NeuroImage 233 (2021) 117911

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NeuroImage
journal homepage: www.elsevier.com/locate/neuroimage

Failure of resting-state frontal–occipital connectivity in linking visual

perception with reading fluency in Chinese children with developmental
dyslexia ✩
Xiujie Yang a,1, Jia Zhang b,1, Yaping Lv b, Fang Wang c, Guosheng Ding b, Manli Zhang d,
Xiangzhi Meng e,∗, Yan Song b,∗
a
Faculty of Psychology, Beijing Normal University, Beijing 100875, China
b
State Key Laboratory of Cognitive Neuroscience and Learning and IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing 100875, China
c
Laboratory of Applied Brain and Cognitive Sciences, School of Business and Management, Shanghai International Studies University, Shanghai, China
d
Maastricht Brain Imaging Center, Department Cognitive Neuroscience, Faculty of Psychology and Neuroscience, Maastricht University, Maastricht, the Netherlands
e
School of Psychological and Cognitive Sciences, Beijing Key Laboratory of Behavioral and Mental Health, Peking University, Beijing 100871, China

a r t i c l e i n f o a b s t r a c t

Keywords: It is widely accepted that impairment in visual perception impedes children’s reading development, and further
Texture discrimination task (TDT) studies have demonstrated significant enhancement in reading fluency after visual perceptual training. However,
Reading fluency the mechanism of the neural linkage between visual perception and reading is unclear. The purpose of this
Resting-state functional connectivity
study was to examine the intrinsic functional relationship between visual perception (indexed by the texture
Primary visual cortex
discrimination task,TDT) and reading ability (character reading and reading fluency) in Chinese children with
Left middle frontal gyrus
Developmental dyslexia developmental dyslexia (DD) and those with typical development (TD). The resting-state functional connectivity
(RSFC) between the primary visual cortex (V1, BA17) and the entire brain was analyzed. In addition, how RSFC
maps are associated with TDT performance and reading ability in the DD and TD groups was examined. The results
demonstrated that the strength of the RSFC between V1 and the left middle frontal gyrus (LMFG, BA9/BA46)
was significantly correlated with both the threshold (SOA) of the TDT and reading fluency in TD children but
not in DD children. Moreover, LMFG-V1 resting-state connectivity played a mediating role in the association of
visual texture discrimination and reading fluency, but not in character reading, in TD children. In contrast, this
mediation was absent in DD children, albeit their strengths of RSFC between V1 and the left middle frontal gyrus
(LMFG) were comparable to those for the TD group. These findings indicate that typically developing children
use the linkage of the RSFC between the V1 and LMFG for visual perception skills, which in turn promote fluent
reading; in contrast, children with dyslexia, who had higher TDT thresholds than TD children, could not take
advantage of their frontal–occipital connectivity to improve reading fluency abilities. These findings suggest that
visual perception plays an important role in reading skills and that children with developmental dyslexia lack
the ability to use their frontal–occipital connectivity to link visual perception with reading fluency.

1. Introduction in developmental dyslexia (Eden et al., 1996;(Facoetti et al., 2010)

Developmental dyslexia (DD) is a failure to acquire reading skills
that affects approximately 5–10% of children, despite otherwise av-
erage/above average intelligence and adequate education experience
(Gori and Facoetti, 2014; McBride, 2015). Emerging studies have
demonstrated that visual perceptual processing deficits may result
Lobier et al., 2012; (Vidyasagar and Pammer, 2010)). Reading re-
quires visual resources to rapidly select the sublexical units through
the mapping of visual orthography with phonology codes (Farmer and
Klein, 1995) Ferretti et al., 2008; Franceschini et al., 2012;(Hari and
Renvall, 2001) Ho et al., 2000; (Plaza and Cohen, 2007)(Walker et al.,
2006). Some studies have revealed that visual perceptual interventions

✩
This work was supported by the National Natural Science Foundation of China (31971039, 81371206, 31871099, and 32000757), the National Defense Basic Sci-
entific Research Program of China (2018110B011), and the Beijing Brain Initiative of Beijing Municipal Science and Technology Commission (Z181100001518003).
We sincerely thank the children, parents, and schools for their participation and cooperation in our study.
∗
Corresponding authors.
E-mail addresses: mengxzh@pku.edu.cn (X. Meng), songyan@bnu.edu.cn (Y. Song).
1
Xiujie Yang and Jia Zhang contributed equally to this manuscript.

