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Intrinsic Functional Brain Architecture Derived from Graph Theoretical Analysis in the Human Fetus
Open accessAbstract
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, 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]
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Cites
Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing
Benjamini, Y., & Hochberg, Y. (1995) · Journal of the Royal Statistical Society Series B: Statistical Methodology · doi:10.1111/j.2517-6161.1995.tb02031.x · Cited by 109,482
A default mode of brain function
Raichle, M. E., MacLeod, A. M., Snyder, A. Z., Powers, W. J., Gusnard, D. A., & Shulman, G. L. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.98.2.676 · Cited by 12,190
The organization of the human cerebral cortex estimated by intrinsic functional connectivity
Thomas Yeo, B. T., Krienen, F. M., Sepulcre, J., Sabuncu, M. R., Lashkari, D., Hollinshead, M., Roffman, J. L., Smoller, J. W., Zöllei, L., Polimeni, J. R., et al. (2011) · Journal of Neurophysiology · doi:10.1152/jn.00338.2011 · Cited by 9,182
The human brain is intrinsically organized into dynamic, anticorrelated functional networks
Fox, M. D., Snyder, A. Z., Vincent, J. L., Corbetta, M., Van Essen, D. C., & Raichle, M. E. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504136102 · Cited by 8,553
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
The organization of the human cerebellum estimated by intrinsic functional connectivity
Buckner, R. L., Krienen, F. M., Castellanos, A., Diaz, J. C., & Yeo, B. T. T. (2011) · Journal of Neurophysiology · doi:10.1152/jn.00339.2011 · Cited by 7,304
The relation of strength of stimulus to rapidity of habit formation
Yerkes, R. M., & Dodson, J. D. (1908) · Journal of Comparative Neurology and Psychology · doi:10.1002/cne.920180503 · Cited by 6,911
Conn : A Functional Connectivity Toolbox for Correlated and Anticorrelated Brain Networks
Whitfield-Gabrieli, S., & Nieto-Castanon, A. (2012) · Brain Connectivity · doi:10.1089/brain.2012.0073 · Cited by 4,885
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
Mapping the structural core of human cerebral cortex
Hagmann, P., Cammoun, L., Gigandet, X., Meuli, R., Honey, C. J., Wedeen, V. J., & Sporns, O. (2008) · PLoS Biology · doi:10.1371/journal.pbio.0060159 · Cited by 4,173
Functional-anatomic fractionation of the brain’s default network
Andrews-Hanna, J. R., Reidler, J. S., Sepulcre, J., Poulin, R., & Buckner, R. L. (2010) · Neuron · doi:10.1016/j.neuron.2010.02.005 · Cited by 2,767
Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances
Volpe, J. J. (2008) · The Lancet Neurology · doi:10.1016/s1474-4422(08)70294-1 · Cited by 2,501
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
Intrinsic functional architecture in the anaesthetized monkey brain
Vincent, J. L., Patel, G. H., Fox, M. D., Snyder, A. Z., Baker, J. T., Van Essen, D. C., Zempel, J. M., Snyder, L. H., Corbetta, M., & Raichle, M. E. (2007) · Nature · doi:10.1038/nature05758 · Cited by 1,786
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
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
Default Mode Network Activity and Connectivity in Psychopathology
Whitfield-Gabrieli, S., & Ford, J. M. (2012) · Annual Review of Clinical Psychology · doi:10.1146/annurev-clinpsy-032511-143049 · Cited by 1,465
Scale-Free Brain Functional Networks
Eguı́luz, V. M., Chialvo, D. R., Cecchi, G., Baliki, M. N., & Apkarian, A. V. (2005) · Physical Review Letters · doi:10.1103/physrevlett.94.018102 · Cited by 1,464
Fransson, P. (2005) · Human Brain Mapping · doi:10.1002/hbm.20113 · Cited by 1,388
Development of distinct control networks through segregation and integration
Fair, D. A., Dosenbach, N. U. F., Church, J. A., Cohen, A. L., Brahmbhatt, S., Miezin, F. M., Barch, D. M., Raichle, M. E., Petersen, S. E., & Schlaggar, B. L. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0705843104 · Cited by 1,244
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
Fransson, P., & Marrelec, G. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.05.059 · Cited by 1,213 · cited 2×
“For example, from graph analysis of fMRI datasets we have learned that the human brain is organized with small world topology [6] and that the posterior cingulate and insular cortices are connectivity hubs [7–9].”
