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Linguistic Outcomes Following Traumatic Brain Injury in Children

Linda Ewing-Cobbs and Marcia Barnes


Recent studies of outcome after traumatic brain injury (TBI) emphasize the adverse effect of diffuse brain injury on
linguistic development. This article reviews studies of lexical development, discourse processes, and reading in
children and adolescents with TBI. The child's developmental level at the time of injury is related to the pattern of
deficits. Young children who sustain severe TBI are particularly vulnerable to linguistic deficits at both lexical and
discourse levels. TBI in older children and adolescents preferentially disrupts higher-order discourse functions.
The contribution of deficits in fundamental processes, such as working memory and processing speed, to
linguistic outcomes requires further investigation.
Copyright 2002, Elsevier Science (USA), All rights reserved.

RAIN INJURY sustained during childhood


and adolescence has variable effects on language competence depending on a host of variables, including age at the time of injury, the
presence of focal versus diffuse brain injury, and
the developmental trajectory of specific linguistic
functions at the time of injury. Early studies of
linguistic outcomes after acquired brain injury during childhood often examined samples of mixed
etiologies and focused on categorization of specific
symptoms, j'2 More recent studies emphasize the
range of language functions potentially affected by
children with homogeneous etiologies and examine interrelationships with other cognitive functions. It is increasingly evident that linguistic outcomes vary considerably depending on the nature
of the brain insult. Linguistic outcomes are quite
favorable following perinatal and early focal insults. However, the outcome for children sustaining diffuse brain injuries early in life is significantly less favorable, suggesting less adequate
mechanisms of behavioral and neural plasticity. As
emphasized by Ewing-Cobbs et al, 3 understanding
of the consequences of brain injury in children
requires the formulation of research questions that
account for models of neural and cognitive development. For example, examination of how brain
injury in childhood affects language development
should begin with a model of language acquisition
and ask how and to what extent injury to various
neural mechanisms affects the developing language system. 4 Studies of children who sustain
perinatal focal injuries are essential for understanding how a relatively discrete lesion impacts subsequent development and the extent to which remaining tissue reorganizes and acquires a range of
representations. Lesions acquired later during
childhood following acquisition of some language
functions permit examination of both recovery (ie,
restoration of a previously acquired function) and

reorganization of neural structures and behavioral


functions (ie, shifting) of a function to an alternative area of the brain or using different strategies to
accomplish a specific goal). 5
Age at the time of brain injury may show striking relationships with the eventual level of outcome in varied skill domains. Hebb 6 hypothesized
that the earlier a brain lesion was sustained, the
greater the potential impact on later development
because brain injury was likely to adversely affect
the acquisition of new skills. Rutter 7 and EwingCobbs et al s extended Hebb's formulation to include predictions of the impact of brain injury on
developing as compared to established skills. They
inferred that skills in a rapid stage of development
might be most vulnerable to disruption by brain
injury; conversely, skills that were well-consolidated might be more resistant to disruption. Dennis 9 developed a heuristic for examining age-related changes after brain injury during childhood.
Skills were divided into three levels of maturation:
emerging (not yet functional), developing (partially acquired but incompletely functional), and
established (fully acquired). Within this frame-

From the Department of Pediatrics, University of Texas


Houston Health Science Center, Houston, Texas; and the Department of Psychology, Hospital for Sick Children and the
Department of Pediatrics, University of Toronto, Toronto, Ontario.
Preparation of this article was supported in part by NIH
Grants RO1 NS 29462, RO1 NS 21889, RO1 HD 27597, U.S.
Department of Education Grant H133B40002, PO1 HD35946,
and Project Grant from Ontario Ministry of Health and the
Ontario Mental Health Foundation.
Address reprint requests to Linda Ewing-Cobbs, PhD, Department of Pediatrics, University of Texas-Houston Health
Science Center, 7000 Fannin-UCT 2401, Houston, TX 77030.
Copyright 2002, Elsevier Science (USA). All rights reserved.
1071-9091/02/0903-0006535.00/0
doi:l O.1053/spen.2002.35502