https://doi.org/10.1016/j.neuroimage.2021.117911
Received 1 July 2020; Received in revised form 22 February 2021; Accepted 23 February 2021
Available online 10 March 2021
1053-8119/© 2021 The Author(s). Published by Elsevier Inc. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/)
X. Yang, J. Zhang, Y. Lv et al.
promote reading performance in children with dyslexia (Chouake et al.,
2012; Franceschini et al., 2013; Meng et al., 2014; Zorzi et al., 2012).
Chinese characters are logographs with a number of strokes packed
into a square shape, which is in contrast to English words, which exhibit
different lengths (Ho and Bryant, 1999; (Tan et al., 2001a)). The com-
plexity of a character requires children to concentrate more on the subtle
differences between strokes (McBride, 2016). Second, more than 39%
of Chinese characters are compound characters with a phonetic radical
and a semantic radical (Zhou et al., 1978). Children have to make use
of visual perception to distinguish the phonetic radical to pronounce
it and distinguish the semantic radical to understand the meaning of
this character (McBride-Chang et al., 2005(Yang et al., 2019)). Further-
more, Chinese characters are logographs with less regularity in sound-
print mapping (Meng et al., 2014). Children have to address phonol-
ogy in Chinese scripts and focus on the specific visual processes as-
sociated with orthographic analyses of Chinese characters (Yang and
Meng, 2020; Wang et al., 2012). Altogether, reading Chinese characters
necessitates a great interactivity between phonology and orthography
and requires a heavy cognitive demand for visual perception.
Children with dyslexia are characterized by dysfunction of the left
middle frontal gyrus (LMFG, BA9/BA46). Several neuroimaging stud-
ies have proposed that the involvement of the LMFG during visuospa-
tial analysis (Chen et al., 2002; Liu et al., 2008(Tan et al., 2001b)) and
through the rhyme judgment task (Ip et al., 2019; Kovelman et al., 2012;
Siok et al., 2008; Tan et al., 2005; (Siok et al., 2003)) possibly con-
tributes to identifying reading performance across languages. Siok et al.
(2004a, 2004b,; 2008; (Siok et al., 2009)) repeatedly found that chil-
dren briefly retained “graphic” radicals in visual form while retriev-
ing the pronunciation of characters when the LMFG was activated. This
gyrus might explain the functional and structural abnormalities in map-
ping a character’s visual orthography to pronunciation in children with
dyslexia (Perfetti et al., 2006).
Considering the intensive visuospatial analysis and the pronunci-
ation of various strokes demanded in Chinese reading, it is critical
to specifically determine how visual perception correlates to reading
and the neural mechanisms underlying their relationships in these chil-
dren. Some behavioral studies have shown that visual perception con-
tributes to Chinese character reading through its role in acquiring visual-
orthographic knowledge (e.g., Huang and Hanley, 1995, 1997; (Ho and
Bryant, 1997)1999; Siok and Fletcher, 2001). However, precisely how
visual perception and reading processes are linked in neural mechanisms
remains unclear. Resting-state functional connectivity (RSFC) provides
an approach to uncover the temporal synchronization of functionally
related brain regions and to examine the functional relevance of intrin-
sic brain activity patterns with behavioral performance. Previous studies
have proposed that correlating the strength of the RSFC with behavioral
performance provides more direct evidence about the neural bases of a
wide range of cognitive functions (Wang et al., 2012).
There have been a small number of fMRI studies investigating the un-
derlying neural linkage of Chinese word processing with RSFC (Li et al.,
2013; Wang et al., 2012; Zhou et al., 2015). Of note, many of these
studies have confirmed the importance of the function(s) of the LMFG
and its connections with other brain regions in the resting state among
Chinese readers (Li et al., 2013; Wang et al., 2012). However, only high-
level neural areas were calculated as seed regions to indicate the func-
tional connectivity in these studies. A more fundamental sensory pro-
cessing area, the primary visual cortex (V1, BA17), has not been set as
a seed region to explore its neural linkage with children’s reading per-
formance. Importantly, abnormal lateralization of the primary visual
cortex (V1) in the dyslexic population (Jenner et al., 1999) and abnor-
mal visual magnocellular neurons defined in V1 (Evans et al., 1994;
Johnston et al., 2017; Stein, 2019) may account for the known visual
perception deficits measured in dyslexic individuals. For instance, asym-
metry in the size of neurons in the primary visual cortex (V1) in dyslexic
individuals was shown to be associated with decreased visual perception
ability (Jenner et al., 1999). Previous behavioral evidence has illustrated
2
NeuroImage 233 (2021) 117911
that training on the visual texture discrimination task (TDT) induces
long-lasting behavioral improvement restricted to the trained eye and
trained visual field quadrant that did not transfer to other quadrants
(Karni and Sagi, 1991). In most perceptual learning models, this speci-
ficity is attributed to neural plasticity in the early visual cortex, such as
the primary visual cortex (V1), where neurons are highly selective for
stimulus location and orientation. Significant TDT learning effects on
V1 activity have been observed in many functional magnetic resonance
imaging (fMRI) studies in humans (Schwartz et al., 2002; Walker et al.,
2005; Yotsumoto et al., 2009). For instance, activation of the primary
visual cortex (V1) increases in the early encoding phase of TDT training
but returns to baseline levels in the later retention phase (Yotsumoto
et al., 2008). Moreover, the functional connectivity between V1 and the
lateral/medial temporal cortex is also increased after weeks of training
(Kang et al., 2018). On the other hand, (Wang et al., 2016a) demon-
strated that the earliest ERP C1 component, known to reflect V1 activ-
ity driven by feedforward inputs, was not modulated by visual texture
discrimination training. In contrast, one anterior ERP component over
the prefrontal cortex was progressively modified each day. This ERP
result suggests that changes in V1 activity induced by TDT learning pri-
marily originate from relatively late, higher-order cortical processing
(Ding et al., 2014). Overall, these results suggest that visual texture dis-
crimination should primarily involve the primary visual cortex (V1) as
well as the functional connectivity between V1 and the higher-order
brain cortex.
Therefore, the present study focused on visual perception and its
neural relationship with children’s reading performance. Specifically,
we selected V1 as the seed point and focused on how the FCs between
V1 and other cortical regions influence the connection between visual
