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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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“Our results are also consistent with previous diffusion imaging studies in humans showing that the fiber tracts of the cingulum, superior frontaloccipital fasciculus (comparable to the frontoparietal fasciculus tract in rats), and the corpus callosum form the major direct neuroanatomical inks among DMN regions (43).”
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“Most DMN studies show that the dorsal cingulum mediates the MPFC-PCC pathway, while the ventral cingulum supports communications between the PCC and ATL/AMG (Greicius et al., 2009; Sethi et al., 2015; van den Heuvel et al., 2009, 2008).”
Resting‐state functional connectivity MRI reveals active processes central to cognition
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“…several studies suggest that structural connections or anatomical connectivity constrains the functional coupling (Greicius et al., 2009; van den Heuvel et al., 2009) by shaping the flow of information along preferential pathways (Bressler and Menon, 2010) and promoting a balance between the…”
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“Diffusion tensor imaging demonstrated that this cortical area has direct white matter connections to other key regions, including the DACC (van den Heuvel et al., 2009), the inferior parietal lobe (Uddin et al., 2010), and the temporoparietal junction (Kucyi et al., 2012), making the insula (rAI)…”
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“…suggests that functional connectivity is constrained by the underlying structural connectivity (Greicius et al., 2009; Honey et al., 2009; van den Heuvel et al., 2009; Van Dijk et al., 2010), however dynamic changes in functional connectivity over time suggest that other complex processes also…”
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“Resting-state FC has been predominantly examined with functional magnetic resonance imaging (fMRI) as correlations between blood oxygenation level-dependent (BOLD) signals (van den Heuvel et al., 2009).”
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“These specific hub regions were found to be more densely connected among themselves than to other regions of the human connectome, suggesting a “rich-club” organization (van den Heuvel and Sporns, 2011).”
BackgroundThe Fine-Scale Functional Correlation of Striate Cortex in Sighted and Blind People
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BackgroundNeonatal brain resting-state functional connectivity imaging modalities
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“Second, the fiber tracts connecting two ROIs are not uniformly distributed within each ROI, further highlighting the effects that the individual differences in ROI definitions can have on the successful outcomes of fiber tracking (Van den Heuvel et al., 2009).”
InfluentialSex differences and menstrual cycle effects in cognitive and sensory resting state networks
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Garcés, P., Pereda, E., Hernandez-Tamames, J. A., del Pozo, F., Maestú, F., & Pineda‐Pardo, J. A. (2015) · Human Brain Mapping · doi:10.1002/hbm.22995 · Cited by 83
“The dashed line corresponds to the identity line y 5 x. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.] r 29 r resting-state fMRI networks are supported by structural connections that can be identified using DWI [van den Heuvel et al., 2009].”
BackgroundMethodBos, D. J., Oranje, B., Achterberg, M., Vlaskamp, C., Ambrosino, S., de Reus, M. A., van den Heuvel, M. P., Rombouts, S. A. R. B., & Durston, S. (2017) · Journal of Child Psychology and Psychiatry · doi:10.1111/jcpp.12712 · Cited by 84
“Furthermore, even though brain structure is thought to be highly predictive of function, there is not a one-to-one relationship between them (Honey, Thivierge, & Sporns, 2010; Honey et al., 2009; van den Heuvel, Mandl, Kahn, & Hulshoff Pol, 2009).”
Brain structural alterations are distributed following functional, anatomic and genetic connectivity
Cauda, F., Nani, A., Manuello, J., Premi, E., Palermo, S., Tatu, K., Duca, S., Fox, P. T., & Costa, T. (2018) · Brain · doi:10.1093/brain/awy252 · Cited by 77
The salience network dynamics in perceptual decision-making
Chand, G. B., & Dhamala, M. (2016) · NeuroImage · doi:10.1016/j.neuroimage.2016.04.018 · Cited by 80
“…has demonstrated that this cortical area has direct white matter connections to other key regions within these networks, including the dACC (van den Heuvel et al., 2009), the inferior parietal lobe (Uddin et al., 2010), and the temporo-parietal junction (Kucyi et al., 2012) making the insula well…”
van den Heuvel, M. P., & Pol, H. E. H. (2009) · Human Brain Mapping · doi:10.1002/hbm.20893 · Cited by 79
A Neuronal Basis for Task-Negative Responses in the Human Brain
Lin, P., Hasson, U., Jovicich, J., & Robinson, S. (2010) · Cerebral Cortex · doi:10.1093/cercor/bhq151 · Cited by 76
“It is also reflected in anatomical connections (Greicius et al. 2009; van den Heuvel et al. 2009).”
