Cognitive and brain development is independently influenced by socioeconomic status and polygenic scores for educational attainment

N. Judd; B. Sauce; J. Wiedenhoeft; J. Tromp; B. Chaarani; A. Schliep; B. van Noort; J. Penttilä; Y. Grimmer; C. Insensee; A. Becker; T. Banaschewski; A.L.W. Bokde; E.B. Quinlan; S. Desrivières; H. Flor; A. Grigis; P. Gowland; A. Heinz; B. Ittermann; J.-L. Martinot; M.-L.P. Martinot; E. Artiges; F. Nees; D.P. Orfanos; T. Paus; L. Poustka; S. Hohmann; S. Millenet; J.H. Fröhner; M.N. Smolka; H. Walter; R. Whelan; G. Schumann; H. Garavan; T. Klingberg

doi:10.1073/pnas.2001228117

Cognitive and brain development is independently influenced by socioeconomic status and polygenic scores for educational attainment

N. Judd, B. Sauce, J. Wiedenhoeft, J. Tromp, B. Chaarani, A. Schliep, B. van Noort, J. Penttilä, Y. Grimmer, C. Insensee, A. Becker, T. Banaschewski, A.L.W. Bokde, E.B. Quinlan, S. Desrivières, H. Flor, A. Grigis, P. Gowland, A. Heinz, B. IttermannJ.-L. Martinot, M.-L.P. Martinot, E. Artiges, F. Nees, D.P. Orfanos, T. Paus, L. Poustka, S. Hohmann, S. Millenet, J.H. Fröhner, M.N. Smolka, H. Walter, R. Whelan, G. Schumann, H. Garavan, T. Klingberg

Research output: Contribution to Journal › Article › Academic › peer-review

Abstract

© 2020 National Academy of Sciences. All rights reserved.Genetic factors and socioeconomic status (SES) inequalities play a large role in educational attainment, and both have been associated with variations in brain structure and cognition. However, genetics and SES are correlated, and no prior study has assessed their neural associations independently. Here we used a polygenic score for educational attainment (EduYears-PGS), as well as SES, in a longitudinal study of 551 adolescents to tease apart genetic and environmental associations with brain development and cognition. Subjects received a structural MRI scan at ages 14 and 19. At both time points, they performed three working memory (WM) tasks. SES and EduYears-PGS were correlated (r = 0.27) and had both common and independent associations with brain structure and cognition. Specifically, lower SES was related to less total cortical surface area and lower WM. EduYears-PGS was also related to total cortical surface area, but in addition had a regional association with surface area in the right parietal lobe, a region related to nonverbal cognitive functions, including mathematics, spatial cognition, and WM. SES, but not EduYears-PGS, was related to a change in total cortical surface area from age 14 to 19. This study demonstrates a regional association of EduYears-PGS and the independent prediction of SES with cognitive function and brain development. It suggests that the SES inequalities, in particular parental education, are related to global aspects of cortical development, and exert a persistent influence on brain development during adolescence.

Original language	English
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	117
Issue number	22
DOIs	https://doi.org/10.1073/pnas.2001228117
Publication status	Published - 2 Jun 2020
Externally published	Yes