perception and reading abilities. This focus will provide important evi-
dence to improve the present understanding of the fundamental mecha-
nisms of dyslexia and will aid in the development of improved methods
to help children who are in need.
The texture discrimination task (TDT) has been widely used to indi-
cate visual perception (Wang et al., 2012; Schwartz et al., 2002), and
behavioral work has shown that reading performance can be enhanced
by visual TDT training (Meng et al., 2014). In recent decades, studies
on neural mechanisms of the TDT have found that changes in the pri-
mary visual cortex (V1) might underpin perceptual learning (Karni and
Sagi, 1991; 4). Meanwhile, top-down influences exerted on V1 from later
visual processing stages (V2 to V4) or from frontoparietal attention net-
works have also been modulated with perceptual learning (Ahissar and
Hochstein, 1996; Merigan, 2000; Wang et al., 2013, 2016a; Wang et al.,
2016b; Yotsumoto et al., 2013; Zhang et al., 2015; Wang et al., 2016b).
We therefore made use of this task to assess children’s visual percep-
tion. Moreover, we examined whether the strengths of the RSFCs were
associated with visual perception and reading performance, as well as
how the RSFCs influenced the relationships between TDT and Chinese
reading skills.
We now know that the brain areas supporting reading are influenced
by culture (Bolger et al., 2005; Pugh et al., 2005). In the case of Chi-
nese individuals, deficits in visual-orthographic and semantic processes
might be characterized by dysfunction of the LMFG and its connection
with other brain regions (Perfetti et al., 2006; Xu et al., 2019). Therefore,
it was anticipated that TDT performance might correlate with RSFCs be-
tween the V1 and LMFG, and the RSFC might be positively associated
with children’s reading fluency performance, which involves semantic
processes.
2. Methods
2.1. Participants
For this study, fifty-two Chinese-speaking children in grades four,
five, and six were recruited. This study was approved by the Ethics
Committee of the University. All parents of participating children pro-
X. Yang, J. Zhang, Y. Lv et al.
Table 1
Demographic characteristics (mean ± SD) and reading scores of the TD and DD groups.
TD group
N 25
Age 10.4 ±
Sex(male/female) 12/13
Nonverbal IQ 83.2 ±
Chinese character recognition (%) 89.1 ±
Reading fluency 49.8 ±
Note. TD= Typically Developing Children DD=Children with Developmental Dyslexia.
vided written informed consent according to the Declaration of Helsinki.
All participants were right-handed and had normal or corrected-to-
normal vision. We excluded children with left handedness because
of the evidence that they might show more variability in language
dominance and, arguably, in the lateralization of other brain areas
(McManus, 1985a, 1985b; Pujol et al., 1999, Cai et al., 2010(Van der
Haegen et al., 2012)).
No participants had a history of neurological disease or other psy-
chiatric disorders. We assessed all participants with the cancelation test,
which was adopted from the Wechsler Preschool and Primary Scale of
Intelligence-Fourth Edition, WPPSI (Wechsler, 2012), to assess the chil-
dren’s general attention ability. Afterwards, for children who were sus-
pected of having attention problems, the administrators who were blind
to the results of the evaluation further performed the ADHD assessment
from the Diagnostic and Statistical Manual of Mental Disorders-Fourth Edi-
tion (DSM-IV) (American Psychiatric Association, 1994) (American Psy-
chiatric Association 1994) to characterize whether he/she should be di-
agnosed with ADHD.
For the resting-state fMRI session, data from 9 children (TD: n = 3,
DD: n = 6) were excluded due to excessive head motion (> 3 mm max-
imum translation or 3° rotation). As a result, 25 TD children (mean
age=10.4 ± 1.0 years old) and 18 DD children (mean age= 10.2 ± 1.0
years old) were included in the final resting-state fMRI analysis. Age
and IQ were matched between the two groups. Demographic data and
scores of the reading tests are reported in Table 1.
2.2. Reading measures
The Standardized Chinese Character Recognition Test was used to
assess character reading. It consists of 210 characters and is divided
into ten groups based on reading difficulty (Wang and Tao, 1993) . The
participants were asked to write down a compound word based on a
constituent morpheme provided on the sheet. Their performance was
measured by the total number of correct characters (morphemes) that
they could utilize in word compositions. The correct characters each
participant completed corresponded to a specific normal reading grade
(Wang and Tao, 1993).
The Reading Fluency Test was utilized to examine children’s reading
fluency ability. It was composed of 95 sentences (You et al., 2011). Each
sentence was paired with five multiple-choice pictures. The participants
were asked to read each sentence and select, from five pictures, the one
that best illustrated the meaning of the sentence. All of the sentences in
this test were composed of high-frequency characters and words. The
children were encouraged to complete as many paragraphs as possible
within seven minutes. The total number of sentences that the partici-
pants could understand determined the performance score.
2.3. Grouping criteria
As assessed by Raven’s Standard Progressive Matrices, all 52 children
had typically developed nonverbal IQ scores (Zhang and Wang, 1985).
The control group of typically developing readers all obtained above
average scores in the Chinese character recognition test. Children were
placed in the dyslexia group if they scored either (1) at least 1.5 SDs be-
3
NeuroImage 233 (2021) 117911
DD group T value P-value
18 - -
1.0 10.2 ± 1.0 0.31 n.s.
12/6 – –
13.1 80.8 ± 13.7 0.71 n.s.
8.6 17.5 ± 15.4 18.96 p < 0.001
7.0 37.0 ± 3.7 6.88 p < 0.001
low the norm in the character recognition test and lower than the mean
scores for their grades in the reading fluency test or (2) at least 1 SD
below in the character recognition test and 0.5 SDs below in the read-
ing fluency test. This group criteria have been widely used in screening
Chinese-speaking children with dyslexia (e.g., Meng et al., 2014).
The texture discrimination task (TDT) has been used in numerous
visual perceptual learning studies, including in normal adults (Karni and
Sagi, 1991. Schwartz et al., 2002. Yotsumoto et al., 2008; Wang et al.,
2016a), children with dyslexia (Meng et al., 2014; Wang et al., 2014)
and children with autism(Harris et al., 2015) (Meng et al., 2007).
We revised the parameters based on these studies. The stimuli, white
(54 cd/m2) on a uniform black background, were displayed on a 21-
inch gamma linearized CRT monitor (1024 × 768 pixels at 85 Hz) at a
110 cm viewing distance in the behavioral pretest.
The visual stimulus was a texture display made of 19 × 19 high-
contrast horizontal line segments positioned in the central visual field,
covering an area of a 14° × 14° visual angle (Fig. 1). The lines were