Seminars in Pediatric Neurology, Vol 9, No 3 (September), 2002: pp 209-217

209

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work, skills can be evaluated in relation to the


normal age of acquisition, the order of acquisition
relative to other related skills, the rate of skill
acquisition, the strategy for implementing a skill,
the degree of mastery or final level of competence,
and the maintenance of specific skills at various
ages. Developmental frameworks of this nature
imply that language outcomes after brain injury
ought to be sensitive to the repertoire of language
skills that the child has acquired, is currently acquiring, and has yet to acquire at the time of injury
as well as the effect that particular brain injuries
have on those developed and developing skills.
Comparison of children with focal and diffuse/
multifocal brain injuries arising from different origins suggests potentially interesting dissociations
in the acquisition and maintenance of cognitive
functions that reflect the pathophysiology of each
disorder. Recent prospective studies of unilateral
focal lesions include children with single lesions of
vascular origin verified by neuroimaging studies. 1~ Children with ongoing seizure disorders
are typically excluded to minimize possible diffuse
brain injury or progressive lesions. In contrast, the
deficits commonly observed after traumatic brain
injury (TBI) reflect the combination of diffuse and
multifocal cerebral damage. The diffuse injury
consists of the cumulative effects of diffuse axonal
injury, hypoperfusion, excitotoxic cascades of neurotransmitters, and chronic alterations in neurotransmitter functions. 12-14 Focal injury associated
with TBI occurs most often in prefrontal regions
with concomitant disruption of executive functions. 15,16
Developmental outcomes vary considerably depending on the presence of focal versus diffuse
brain injuries. 17'18 Children with focal lesions benefit from substantial reorganization of function,
suggesting that the unaffected neural substrate is
able to mediate abilities by expansion of the functioning of a given region, retraction of functioning
within regions, or a shift as a different region
mediates the ability. 5 However, this reorganization
is exquisitely sensitive to age at injury, that is,
perinatal lesions of this type produce the best
reorganization of neural and behavioral functioning; similar focal lesions in older children may
produce more pronounced behavioral deficits reminiscent of those observed after similar focal lesions in adults. 19 In contrast, brain lesions from a
variety of causes producing diffuse neuronal in-

EWING-COBBS AND BARNES

jury, including TBI, infectious disease, and cranial


irradiation, typically result in the opposite pattern
of outcomes. That is, more adverse outcomes are
observed in younger children than in older children. 16,2o-26
The remainder of this article focuses on describing linguistic outcomes in children with a particular form of diffuse brain injury, TBI. The article
will (1) describe linguistic outcomes in children
and adolescents who sustain TBI in the areas of
lexical development, narrative processes, and reading; (2) where possible, relate these linguistic outcomes to features of the brain injury; (3) discuss
the effect of the child's developmental level at the
time of injury on different linguistic outcomes; and
(4) consider how fundamental cognitive processes
commonly affected by TBI might influence these
linguistic outcomes.
LINGUISTIC OUTCOMES AFTER TBI IN
CHILDREN

The study of components of linguistic function


in children with TBI who are injured in early
versus later childhood illustrates some of the ways
in which different outcomes are related to language
development before the injury as well as to the
greater vulnerability of the immature brain to the
effects of diffuse injury. Disorders involving diffuse and focal brain insults acquired at different
points during development provide the opportunity
to examine questions such as how age at injury
influences recovery of previously acquired skills,
acquisition of new skills, maintenance of skills
over time, and acquisition of later-developing
skills. When examined longitudinally, outcomes in
clinical populations can be characterized according
to developmental models characterizing the onset
and development of specific abilities. The timing
of skill onset can be depicted as normal or delayed.
Deficit and lag constructs refer to the degree of
skill development. Deficit implies that the maximal
performance was below normative levels, whereas
lag implies a skill that was originally deficient
"caught up" over time to a normal level. 27"2s

Lexical Comprehension and Production


TBI infrequently produces significant aphasic
disturbances in children regardless of age at injury.
However, more subtle comprehension and expression deficits at the lexical or word level are seen,
particularly in those children who sustain their

