Global Network Organization of the Fetal Functional Connectome
Open accessAbstract
Recent advances in brain imaging have enabled non-invasive in vivo assessment of the fetal brain. Characterizing brain development in healthy fetuses provides baseline measures for identifying deviations in brain function in high-risk clinical groups. We examined 110 resting state MRI data sets from fetuses at 19 to 40 weeks’ gestation. Using graph-theoretic techniques, we characterized global organizational features of the fetal functional connectome and their prenatal trajectories. Topological features related to network integration (i.e., global efficiency) and segregation (i.e., clustering) were assessed. Fetal networks exhibited small-world topology, showing high clustering and short average path length relative to reference networks. Likewise, fetal networks’ quantitative small world indices met criteria for small-worldness (σ > 1, ω = [−0.5 0.5]). Along with this, fetal networks demonstrated global and local efficiency, economy, and modularity. A right-tailed degree distribution, suggesting the presence of central areas that are more highly connected to other regions, was also observed. Metrics, however, were not static during gestation; measures associated with segregation—local efficiency and modularity—decreased with advancing gestational age. Altogether, these suggest that the neural circuitry underpinning the brain’s ability to segregate and integrate information exists as early as the late 2nd trimester of pregnancy and reorganizes during the prenatal period. Significance statement. Mounting evidence for the fetal origins of some neurodevelopmental disorders underscores the importance of identifying features of healthy fetal brain functional development. Alterations in prenatal brain connectomics may serve as early markers for identifying fetal-onset neurodevelopmental disorders, which in turn provide improved surveillance of at-risk fetuses and support the initiation of early interventions.
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Fetal networks exhibit efficient small-world organization.
“Fetal networks, like adults, exhibit efficient small-world organization, suggesting that regions are simultaneously well integrated with topologically distant regions of the brain while forming specialized clusters with their close-by neighbors [69, 70].”
From Brain structural and functional outcomes in the offspring of women experiencing psychological distress during pregnancy (2024) · cites this paper as [69]
Fetal resting-state networks form clusters or modules; this modularity decreases with advancing gestational age.
“Fetal resting-state networks also tend to form clusters or modules; this tendency, called modularity, decreases with advancing gestational age [69, 70].”
From Brain structural and functional outcomes in the offspring of women experiencing psychological distress during pregnancy (2024) · cites this paper as [69]
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Collective dynamics of ‘small-world’ networks
Watts, D. J., & Strogatz, S. H. (1998) · Nature · doi:10.1038/30918 · Cited by 43,060 · see citing works
Modularity and community structure in networks
Newman, M. E. J. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0601602103 · Cited by 12,256 · see citing works
Jenkinson, M., Bannister, P., Brady, M., & Smith, S. (2002) · NeuroImage · doi:10.1006/nimg.2002.1132 · Cited by 11,888 · see citing works
Complex brain networks: graph theoretical analysis of structural and functional systems
Bullmore, E., & Sporns, O. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2575 · Cited by 11,820 · see citing works
Complex network measures of brain connectivity: Uses and interpretations
Rubinov, M., & Sporns, O. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2009.10.003 · Cited by 11,522 · see citing works
AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages
Cox, R. W. (1996) · Computers and Biomedical Research · doi:10.1006/cbmr.1996.0014 · Cited by 10,913 · see citing works
Functional connectivity in the motor cortex of resting human brain using echo‐planar mri
Biswal, B., Zerrin Yetkin, F., Haughton, V. M., & Hyde, J. S. (1995) · Magnetic Resonance in Medicine · doi:10.1002/mrm.1910340409 · Cited by 9,812 · see citing works
Strogatz, S. H. (2001) · Nature · doi:10.1038/35065725 · Cited by 8,236 · see citing works
Power, J. D., Barnes, K. A., Snyder, A. Z., Schlaggar, B. L., & Petersen, S. E. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2011.10.018 · Cited by 7,429 · see citing works
