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Functionally linked resting‐state networks reflect the underlying structural connectivity architecture of the human brain
Open accessAbstract
During rest, multiple cortical brain regions are functionally linked forming resting‐state networks. This high level of functional connectivity within resting‐state networks suggests the existence of direct neuroanatomical connections between these functionally linked brain regions to facilitate the ongoing interregional neuronal communication. White matter tracts are the structural highways of our brain, enabling information to travel quickly from one brain region to another region. In this study, we examined both the functional and structural connections of the human brain in a group of 26 healthy subjects, combining 3 Tesla resting‐state functional magnetic resonance imaging time‐series with diffusion tensor imaging scans. Nine consistently found functionally linked resting‐state networks were retrieved from the resting‐state data. The diffusion tensor imaging scans were used to reconstruct the white matter pathways between the functionally linked brain areas of these resting‐state networks. Our results show that well‐known anatomical white matter tracts interconnect at least eight of the nine commonly found resting‐state networks, including the default mode network, the core network, primary motor and visual network, and two lateralized parietal‐frontal networks. Our results suggest that the functionally linked resting‐state networks reflect the underlying structural connectivity architecture of the human brain. Hum Brain Mapp 2009. © 2009 Wiley‐Liss, Inc.
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“Anterior and posterior callosal fibres and fibres such as the inferior-fronto-occipital fasciculus provide major connections within the anterior and posterior components of the default mode network regions (van den Heuvel et al., 2009)”
From White matter diffusion alterations precede symptom onset in autosomal dominant Alzheimer’s disease (2018) · cites this paper as van den Heuvel et al., 2009
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“The AIC and ACC are known to be functionally (Taylor et al., 2009) and structurally (van den Heuvel et al., 2009) connected.”
From An Interoceptive Predictive Coding Model of Conscious Presence (2012) · cites this paper as van den Heuvel et al., 2009
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“higher FA has been associated with better functional connectivity between anatomically distant gray matter regions using resting-state fMRI (functional MRI) 35,47,48”
From Physical exercise keeps the brain connected: biking increases white matter integrity in patients with schizophrenia and healthy controls. (2015) · cites this paper as [47]
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“The AIC and ACC are known to be functionally (Taylor et al., 2009) and structurally (van den Heuvel et al., 2009) connected.”
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BackgroundLinking Structure and Function in Macroscale Brain Networks
Suárez, L. E., Markello, R. D., Betzel, R. F., & Mišić, B. (2020) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2020.01.008 · Cited by 769
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Self-citationGlobal Connectivity of Prefrontal Cortex Predicts Cognitive Control and Intelligence
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Network dysfunction after traumatic brain injury
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Self-citationFunctional connectivity density mapping
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“Moreover, the overall resting functional connectivity (short- and long-range interconnections) of the gray matter (4-mm isotropic spatial resolution) was shown to correspond well with the structural connections determined with diffusion tensor imaging (DTI) (15) and to be associated with intellectual performance (16).”
BackgroundCan structure predict function in the human brain?
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“Note the presence of dense pathways between the medial frontal cortex and the PCC as well as lateral parietal cortex, as well as the relative absence of connections between the lateral parietal cortex and the precuneus (see also Van den Heuvel et al., 2009a).”
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BackgroundStructural foundations of resting-state and task-based functional connectivity in the human brain
Hermundstad, A. M., Bassett, D. S., Brown, K., Aminoff, E., Clewett, D., Freeman, S., Frithsen, A., Johnson, A., Tipper, C. M., Miller, M. B., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1219562110 · Cited by 580
The modular and integrative functional architecture of the human brain
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“Both FA and fiber density have been used previously to quantify structural connectivity, particularly to characterize white matter integrity (Hagmann et al., 2008; van den Heuvel et al., 2008).”