BackgroundInfluentialHippocampal‐ DMN disconnectivity in MS is related to WM lesions and depression
Rocca, M. A., Pravatà, E., Valsasina, P., Radaelli, M., Colombo, B., Vacchi, L., Gobbi, C., Comı, G., Falini, A., & Filippi, M. (2015) · Human Brain Mapping · doi:10.1002/hbm.22992 · Cited by 79
“…of afferent/efferent WM tracts connected to the hippocampus passing through WM lesions and/or the selective involvement of WM tracts which contribute to the architecture of the DMN (e.g., the cingulum, superior-fronto-occipital fasciculus, and corpus callosum) [van den Heuvel et al., 2009].”
BackgroundAn edge-centric perspective on the human connectome: link communities in the brain
de Reus, M. A., Saenger, V. M., Kahn, R. S., & van den Heuvel, M. P. (2014) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0527 · Cited by 80
Self-citationMenon, V., Gallardo, G., Pinsk, M. A., Nguyen, V.-D., Li, J., Cai, W., & Wassermann, D. (2020) · eLife · doi:10.7554/elife.53470 · Cited by 79
Ohla, K., Toepel, U., le Coutre, J., & Hudry, J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0032434 · Cited by 76
Shu, N., Duan, Y., Xia, M., Schoonheim, M. M., Huang, J., Ren, Z., Sun, Z., Ye, J., Dong, H., Shi, F., et al. (2016) · Scientific Reports · doi:10.1038/srep29383 · Cited by 80
Cerebral functional connectivity periodically (de)synchronizes with anatomical constraints
Liégeois, R., Ziegler, E., Phillips, C. L. M., Geurts, P., Gómez, F. A., Bahri, M. A., Yeo, B. T. T., Soddu, A., Vanhaudenhuyse, A., Laureys, S., et al. (2015) · Brain Structure and Function · doi:10.1007/s00429-015-1083-y · Cited by 74
“Phases of (de)synchronization between functional and structural connectivities The link between structural and functional connectivities was established a few years ago (Honey et al. 2009; van den Heuvel et al. 2009).”
BackgroundTract-specific white matter hyperintensities disrupt neural network function in Alzheimer’s disease
Taylor, A. N. W., Kambeitz-Ilankovic, L., Gesierich, B., Simon-Vermot, L., Franzmeier, N., Araque Caballero, M. Á., Müller, S., Hesheng, L., Ertl-Wagner, B., Bürger, K., et al. (2017) · Alzheimer's & Dementia · doi:10.1016/j.jalz.2016.06.2358 · Cited by 73
Connectomics and Neuroticism: An Altered Functional Network Organization
Servaas, M. N., Geerligs, L., Renken, R. J., Marsman, J.-B. C., Ormel, J., Riese, H., & Aleman, A. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.169 · Cited by 76
Briand, M., Gosseries, O., Staumont, B., Laureys, S., & Thibaut, A. (2020) · Frontiers in Neurology · doi:10.3389/fneur.2020.00933 · Cited by 79
Human fetal brain connectome: structural network development from middle fetal stage to birth
Song, L., Mishra, V., Ouyang, M., Peng, Q., Slinger, M., Liu, S., & Huang, H. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00561 · Cited by 71
Liao, W., Zhang, Z., Mantini, D., Xu, Q., Wang, Z., Chen, G., Jiao, Q., Zang, Y., & Lu, G. (2013) · Brain Connectivity · doi:10.1089/brain.2012.0132 · Cited by 72
“A similar correspondence has been also revealed between the ICN estimated by temporal activity correlations and the ACN estimated via WM tractography (Hagmann et al., 2008, 2010; Honey et al., 2009; van den Heuvel et al., 2009).”