0.46° × 0.04° in size and spaced 0.76° apart. The position of each line
segment was jittered randomly by 0° ~ 0.1° A randomly rotated letter
‘‘T’’ or ‘‘L’’ was presented at the center of the texture stimuli. A target
was generated by tilting three adjacent bars in the texture stimuli from
horizontal to 135°, forming either a horizontal or a vertical configura-
tion (Fig. 1). The target array was embedded in the upper-left visual field
at a location 2.5°~5° away from the fixation. A mask of the same size as
the stimuli was made of 19 × 19 randomly oriented V-shaped patterns
except at the fixation, where a superimposed “T” and “L” were used to
mask the “T” or “L” in the stimulus pattern (Fig. 1). The stimuli were
generated by a MATLAB program, and the experiment was performed
with E-prime (Fig. 2).
Children’s performance was measured using an adapted procedure
(staircase) with a starting SOA value of 600 ms. The staircase fol-
lowed a 2-down, 1-up rule, which resulted in a 70.7% convergence
rate (Leek, 2001). Each staircase (approximately 60 trials) consisted of
four preliminary reversals and six experimental reversals. The geometric
mean of the experimental reversals was taken as the threshold for each
staircase. Each participant completed three staircases. The step size was
36 ms until the fourth reversal and then changed to 24 ms. All partici-
pants practiced the task (40 trials) before the formal experiment.
The procedure for TDT in the task-based fMRI scan was as follows:
(1) the presentation time of the first fixation was 400 ms, (2) a fixed SOA
time of 564 ms was applied, and (3) the response time window was fixed
at 2 s; thus, participants were told that they needed to react as soon as
possible while guaranteeing accuracy. Beginning with a fixation block,
the fMRI sequence that subjects received was comprised of three 26.4 s
experimental blocks (8 trials), each of which was followed by a 24 s
fixation block.
2.4. Imaging data acquisition
In the scanner, children viewed the stimuli through a mirror located
above their eyes, and the stimuli were back-projected by a video projec-
tor (1024 × 768 pixels at 60 Hz) onto a translucent screen placed inside
the scanner bore. The viewing distance was 60 cm, which made the TDT
stimuli have the same visual angle as that in the behavioral pretest.
X. Yang, J. Zhang, Y. Lv et al.
Images were acquired using a Siemens TRIO 3T scanner at the Imag-
ing Center for Brain Research, Beijing Normal University. The partici-
pants laid in the scanner with their heads fixed with straps and foam
pads to minimize head movement, holding an optical response box
in their hands. The resting-state functional images were acquired be-
fore the anatomical imaging scan and task fMRI experiment. Data com-
prised 180 continuous echo-planar imaging (EPI) functional volumes
[40 slices, repetition time (TR) = 2400 ms, echo time (TE) = 30 ms, flip
angle = 81°, field of view (FOV) = 192 mm, matrix size = 64 × 64, voxel
size = 3.0 × 3.0 × 3.0 mm3 , and slice orientation: transversal]. During
the scan, participants were instructed to relax with their eyes closed,
not to think about anything systematically and not to fall asleep.
For functional images of the task fMRI experiment, an EPI se-
quence was used to measure blood oxygenation level-dependent (BOLD)
changes with the same parameters as those used in the resting state. In
addition, the following high-resolution T1-weighted anatomical images
were also acquired using a 3D MPRAGE sequence: 176 slices, repeti-
tion time (TR) = 2300 ms, echo time (TE) = 4.18 ms, flip angle = 9°,
field of view (FOV) = 256 mm, matrix size = 256 × 256, and voxel
size = 1.0 × 1.0 × 1.0 mm3 .
2.5. Task-based fMRI data preprocessing and analysis
Task fMRI data were preprocessed and analyzed using Statistical
Parametric Mapping (SPM12, http://www.fil.ion.ucl.ac.uk/spm). The
first 2 volumes were discarded to allow for the magnetic saturation effect
and adaptation of the participants to the scanning noise. The remain-
ing images were corrected for the acquisition time delay between dif-
ferent slices and corrected for head motion, followed by normalization
to Montreal Neurological Institute (MNI) space using T1-image unified
segmentation and smoothed for decreasing spatial noise (using a 6-mm
full-width at half maximum Gaussian kernel). The high-pass filter was
set to 128 s.
4
NeuroImage 233 (2021) 117911
Fig. 1. The experimental stimuli display. The
texture stimulus (left) was composed of three
adjacent diagonal bars (vertically or horizon-
tally aligned) embedded within a background
of horizontal bars, with the letter “T” or “L” as
the fixation. The mask (right) was made of ran-
domly oriented V”, with superimposed T and L
at the fixation position.
Fig. 2. Trial sequences of texture discrimina-
tion task (TDT).
However, due to children’s emotions and circumstances, especially
with respect to dyslexia, only some of the children completed the TDT
task-based fMRI scanning sessions, including 24 TD children and 19 DD
children. Among them, 15 children (TD: n = 6, DD: n = 9) were excluded
due to excessive head movement (> 3 mm maximum translation or 3°
rotation) or behavioral accuracy values that were too low (< 25%) dur-
ing the scan, leaving 18 TD children and 10 DD children included for
analysis.
For the first-level analysis, data from each participant were entered
into a general linear model (GLM) to construct a multiple regression
design matrix. The six movement parameters of the realignment (body
translation in the x-, y- and z-planes and rotation around the x-, y- and
z-axes) were also added to the design as multiple regressors. Through
model estimation, the contrast of the TDT for the experimental condition
versus that at baseline (fixation block) was applied to compute simple
main effects and produce individual beta-weight images. One-sample
t-tests were performed on beta-weighted images for experimental con-
ditions to compare participants in the TD and DD groups. Since the key
issue in the study was V1 activation, we conducted statistical analysis
using the mask of BA17 (V1 generally refers to the BA17). The thresh-
old of the activation maps was set at voxel level p < 0.001 and cluster
level FWE-corrected p < 0.05. Then, the overlap region of the activation
maps for each group was made, which was used as the region of interest
(ROI) for further resting-state data analysis.
2.6. Resting-state fMRI data preprocessing
Preprocessing of resting-state functional images was performed us-
ing the Data Processing Assistant for Resting-State fMRI (Yan and
Zang, 2010). The first 10 volumes were discarded. In addition to the
same procedure used for the task fMRI images, the remaining 170 im-
ages were preprocessed as follows: (1) after spatial smoothing, the linear
trend of the time course was removed; (2) temporal bandpass filtering
X. Yang, J. Zhang, Y. Lv et al.
