Neonatal brain dynamic functional connectivity in term and preterm infants and its association with early childhood neurodevelopment

Abstract

Brain dynamic functional connectivity characterises transient connections between brain regions. Features of brain dynamics have been linked to emotion and cognition in adult individuals, and atypical patterns have been associated with neurodevelopmental conditions such as autism. Although reliable functional brain networks have been consistently identified in neonates, little is known about the early development of dynamic functional connectivity. In this study we characterise dynamic functional connectivity with functional magnetic resonance imaging (fMRI) in the first few weeks of postnatal life in term-born (n = 324) and preterm-born (n = 66) individuals. We show that a dynamic landscape of brain connectivity is already established by the time of birth in the human brain, characterised by six transient states of neonatal functional connectivity with changing dynamics through the neonatal period. The pattern of dynamic connectivity is atypical in preterm-born infants, and associated with atypical social, sensory, and repetitive behaviours measured by the Quantitative Checklist for Autism in Toddlers (Q-CHAT) scores at 18 months of age. © The Author(s) 2024.

This work was supported by the European Research Council under the European Union's Seventh Framework Programme (FP7/20072013)/ERC grant agreement no. 319456 (dHCP project) and a Wellcome Trust Seed Award in Science [217316/Z/19/Z] to DB. This study represents independent research part funded by the National Institute for Health and Care Research (NIHR) Maudsley Biomedical Research Centre (BRC) at South London and Maudsley NHS Foundation Trust and King's College London. The authors also acknowledge support in part from the Engineering and Physical Sciences Research Council (EPSRC) Centre for Medical Engineering at Kings College London [WT 203148/Z/16/Z], MRC strategic grant [MR/K006355/1], the Department of Health through an NIHR Comprehensive Biomedical Research Centre Award (to King's College Hospital NHS Foundation Trust). The results leading to this publication have received funding from the Innovative Medicines Initiative 2 Joint Undertaking under grant agreement No 777394 for the project AIMS-2-TRIALS. This Joint Undertaking receives support from the European Union's Horizon 2020 research and innovation programme and EFPIA and AUTISM SPEAKS, Autistica, SFARI. S.F.M. and O.G.G. were supported by grants from the UK Medical Research Council [MR/N013700/1] and [MR/P502108/1] respectively. J.O.M., T.A., G.M., and A.D.E. received support from the Medical Research Council Centre for Neurodevelopmental Disorders, King's College London [MR/N026063/1]. L.C.-G. received support from Project PID2021-129022OA-I00 funded by MCIN/AEI/10.13039/501100011033/FEDER, EU, and CAM-Spain under the line support for R&D projects for Beatriz Galindo researchers BGP18/00178. J.J.T. was supported by grants from the Finnish Medical Foundation, Sigrid Juselius Foundation, Signe and Ane Gyllenberg Foundation, Emil Aaltonen Foundation and Hospital District of Southwest Finland State Research Grants. J.O.M. is supported by a Sir Henry Dale Fellowship jointly funded by the Wellcome Trust and the Royal Society [206675/Z/17/Z]. T.A. is supported by an MRC Clinician Scientist Fellowship [MR/P008712/1] and Transition Support Award [MR/V036874/1]. 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 funders, the NHS, the National Institute for Health Research, the Department of Health and Social Care, or the IHI-JU2. The funders had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication.