High-cost, high-capacity backbone for global brain communication
Open accessAbstract
Network studies of human brain structural connectivity have identified a specific set of brain regions that are both highly connected and highly central. Recent analyses have shown that these putative hub regions are mutually and densely interconnected, forming a “rich club” within the human brain. Here we show that the set of pathways linking rich club regions forms a central high-cost, high-capacity backbone for global brain communication. Diffusion tensor imaging (DTI) data of two sets of 40 healthy subjects were used to map structural brain networks. The contributions to network cost and communication capacity of global cortico-cortical connections were assessed through measures of their topology and spatial embedding. Rich club connections were found to be more costly than predicted by their density alone and accounted for 40% of the total communication cost. Furthermore, 69% of all minimally short paths between node pairs were found to travel through the rich club and a large proportion of these communication paths consisted of ordered sequences of edges (“path motifs”) that first fed into, then traversed, and finally exited the rich club, while passing through nodes of increasing and then decreasing degree. The prevalence of short paths that follow such ordered degree sequences suggests that neural communication might take advantage of strategies for dynamic routing of information between brain regions, with an important role for a highly central rich club. Taken together, our results show that rich club connections make an important contribution to interregional signal traffic, forming a central high-cost, high-capacity backbone for global brain communication.
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Richly connected subnetworks are metabolically expensive, consuming nearly 50% of cortical metabolism in humans.
“but are also metabolically expensive, consuming nearly 50% of cortical metabolism in humans (Heuvel et al., 2012)”
From An Integrated World Modeling Theory (IWMT) of Consciousness (2020) · cites this paper as Heuvel et al., 2012
The dynamics of the default mode, salience and frontoparietal control networks form the computational core of a brain's dynamic internal working model of the body in the world, entraining sensory and motor systems to create multi-sensory representations of the world at various time scales from the perspective of someone who has a body, all in the service of allostasis.
“My key hypothesis is that the dynamics of the default mode, salience and frontoparietal control networks form the computational core of a brain’s dynamic internal working model of the body in the world, entraining sensory and motor systems to create multi-sensory representations of the world at various time scales from the perspective of someone who has a body, all in the service of allostasis (”
From The theory of constructed emotion: an active inference account of interoception and categorization (2016) · cites this paper as van den Heuvel et al., 2012
Cites
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 · see citing works
Self-citationBuckner, R. L., Sepulcre, J., Talukdar, T., Krienen, F. M., Liu, H., Hedden, T., Andrews-Hanna, J. R., Sperling, R. A., & Johnson, K. A. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.5062-08.2009 · Cited by 2,862 · 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
Efficiency of Functional Brain Networks and Intellectual Performance
van den Heuvel, M. P., Stam, C. J., Kahn, R. S., & Hulshoff Pol, H. E. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.1443-09.2009 · Cited by 1,078 · see citing works
Self-citationWeight consistency specifies regularities of macaque cortical networks
Markov, N. T., Misery, P., Falchier, A., Lamy, C., Vezoli, J., Quilodran, R., Gariel, M. A., Giroud, P., Ercsey-Ravasz, M., Pilaz, L. J., et al. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhq201 · Cited by 386 · see citing works
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Self-citationThe connectomics of brain disorders
Fornito, A., Zalesky, A., & Breakspear, M. (2015) · Nature Reviews Neuroscience · doi:10.1038/nrn3901 · Cited by 1,734 · see citing works
The theory of constructed emotion: an active inference account of interoception and categorization
Barrett, L. F. (2016) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsw154 · Cited by 1,426 · see citing works
“…sensory and motor systems to create multi-sensory representations of the world at various time scales from the perspective of someone who has a body, all in the service of allostasis (for evidence consistent with this view, see van den Heuvel et al. , 2012; van den Heuvel and Sporns, 2011, 2013).”