LINGUISTIC OUTCOMES FOLLOWING TBI

injury in infancy or the preschool years. Language


outcomes in studies of children injured before
school age support a model showing initial deficit,
variable recovery, and a stable persistent deficit
over time consistent with a deficit model. Young
children with severe injuries have greater difficulty
than children with mild to moderate injuries on
measures of expressive language early in recovery.
Although significant recovery of expressive abilities has been noted within the first year after injury,
by 2 years after early TBI, significant deficits in
both receptive and expressive language persist. 2~'24
In contrast to the studies of children injured in
infancy and the preschool years, the rate of deficits
in lexicaMevel functions (eg, visual naming, describing the function of objects, sentence repetition, and word fluency) in school-aged children
and adolescents with moderate to severe TBI is
much lower in the early stages of recovery, affecting only about 20% of these samples. 29'3~ Over
longer recovery periods, youth with severe injuries
show mild deficits on standardized measures of
global receptive and expressive linguistic functioning as well as in specific areas of linguistic function including expressive naming 3L'32 and word
fluency. 33'34 However, other lexical-level functions, such as visual confrontation naming, tactile
naming, and sentence repetition appear to be unaffected in the longer term for children with severe
TBI who sustain their injuries after the preschool
years.3 ~,33,35

Discourse Processes
Although marked deficits on tests of word- and
sentence-language affect only a small proportion
of older children with severe TBI, these children
often have striking discourse deficits and fail to use
language to communicate effectively. 36 Not surprisingly, children injured at a younger age who
have deficits at the lexical-level also have difficulties in discourse-level language. We first discuss
studies that examine some of the components of
discourse function (eg, inferencing). We then discuss studies of discourse competence that examine
a child's ability to bring several linguistic and
general cognitive abilities to bear in understanding
and producing discourse in natural language contexts, such as story telling.
Competence in discourse is dependent on a complex set of cognitive skills incorporating aspects of
language, semantic memory, working memory,

211

and world knowledge. 37 In addition to mastery of


syntax, lexicon, and phonology, discourse accesses
semantic-pragmatic knowledge associated with
telling a story or participating in a conversation. 38
Studies of some of the components of discourse
processing in children several years after TBI reveal semantic-pragmatic language problems including difficulty interpreting ambiguous sentences and metaphors, drawing inferences, and
producing short discourse segments using specific
parts of speech. 36"39 We discuss one of these components of discourse, inferential processing, below.
The ability to make inferences is important for
both oral discourse comprehension and comprehension of written text. Often, what is heard or
read cannot be understood unless an inference is
made to "fill in the gaps." For example, we often
have to integrate our world knowledge with what
we are hearing or reading to understand the message that is being communicated. Likewise, we
must often link what we are heating or reading
with something the speaker or writer said a few
sentences back. Children with TBI have deficits on
standardized discourse tasks that require them to
make inferences about social scenarios. 36 Experimental investigations of inferencing in children
with TB139 have been important for identifying the
sources of these difficulties in inferential comprehension. Children with severe TBI were similar to
controls in their ability to understand literal aspects
of a story, which is consistent with the findings
reported earlier, that children with severe injuries
have preserved lexical- and sentence-level processing. In contrast, children and adolescents with
severe TBI had considerable difficulty making inferences to help them understand a story. This was
the case even when the children with TBI could be
shown to have both the world knowledge needed to
make an inference and the causal reasoning abilities required to make links between two pieces of
information. Their pattern of performance suggested two reasons for the inferencing deficits:
they were inefficient at holding different sources of
relevant information in working memory long
enough to make inferences, and they had problems
knowing when an inference was required to understand what they heard. Difficulties in inferential
comprehension in children with severe TBI might
be related to more primary deficits in aspects of
executive function, such as working memory and
metacognition or comprehension monitoring.