MethodCognitive Flexibility: A Default Network and Basal Ganglia Connectivity Perspective
Vatansever, D., Manktelow, A. E., Sahakian, B. J., Menon, D. K., & Stamatakis, E. A. (2015) · Brain Connectivity · doi:10.1089/brain.2015.0388 · Cited by 77
“However, recent studies revealed extensive DMN functional and structural connectivity to the rest of the brain (van den Heuvel et al., 2009), a greater activity in a wide range of self-referential and memory-based paradigms (Andrews-Hanna et al., 2014; Buckner et al., 2008), taskinduced alterations…”
BackgroundAltered Cingulate Cortex Functional Connectivity in Normal Aging and Mild Cognitive Impairment
Cera, N., Esposito, R., Cieri, F., & Tartaro, A. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00857 · Cited by 75
Griffis, J. C., Metcalf, N. V., Corbetta, M., & Shulman, G. L. (2020) · NeuroImage · doi:10.1016/j.neuroimage.2020.116589 · Cited by 72
“The “dilate” command in DSI_studio (http://dsi-studio.labsolver.org/) was used to dilate the cortical regions by 2 mm to increase the sensitivity of subsequent region-to-region structural connectivity analyses (Van Den Heuvel et al., 2009; Wilson et al., 2011).”
MethodChaudhary, U. J., Carmichael, D. W., Rodionov, R., Thornton, R. C., Bartlett, P., Vulliémoz, S., Micallef, C., McEvoy, A. W., Diehl, B., Walker, M. C., et al. (2012) · Brain · doi:10.1093/brain/aws302 · Cited by 71
“Previous EEG–functional MRI studies with low yield (Salek-Haddadi et al., 2002; Archer et al., 2006; Auer et al., 2008; Donaire et al., 2009; Tyvaert et al., 2009; LeVan et al., 2010; Thornton et al., 2010) have largely recorded seizures for- tuitously in the course of studies aimed at mapping…”
BackgroundResultInfluentialMontag, C., Reuter, M., Weber, B., Markett, S. A., & Schoene‐Bake, J. ‐. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.05.017 · Cited by 76
“There is first evidence that functional connectivities in the resting brain are linked to anatomical connectivities (Van den Heuvel et al., 2009).”
BackgroundBrain network reconfiguration for language and domain-general cognitive control in bilinguals
Wu, J., Yang, J., Chen, M., Li, S., Zhang, Z., Kang, C., Ding, G., & Guo, T. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2019.06.022 · Cited by 72
What Does Imaging Reveal About the Pathology of Amyotrophic Lateral Sclerosis?
Turner, M. R., & Verstraete, E. (2015) · Current Neurology and Neuroscience Reports · doi:10.1007/s11910-015-0569-6 · Cited by 71
Schulz, M., Malherbe, C., Cheng, B., Thomalla, G., & Schlemm, E. (2021) · BMC Medicine · doi:10.1186/s12916-021-01962-1 · Cited by 71
Ibrahim, G. M., Morgan, B. R., Lee, W., Smith, M. L., Donner, E. J., Wang, F., Beers, C. A., Federico, P., Taylor, M. J., Doesburg, S. M., et al. (2014) · Human Brain Mapping · doi:10.1002/hbm.22580 · Cited by 72
“…demonstrate correlated lowfrequency fluctuations in blood oxygen level-dependent (BOLD) signals at rest [Biswal et al., 1995; Raichle and Snyder, 2007; Raichle et al., 2001] that are correlated with underlying structural connectivity patterns [Greicius et al., 2009; van den Heuvel et al., 2009].”
