Abstract
Formation of the functional connectome in early life underpins future learning and behavior. However, our understanding of how the functional organization of brain regions into interconnected hubs (centrality) matures in the early postnatal period is limited, especially in response to factors associated with adverse neurodevelopmental outcomes such as preterm birth. We characterized voxel-wise functional centrality (weighted degree) in 366 neonates from the Developing Human Connectome Project. We tested the hypothesis that functional centrality matures with age at scan in term-born babies and is disrupted by preterm birth. Finally, we asked whether neonatal functional centrality predicts general neurodevelopmental outcomes at 18 months. We report an age-related increase in functional centrality predominantly within visual regions and a decrease within the motor and auditory regions in term-born infants. Preterm-born infants scanned at term equivalent age had higher functional centrality predominantly within visual regions and lower measures in motor regions. Functional centrality was not related to outcome at 18 months old. Thus, preterm birth appears to affect functional centrality in regions undergoing substantial development during the perinatal period. Our work raises the question of whether these alterations are adaptive or disruptive and whether they predict neurodevelopmental characteristics that are more subtle or emerge later in life.
Original language | English |
---|---|
Pages (from-to) | 5585-5596 |
Number of pages | 12 |
Journal | Cerebral Cortex |
Volume | 33 |
Issue number | 9 |
DOIs | |
Publication status | Published - 1 May 2023 |
Keywords
- brain development
- functional centrality
- neonatal
- preterm birth
- resting-state connectivity
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In: Cerebral Cortex, Vol. 33, No. 9, 01.05.2023, p. 5585-5596.
Research output: Contribution to journal › Article › peer-review
TY - JOUR
T1 - Development of neonatal brain functional centrality and alterations associated with preterm birth
AU - Fenn-Moltu, Sunniva
AU - Fitzgibbon, Sean P.
AU - Ciarrusta, Judit
AU - Eyre, Michael
AU - Cordero-Grande, Lucilio
AU - Chew, Andrew
AU - Falconer, Shona
AU - Gale-Grant, Oliver
AU - Harper, Nicholas
AU - Dimitrova, Ralica
AU - Vecchiato, Katy
AU - Fenchel, Daphna
AU - Javed, Ayesha
AU - Earl, Megan
AU - Price, Anthony N.
AU - Hughes, Emer
AU - Duff, Eugene P.
AU - O'muircheartaigh, Jonathan
AU - Nosarti, Chiara
AU - Arichi, Tomoki
AU - Rueckert, Daniel
AU - Counsell, Serena
AU - Hajnal, Joseph V.
AU - Edwards, A. David
AU - Mcalonan, Grainne
AU - Batalle, Dafnis
N1 - Funding Information: 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). The authors acknowledge infrastructure support from the National Institute for Health Research (NIHR) Mental Health Biomedical Research Centre (BRC) at South London, Maudsley NHS Foundation Trust, and Institute of Psychiatry, Psychology and Neuroscience, King's College London, and the NIHR-BRC at Guys, and St Thomas’ Hospitals NHS Foundation Trust (GSTFT). The authors also acknowledge support in part from the Wellcome 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), Medical Research Council Centre grant (MR/N026063/1), the Department of Health through an NIHR Comprehensive Biomedical Research Centre Award (to Guy’s and St. Thomas’ National Health Service [NHS] Foundation Trust in partnership with King’s College London and King’s College Hospital NHS Foundation Trust), the Sackler Institute for Translational Neurodevelopment at King’s College London and the European Autism Interventions (EU-AIMS) trial and the EU AIMS-2-TRIALS, a European Innovative Medicines Initiative Joint Undertaking under Grant Agreements Nos. 115300 and 777394, the resources of which are composed of financial contributions from the European Union’s Seventh Framework Programme (Grant FP7/2007–2013). SF-M and OG-G are supported by grants from the UK Medical Research Council (MR/N013700/1 and MR/P502108/1, respectively). JOM, TA, GM, and ADE received support from the Medical Research Council Centre for Neurodevelopmental Disorders, King’s College London (MR/N026063/1). LC-G is supported by a Beatriz Galindo Fellowship jointly funded by the Ministerio de Educación, Cultura y Deporte and the Universidad Politécnica de Madrid (BEAGAL18/00158). JOM is supported by a Sir Henry Dale Fellowship jointly funded by the Wellcome Trust and the Royal Society (206675/Z/17/Z). TA is supported by a MRC Clinician Scientist Fellowship (MR/P008712/1) and Transition Support Award (MR/V036874/1). DB received support from a Wellcome Trust Seed Award in Science (217316/Z/19/Z). The views expressed are those of the authors and not necessarily those of the NHS, the National Institute for Health Research, or the Department of Health. 