A global optimisation method for robust affine registration of brain images
Jenkinson, M., & Smith, S. M. (2001) · Medical Image Analysis · doi:10.1016/s1361-8415(01)00036-6 · Cited by 6,806 · see citing works
Neurophysiological investigation of the basis of the fMRI signal
Logothetis, N. K., Pauls, J., Augath, M., Trinath, T., & Oeltermann, A. (2001) · Nature · doi:10.1038/35084005 · Cited by 6,542 · see citing works
N4ITK: Improved N3 Bias Correction
Tustison, N. J., Avants, B., Cook, P. A., Zheng, Y., Egan, A., Yushkevich, P. A., & Gee, J. C. (2010) · IEEE Transactions on Medical Imaging · doi:10.1109/tmi.2010.2046908 · Cited by 6,119 · see citing works
Models for Longitudinal Data: A Generalized Estimating Equation Approach
Zeger, S. L., Liang, K., & Albert, P. S. (1988) · Biometrics · doi:10.2307/2531734 · Cited by 4,505 · see citing works
A component based noise correction method (CompCor) for BOLD and perfusion based fMRI
Behzadi, Y., Restom, K., Liau, J., & Liu, T. T. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.04.042 · Cited by 4,502 · see citing works
Movement‐Related effects in fMRI time‐series
Friston, K. J., Williams, S., Howard, R., Frackowiak, R. S. J., & Turner, R. (1996) · Magnetic Resonance in Medicine · doi:10.1002/mrm.1910350312 · Cited by 3,774 · see citing works
Specification of Cerebral Cortical Areas
Rakic, P. (1988) · Science · doi:10.1126/science.3291116 · Cited by 3,127 · see citing works
Classes of small-world networks
Amaral, L. A. N., Scala, A., Barthélémy, M., & Stanley, H. E. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.200327197 · Cited by 3,051 · see citing works
Specificity and Stability in Topology of Protein Networks
Maslov, S., & Sneppen, K. (2002) · Science · doi:10.1126/science.1065103 · Cited by 3,051 · see citing works
A mesoscale connectome of the mouse brain
Oh, S. W., Harris, J. A., Ng, L., Winslow, B., Cain, N., Mihalas, S., Wang, Q., Lau, C., Kuan, L., Henry, A. M., et al. (2014) · Nature · doi:10.1038/nature13186 · Cited by 2,612 · see citing works
Efficiency and Cost of Economical Brain Functional Networks
Achard, S., & Bullmore, E. (2007) · PLoS Computational Biology · doi:10.1371/journal.pcbi.0030017 · Cited by 2,553 · see citing works
Bassett, D. S., & Sporns, O. (2017) · Nature Neuroscience · doi:10.1038/nn.4502 · Cited by 2,398 · see citing works
Achard, S., Salvador, R., Whitcher, B., Suckling, J., & Bullmore, E. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.3874-05.2006 · Cited by 2,393 · see citing works
Scientific collaboration networks. I. Network construction and fundamental results
Newman, M. E. J. (2001) · Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics · doi:10.1103/physreve.64.016131 · Cited by 2,094 · see citing works
The basics of brain development
Stiles, J., & Jernigan, T. L. (2010) · Neuropsychology Review · doi:10.1007/s11065-010-9148-4 · Cited by 2,009 · see citing works
A whole brain fMRI atlas generated via spatially constrained spectral clustering
Craddock, R. C., James, G. A., Holtzheimer, P. E., Hu, X. P., & Mayberg, H. S. (2012) · Human Brain Mapping · doi:10.1002/hbm.21333 · Cited by 1,636 · see citing works
Evolution of the neocortex: a perspective from developmental biology
Rakic, P. (2009) · Nature reviews. Neuroscience · doi:10.1038/nrn2719 · Cited by 1,565 · see citing works
Functional brain networks develop from a local to distributed organization
Fair, D. A., Cohen, A. L., Power, J. D., Dosenbach, N. U. F., Church, J. A., Miezin, F. M., Schlaggar, B. L., & Petersen, S. E. (2009) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000381 · Cited by 1,530 · see citing works
Network ‘Small-World-Ness’: A Quantitative Method for Determining Canonical Network Equivalence
Humphries, M. D., & Gurney, K. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002051 · Cited by 1,442 · see citing works
Normal development of brain circuits
Tau, G. Z., & Peterson, B. S. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.115 · Cited by 1,391 · see citing works
Functional Connectivity and Brain Networks in Schizophrenia
Lynall, M.-E., Bassett, D. S., Kerwin, R., McKenna, P. J., Kitzbichler, M. G., Müller, U., & Bullmore, E. T. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.0333-10.2010 · Cited by 1,348 · see citing works
Sex differences in the structural connectome of the human brain
Ingalhalikar, M., Smith, A., Parker, D., Satterthwaite, T. D., Elliott, M. A., Ruparel, K., Hakonarson, H., Gur, R. E., Gur, R. C., & Verma, R. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1316909110 · Cited by 1,223 · see citing works
