Intrinsic Functional Brain Architecture Derived from Graph Theoretical Analysis in the Human Fetus

Thomason, Moriah E.; Brown, Jesse A.; Dassanayake, Maya T.; Shastri, Rupal; Marusak, Hilary A.; Hernandez-Andrade, Edgar; Yeo, Lami; Mody, Swati; Berman, Susan; Hassan, Sonia S.; Romero, Roberto

doi:10.1371/journal.pone.0094423

Cited by 130Functional Brain Connectivity StudiesAdvanced Neuroimaging Techniques and ApplicationsNeonatal and fetal brain pathology

Intrinsic Functional Brain Architecture Derived from Graph Theoretical Analysis in the Human Fetus

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Thomason, Moriah E., Brown, Jesse A., Dassanayake, Maya T., Shastri, Rupal, Marusak, Hilary A., Hernandez-Andrade, Edgar, Yeo, Lami, Mody, Swati +3 more·2014·PLoS ONE

DOI 10.1371/journal.pone.0094423PMC PMC4006774

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Abstract

The human brain undergoes dramatic maturational changes during late stages of fetal and early postnatal life. The importance of this period to the establishment of healthy neural connectivity is apparent in the high incidence of neural injury in preterm infants, in whom untimely exposure to ex-uterine factors interrupts neural connectivity. Though the relevance of this period to human neuroscience is apparent, little is known about functional neural networks in human fetal life. Here, we apply graph theoretical analysis to examine human fetal brain connectivity. Utilizing resting state functional magnetic resonance imaging (fMRI) data from 33 healthy human fetuses, 19 to 39 weeks gestational age (GA), our analyses reveal that the human fetal brain has modular organization and modules overlap functional systems observed postnatally. Age-related differences between younger (GA <31 weeks) and older (GA≥31 weeks) fetuses demonstrate that brain modularity decreases, and connectivity of the posterior cingulate to other brain networks becomes more negative, with advancing GA. By mimicking functional principles observed postnatally, these results support early emerging capacity for information processing in the human fetal brain. Current technical limitations, as well as the potential for fetal fMRI to one day produce major discoveries about fetal origins or antecedents of neural injury or disease are discussed.

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Posterior cingulate connectivity to the rest of the brain weakens with increasing gestational age.
“Posterior cingulate connectivity to the rest of the brain, for example, weakens with increasing gestational age [64].”
From Brain structural and functional outcomes in the offspring of women experiencing psychological distress during pregnancy (2024) · cites this paper as [64]
The Results section reports that posterior cingulate connectivity to other brain modules became more negative with advancing gestational age. Calling this a general weakening of connectivity to the rest of the brain is broader than the finding: it concerns negative connections between modules, while the Discussion also reports connectivity to prefrontal regions in older fetuses only. (LLM, conf=0.85)
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Age-related increases in long-range connectivity in fetal functional neural connectivity networks in utero
Thomason, M. E., Grove, L. E., Lozon, T. A., Vila, A. M., Ye, Y., Nye, M. J., Manning, J. H., Pappas, A., Hernandez‐Andrade, E. A., Yeo, L., et al. (2014) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2014.09.001 · Cited by 188 · see citing works
Self-citation
Modification of plasma fibrinogen method.
Ellis, B. (1970) · Journal of Clinical Pathology · doi:10.1136/jcp.23.4.374
Cross-hemispheric functional connectivity in the human fetal brain
Thomason, M. E., Dassanayake, M. T., Shen, S., Katkuri, Y., Alexis, M., Anderson, A. L., Yeo, L., Mody, S., Hernandez-Andrade, E., Hassan, S. S., et al. (2013) · Science Translational Medicine · doi:10.1126/scitranslmed.3004978 · Cited by 225 · see citing works
Self-citation
Gestational age-related changes in the fetal functional connectome: in utero evidence for the global signal
Kim, J.-H., De Asis-Cruz, J., Cook, K. M., & Limperopoulos, C. (2023) · Cerebral Cortex · doi:10.1093/cercor/bhac209 · Cited by 19 · see citing works

Authors: Thomason, M. E., Brown, J. A., Dassanayake, M. T., Shastri, R., Marusak, H. A., Hernandez-Andrade, E., Yeo, L., Mody, S., Berman, S., Hassan, S. S., & Romero, R.
Affiliations: United States Department of Health and Human Services (US)
University of California, San Francisco (US)
Wayne State University (US)
Corresponding author: Thomason, Moriah E.
ORCID: Thomason, Moriah E.
Brown, Jesse A.
Marusak, Hilary A.
Yeo, Lami
Mody, Swati
Berman, Susan
Hassan, Sonia S.
Romero, Roberto
Venue: PLoS ONE
Publisher: Public Library of Science (PLoS)
Published: 2014-05-01
Volume: 9
Issue: 5
Pages: e94423
ISSN: 1932-6203 (ISSN-L)
DOI: 10.1371/journal.pone.0094423
PMC: PMC4006774
OpenAlex: W2030993584
Cited by: 130
References: 61
Citations by year: 2026: 7 · 2025: 13 · 2024: 12 · 2023: 9 · 2022: 13 · 2021: 19 · 2020: 9 · 2019: 12 · 2018: 9 · 2017: 6 · 2016: 9 · 2015: 7 · 2014: 5
FWCI: 5.02
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (unspecified)
Locations: PLoS ONE (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders: U.S. Department of Health and Human Services
Wayne State University
W.K. Kellogg Foundation (P3018205)
National Institutes of Health (P3018205)
National Institute of Mental Health (R01MH110793)
National Institute of Environmental Health Sciences (R21ES026022)
National Institute of Child Health and Human Development
Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD-2-3342, N01 HD23342, N01-HD-)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced Neuroimaging Techniques and Applications
Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Neonatal and fetal brain pathology
Keywords: fetal brain, functional brain networks, brain modularity, resting-state functional connectivity, posterior cingulate cortex, gestational age, brain maturation, preterm infants, nerve injury, graph theory
MeSH terms: Adolescent, Adult, Brain, Brain Mapping, Female, Fetus, Gestational Age, Gyrus Cinguli, Humans, Magnetic Resonance Imaging, Pregnancy, Young Adult, Connectome

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Intrinsic Functional Brain Architecture Derived from Graph Theoretical Analysis in the Human Fetus

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