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Hubs in the human fetal brain network
Open accessAbstract
Advances in neuroimaging and network analyses have lead to discovery of highly connected regions, or hubs, in the connectional architecture of the human brain. Whether these hubs emerge in utero, has yet to be examined. The current study addresses this question and aims to determine the location of neural hubs in human fetuses. Fetal resting-state fMRI data (N = 105) was used to construct connectivity matrices for 197 discrete brain regions. We discovered that within the connectional functional organization of the human fetal brain key hubs are emerging. Consistent with prior reports in infants, visual and motor regions were identified as emerging hub areas, specifically in cerebellar areas. We also found evidence for network hubs in association cortex, including areas remarkably close to the adult fusiform facial and Wernicke areas. Functional significance of hub structure was confirmed by computationally deleting hub versus random nodes and observing that global efficiency decreased significantly more when hubs were removed (p < .001). Taken together, we conclude that both primary and association brain regions demonstrate centrality in network organization before birth. While fetal hubs may be important for facilitating network communication, they may also form potential points of vulnerability in fetal brain development.
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“Most hubs are localized in the cerebellum, while some are in the primary and association cortices [71].”
From Brain structural and functional outcomes in the offspring of women experiencing psychological distress during pregnancy (2024) · cites this paper as [71]
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Citations
Cites
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Influential
Cited by
Sorted by citations
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Self-citationAssociation of Prenatal Maternal Anxiety With Fetal Regional Brain Connectivity
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Functional brain connectivity in ex utero premature infants compared to in utero fetuses
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MethodInfluentialCook, K. M., Asis‐Cruz, J. D., Kim, J., Basu, S. K., Andescavage, N. N., Murnick, J. G., Spoehr, E., Liggett, M., du Plessis, A. J., & Limperopoulos, C. (2023) · BMC Medicine · doi:10.1186/s12916-023-03141-w · Cited by 62
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Rutherford, S. E., Sturmfels, P., Angstadt, M., Hect, J. L., Wiens, J., van den Heuvel, M. I., Scheinost, D., Sripada, C., & Thomason, M. E. (2021) · Neuroinformatics · doi:10.1007/s12021-021-09528-5 · Cited by 46
Self-citationThomason, M. E., Palopoli, A. C., Jariwala, N. N., Werchan, D. M., Chen, A., Adhikari, S., Espinoza‐Heredia, C., Brito, N. H., & Trentacosta, C. J. (2021) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2021.101000 · Cited by 43
Self-citationGlobal Network Organization of the Fetal Functional Connectome
De Asis-Cruz, J., Andersen, N., Kapse, K., Khrisnamurthy, D., Quistorff, J., Lopez, C., Vezina, G., & Limperopoulos, C. (2021) · Cerebral Cortex · doi:10.1093/cercor/bhaa410 · Cited by 40
“…range of neuroscience studies involving different species (Watts and Strogatz 1998; Oh et al. 2014; van den Heuvel et al. 2016; Rilling and van den Heuvel 2018) at different scales, using different imaging modalities (e.g., diffusion tensor imaging and EEG) (Ferri et al. 2007) including in vitro…”
BackgroundAge-Related Alterations in EEG Network Connectivity in Healthy Aging
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“…to characterize the functional topography of the human brain from the fetal period through to adulthood (Bathelt, O’Reilly, Clayden, Cross, & De Haan, 2013; De Asis‐Cruz, Bouyssi‐Kobar, Evangelou, Vezina, & Limperopoulos, 2015; Gao et al., 2015; Thomason et al., 2017; van den Heuvel et al., 2018).”
BackgroundResultRobust sex differences in functional brain connectivity are present in utero
Cook, K. M., De Asis-Cruz, J., Lopez, C., Quistorff, J., Kapse, K., Andersen, N., Vezina, G., & Limperopoulos, C. (2023) · Cerebral Cortex · doi:10.1093/cercor/bhac218 · Cited by 31
Early and late development of hub connectivity in the human brain
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Prenatal Programming of Neurodevelopment: Structural and Functional Changes
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Self-citationTrajectories of human brain functional connectome maturation across the birth transition
Ji, L., Menu, I., Majbri, A., Bhatia, T., Trentacosta, C. J., & Thomason, M. E. (2024) · PLoS Biology · doi:10.1371/journal.pbio.3002909 · Cited by 29
Self-citationAutism-related shifts in the brain’s information processing hierarchy
Bernhardt, B. C., Valk, S. L., Hong, S., Soulières, I., & Mottron, L. (2025) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2025.04.008 · Cited by 29
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Graph Theory Measures and Their Application to Neurosurgical Eloquence
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“Some clues may be derived from developmental studies examining hub node formation, though results of these have so far been conflicting [70,71].”