BackgroundAnticorrelations in resting state networks without global signal regression
Chai, X. J., Nieto-Castañón, A., Öngür, D., & Whitfield, S. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.08.048 · Cited by 1,193
Functional topography of the cerebellum for motor and cognitive tasks: An fMRI study
Stoodley, C. J., Valera, E. M., & Schmahmann, J. D. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2011.08.065 · Cited by 1,106
Precuneus shares intrinsic functional architecture in humans and monkeys
Margulies, D. S., Vincent, J. L., Kelly, C., Lohmann, G., Uddin, L. Q., Biswal, B. B., Villringer, A., Castellanos, F. X., Milham, M. P., & Petrides, M. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0905314106 · Cited by 965 · cited 2×
“For example, from graph analysis of fMRI datasets we have learned that the human brain is organized with small world topology [6] and that the posterior cingulate and insular cortices are connectivity hubs [7–9].”
BackgroundWeight-conserving characterization of complex functional brain networks
Rubinov, M., & Sporns, O. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.03.069 · Cited by 903
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
Age-related changes in modular organization of human brain functional networks
Meunier, D., Achard, S., Morcom, A., & Bullmore, E. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2008.09.062 · Cited by 756
Global and local fMRI signals driven by neurons defined optogenetically by type and wiring
Lee, J. H., Durand, R., Gradinaru, V., Zhang, F., Goshen, I., Kim, D., Fenno, L. E., Ramakrishnan, C., & Deisseroth, K. A. (2010) · Nature · doi:10.1038/nature09108 · Cited by 726
Resting-state networks in the infant brain
Fransson, P., Skiöld, B., Horsch, S., Nordell, A., Blennow, M., Lagercrantz, H., & Åden, U. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0704380104 · Cited by 696
Hierarchical modularity in human brain functional networks
David Meunier, A. (2009) · Frontiers in Neuroinformatics · doi:10.3389/neuro.11.037.2009 · Cited by 689
Uncovering Intrinsic Modular Organization of Spontaneous Brain Activity in Humans
Yong He, A., Wang, J., Wang, L. Y., Chen, Z. J., Yan, C., Yang, H., Tang, H., Zhu, C., Gong, Q., Zang, Y., et al. (2009) · PLoS ONE · doi:10.1371/journal.pone.0005226 · Cited by 635
Graph-based network analysis of resting-state functional MRI
Wang, J. (2010) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2010.00016 · Cited by 614
Gao, W., Zhu, H., Giovanello, K. S., Smith, J. K., Shen, D., Gilmore, J. H., & Lin, W. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0811221106 · Cited by 601
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
Fair, D. A., Nigg, J. T., Iyer, S., Bathula, D., Mills, K. L., Dosenbach, N. U. F., Schlaggar, B. L., Mennes, M., Gutman, D., Bangaru, S., et al. (2013) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2012.00080 · Cited by 463
Topological organization of the human brain functional connectome across the lifespan
Cao, M., Wang, J.-H., Dai, Z.-J., Cao, X.-Y., Jiang, L.-L., Fan, F.-M., Song, X.-W., Xia, M.-R., Shu, N., Dong, Q., et al. (2014) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2013.11.004 · Cited by 440
Undirected graphs of frequency-dependent functional connectivity in whole brain networks
Salvador, R., Suckling, J., Schwarzbauer, C., & Bullmore, E. (2005) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2005.1645 · Cited by 437
Normalized Cut Group Clustering of Resting-State fMRI Data
van den Heuvel, M. P., Mandl, R. C. W., & Pol, H. E. H. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002001 · Cited by 418
Altered functional and structural brain network organization in autism
Rudie, J. D., Brown, J. A., Beck-Pancer, D., Hernandez, L. M., Dennis, E. L., Thompson, P. M., Bookheimer, S. Y., & Dapretto, M. (2013) · NeuroImage: Clinical · doi:10.1016/j.nicl.2012.11.006 · Cited by 411
Self-citationHampson, M., Driesen, N. R., Roth, J. K., Gore, J. C., & Constable, R. T. (2010) · Magnetic Resonance Imaging · doi:10.1016/j.mri.2010.03.021 · Cited by 363
