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Brain structure, phenotypic and genetic correlates of reading performance

Nature Human Behaviour volume 7, pages 1120–1134 (2023)Cite this article

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Abstract

Reading is an evolutionarily recent development that recruits and tunes brain circuitry connecting primary- and language-processing regions. We investigated whether metrics of the brain’s physical structure correlate with reading performance and whether genetic variants affect this relationship. To this aim, we used the Adolescent Brain Cognitive Development dataset (n = 9,013) of 9–10-year-olds and focused on 150 measures of cortical surface area (CSA) and thickness. Our results reveal that reading performance is associated with nine measures of brain structure including relevant regions of the reading network. Furthermore, we show that this relationship is partially mediated by genetic factors for two of these measures: the CSA of the entire left hemisphere and, specifically, of the left superior temporal gyrus CSA. These effects emphasize the complex and subtle interplay between genes, brain and reading, which is a partly heritable polygenic skill that relies on a distributed network.

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Fig. 1: Overview of study goals and analytical approaches.
Fig. 2: Effect of left-hemisphere cortical measures on reading performance (n = 9,013).
Fig. 3: Decile plots for PGS of cognitive performance on left-hemisphere CSA measures (n = 4,080).
Fig. 4: Mediation of the CSA on the association between the PGSCP and reading.

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Data availability

ABCD data are publicly available through the NIMH Data Archive (https://data-archive.nimh.nih.gov/abcd). The current study analysed the full baseline sample (n ≅ 11,878) from the ABCD data release 3.0 RDS (https://doi.org/10.15154/1520591) and the Genotyping Data from the ABCD Curated Annual Release 3.0 (NDA Study 901; https://doi.org/10.15154/1519007). All variables included in the current study are listed and described in Supplementary Table 1. GWAS summary statistics used in this study are available from the NHGRI-EBI GWAS Catalogue https://www.ebi.ac.uk/gwas/downloads/summary-statistics and the Oxford Brain Imaging Genetics Server, BIG40 (https://open.win.ox.ac.uk/ukbiobank/big40/). Supplementary Table 7 contains the references and field IDs for all analysed traits.

Code availability

The custom code associated with this study is publicly available at https://github.com/amaiacc/MS-brain-reading-genetics/.

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Acknowledgements

We thank J. Barry and C. Handley for helping with manuscript proofreading. This research is supported by the Basque Government through the BERC 2022–2025 programme and by the Spanish State Research Agency through BCBL Severo Ochoa excellence accreditation no. CEX2020-001010-S. A.C.-C. received funding from the Spanish Ministry of Science and Innovation and the Agencia Estatal de Investigación through Ayudas Juan de la Cierva-Incorporación (ref. no. IJC2018-036023-I), the Programa Fellows Gipuzkoa de atracción y retención de talento from the Diputación Foral de Gipuzkoa. P.M.P-A. is supported by grants from the Spanish Ministry of Science and Innovation (grant no. PID2021-123574NB-I00), from the Basque Government (grant no. PIBA-2021-1-0003) and from the Red guipuzcoana de Ciencia, Tecnología e Innovación of the Diputación Foral de Gipuzkoa (grant no. FA/OF 422/2022). M.C. is supported by the Spanish Ministry of Science and Innovation grant (no. PID2021-122918OB-I00) and ‘La Caixa’ Foundation (grant no. ID 100010434), under the agreement no. HR18-00178-DYSTHAL. The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript. Data used in the preparation of this article were obtained from the ABCD Study (https://abcdstudy.org/) and are held in the National Institute of Mental Health (NIMH) Data Archive. This is a multisite, longitudinal study designed to recruit more than 10,000 children aged 9–10 and follow them over 10 years into early adulthood. The ABCD Study is supported by the NIH and additional federal partners under award numbers U01DA041022, U01DA041028, U01DA041048, U01DA041089, U01DA041106, U01DA041117, U01DA041120, U01DA041134, U01DA041148, U01DA041156, U01DA041174, U24DA041123 and U24DA041147. A full list of supporters is available at https://abcdstudy.org/federal-partners/. A listing of participating sites and a complete listing of the study investigators can be found at https://abcdstudy.org/principal-investigators/. ABCD consortium investigators designed and implemented the study and/or provided data but did not necessarily participate in the analysis or writing of this report. This manuscript reflects the views of the authors and may not reflect the opinions or views of the NIH or ABCD consortium investigators. The ABCD data repository grows and changes over time. The ABCD data used in this report came from https://doi.org/10.15154/1520591 and https://doi.org/10.15154/1519007 (genotyping data).

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Authors and Affiliations

  1. Basque Center on Cognition, Brain and Language (BCBL), Donostia-San Sebastián, Spain

    Amaia Carrión-Castillo, Pedro M. Paz-Alonso & Manuel Carreiras

  2. Ikerbasque, Basque Foundation for Science, Bilbao, Spain

    Pedro M. Paz-Alonso & Manuel Carreiras

  3. University of the Basque Country, Bilbao, Spain

    Manuel Carreiras

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  1. Amaia Carrión-Castillo
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  3. Manuel Carreiras
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All authors conceived and designed the study. A.C.-C. analysed the data, made figures and wrote the first draft of the paper. All authors discussed the results and contributed towards the writing of the final version of the manuscript.

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Correspondence to Amaia Carrión-Castillo or Manuel Carreiras.

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Carrión-Castillo, A., Paz-Alonso, P.M. & Carreiras, M. Brain structure, phenotypic and genetic correlates of reading performance. Nat Hum Behav 7, 1120–1134 (2023). https://doi.org/10.1038/s41562-023-01583-z

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