(0.01–0.08 Hz) was performed to reduce the effects of low-frequency
drift and high-frequency noise (Fox et al., 2005); and (3) 24 head mo-
tion parameters and two repressors, including the white matter and cere-
brospinal fluid signals, were removed as nuisance covariates to control
physiological effects and head motion in children. The global signals re-
mained. To examine the potential influence of excessive head motion
in the DD group, we calculated the mean frame-wise displacement (FD)
for each remaining participant. All individualized mean FD values fell
within a reasonable range (i.e., no more than 0.2) suggested by previ-
ous studies (Yan et al., 2013) and were tested for group differences us-
ing a two-sample t-test. Furthermore, as suggested by previous research
(Guo et al., 2019; 2020), the mean FD was taken as a covariate in lin-
ear regression models in the following analysis to parse out the effect of
head motion.
2.7. Resting-state functional connectivity (RSFC) analysis
The resting-state functional connectivity (RSFC) analysis made use
of the overlap region of the activation maps based on the TDT-based
fMRI results for each group as the seed ROI. Then, the mean time series
of this V1 seed ROI was extracted by averaging the time series of all
voxels within it. An RSFC map for each participant was obtained after
correlation analysis between the mean time series of V1 and other brain
regions in a voxel-wise manner. To improve the normality of the correla-
tion coefficients, we used z–FC maps instead of r–FC maps in subsequent
analyses by using Fisher r–to–z transformation. A one-sample t-test was
computed on an individual z–FC map to generate the group z–FC map
for each group separately, which was used as a mask for further analysis.
2.8. Statistical analyses at the group level
To identify the cortical regions whose RSFC with the V1 seed were
associated with the observed group difference in TDT performance, we
conducted a linear regression analysis in which the V1-associated z–FC
images across two groups were entered as a dependent variable, with the
variables of TDT performance, group, and their interaction as three re-
gressors of interest. This voxel-based analysis was conducted across the
entire brain. Sex, age and mean FD were entered as covariates of nonin-
terest. We used “1″ and “−1″ to code the nominal variable of the group,
“1″ to represent the TD group, and “−1″ to represent the DD group.
The regressor denoting the interaction between TDT performance and
group was generated by multiplying their values. Of note, for this encod-
ing approach of variables, a negative interaction effect indicates that the
slope of the TDT performance for the TD group is less positive (or more
negative) than that for the DD group. After identifying brain regions
exhibiting significant interaction effects of TDT performance × group,
we further conducted simple-effect analyses for each region by calculat-
ing the correlation between TDT performance and V1-associated RSFC
within each group. This statistical analysis method has been widely used
to examine different effects of group differences on various brain regions
(e.g., de Chastelaine et al., 2017; Hsu et al., 2018; Li et al., 2017). The
AAL template (Tzourio-Mazoyer et al., 2002) was used as an explicit
mask with the exception of the cerebellum, and multiple comparison
correction was applied at p < 0.05 using AlphaSim.
2.9. Correlation between TDT-associated RSFC and reading fluency
Regions exhibiting significant interaction effects in the above lin-
ear model were considered ROIs in our following analyses. We first ex-
tracted the z–FC values between these ROIs and V1 (hereafter “V1-ROIs
RSFC”). Then, we calculated the correlation between the V1-ROI RSFC
and reading fluency for each group.
To verify the observed differences in correlation between TD and
DD, we further used a nonparametric permutation test to examine the
significance of group differences in the correlation of reading fluency
and V1-ROI RSFC. We conducted the permutation tests in a ROI-wise
5
NeuroImage 233 (2021) 117911
Fig. 3. The behavioral result of SOA for two groups. ∗ ∗ ∗ : p < 0.001.
approach, in which the RSFC of all voxels within a brain region was
averaged and entered into the analyses. In each permutation, the divi-
sion of participants into the two groups was randomized, and the sample
size for each group remained unchanged. Then, Pearson’s correlation of
reading fluency and RSFC was computed and transformed to Fisher’s
Z-score for each of the two randomized groups. The Z-scores were sub-
tracted between groups. This procedure was repeated 10,000 times, and
we obtained a permutation distribution of group differences in the cor-
relation Z-score. The null hypothesis was that there was no group dif-
ference in the correlation between reading fluency and V1-ROI RSFC.
3. Results
3.1. Behavioral TDT results
As illustrated in Fig. 3, the threshold of TDT (SOA) for the DD
group was significantly higher than that of the TD group (TD vs. DD:
mean = 563.15 vs. 854.62 ms; t (50) = −2.948, p < 0.006). Next, we
performed correlation analyses between the TDT and reading abilities.
The original threshold SOA of TDT was log-transformed to minimize
the influence of skewness. As illustrated in Fig. 4, the log-transformed
threshold of TDT was significantly associated with the performance on
the standardized Chinese character recognition test (rcharacter = −0.316,
p < 0.039), as well as the performance on the reading fluency test
(rfluency = −0.326, p < 0.033). After controlling for age and sex, the
two correlations remained significant (rcharacter = 0.310, p < 0.049;
rfluency = −0.319, p < 0.042). We also calculated the correlations be-
tween TDT and reading for the TD and DD groups. It turned out
that only in the TD group was TDT associated with reading fluency
(rfluency = −0.486, p < 0.015), while other correlations were not sig-
nificant in either group.
3.2. Task-based fMRI results
Using task-based functional MRI data acquired from 18 TD children
and 10 children with dyslexia, we estimated the BOLD activities in V1
using the BA17 mask. As shown in Fig. 5, voxels in V1 were maximally
and broadly activated during the TDT task for both the TD and DD
groups (TD: 3, −84, −3, MNI coordinate; t = 14.42, cluster size = 267;
DD: 12, −87, 0, MNI coordinate; t = 25.8, cluster size = 164, voxel level
p < 0.001, cluster level FWE-corrected p < 0.05). Then, we made the
overlap of the activation maps of the TD and DD groups (Fig. 5C) and
extracted the averaged BOLD signals in this overlap region. We found
that children with DD exhibited significantly higher V1 activation than
TD children (t (26) = 5.419, p < 0.001, two-sample t-test; see Fig. 5D).
3.3. Resting-state fMRI results
Analyses demonstrated that the DD group exhibited increased head
motion values compared to the TD group during resting-state fMRI (t
X. Yang, J. Zhang, Y. Lv et al. NeuroImage 233 (2021) 117911

