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Uncovering Intrinsic Modular Organization of Spontaneous Brain Activity in Humans
Open accessAbstract
The characterization of topological architecture of complex brain networks is one of the most challenging issues in neuroscience. Slow (<0.1 Hz), spontaneous fluctuations of the blood oxygen level dependent (BOLD) signal in functional magnetic resonance imaging are thought to be potentially important for the reflection of spontaneous neuronal activity. Many studies have shown that these fluctuations are highly coherent within anatomically or functionally linked areas of the brain. However, the underlying topological mechanisms responsible for these coherent intrinsic or spontaneous fluctuations are still poorly understood. Here, we apply modern network analysis techniques to investigate how spontaneous neuronal activities in the human brain derived from the resting-state BOLD signals are topologically organized at both the temporal and spatial scales. We first show that the spontaneous brain functional networks have an intrinsically cohesive modular structure in which the connections between regions are much denser within modules than between them. These identified modules are found to be closely associated with several well known functionally interconnected subsystems such as the somatosensory/motor, auditory, attention, visual, subcortical, and the "default" system. Specifically, we demonstrate that the module-specific topological features can not be captured by means of computing the corresponding global network parameters, suggesting a unique organization within each module. Finally, we identify several pivotal network connectors and paths (predominantly associated with the association and limbic/paralimbic cortex regions) that are vital for the global coordination of information flow over the whole network, and we find that their lesions (deletions) critically affect the stability and robustness of the brain functional system. Together, our results demonstrate the highly organized modular architecture and associated topological properties in the temporal and spatial brain functional networks of the human brain that underlie spontaneous neuronal dynamics, which provides important implications for our understanding of how intrinsically coherent spontaneous brain activity has evolved into an optimal neuronal architecture to support global computation and information integration in the absence of specific stimuli or behaviors.
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Cites
Emergence of Scaling in Random Networks
Barabási, A.-L., & Albert, R. (1999) · Science · doi:10.1126/science.286.5439.509 · Cited by 36,135
Finding and evaluating community structure in networks
Newman, M. E. J., & Girvan, M. (2004) · Physical Review E · doi:10.1103/physreve.69.026113 · Cited by 13,931
Control of goal-directed and stimulus-driven attention in the brain
Corbetta, M., & Shulman, G. L. (2002) · Nature Reviews Neuroscience · doi:10.1038/nrn755 · Cited by 12,881
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
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
The Brain's Default Network: Anatomy, Function, and Relevance to Disease
Buckner, R. L., Andrews‐Hanna, J. R., & Schacter, D. L. (2008) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1440.011 · Cited by 9,761
Error and attack tolerance of complex networks
Albert, R., Jeong, H., & Barabási, A.-L. (2000) · Nature · doi:10.1038/35019019 · Cited by 7,534
Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging
Fox, M. D., & Raichle, M. E. (2007) · Nature Reviews Neuroscience · doi:10.1038/nrn2201 · Cited by 6,700
Functional connectivity in the resting brain: a network analysis of the default mode hypothesis
Greicius, M. D., Krasnow, B., Reiss, A. L., & Menon, V. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0135058100 · Cited by 6,358
(2023) · doi:10.1126/science · Cited by 6,063
Consistent resting-state networks across healthy subjects
Damoiseaux, J. S., Rombouts, S. A. R. B., Barkhof, F., Scheltens, P., Stam, C. J., Smith, S. M., & Beckmann, C. F. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0601417103 · Cited by 4,326
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 cartography of complex metabolic networks
Guimerà, R., & Nunes Amaral, L. A. (2005) · Nature · doi:10.1038/nature03288 · Cited by 3,983
Investigations into resting-state connectivity using independent component analysis
Beckmann, C. F., DeLuca, M., Devlin, J. T., & Smith, S. M. (2005) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2005.1634 · Cited by 3,398
The Human Connectome: A Structural Description of the Human Brain
Sporns, O., Tononi, G., & Kötter, R. (2005) · PLoS Computational Biology · doi:10.1371/journal.pcbi.0010042 · Cited by 3,260
Mesulam, M. (1998) · Brain · doi:10.1093/brain/121.6.1013 · Cited by 3,072
Regional homogeneity approach to fMRI data analysis.