Carhart-Harris, R. L., Leech, R., Hellyer, P. J., Shanahan, M., Feilding, A., Tagliazucchi, E., Chialvo, D. R., & Nutt, D. (2014) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2014.00020 · Cited by 1,252 · see citing works
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Sporns, O. (2013) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2012.11.015 · Cited by 1,067 · see citing works
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Zalesky, A., Fornito, A., Cocchi, L., Gollo, L. L., & Breakspear, M. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1400181111 · Cited by 753 · see citing works
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Evidence for a large-scale brain system supporting allostasis and interoception in humans
Kleckner, I. R., Zhang, J., Touroutoglou, A., Chanes, L., Xia, C., Simmons, W. K., Quigley, K. S., Dickerson, B. C., & Feldman Barrett, L. (2017) · Nature Human Behaviour · doi:10.1038/s41562-017-0069 · Cited by 641 · see citing works
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Towlson, E. K., Vértes, P. E., Ahnert, S. E., Schafer, W. R., & Bullmore, E. T. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.3784-12.2013 · Cited by 343 · see citing works
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Self-citationRoberts, J. A., Gollo, L. L., Abeysuriya, R. G., Roberts, G., Mitchell, P. B., Woolrich, M. W., & Breakspear, M. (2019) · Nature Communications · doi:10.1038/s41467-019-08999-0 · Cited by 264 · see citing works
Optimally controlling the human connectome: the role of network topology
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Pain and analgesia: the value of salience circuits
Borsook, D., Edwards, R., Elman, I., Becerra, L., & Levine, J. (2013) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2013.02.003 · Cited by 215 · see citing works
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Structural network alterations and neurological dysfunction in cerebral amyloid angiopathy
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Scholtens, L. H., Schmidt, R., de Reus, M. A., & van den Heuvel, M. P. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.0752-14.2014 · Cited by 160 · see citing works
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Imaging human brain networks to improve the clinical efficacy of non-invasive brain stimulation
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Ray, S., Miller, M., Karalunas, S., Robertson, C., Grayson, D. S., Cary, R. P., Hawkey, E., Painter, J. G., Kriz, D., Fombonne, E., et al. (2014) · Human Brain Mapping · doi:10.1002/hbm.22603 · Cited by 149 · see citing works
Safron, A. (2020) · Frontiers in Artificial Intelligence · doi:10.3389/frai.2020.00030 · Cited by 133 · see citing works
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Lin, A., Yang, R., Dorkenwald, S., Matsliah, A., Sterling, A. R., Schlegel, P., Yu, S.-C., McKellar, C. E., Costa, M., Eichler, K., et al. (2024) · Nature · doi:10.1038/s41586-024-07968-y · Cited by 147 · see citing works
Intrinsic functional connectivity variance and state‐specific under‐connectivity in autism
Chen, H., Nomi, J. S., Uddin, L. Q., Duan, X., & Chen, H. (2017) · Human Brain Mapping · doi:10.1002/hbm.23764 · Cited by 137 · see citing works
van den Heuvel, M. P., de Reus, M. A., Feldman Barrett, L., Scholtens, L. H., Coopmans, F. M. T., Schmidt, R., Preuss, T. M., Rilling, J. K., & Li, L. (2015) · Human Brain Mapping · doi:10.1002/hbm.22828 · Cited by 131 · see citing works
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Chen, Z., Liu, M., Gross, D. W., & Beaulieu, C. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00716 · Cited by 77 · see citing works
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Yoon, S., Kim, J. E., Hwang, J., Kim, T.-S., Kang, H. J., Namgung, E., Ban, S., Oh, S., Yang, J., Renshaw, P. F., et al. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.11.027 · Cited by 71 · see citing works
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Kemmerer, D. (2019) · doi:10.1093/oso/9780190682620.001.0001 · Cited by 42 · see citing works
Turk, E., Scholtens, L. H., & van den Heuvel, M. P. (2016) · Human Brain Mapping · doi:10.1002/hbm.23141 · Cited by 27 · see citing works
Self-citation
- Authors
- van den Heuvel, M. P., Kahn, R. S., Goñi, J., & Sporns, O.
- Affiliations
- Department of Psychiatry, University Medical Center Utrecht, Rudolf Magnus Institute of Neuroscience, 3905 GA, Utrecht, The Netherlands; and
- University Medical Center Utrecht (NL)
- Indiana University Bloomington (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2012-06-18
- Volume
- 109
- Issue
- 28
- Pages
- 11372-11377
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3396547
- OpenAlex
- W1990574575
- Cited by
- 781
- References
- 5
- Citations by year
- 2026: 30 · 2025: 38 · 2024: 41 · 2023: 63 · 2022: 69 · 2021: 47 · 2020: 65 · 2019: 75 · 2018: 68 · 2017: 43 · 2016: 74 · 2015: 63 · 2014: 56 · 2013: 45 · 2012: 4
- FWCI
- 27.54
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Pure Amsterdam UMC (publishedVersion, other-oa)
- Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- 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
- rich club, structural brain connectivity, network cost, communication skills, hub regions, corticocortical connections, information routing, diffusion tensor imaging, brain network topology
- MeSH terms
- Algorithms, Brain, Brain Mapping, Communication, Humans, Models, Biological, Models, Neurological, Neural Pathways, Neurons, Models, Statistical, Diffusion Tensor Imaging
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