Hierarchical Organization of Human Cortical Networks in Health and Schizophrenia
Bassett, D. S., Bullmore, E. T., Verchinski, B. A., Mattay, V. S., Weinberger, D. R., & Meyer‐Lindenberg, A. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1929-08.2008 · Cited by 1,203 · see citing works
Concurrent overproduction of synapses in diverse regions of the primate cerebral cortex
Rakic, P., Bourgeois, J.-P., Eckenhoff, M. F., Zecevic, N., & Goldman-Rakic, P. S. (1986) · Science · doi:10.1126/science.3952506 · Cited by 1,133 · cited 1× · see citing works
“A series of carefully orchestrated processes including neurogenesis, neural migration, and neural circuitry formation, among others, commence during the third embryonic week and are shaped by genetic and later, epigenetic and environmental factors (Rakic et al. 1986; Rakic 1988; Kostovic and Rakic 1990; Kostović and J…”
BackgroundThe Underpinnings of the BOLD Functional Magnetic Resonance Imaging Signal
Logothetis, N. K. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-10-03963.2003 · Cited by 1,024 · see citing works
Development of the human cerebral cortex: Boulder Committee revisited
Bystron, I., Blakemore, C., & Rakic, P. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2252 · Cited by 977 · see citing works
The neural basis of the blood–oxygen–level–dependent functional magnetic resonance imaging signal
Logothetis, N. K. (2002) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2002.1114 · Cited by 952 · see citing works
Kostović, I., & RAKIC, P. T. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.902970309 · Cited by 912 · see citing works
Small-World Brain Networks Revisited
Bassett, D. S., & Bullmore, E. T. (2016) · The Neuroscientist · doi:10.1177/1073858416667720 · Cited by 840 · see citing works
Adaptive reconfiguration of fractal small-world human brain functional networks
Bassett, D. S., Meyer-Lindenberg, A., Achard, S., Duke, T., & Bullmore, E. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0606005103 · Cited by 814 · see citing works
Development of large-scale functional brain networks in children
Supekar, K., Musen, M., & Menon, V. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000157 · Cited by 807 · see citing works
Longitudinal Analysis of Neural Network Development in Preterm Infants
Smyser, C. D., Inder, T. E., Shimony, J. S., Hill, J. E., Degnan, A. J., Snyder, A. Z., & Neil, J. J. (2010) · Cerebral Cortex · doi:10.1093/cercor/bhq035 · Cited by 791 · see citing works
The Segregation and Integration of Distinct Brain Networks and Their Relationship to Cognition
Cohen, J. R., & D’Esposito, M. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.2965-15.2016 · Cited by 767 · see citing works
Hallquist, M. N., Hwang, K., & Luna, B. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2013.05.116 · Cited by 753 · see citing works
Graph analysis of the human connectome: Promise, progress, and pitfalls
Fornito, A., Zalesky, A., & Breakspear, M. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2013.04.087 · Cited by 743 · see citing works
Identifying the role that animals play in their social networks
Lusseau, D., & Newman, M. (2004) · Proceedings of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rsbl.2004.0225 · Cited by 733 · see citing works
Ojemann, J. G., Akbudak, E., Snyder, A. Z., McKinstry, R. C., Raichle, M. E., & Conturo, T. E. (1997) · NeuroImage · doi:10.1006/nimg.1997.0289 · Cited by 699 · see citing works
The brainstem reticular formation is a small-world, not scale-free, network
Humphries, M. D., GURNEY, K. N., & Prescott, T. J. (2005) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2005.3354 · Cited by 609 · see citing works
Emergence of resting state networks in the preterm human brain
Doria, V., Beckmann, C. F., Arichi, T., Merchant, N., Groppo, M., Turkheimer, F. E., Counsell, S. J., Murgasova, M., Aljabar, P., Nunes, R. G., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1007921107 · Cited by 574 · see citing works
Energetic cost of brain functional connectivity
Tomasi, D. G., Wang, G., & Volkow, N. D. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1303346110 · Cited by 569 · see citing works
The development of cerebral connections during the first 20–45 weeks’ gestation
Kostović, I., & Milošević, N. J. (2006) · Seminars in Fetal and Neonatal Medicine · doi:10.1016/j.siny.2006.07.001 · Cited by 568 · see citing works
The functional architecture of the infant brain as revealed by resting-state fMRI
