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A Functional Magnetic Resonance Imaging Study of Left Hemisphere Language Dominance in Children
Lyn M. Balsamo, MA;
Benjamin Xu, PhD;
Cecile B. Grandin, MD, PhD;
Jeffrey R. Petrella, MD;
Suzanne H. Braniecki, MA;
Teresa K. Elliott, PhD;
William D. Gaillard, MD
Arch Neurol. 2002;59:1168-1174.
ABSTRACT
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Background Functional magnetic resonance imaging is a noninvasive method of assessing
language dominance in a pediatric population.
Objective To determine the pattern of receptive language lateralization in healthy
children.
Design We used functional magnetic resonance imaging to assess an auditory
language task in 11 children (7 girls, 4 boys; mean age, 8.5 years). Participants
alternately rested and listened to descriptors of nouns presented auditorily,
naming the object described silently. Asymmetry indices ([(left - right)/(left
+ right)]) were calculated for a priori–determined regions of interest.
Results The results showed strong activation bilaterally, with greater activation
on the left in the superior and middle temporal gyri. Other areas of activation
included the cuneus, the left inferior temporal gyrus, the prefrontal area,
and the left fusiform and lingual gyri. Regions of interest analysis of individual
scans showed additional activation in the left frontal lobe. Asymmetry indices
showed strong left lateralization of the inferior frontal gyrus, middle frontal
gyrus, and the Wernicke region.
Conclusions Hemispheric lateralization was clearly demonstrated in 8 children. As
in adults, left hemisphere lateralization of receptive language is present
at age 8 years.
INTRODUCTION
IN MOST ADULTS, language function is primarily subserved by the left
hemisphere, as indicated by various methods of assessment: lesions studies,1 the intracarotid sodium amobarbital procedure (IAP),2 electrocortical stimulation,3
and functional neuroimaging.4-5
However, the question remains as to whether left hemisphere specificity for
language is innate or whether dominance develops as language is acquired.
Findings of anatomical asymmetries in the left planum temporale, or
auditory association area, of neonates and infants,6-7
in addition to functional asymmetries in infants favoring the left hemisphere,8-10 suggest that a left
hemispheric specialization for language is present at birth. On the other
hand, language has been found to develop to within the normal range on standardized
measures in those with unilateral injury to the left hemisphere before the
age of 6 months.11 These findings lend support
to the equipotentiality hypothesis that proposes the equal capacity of either
hemisphere to subserve language function. Moreover, infants and children do
not suffer the same neurological consequences as do adults with analogous
lesions of the left hemisphere,12-13
suggesting the developing brain's functional plasticity. However, despite
evidence of plasticity, other investigators have found language deficits after
early left hemisphere insult.14
In the absence of brain injury, there are 2 possible explanations for
the development of left hemisphere language dominance: (1) Language is solely
supported by the left hemisphere from birth; or (2) Language is supported
by both hemispheres at an early age but becomes increasingly consolidated
in the left hemisphere as language competency increases. The critical window
of language development and neural plasticity has been debated to some extent,
with some investigators proposing that it extends to puberty15-16
and others asserting a more conservative age of 5 or 6 years.17
Functional magnetic resonance imaging (fMRI) has been shown to be an
effective means of assessing laterality, with numerous advantages over the
more invasive IAP procedure in terms of its safety, noninvasiveness, replicability,
and ability to apply to a nonclinical population.18-21
Review of the adult imaging literature in the area of auditory language paradigms
reveals several consistent findings: (1) The presentation of auditory lexical
stimuli, when contrasted with the absence of sounds, activates the superior
temporal gyrus (STG) bilaterally, extending beyond the primary auditory cortex.