Fig. 4. Correlation plots between SOA of TDT and reading tests. (A) Scatter plots depicting the relationship between the SOA of TDT and the percentage of Chinese
character recognition. (B) Scatter plots depicting the relationship between the SOA of TDT and reading fluency.

Fig. 5. V1 activation maps, overlap region in the activation maps and difference between the TD and DD groups. (A) V1 activation map in the TD group. (B) V1
activation map in the DD group. (C) The overlap region within the TD and DD groups. Red represents activation in the DD group. Blue represents activation in the
TD group. Pink represents the overlap region between the TD and DD groups. (D) V1 activation difference between the two groups.

(41)= 2.434, p = 0.019). However, none of the participants met the cri-
terion of mean FD > 0.2 (Yan et al., 2013). For each group of children,
the resting-state time course was extracted for the overlap activated V1
region obtained during the task-based fMRI TDT task. For each partic-
ipant, we obtained the RSFC map via correlation analysis between the
mean time series of this overlap and the whole brain in a voxel-wise
manner. The RSFC maps showed that there were wide areas that had
significant FCs with V1 for both the TD and DD groups (voxel level p
< 0.001, cluster level FWE-corrected p < 0.05, see Fig. 6), suggesting
the important role of V1, even in the resting-state brain. Next, our focus
was to identify brain regions in which the RSFC with V1 significantly
correlated with TDT performance and reading skills and whether such
associations were distinct across the DD group and the TD group. There-
fore, we performed the following linear regression analyses in the TD
and DD groups.
3.4. Group differences in the relationship between V1-associated RSFC and
TDT performance
We first performed linear regression analyses to explore the
brain regions showing group differences in the relationship between
V1-associated RSFC and children’s TDT performance. The results
demonstrated significant negative interaction effects of TDT perfor-
mance × group on V1-associated RSFC in two brain regions, including
the left superior frontal gyrus (SFG) extended to the left MFG and the left
MFG (p < 0.005, AlphaSim corrected to p < 0.05, Fig. 7). We did not
observe significant positive interaction effects. Specifically, in the TD
group, there was a significant negative correlation between TDT per-
formance and V1-associated RSFC in the left SFG (r (23) = −0.624, p <
0.001) and the left MFG (r (23) = −0.692, p < 0.001). In the DD group,
there was a trend for a positive correlation between TDT performance
and V1-associated RSFC in the left SFG (r (16) = 0.440, p = 0.068) and
the left MFG (r (16) = 0.336, p = 0.173).
3.5. RSFC correlates with reading fluency
In the following analysis, we aimed to (1) examine whether the RSFC
between V1 and SFG/MFG that we observed above was related to read-
ing ability and (2) to determine whether these correlations differ be-
tween the two groups. Therefore, we performed correlation analyses
between RSFC and reading fluency in the TD and DD groups. Specifi-
cally, we extracted and averaged the z-FC values of the voxels within
SFG/MFG in the V1 z-FC maps and performed Pearson correlation anal-
ysis with the SOA of TDT and reading fluency. As shown in Fig. 8, in
the TD group, we found that the RSFC between V1 and MFG predicted
children’s reading fluency well (r (23) = 0.564, p = 0.003). Moreover,
this effect remained significant after controlling for age, sex and mean
FD (r (20) = 0.662, p = 0.001). We did not observe a significant corre-
lation between the V1-SFG RSFC and TD children’s reading fluency (r
(23) = 0.317, p = 0.123).
For the DD group, no significant results were observed for either the
left MFG (r (16) = −0.101, p = 0.691) or SFG (r (16) = 0.197, p = 0.434).