Fransson, P., Åden, U., Blennow, M., & Lagercrantz, H. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhq071 · Cited by 542 · see citing works
The Ubiquity of Small-World Networks
Telesford, Q. K., Joyce, K. E., Hayasaka, S., Burdette, J. H., & Laurienti, P. J. (2011) · Brain Connectivity · doi:10.1089/brain.2011.0038 · Cited by 517 · see citing works
Mapping sources of correlation in resting state FMRI, with artifact detection and removal
Jo, H. J., Saad, Z. S., Simmons, W. K., Milbury, L. A., & Cox, R. W. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.04.246 · Cited by 509 · see citing works
Early patterns of electrical activity in the developing cerebral cortex of humans and rodents
Khazipov, R., & Luhmann, H. J. (2006) · Trends in Neurosciences · doi:10.1016/j.tins.2006.05.007 · Cited by 482 · see citing works
The development of the subplate and thalamocortical connections in the human foetal brain
Kostović, I., & Judaš, M. (2010) · Acta Paediatrica · doi:10.1111/j.1651-2227.2010.01811.x · Cited by 462 · see citing works
Reduction of motion-related artifacts in resting state fMRI using aCompCor
Muschelli, J., Nebel, M. B., Caffo, B. S., Barber, A. D., Pekar, J. J., & Mostofsky, S. H. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2014.03.028 · Cited by 431 · see citing works
Cognitive fitness of cost-efficient brain functional networks
Bassett, D. S., Bullmore, E. T., Meyer‐Lindenberg, A., Apud, J. A., Weinberger, D. R., & Coppola, R. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0903641106 · Cited by 429 · see citing works
The Neonatal Connectome During Preterm Brain Development
van den Heuvel, M. P., Kersbergen, K. J., de Reus, M. A., Keunen, K., Kahn, R. S., Groenendaal, F., de Vries, L. S., & Benders, M. J. N. L. (2015) · Cerebral Cortex · doi:10.1093/cercor/bhu095 · Cited by 386 · see citing works
The development of synapses in cerebral cortex of the human fetus
Molliver, M. E., Kostović, I., & der Loos, H. V. (1973) · Brain Research · doi:10.1016/0006-8993(73)90741-5 · Cited by 385 · see citing works
Hayasaka, S., & Laurienti, P. J. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2009.12.051 · Cited by 374 · see citing works
Gholipour, A., Rollins, C. K., Velasco‐Annis, C., Ouaalam, A., Akhondi‐Asl, A., Afacan, O., Ortinau, C. M., Clancy, S., Limperopoulos, C., Yang, E., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-00525-w · Cited by 357 · see citing works
Self-citationDevelopment of human brain cortical network architecture during infancy
Gao, W., Alcauter, S., Smith, J. K., Gilmore, J. H., & Lin, W. (2015) · Brain Structure and Function · doi:10.1007/s00429-014-0710-3 · Cited by 356 · see citing works
Electroencephalography in premature and full-term infants. Developmental features and glossary
André, M., Lamblin, M., D'Allest, A. M., Curzi-Dascalova, L., MOUSSALLISALEFRANQUE, F., Tich, S. N. T., Vecchierini, M.-F., Wallois, F., Walls-Esquivel, E., & Plouin, P. (2010) · Neurophysiologie Clinique · doi:10.1016/j.neucli.2010.02.002 · Cited by 349 · see citing works
van den Heuvel, M. P., Bullmore, E. T., & Sporns, O. (2016) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2016.03.001 · Cited by 328 · see citing works
Rapid Cortical Oscillations and Early Motor Activity in Premature Human Neonate
Milh, M., Kamińska, A., Huon, C., Lapillonne, A., Ben‐Ari, Y., & Khazipov, R. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhl069 · Cited by 322 · see citing works
Development of neonatal EEG activity: From phenomenology to physiology
Vanhatalo, S., & Kaila, K. (2006) · Seminars in Fetal and Neonatal Medicine · doi:10.1016/j.siny.2006.07.008 · Cited by 314 · see citing works
Small-World Propensity and Weighted Brain Networks
Muldoon, S. F., Bridgeford, E., & Bassett, D. S. (2016) · Scientific Reports · doi:10.1038/srep22057 · Cited by 305 · see citing works
Fetal Testosterone Influences Sexually Dimorphic Gray Matter in the Human Brain
Lombardo, M. V., Ashwin, E., Auyeung, B., Chakrabarti, B., Taylor, K., Hackett, G., Bullmore, E. T., & Baron-Cohen, S. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.4389-11.2012 · Cited by 302 · see citing works
Jo, H. J., Gotts, S. J., Reynolds, R. C., Bandettini, P. A., Martin, A. D., Cox, R. W., & Saad, Z. S. (2013) · Journal of Applied Mathematics · doi:10.1155/2013/935154 · Cited by 277 · see citing works
Luhmann, H. J., Sinning, A., Yang, J., Reyes‐Puerta, V., Stüttgen, M. C., Kirischuk, S., & Kilb, W. (2016) · Frontiers in Neural Circuits · doi:10.3389/fncir.2016.00040 · Cited by 275 · see citing works