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“Spontaneous fluctuations in the low frequency (0.01–0.1 Hz) BOLD signal contain information about the connectivity between distinct brain regions and reveal the brain’s functional architecture, organized in resting-state networks (RSN) (van den Heuvel et al., 2018; Fransson, 2005).”
BackgroundInfluentialSubcortico-Cortical Functional Connectivity in the Fetal Brain: A Cognitive Development Blueprint
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Motion correction and volumetric reconstruction for fetal functional magnetic resonance imaging data
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BackgroundMethodImaging Developmental and Interventional Plasticity Following Perinatal Stroke
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“for primary sensory functions (vision, audition, and sensorimotor) appear to develop very early, before birth.(163) Throughout childhood, networks strengthen and follow a local-to-global pattern of development.”
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Fetal behavior during MRI changes with age and relates to network dynamics
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Developmental Pathoconnectomics and Advanced Fetal MRI
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“…connectivity patterns in utero precede and may guide functional selectivity of certain brain regions, such as the fusiform face area (van den Heuvel et al., 2018), and that macroscale characteristics of fetal functional networks share significant overlap with adult networks (Turk et al.,…”
BackgroundSelf-citationAn integrative perspective on the role of touch in the development of intersubjectivity
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MethodAdvances in Fetal Brain Imaging
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“…Milan, Italy 4 Vita-Salute San Raffaele University, Milan, Italy 1 3 to accommodate motion in a fetal rs-fMRI time-series (Ferrazzi et al., 2014; Van den Heuvel et al., 2018; Thomason et al., 2018; Van Dijk et al., 2012) and on spatial normalization of the functional time-series to…”
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“In the past, brain extraction of fetal fMRI data was performed by manually (Thomason et al., 2014, 2015) or semi-automatically (Thomason et al., 2013; van den Heuvel et al., 2018) segmenting the brain from the surrounding tissue.”
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Utilizing functional neuroimaging to study early language development
Olson, H. A., Day, T. K. M., Hiersche, K. J., Manning, B. L., Bradley, H., Choi, S. J., Abdurokhmonova, G., McCormick, S. A., Conrad, A. L., Scheinost, D., et al. (2025) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2025.101641 · Cited by 4
Fetal functional connectivity prospectively associates with autistic traits in toddlerhood
Chen, B., Menu, I., Ji, L., Trentacosta, C. J., & Thomason, M. E. (2025) · NeuroImage Clinical · doi:10.1016/j.nicl.2025.103938 · Cited by 4
Self-citationMorphological development of the human fetal striatum during the second trimester
Tian, M., Xu, F., Xia, Q., Tang, Y., Zhang, Z., Lin, X., Meng, H., Feng, L., & Liu, S. (2021) · Cerebral Cortex · doi:10.1093/cercor/bhab532 · Cited by 4
Zhang, S., Wang, R., Han, Z., Yu, S., Gao, H. B., Jiang, X., & Zhang, T. (2022) · Chaos Solitons & Fractals · doi:10.1016/j.chaos.2022.112018 · Cited by 4
Li, B., Li, W., Guo, Y., Wang, Y., Xu, L., Yang, Y., Xu, S.-G., Tan, Z., Mei, Y., & Wang, K.-Y. (2023) · Frontiers in Neurology · doi:10.3389/fneur.2023.1266167 · Cited by 4
“It also reveals that these are essential compensatory brain regions that enable integration and coupling across the whole brain at the acute phase of sTBI (20).”
BackgroundKipping, J., Margulies, D. S., Eickhoff, S. B., Lee, A., & Qiu, A. (2018) · NeuroImage · doi:10.1016/j.neuroimage.2018.04.067 · Cited by 4
Correa, S., Nichols, E. S., Mueller, M. E., de Vrijer, B., Eagleson, R. A., McKenzie, C. A., de Ribaupierre, S., & Duerden, E. G. (2023) · Cerebral Cortex · doi:10.1093/cercor/bhad190 · Cited by 5
Hayat, T. T. A., & Sami, M. B. (2020) · Development and Psychopathology · doi:10.1017/s0954579420000218 · Cited by 2
“Furthermore. of the dominant hubs, there appears to be age-related variation in some frontal and temporal hubs (van den Heuvel et al., 2018).”
BackgroundLes stress pendant les 1 000 premiers jours de la vie quand tout commence
Verney, C., & Vitalis, T. (2023) · médecine/sciences · doi:10.1051/medsci/2023124 · Cited by 3
Schirmer, M. D., & Chung, A. W. (2019) · Lecture notes in computer science · doi:10.1007/978-3-030-32391-2_6 · Cited by 6
“Such hubs are the first to develop and present at birth, with strong similarity to adults [14, 12].”