Activation is consistently more extensive on the left, suggesting a specificity
for language processing in this area22-25;
and (2) Semantic processing of auditory stimuli, such as listening to speech
or performing a semantic decision task, appears to activate a network, including
most consistently although not exclusively, the left inferior frontal gyrus
(IFG),22, 26-29
the left middle temporal gyrus (MTG),22, 26, 30-31
and the left temporoparietal area.23, 26-28,31
Hertz-Pannier et al20 demonstrated the
efficacy of fMRI to identify language cortices in the frontal lobes of children
and adolescents with epilepsy using a word generation task, and more recently,
Gaillard et al32 provided similar evidence
with healthy children using a reading task. There have been a small number
of fMRI studies of receptive language conducted with children. In a study
of six 6- to 10-year-old children (mean age, 8 years), Ulualp et al33 used a passive story listening task that activated
frontal and temporal areas, consistent with adult studies. They did not find
a pattern of lateralization in primary and secondary auditory cortices. However,
their paradigm did not require an active response and perhaps did not sufficiently
provoke activity in the language cortex. Studies from Booth and colleagues34-35 provide inconsistent conclusions.
In their first study of auditory comprehension, they found evidence for bilateral
activation. Six children (aged 9-12 years) listened to sentences ranging in
complexity, after which they were required to identify elements of the sentence.
The authors found bilateral activation of the STG and IFG regions but conjectured
that bilateral activation may have been a product of task complexity, which
has been shown to increase activation in homologous areas of the right hemisphere.36 However, in a second, similar study, in which an
alternate method of calculating asymmetry indices was used, left lateralization
was found.35 Given these differences in paradigms
and in analysis, it is difficult to draw conclusions about language representation
in children of that age.
Our study was designed to assess language laterality in normally developing
8-year-old children using fMRI and an auditory language task. The auditory
paradigm implemented was expected to produce activation patterns of the IFG,
MTG, and STG. The task was designed to require a response, thus ensuring a
degree of higher-order processing.
SUBJECTS AND METHODS
SUBJECTS
Participants were 11 children (7 female, 4 male). They ranged in age
from 7.3 to 9.6 years (mean [SD], 8.5 [0.9] years). Participants were recruited
from the community via posted advertisements. They were paid for their participation.
All participants had normal neurologic examination results, normal structural
MRI results, and were healthy. All were right-handed as assessed by a modified
version of the Edinburgh Handedness Inventory,37
using 7 of the 10 original items most suitable for children. All children
had a handedness score of 100, indicating strong preference for the right
hand. If a participant had a diagnosis of learning or attentional difficulties,
or English was not his or her first language, he or she was excluded from
the study. Testing administered to 10 of the children subsequent to their
scan indicated that, on average, these children performed in the high average-to-superior
range on standardized measures of expressive naming, reading, and cognition.
Children received a tour of the MRI facilities prior to scanning. This study
received prior approval by the National Institutes of Neurological Disorders
and Stroke institutional review board. Written parental consent and child
assent were obtained.
PARADIGM
Stimuli for the Auditory Response Naming task consisted of auditorily
presented several-word phrases.27 The participant
silently named the object the phrase described. For example, the correct response
to the phrase "long yellow fruit" was "banana." Covert responses were used
to minimize motion artifacts. Descriptions of age-appropriate items were generated
from the Peabody Picture Vocabulary Test,38
the One-Word Expressive Picture Vocabulary Test,39
and the Boston Naming Test.40 Seven clues were
presented in each 32-second epoch (interstimulus interval of 0.5 seconds).
The individual had approximately 4 seconds to listen and to respond to the
stimulus. Task difficulty was adjusted based on age so that participants would
respond accurately approximately 85% of the time. The naming task alternated
with a control task, in which the background noise of the scanner was present;
the participant was instructed to rest during these periods. There were 6
cycles of the rest and task conditions for total task duration of 6 minutes
24 seconds. The same speaker delivered the stimuli binaurally over the scanner
intercom into headphones worn by the participant. The headphones attenuated
the noise of the scanner. A test run in which a sentence was read to the participant
and the participant was asked to repeat it was conducted to ensure that the
participant could adequately hear the stimuli.
IMAGING PARAMETERS
Images were collected with a 1.5-T General Electric Signa scanner (General
Electric, Milwaukee, Wis) equipped with a birdcage radio frequency coil. The
participant's head was stabilized with a forehead strap and foam padding.