6
X. Yang, J. Zhang, Y. Lv et al. NeuroImage 233 (2021) 117911

Fig. 6. Z-FC maps of the V1 in TD and DD groups. (A) Maps show voxels having significant FC with V1 in the TD group. (B) Maps show voxels having significant FC
with V1 in the DD group. The threshold was set at voxel level p < 0.001 and cluster level FWE-corrected p < 0.05.

Fig. 7. Group differences of the relationship

between the V1 Z-FC map and TDT perfor-
mance within the left SFG and the left MFG.
∗
Significance of negative correlation between
V1-SFG/MFG RSFC and TDT performance only
in the TD group.

Fig. 8. (A) Scatter plots depicting the relationship between FC strength in the V1-MFG and reading fluency in the TD and DD groups. (B) Scatter plots depicting the
relationship between FC strength in the V1-SFG and reading fluency in the TD and DD groups.

7
X. Yang, J. Zhang, Y. Lv et al.
Fig. 9. Two-wise correlations among FC of the V1-LMFG, SOA of the TDT and reading fluency in TD children. The r value (−0.542) was the correlation between the
SOA of the TDT and reading fluency after controlling for age, sex, and head motion, while the r value (−0.158) was the correlation between the SOA of the TDT and
reading fluency after controlling for age, sex, head motion, and V1-LMFG connection. ∗ ∗ ∗ p<0.001, ∗ ∗ p<0.01, ∗ p<0.05.
To address the possibility that the strength of related FC in children with
dyslexia was weaker than that in TD children, we extracted and aver-
aged the z−FC values between the aforementioned MFG region and the
voxels of V1 in the TD and DD groups. The results showed no signif-
icant difference in the strength of LMFG-V1 resting-state connectivity
between the two groups (t (41) = −0.429, p = 0.67, two-sample t-test),
suggesting that the strength of related FC in children with dyslexia was
not weaker than that observed in TD children.
Moreover, we used a nonparametric permutation test to examine the
significance of group differences in the correlation of reading fluency
and the V1-MFG RSFC. We found that the TD group showed a signifi-
cantly more positive correlation of reading fluency and V1-MFG RSFC
than the DD group (p < 0.05, permutation 10,000 times). These tests
further confirmed the findings of significant group differences observed
in the correlation analyses.
LMFG-V1 Mediates the Relationship between TDT and Reading Fluency.
Finally, we conducted a mediation analysis to examine how the cor-
relation between the TDT and reading fluency was influenced by the
LMFG-V1 resting-state connectivity in TD children. Age, sex, and head
motion were considered as confounding factors. The mediation analy-
sis revealed that V1-LMFG connectivity fully mediated the association
of TDT and reading fluency, indirect estimate = 0.35, p = 0.013. More-
over, after controlling for the effect of the LMFG-V1 resting-state con-
nectivity and other covariates, the correlation between TDT and reading
fluency was no longer significant (r = −0.158, p = 0.494). We summa-
rized that there were pairwise correlations among FC of the V1-LMFG,
SOA of the TDT and reading fluency (see Fig. 9). Taken together, this re-
sult indicates that the V1-LMFG connection might function as the neural
substrate linking TDT and reading fluency in TD children.
As the groups were quite imbalanced, we also performed the above-
mentioned analysis by randomly selecting 10 children from the TD
group and reconducting the analyses together with 10 DD children (Sup-
plementary Material, Figure S1-S5). Specifically, we first performed ac-
tivation analysis during the TDT task in these two groups. Then, we
identified the overlapping active region in V1 in the two groups. In the
following RSFC analysis, this overlapping region of V1 was regarded as
the seed region. The results showed that the V1-MFG RSFC pattern was
only correlated with reading fluency in the TD group, which was quite
similar to the main analysis in which 18 TD and 10 DD children were
included. In addition, we performed the analysis again by regressing
out the global signal. The V1-LMFG connection effect was reproducible
in the TD group, which was consistent with the main analysis. Finally,
to make it more convincing, we additionally selected the second visual
cortex (V2) as the seed, created its resting-state functional connectivity
with the whole brain regions, and performed a similar linear regression
analysis. In contrast with previous results with V1 as the seed, we did
not find such frontal–occipital connectivity linked to reading fluency in
8
NeuroImage 233 (2021) 117911
the TD group. Please refer to the Supplementary Material (Figure S6)
for details.
4. Discussion
The present study investigated the brain mechanism of the relation-
ship between visual perception, particularly visual texture discrimina-
tion, and reading in Chinese DD and TD children. The results showed
that the participants’ performance in the TDT task was significantly as-
sociated with character reading accuracy and reading fluency, and the
threshold of TDT (SOA) in the DD group was significantly higher in
the TD group, suggesting a deficit in basic visual texture discrimina-
tion in DD children. As mentioned earlier, the Chinese writing system
is logographic in nature, and Chinese characters are visually complex.
Effective use of visual perception, which is thought to be the core cogni-
tive processing in TDT (Censor et al., 2009; Schubo et al., 2001), allows
readers to concentrate on character features and the lengths of sentences
(Zhou et al., 2015).
Moreover, TDT task-based fMRI indicated that children with DD ex-
hibited significantly stronger V1 activation than TD children. Previous
neuroimaging studies utilizing TDT have demonstrated that changes
in the primary visual cortex (V1) might underpin individuals’ visual
perception (Karni and Sagi, 1991; Schwartz et al., 2002; Yotsumoto
et al., 2008). Moreover, over the course of completing TDT, the ERP
components over the occipital cortex and the prefrontal cortex were
progressively modified, suggesting that experience-dependent changes
may take place in the higher-level visual cortex (Wang et al., 2016a).
Therefore, stronger V1 activation in children with DD might, on the one
hand, indicate that those children probably require more V1 neuronal
resources when discriminating the visual texture (Pourtois et al., 2008),
given that hyperactivation might help them compensate for their ineffi-
ciency in completing this task. In contrast, it is also possible that children
with DD lack regulated resources from high-level cognitive processing,
such as visual-spatial attention (Franceschini et al., 2012), and there-
fore might need to activate V1 as much as possible to compensate for
the lack of regulations from higher-level cognitive processing.
The RSFC between V1 and LMFG was found to mediate the relation-
ship between TDT and reading fluency in TD children. When children
read printed texts, their visual systems confront several challenges, in-
cluding the competing visual constraint of congregating different words
into a sentence in a certain sequence (Johnston et al., 2017). V1 is fun-
damental for high-level cognitive processing, such as word recognition
(Jenner et al., 1999). There were findings showing abnormal neuronal
activations in the primary visual cortex (V1) in dyslexic individuals who
were associated with their decreased visual perceptual ability (Rosen &
Galaburda, 1999). Of note, abnormal visual magnocellular neurons de-
X. Yang, J. Zhang, Y. Lv et al.
fined in V1 successfully explained the visual perception deficits in Chi-
nese dyslexic individuals (Qian et al., 2015).
In contrast to alphabetic reading systems, Chinese reading involves
characters occupying two-dimensional space both in height and width,
and their structures are much more visually complex (McBride, 2015;
Wang et al., 2012). Some previous studies have established that the
LMFG is significantly activated when completing visual perception tasks
( (Belger et al., 1998) ; (Carlson et al., 1998) Zhou et al., 2015). Strong
activation of the LMFG in reading might be associated with visual prints
across languages, such as the unique square configuration of Chinese lo-
gographs. In line with this, neuroimaging studies have established that
LMFG is activated in visuo-orthographic processing of Chinese reading
(Chen et al., 2002; Kuo et al., 2004; Siok et al. 2004a, 2004b), which was
also observed in English reading (Kovelman et al., 2012; Ip et al., 2019).
Comparing French and Chinese reading, another study has revealed that
the LMFG is not specific to Chinese writing but includes representations
of handwriting gestures that are engaged in both alphabetical and non-