212

These higher-order pragmatic-semantic deficits


likely also contribute to the communicative, social,
and academic skill deficits that characterize the late
outcome of children with s e v e r e T B I . 37'40'41
Another approach to the study of linguistic outcomes after TBI is to examine language comprehension and expression in more natural discourse
contexts, such as story-telling and conversations.
Children with severe TBI tell and retell stories that
are short and semantically impoverished. Despite
producing semantically impoverished stories,
some components of their discourse, such as syntactic complexity and narrative fluency, appear
intact. 42-44 Some studies have reported a dissociation between sentence-level and textual-level cohesion in the narratives of children with TBI,
suggesting that these children were able to relate
information within sentences, but that they had a
great deal of difficulty relating or linking information ac~;oss sentences in the stories they produced. 44 These findings are similar to those reported for story comprehension and inferencing
above. That is, children with severe TBI seem to
have problems linking up information across sentences or ideas within a discourse whether they are
listening or speaking. Moreover, children with severe TBI consistently show significant discourse
deficits in areas including recalling propositions
necessary to convey the story content, preserving
the gist of the story, sequencing the narrative
action, 43-45 and summarizing and inferring the central meaning. 46 So, although the narrative reproductions of children with severe TBI show relative
preservation of narrative economy, syntactic complexity, and local or sentence-level cohesion, their
semantic content is significantly deficient.
Because there is a developmental sequence in
the acquisition of story-telling skills, narrative discourse is an area that lends itself to investigation of
potential age at injury effects on the development
of linguistic skills. For example, early narratives
emerge around age 2, when a child can refer to a
past event; at age 3, the child can sequence two
actions; by age 4, the child can convey more than
two events involving multiple actions; by age 5,
the basic narrative structure is attained and the
child may tell stories with beginnings, action sequences, and an ending; at ages 8 to 9, causal
relations and a central theme emerge. 45 If skills
that are developing rapidly are more vulnerable to
disruption by brain injury, then the development of

EWlNG-COBBS AND BARNES

narrative discourse skills may be particularly sensitive to the effects of TBI sustained during the
preschool and early elementary years. The few
available studies of discourse-level language in
children injured in infancy and the preschool years
do tend to show greater deficits in discourse outcomes than those children injured at an older age.
Available data suggest that in comparison to TBI
sustained in older children and adolescents, TBI
sustained during the preschool years is related to
less adequate development of narrative disc o u r s e . 45"47 However, the influence of developmental stage at the time of injury upon discourse
competence is unclear. Although children injured
at younger ages perform less adequately on some
discourse tasks than children injured at older ages,
the relationship of age at injury and stage of narrative development to the pattern of discourse
outcomes requires further investigation.

Reading
Reading is a linguistic skill that is critical for
both academic and vocational success, though it
has received less attention than other aspects of
language outcome after childhood TBI. Reading is
a skill that has a protracted developmental course
and that is made up of several component skills
that are acquired at different ages. In preschoolers,
the development of vocabulary, phonologic awareness, phonologic memory, and rapid naming skills
are related to the later acquisition of word decoding. 48-5~In the early primary grades, children learn
the alphabetic principle and strategies for decoding
words accurately at the same time as language
skills related to later reading competency are rapidly developing. Reading fluency and language
skills, such as vocabulary and inferential processing, continue to develop into the later grades. The
unfolding of these developmentally staggered
reading and reading-related skills across a broad
age range makes reading an ideal skill for agebased comparisons in disorders where age of insult
varies, such as TBI. By comparing components of
reading in children who are injured at different
points in their development, we can address
whether diffuse acquired brain injuries affect the
acquisition or maintenance of particular reading
and reading-related skills.
Barnes et a123 studied the reading of children
who sustained TBI at different ages and of similar
severity an average of 3 years after the injury.

LINGUISTIC OUTCOMES FOLLOWING TBI

Children were grouped according to whether their


injury was sustained: (1) before schooling and the
formal instruction of reading, or before age 6; (2)
during the rapid phase of learning how to read,
which corresponds to the early primary grades; and
(3) after basic decoding skills were acquired, by
studying students injured in the intermediate to
senior elementary grades. Sustaining TBI before
the onset of formal instruction in reading was a
significant risk factor for reading difficulties. The
poorest word decoding outcomes were obtained for
the children injured at the youngest ages before
learning to read, and the next poorest for children
injured at a time when they are rapidly acquiring
reading skills, but when those skills may not yet be
consolidated. TBI seemed to have less effect on
maintenance of word decoding, that is, children
who were injured after they had acquired worddecoding skills did not lose the ability to decode or
read words. Although adolescents did not show
deficits in word decoding, they had less adequate
development of reading comprehension, which is
not surprising, given what the effects of severe TBI
on discourse functions as discussed earlier.
In a longitudinal study, Ewing-Cobbs et a151
prospectively evaluated the development of reading abilities from the time of injury until 5 to 8
years after TBI. Using growth curve analyses, they
examined the rate of change in age-standardized
reading scores across the follow-up interval in
relation to age at injury and the severity of TBI.
Word decoding scores increased more over time in
adolescents than in children ages 5 to 10 at the time
of injury. By 5 years after the injury, the youngest
children with severe TBI had the lowest word
decoding scores of any age or severity groups.
Although the mean scores remained in the average
range, the youngest children showed less adequate
development of word decoding skill over time.
Despite declines in word decoding competence,
younger children did not show concomitant decreases in comprehension scores. In contrast, reading comprehension scores tended to be lower in
adolescents than children across the extended follow-up.
Diffuse brain injuries appear to affect the acquisition of word decoding skills in young children
and reading comprehension skills in older children
and adolescents. Thus, relatively diffuse injuries
acquired early in development may interfere with
the normal developmental trajectory of learning of

