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Optimally controlling the human connectome: the role of network topology
Richard F. Betzel, Shi Gu, John D. Medaglia and 2 more
Scientific Reports · 2016 · CC BY
Abstract
To meet ongoing cognitive demands, the human brain must seamlessly transition from one brain state to another, in the process drawing on different cognitive systems. How does the brain’s network of anatomical connections help facilitate such transitions? Which features of this network contribute to making one transition easy and another transition difficult? Here, we address these questions using network control theory. We calculate the optimal input signals to drive the brain to and from states dominated by different cognitive systems. The input signals allow us to assess the contributions made by different brain regions. We show that such contributions, which we measure as energy, are correlated with regions’ weighted degrees. We also show that the network communicability, a measure of direct and indirect connectedness between brain regions, predicts the extent to which brain regions compensate when input to another region is suppressed. Finally, we identify optimal states in which the brain should start (and finish) in order to minimize transition energy. We show that the optimal target states display high activity in hub regions, implicating the brain’s rich club. Furthermore, when rich club organization is destroyed, the energy cost associated with state transitions increases significantly, demonstrating that it is the richness of brain regions that makes them ideal targets.
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Read at PubMed CentralReferences 87
- 1.
- 2.
Honey C.. Predicting human resting-state functional connectivity from structural connectivity. Proceedings of the National Academy of Sciences 106, 2035–2040 (2009 ).
Not in our library10.1073/pnas.0811168106
- 3.
Hermundstad A. M.. Structural foundations of resting-state and task-based functional connectivity in the human brain. Proceedings of the National Academy of Sciences 110, 6169–6174 (2013 ).
Not in our library10.1073/pnas.1219562110
- 4.
- 5.
Becker C. O.. Accurately predicting functional connectivity from diffusion imaging. arXiv preprint arXiv:1512.02602 (2015).
Not in our library
- 6.
Deco G., Jirsa V. K. & McIntosh A. R. Emerging concepts for the dynamical organization of resting-state activity in the brain. Nature Reviews Neuroscience 12, 43–56 (2011 ).
Not in our library10.1038/nrn2961
- 7.
Goñi J.. Resting-brain functional connectivity predicted by analytic measures of network communication. Proceedings of the National Academy of Sciences 111, 833–838 (2014 ).
Not in our library10.1073/pnas.1315529111
- 8.
Allen E. A.. Tracking whole-brain connectivity dynamics in the resting state. Cerebral cortex bhs352 (2012 ).
Not in our library10.1093/cercor/bhs352
- 9.
- 10.
Betzel R. F., Fukushima M., He Y., Zuo X.-N. & Sporns O. Dynamic fluctuations coincide with periods of high and low modularity in resting-state functional brain networks. NeuroImage 127, 287–297 (2016 ).
Not in our library10.1016/j.neuroimage.2015.12.001
- 11.
Bassett D. S.. Dynamic reconfiguration of human brain networks during learning. Proceedings of the National Academy of Sciences 108, 7641–7646 (2011 ).
Not in our library10.1073/pnas.1018985108
- 12.
Braun U.. Dynamic reconfiguration of frontal brain networks during executive cognition in humans. Proceedings of the National Academy of Sciences 112, 11678–11683 (2015 ).
Not in our library10.1073/pnas.1422487112
- 13.
- 14.
Wilson H. R. & Cowan J. D. Excitatory and inhibitory interactions in localized populations of model neurons. Biophysical journal 12, 1 (1972 ).
Not in our library10.1016/s0006-3495(72)86068-5
- 15.
- 16.
Marreiros A. C., Kiebel S. J. & Friston K. J. A dynamic causal model study of neuronal population dynamics. Neuroimage 51, 91–101 (2010 ).
Not in our library10.1016/j.neuroimage.2010.01.098
- 17.
Freyer F.. Biophysical mechanisms of multistability in resting-state cortical rhythms. The Journal of Neuroscience 31, 6353–6361 (2011 ).
Not in our library10.1523/jneurosci.6693-10.2011
- 18.
- 19.
Breakspear M., Heitmann S. & Daffertshofer A. Generative models of cortical oscillations: neurobiological implications of the kuramoto model. Frontiers in human neuroscience 4 (2010 ).
Not in our library10.3389/fnhum.2010.00190
- 20.
Haimovici A., Tagliazucchi E., Balenzuela P. & Chialvo D. R. Brain organization into resting state networks emerges at criticality on a model of the human connectome. Physical review letters 110, 178101 (2013 ).
