A universal reading network and its modulation by writing system and reading ability in French and Chinese children

  1. Xiaoxia Feng
  2. Irene Altarelli
  3. Karla Monzalvo
  4. Guosheng Ding
  5. Franck Ramus
  6. Hua Shu
  7. Stanislas Dehaene
  8. Xiangzhi Meng  Is a corresponding author
  9. Ghislaine Dehaene-Lambertz  Is a corresponding author
  1. Cognitive Neuroimaging Unit, CEA DRF/I2BM, INSERM, NeuroSpin Center, Université Paris-Saclay, France
  2. State Key Laboratory of Cognitive Neuroscience and Learning & IDG/McGovern Institute for Brain Research, Beijing Normal University, China
  3. Université de Paris, LaPsyDÉ, CNRS, France
  4. Laboratoire de Sciences Cognitives et Psycholinguistique (ENS, CNRS, EHESS), Ecole Normale Supérieure, PSL Research University, France
  5. Collège de France, Université PSL Paris Sciences Lettres, France
  6. School of Psychological and Cognitive Sciences, Beijing Key Laboratory of Behavior and Mental Health, Peking University, China
  7. PekingU-PolyU Center for Child Development and Learning, Peking University, China
8 figures, 5 tables and 7 additional files

Figures

Figure 1 with 1 supplement
Category-specific circuits.

(A) Category-specific circuits across all participants (voxel-level p<0.001, cluster-level FWE corrected p<0.05). On the left, the reading circuit identified by the contrast Words > [Faces, Houses] …

Figure 1—figure supplement 1
Language × reading ability ANOVA analysis on children's activation to words.

(A) A few voxels in the left fusiform gyrus, left precentral and left superior temporal sulcus reached the voxel threshold (p=0.001) in the 2 × 2 language × reading ability ANOVA analysis. Only the …

Neural correlates of inter-individual variability in reading scores.

(A) The figure shows the regions whose activation in the words versus fixation contrast was positively correlated with reading scores across all participants at the whole-brain level (voxel-wise p<0.…

Regions of interest (ROIs) used to analyze the data.

(A) Each sphere represents a peak reported in the literature; Labels in white background indicate foci reported in meta-analyses of dyslexia in alphabetic languages; Labels in black background …

Figure 4 with 1 supplement
Effects of Reading ability and Language on the words versus fixation contrast in the selected ROIs.

Brain slices showed the literature-based ROIs (cyan) overlaid on the reading circuit (red-yellow) in our participants (Words > [Faces, Houses]). Plots show the mean activation for words > fixation, …

Figure 4—source data 1

Activation to words in each of the four groups and ROIs.

https://cdn.elifesciences.org/articles/54591/elife-54591-fig4-data1-v2.xlsx
Figure 4—figure supplement 1
Profile of activation to words (relative to fixation) in ROIs where the ANOVA did not reveal a significant effect.

Two ROIs on the right hemisphere (e.g. R.FFG and R.IOG) were not within the reading circuit identified in our participants. Neither the interaction of language × reading ability nor main effect of …

Figure 5 with 1 supplement
Multivariate pattern analysis indicating that the word-induced activation is less reproducible in poor readers.

Within the designated ROIs, we computed the correlation coefficient of the multivoxel patterns for the word versus fixation contrast in run 1 and in run 2 (within-category correlation). For the …

Figure 5—source data 1

Correlation coefficients for within-category patterns and between-category patterns in each of the four groups and ROIs.

https://cdn.elifesciences.org/articles/54591/elife-54591-fig5-data1-v2.xlsx
Figure 5—figure supplement 1
MVPA analyses.

All these regions showed a main effect of condition, with higher correlation coefficients in within-category than between-category. Besides, the left MFG and STS showed a main effect of reading …

Mosaic of preferences for different visual categories (Words, Faces and Houses) in the ventral visual cortex.

(A) Slices show the activation difference between a given category and the others across all participants. (B) fMRI signal change of Words relative to fixation in both Chinese and French children in …

Figure 6—source data 1

Activaions to different categories relative to fixation in ROIs in the ventral visual cortex.

https://cdn.elifesciences.org/articles/54591/elife-54591-fig6-data1-v2.xlsx
Author response image 1
Sensitivity analysis with a variety of priors in the post-hoc pairwise comparisons between controls and impaired-readers in each language (Left: Chinese children; Right: French children).
Author response image 2
Sensitivity analysis with a variety of priors in the post-hoc pairwise comparisons between Chinese and French children separately in control and impaired-reading children (Left: Controls; Right: impaired-readers).