BackgroundAlcohol increases spontaneous BOLD signal fluctuations in the visual network
Esposito, F., Pignataro, G., di Renzo, G., Spinali, A., Paccone, A., Tedeschi, G., & Annunziato, L. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.06.061 · Cited by 71
“…structural connectivity architecture of the human brain, as visible with diffusion tensor imaging (DTI) (Greicius et al., 2009; van den Heuvel et al., 2009); (iii) for at least six of the nine known RSNs, the time-course of spontaneous BOLD activity is correlated with…”
Determining functional connectivity using fMRI data with diffusion-based anatomical weighting
Bowman, F. D., Zhang, L., Derado, G., & Chen, S. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.05.032 · Cited by 70
“Several RSN regions have been shown to exhibit strong SC (Skudlarski et. al., 2008; van den Heuvel et al., 2009; Greicius, et al., 2009).”
Spontaneous functional network dynamics and associated structural substrates in the human brain
Liao, X., Yuan, L., Zhao, T., Dai, Z., Shu, N., Xia, M., Yang, Y., Evans, A. C., & Yong He, A. (2015) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2015.00478 · Cited by 68
Diffusion tensor imaging comparison of progressive supranuclear palsy and corticobasal syndromes
Whitwell, J. L., Schwarz, C. G., Reid, R. I., Kantarci, K., Jack, C. R., & Josephs, K. A. (2014) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2014.01.023 · Cited by 66
Amygdala–cingulate intrinsic connectivity is associated with degree of social inhibition
Blackford, J. U., Clauss, J. A., Avery, S. N., Cowan, R. L., Benningfield, M. M., & VanDerKlok, R. M. (2014) · Biological Psychology · doi:10.1016/j.biopsycho.2014.02.003 · Cited by 67
Exploring brain functional plasticity in world class gymnasts: a network analysis
Wang, J., Lü, M., Fan, Y., Wen, X., Zhang, R., Wang, B., Ma, Q., Zheng, S. M., Yong He, A., Wang, J., et al. (2015) · Brain Structure and Function · doi:10.1007/s00429-015-1116-6 · Cited by 69
The homotopic connectivity of the functional brain: a meta-analytic approach
Mancuso, L., Costa, T., Nani, A., Manuello, J., Liloia, D., Gelmini, G., Panero, M., Duca, S., & Cauda, F. (2019) · Scientific Reports · doi:10.1038/s41598-019-40188-3 · Cited by 69
Intrinsic connectome organization across temporal scales: New insights from cross-modal approaches
Sadaghiani, S., & Wirsich, J. (2019) · Network Neuroscience · doi:10.1162/netn_a_00114 · Cited by 67
“Once again, this conceptual evolution parallels that in fMRI in which the existence of intrinsic FC was similarly validated by its spatial relationship to structural connectivity (Honey et al., 2009; Skudlarski et al., 2008; van den Heuvel et al., 2009).”
BackgroundModeling regional changes in dynamic stability during sleep and wakefulness
Ipiña, I. P., Kehoe, P. D., Kringelbach, M. L., Laufs, H., Ibáñez, A. M., Deco, G., Perl, Y. S., & Tagliazucchi, E. (2020) · NeuroImage · doi:10.1016/j.neuroimage.2020.116833 · Cited by 67
Mapping the structural and functional network architecture of the medial temporal lobe using 7T MRI
Shah, P., Bassett, D. S., Wisse, L. E. M., Detre, J. A., Stein, J. M., Yushkevich, P. A., Shinohara, R. T., Pluta, J. B., Valenciano, E., Daffner, M., et al. (2017) · Human Brain Mapping · doi:10.1002/hbm.23887 · Cited by 64
Korgaonkar, M. S., Ram, K., Williams, L. M., Gatt, J. M., & Grieve, S. M. (2014) · Human Brain Mapping · doi:10.1002/hbm.22446 · Cited by 74
“Functional connectivity measured at rest within this network has been shown to be associated with underlying structural connections measured using Diffusion Tensor Imaging (Greicius et al., 2009; van den Heuvel et al., 2008, 2009).”
Method
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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