Funding

Disorders) (695313), ERANID (Understanding the Interplay between Cultural, Biological, and Subjective Factors in Drug Use Pathways) (PR-ST-0416-10004), BRIDGET (JPND: Brain Imaging, Cognition Dementia and Next-Generation Genomics) (MR/N027558/1), Human Brain Project (HBP SGA 2, 785907), FP7 Project MATRICS (603016), Medical Research Council Grant c-VEDA (Consortium on Vulnerability to Externalizing Disorders and Addictions) (MR/N000390/ 1), National Institute for Health Research Biomedical Research Centre at South London, Maudsley National Health Service Foundation Trust, King’s College London, Bundesministerium für Bildung und Forschung (Grants 01GS08152, 01EV0711; Forschungsnetz AERIAL 01EE1406A, 01EE1406B), Deutsche For-schungsgemeinschaft (Grants SM 80/7-2, SFB 940, TRR 265, NE 1383/14-1), Medical Research Foundation and Medical Research Council (Grants MR/ R00465X/1, MR/S020306/1), and NIH-funded ENIGMA (Grants 5U54EB020403-05, 1R56AG058854-01). Further support was provided by grants from the Agence Nationale de la Recherche (ANR) (Projects AF12-NEUR0008-01-WM2NA, ANR-12-SAMA-0004), Eranet Neuron (ANR-18-NEUR00002-01), Fondation de France (00081242), Fondation pour la Recherche Médicale (DPA20140629802), Mission Interministérielle de Lutte-contre-les-Drogues-et-les-Conduites-Addictives, Assistance-Publique-Hôpitaux-de-Paris, and INSERM (interface grant), Paris Sud University (IDEX 2012), Fondation de l’Avenir (Grant AP-RM-17-013), Fédération pour la Recherche sur le Cerveau, NIH, and Science Foundation Ireland (16/ ERCD/3797) (Axon, Testosterone and Mental Health during Adolescence; R01 MH085772-01A1), and NIH Consortium Grant U54 EB020403, supported by a cross-NIH alliance that funds Big Data to Knowledge Centers of Excellence. This work received support from the following sources: Vetenskapsradet (Swedish Research Council; 2015-02850), Wenner-Gren Foundation (UPD2018-0295), NIH (Meaningful Data Compression and Reduction of High-Throughput Sequencing Data) (1 U01 CA198952-01), European Union-funded FP6 Integrated Project IMAGEN (Reinforcement-Related Behaviour in Normal Brain Function and Psychopathology) (LSHMCT-2007-037286), Horizon 2020-funded European Research Council Advanced Grant STRATIFY (Brain Network-Based Stratification of Reinforcement-Related Disorders) (695313), ERANID (Understanding the Interplay between Cultural, Biological, and Subjective Factors in Drug Use Pathways) (PR-ST-0416-10004), BRIDGET (JPND: Brain Imaging, Cognition Dementia and Next-Generation Genomics) (MR/N027558/1), Human Brain Project (HBP SGA 2, 785907), FP7 Project MATRICS (603016), Medical Research Council Grant c-VEDA (Consortium on Vulnerability to Externalizing Disorders and Addictions) (MR/N000390/ 1), National Institute for Health Research Biomedical Research Centre at South London, Maudsley National Health Service Foundation Trust, King's College London, Bundesministerium für Bildung und Forschung (Grants 01GS08152, 01EV0711; Forschungsnetz AERIAL 01EE1406A, 01EE1406B), Deutsche Forschungsgemeinschaft (Grants SM 80/7-2, SFB 940, TRR 265, NE 1383/14-1), Medical Research Foundation and Medical Research Council (Grants MR/ R00465X/1, MR/S020306/1), and NIH-funded ENIGMA (Grants 5U54EB020403-05, 1R56AG058854-01). Further support was provided by grants from the Agence Nationale de la Recherche (ANR) (Projects AF12-NEUR0008-01-WM2NA, ANR-12SAMA-0004), Eranet Neuron (ANR-18-NEUR00002-01), Fondation de France (00081242), Fondation pour la Recherche Médicale (DPA20140629802), Mission Interministérielle de Lutte-contre-les-Drogues-et-les-Conduites-Addictives, Assistance-Publique-Hôpitaux-de-Paris, and INSERM (interface grant), Paris Sud University (IDEX 2012), Fondation de l'Avenir (Grant AP-RM-17-013), Fédération pour la Recherche sur le Cerveau, NIH, and Science Foundation Ireland (16/ ERCD/3797) (Axon, Testosterone and Mental Health during Adolescence; R01 MH085772-01A1), and NIH Consortium Grant U54 EB020403, supported by a cross-NIH alliance that funds Big Data to Knowledge Centers of Excellence. ACKNOWLEDGMENTS. This work received support from the following sources: Vetenskapsradet (Swedish Research Council; 2015-02850), Wen-ner-Gren Foundation (UPD2018-0295), NIH (Meaningful Data Compression and Reduction of High-Throughput Sequencing Data) (1 U01 CA198952-01), European Union-funded FP6 Integrated Project IMAGEN (Reinforcement-Related Behaviour in Normal Brain Function and Psychopathology) (LSHM-CT-2007-037286), Horizon 2020-funded European Research Council Advanced Grant STRATIFY (Brain Network-Based Stratification of Reinforcement-Related

