Convergent and divergent brain structural and functional abnormalities associated with developmental dyslexia

  1. Xiaohui Yan
  2. Ke Jiang
  3. Hui Li
  4. Ziyi Wang
  5. Kyle Perkins
  6. Fan Cao

  • Curated by eLife

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    Evaluation Summary:

    In this rigorously conducted meta-analytic study, the authors investigated the functional and structural abnormalities associated with developmental dyslexia across languages. Convergent and divergent functional and structural changes as well as language-universal and language-specific brain alternations related to dyslexia are found. In general, the study has generated important results and the findings are of interest to readers in educational psychology/neuroscience fields, especially those focusing on reading development and dyslexia. The analytic approach used in this study is cutting-edge, the data support the main claims, and a detailed discussion is presented.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 agreed to share their name with the authors.)

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Abstract

Brain abnormalities in the reading network have been repeatedly reported in individuals with developmental dyslexia (DD); however, it is still not totally understood where the structural and functional abnormalities are consistent/inconsistent across languages. In the current multimodal meta-analysis, we found convergent structural and functional alterations in the left superior temporal gyrus across languages, suggesting a neural signature of DD. We found greater reduction in grey matter volume and brain activation in the left inferior frontal gyrus in morpho-syllabic languages (e.g. Chinese) than in alphabetic languages, and greater reduction in brain activation in the left middle temporal gyrus and fusiform gyrus in alphabetic languages than in morpho-syllabic languages. These language differences are explained as consequences of being DD while learning a specific language. In addition, we also found brain regions that showed increased grey matter volume and brain activation, presumably suggesting compensations and brain regions that showed inconsistent alterations in brain structure and function. Our study provides important insights about the etiology of DD from a cross-linguistic perspective with considerations of consistency/inconsistency between structural and functional alterations.

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  1. Version published to 10.7554/elife.69523 on eLife
  2. eLife

    Author Response:

    Reviewer #1:

    Systematic reviews and meta-analyses are essential tools for synthesizing empirical evidence to advance our knowledge in life science. In this rigorously conducted meta-analytic study, the authors analyzed the data from 119 experiments from 110 published articles (92 on brain functional experiments from 87 articles and 27 on brain structural experiments from 23 papers) and investigated the functional and structural abnormalities associated with developmental dyslexia across languages. Convergent and divergent functional and structural changes as well as language-universal and language-specific brain alternations related to dyslexia are found. In general, the study has generated important results and the findings are interesting.

    I have the following comment:

    Dyslexia in alphabetic languages is generally related to phonological deficits, so there are many neuroimaging experiments using phonology-based tasks. In Chinese, the core deficits of dyslexia are unknown, and neuroimaging tasks devised in the literature are more diverse. Although the authors have done well in Table 1 to specify the experimental tasks in various languages, the meta-analysis did not take into account the task types. I believe that in this article, it is not necessary to conduct task-type based meta-analyses, but one sentence or two in the Discussion section to mention this possibility and the limitation is necessary.

    We actually conducted a confirmation analysis in which we matched task in the two language groups. The results are consistent with the original findings. Please see pages 15-17, 36-37.

    Reviewer #2:

    In the present study, Xiaohui Yan and colleagues attempt to summarize the existing evidence on neurofunctional and neuroanatomical impairments in dyslexia (aka specific reading disorder) in different languages in a meta-analytic manner. The research questions the authors asked are essential but remain largely open. The meta-analysis is a powerful approach to address these problems, and the findings are appealing. Both universal and language-specific neural manifestations in dyslexia are revealed. With this knowledge, the researchers can design experiments to reveal/examine more specific hypotheses, while the educators can refine diagnostic methods and intervention programs. This study has several strengths, including (1) the research questions are explicitly and precisely declared at the beginning; (2) an advanced meta-analytic method (AES-SDM) was used; (3) a series of complementary analyses are done, including a confirmation study with well-matched English and Chinese studies was conducted; (4) a comprehensive discussion is given. At the same time, as too many questions are asked, the analyses/results/interpretations became quite complicated and sometimes hard to follow. In addition, several factors need to be further taken into consideration in data analysis and result explanation. Finally, it should be noted that given meta-analysis is a way to summarize the previous findings, it is necessary to conduct further studies based on it to directly examine the hypotheses. All in all, the main claims are supported by the data, while additional analyses would provide further support.

    I have three main concerns:

    1. The imbalanced numbers of studies in alphabetic and morpho-syllabic languages may bias the results of primary meta-analysis pooling all studies together. Specifically, since there are many more alphabetic studies in this field, the results will mainly reflect patterns in these languages. This can be seen, e.g., when comparing figures S1-S2 with figures S3-S6. In this case, the result cannot answer whether there are the same functional and structural impairments in dyslexia in alphabetic and morpho-syllabic languages (i.e., the "both" question). The same issue exists for the multi-modal analysis across languages.

    We agree with the reviewer. We deleted the overall analysis and only keep analysis for each language group, as well as the comparisons and conjunctions between them, so that the results can show language differences as well as common findings in both groups.