Zang, Y., Jiang, T., Lu, Y., He, Y., & Tian, L. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2003.12.030 · Cited by 2,614
Self-citationEfficiency 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
Murphy, K., Birn, R. M., Handwerker, D. A., Jones, T. B., & Bandettini, P. A. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2008.09.036 · Cited by 2,387
Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging
Behrens, T. E. J., Johansen-Berg, H., Woolrich, M. W., Smith, S. M., Wheeler-Kingshott, C. A. M., Boulby, P. A., Barker, G. J., Sillery, E. L., Sheehan, K., Ciccarelli, O., et al. (2003) · Nature Neuroscience · doi:10.1038/nn1075 · Cited by 2,330
Spontaneous neuronal activity distinguishes human dorsal and ventral attention systems
Fox, M. D., Corbetta, M., Snyder, A. Z., Vincent, J. L., & Raichle, M. E. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0604187103 · Cited by 2,101
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
Raichle, M. E., & Mintun, M. A. (2006) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.29.051605.112819 · Cited by 1,630
Reduced resting-state brain activity in the “default network” in normal aging
Damoiseaux, J. S., Beckmann, C. F., Arigita, E. J. S., Barkhof, F., Scheltens, P., Stam, C. J., Smith, S. M., & Rombouts, S. A. R. B. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhm207 · Cited by 1,187
He, Y., Chen, Z., & Evans, A. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.0141-08.2008 · Cited by 965
Self-citationMapping Human Whole-Brain Structural Networks with Diffusion MRI
Hagmann, P., Kurant, M., Gigandet, X., Thiran, P., Wedeen, V. J., Meuli, R., & Thiran, J.-P. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000597 · Cited by 788
Detection of functional connectivity using temporal correlations in MR images
Hampson, M., Peterson, B. S., Skudlarski, P., Gatenby, J. C., & Gore, J. C. (2002) · Human Brain Mapping · doi:10.1002/hbm.10022 · Cited by 699
Analysis of a large fMRI cohort: statistical and methodological issues for group analyses
Thirion, B., Pinel, P., Mériaux, S., Roche, A., Dehaene, S., & Poline, J.-B. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2006.11.054 · Cited by 563
Studying the human brain anatomical network via diffusion-weighted MRI and graph theory
Iturria-Medina, Y., Sotero, R. C., Canales-Rodríguez, E. J., Alemán-Gómez, Y., & Melie-García, L. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2007.10.060 · Cited by 506
Motifs, modules and games in bacteria
Wolf, D. M., & Arkin, A. P. (2003) · Current Opinion in Microbiology · doi:10.1016/s1369-5274(03)00033-x · Cited by 303
Simulation of robustness against lesions of cortical networks
Kaiser, M., Martin, R., Andras, P., & Young, M. P. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05574.x · Cited by 244
Research works printed but not linked: 52
- Y He, 2007, Regional coherence changes in the early stages of Alzheimer's disease: a combined structural and resting-state functional MRI study., Neuroimage, 35, 488, 10.1016/j.neuroimage.2006.11.042 · DOI · Paper page
- AM Wink, 2006, Age and cholinergic effects on hemodynamics and functional coherence of human hippocampus., Neurobiology of Aging, 27, 1395, 10.1016/j.neurobiolaging.2005.08.011 · DOI
- KJ Friston, 1993, Functional connectivity: the principal-component analysis of large (PET) data sets., J Cereb Blood Flow Metab, 13, 5, 10.1038/jcbfm.1993.4 · DOI · Paper page
- T Jiang, 2004, Modulation of functional connectivity during the resting state and the motor task., Hum Brain Mapp, 22, 63, 10.1002/hbm.20012 · DOI
- MJ Lowe, 1998, Functional connectivity in single and multislice echoplanar imaging using resting-state fluctuations., Neuroimage, 7, 119, 10.1006/nimg.1997.0315 · DOI · Paper page
- D Cordes, 2001, Frequencies Contributing to Functional Connectivity in the Cerebral Cortex in “Resting-state” Data., AJNR Am J Neuroradiol, 22, 1326