Glover, V., O'Donnell, K. J., O'Connor, T. G., & Fisher, J. (2018) · Development and Psychopathology · doi:10.1017/s095457941800038x · Cited by 271 · see citing works
The fetal origins of mental illness
al-Haddad, B. J. S., Oler, E., Armistead, B., Elsayed, N. A., Weinberger, D. R., Bernier, R., Burd, I. D., Kapur, R. P., Jacobsson, B., Wang, C., et al. (2019) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2019.06.013 · Cited by 265 · see citing works
Neural histology and neurogenesis of the human fetal and infant brain
Kostović, I., Sedmak, G., & Judáš, M. (2018) · NeuroImage · doi:10.1016/j.neuroimage.2018.12.043 · Cited by 259 · see citing works
Unified Framework for Development, Deployment and Robust Testing of Neuroimaging Algorithms
Joshi, A. P., Scheinost, D., Okuda, H., Belhachemi, D., Murphy, I., Staib, L. H., & Papademetris, X. (2011) · Neuroinformatics · doi:10.1007/s12021-010-9092-8 · Cited by 227 · see citing works
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
Hallquist, M. N., & Hillary, F. G. (2018) · Network Neuroscience · doi:10.1162/netn_a_00054 · Cited by 219 · see citing works
Neurogenesis Continues in the Third Trimester of Pregnancy and Is Suppressed by Premature Birth
Malik, S. K., Vinukonda, G., Vose, L. R., Diamond, D., Bhimavarapu, B. B. R., Hu, F., Zia, M., Hevner, R. F., Zečević, N., & Ballabh, P. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.4445-12.2013 · Cited by 203 · see citing works
Development of BOLD signal hemodynamic responses in the human brain
Arichi, T., Fagiolo, G., Varela, M., Melendez-Calderon, A., Allievi, A., Merchant, N. M., Tusor, N., Counsell, S. J., Burdet, E., Beckmann, C. F., et al. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.06.054 · Cited by 202 · see citing works
Programmed cell death in the developing human telencephalon
Rakić, S., & Zečević, N. (2000) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2000.00153.x · Cited by 202 · see citing works
Prenatal growth in humans and postnatal brain maturation into late adolescence
Raznahan, A., GREENSTEIN, D. K., Lee, N., CLASEN, L. S., & Giedd, J. N. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1203350109 · Cited by 190 · see citing works
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
Human Cortex Development: Estimates of Neuronal Numbers Indicate Major Loss Late During Gestation
Rabinowicz, T., de Courten-Myers, G. M., Petetot, J. M.-C., XI, G., & de los Reyes, E. (1996) · Journal of Neuropathology and Experimental Neurology · doi:10.1097/00005072-199603000-00007 · Cited by 184 · see citing works
Cao, M., Yong He, A., Dai, Z., Liao, X., Jeon, T., Ouyang, M., Chalak, L. F., Bi, Y., Rollins, N. K., Dong, Q., et al. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhw038 · Cited by 182 · see citing works
Exploring early human brain development with structural and physiological neuroimaging
Vasung, L., Abaci Turk, E., Ferradal, S. L., Sutin, J., Stout, J. N., Ahtam, B., Lin, P.-Y., & Grant, P. E. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2018.07.041 · Cited by 177 · see citing works
Wu, K., Taki, Y., Sato, K., Hashizume, H., Sassa, Y., Takeuchi, H., Thyreau, B., Yong He, A., Evans, A. C., Li, X., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0055347 · Cited by 176 · see citing works
The emergence of functional architecture during early brain development
Keunen, K., Counsell, S. J., & Benders, M. J. N. L. (2017) · NeuroImage · doi:10.1016/j.neuroimage.2017.01.047 · Cited by 176 · see citing works
Functional Connectome of the Fetal Brain
Turk, E., van den Heuvel, M. I., Benders, M. J., de Heus, R., Franx, A., Manning, J. H., Hect, J. L., Hernandez-Andrade, E., Hassan, S. S., Romero, R., et al. (2019) · The Journal of Neuroscience · doi:10.1523/jneurosci.2891-18.2019 · Cited by 176 · see citing works
Functional structure of cortical neuronal networks grownin vitro
Bettencourt, L. M. A., Stephens, G. J., Ham, M., & Gross, G. W. (2007) · Physical Review E · doi:10.1103/physreve.75.021915 · Cited by 174 · see citing works
Sex and Age Effects of Functional Connectivity in Early Adulthood
Zhang, C., Cahill, N. D., Arbabshirani, M. R., White, T. J. H., Baum, S. A., & Michael, A. M. (2016) · Brain Connectivity · doi:10.1089/brain.2016.0429 · Cited by 170 · see citing works
Vasung, L., Huang, H., Jovanov‐Milošević, N., Pletikos, M., Mori, S., & Kostović, I. (2010) · Journal of Anatomy · doi:10.1111/j.1469-7580.2010.01260.x · Cited by 169 · see citing works
Human cortex development: estimates of neuronal numbers indicate major loss late during gestation.