Wilde, J. P. D., Rivers, A. W., & Price, D. L. (2004) · Progress in Biophysics and Molecular Biology · doi:10.1016/j.pbiomolbio.2004.08.010 · Cited by 351
Serag, A., Aljabar, P., Ball, G., Counsell, S. J., Boardman, J. P., Rutherford, M., Edwards, A. D., Hajnal, J. V., & Rueckert, D. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.09.062 · Cited by 316
Johnston, J. M., Vaishnavi, S. N., Smyth, M. D., Zhang, D., He, B. J., Zempel, J. M., Shimony, J. S., Snyder, A. Z., & Raichle, M. E. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0573-08.2008 · Cited by 296
Functional maturation of the executive system during adolescence
Satterthwaite, T. D., Wolf, D. H., Erus, G., Ruparel, K., Elliott, M. A., Gennatas, E. D., Hopson, R., Jackson, C., Prabhakaran, K., Bilker, W. B., et al. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.2345-13.2013 · Cited by 276
Changes in the interaction of resting-state neural networks from adolescence to adulthood
Stevens, M. C., Pearlson, G. D., & Calhoun, V. D. (2009) · Human Brain Mapping · doi:10.1002/hbm.20673 · Cited by 256
Satterthwaite, T. D., Wolf, D. H., Ruparel, K., Erus, G., Elliott, M. A., Eickhoff, S. B., Gennatas, E. D., Jackson, C., Prabhakaran, K., Smith, A., et al. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2013.06.045 · Cited by 253
Fransson, P., Skiöld, B., Engström, M., Hallberg, B., Mosskin, M., Ådén, U., Lagercrantz, H., & Blennow, M. (2009) · Pediatric Research · doi:10.1203/pdr.0b013e3181b1bd84 · Cited by 248
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
Self-citationDevelopment of Human Brain Structural Networks Through Infancy and Childhood
Huang, H., Shu, N., Mishra, V., Jeon, T., Chalak, L., Wang, Z. J., Rollins, N., Gong, G., Cheng, H., Peng, Y., et al. (2015) · Cerebral Cortex · doi:10.1093/cercor/bht335 · Cited by 223
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
Functional immaturity of cortico-basal ganglia networks in Gilles de la Tourette syndrome
Worbe, Y., Malherbe, C., Hartmann, A., Pélégrini‐Issac, M., Messé, A., Vidailhet, M., Lehéricy, S., & Benali, H. (2012) · Brain · doi:10.1093/brain/aws056 · Cited by 198
Resting-state fMRI can reliably map neural networks in children
Thomason, M. E., Dennis, E. L., Joshi, A. A., Joshi, S. H., Dinov, I. D., Chang, C., Henry, M. L., Johnson, R. F., Thompson, P. M., Toga, A. W., et al. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.11.080 · Cited by 170
Self-citationDefault-mode function and task-induced deactivation have overlapping brain substrates in children
Thomason, M. E., Chang, C. E., Glover, G. H., Gabrieli, J. D. E., Greicius, M. D., & Gotlib, I. H. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.03.029 · Cited by 142
Self-citationWatching 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
Ongoing physiological processes in the cerebral cortex
Leopold, D. A., & Maier, A. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2011.10.059 · Cited by 127
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
Modeling Structure-Function Relationships in Synthetic DNA Sequences using Attribute Grammars
Cai, Y., Lux, M. W., Adam, L., & Peccoud, J. (2009) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000529 · Cited by 52
Large-scale Cortical Network Properties Predict Future Sound-to-Word Learning Success
Sheppard, J. P., Wang, J., & Wong, P. C. M. (2012) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_00210 · Cited by 44
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Welsh, R. C., Nemec, U., & Thomason, M. E. (2011) · Topics in Magnetic Resonance Imaging · doi:10.1097/rmr.0b013e318267f932 · Cited by 27
Self-citationUsing Multiparametric Data with Missing Features for Learning Patterns of Pathology
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Metadata
- 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
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2014-05-01
- Volume
- 9
- Issue
- 5
- Pages
- e94423
- ISSN
- 1932-6203 (ISSN-L)
- 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
- 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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