- MD Fox, 2005, The human brain is intrinsically organized into dynamic, anticorrelated functional networks., Proc Natl Acad Sci U S A, 102, 9673, 10.1073/pnas.0504136102 · DOI · Paper page
- R Salvador, 2005, Neurophysiological architecture of functional magnetic resonance images of human brain., Cereb Cortex, 15, 1332, 10.1093/cercor/bhi016 · DOI · Paper page
- V Kiviniemi, 2003, Independent component analysis of nondeterministic fMRI signal sources., Neuroimage, 19, 253, 10.1016/S1053-8119(03)00097-1 · DOI · Paper page
- M De Luca, 2006, fMRI resting state networks define distinct modes of long-distance interactions in the human brain., NeuroImage, 29, 1359, 10.1016/j.neuroimage.2005.08.035 · DOI · Paper page
- SH Strogatz, 2001, Exploring complex networks., Nature, 410, 268, 10.1038/35065725 · DOI · Paper page
- S Boccaletti, 2006, Complex networks: structure and dynamics., Phys Reports, 175, 10.1016/j.physrep.2005.10.009 · DOI · Paper page
- S Achard, 2006, A resilient, low-frequency, small-world human brain functional network with highly connected association cortical hubs., J Neurosci, 26, 63, 10.1523/JNEUROSCI.3874-05.2006 · DOI · Paper page
- J Wang, 2008, Parcellation-dependent small-world brain functional networks: A resting-state fMRI study., Hum Brain Mapp
- Y Liu, 2008, Disrupted small-world networks in schizophrenia., Brain, 131, 945, 10.1093/brain/awn018 · DOI · Paper page
- L Wang, 2008, Altered small-world brain functional networks in children with attention-deficit/hyperactivity disorder., Hum Brain Mapp
- Y He, 2007, Small-world anatomical networks in the human brain revealed by cortical thickness from MRI., Cereb Cortex, 17, 2407, 10.1093/cercor/bhl149 · DOI · Paper page
- G Gong, 2008, Mapping Anatomical Connectivity Patterns of Human Cerebral Cortex Using In Vivo Diffusion Tensor Imaging Tractography., Cereb Cortex
- R Guimera, 2005, The worldwide air transportation network: Anomalous centrality, community structure, and cities' global roles., Proc Natl Acad Sci U S A, 102, 7794, 10.1073/pnas.0407994102 · DOI · Paper page
- JD Han, 2004, Evidence for dynamically organized modularity in the yeast protein-protein interaction network., Nature, 430, 88, 10.1038/nature02555 · DOI · Paper page
- LH Hartwell, 1999, From molecular to modular cell biology., Nature, 402, C47, 10.1038/35011540 · DOI · Paper page
- JW Scannell, 1999, The connectional organization of the cortico-thalamic system of the cat., Cereb Cortex, 9, 277, 10.1093/cercor/9.3.277 · DOI · Paper page
- C Zhou, 2006, Hierarchical organization unveiled by functional connectivity in complex brain networks., Phys Rev Lett, 97, 238103, 10.1103/PhysRevLett.97.238103 · DOI · Paper page
- ZJ Chen, 2008, Revealing Modular Architecture of Human Brain Structural Networks by Using Cortical Thickness from MRI., Cereb Cortex
- AJ Schwarz, 2008, Community structure and modularity in networks of correlated brain activity., Magn Reson Imaging, 26, 914, 10.1016/j.mri.2008.01.048 · DOI
- L Ferrarini, 2008, Hierarchical functional modularity in the resting-state human brain., Hum Brain Mapp
- D Meunier, 2009, Age-related changes in modular organization of human brain functional networks., Neuroimage, 44, 715, 10.1016/j.neuroimage.2008.09.062 · DOI · Paper page
- N Tzourio-Mazoyer, 2002, Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain., Neuroimage, 15, 273, 10.1006/nimg.2001.0978 · DOI · Paper page
- R Guimera, 2005, Cartography of complex networks: modules and universal roles., J Stat Mech Theor Exp, P02001
- R Guimera, 2004, Modularity from fluctuations in random graphs and complex networks., Phys Rev E Stat Nonlin Soft Matter Phys, 70, 025101, 10.1103/PhysRevE.70.025101 · DOI · Paper page
- P Fransson, 2005, Spontaneous low-frequency BOLD signal fluctuations: an fMRI investigation of the resting-state default mode of brain function hypothesis., Hum Brain Mapp, 26, 15, 10.1002/hbm.20113 · DOI · Paper page