Functional images were acquired with a single-shot, blipped, gradient-echo
echo-planar sequence (EPI) (echo time [TE] = 40 milliseconds, field of view
[FOV] = 22 cm x 22 cm, acquisition matrix = 64 x 64). Subsequent
to the collection of the functional images, anatomical images were acquired
using a 3-dimensional fast spin-echo gradient sequence with an inversion impulse
(TE = 3.5 milliseconds, repetition time [TR] = 10.1 seconds, TI = 600 milliseconds,
flip angle = 20°, slice thickness = 5 mm, FOV = 24 cm x 24 cm, acquisition
matrix = 256 x 256, voxel size = 3.4375 mm x 3.4375 mm x
5 mm). For both the functional and structural images, the whole brain was
imaged with the collection of 20 contiguous axial images parallel to the anterior-posterior
commissure plane. Total scanning time was 18 minutes.
DATA ANALYSIS
Group Data
The data were processed and analyzed using the general linear model41 with statistical parametric mapping 99 software (Wellcome
Department of Cognitive Neurology, London, England). Prior to statistical
analysis, all images were normalized to an EPI template conforming to the
Talairach and Tournoux42 convention and then
smoothed (full width at half maximum = 8 mm3). To minimize false-positive
and false-negative results, 2 different statistical analyses were performed:
a fixed-effect design and a more stringent conjunction analysis.43 t Tests were used for all statistical contrasts of the
rest condition to the experimental condition. The fixed analysis combined
all scans of the same condition within a group. Individual voxels were significantly
activated if they survived a height threshold of P<.001
(corrected for multiple comparisons) and an extent threshold of 10 voxels.
For the conjunction analysis, individual voxels were significantly activated
only if each subject activated the identical voxel at or above a height threshold
of P<.05 (corrected). Thus, voxels not activated
in every subject were effectively eliminated.
Individual Data
Analysis of data at the individual level can be a source of additional
information. Analysis of individual participant data was conducted using a
region of interest approach. A priori regions of interest (for each hemisphere)
were drawn on raw EPI images: IFG, middle frontal gyrus (MFG), the Wernicke
area, and MTG. Analyses of individual regions were conducted using semiautomated
image-analyzing software that subtracted signal change between control and
task conditions on a voxel-by-voxel basis. A voxel was significantly activated
if it survived a threshold value of t>3.0. 44 The total number of activated voxels in each region
was automatically calculated.
Lateralization of each region was determined with the calculation of
an asymmetry index (AI). The AI for each region was calculated using the formula:
AI = [left - right / left + right], with left and right representing
the number of activated voxels in the respective hemisphere. A positive AI
(>+0.2) indicated left-hemisphere dominance and a negative AI (<–0.2)
indicated right-hemisphere dominance. Any value falling between –0.2
and +0.2 was considered to be indicative of bilateral activation.45 Two other criteria were also met to consider an AI
valid: (1) At least 4 voxels were activated in a particular region; and (2)
There was at least a 3-voxel difference between homologous regions.44
RESULTS
STATISTICAL PARAMETRIC MAPPING GROUP RESULTS
Fixed-Effect Analysis
When compared with the rest task, Auditory Responsive Naming strongly
activated the following regions bilaterally but with greater activation on
the left: MTG (Brodmann area [BA] 22 and 21), STG (BA22), inferior occipital
gyrus (IOG) (BA18), and the cuneus (BA18). There was also activation in the
cerebellum bilaterally, the left inferior temporal gyrus (ITG) (BA37), the
left fusiform gyrus (BA18), the left lingual gyrus, and the left MFG (BA9).
Some activation was found in the frontal medialis region (BA10) bilaterally
and the right superior frontal gyrus (SFG) (BA10). Table 1 presents the z score for each area of activation as well
as the number of voxels activated in the respective area. Figure 1 shows the group activation map.
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Table 1. Fixed-Effect Statistical Parametric Mapping Analysis*
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Figure 1. Statistical parametric mapping
results of the fixed-effect analysis. These select images are presented in
the neurologic convention: the left side of the picture represents the left
hemisphere. Activation in the middle temporal gyrus and superior temporal
gyrus is bilateral but is more intense and extensive on the left.
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Conjunction Analysis
The conjunction analysis in Figure 2 showed strongly lateralized and highly significant activation in
the left MTG and STG, which largely replicated the fixed-effect analysis.
Smaller homologous regions in the right hemisphere were also activated (Table 2).
