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Structural and functional asymmetry of the neonatal cerebral cortex

Nature Human Behaviour volume 7, pages 942–955 (2023)Cite this article

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Abstract

Features of brain asymmetry have been implicated in a broad range of cognitive processes; however, their origins are still poorly understood. Here we investigated cortical asymmetries in 442 healthy term-born neonates using structural and functional magnetic resonance images from the Developing Human Connectome Project. Our results demonstrate that the neonatal cortex is markedly asymmetric in both structure and function. Cortical asymmetries observed in the term cohort were contextualized in two ways: by comparing them against cortical asymmetries observed in 103 preterm neonates scanned at term-equivalent age, and by comparing structural asymmetries against those observed in 1,110 healthy young adults from the Human Connectome Project. While associations with preterm birth and biological sex were minimal, significant differences exist between birth and adulthood.

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Fig. 1: Distribution of GA at birth and PMA at scan for preterm and term-born neonates.
Fig. 2: Median asymmetry indices of structural and functional asymmetries across the healthy term-born neonatal cohort scanned at TEA.
Fig. 3: \(-{\log}_{10}{(P)}_{{\mathrm{...mcfwe}}}\) value maps for structural and functional asymmetries in the healthy term-born neonatal cortex at TEA.
Fig. 4: Median asymmetry indices of structural and functional asymmetries across the healthy term-born neonatal cohort scanned at TEA.
Fig. 5: Comparison of structural asymmetries between the dHCP and HCP—YA.
Fig. 6: Development and validation of a symmetric surface-based atlas.

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Data availability

The images used to produce the figures shown here are available as scenes through https://balsa.wustl.edu/study/2xrBN. UKB asymmetry summary measures reported in Sha et al.29 are available at https://archive.mpi.nl/mpi/islandora/object/mpi:1839_24c1553d_3ee8_4879_8877_79ca19a0ac6a?asOfDateTime=2021-11-02T14:30:48.830Z. The following templates are publicly available: dhcpSym spatiotemporal cortical surface atlas: https://brain-development.org/brain-atlases/atlases-from-the-dhcp-project/cortical-surface-template/; HCP sulcal depth template: https://github.com/Washington-University/HCPpipelines/tree/master/global/templates/standard_mesh_atlases; deformations between HCP fs_LR and FreeSurfer fsaverage space: https://github.com/Washington-University/HCPpipelines/tree/master/global/templates/standard_mesh_atlases/resample_fsaverage. Demographic data for the dHCP are available at https://github.com/BioMedIA/dHCP-release-notes/blob/master/supplementary_files/combined.tsv.

Code availability

This study utilized the following open software and code: surface atlas creation (without symmetrization): https://github.com/jelenabozek/SurfaceAtlasConstruction; dHCP structural pipeline: https://github.com/BioMedIA/dhcp-structural-pipeline and dHCP functional pipeline: https://git.fmrib.ox.ac.uk/seanf/dhcp-neonatal-fmri-pipeline/-/tree/master; FSL version 6.0.3 (for MIGP and MELODIC): https://fsl.fmrib.ox.ac.uk/fsl/fslwiki/; symmetrizing resting-state timeseries: https://git.fmrib.ox.ac.uk/seanf/asymmetry-analysis; surface registration, metric and anatomical mesh resampling: https://github.com/ecr05/dHCP_template_alignment; MSM: https://github.com/ecr05/MSM_HOCR/releases; dHCP MSM configuration file: https://github.com/ecr05/dHCP_template_alignment/blob/master/configs/config_subject_to_40_week_template_3rd_release; HCP MSM configuration file optimized for sulcal depth: https://github.com/metrics-lab/CorticalAsymmetry/blob/main/config_standard_MSMstrain_HCP_CorticalAsymmetry; PALM version alpha119: https://github.com/andersonwinkler/PALM; INTERGROWTH-21 growth curves: http://intergrowth21.ndog.ox.ac.uk/; Connectome Workbench: https://www.humanconnectome.org/software/connectome-workbench; Pingouin Python package version 0.5.3: https://pingouin-stats.org/. Code used to perform image processing and asymmetry analyses is available at https://github.com/metrics-lab/CorticalAsymmetry.