BackgroundMethodResultA cross-disorder connectome landscape of brain dysconnectivity
van den Heuvel, M. P., & Sporns, O. (2019) · Nature Reviews Neuroscience · doi:10.1038/s41583-019-0177-6 · Cited by 462
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Madden, D. J., Bennett, I. J., Burzynska, A. Z., Potter, G. G., Chen, N., & Song, A. W. (2011) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2011.08.003 · Cited by 510
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BackgroundThe human connectome: Origins and challenges
Sporns, O. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2013.03.023 · Cited by 449
“Other studies (e.g. Greicius et al., 2009; Hagmann et al., 2010; Skudlarski et al., 2008; van den Heuvel et al., 2009), including some in nonhuman primates (Adachi et al., 2012), have confirmed a robust, albeit complex, relationship between structural connections and spontaneous dynamic…”
BackgroundSmall-world human brain networks: Perspectives and challenges
Liao, X., Vasilakos, A. V., & Yong He, A. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.03.018 · Cited by 443
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“ICNs are large-scale networks identified by connectivity methods that are associated with characteristic functions (17,18), are stable across tasks (19,20) and over time (21,22), correspond to anatomical white matter tracts (23), and demonstrate direct behavioral correlates (24Y26).”
Developmental pathways to amygdala–prefrontal function and internalizing symptoms in adolescence
Burghy, C. A., Stodola, D. E., Ruttle, P. L., Molloy, E. K., Armstrong, J. M., Oler, J. A., Fox, M. E., Hayes, A. S., Kalin, N. H., Essex, M. J., et al. (2012) · Nature Neuroscience · doi:10.1038/nn.3257 · Cited by 397
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“…subjects' aptitude for different cognitive tasks (Baldassarre et al., 2012; Hampson et al., 2006; Koyama et al., 2011; Seeley et al., 2007; van den Heuvel et al., 2009b; Zhu et al., 2011), facilitate refinement of neuro-anatomical models (Dosenbach and Fair, 2007; Fox et al., 2006a), and account…”
BackgroundMethodExploring the network dynamics underlying brain activity during rest
Cabral, J., Kringelbach, M. L., & Deco, G. (2014) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2013.12.005 · Cited by 351
“In van den Heuvel et al. (2009b), functional network properties were explored at the voxel scale (64 mm3), resulting in graphs with 9500 nodes.”
BackgroundMethodDisrupted Functional Brain Connectome in Individuals at Risk for Alzheimer's Disease
Wang, J., Zuo, X., Dai, Z., Xia, M., Zhao, Z., Zhao, X., Jia, J., Han, Y., & He, Y. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.03.026 · Cited by 432
Resting-State Functional MR Imaging: A New Window to the Brain
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Rich-club organization of the newborn human brain
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Cai, W., Ryali, S., Chen, T., Li, C.-S. R., & Menon, V. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.3048-14.2014 · Cited by 362
“Consistent with previous resting-state fMRI (Seeley et al., 2007; Sridharan et al., 2008; Smith et al., 2009) and structural connectivity (van den Heuvel et al., 2009; Allman et al., 2010) studies, we found that the rAI has stronger intrinsic functional connectivity with the ACC.”
ResultInjured Brains and Adaptive Networks: The Benefits and Costs of Hyperconnectivity
Hillary, F. G., & Grafman, J. H. (2017) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2017.03.003 · Cited by 388
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“This approach allows for a direct comparison with the Structural Connectome defined over the same parcellation scheme (van den Heuvel et al., 2009) and has been particularly useful for the optimization and validation of resting-state models through the comparison with the simulated FC matrix (Honey…”
MethodMennes, M., Kelly, C. A. M., Zuo, X., Martino, A. D., Biswal, B. B., Castellanos, F. X., & Milham, M. P. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.01.002 · Cited by 368
“Still, given that our understanding of structure/function relationships in resting-state fMRI is only just emerging, this issue merits further examination (Greicius et al., 2009; Hagmann et al., 2008; Honey et al., 2009; Skudlarski et al., 2008; van den Heuvel et al., 2009).”