Rabinowicz, T., de Courten‐Myers, G. M., Petétot, J. M.-C., Xi, G., & Reyes, E. D. L. (1996) · PubMed · Cited by 169 · see citing works
Weak functional connectivity in the human fetal brain prior to preterm birth
Thomason, M. E., Scheinost, D., Manning, J. H., Grove, L. E., Hect, J. L., Marshall, N. A., Hernandez‐Andrade, E. A., Berman, S., Pappas, A., Yeo, L., et al. (2017) · Scientific Reports · doi:10.1038/srep39286 · Cited by 153 · see citing works
Small-world network organization of functional connectivity of EEG slow-wave activity during sleep
Ferri, R., Rundo, F., Bruni, O., Terzano, M. G., & Stam, C. J. (2006) · Clinical Neurophysiology · doi:10.1016/j.clinph.2006.10.021 · Cited by 142 · see citing works
Altered Network Topologies and Hub Organization in Adults with Autism: A Resting-State fMRI Study
Itahashi, T., Yamada, T., Watanabe, H., Nakamura, M., Jimbo, D., Shioda, S., Toriizuka, K., Kato, N., & Hashimoto, R. (2014) · PLoS ONE · doi:10.1371/journal.pone.0094115 · Cited by 139 · see citing works
Watching the fetal brain at ‘rest’
Schöpf, V., Kasprian, G., Brugger, P. C., & Prayer, D. (2012) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2011.10.006 · Cited by 137 · see citing works
Early Brain Activity Relates to Subsequent Brain Growth in Premature Infants
Benders, M. J. N. L., Palmu, K., Menache, C. C., Borradori-Tolsa, C., Lazeyras, F., Sizonenko, S. V., Dubois, J., Vanhatalo, S., & Hüppi, P. S. (2014) · Cerebral Cortex · doi:10.1093/cercor/bhu097 · Cited by 133 · see citing works
Intrinsic Functional Brain Architecture Derived from Graph Theoretical Analysis in the Human Fetus
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., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0094423 · Cited by 130 · see citing works
Growth of Thalamocortical Fibers to the Somatosensory Cortex in the Human Fetal Brain
Krsnik, Ž., Majić, V., Vasung, L., Huang, H., & Kostović, I. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00233 · Cited by 127 · see citing works
Sex differences in functional connectivity during fetal brain development
Wheelock, M. D., Hect, J. L., Hernandez-Andrade, E., Hassan, S. S., Romero, R., Eggebrecht, A. T., & Thomason, M. E. (2019) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2019.100632 · Cited by 126 · see citing works
Development of hemodynamic responses and functional connectivity in rat somatosensory cortex
Colonnese, M. T., Phillips, M. A., Constantine‐Paton, M., Kaila, K., & Jasanoff, A. (2007) · Nature Neuroscience · doi:10.1038/nn2017 · Cited by 124 · see citing works
Kostović, I., & JUDAS, M. (2007) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2007.04.018 · Cited by 119 · see citing works
Chen, Y., Wang, S.-J., Hilgetag, C. C., & Zhou, C. (2013) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002937 · Cited by 116 · see citing works
International Symposium on Biomedical Imaging
(2009) · IEEE Transactions on Image Processing · doi:10.1109/tip.2009.2032059 · Cited by 116 · see citing works
Tolonen, M., Palva, J. M., Andersson, S., & Vanhatalo, S. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2006.12.070 · Cited by 114 · see citing works
A Window for the Study of Prenatal Sex Hormone Influences on Postnatal Development
Finegan, J. K., Bartleman, B., & Wong, P. Y. (1989) · The Journal of Genetic Psychology · doi:10.1080/00221325.1989.9914580 · Cited by 113 · see citing works
Hubs in the human fetal brain network
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. (2018) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2018.02.001 · Cited by 108 · cited 1× · see citing works
“…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…”
Backgroundde Zegher, F., Devlieger, H., & Veldhuis, J. D. (1992) · Pediatric Research · doi:10.1203/00006450-199211000-00025 · Cited by 104 · see citing works
Subplate cells: amplifiers of neuronal activity in the developing cerebral cortex
Luhmann, H. J. (2009) · Frontiers in Neuroanatomy · doi:10.3389/neuro.05.019.2009 · Cited by 95 · see citing works
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