BackgroundYorita, A., Kawayama, T., Inoue, M., Kinoshita, T., Oda, H., Tokunaga, Y., Tateishi, T., Shoji, Y., Uchimura, N., Abe, T., et al. (2024) · Journal of Clinical Medicine · doi:10.3390/jcm13092556 · Cited by 3
“To investigate the possibility that the secondary visual cortex functions as a hub, we analysed the degree and betweenness centralities using graph theoretical analysis [54].”
MethodIndividual Topological Analysis of Synchronization-Based Brain Connectivity
Lombardi, A., Amoroso, N., Diacono, D., Monaco, A., Tangaro, S., & Bellotti, R. (2020) · Applied Sciences · doi:10.3390/app10093275 · Cited by 2
Im, K. (2021) · Advances in magnetic resonance technology and applications · doi:10.1016/b978-0-12-816633-8.00004-1 · Cited by 1
The Representation of Nociception and Pain in the Developing Brain
Lorenzo Fabrizi, D., & Fitzgerald, M. (2025) · Annual Review of Physiology · doi:10.1146/annurev-physiol-040125-112145 · Cited by 1
Early functional organization of the anterior and posterior hippocampus in the fetal brain
Nichols, E. S., Al‐Saoud, S., Fang, M., Eagleson, R. A., de Vrijer, B., McKenzie, C. A., de Ribaupierre, S., & Duerden, E. G. (2025) · Cerebral Cortex · doi:10.1093/cercor/bhaf327 · Cited by 2
“Although the presence of functional connectivity networks has been well-established in the fetal brain (van den Heuvel and Thomason 2016; van den Heuvel et al. 2018; Thomason 2020), the third trimester covers a three-month period in which large developmental changes occur (Clouchoux et al. 2012;…”
Li, X., Hect, J. L., Thomason, M. E., & Zhu, D. (2019) · arXiv (Cornell University) · doi:10.48550/arxiv.1906.03691 · Cited by 1
“For fetal neurodevelopmental studies, existing works focus on analysis of the functional connectivity in fetal brain, such as discoveries of functional networks and identification of highly connected hubs [4].”
BackgroundSelf-citationAutomated Brain Masking of Fetal Functional MRIPreprint
Rutherford, S. E., Sturmfels, P., Angstadt, M., Hect, J. L., Wiens, J., van den Heuval, M., Scheinost, D., Thomason, M. E., & Sripada, C. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/525386 · Cited by 1
Self-citationMoore, J. W., Wilson, S., Oldehinkel, M., Cordero‐Grande, L., Uus, A. U., Kyriakopoulou, V., Duff, E. P., O’Muircheartaigh, J., Rutherford, M., Andreae, L. C., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.06.26.546607 · Cited by 1
Moore, J. W., Wilson, S., Oldehinkel, M., Cordero‐Grande, L., Uus, A. U., Kyriakopoulou, V., Duff, E. P., O’Muircheartaigh, J., Rutherford, M., Andreae, L. C., et al. (2023) · doi:10.7554/elife.90536 · Cited by 2
Characterizing Large-Scale Human Circuit Development with In Vivo NeuroimagingPreprint
Arichi, T. (2024) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a041496 · Cited by 1
Early Childhood Brain Development and Schizophrenia: An Imaging Perspective
Gilmore, J. H. (2020) · Springer eBooks · doi:10.1007/978-3-030-35206-6_15
Gountas, J. (2020) · Scholarly Journal of Psychology and Behavioral Sciences · doi:10.32474/sjpbs.2020.03.000166
“Amalric [39] found that blind mathematicians process advanced mathematics in similar brain networks as sighted without the visual experience.”
BackgroundA blueprint of the developing mind
Turk, E. (2022) · Utrecht University Repository (Utrecht University) · doi:10.33540/627
Self-citationVasilkovska, T., Adhikari, M. H., Audekerke, J. V., Pustina, D., Cachope, R., Tang, H., Liu, L., Muñoz-Sanjuán, I., der Linden, A. V., & Verhoye, M. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.11.19.517166
Wu, Z., Yu, J., Chen, X., Shen, J. F., Xie, S., & Zeng, Y. (2023) · Multimedia Tools and Applications · doi:10.1007/s11042-023-17918-x
“Our results revealed that infant brain structural network exhibited sets of hub nodes in limbic subsystem, superior frontal, insula, fusiform, and lingual gyrus, which is in line with the findings in [38, 42].”