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skills, such as reading, but may not affect skill


maintenance once the skill has been learned and is
better consolidated. These findings on reading in
children with TBI are in keeping with Hebb's 6
notion that brain injuries affect learning through
interfering with the acquisition of new skills.
One aspect of reading that is significantly affected by TBI, but which has not yet been studied
with respect to age at injury, is reading speed or
fluency. Children with TBI have deficits in reading
speed or fluency even when their word decoding
accuracy is comparable to controlsY Some models
of reading posit that reading speed is causally
related to reading comprehension; slow word decoding produces a reading "bottleneck" such that
words and sentences cannot be integrated quickly
enough to understand what has been read. Consistent with these models of reading, slow word
decoding in the TBI group was related to their
deficits in reading comprehension. The fact that
children with TBI have dual deficits in skills related to reading comprehension (ie, they are slow
readers and they have difficulties in discourse processing as reviewed above) suggests that they are
at significant risk for reading comprehension disability.

Influence of Focal Lesions on Linguistic


Outcomes
Focal left hemisphere injury is related to some
linguistic deficits after TBI. Ewing-Cobbs et a132'44
showed that children who sustained TBI producing
focal left hemisphere findings on acute CT with
concomitant impairment on baseline measures of
expressive and receptive language function, had
persistent linguistic deficits when examined 6
months to several years after the injury. In comparison to children with TBI of comparable severity without initial language impairment, the children with focal left hemisphere injuries had slowed
naming of pictured objects and reduced word retrieval. In the same children, marked disruption in
narrative discourse was evident.
In a subsequent study by Brookshire et al, 42
discourse competence was significantly related to
the severity of TBI as indicated by Glasgow Coma
Scale scores. However, narrative competence was
not related to any MRI findings, including the
locus of focal lesions, volume of lesions, or the
degree of cerebral atrophy. Thus, lexical-level impairments after severe TBI are related to focal left

214

hemisphere brain injury, whereas impairments in


narrative discourse are not so clearly related to
specific features of the brain injury.
Focal aspects of an acquired diffuse brain injury
may also be important in determining outcomes in
reading and other areas. Focal left hemisphere
injury is related to the reading outcomes in childhood TBI samples. 23"52 Whether focal injuries interact in some manner with age at injury to predict
developmental trajectories for reading and readingrelated skills, however, is a question that has not
been addressed, to date, in these studies of TBI in
childhood. Frontal lobe contusions have also been
associated with poor understanding of language
associated with mental states and intentions, especially in children injured at younger ages. 53
Clearly, additional research is needed to clarify the
relative contributions of focal and diffuse brain
injury sustained at different ages to the development of specific linguistic functions.

Relationships of Linguistic Deficits and


Executive Functions
Complex linguistic behaviors are dependent on
the level of functioning of other cognitive systems.
Cognitive variables, including speed of processing,
working memory, and metacognition, clearly influence performance on a plethora of linguistic tasks.
For example, Turkstra and Holland 54 noted that
syntactic comprehension was substantially affected
by task characteristics, such as working memory
load. When the working memory load of items was
reduced, adolescents with TBI successfully demonstrated understanding of a variety of syntactic
forms that they could not demonstrate under high
memory load conditions. Similarly, in the inferencing study discussed above, inferential processing
was not different from that in normally developing
children when the working memory load was reduced. 39
In one study that explicitly tested the relationship between executive processing and language
variables, Brookshire et a142 examined the interrelationship of narrative discourse variables and selected neuropsychologic variables. Recall of core
story elements was related to the adequacy of
nonverbal problem-solving and verbal fluency.
There were no significant relationships between
discourse variables and any measures of declarative memory. This is in keeping with previously
discussed findings on story comprehension in