- CJ Stam, 2007, Small-world networks and functional connectivity in Alzheimer's disease., Cereb Cortex, 17, 92, 10.1093/cercor/bhj127 · DOI · Paper page
- DJ Watts, 1998, Collective dynamics of ‘small-world’ networks., Nature, 393, 440, 10.1038/30918 · DOI · Paper page
- V Latora, 2001, Efficient behavior of small-world networks., Phys Rev Lett, 87, 198701, 10.1103/PhysRevLett.87.198701 · DOI · Paper page
- R Guimera, 2007, Classes of complex networks defined by role-to-role connectivity profiles., Nat Phys, 3, 63, 10.1038/nphys489 · DOI · Paper page
- LC Freeman, 1977, A set of measures of centrality based upon betweenness., Sociometry, 35, 10.2307/3033543 · DOI · Paper page
- M Kaiser, 2004, Edge vulnerability in neural and metabolic networks., Biol Cybern, 90, 311, 10.1007/s00422-004-0479-1 · DOI
- JA Bullinaria, 2007, Understanding the emergence of modularity in neural systems., Cognitive Science, 31, 673, 10.1080/15326900701399939 · DOI
- O Sporns, 2000, Theoretical neuroanatomy: relating anatomical and functional connectivity in graphs and cortical connection matrices., Cereb Cortex, 10, 127, 10.1093/cercor/10.2.127 · DOI · Paper page
- R Kotter, 2003, Network participation indices: characterizing component roles for information processing in neural networks., Neural Netw, 16, 1261, 10.1016/j.neunet.2003.06.002 · DOI
- O Sporns, 2007, Identification and classification of hubs in brain networks., PLoS ONE, 2, e1049, 10.1371/journal.pone.0001049 · DOI · Paper page
- HB Fraser, 2005, Modularity and evolutionary constraint on proteins., Nat Genet, 37, 351, 10.1038/ng1530 · DOI
- V Spirin, 2006, A metabolic network in the evolutionary context: multiscale structure and modularity., Proc Natl Acad Sci U S A, 103, 8774, 10.1073/pnas.0510258103 · DOI
- A Hintze, 2008, Evolution of complex modular biological networks., PLoS Comput Biol, 4, e23, 10.1371/journal.pcbi.0040023 · DOI
- CJ Honey, 2007, Network structure of cerebral cortex shapes functional connectivity on multiple time scales., Proc Natl Acad Sci U S A, 104, 10240, 10.1073/pnas.0701519104 · DOI · Paper page
- R Salvador, 2005, Undirected graphs of frequency-dependent functional connectivity in whole brain networks., Philos Trans R Soc Lond B Biol Sci, 360, 937, 10.1098/rstb.2005.1645 · DOI · Paper page
- MX Cohen, 2008, Covariance-based subdivision of the human striatum using T1-weighted MRI., Eur J Neurosci, 27, 1534, 10.1111/j.1460-9568.2008.06117.x · DOI
- AL Cohen, 2008, Defining functional areas in individual human brains using resting functional connectivity MRI., Neuroimage, 41, 45, 10.1016/j.neuroimage.2008.01.066 · DOI · Paper page
- KE Stephan, 2003, Lateralized cognitive processes and lateralized task control in the human brain., Science, 301, 384, 10.1126/science.1086025 · DOI · Paper page
- RM Birn, 2006, Separating respiratory-variation-related fluctuations from neuronal-activity-related fluctuations in fMRI., Neuroimage, 31, 1536, 10.1016/j.neuroimage.2006.02.048 · DOI · Paper page
- LD-G Danon, 2005, Comparing community structure identification., J Stat mech Theor Exp, P09008
- DC Van Essen, 2005, A Population-Average, Landmark- and Surface-based (PALS) atlas of human cerebral cortex., Neuroimage, 28, 635, 10.1016/j.neuroimage.2005.06.058 · DOI · Paper page
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Metadata
- Authors
- He, Y., Wang, J., Wang, L., Chen, Z. J., Yan, C., Yang, H., Tang, H., Zhu, C., Gong, Q., Zang, Y., & Evans, A. C.
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2009-04-21
- Volume
- 4
- Issue
- 4
- Pages
- e5226
- ISSN
- 1932-6203 (ISSN-L)
- OpenAlex
- W2028645759
- Cited by
- 630
- References
- 31
- FWCI
- 19.03
- Type
- journal article
- Language
- en
- Open access
- gold
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