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To cite this article: Haeme R. P. Park , Gjurgjica Badzakova-Trajkov & Karen E. Waldie (2012) Brain activity in
bilingual developmental dyslexia: An fMRI study, Neurocase: The Neural Basis of Cognition, 18:4, 286-297, DOI:
10.1080/13554794.2011.588182
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NEUROCASE
2012, 18 (4), 286–297
The aim of this study was to identify the neural substrates of an adult English-German bilingual with dyslexia (in
both languages) during lexical decision-making using functional magnetic resonance imaging (fMRI). A lexical
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decision task with five conditions in a block design was employed (nonverbal shape judgment, lettercase judgment,
regular word judgment, irregular word judgment, and nonword judgment), and the activation was compared to a
non-dyslexic control bilingual and a control monolingual participant. Both of the control participants matched the
dyslexic bilingual BK on age, sex, IQ, handedness, and education level. Results indicated that the bilingual adult
with dyslexia was strongly right lateralized for stimuli that required phonological processing, a profile that differed
particularly from the activation observed from the monolingual participant. These results are consistent with the
idea of increased activation (mostly in the right hemisphere) during linguistic tasks in adults with dyslexia and in
late proficient bilinguals relative to monolinguals. Findings also suggest that the additional activation observed in
both of the bilinguals are similar, suggesting that these effects are not additive in the dyslexic bilingual.
Reading is a complex cognitive task which is Coltheart, 2001). The lexical component works
acquired slowly throughout childhood and requires by matching the word to the orthographic lex-
explicit teaching. To read and write well, a per- icon of the individual, which allows the reader
son needs orthographic knowledge, which involves to understand irregular and regular words. The
the ability to translate spoken language into a non-lexical component functions by mapping
written form, as well as phonological awareness, letters to their phonological sounds, and allows
which is the ability to understand sound struc- the pronunciation of regular words and non-
tures and detect phonemes (Harm & Seidenberg, words. These specific spelling-to-sound rules
1999; Hoien, Lundberg, Stanovich & Bjaalid, 1995; are operated by phonemes, and are named
Fromkin, 2000; Joubert et al., 2004). Phonological grapheme-phoneme correspondence rules (GPC;
awareness, especially, has been determined to be Coltheart, Rastle, Perry, Langdon, & Ziegler,
one of the strongest predictors of reading ability 2001; Joubert et al., 2004). When these pro-
(Castles & Coltheart, 2004; McBride-Chang, 1995). cesses are interrupted and/or the reader is unable
Jackson and Coltheart’s Dual-Route Cascade to utilize the GPC system, he/she is thought
model (DRC) describes reading as having to have dyslexia (Demonet, Taylor, & Chaix,
two routes, lexical and non-lexical (Jackson & 2004).
Address correspondence to Karen E. Waldie, PhD, Department of Psychology, The University of Auckland, Private Bag 92019,
Auckland 1142, New Zealand. (E-mail: k.waldie@auckland.ac.nz).
c 2012 Psychology Press, an imprint of the Taylor & Francis Group, an Informa business
http://www.psypress.com/neurocase http://dx.doi.org/10.1080/13554794.2011.588182
BRAIN ACTIVITY IN BILINGUAL DYSLEXIA 287
Developmental dyslexia is a hereditary neurode- Pugh et al., 2008; Vellutino, Fletcher, Snowling, &
velopmental disorder, which is diagnosed if an indi- Scanlon, 2004).
vidual is unable to learn to read with proper facility Interestingly, the additional cortical activity
despite normal intelligence, intact senses, proper reported in adults with dyslexia during linguistic
instruction, and normal motivation (APA, 2000; tasks has also been reported in bilingual individ-
4th ed. revised, DSM-IV TR). As noted, a spe- uals (i.e., those who are able to speak and use
cific phonological processing deficit is thought to two languages). The idea that language is more
characterize the decoding impairment of the major- widely and bilaterally represented in bilinguals
ity of individuals with dyslexia (Demonet et al., has been investigated using a range of techniques.
