Maturational networks of human fetal brain activity reveal emerging connectivity patterns prior to ex-utero exposure

Vyacheslav R Karolis; Sean P. Fitzgibbon; Lucilio Cordero-Grande; Seyedeh-Rezvan Farahibozorg; Anthony N. Price; Emer J. Hughes; Ahmed E. Fetit; Vanessa Kyriakopoulou; Maximilian Pietsch; Mary A. Rutherford; Daniel Rueckert; Joseph V. Hajnal; A. David Edwards; Jonathan O'Muircheartaigh; Eugene P. Duff; Tomoki Arichi

doi:10.1038/s42003-023-04969-x

Maturational networks of human fetal brain activity reveal emerging connectivity patterns prior to ex-utero exposure

Vyacheslav R Karolis^*, Sean P. Fitzgibbon, Lucilio Cordero-Grande, Seyedeh-Rezvan Farahibozorg, Anthony N. Price, Emer J. Hughes, Ahmed E. Fetit, Vanessa Kyriakopoulou, Maximilian Pietsch, Mary A. Rutherford, Daniel Rueckert, Joseph V. Hajnal, A. David Edwards, Jonathan O'Muircheartaigh, Eugene P. Duff, Tomoki Arichi

^*Corresponding author for this work

1Department of Hepatology, Imperial College London, London, UK. 2Institute of Liver Studies at King's College School of Medicine at King's College Hospital, London, UK. 3Institute of Human Health and Performance, University College London, London, UK. 4Department of Asthma Allergy and Lung Biology, King's College London, London, UK. 5Division of Critical Care Medicine, University of Alberta, Edmonton, Canada.
Oxford Autoimmune Neurology Group, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, UK.; Department of Neurology, Oxford University Hospitals NHS Foundation Trust, Oxford, UK.
Biomedical Image Technologies
School of Biomedical Engineering and Imaging Sciences
Department of Materials, Imperial College London, London SW7 2AZ, United Kingdom; Department of Bioengineering, Imperial College London, London SW7 2AZ, United Kingdom; Institute of Biomedical Engineering, Imperial College London, London SW7 2AZ, United Kingdom.
Department of Forensic and Neurodevelopmental Sciences
Paediatric Neurosciences
PICU Evelina London Children's Hospital

Research output: Contribution to journal › Article › peer-review

7 Citations (Scopus)

Abstract

A key feature of the fetal period is the rapid emergence of organised patterns of spontaneous brain activity. However, characterising this process in utero using functional MRI is inherently challenging and requires analytical methods which can capture the constituent developmental transformations. Here, we introduce a novel analytical framework, termed "maturational networks" (matnets), that achieves this by modelling functional networks as an emerging property of the developing brain. Compared to standard network analysis methods that assume consistent patterns of connectivity across development, our method incorporates age-related changes in connectivity directly into network estimation. We test its performance in a large neonatal sample, finding that the matnets approach characterises adult-like features of functional network architecture with a greater specificity than a standard group-ICA approach; for example, our approach is able to identify a nearly complete default mode network. In the in-utero brain, matnets enables us to reveal the richness of emerging functional connections and the hierarchy of their maturational relationships with remarkable anatomical specificity. We show that the associative areas play a central role within prenatal functional architecture, therefore indicating that functional connections of high-level associative areas start emerging prior to exposure to the extra-utero environment.

Original language	English
Article number	661
Journal	Communications Biology
Volume	6
Issue number	1
DOIs	https://doi.org/10.1038/s42003-023-04969-x
Publication status	Published - 22 Jun 2023

Keywords

Adult
Pregnancy
Female
Infant, Newborn
Humans
Brain/diagnostic imaging
Brain Mapping/methods
Fetus
Magnetic Resonance Imaging

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10.1038/s42003-023-04969-xLicence: CC BY

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Karolis, V. R., Fitzgibbon, S. P., Cordero-Grande, L., Farahibozorg, S.-R., Price, A. N., Hughes, E. J., Fetit, A. E., Kyriakopoulou, V., Pietsch, M., Rutherford, M. A., Rueckert, D., Hajnal, J. V., Edwards, A. D., O'Muircheartaigh, J., Duff, E. P., & Arichi, T. (2023). Maturational networks of human fetal brain activity reveal emerging connectivity patterns prior to ex-utero exposure. Communications Biology, 6(1), Article 661. https://doi.org/10.1038/s42003-023-04969-x

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title = "Maturational networks of human fetal brain activity reveal emerging connectivity patterns prior to ex-utero exposure",

abstract = "A key feature of the fetal period is the rapid emergence of organised patterns of spontaneous brain activity. However, characterising this process in utero using functional MRI is inherently challenging and requires analytical methods which can capture the constituent developmental transformations. Here, we introduce a novel analytical framework, termed {"}maturational networks{"} (matnets), that achieves this by modelling functional networks as an emerging property of the developing brain. Compared to standard network analysis methods that assume consistent patterns of connectivity across development, our method incorporates age-related changes in connectivity directly into network estimation. We test its performance in a large neonatal sample, finding that the matnets approach characterises adult-like features of functional network architecture with a greater specificity than a standard group-ICA approach; for example, our approach is able to identify a nearly complete default mode network. In the in-utero brain, matnets enables us to reveal the richness of emerging functional connections and the hierarchy of their maturational relationships with remarkable anatomical specificity. We show that the associative areas play a central role within prenatal functional architecture, therefore indicating that functional connections of high-level associative areas start emerging prior to exposure to the extra-utero environment.",