alphabetical languages(Feng et al., 2020) . Taken together, the func-
tional connectivity between V1 and the LMFG is reasonable supposed
to be the supportive neural basis underlying the connection of visual
perception and fluent reading, particularly Chinese reading.
In contrast, in children with DD, even though the strength of the FC
between the V1 and LMFG was comparable to that of TD children, the
LMFG-V1 resting-state FC did not correlate with either visual percep-
tion or reading fluency. These findings indicate that Chinese children
with DD cannot take advantage of the FC between the V1 and LMFG
to link visual perception and reading fluency. This might be because
children with DD may lack visual spatial attentional resources to co-
ordinate visual perception and reading processes. Indeed, the V1 sys-
tem is fundamental in processing basic visual information, while the
LMFG was found to be important in supporting visual spatial atten-
tion during Chinese reading (Siok et al. 2004a, 2004b). Furthermore,
Perfetti et al. (2006) proposed that the LMFG is recruited to coordinate
visual-orthographic and semantic information during Chinese reading.
Taken together, these findings suggest that in children with DD, frontal–
occipital connectivity might be dissociated from a precise spatial sam-
pling of visual input, and they performed a substandard coordination of
visual perception and reading fluency.
The role of frontal–occipital connectivity in character reading was
not established, possibly because children required fewer visual per-
ceptual resources during character reading than sentence reading. In-
deed, in the reading fluency task, sentences consisting of multiple char-
acters in a spatial sequence were presented. Due to the constraint of
humans’ attention resources, children need efficient attention shift-
ing/allocating across successive fixations and to disengage in irrelevant
noise (Moores et al., 2011) . In the character recognition task, the target
characters were presented one by one and without time pressure. Corre-
spondingly, Liu et al. (2015) found that visual perception still predicted
reading comprehension after controlling for Chinese character reading,
suggesting that visual perception is more essential for reading multiple
sentences than for reading single characters.
Apart from visual-orthographic processing in Chinese, the different
correlations of resting-state functional connectivity with reading fluency
between typically developing children and children with dyslexia might
also be related to phonological processing (Ip et al., 2019), which might
not be limited in Chinese. For example, Kovelman et al. (2012) em-
ployed fMRI to identify the neural correlates of phonological awareness
using an auditory word-rhyming task in English-speaking children who
were typical readers or who had dyslexia and found that typically de-
veloping children, rather than children with dyslexia, recruited the left
dorsolateral prefrontal cortex (DLPFC) when making explicit phonolog-
ical judgments. Notably, the DLPFC in the Kovelman et al. (2012) study
nicely overlaps with the LMFG (BA9) in the current study. Taken to-
gether, the association of LMFG-V1 resting-state FC and reading fluency
might not only require the processes of visual orthography but may also
reflect the rapid retrieval and maintenance of phonological information.
9
NeuroImage 233 (2021) 117911
Collectively, compared to recent fMRI studies that reported Chinese
dyslexic dysfunction in isolated dorsal regions, such as the IPS/SPL (Siok
et al., 2009), the V5/MT (Qian and Bi, 2015; Qian et al., 2015) and the
LMFG (Siok et al. 2004a, 2004b), our results extend these findings by
establishing altered synchronization in the linkage of the primary vi-
sual cortex and the dorsal area (i.e., LMFG) in Chinese children with
DD. However, this study has some limitations. The sample size for task-
based fMRI data was relatively small due to excessive head motion in
some children. Task-based fMRI between TD children and children with
DD still needs further investigation. Moreover, because visual percep-
tion involves spatial attention (Wang et al., 2013; 2016b) and TDT might
correlate with reading fluency performance via children’s spatial atten-
tion ability, further study is still required to provide direct evidence for
why the RSFCs among children with DD fail to mediate the associations
between TDT and reading fluency. Last, apart from V1, connections of
the LMFG to other brain areas has been found to be important for fluent
Chinese reading (Zhou et al., 2015). More RSFCs between the LMFG and
other brain areas with the LMFG as a seed region might be required to
determine their linkages with Chinese reading.
In conclusion, the current study mapped out the V1-LMFG resting-
state connectivity that correlated with visual texture discrimination and
Chinese reading fluency and demonstrated the mediating role of the V1-
LMFG resting-state connectivity in the associations between TDT and
reading fluency among the TD group. In contrast, there was no such me-
diation effect in DD children. These findings revealed that the functional
connectivity of the V1 and LMFG might be the common underlying neu-
ral mechanisms supporting the relationship between complicated visual
perception and fluent reading, whereas in DD children, frontal–occipital
connectivity might be dissociated from a precise spatial sampling of vi-
sual input and was not involved in their development of reading skills.
Author statement
Xiujie Yang: conceptualization, methodology, formal analysis, writ-
ing – original draft, writing – review & editing, visualization.
Jia Zhang: methodology, formal analysis, validation, writing – re-
view & editing, visualization.
Yaping Lv: methodology, validation, formal analysis.
Fang Wang: methodology, validation.
Guosheng Ding: software, methodology, validation, writing- re-
viewing.
Manli Zhang: writing- reviewing and editing, validation.
Xiangzhi Meng: conceptualization, writing – original draft, writing-
reviewing, validation, supervision.
Yan Song: conceptualization, writing- reviewing, validation, super-
vision.
Data and code availability statements
All of the data used in the current study were collected and shared
by Song’s lab, Meng’s lab (corresponding authors’ labs), and Ding’s lab.
This experiment includes fifty-two Chinese-speaking children. Written
consent was obtained from each participant and his/her guardians be-
fore the experiment. All of the participants were selected and recruited
from several primary schools in Beijing, China.
We acknowledged that sharing data is a very good idea and practice.
However, we had promised our participants that we would keep all of
their information as well as the data a secret and not share with others
unless we get their permission. Given the project is still ongoing, cur-
rently we prefer to keep the participants’ information and the data that
we collected in privacy before the project is completely done. Neverthe-
less, the data that support the findings of this study are available from
the corresponding author upon reasonable request with signing a data
sharing agreement.
In the data-sharing agreement, the receiver should state as specifi-
cally as possible how the receiver will use the data. For the period of
X. Yang, J. Zhang, Y. Lv et al.
agreement, we clearly define that the provider will give the data to the
receiver within three working days upon request, and the receiver will
be able to use the data within ten working days. To ensure that data re-
main confidential, the data should be returned to the provider or should
be deleted from their hard drives after usage. The receiver cannot share,
sell or distribute data findings or any part of the database to another
agency. Because some data contain information that can be linked to
individuals, personal data should remain confidential and should not be
disclosed verbally or in writing to an unauthorised third party, by acci-
dent or otherwise. The receiver should not report information that iden-
tifies individuals. Data will be transferred from the provider to the re-
ceiver electronically. For data security, electronic copies of data should
be password protected or kept on a secure disk. Everyone at the receiver
agency have the same level of access to data. If the receiver generates
a report based on the data, the report belongs to the receiver and the
provider. The monetary costs of sharing the data should be paid by the
receiver if needed.
Supplementary materials
Supplementary material associated with this article can be found, in
the online version, at doi:10.1016/j.neuroimage.2021.117911.
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