Funders	Funder number
BRIDGET
ERANID	PR-ST-0416-10004
EraNet Neuron	ANR-18-NEUR00002-01
European Union-funded FP6	LSHM-CT-2007-037286
Horizon 2020-funded European Research Council	695313
Maudsley National Health Service Foundation Trust
Testosterone and Mental Health	R01 MH085772-01A1, U54 EB020403
Vetenskapsradet
National Institutes of Health	5U54EB020403-05, 1R56AG058854-01
National Cancer Institute	U01CA198952
Wenner-Gren Foundation	UPD2018-0295
Fondation de l'Avenir pour la Recherche Médicale Appliquée	AP-RM-17-013
King’s College London
Seventh Framework Programme	603016
EU Joint Programme – Neurodegenerative Disease Research	785907, MR/N027558/1
Wenner-Gren Stiftelserna
Medical Research Council	MR/N000390/ 1
King's College London
Science Foundation Ireland	16/ ERCD/3797
Deutsche Forschungsgemeinschaft	SM 80/7-2, NE 1383/14-1, SFB 940, TRR 265
Agence Nationale de la Recherche	ANR-12-SAMA-0004, AF12-NEUR0008-01-WM2NA
Institut national de la santé et de la recherche médicale
Bundesministerium für Bildung und Forschung	01GS08152, 01EV0711, AERIAL 01EE1406A, 01EE1406B
Fondation pour la Recherche Médicale	DPA20140629802
Vetenskapsrådet	2015-02850
Fondation de France	00081242
Fédération pour la Recherche sur le Cerveau
Université Paris-Sud
Medical Research Foundation	MR/ R00465X/1, MR/S020306/1
National Institute for Health Research Southampton Biomedical Research Centre

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10.1073/pnas.2001228117

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Judd, N., Sauce, B., Wiedenhoeft, J., Tromp, J., Chaarani, B., Schliep, A., van Noort, B., Penttilä, J., Grimmer, Y., Insensee, C., Becker, A., Banaschewski, T., Bokde, A. L. W., Quinlan, E. B., Desrivières, S., Flor, H., Grigis, A., Gowland, P., Heinz, A., ... Klingberg, T. (2020). Cognitive and brain development is independently influenced by socioeconomic status and polygenic scores for educational attainment. Proceedings of the National Academy of Sciences of the United States of America, 117(22). https://doi.org/10.1073/pnas.2001228117

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title = "Cognitive and brain development is independently influenced by socioeconomic status and polygenic scores for educational attainment",

abstract = "{\textcopyright} 2020 National Academy of Sciences. All rights reserved.Genetic factors and socioeconomic status (SES) inequalities play a large role in educational attainment, and both have been associated with variations in brain structure and cognition. However, genetics and SES are correlated, and no prior study has assessed their neural associations independently. Here we used a polygenic score for educational attainment (EduYears-PGS), as well as SES, in a longitudinal study of 551 adolescents to tease apart genetic and environmental associations with brain development and cognition. Subjects received a structural MRI scan at ages 14 and 19. At both time points, they performed three working memory (WM) tasks. SES and EduYears-PGS were correlated (r = 0.27) and had both common and independent associations with brain structure and cognition. Specifically, lower SES was related to less total cortical surface area and lower WM. EduYears-PGS was also related to total cortical surface area, but in addition had a regional association with surface area in the right parietal lobe, a region related to nonverbal cognitive functions, including mathematics, spatial cognition, and WM. SES, but not EduYears-PGS, was related to a change in total cortical surface area from age 14 to 19. This study demonstrates a regional association of EduYears-PGS and the independent prediction of SES with cognitive function and brain development. It suggests that the SES inequalities, in particular parental education, are related to global aspects of cortical development, and exert a persistent influence on brain development during adolescence.",

author = "N. Judd and B. Sauce and J. Wiedenhoeft and J. Tromp and B. Chaarani and A. Schliep and {van Noort}, B. and J. Penttil{\"a} and Y. Grimmer and C. Insensee and A. Becker and T. Banaschewski and A.L.W. Bokde and E.B. Quinlan and S. Desrivi{\`e}res and H. Flor and A. Grigis and P. Gowland and A. Heinz and B. Ittermann and J.-L. Martinot and M.-L.P. Martinot and E. Artiges and F. Nees and D.P. Orfanos and T. Paus and L. Poustka and S. Hohmann and S. Millenet and J.H. Fr{\"o}hner and M.N. Smolka and H. Walter and R. Whelan and G. Schumann and H. Garavan and T. Klingberg",

year = "2020",

month = jun,

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doi = "10.1073/pnas.2001228117",

language = "English",

volume = "117",

journal = "Proceedings of the National Academy of Sciences of the United States of America",

issn = "0027-8424",

publisher = "National Acad Sciences",

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Judd, N, Sauce, B, Wiedenhoeft, J, Tromp, J, Chaarani, B, Schliep, A, van Noort, B, Penttilä, J, Grimmer, Y, Insensee, C, Becker, A, Banaschewski, T, Bokde, ALW, Quinlan, EB, Desrivières, S, Flor, H, Grigis, A, Gowland, P, Heinz, A, Ittermann, B, Martinot, J-L, Martinot, M-LP, Artiges, E, Nees, F, Orfanos, DP, Paus, T, Poustka, L, Hohmann, S, Millenet, S, Fröhner, JH, Smolka, MN, Walter, H, Whelan, R, Schumann, G, Garavan, H & Klingberg, T 2020, 'Cognitive and brain development is independently influenced by socioeconomic status and polygenic scores for educational attainment', Proceedings of the National Academy of Sciences of the United States of America, vol. 117, no. 22. https://doi.org/10.1073/pnas.2001228117

Cognitive and brain development is independently influenced by socioeconomic status and polygenic scores for educational attainment. / Judd, N.; Sauce, B.; Wiedenhoeft, J. et al.
In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 117, No. 22, 02.06.2020.