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Acknowledgements

The authors thank the participants and families recruited in the dHCP, and all the neonatal staff at the Evelina Newborn Imaging Center, St Thomas’ Hospital, Guy’s & St Thomas’ NHS Foundation Trust, London, UK. The authors acknowledge use of the research computing facility at King’s College London, Rosalind (https://rosalind.kcl.ac.uk), which is delivered in partnership with the National Institute for Health Research (NIHR) Biomedical Research Centres at South London & Maudsley and Guy’s & St Thomas’ NHS Foundation Trusts, and part-funded by capital equipment grants from the Maudsley Charity (award 980) and Guy’s & St Thomas’ Charity (TR130505). The views expressed are those of the authors and not necessarily those of the NHS, the NIHR, King’s College London or the Department of Health and Social Care. The dHCP project was funded by the European Research Council (ERC) under the European Union Seventh Framework Programme (FR/2007-2013)/ERC grant agreement no. 319,456. This study was supported in part by the Wellcome Engineering and Physical Sciences Research Council Centre for Medical Engineering at King’s College London (grant WT 203,148/Z/16/Z) and the Medical Research Council (UK) (grant MR/K006355/1). Data were provided (in part) by the HCP, WU-Minn Consortium (Principal Investigators: D.V.E. and K.U.; 1U54MH091657) funded by the 16 NIH Institutes and Centers that support the NIH Blueprint for Neuroscience Research; and by the McDonnell Center for Systems Neuroscience at Washington University. L.Z.J.W. is supported by funding from the Commonwealth Scholarship Commission, UK. E.C.R. is supported by an Academy of Medical Sciences/the British Heart Foundation/the Government Department of Business, Energy and Industrial Strategy/the Wellcome Trust Springboard Award (SBF003/1116) and E.C.R. and S.M.S. are supported by a Wellcome Collaborative Award (215573/Z/19/Z). J.O. and A.D.E. received support from the Medical Research Council Centre for Neurodevelopmental Disorders, King’s College London (grant MR/N026063/1). J.O. is supported by a Sir Henry Dale Fellowship jointly funded by the Wellcome Trust and the Royal Society (grant 206,675/Z/17/Z). The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.

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Authors and Affiliations

  1. Centre for the Developing Brain, Department of Perinatal Imaging and Health, School of Biomedical Engineering and Imaging Sciences, King’s College London, London, UK

    Logan Z. J. Williams, Ralica Dimitrova, Tanya Poppe, Antonios Makropoulos, Jonathan O’Muircheartaigh, Lucilio Cordero-Grande, Anthony N. Price, Joseph V. Hajnal, A. David Edwards & Emma C. Robinson

  2. Department of Biomedical Engineering, School of Biomedical Engineering and Imaging Science, King’s College London, London, UK

    Logan Z. J. Williams, Anthony N. Price, Joseph V. Hajnal & Emma C. Robinson

  3. Centre for Functional MRI of the Brain (FMRIB), Wellcome Centre for Integrative Neuroimaging, Nuffield Department of Clinical Neurosciences, University of Oxford, John Radcliffe Hospital, Oxford, UK

    Sean P. Fitzgibbon, Eugene P. Duff & Stephen M. Smith

  4. Faculty of Electrical Engineering and Computing, University of Zagreb, Zagreb, Croatia

    Jelena Bozek

  5. Emotion and Development Branch, National Institute of Mental Health, National Institutes of Health, Bethesda, MD, USA

    Anderson M. Winkler

  6. Department of Computing, Imperial College London, London, UK

    Andreas Schuh, John Cupitt & Daniel Rueckert

  7. Department for Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, Psychology and Neuroscience, King’s College London, London, UK

    Jonathan O’Muircheartaigh

  8. MRC Centre for Neurodevelopmental Disorders, King’s College London, London, UK

    Jonathan O’Muircheartaigh & A. David Edwards

  9. UK Dementia Research Institute, Department of Brain Sciences, Imperial College London, London, UK

    Eugene P. Duff

  10. Biomedical Image Technologies, ETSI Telecomunicación, Universidad Politécnica de Madrid and CIBER-BBN, ISCIII, Madrid, Spain

    Lucilio Cordero-Grande

  11. Klinikum rechts der Isar, Technical University of Munich, Munich, Germany

    Daniel Rueckert

  12. Neonatal Intensive Care Unit, Evelina London Children’s Hospital, London, UK

    A. David Edwards

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Contributions

L.Z.J.W., S.P.F., A.M.W., T.P., J.O., E.P.D., S.M.S., A.D.E. and E.C.R. designed the research. L.Z.J.W., S.P.F., J.B., A.S., A.M. and J.C. performed research. L.Z.J.W. analysed data. L.Z.J.W., A.D.E. and E.C.R. wrote the manuscript. All authors reviewed and edited the manuscript.

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Correspondence to Logan Z. J. Williams or Emma C. Robinson.

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Nature Human Behaviour thanks Rhodri Cusack, Clyde Francks and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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Williams, L.Z.J., Fitzgibbon, S.P., Bozek, J. et al. Structural and functional asymmetry of the neonatal cerebral cortex. Nat Hum Behav 7, 942–955 (2023). https://doi.org/10.1038/s41562-023-01542-8

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