Backgroundvan 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
Network neuroscience theory of human intelligence
Barbey, A. K. (2018) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2017.10.001 · Cited by 355
Uddin, L. Q. (2010) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2010.00021 · Cited by 343
“More importantly, patterns of resting-state correlations are thought to refl ect functional architecture of the brain (Hagmann et al., 2008; Margulies et al., 2009; van den Heuvel et al., 2009).”
Noninvasive Functional and Structural Connectivity Mapping of the Human Thalamocortical System
Zhang, D., Snyder, A. Z., Shimony, J. S., Fox, M., & Raichle, M. E. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp182 · Cited by 351
Petrides, M., Tomaiuolo, F., Yeterian, E. H., & Pandya, D. Ν. (2011) · Cortex · doi:10.1016/j.cortex.2011.07.002 · Cited by 353
“…brain with probabilistic DTI tractography (e.g., Behrens et al., 2007) or functional connectivity analysis (e.g., Margulies et al., 2009; van den Heuvel et al., 2009), these must be interpreted with caution and in the context of the experimentally studied pathways in themacaquemonkey (Berlucchi…”
BackgroundDefault mode network abnormalities in mesial temporal lobe epilepsy: A study combining fMRI and DTI
Liao, W., Zhang, Z., Pan, Z., Mantini, D., Ding, J., Duan, X., Luo, C., Wang, Z., Tan, Q., Lu, G., et al. (2010) · Human Brain Mapping · doi:10.1002/hbm.21076 · Cited by 330
“Previous r 892 r studies also suggested that resting state functional connectivity reflects the underlying structural connectivity architecture [Greicius et al., 2009; Honey et al., 2009; van den Heuvel et al., 2008, 2009].”
BackgroundMethodResultInfluentialThe Dynamical Balance of the Brain at Rest
Deco, G., & Corbetta, M. (2010) · The Neuroscientist · doi:10.1177/1073858409354384 · Cited by 323
Anterior insula as a gatekeeper of executive control
Molnar-Szakacs, I., & Uddin, L. Q. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104736 · Cited by 333
Raznahan, A., Lerch, J. P., Lee, N., Greenstein, D. K., Wallace, G. L., Stockman, M., CLASEN, L. S., Shaw, P. W., & Giedd, J. N. (2011) · Neuron · doi:10.1016/j.neuron.2011.09.028 · Cited by 304
Hagen, E. V. D., Stoyanova, R. S., Baron‐Cohen, S., & Calder, A. J. (2012) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nss053 · Cited by 315
“One study (van den Heuvel et al., 2009) also found that well-described white matter tracts link brain areas within several of the common resting state networks, suggesting that the regions in these networks are also structurally connected.”
BackgroundThe Corticocortical Structural Connectivity of the Human Insula
Ghaziri, J., Tucholka, A., Girard, G., Houde, J., Boucher, O., Gilbert, G., Descoteaux, M., Lippé, S., Rainville, P., & Nguyen, D. K. (2015) · Cerebral Cortex · doi:10.1093/cercor/bhv308 · Cited by 328
The Default Mode Network in Healthy Aging and Alzheimer′s Disease
Mevel, K., Chételat, G., Eustache, F., & Desgranges, B. (2011) · International Journal of Alzheimer’s Disease · doi:10.4061/2011/535816 · Cited by 302
“In these conditions, deactivations intensity depends on attention load so that a cognitive task requiring low attention levels will induce weak deactivations, while greater deactivations will be associated with tasks requiring high attention levels.”
BackgroundGuye, M., Bettus, G., Bartoloméi, F., & Cozzone, P. J. (2010) · Magnetic Resonance Materials in Physics Biology and Medicine · doi:10.1007/s10334-010-0205-z · Cited by 314
“tivity measured by MRI ([11–19]; [5] for review).”