2004). Their ability to sound out a word by using These include cortical stimulation (Ojemann &
the GPC rule system is highly compromised, and Whitaker, 1978), electroencephalography (Genesee
the individual is unable to fluently read pronounce- et al., 1978), tachistoscopic and dichotic-listening
able nonwords such as blint. The underlying neural (as reviewed by Hull & Vaid, 2006) and, more
impairment(s) has been more difficult to determine, recently, with neuroimaging techniques such as
however. fMRI (e.g., Kim, Relkin, Lee, & Hirsch, 1997; Illes
A disturbance in planum temporal asymme- et al., 1999; Meschyan & Hernandez, 2006; Pillai
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try has been traditionally assumed to be causally et al., 2003). Although Paradis (2004) argued that
related to dyslexia but recent evidence suggests the right hemisphere is no more involved during L2
that parietal (rather than temporal) asymmetry processing than it is for L1, there still appears to be
is the most relevant morphological characteristic considerable debate whether the neural bases of lan-
(see review by Habib, 2000). Robichon and Habib guage organization in bilinguals is exactly identical
(1998), for example, found that the parietal oper- to monolinguals.
culum is less asymmetrical in dyslexics than in As reviewed by Abutalebi (2008), bilinguals gen-
controls, and that the degree of asymmetry of this erally utilize the same cortical networks as mono-
area is inversely related to phonological task perfor- linguals during language tasks. However, when the
mance. Dyslexic adults also show reduced left but second language (L2) of a bilingual is compared
increased right hemisphere activation in temporal- to the native language (L1), there are reports of
parietal regions during phonological processing, a greater left hemispheric “spread”. Researchers also
pattern the opposite of that observed in typical stress the importance of factors such as the age
readers (Shaywitz et al., 1998). of L2 acquisition and proficiency level when L1
More recent reviews of neuroimaging studies, and L2 activity in bilinguals are compared (Illes
namely functional magnetic resonance imaging et al., 1999; Meschyan & Hernandez, 2006; Perani
(fMRI), have similarly emphasized a reduction et al., 1998).
or absence of activity in left hemisphere tem- Investigating the role of such factors,
poroparietal cortex in dyslexic individuals during Wartenburger et al. (2003) found that the cor-
language tasks (McCrory, 2004; Maisog, Einbinder, tical representation of grammaticality judgments
Flowers, Turkeltaub, & Eden, 2008; Temple, 2002). is only affected by age of acquisition, whereas the
McCrory (2004) found different activation pat- cortical representation of semantic judgments is
terns during reading tasks in dyslexic participants affected by language proficiency. More extensive
compared to typical readers in language-related activations were observed in areas such as the
left hemispheric regions, including the inferior left inferior frontal gyrus (Broca’s area) and right
frontal gyrus and the angular gyrus. Demonet middle gyrus (Wartenburger et al., 2003). More
et al. (2004) also reported that activation in the global activations were also observed in Liu, Hu,
right hemispheric regions were more robust in Guo, and Peng’s study (2010) where regions such
dyslexic participants when compared to typical as the putamen, supplementary motor areas and
readers. Such results emphasize that there are cerebellum were bilaterally activated during a pic-
neural differences between dyslexic readers and ture naming task in L2, compared to L1. Using a
those who read normally when engaged in lin- dual-task language paradigm, Badzakova-Trajkov,
guistic processes (Eden et al., 2004), with the Kirk, and Waldie (2008) also found more bilateral
right hemispheric activity thought to be a compen- involvement in late L2 speakers (living in their
satory mechanism, perhaps due to the extra cogni- L2/English environment) compared to monolin-
tive effort required during phonological processing gual control participants. The authors concluded
(Grigorenko, 2001; Joseph, Noble, & Eden, 2001; that late proficient bilinguals may engage both
288 PARK, BADZAKOVA-TRAJKOV, WALDIE
hemispheres to a greater extent than monolinguals BK was diagnosed with dyslexia in the German
when reading. language at the age of 8 in her native Austria.
The observation that these two different exper- In 2006 she was administered a battery of tests
imental groups (i.e., bilingual participants who by a neuropsychologist that included the Wechsler
read proficiently, and monolingual individuals with Adult Intelligence Scale (WAIS; Wechsler, 1971),
developmental dyslexia) both appear to utilize the Wide Range Achievement Test (WRAT-3;
additional areas of cerebral cortex during language Wilkinson, 1993), the Coltheart online reading
tasks than is typical of monolingual proficient read- test (Coltheart, 2004), and the Woodcock–Johnson
ers, presented to us interesting questions regarding Tests of Achievement (Woodcock, Mather, &
the brain activity of individuals who are both bilin- McGrew, 2001). In brief, the results revealed that
gual and diagnosed with dyslexia. Much of the BK had a full-scale IQ of 114 and a reading age
existing literature on bilingual dyslexia has focused (in English) of 10 years. Her nonword reading
on assessing the cognitive skills of children who was extremely poor, suggesting a primary problem
are not achieving as expected in their second lan- with phonological processing. She has no history of
guage (e.g., Everatt, Smythe, Adams, & Ocampo, neurological problems or mental health problems.