keywords = "Adult, Pregnancy, Female, Infant, Newborn, Humans, Brain/diagnostic imaging, Brain Mapping/methods, Fetus, Magnetic Resonance Imaging",

author = "Karolis, {Vyacheslav R} and Fitzgibbon, {Sean P.} and Lucilio Cordero-Grande and Seyedeh-Rezvan Farahibozorg and Price, {Anthony N.} and Hughes, {Emer J.} and Fetit, {Ahmed E.} and Vanessa Kyriakopoulou and Maximilian Pietsch and Rutherford, {Mary A.} and Daniel Rueckert and Hajnal, {Joseph V.} and Edwards, {A. David} and Jonathan O'Muircheartaigh and Duff, {Eugene P.} and Tomoki Arichi",

note = "{\textcopyright} 2023. The Author(s).",

year = "2023",

month = jun,

day = "22",

doi = "10.1038/s42003-023-04969-x",

language = "English",

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Karolis, VR, Fitzgibbon, SP, Cordero-Grande, L, Farahibozorg, S-R, Price, AN, Hughes, EJ, Fetit, AE, Kyriakopoulou, V , Pietsch, M , Rutherford, MA, Rueckert, D, Hajnal, JV , Edwards, AD , O'Muircheartaigh, J, Duff, EP & Arichi, T 2023, 'Maturational networks of human fetal brain activity reveal emerging connectivity patterns prior to ex-utero exposure', Communications Biology, vol. 6, no. 1, 661. https://doi.org/10.1038/s42003-023-04969-x

TY - JOUR

T1 - Maturational networks of human fetal brain activity reveal emerging connectivity patterns prior to ex-utero exposure

AU - Karolis, Vyacheslav R

AU - Fitzgibbon, Sean P.

AU - Cordero-Grande, Lucilio

AU - Farahibozorg, Seyedeh-Rezvan

AU - Price, Anthony N.

AU - Hughes, Emer J.

AU - Fetit, Ahmed E.

AU - Kyriakopoulou, Vanessa

AU - Pietsch, Maximilian

AU - Rutherford, Mary A.

AU - Rueckert, Daniel

AU - Hajnal, Joseph V.

AU - Edwards, A. David

AU - O'Muircheartaigh, Jonathan

AU - Duff, Eugene P.

AU - Arichi, Tomoki

PY - 2023/6/22

Y1 - 2023/6/22

N2 - A key feature of the fetal period is the rapid emergence of organised patterns of spontaneous brain activity. However, characterising this process in utero using functional MRI is inherently challenging and requires analytical methods which can capture the constituent developmental transformations. Here, we introduce a novel analytical framework, termed "maturational networks" (matnets), that achieves this by modelling functional networks as an emerging property of the developing brain. Compared to standard network analysis methods that assume consistent patterns of connectivity across development, our method incorporates age-related changes in connectivity directly into network estimation. We test its performance in a large neonatal sample, finding that the matnets approach characterises adult-like features of functional network architecture with a greater specificity than a standard group-ICA approach; for example, our approach is able to identify a nearly complete default mode network. In the in-utero brain, matnets enables us to reveal the richness of emerging functional connections and the hierarchy of their maturational relationships with remarkable anatomical specificity. We show that the associative areas play a central role within prenatal functional architecture, therefore indicating that functional connections of high-level associative areas start emerging prior to exposure to the extra-utero environment.

AB - A key feature of the fetal period is the rapid emergence of organised patterns of spontaneous brain activity. However, characterising this process in utero using functional MRI is inherently challenging and requires analytical methods which can capture the constituent developmental transformations. Here, we introduce a novel analytical framework, termed "maturational networks" (matnets), that achieves this by modelling functional networks as an emerging property of the developing brain. Compared to standard network analysis methods that assume consistent patterns of connectivity across development, our method incorporates age-related changes in connectivity directly into network estimation. We test its performance in a large neonatal sample, finding that the matnets approach characterises adult-like features of functional network architecture with a greater specificity than a standard group-ICA approach; for example, our approach is able to identify a nearly complete default mode network. In the in-utero brain, matnets enables us to reveal the richness of emerging functional connections and the hierarchy of their maturational relationships with remarkable anatomical specificity. We show that the associative areas play a central role within prenatal functional architecture, therefore indicating that functional connections of high-level associative areas start emerging prior to exposure to the extra-utero environment.

KW - Adult

KW - Pregnancy

KW - Female

KW - Infant, Newborn

KW - Humans

KW - Brain/diagnostic imaging

KW - Brain Mapping/methods

KW - Fetus

KW - Magnetic Resonance Imaging

U2 - 10.1038/s42003-023-04969-x

DO - 10.1038/s42003-023-04969-x

M3 - Article

C2 - 37349403

SN - 2399-3642

VL - 6

JO - Communications Biology

JF - Communications Biology

IS - 1

M1 - 661

ER -

Maturational networks of human fetal brain activity reveal emerging connectivity patterns prior to ex-utero exposure

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Keywords

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