Not in our library10.1103/physrevlett.110.178101
- 21.
Abdelnour F., Voss H. U. & Raj A. Network diffusion accurately models the relationship between structural and functional brain connectivity networks. Neuroimage 90, 335–347 (2014 ).
Not in our library10.1016/j.neuroimage.2013.12.039
- 22.
Mišic B.. Cooperative and competitive spreading dynamics on the human connectome. Neuron 86, 1518–1529 (2015 ).
Not in our library10.1016/j.neuron.2015.05.035
- 23.
Kalman R. E. Mathematical description of linear dynamical systems. Journal of the Society for Industrial & Applied Mathematics, Series A: Control 1, 152–192 (1963 ).
Not in our library
- 24.
Liu Y.-Y., Slotine J.-J. & Barabási A.-L. Controllability of complex networks. Nature 473, 167–173 (2011 ).
Not in our library10.1038/nature10011
- 25.
Sun J. & Motter A. E. Controllability transition and nonlocality in network control. Physical Review Letters 110, 208701 (2013 ).
Not in our library10.1103/physrevlett.110.208701
- 26.
Rosin B.. Closed-loop deep brain stimulation is superior in ameliorating parkinsonism. Neuron 72, 370–384 (2011 ).
Not in our library10.1016/j.neuron.2011.08.023
- 27.
Taylor P. N.. Optimal control based seizure abatement using patient derived connectivity. Frontiers in Neuroscience 9, 202 (2015 ).
Not in our library10.3389/fnins.2015.00202
- 28.
Fox M. D., Halko M. A., Eldaief M. C. & Pascual-Leone A. Measuring and manipulating brain connectivity with resting state functional connectivity magnetic resonance imaging (fcmri) and transcranial magnetic stimulation (tms). Neuroimage 62, 2232–2243 (2012 ).
Not in our library10.1016/j.neuroimage.2012.03.035
- 29.
Yan G., Ren J., Lai Y.-C., Lai C.-H. & Li B. Controlling complex networks: How much energy is needed? Physical review letters 108, 218703 (2012 ).
Not in our library10.1103/physrevlett.108.218703
- 30.
Wang W.-X., Ni X., Lai Y.-C. & Grebogi C. Optimizing controllability of complex networks by minimum structural perturbations. Physical Review E 85, 026115 (2012 ).
Not in our library10.1103/physreve.85.026115
- 31.
Cowan N. J., Chastain E. J., Vilhena D. A., Freudenberg J. S. & Bergstrom C. T. Nodal dynamics, not degree distributions, determine the structural controllability of complex networks. PloS one 7, e38398 (2012 ).
Not in our library10.1371/journal.pone.0038398
- 32.
Pósfai M., Liu Y.-Y., Slotine J.-J. & Barabási A.-L. Effect of correlations on network controllability. Scientific reports 3 (2013 ).
Not in our library10.1038/srep01067
- 33.
Ruths J. & Ruths D. Control profiles of complex networks. Science 343, 1373–1376 (2014 ).
Not in our library10.1126/science.1242063
- 34.
Pasqualetti F., Zampieri S. & Bullo F. Controllability metrics, limitations and algorithms for complex networks. Control of Network Systems, IEEE Transactions on 1, 40–52 (2014 ).
Not in our library
- 35.
- 36.
Yeo B. T.. The organization of the human cerebral cortex estimated by intrinsic functional connectivity. Journal of neurophysiology 106, 1125–1165 (2011 ).
Not in our library10.1152/jn.00338.2011
- 37.
van den Heuvel M. P. & Sporns O. Rich-club organization of the human connectome. The Journal of neuroscience 31, 15775–15786 (2011 ).
Not in our library10.1523/jneurosci.3539-11.2011
- 38.
Lin C. T. Structural controllability. Automatic Control, IEEE Transactions on 19, 201–208 (1974 ).
Not in our library
- 39.
Pascual-Leone A., Walsh V. & Rothwell J. Transcranial magnetic stimulation in cognitive neuroscience-virtual lesion, chronometry, and functional connectivity. Current opinion in neurobiology 10, 232–237 (2000 ).
Not in our library10.1016/s0959-4388(00)00081-7
- 40.
Silvanto J. & Muggleton N. G. New light through old windows: Moving beyond the “virtual lesion” approach to transcranial magnetic stimulation. Neuroimage 39, 549–552 (2008 ).
Not in our library10.1016/j.neuroimage.2007.09.008
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