2000; Miller Guron, & Lundberg, 2003). Very lit-
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Participants
Stimuli and procedure
Adult dyslexic bilingual
A blocked experimental design with a “go/no-go”
BK is a 35-year-old German-English right- lexical decision response paradigm was employed
handed female with developmental dyslexia. She in this study (e.g., participants were instructed
is a native Austrian who started learning English to respond to a correct answer with their right-
(L2) at school from the age of 10. She is a profi- hand by pressing a mouse button and refrain from
cient speaker of both German and English, and is responding for the incorrect response). Ten exper-
well-educated with tertiary qualifications including imental and 10 fixation/baseline blocks were used
a Masters in Graphic Design. She migrated to New for the five conditions/tasks in the study (two exper-
Zealand in 2003, and has been living and working imental blocks per condition). Each experimental
in her L2 environment since then. block lasted for 48 seconds and was preceded by
BRAIN ACTIVITY IN BILINGUAL DYSLEXIA 289
an 18-second fixation/baseline block. Stimuli were gap: 0 mm; resulting in 1 × 1 × 1 mm voxels, axial
presented in Courier New Bold, 35 font size, using acquisition, parallel to AC-PC line, ensuring whole
E-Prime (Psychological Software Tools, Pittsburgh, brain coverage). Thirty-two scans were acquired for
PA). Twenty stimuli were randomly presented in a each condition along with 60 scans for the fixation
black font on a grey background for each experi- period resulting in a total of 220 T2∗ -weighted vol-
mental block. Each stimulus was presented for 2000 umes for each of the subjects (nonverbal, lettercase
ms followed by a 400-ms interstimulus interval, judgment, regular, irregular, and nonword task) in
which was a blank grey screen. the EPI sequence. In addition, 2 initial “dummy”
The nonverbal task consisted of black shapes scans were also collected at the beginning of each
with either pointy or smooth edges. The partici- sequence to control for T1 saturation but these were
pant was required to press the mouse button for not included in the analysis.
shapes with at least one sharp edge. The letter- The EPI acquisition sequence parameters were as
case judgment task consisted of upper-case and follows: TR = 3000 ms; TE = 50 ms; flip angle = 90◦
lower-case letters (e.g., NKWZL or jdfgn). The par- FOV = 19.2 cm; matrix size: 64 × 64; with inter-
ticipant was required to press the mouse button for leaved slice acquisition, starting at the bottom; 30
upper-case stimuli (50% of trials). The regular word slices parallel to AC-PC line; slice thickness: 3 mm;
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lexical decision task consisted of real words (con- 25% gap: resulting in 3 × 3 × 4 mm voxels.
crete nouns) and pronounceable nonwords matched
on length (e.g., BANK or LORC). The participant
was required to press the mouse button for stim- Image pre-processing and analysis
uli that were real words (50% of trials). Stimuli
in the irregular word condition were words which SPM5 software (Wellcome Department of Imaging
did not follow the grapheme-phoneme correspon- Neuroscience, London, UK; http://www.fil.
dence (GPC) rules, and pronounceable nonwords ion.ucl.ac.uk) was used for image processing and
matched on length (e.g., SHOE or NINT). The analysis. The first volume of the first session was
participant was required to press the mouse but- used as a reference for coregistration of the first
ton for stimuli that were real words (50% of trials). volume for the rest of the sessions. The remaining
Stimuli in the nonword lexical decision task (also volumes were realigned to the first volume within
referred to as the “phonological” task) were all each session and a mean of all volumes across the
nonwords, but half were pseudohomophones (i.e., conditions were created.