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. Funding Information: 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). The authors acknowledge infrastructure support from the National Institute for Health Research (NIHR) Mental Health Biomedical Research Centre (BRC) at South London, Maudsley NHS Foundation Trust, and Institute of Psychiatry, Psychology and Neuroscience, King's College London, and the NIHR-BRC at Guys, and St Thomas' Hospitals NHS Foundation Trust (GSTFT). The authors also acknowledge support in part from the Wellcome 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), Medical Research Council Centre grant (MR/N026063/1), the Department of Health through an NIHR Comprehensive Biomedical Research Centre Award (to Guy's and St. Thomas' National Health Service [NHS] Foundation Trust in partnership with King's College London and King's College Hospital NHS Foundation Trust), the Sackler Institute for Translational Neurodevelopment at King's College London and the European Autism Interventions (EUAIMS) trial and the EU AIMS-2-TRIALS, a European Innovative Medicines Initiative Joint Undertaking under Grant Agreements Nos. 115300 and 777394, the resources of which are composed of financial contributions from the European Union's Seventh Framework Programme (Grant FP7/2007-2013). SF-M and OGG are supported by grants from the UK Medical Research Council (MR/N013700/1 and MR/P502108/1, respectively). JOM, TA, GM, and ADE received support from the Medical Research Council Centre for Neurodevelopmental Disorders, King's College London (MR/N026063/1). LC-G is supported by a Beatriz Galindo Fellowship jointly funded by the Ministerio de Educación, Cultura y Deporte and the Universidad Politécnica de Madrid (BEAGAL18/00158). JOM is supported by a Sir Henry Dale Fellowship jointly funded by the Wellcome Trust and the Royal Society (206675/Z/17/Z). TA is supported by a MRC Clinician Scientist Fellowship (MR/P008712/1) and Transition Support Award (MR/V036874/1). DB received support from a Wellcome Trust Seed Award in Science (217316/Z/19/Z). The views expressed are those of the authors and not necessarily those of the NHS, the National Institute for Health Research, or the Department of Health. 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. Publisher Copyright: © 2022 The Author(s).
PY - 2023/5/1
Y1 - 2023/5/1
N2 - Formation of the functional connectome in early life underpins future learning and behavior. However, our understanding of how the functional organization of brain regions into interconnected hubs (centrality) matures in the early postnatal period is limited, especially in response to factors associated with adverse neurodevelopmental outcomes such as preterm birth. We characterized voxel-wise functional centrality (weighted degree) in 366 neonates from the Developing Human Connectome Project. We tested the hypothesis that functional centrality matures with age at scan in term-born babies and is disrupted by preterm birth. Finally, we asked whether neonatal functional centrality predicts general neurodevelopmental outcomes at 18 months. We report an age-related increase in functional centrality predominantly within visual regions and a decrease within the motor and auditory regions in term-born infants. Preterm-born infants scanned at term equivalent age had higher functional centrality predominantly within visual regions and lower measures in motor regions. Functional centrality was not related to outcome at 18 months old. Thus, preterm birth appears to affect functional centrality in regions undergoing substantial development during the perinatal period. Our work raises the question of whether these alterations are adaptive or disruptive and whether they predict neurodevelopmental characteristics that are more subtle or emerge later in life.
AB - Formation of the functional connectome in early life underpins future learning and behavior. However, our understanding of how the functional organization of brain regions into interconnected hubs (centrality) matures in the early postnatal period is limited, especially in response to factors associated with adverse neurodevelopmental outcomes such as preterm birth. We characterized voxel-wise functional centrality (weighted degree) in 366 neonates from the Developing Human Connectome Project. We tested the hypothesis that functional centrality matures with age at scan in term-born babies and is disrupted by preterm birth. Finally, we asked whether neonatal functional centrality predicts general neurodevelopmental outcomes at 18 months. We report an age-related increase in functional centrality predominantly within visual regions and a decrease within the motor and auditory regions in term-born infants. Preterm-born infants scanned at term equivalent age had higher functional centrality predominantly within visual regions and lower measures in motor regions. Functional centrality was not related to outcome at 18 months old. Thus, preterm birth appears to affect functional centrality in regions undergoing substantial development during the perinatal period. Our work raises the question of whether these alterations are adaptive or disruptive and whether they predict neurodevelopmental characteristics that are more subtle or emerge later in life.
KW - brain development
KW - functional centrality
KW - neonatal
KW - preterm birth
KW - resting-state connectivity
UR - https://www.scopus.com/pages/publications/85158002766
U2 - 10.1093/cercor/bhac444
DO - 10.1093/cercor/bhac444
M3 - Article
C2 - 36408638
AN - SCOPUS:85158002766
SN - 1047-3211
VL - 33
SP - 5585
EP - 5596
JO - Cerebral Cortex
JF - Cerebral Cortex
IS - 9
ER -