EWlNG-COBBS AND BARNES

which children with severe TBI were as able as


controls to answer questions about literal story
content (tapping declarative memory), yet had significant difficulty answering inference questions. 39
Performance on reading tasks may also be disrupted by deficits in fundamental skills (such as
processing speed) or in executive skills (such as
working memory), and metacognitive processing
(such as comprehension monitoring). Relationships between TBI, reading rate, and reading comprehension underscore the importance of considering the impact of fundamental variables, such as
processing speed, that may affect performance
across a number of linguistic and nonlinguistic
domains. To understand the reading comprehension deficits of children with TBI, model-driven
studies will need to investigate not only readingspecific skills such as word decoding, but also
other cognitive and executive competencies such
as processing speed, working memory, and metacognitive monitoring.
SUMMARY AND FUTURE DIRECTIONS

Diffuse cerebral injuries, such as those produced


by TBI, significantly affect linguistic outcomes and
have the most devastating and persistent effects in
children injured in infancy and the preschool years.
Language outcomes after severe TBI fit a deficit
model; the linguistic skills that are affected by
severe TBI often do not attain normal developmental levels even several years post-injury. This pattern stands in contrast to language outcomes in
children with perinatal focal unilateral lesions who
show early delays in lexical comprehension and
production following both left and right hemisphere injury, 11'55'56 followed by a considerable
amount of catch-up by the preschool years. 11.57
In previous decades, the prevailing view that
young children recovered well from early brain
insults resulted in limited emphasis on assessment
and intervention. Because young children appear to
be particularly vulnerable to the effects of diffuse
brain insults, assessment must target skills that
emerge at specific ages and must evaluate the
adequacy of maintenance and further development
of these skills over time. For example, assessments
might emphasize phonological awareness and lexical development in younger children and prioritize
inferencing and comprehension processes for older
children and adolescents. To minimize the impact
of deficits in preschool-aged children, early inter-

LINGUISTIC OUTCOMES FOLLOWING TBI

215

vention in basic speech and language may be


required. Clearly, assessment of skills related to
early reading competence is essential to detect
weaknesses in lexical, phonological, or fluency
skills necessary for appropriate development of
reading.
Regardless of age at injury, TBI has the most
striking adverse effects on semantic-pragmatic
rather than lexical language functions. Narrative
discourse in children with TBI is characterized by
adequate syntactic complexity and fluency. However, deficits are prominent in semantic-pragmatic
areas involving recalling semantic content of stories, preserving the gist o f the story, and inferring
meaning. Not surprisingly, these discourse-level
deficits occur not only in oral language areas, but
also in reading comprehension. Assessment approaches should initially assess whether any problems are present at lexical and sentence levels that
may require intervention to strengthen the foundation for higher-order linguistic processes. If deficits
are present at the discourse level, components of
discourse, such as inferencing, understanding of
nonliteral language, and social language, must be
evaluated and addressed.
Alterations in fundamental cognitive skills, such
as processing speed and efficiency of working
memory, and executive skills, such as metacognitive processes, may contribute to deficits in developing language skills. Therefore, as part of a c o m -

prehensive assessment, children with TBI should


also receive periodic evaluation that includes both
linguistic and executive functioning to identify
specific areas of concern. For example, if working
memory is poor, then intervention may also need to
address strategies to compensate for these fundamental deficits. Deficits in processing speed may
affect both oral and written discourse comprehension. To address processing speed weaknesses affecting reading, intervention might include strategies for enhancing comprehension. To increase
fluency at the word level, strategies such as preteaching vocabulary and rereading text may be
helpful. To increase retention and integration of
information, semantic content could be reinforced
using strategies, such as rereading, summarizing
paragraphs or other units of text, or taking notes to
facilitate retention o f information and integration
of ideas.
To guide assessment and intervention initiatives,
future studies of linguistic outcome after TBI in
children will need to carefully investigate interrelationships between the child's repertoire of language skills at the time o f injury, the developmental trajectory of specific linguistic skills following
the injury, the impact of focal and diffuse brain
lesions at different ages, and in the integrity of
fundamental cognitive abilities that may influence
the development of complex linguistic skills
throughout the course o f development.

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