BackgroundMethodThe parcellation-based connectome: limitations and extensions
de Reus, M. A., & van den Heuvel, M. P. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2013.03.053 · Cited by 282
“…al., 2005; van den Heuvel et al., 2009a), short communication relays (Hagmann et al., 2007; Kaiser and Hilgetag, 2006; Sporns and Zwi, 2004; van den Heuvel et al., 2009b, 2012; Varshney et al., 2011) and the formation of a small set of densely connected and centrally placed hub nodes, playing a…”
BackgroundMethodInfluentialHerbet, G., & Duffau, H. (2020) · Physiological Reviews · doi:10.1152/physrev.00033.2019 · Cited by 321
Use of fNIRS to assess resting state functional connectivity
Lu, C., Zhang, Y.-J., Biswal, B. B., Zang, Y., Peng, D.-L., & Zhu, C.-Z. (2009) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2009.11.010 · Cited by 301
The (in)stability of functional brain network measures across thresholds
Garrison, K. A., Scheinost, D., Finn, E. S., Shen, X., & Constable, R. T. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2015.05.046 · Cited by 305
“In attempts to show that results are not sensitive to the choice of threshold, findings are often reported across a narrow range of thresholds (e.g., Cole et al., 2013, top 2-10%; van den Heuvel et al., 2009a, r=0.3-0.5).”
InfluentialNetwork-Level Structure-Function Relationships in Human Neocortex
Mišić, B., Betzel, R. F., de Reus, M. A., van den Heuvel, M. P., Berman, M. G., McIntosh, A. R., & Sporns, O. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhw089 · Cited by 293
Cerliani, L., Thomas, R. M., Jbabdi, S., Siero, J. C. W., Nanetti, L., Crippa, A., Gazzola, V., D'Arceuil, H. E., & Keysers, C. (2011) · Human Brain Mapping · doi:10.1002/hbm.21338 · Cited by 299
“…young [Rose, 1928], Craig [2010] proposed that large interindividual structural differences might be observed in the TG, and various dissection studies indeed reported considerable morphological variability in this region [Naidich et al., 2004; Ture et al., 1999; Varnavas and Grand, 1999].”
BackgroundHam, T., Leff, A., de Boissezon, X., Joffe, A., & Sharp, D. J. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.4692-12.2013 · Cited by 271
“Tractography evidence shows that the region has direct white matter connections to other key regions within these networks, including the dACC (van den Heuvel et al., 2009), the temporoparietal junction (Kucyi et al., 2012), and the inferior parietal lobe (Uddin et al., 2010).”
BackgroundEbisch, S. J. H., Gallese, V., Willems, R. M., Mantini, D., Groen, W. B., Romani, G. L., Buitelaar, J. K., & Harold Bekkering, A. (2010) · Human Brain Mapping · doi:10.1002/hbm.21085 · Cited by 292
“Moreover, neuroimaging evidence suggested a close, eventually antagonistic, interaction between the insula network (in particular, right anterior insula) and the DMN [Sridharan et al., 2008; Uddin et al., 2008].”
Keeser, D., Padberg, F., Reisinger, E., Pogarell, O. M., Kirsch, V., Palm, U., Karch, S., Möller, H. ‐., Nitsche, M. A., & Mulert, C. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.12.004 · Cited by 287
“…tDCS. Past studies have found direct neuronal activity between the medial prefrontal cortex and the hippocampus in rodents during spatial workingmemory tasks (Jones and Wilson, 2005; Siapas et al., 2005) and there is evidence for a fronto-parietal network (Laufs, 2008; van den Heuvel et al., 2009).”
Abdelnour, F., Voss, H. U., & Raj, A. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2013.12.039 · Cited by 260
“6) are evaluated at 15% level. connectivity to the posterior cingulate cortex (van den Heuvel et al., 2008, 2009).”
BackgroundMR connectomics: Principles and challenges
Hagmann, P., Cammoun, L., Gigandet, X., Gerhard, S., Grant, P. E., Wedeen, V. J., Meuli, R. A., Thiran, J., Honey, C. J., & Sporns, O. (2010) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2010.01.014 · Cited by 276
A systematic literature review of resting state network—functional MRI in bipolar disorder
Vargas, C., López‐Jaramillo, C., & Vieta, E. (2013) · Journal of Affective Disorders · doi:10.1016/j.jad.2013.05.083 · Cited by 278
“However, defining a region of interest as a “seed voxel” introduces potential biases in evaluation and does not allow a global view of the brain connectivity the same way as the ICA analysis can do (Van den Heuvel and Pol, 2011; Van den Heuvel et al., 2009).”