Tables

Table 1
Characteristics of the four groups.
ChineseFrench
Typical readersPoor readersTypicalPoor readers
Sample size24242424
Age in months (SD)123 (11)123 (10)123 (11)123 (10)
Sex13M/11F16M/8F13M/11F16M/8F
Reading ability
(CI 95%)
0.67
(0.49 ~ 0.86)
−1.74
(−1.95 ~ −1.54)
0.73
(0.39 ~ 1.07)
−2.16
(−2.38 ~ −1.94)
Table 2
Regions of significant activations for each visual category vs. the two others across all participants.
RegionMNI coordinatesPeak p-valuePeak z-value
Words > others
 Left inferior frontal gyrus−48 12 302.06e-198.93
 Left precentral−39 0 361.45e-188.72
−51 6 392.91e-147.51
 Left superior temporal gyrus/sulcus−57 −30 32.39e-198.92
 Left middle temporal gyrus−51 −42 67.89e-188.52
 Left fusiform gyrus−48 −57 −151.69e-178.43
 Left Inferior parietal sulcus−45 −39 424.29e-147.46
 Right superior temporal sulcus57 −27 38.94e-106.02
Faces > others
 Left fusiform gyrus−39 −48 −213.28e-178.35
 Right fusiform gyrus42 −54 −186.14e-2610.47
 Right amygdala/hippocampus18 −9 −186.11e-229.56
 Left amygdala/hippocampus−18 −9 −183.91e-157.77
Houses > others
 Left fusiform gyrus−30 −48 −69.01e-5315.24
 Right fusiform gyrus30 −45 −92.90e-5014.86
27 −63 −92.40e-229.65
 Left calcarine−18 −54 98.66e-106.02
Table 3
Regions significantly correlated with reading scores across all participants at the whole-brain level.
RegionMNI coordinatesPeak p-valuePeak z-valueR-value
Left fusiform gyrus−42 −45 −186.65e-64.360.490
Right fusiform gyrus42 −66 −249.96e-64.270.512
Left precentral−36 −3 572.75e-64.540.467
Right precentral54 18 331.29e-54.210.432
Left middle frontal gyrus−36 12 271.92e-54.120.468
Right middle frontal gyrus45 6 547.72e-64.320.460
Left superior temporal sulcus−57 −24 01.00e-54.260.510
Right middle occipital gyrus27 −69 426.34e-64.370.448
Table 4
Bayes factor (BF10) in Bayesian ANOVA analyses of children’s activation to words versus fixation.
ROIsMain effect of languageMain effect of reading abilityInteractionPost-hoc analyses
Typical readers
(Chinese vs. French)
Poor readers
(Chinese vs. French)
Chinese children
(typical vs. poor readers)
French children
(typical vs. poor readers)
FFG0.2161528.9660.3130.2270.33713.57793.163
MFG80.2119.9480.3052.837309.6511.61629.351
STS0.22037.5070.3090.3870.2596.9335.076
PCG1.5325.6250.2751.7821.0752.6622.661
SPL7.0520.5620.3234.4861.7820.8220.332
pSTG9.9080.2891.0540.61674.0140.21523.744
  1. The value of Bayes factor BF10 means that data are n times more likely under alternative hypothesis (H1) than null hypothesis (H0). The alternative hypothesis in comparisons between typical and poor readers is group 1 (typical) > group2 (poor); the alternative hypothesis in comparisons between languages is group 1 (Chinese) > group2 (French).

Author response table 1
MeanCI 95%
Chinese typical readers0.670.44 ~ 0.89
Chinese impaired readers0.690.47 ~ 0.91
French typical readers-0.41-0.85 ~ 0.36
French impaired readers-0.11-0.63 ~ 0.41

Additional files

Supplementary file 1

Demography and performance on literacy tests for Chinese children.

https://cdn.elifesciences.org/articles/54591/elife-54591-supp1-v2.docx
Supplementary file 2

Demography and performance on literacy tests for French children.

https://cdn.elifesciences.org/articles/54591/elife-54591-supp2-v2.docx
Supplementary file 3

Regions of significant activations for each visual category vs. the two others in each group (individual voxel p=0.001, cluster-level FWE corrected).

https://cdn.elifesciences.org/articles/54591/elife-54591-supp3-v2.docx
Supplementary file 4

Summary of activation foci in meta-analyses of dyslexia in alphabetic languages.

https://cdn.elifesciences.org/articles/54591/elife-54591-supp4-v2.docx
Supplementary file 5

Summary of foci in meta-analyses of reading in Chinese.

https://cdn.elifesciences.org/articles/54591/elife-54591-supp5-v2.docx
Supplementary file 6

Distance between individual center of 10 most activated voxels and group peaks.

https://cdn.elifesciences.org/articles/54591/elife-54591-supp6-v2.docx
Transparent reporting form
https://cdn.elifesciences.org/articles/54591/elife-54591-transrepform-v2.pdf

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