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Figure 2. Statistical parametric mapping
results of the conjunction analysis. An activated voxel reflects that it was
significantly activated in each of the 11 participants. Activation is highly
lateralized to the left middle temporal gyrus.
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Table 2. Conjunction Statistical Parametric Mapping Analysis*
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REGIONS OF INTEREST RESULTS
On a subject-by-subject basis, laterality based on regions of interest
was most efficiently determined at a threshold of t
= 3 (Table 3). Mean asymmetry
indices per region revealed moderate left lateralization in each region and
are presented in Figure 3. The MFG
and Wernicke area were most strongly lateralized to the left, with asymmetry
indices of 0.43 and 0.41, respectively. Weaker lateralized activation was
found in the MTG (mean, 0.20).
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Table 3. Participant Region of Interest Asymmetry Indices and Activated
Voxels in Left Hemisphere*
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Figure 3. Mean asymmetry indices for each
region. An asymmetry index of 0.2 or greater indicates left hemisphere dominance.
IFG indicates inferior frontal gyrus; MFG, middle frontal gyrus; and MTG,
middle temporal gyrus.
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COMMENT
This fMRI study was designed to examine language laterality in children.
Results of the study revealed highly lateralized activation in the left MTG
and STG. These findings strongly indicate left hemisphere language dominance
for auditory comprehension in children between the ages of 7 and 9 years.
Group analysis showing bilateral activation of the STG, including the primary
auditory cortex, is consistent with other studies of auditory stimuli. Activation
was asymmetrical, favoring the left hemisphere, which reflects the lexical
component of the stimuli.24, 46
As anticipated, our results showed strong activation in the MTG. The MTG has
been consistently associated with semantic processing30-31,47-48
although it has also been implicated in phonological processing.24, 28, 49-50
In addition to the hypothesized areas of activation, the fixed-effect
analysis also revealed significant activation of the left cuneus, left ITG,
and bilateral prefrontal areas. Findings suggest that the cuneate region is
used in creating a visual image.27, 34, 51-52
The paradigm used in our study may be conducive to this process since each
stimulus describes a concrete noun of which one can easily generate a mental
image. Activation of the ITG and prefrontal areas (BA10) are also consistent
with previous studies that found these areas to be implicated in semantic
processing, object recognition, and working memory, respectively.22, 34, 46, 50, 53-54
Examination of the mean asymmetry indices per region showed all regions
to be lateralized to the left hemisphere, providing additional support for
the presence of strong lateralization in children as young as 7 years. Standard
deviations are large, indicating substantial subject variability in the amount
of voxels activated in each region and in asymmetry indices. Because of the
extent of anatomical variability in language cortices, the group-analysis
method of analyzing data is insufficient and at times inaccurate.55 Analysis on a case-by-case basis can provide meaningful
information. Overall, 8 of the 11 participants showed clear evidence of left
hemisphere language dominance. Two of the remaining children expressed bilateral
activation, and one child's scan was nondiagnostic. With the use of additional
scans and alternate language paradigms, more conclusive evidence of hemispheric
dominance was provided for 2 participants.
The group analyses did not produce any significant activation in the
IFG as predicted; however, in the individual analyses, IFG and/or adjacent
MFG activation was observed in most participants. There are several technical
issues that pertain to the acquisition and analysis of child-specific data
that may contribute to these conflicting findings.32
Many of these technical issues derive from anatomical differences between
children and adults. For example, children's brains are smaller,56
partly due to the process of myelination and synaptic pruning, which is not
complete until adolescence.57 Myelination proceeds
from posterior (occipital) to anterior (frontal) brain regions; thus, the
frontal lobes may be particularly susceptible to distortion since they are
less developed than the temporal lobes in the child brain.58
Furthermore, there is substantial individual variability in the location of
language cortices.59 Distortion created when
normalizing a child-size brain into a standard stereotactic space based on
an adult-size brain, in conjunction with normal individual variability, may
eliminate consistent areas of frontal lobe activation across individuals.
Thus, an adult-based model may not be optimal (although will be used until
a pediatric atlas becomes available). Finally, we speculate that variability
in location of frontal lobe activation may reflect the use of different word-finding
strategies among children.