PHEAT, BRANE), and pronounceable nonsense The T1-weighted structural image was coregis-
words again matched on length (e.g., CORTO). The tered to the mean of the functional volumes. By
participant was required to press the mouse button using the unified segmentation procedure, normal-
for stimuli that sounded like a real word (subjects ization parameters were estimated (Ashburner &
were instructed to think but not speak out loud). Friston, 2005). This was then used to normal-
All participants were required to run through as ize both the functional and structural images to
many practice trials of the experimental block as the stereotactic coordinate system defined by the
necessary to achieve 90% accuracy. No feedback Montreal Neurological Institute (MNI). Lastly, the
was given during the experimental trials. The accu- functional volumes were spatially smoothed using
racy data were also recorded. All procedures were an anisotropic Gaussian filter of 9 × 9 × 12 mm
approved by the University of Auckland Human (three times the voxel size) at full-width at half-
Participants Ethics Committee. maximum (FWHM).
For each participant, the pre-processed func-
tional volumes were subjected to 1st-level or fixed-
Image acquisition effects analysis using the general linear model
applied at each voxel across the whole brain.
Images were acquired using a 1.5T Siemens Conditions were modeled by boxcar waveform con-
Avanto scanner (Erlangen, Germany). Scanning volved with a canonical haemodynamic response
sessions began with acquisition of T1-weighted function. Contrast images of interest were also
structural volumes using 3D MP-RAGE sequence produced for: (1) Nonverbal minus (i.e., versus)
(TR = 11 ms; TE = 4.94 ms; flip angle: 15◦ ; FOV: Baseline; (2) Lettercase judgment versus Baseline;
25.6 × 20.8 cm; 170 to 176 axial slices parallel to (3) Regular word versus Baseline; (4) Irregular word
the AC-PC line; matrix size: 256 × 208; interslice versus Baseline; (5) Nonword task versus baseline;
290 PARK, BADZAKOVA-TRAJKOV, WALDIE
and (6) Nonword task versus Lettercase judgment. In the Regular word versus Baseline condition,
An uncorrected threshold of p < .01, and a con- BK showed significant right hemispheric activity in
tiguity threshold of 10 voxels was used for each the superior frontal gyrus and the lingual gyrus.
comparison and each subject. Left hemispheric activations were also seen in the
lingual and frontal gyri. IH also showed significant
bilateral activation in the fusiform gyrus and infe-
Laterality Index calculations
rior frontal gyrus. RW showed the least amount of
activation. In contrast to the bilingual participants,
A laterality index (LI) was calculated to determine
RW’s activations were mainly lateralized to the left
the language lateralization for each of the subjects
hemisphere in regions such as the left angular and
for the conditions of interest. This was done by
fusiform gyri.
computing the number of voxels that were signifi-
In the Irregular word versus Baseline condition,
cantly activated in a region of interest in each cere-
both BK and IH showed both right and left hemi-
bral hemisphere using the LI toolbox available from
spheric activity. BK showed robust activation in
the official SPM website (Wilke & Lidzba, 2007).
the left inferior and middle temporal gyri, and the
Laterality indices range in values from –1 to +1,
left lingual and precentral gyri. Right hemisphere
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TABLE 1
Cortical regions showing significant activations in the three participants for the Nonword
task versus Baseline only
Cluster extent in mm3 , t-values, Brodmann areas (BA) and Talairach coordinates for the peak
activation voxel are also shown.
right middle frontal and orbital gyri. Activity in the left inferior occipital gyrus. In the right hemisphere,
left cerebellum was also observed. IH showed sig- activations were seen in the middle frontal gyrus
nificant bilateral activity with robust activations in and the cerebellum. The descriptive behavioural
the left and right inferior frontal gyri and inferior results (see Figure 2) showed that the control par-
temporal gyri (Figure 1B). Other activity was found ticipants outperformed BK in most of the tasks. It
in the right middle frontal gyrus, right superior should be noted, however, that BK’s performance
parietal lobule and the right inferior and middle on the Nonword task was only marginally worse
temporal gyri. Further left hemispheric activations than the controls. This was due in part to the
were observed in the precentral gyrus. Significant control subjects finding the task difficult as well.