Biological basis of neurodevelopmental disabilities
Kielty, K., Risen, S., & Melendez-Zaidi, A. E. (2024) · Elsevier eBooks · doi:10.1016/b978-0-12-824060-1.00003-1 · Cited by 1
Wasserman, T. H., & Wasserman, L. D. (2024) · Springer eBooks · doi:10.1007/978-3-031-78732-4_5
Wasserman, T. H., & Wasserman, L. D. (2024) · Springer eBooks · doi:10.1007/978-3-031-78732-4_10
Connectivité fonctionnelle du cerveau fœtal et néonatal : de la technique à l’application
Argyropoulou, M. I., Lopes, R., & Astrakas, L. G. (2025) · Bulletin de l Académie Nationale de Médecine · doi:10.1016/j.banm.2024.11.025
Evaluating the effects of volume censoring on fetal functional connectivity
Kim, J., Asis‐Cruz, J. D., Cook, K. M., & Limperopoulos, C. (2025) · Scientific Reports · doi:10.1038/s41598-025-96538-x
Maternal Prenatal Psychological Stress and Iron Levels in the Fetal Brain
Chen, B., Ji, L., Yoon, Y. B., Duffy, M., Menu, I., Trentacosta, C. J., & Thomason, M. E. (2025) · Developmental Psychobiology · doi:10.1002/dev.70062
Self-citationSun, H., Toyonaga, T., Mehta, S., Liu, H., Camp, C., Rossano, S. M., Fowles, K., Martins, S., Spann, M. N., Groman, S., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.09.03.674103
“For example, major white-matter tracts are present in the third trimester 2 , leading to the establishment of highly connected hub regions and an adult-like network organization by birth 3 .”
Charting the Normal Development of Structural Brain Connectivity in Utero Using Diffusion MRI
Karimi, D., Li, B., Taymourtash, A., Jaimes, C. E., Grant, P. E., & Warfield, S. K. (2026) · Human Brain Mapping · doi:10.1002/hbm.70609
Trajectories of functional connectivity in brain maturation
Liang, X., Sun, L., Cao, M., & Yong He, A. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-19099-5.00009-x
Cook, K. M., Asis‐Cruz, J. D., Kim, J.-H., Basu, S. K., Andescavage, N. N., Murnick, J., Spoehr, E., Liggett, M., du Plessis, A. J., & Limperopoulos, C. (2023) · Figshare · doi:10.6084/m9.figshare.24558050
Chen, B., Ji, L., Menu, I., Taylor, A., Trentacosta, C. J., & Thomason, M. E. (2026) · Neuroimage Reports · doi:10.1016/j.ynirp.2026.100326
“…sensory networks (e.g., visual, somatosensory) and thalamocortical pathways warrant further investigation, as these connections are among the earliest to form and mature and serve as functional hubs in the fetal brain (Sch ¨ opf et al., 2012; Taymourtash et al., 2023; van den Heuvel et al., 2018).”
Self-citation
Metadata
- Authors
- van den Heuvel, M. I., Turk, E., Manning, J. H., Hect, J., Hernandez-Andrade, E., Hassan, S. S., Romero, R., van den Heuvel, M. P., & Thomason, M. E.
- Affiliations
- University Medical Center Utrecht (NL)
- National Institutes of Health (US)
- Wayne State University (US)
- United States Department of Health and Human Services (US)
- Venue
- Developmental Cognitive Neuroscience
- Publisher
- Elsevier BV
- Published
- 2018-04
- Volume
- 30
- Pages
- 108-115
- ISSN
- 1878-9293 (ISSN-L)
- PMC
- PMC5963507
- OpenAlex
- W2793015464
- Cited by
- 108
- References
- 68
- Citations by year
- 2026: 9 · 2025: 11 · 2024: 14 · 2023: 21 · 2022: 14 · 2021: 11 · 2020: 14 · 2019: 12 · 2018: 2
- FWCI
- 5.80
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Developmental Cognitive Neuroscience (publishedVersion, cc-by-nc-nd)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Pure Amsterdam UMC (publishedVersion, other-oa)
- Research portal (Tilburg University) (submittedVersion, cc-by-nc-nd)
- Data Archiving and Networked Services (DANS) (submittedVersion, cc-by-nc-nd)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
- Amsterdam UMC (VU Amsterdam) - Institutional Repository (submittedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- Funders
- Nederlandse Organisatie voor Wetenschappelijk Onderzoek (452-16-015)
- U.S. Department of Health and Human Services
- National Institutes of Health (ES020957, ES026022, MH110793)
- National Alliance for Research on Schizophrenia and Depression
- Eunice Kennedy Shriver National Institute of Child Health and Human Development
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced Neuroimaging Techniques and Applications
- Physical Sciences › Physics and Astronomy › Statistical and Nonlinear Physics › Complex Network Analysis Techniques
- Keywords
- human fetal brain, brain network development, resting-state functional connectivity, cerebellum, visual cortex, motor cortex, association cortex, fusiform face area, Wernicke's area, global efficiency, fetal brain development
- MeSH terms
- Adult, Brain, Female, Humans, Male, Neural Pathways, Pregnancy, Young Adult
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