Two fMRI studies of auditory comprehension in children have found predominantly
bilateral activation.33-34 Consistent
with these studies, analysis of our data at the individual level showed similar
areas of activation in the temporal cortex, the IFG, and the prefrontal area.
However, our study differed substantially in terms of lateralization. We found
strong lateralization in the left hemisphere for the Auditory Responsive Naming
paradigm. There may be a number of reasons for this difference. First, our
sample size was larger than the other child studies and the age range more
restricted. Second, our task differed from the others in that it was not overly
difficult nor was it a passive task, as it required covert responses. Furthermore,
each study used a different auditory language comprehension paradigm. Finally,
Booth et al34-35 and Ulualp et
al33 used alternative methods from those used
in our study to calculate laterality. Different analyses may affect outcome.
For example, the earlier study by Booth et al34
calculated correlations between percentage of voxels activated in each hemispheric
region but when similar data were examined with an analysis of variance using
percentage of activated voxels in hemispheres and regions as independent variables,
left lateralization was found.35 The selection
of the formula implemented in our study was based on its correspondence to
Wada testing.19
In comparison with an analogous study conducted with 24 adults,60 there were no differences found between the number
of activated voxels within regions or in asymmetry indices. In other words,
on an identical listening comprehension task, children and adults show highly
similar patterns in the extent of activation and degree of lateralization.
In conclusion, there are several limitations of this study necessary to address.
First, we used a small sample of children; therefore, broad conclusions are
difficult to make. Second, language and cognitive testing indicated that these
children performed in the high average to superior range; thus, it is possible
that highly lateralized language in children of this age is partially a product
of their substantial language and cognitive capacities. Finally, because we
did not obtain behavioral data, we have no concrete evidence that the children
were actually performing the task as instructed. However, the consistency
of activation patterns across participants suggests task compliance.
This study used fMRI to demonstrate left hemispheric language dominance
of auditory comprehension in normally developing 8-year-old children. At this
age, children show a lateralized pattern highly similar to that of adults.
Our data provide preliminary neuroimaging evidence in support of those anatomic,
evoked response potential, and early unilateral injury findings that suggest
early left hemisphere language lateralization.
AUTHOR INFORMATION
Accepted for publication January 31, 2002.
Author contributions: Study concept and design (Dr Grandin, Ms Braniecki, and Drs Elliott and Gaillard);
acquisition of data (Mss Balsamo and Braniecki and Drs Xu,
Grandin, Petrella, and Gaillard); analysis and interpretation of data (Ms Balsamo and Drs Grandin, Elliott, and Gaillard); drafting
of the manuscript (Ms Balsamo and Dr Gaillard); critical
revision of the manuscript for important intellectual content (Drs Xu, Grandin, and Petrella, Elliott, and Gaillard and Ms Braniecki);
statistical expertise (Drs Xu and Gaillard); obtained
funding (Dr Gaillard); administrative, technical,
and material support (Drs Xu, Grandin, Petrella, and Gaillard
and Ms Braniecki); study supervision (Drs Elliott
and Gaillard).
This study was supported by grant K08-NS1663 from the National Institute
of Neurological Disorders and Stroke (NINDS), Bethesda, Md; the Epilepsy Research
Branch, NINDS; and a grant from the Board of Lady Visitors, Children's National
Medical Center, Washington, DC.
We thank William Theodore, MD, for his continued support and for making
the Epilepsy Research Branch resources available. We also thank Suzanne Reigle,
BA, for her help in preparing the manuscript.
Corresponding author and reprints: William D. Gaillard, MD, Department
of Neurology, Children's National Medical Center, 111 Michigan Ave NW, Washington,
DC 20010 (e-mail: gaillardw{at}ninds.nih.gov).
From the Department of Neurology, Children's National Medical Center,
George Washington School of Medicine, Washington, DC (Mss Balsamo and Braniecki
and Dr Gaillard); Epilepsy Research Branch, National Institute of Neurological
Disorders and Stroke, National Institutes of Health, Bethesda, Md (Mss Balsamo
and Braniecki and Drs Xu, Grandin, Petrella, and Gaillard); and American University,
Washington, DC (Ms Balsamo and Dr Elliott).
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