Development of the Human Fetal Auditory Cortex: Growth of Afferent Fibres
Krmpotić‐Nemanić, J., Kostović, I., Kelović, Z., Nemanić, Đ., & Mrzljak, L. (1983) · Cells Tissues Organs · doi:10.1159/000145727 · Cited by 89 · see citing works
Self‐organization of repetitive spike patterns in developing neuronal networks in vitro
Sun, J., Kilb, W., & Luhmann, H. J. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07383.x · Cited by 88 · see citing works
Functional properties of resting state networks in healthy full-term newborns
De Asis-Cruz, J., Bouyssi-Kobar, M., Evangelou, I., Vezina, G., & Limperopoulos, C. (2015) · Scientific Reports · doi:10.1038/srep17755 · Cited by 85 · see citing works
Self-citationComprehensive Pediatric Hospital Medicine
(2007) · Elsevier eBooks · doi:10.1016/b978-0-323-03004-5.x5001-7 · Cited by 81 · see citing works
Association of Prenatal Maternal Anxiety With Fetal Regional Brain Connectivity
De Asis-Cruz, J., Krishnamurthy, D., Zhao, L., Kapse, K., Vezina, G., Andescavage, N., Quistorff, J., Lopez, C., & Limperopoulos, C. (2020) · JAMA Network Open · doi:10.1001/jamanetworkopen.2020.22349 · Cited by 81 · see citing works
Self-citation(2010) · Cambridge University Press eBooks · doi:10.1017/cbo9780511711848 · Cited by 71 · see citing works
Marrelec, G., & Fransson, P. (2011) · PLoS ONE · doi:10.1371/journal.pone.0014788 · Cited by 71 · see citing works
Asis‐Cruz, J. D., Donofrio, M. T., Vézina, G., & Limperopoulos, C. (2017) · NeuroImage Clinical · doi:10.1016/j.nicl.2017.09.020 · Cited by 69 · see citing works
Self-citationKostović, I., Išasegi, I. Ž., & Krsnik, Ž. (2018) · Journal of Anatomy · doi:10.1111/joa.12920 · Cited by 67 · see citing works
Functional brain connectivity in ex utero premature infants compared to in utero fetuses
De Asis-Cruz, J., Kapse, K., Basu, S. K., Said, M., Scheinost, D., Murnick, J., Chang, T., du Plessis, A., & Limperopoulos, C. (2020) · NeuroImage · doi:10.1016/j.neuroimage.2020.117043 · Cited by 63 · see citing works
Self-citationRobinson, R., Lahti‐Pulkkinen, M., Heinonen, K., Reynolds, R. M., & Räikkönen, K. (2018) · Pediatric Research · doi:10.1038/s41390-018-0173-y · Cited by 55 · see citing works
You, X., Norr, M. E., Murphy, E. R., Kuschner, E. S., Bal, E., Gaillard, W. D., Kenworthy, L. E., & Vaidya, C. J. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00482 · Cited by 52 · see citing works
Vasung, L., Rollins, C. K., Yun, H. J., Velasco‐Annis, C., Zhang, J., Wagstyl, K., Evans, A. C., Warfield, S. K., Feldman, H. A., Grant, P. E., et al. (2019) · Cerebral Cortex · doi:10.1093/cercor/bhz200 · Cited by 51 · see citing works
Lord, A., Ehrlich, S., Borchardt, V., Geisler, D., Seidel, M., Huber, S., Murr, J., & Walter, M. (2016) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2016.02.001 · Cited by 45 · see citing works
Comparative Primate Connectomics
Rilling, J. K., & van den Heuvel, M. P. (2018) · Brain Behavior and Evolution · doi:10.1159/000488886 · Cited by 45 · see citing works
Neurodevelopment, Aging and Cognition
(1992) · Birkhäuser Boston eBooks · doi:10.1007/978-1-4684-6805-2 · Cited by 44 · see citing works
Oxygen Delivery to the Brain Before and After Birth
Jones, M., Rosenberg, A. A., Simmons, M. A., et al. (1982) · Science · doi:10.1126/science.6801768 · Cited by 43 · see citing works
Development of Acetylcholinesterase (Ache) Staining in Human Fetal Auditory Cortex
Krmpotić‐Nemanić, J., Kostović, I., Kelović, Z., & Nemanić, Đ. (1980) · Acta Oto-Laryngologica · doi:10.3109/00016488009127153 · Cited by 41 · see citing works
Atlas55+: Brain Functional Atlas of Resting-State Networks for Late Adulthood
Doucet, G. E., Labache, L., Thompson, P. M., Joliot, M., Frangou, S., & Initiative, A. D. N. (2020) · Cerebral Cortex · doi:10.1093/cercor/bhaa321 · Cited by 34 · see citing works
Is Autism, at Least in Part, a Disorder of Fetal Programming?
Szatmári, P. (2011) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2011.99 · Cited by 33 · see citing works
How are specific connections formed between thalamus and cortex?