BackgroundMethodThe Default Mode Network’s Role in Discrete Emotion
Satpute, A. B., & Lindquist, K. A. (2019) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2019.07.003 · Cited by 280
“Medial temporal lobe, precuneus, PCC, retrosplenial cortex, TPJ, lateral PFC, MPFC, lateral temporal lobe Integration of cognitive and emotion processing [114]”
Redefining the role of limbic areas in cortical processing
Chanes, L., & Barrett, L. F. (2016) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2015.11.005 · Cited by 259
Evolutionarily Novel Functional Networks in the Human Brain?
Mantini, D., Corbetta, M., Romani, G. L., Orban, G. A., & Vanduffel, W. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.4392-12.2013 · Cited by 259
Evidence for Functional Networks within the Human Brain's White Matter
Peer, M., Nitzan, M., Bick, A. S., Levin, N., & Arzy, S. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.3872-16.2017 · Cited by 258
“Past studies attempted to identify whitematter tracts connecting disconnected nodes of cortical networks (Damoiseaux and Greicius, 2009; Greicius et al., 2009; van den Heuvel et al., 2009).”
Calhoun, V. D., Jing Sui （Beijing Normal University）， my correct affiliation is beijing normal university, N. Q. U. O. S. A. T., Kiehl, K. A., Turner, J. A., Allen, E. A., & Pearlson, G. D. (2012) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2011.00075 · Cited by 254
“…functional data and suggest that a direct combination of structural and functional findings will prove useful (Calhoun et al., 2006; Calhoun and Adali, 2009; van den Heuvel et al., 2009; Michael et al., 2010; Segall and Calhoun, 2011; Sui and Calhoun, 2011; Wang et al., 2011; Zalesky et al., 2011).”
BackgroundDisruption of functional networks in dyslexia: a whole-brain, data-driven analysis of connectivity
Finn, E. S., Shen, X., Holahan, J. M., Scheinost, D., Lacadie, C., Papademetris, X., Shaywitz, S. E., Shaywitz, B. A., & Constable, R. T. (2014) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.08.031 · Cited by 248
Messé, A., Rudrauf, D., Benali, H., & Marrelec, G. (2014) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1003530 · Cited by 215
Metadata
- Authors
- van den Heuvel, M. P., Mandl, R. C. W., Kahn, R. S., & Hulshoff Pol, H. E.
- Affiliations
- University Medical Center Utrecht (NL)
- Venue
- Human Brain Mapping
- Publisher
- Wiley
- Published
- 2009-02-23
- Volume
- 30
- Issue
- 10
- Pages
- 3127-3141
- ISSN
- 1065-9471 (ISSN-L)
- 1097-0193
- PMC
- PMC6870902
- OpenAlex
- W2022671987
- Cited by
- 987
- References
- 84
- Citations by year
- 2026: 19 · 2025: 28 · 2024: 28 · 2023: 45 · 2022: 51 · 2021: 47 · 2020: 57 · 2019: 60 · 2018: 69 · 2017: 80 · 2016: 72 · 2015: 79 · 2014: 84 · 2013: 94 · 2012: 74
- FWCI
- 27.75
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Human Brain Mapping (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Pure Amsterdam UMC (submittedVersion)
- Amsterdam UMC (VU Amsterdam) - Institutional Repository (submittedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- 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
- resting-state networks, functional connectivity, structural connectivity, white matter tracts, default mode network, core network, visual network
- MeSH terms
- Adolescent, Adult, Brain, Brain Mapping, Female, Humans, Image Processing, Computer-Assisted, Magnetic Resonance Imaging, Male, Models, Neurological, Nerve Fibers, Myelinated, Nerve Net, Neural Pathways, Oxygen, Rest, Diffusion Magnetic Resonance Imaging, Young Adult
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