Research output: Contribution to Journal › Article › Academic › peer-review

TY - JOUR

T1 - Cognitive and brain development is independently influenced by socioeconomic status and polygenic scores for educational attainment

AU - Judd, N.

AU - Sauce, B.

AU - Wiedenhoeft, J.

AU - Tromp, J.

AU - Chaarani, B.

AU - Schliep, A.

AU - van Noort, B.

AU - Penttilä, J.

AU - Grimmer, Y.

AU - Insensee, C.

AU - Becker, A.

AU - Banaschewski, T.

AU - Bokde, A.L.W.

AU - Quinlan, E.B.

AU - Desrivières, S.

AU - Flor, H.

AU - Grigis, A.

AU - Gowland, P.

AU - Heinz, A.

AU - Ittermann, B.

AU - Martinot, J.-L.

AU - Martinot, M.-L.P.

AU - Artiges, E.

AU - Nees, F.

AU - Orfanos, D.P.

AU - Paus, T.

AU - Poustka, L.

AU - Hohmann, S.

AU - Millenet, S.

AU - Fröhner, J.H.

AU - Smolka, M.N.

AU - Walter, H.

AU - Whelan, R.

AU - Schumann, G.

AU - Garavan, H.

AU - Klingberg, T.

PY - 2020/6/2

Y1 - 2020/6/2

N2 - © 2020 National Academy of Sciences. All rights reserved.Genetic factors and socioeconomic status (SES) inequalities play a large role in educational attainment, and both have been associated with variations in brain structure and cognition. However, genetics and SES are correlated, and no prior study has assessed their neural associations independently. Here we used a polygenic score for educational attainment (EduYears-PGS), as well as SES, in a longitudinal study of 551 adolescents to tease apart genetic and environmental associations with brain development and cognition. Subjects received a structural MRI scan at ages 14 and 19. At both time points, they performed three working memory (WM) tasks. SES and EduYears-PGS were correlated (r = 0.27) and had both common and independent associations with brain structure and cognition. Specifically, lower SES was related to less total cortical surface area and lower WM. EduYears-PGS was also related to total cortical surface area, but in addition had a regional association with surface area in the right parietal lobe, a region related to nonverbal cognitive functions, including mathematics, spatial cognition, and WM. SES, but not EduYears-PGS, was related to a change in total cortical surface area from age 14 to 19. This study demonstrates a regional association of EduYears-PGS and the independent prediction of SES with cognitive function and brain development. It suggests that the SES inequalities, in particular parental education, are related to global aspects of cortical development, and exert a persistent influence on brain development during adolescence.

AB - © 2020 National Academy of Sciences. All rights reserved.Genetic factors and socioeconomic status (SES) inequalities play a large role in educational attainment, and both have been associated with variations in brain structure and cognition. However, genetics and SES are correlated, and no prior study has assessed their neural associations independently. Here we used a polygenic score for educational attainment (EduYears-PGS), as well as SES, in a longitudinal study of 551 adolescents to tease apart genetic and environmental associations with brain development and cognition. Subjects received a structural MRI scan at ages 14 and 19. At both time points, they performed three working memory (WM) tasks. SES and EduYears-PGS were correlated (r = 0.27) and had both common and independent associations with brain structure and cognition. Specifically, lower SES was related to less total cortical surface area and lower WM. EduYears-PGS was also related to total cortical surface area, but in addition had a regional association with surface area in the right parietal lobe, a region related to nonverbal cognitive functions, including mathematics, spatial cognition, and WM. SES, but not EduYears-PGS, was related to a change in total cortical surface area from age 14 to 19. This study demonstrates a regional association of EduYears-PGS and the independent prediction of SES with cognitive function and brain development. It suggests that the SES inequalities, in particular parental education, are related to global aspects of cortical development, and exert a persistent influence on brain development during adolescence.

U2 - 10.1073/pnas.2001228117

DO - 10.1073/pnas.2001228117

M3 - Article

SN - 0027-8424

VL - 117

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

IS - 22

ER -

Cognitive and brain development is independently influenced by socioeconomic status and polygenic scores for educational attainment

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