delivery & Management-Therapeutics, at Pearson for her functioning in preterm and full-term infants. Inter J Child Health
support. Hum Dev. 2012;5:325–340.
21. Mulder H, Hoofs H, Verhagan J, et al. Psychometric properties and
convergent and predictive validity of an executive function test
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