Shatz, C. J. (1992) · Current Opinion in Neurobiology · doi:10.1016/0959-4388(92)90166-i · Cited by 32 · see citing works
Modern Methods for Interrogating the Human Connectome
Lowe, M. J., Sakaie, K., Beall, E. B., Calhoun, V. D., Bridwell, D. A., Rubinov, M., & Rao, S. M. (2016) · Journal of the International Neuropsychological Society · doi:10.1017/s1355617716000060 · Cited by 28 · see citing works
Intensity-based masking: A tool to improve functional connectivity results of resting-state fMRI
Peer, M., Abboud, S., Hertz, U., Amedi, A., & Arzy, S. (2016) · Human Brain Mapping · doi:10.1002/hbm.23182 · Cited by 28 · see citing works
Rotem‐Kohavi, N., Williams, L. J., & Oberlander, T. F. (2020) · Seminars in Perinatology · doi:10.1016/j.semperi.2020.151223 · Cited by 12 · see citing works
Developmental Reorganization of the Human Association Cortex during Perinatal and Postnatal Life
Kostović, I., Petanjek, Z., Delalle, I., & Judáš, M. (1992) · Birkhäuser Boston eBooks · doi:10.1007/978-1-4684-6805-2_1 · Cited by 10 · see citing works
Fetal functional imaging portrays heterogeneous development of emerging human brain networks
Jakab, A., Schwartz, E., Kasprian, G., Gruber, G. M., Prayer, D., Schöpf, V., & Langs, G. (2014) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2014.00852 · Cited by 10 · see citing works
Li, X., Hect, J. L., Thomason, M. E., & Zhu, D. (2020) · IEEE International Symposium on Biomedical Imaging (ISBI) · doi:10.1109/isbi45749.2020.9098606 · Cited by 10 · see citing works
Functional Imaging in the Fetus
Schöpf, V., Kasprian, G. J., & Prayer, D. (2011) · Topics in Magnetic Resonance Imaging · doi:10.1097/rmr.0b013e3182699283 · Cited by 8 · see citing works
Hartley, C., Farmer, S. F., & Luc Berthouze, A. (2020) · PLoS ONE · doi:10.1371/journal.pone.0226772 · Cited by 7 · see citing works
Degree distributions in mesoscopic and macroscopic functional brain networksPreprint
Hayasaka, S., & Laurienti, P. J. (2009) · arXiv (Cornell University) · doi:10.48550/arxiv.0903.4168 · Cited by 4 · see citing works
de Ungria, M., & Daru, J. A. (2007) · Comprehensive Pediatric Hospital Medicine · doi:10.1016/b978-032303004-5.50052-1 · Cited by 1 · see citing works
Flagged first, then by citations
Research works printed but not linked: 2
- Kostovic I, Molliver ME. 1974. A new interpretation of the laminar development of cerebral cortex: synaptogenesis in different layers of neopallum in the human fetus. Anat Rec. 178:395–395. [Google Scholar]
- Volpe JJ, Inder TE, Darras BT, Vries LS, Plessis AJ, Neil J, Perlman JM. 2017. Volpe's Neurology of the Newborn E-Book. Philadelphia, PA: Elsevier Health Sciences. [Google Scholar]
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Wu, Y., De Asis-Cruz, J., & Limperopoulos, C. (2024) · Molecular Psychiatry · doi:10.1038/s41380-024-02449-0 · Cited by 124 · 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
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
Self-citationKim, J.-H., De Asis-Cruz, J., Krishnamurthy, D., & Limperopoulos, C. (2023) · eLife · doi:10.7554/elife.80878 · Cited by 10 · see citing works
Self-citation
- Authors
- De Asis-Cruz, J., Andersen, N., Kapse, K., Khrisnamurthy, D., Quistorff, J., Lopez, C., Vezina, G., & Limperopoulos, C.
- Affiliations
- Developing Brain Institute, Children's National, 111 Michigan Ave NW, Washington DC 20010
- Children's National (US)
- Division of Diagnostic Imaging and Radiology, 111 Michigan Ave NW, Washington DC 20010
- Corresponding author
- Limperopoulos, Catherine
- Venue
- Cerebral Cortex
- Publisher
- Oxford University Press (OUP)
- Published
- 2021-02-09
- Volume
- 31
- Issue
- 6
- Pages
- 3034-3046
- ISSN
- 1047-3211 (ISSN-L)
- 1460-2199
- PMC
- PMC8107792
- OpenAlex
- W3126661780
- Cited by
- 40
- References
- 140
- Citations by year
- 2026: 6 · 2025: 8 · 2024: 11 · 2023: 6 · 2022: 7 · 2021: 2
- FWCI
- 2.01
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor)
- Locations
- Cerebral Cortex (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Heart, Lung, and Blood Institute (R01 HL116585–01)
- National Institutes of Health
- Canadian Institute of Health Research (MOP-81116)
- 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
- fetal brain, functional connectome, resting-state MRI, small-world networks, brain development, gestational age, network efficiency, clustering, modularity, degree distribution, prenatal neurodevelopment, neurodevelopmental disorders, graph theory
- MeSH terms
- Brain, Female, Fetus, Humans, Longitudinal Studies, Magnetic Resonance Imaging, Nerve Net, Pregnancy, Prospective Studies, Fetal Development, Connectome
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