activations were found mainly in the left hemisphere The laterality indices results for the Nonword
for RW, suggesting left lateralization for language task versus Lettercase judgment contrast indicated
(Figure 1C). Regions of activity observed included clear differences between the bilingual subjects and
the left inferior frontal gyrus, left inferior parietal the monolingual subject, with RW showing a strong
lobule and the left precentral gyrus, as well as the left lateralization for language compared to BK
292 PARK, BADZAKOVA-TRAJKOV, WALDIE
TABLE 2
Cortical regions showing significant activations in the three participants for the Nonword
task versus Lettercase only
Cluster extent in mm3 , t-values, Brodmann areas (BA) and Talairach coordinates for the peak
activation voxel are also shown.
and IH (see Figure 3). BK showed consistent right activation differences were only observed during
hemispheric dominance for both regions of inter- linguistic processing and not during the nonverbal
est (frontal and temporal lobes) in comparison to or lettercase judgment tasks.
IH who exhibited a more bilateral activation for In the nonverbal condition, similar bilateral acti-
language in the temporal lobe. vations were observed for all three participants.
These were mainly limited to the occipital and tem-
poral lobes, with some parietal and minimal frontal
DISCUSSION activity. This pattern was also observed for the
lettercase judgment condition. These results were
The results from the present study indicate that expected, as both conditions include stimuli that
different neural networks subserve linguistic func- are not semantically based and require low levels of
tioning in the dyslexic bilingual (BK), the control cognitive effort. Interestingly, BK showed the most
bilingual (IH), and the control monolingual (RW). significant clusters and spread of activations in both
Differences between participants were particularly conditions, suggesting that adults with dyslexia may
evident in the regular, irregular and nonword lex- utilize a larger area of the brain for a range of
ical decision tasks, which indicate that clear brain tasks.
BRAIN ACTIVITY IN BILINGUAL DYSLEXIA 293
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Figure 1. Significant clusters of activation for the dyslexic bilingual (A), the control bilingual (B), and the control monolingual (C) for
the Nonword versus Lettercase judgment contrast on section overlay.
The monolingual RW showed significant and Mosley, 2000). Right hemisphere involvement is
strong left lateralization, particularly in the also somewhat dependent on task methodology.
occipito-temporal region and inferior frontal cor- Demonet, Thierry, and Cardebat (2005) noted
tex during all three linguistic tasks. The left inferior that reduced asymmetry is often associated with
frontal gyrus is involved in both speech perception single-word processing rather than syntax or
and phonological aspects of reading (Habib, 2000; sentence processing and in comprehension tasks
Owen, Borowsky, & Sarty, 2004). Some right (rather than production tasks). This observation is
hemispheric activity was also observed. This was in line with the current findings using lexical deci-
expected, as complete lateralization of language sion. Nevertheless, the extent of right hemisphere
tasks to the left hemisphere is rarely observed. activity was small in RW compared to the bilingual
Evidence suggests that the right hemisphere subjects.
participates in certain aspects of language recog- In contrast, the dyslexic bilingual BK showed
nition and identification (Fabbro, 2001; Waldie & relative hypoactivation of the left hemisphere
294 PARK, BADZAKOVA-TRAJKOV, WALDIE
0.6
the weak left hemisphere network. Surprisingly,
0.4 the Nonword condition elicited poor performances
across all three subjects (including the two con-
0.2 trol participants), indicating that this task was more
0
difficult than the other tasks. Nevertheless, BK per-
Nonverbal Letter Case Regular Irregular Phonological formed the worst, as expected, with an accuracy
Task conditions of 50%.
Figure 2. Accuracy rates for the dyslexic bilingual (BK), the
The control bilingual IH consistently exhibited
control bilingual (IH), and the control monolingual (RW) for a bilateral pattern of activation across all the
each of the five task conditions. task conditions. Interestingly, activity in the left
occipito-temporal regions was limited for both BK
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The control bilingual IH showed significant in a second language. Our study also increases
activations in both the left and right inferior frontal understanding of bilingual dyslexia, raising the
areas, which indicate that the typical left hemi- possibility that these individuals are atypically
spheric reading network was successfully utilized. lateralized and may depend on alternate cortical
The additional cortical activity observed in IH’s resources during language processing.
case is likely to be linked to the fact that English
words were used rather than her native German. Original manuscript received 6 December 2010
This is consistent with findings of compensatory Revised manuscript accepted 23 March 2011
neural activity in bilinguals when using their second First published online 25 October 2011
language, as the extra cortical effort often elicits
recruitment of other areas during linguistically-
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