Fetal functional imaging portrays heterogeneous development of emerging human brain networks
Open accessAbstract
The functional connectivity architecture of the adult human brain enables complex cognitive processes, and exhibits a remarkably complex structure shared across individuals. We are only beginning to understand its heterogeneous structure, ranging from a strongly hierarchical organization in sensorimotor areas to widely distributed networks in areas such as the parieto-frontal cortex. Our study relied on the functional magnetic resonance imaging (fMRI) data of 32 fetuses with no detectable morphological abnormalities. After adapting functional magnetic resonance acquisition, motion correction, and nuisance signal reduction procedures of resting-state functional data analysis to fetuses, we extracted neural activity information for major cortical and subcortical structures. Resting fMRI networks were observed for increasing regional functional connectivity from 21st to 38th gestational weeks (GWs) with a network-based statistical inference approach. The overall connectivity network, short range, and interhemispheric connections showed sigmoid expansion curve peaking at the 26-29 GW. In contrast, long-range connections exhibited linear increase with no periods of peaking development. Region-specific increase of functional signal synchrony followed a sequence of occipital (peak: 24.8 GW), temporal (peak: 26 GW), frontal (peak: 26.4 GW), and parietal expansion (peak: 27.5 GW). We successfully adapted functional neuroimaging and image post-processing approaches to correlate macroscopical scale activations in the fetal brain with gestational age. This in vivo study reflects the fact that the mid-fetal period hosts events that cause the architecture of the brain circuitry to mature, which presumably manifests in increasing strength of intra- and interhemispheric functional macro connectivity.
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Network strength shows a non-linear, sigmoid expansion mid-gestation first at the occipital lobe around 26 GW, followed by the temporal, frontal, and parietal networks.
“Likewise, network strength shows a non-linear, sigmoid expansion mid-gestation first at the occipital lobe at around 26 GW, followed by the temporal, frontal, and parietal networks [65].”
From Brain structural and functional outcomes in the offspring of women experiencing psychological distress during pregnancy (2024) · cites this paper as [65]
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“Likewise, network strength shows a non-linear, sigmoid expansion mid-gestation fi rst at the occipital lobe at around 26 GW, followed by the temporal, frontal, and parietal networks [65].”
BackgroundEarly human brain development: Starring the subplate
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Thomason, M. E., Hect, J. L., Rauh, V. A., Trentacosta, C., Wheelock, M. D., Eggebrecht, A. T., Espinoza-Heredia, C., & Burt, S. A. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2019.02.017 · Cited by 94 · see citing works
Thomason, M. E., Hect, J. L., Waller, R. E., & Curtin, P. C. P. (2021) · Neuropsychopharmacology · doi:10.1038/s41386-021-01066-7 · Cited by 78 · see citing works
Richmond, S., Johnson, K. A., Seal, M. L., Allen, N. B., & Whittle, S. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.08.024 · Cited by 70 · see citing works
Early development of sleep and brain functional connectivity in term-born and preterm infants
Uchitel, J., Vanhatalo, S., & Austin, T. (2021) · Pediatric Research · doi:10.1038/s41390-021-01497-4 · Cited by 74 · see citing works
Global 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 · see citing works
Aertsen, M., Diogo, M. C., Dymarkowski, S., Deprest, J. A., & Prayer, D. (2019) · Prenatal Diagnosis · doi:10.1002/pd.5579 · Cited by 36 · see citing works
Self-citationRobust 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 · see citing works
Motion correction and volumetric reconstruction for fetal functional magnetic resonance imaging data
Sobotka, D., Ebner, M., Schwartz, E., Nenning, K.-H., Taymourtash, A., Vercauteren, T., Ourselin, S., Kasprian, G., Prayer, D., Langs, G., et al. (2022) · NeuroImage · doi:10.1016/j.neuroimage.2022.119213 · Cited by 20 · see citing works
Self-citationKim, 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
Differential age-dependent development of inter-area brain connectivity in term and preterm neonates
Arimitsu, T., Shinohara, N., Minagawa‐Kawai, Y., Hoshino, E., Hata, M., & Takahashi, T. (2022) · Pediatric Research · doi:10.1038/s41390-022-01939-7 · Cited by 12 · see citing works
Kim, J.-H., De Asis-Cruz, J., Krishnamurthy, D., & Limperopoulos, C. (2023) · eLife · doi:10.7554/elife.80878 · Cited by 10 · see citing works
Canini, M., Pecco, N., Caglioni, M., Katušić, A., Išasegi, I. Ž., Oprandi, C., Scifo, P., Pozzoni, M., Lorioli, L., Garbetta, G., et al. (2023) · Journal of Neuroscience Research · doi:10.1002/jnr.25207 · Cited by 10 · see citing works
Spaceborne and spaceborn: Physiological aspects of pregnancy and birth during interplanetary flight
Holden, A. V. (2025) · Experimental Physiology · doi:10.1113/ep092290 · Cited by 3 · see citing works
Automated 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 · see citing works
Patterns of Early Myelination Identify Functionally Relevant Brain NetworksPreprint
Deoni, S., Bruchhage, M. M. K., Dean, D., D’Sa, V. A., & Schnieder, N. (2022) · Research Square · doi:10.21203/rs.3.rs-2002561/v1 · Cited by 1 · see citing works
A blueprint of the developing mind
Turk, E. (2022) · doi:10.33540/627
- Authors
- Jakab, A., Schwartz, E., Kasprian, G., Gruber, G. M., Prayer, D., Schöpf, V., & Langs, G.
- Affiliations
- Medical University of Vienna (AT)
- Massachusetts Institute of Technology (US)
- Venue
- Frontiers in Human Neuroscience
- Publisher
- Frontiers Media SA
- Published
- 2014-10-22
- Volume
- 8
- Pages
- 852-852
- ISSN
- 1662-5161 (ISSN-L)
- PMC
- PMC4205819
- OpenAlex
- W1966081525
- Cited by
- 10
- References
- 89
- Citations by year
- 2025: 1 · 2023: 2 · 2022: 3 · 2021: 2 · 2019: 2
- FWCI
- 0.00
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Frontiers in Human Neuroscience (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by)
- Frontiers Research Foundation
- Funders
- European Commission (EU-FP7)
- Austrian Science Fund (P23205)
- Oesterreichische Nationalbank (P23205-B09)
- 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 › Radiology, Nuclear Medicine and Imaging › Advanced MRI Techniques and Applications
- Keywords
- fetal brain development, resting-state functional connectivity, gestational age, interhemispheric connections, cortical development, subcortical structures, fetal neuroimaging
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