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

Lucas G S França; Judit Ciarrusta; Oliver Gale-Grant; Sunniva Fenn-Moltu; Sean Fitzgibbon; Andrew Chew; Shona Falconer; Ralica Dimitrova; Lucilio Cordero-Grande; Anthony N Price; Emer Hughes; Jonathan O'Muircheartaigh; Eugene Duff; Jetro J Tuulari; Gustavo Deco; Serena J Counsell; Joseph V Hajnal; Chiara Nosarti; Tomoki Arichi; A David Edwards; Grainne McAlonan; Dafnis Batalle

doi:10.1038/s41467-023-44050-z

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

Nat Commun. 2024 Feb 8;15(1):16. doi: 10.1038/s41467-023-44050-z.

Authors

Lucas G S França^{1

2

3}, Judit Ciarrusta^{1

2}, Oliver Gale-Grant^{1

2}, Sunniva Fenn-Moltu^{1

2}, Sean Fitzgibbon⁴, Andrew Chew², Shona Falconer², Ralica Dimitrova^{1

2}, Lucilio Cordero-Grande^{2

5

6}, Anthony N Price², Emer Hughes², Jonathan O'Muircheartaigh^{1

2

7}, Eugene Duff^{4

8

9}, Jetro J Tuulari^{10

11

12}, Gustavo Deco^{13

14

15

16}, Serena J Counsell², Joseph V Hajnal², Chiara Nosarti^{2

17}, Tomoki Arichi^{2

7

18

19}, A David Edwards^#^{2

7}, Grainne McAlonan^#¹, Dafnis Batalle^#^{20

21}

Affiliations

¹ Department of Forensic and Neurodevelopmental Science, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, SE5 8AF, UK.
² Centre for the Developing Brain, School of Biomedical Engineering & Imaging Sciences, King's College London, London, SE1 7EH, UK.
³ Department of Computer and Information Sciences, Faculty of Engineering and Environment, Northumbria University, Newcastle upon Tyne, NE1 8ST, UK.
⁴ Oxford Centre for Functional Magnetic Resonance Imaging of the Brain, Wellcome Centre for Integrative Neuroimaging, University of Oxford, Oxford, OX3 9DU, UK.
⁵ Biomedical Image Technologies, ETSI Telecomunicación, Universidad Politécnica de Madrid, 28040, Madrid, Spain.
⁶ Centro de Investigación Biomédica en Red de Bioingeniería, Biomateriales y Nanomedicina, Instituto de Salud Carlos III, 28029, Madrid, Spain.
⁷ MRC Centre for Neurodevelopmental Disorders, King's College London, London, SE1 1UL, UK.
⁸ Department of Brain Sciences, Imperial College London, London, W12 0BZ, UK.
⁹ UK Dementia Research Institute at Imperial College London, London, W12 0BZ, UK.
¹⁰ FinnBrain Birth Cohort Study, Turku Brain and Mind Center, Institute of Clinical Medicine, University of Turku, 20500, Turku, Finland.
¹¹ Turku Collegium for Science and Medicine and Technology, University of Turku, 20500, Turku, Finland.
¹² Department of Psychiatry, University of Turku and Turku University Hospital, 20500, Turku, Finland.
¹³ Center for Brain and Cognition, Computational Neuroscience Group, Department of Information and Communication Technologies, Pompeu Fabra University, 08002, Barcelona, Spain.
¹⁴ Catalan Institution for Research and Advanced Studies, 08010, Barcelona, Spain.
¹⁵ Department of Neuropsychology, Max Planck Institute for Human Cognitive and Brain Sciences, 04103, Leipzig, Germany.
¹⁶ School of Psychological Sciences, Monash University, Melbourne, VIC, 3010, Australia.
¹⁷ Department of Child and Adolescent Psychiatry, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, SE5 8AF, UK.
¹⁸ Department of Paediatric Neurosciences, Evelina London Children's Hospital, Guy's and St Thomas' NHS Foundation Trust, London, SE1 7EH, UK.
¹⁹ Department of Bioengineering, Imperial College London, London, SW7 2AZ, UK.
²⁰ Department of Forensic and Neurodevelopmental Science, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, SE5 8AF, UK. dafnis.batalle@kcl.ac.uk.
²¹ Centre for the Developing Brain, School of Biomedical Engineering & Imaging Sciences, King's College London, London, SE1 7EH, UK. dafnis.batalle@kcl.ac.uk.

^# Contributed equally.

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.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Adult
Autistic Disorder*
Brain / pathology
Brain Mapping
Child, Preschool
Humans
Infant
Infant, Newborn
Infant, Premature*
Magnetic Resonance Imaging

Abstract

Publication types

MeSH terms

Grants and funding