    1. Age range difference may significantly influence the results of the primary meta-analysis across languages. It is shown in p. 15, lines 297-298, "the mean age was 16.55 years for controls and 16.23 years for participants with DD." However, such adolescent age ranges are a result of pooling studies in children and adults together. Given that (1) it has been revealed in previous literatures that participant's age modulates the neural manifestation in dyslexia, (2) fewer adolescent studies exist in alphabetic languages, and (3) research on morpho-syllabic languages is almost with children, the findings of the primary analysis might be influenced by age-related effect.

    We conducted a confirmation analysis with only alphabetic studies on children and we replicated previous findings of language differences between alphabetic and morpho-syllabic languages (page 15, 36). It suggests the language differences we found cannot be due to unmatched age ranges in the two language groups.

    1. Some statements are out of the scope of this study and can be misleading. For instance, in the abstract (p.2, lines 17-19), it says, "…it is still not totally understood where and why the structural and functional abnormalities are consistent/inconsistent across languages." However, while the "why" question is an important one, unfortunately, the current meta-analysis does not answer it.

    We deleted “why” in the abstract.

  3. eLife

    Evaluation Summary:

    In this rigorously conducted meta-analytic study, the authors investigated the functional and structural abnormalities associated with developmental dyslexia across languages. Convergent and divergent functional and structural changes as well as language-universal and language-specific brain alternations related to dyslexia are found. In general, the study has generated important results and the findings are of interest to readers in educational psychology/neuroscience fields, especially those focusing on reading development and dyslexia. The analytic approach used in this study is cutting-edge, the data support the main claims, and a detailed discussion is presented.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 agreed to share their name with the authors.)

  4. eLife

    Reviewer #1 (Public Review):

    Systematic reviews and meta-analyses are essential tools for synthesizing empirical evidence to advance our knowledge in life science. In this rigorously conducted meta-analytic study, the authors analyzed the data from 119 experiments from 110 published articles (92 on brain functional experiments from 87 articles and 27 on brain structural experiments from 23 papers) and investigated the functional and structural abnormalities associated with developmental dyslexia across languages. Convergent and divergent functional and structural changes as well as language-universal and language-specific brain alternations related to dyslexia are found. In general, the study has generated important results and the findings are interesting.

    I have the following comment:

    Dyslexia in alphabetic languages is generally related to phonological deficits, so there are many neuroimaging experiments using phonology-based tasks. In Chinese, the core deficits of dyslexia are unknown, and neuroimaging tasks devised in the literature are more diverse. Although the authors have done well in Table 1 to specify the experimental tasks in various languages, the meta-analysis did not take into account the task types. I believe that in this article, it is not necessary to conduct task-type based meta-analyses, but one sentence or two in the Discussion section to mention this possibility and the limitation is necessary.

  5. eLife

    Reviewer #2 (Public Review):

    In the present study, Xiaohui Yan and colleagues attempt to summarize the existing evidence on neurofunctional and neuroanatomical impairments in dyslexia (aka specific reading disorder) in different languages in a meta-analytic manner. The research questions the authors asked are essential but remain largely open. The meta-analysis is a powerful approach to address these problems, and the findings are appealing. Both universal and language-specific neural manifestations in dyslexia are revealed. With this knowledge, the researchers can design experiments to reveal/examine more specific hypotheses, while the educators can refine diagnostic methods and intervention programs. This study has several strengths, including (1) the research questions are explicitly and precisely declared at the beginning; (2) an advanced meta-analytic method (AES-SDM) was used; (3) a series of complementary analyses are done, including a confirmation study with well-matched English and Chinese studies was conducted; (4) a comprehensive discussion is given. At the same time, as too many questions are asked, the analyses/results/interpretations became quite complicated and sometimes hard to follow. In addition, several factors need to be further taken into consideration in data analysis and result explanation. Finally, it should be noted that given meta-analysis is a way to summarize the previous findings, it is necessary to conduct further studies based on it to directly examine the hypotheses. All in all, the main claims are supported by the data, while additional analyses would provide further support.

    I have three main concerns:

    1. The imbalanced numbers of studies in alphabetic and morpho-syllabic languages may bias the results of primary meta-analysis pooling all studies together. Specifically, since there are many more alphabetic studies in this field, the results will mainly reflect patterns in these languages. This can be seen, e.g., when comparing figures S1-S2 with figures S3-S6. In this case, the result cannot answer whether there are the same functional and structural impairments in dyslexia in alphabetic and morpho-syllabic languages (i.e., the "both" question). The same issue exists for the multi-modal analysis across languages.

    2. Age range difference may significantly influence the results of the primary meta-analysis across languages. It is shown in p. 15, lines 297-298, "the mean age was 16.55 years for controls and 16.23 years for participants with DD." However, such adolescent age ranges are a result of pooling studies in children and adults together. Given that (1) it has been revealed in previous literatures that participant's age modulates the neural manifestation in dyslexia, (2) fewer adolescent studies exist in alphabetic languages, and (3) research on morpho-syllabic languages is almost with children, the findings of the primary analysis might be influenced by age-related effect.

    3. Some statements are out of the scope of this study and can be misleading. For instance, in the abstract (p.2, lines 17-19), it says, "...it is still not totally understood where and why the structural and functional abnormalities are consistent/inconsistent across languages." However, while the "why" question is an important one, unfortunately, the current meta-analysis does not answer it.

  6. Version published to 10.1101/2021.05.10.443380v1 on bioRxiv