Cortical rich club regions can organize state-dependent functional network formation by engaging in oscillatory behavior

NeuroImage

Volumn 146, Issue , 2017, Pages 561-574

  Senden, Mario ^a   Reuter, Niels ^a,e   van den Heuvel, Martijn P ^c   Goebel, Rainer ^a,b   Deco, Gustavo ^d  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^d UNIVERSITAT POMPEU FABRA   (Spain)

^e Institute of Neuroscience and Medicine INM 1 Research Centre Jülich   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; BOLD SIGNAL; BRAIN CORTEX; BRAIN REGION; CONTROLLED STUDY; EXECUTIVE FUNCTION; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HUMAN; HUMAN EXPERIMENT; MALE; MATHEMATICAL ANALYSIS; MATHEMATICAL MODEL; MENTAL TASK; NERVE CELL NETWORK; NEUROPHYSIOLOGY; NORMAL HUMAN; PROCESS OPTIMIZATION; BIOLOGICAL MODEL; BRAIN; CONNECTOME; CORTICAL SYNCHRONIZATION; DIFFUSION WEIGHTED IMAGING; ELECTROENCEPHALOGRAM; NERVE TRACT; PHYSIOLOGY; YOUNG ADULT;

ADULT; BRAIN; BRAIN WAVES; CEREBRAL CORTEX; CONNECTOME; CORTICAL SYNCHRONIZATION; DIFFUSION MAGNETIC RESONANCE IMAGING; FEMALE; HUMANS; MALE; MODELS, NEUROLOGICAL; NEURAL PATHWAYS; YOUNG ADULT;

EID: 85012109002     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2016.10.044     Document Type: Article

References (64)

1. Baars, B.J., Global workspace theory of consciousness: toward a cognitive neuroscience of human experience. Boundaries Conscious.: Neurobiol. Neuropathol. 150 (2005), 45–53.
2. Bear, M.F., Connors, B., Paradiso, M., Neuroscience: Exploring the Brain. 3rd Revise, 2006, Lippincott Williams and Wilkins, Baltimore.
3. Braga, R.M., Sharp, D.J., Leeson, C., Wise, R.J., Leech, R., Echoes of the brain within default mode, association, and heteromodal cortices. J. Neurosci. 33:35 (2013), 14031–14039.
4. Breakspear, M., Roberts, J.A., Terry, J.R., Rodrigues, S., Mahant, N., Robinson, P.A., A unifying explanation of primary generalized seizures through nonlinear brain modeling and bifurcation analysis. Cereb. Cortex 16:9 (2006), 1296–1313, 10.1093/cercor/bhj072.
5. Cabral, J., Hugues, E., Deco, G., Simulated functional networks in health and schizophrenia: a graph theoretical approach. BMC Neurosci., 12(Suppl 1), 2011, P63.
6. Cabral, J., Luckhoo, H., Woolrich, M., Joensson, M., Mohseni, H., Baker, A., Deco, G., Exploring mechanisms of spontaneous functional connectivity in MEG: how delayed network interactions lead to structured amplitude envelopes of band-pass filtered oscillations. Neuroimage 90 (2014), 423–435.
7. Cole, M.W., Reynolds, J.R., Power, J.D., Repovs, G., Anticevic, A., Braver, T.S., Multi-task connectivity reveals flexible hubs for adaptive task control. Nat. Neurosci. 16:9 (2013), 1348–1355.
8. Colizza, V., Flammini, A., Serrano, M.A., Vespignani, A., Detecting rich-club ordering in complex networks. Nat. Phys. 2:2 (2006), 110–115.
9. Damasio, A.R., Time-locked multiregional retroactivation: a systems-level proposal for the neural substrates of recall and recognition. Cognition 33:1 (1989), 25–62.
10. de Reus, M.A., van den Heuvel, M.P., Estimating false positives and negatives in brain networks. NeuroImage 70 (2013), 402–409, 10.1016/j.neuroimage.2012.12.066.
11. de Reus, M.A., van den Heuvel, M.P., Simulated rich club lesioning in brain networks: a scaffold for communication and integration?. Front. Human. Neurosci., 8, 2014, 10.3389/fnhum.2014.00647.
12. Deco, G., Jirsa, V.K., Ongoing cortical activity at rest: criticality, multistability, and ghost attractors. J. Neurosci. 32:10 (2012), 3366–3375, 10.1523/JNEUROSCI.2523-11.2012.
13. Deco, G., Jirsa, V.K., McIntosh, A.R., Emerging concepts for the dynamical organization of resting-state activity in the brain. Nat. Rev. Neurosci. 12:1 (2011), 43–56, 10.1038/nrn2961.
14. Deco, G., Senden, M., Jirsa, V., How anatomy shapes dynamics: a semi-analytical study of the brain at rest by a simple spin model. Front. Comput. Neurosci., 2012, 10.3389/fncom.2012.00068.
15. Dehaene, S., Naccache, L., Towards a cognitive neuroscience of consciousness: basic evidence and a workspace framework. Cognition 79:1 (2001), 1–37.
16. Dehaene, S., Changeux, J.-P., Experimental and theoretical approaches to conscious processing. Neuron 70:2 (2011), 200–227.
17. Desikan, R.S., Ségonne, F., Fischl, B., Quinn, B.T., Dickerson, B.C., Blacker, D., et al. An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 31:3 (2006), 968–980.
18. Eriksen, B.A., Eriksen, C.W., Effects of noise letters upon the identification of a target letter in a nonsearch task. Percept. Psychophys. 16:1 (1974), 143–149.
19. Flourens, P., 1842. Recherches expérimentales sur les propriétés et les fonctions du système nerveux dans les animaux vertébrés. Ballière.
20. Flowers, K.A., Robertson, C., The effect of Parkinson's disease on the ability to maintain a mental set. J. Neurol. Neurosurg. Psychiatry 48:6 (1985), 517–529.
21. Freyer, F., Aquino, K., Robinson, P.A., Ritter, P., Breakspear, M., Bistability and non-gaussian fluctuations in spontaneous cortical activity. J. Neurosci. 29:26 (2009), 8512–8524, 10.1523/JNEUROSCI.0754-09.2009.
22. Freyer, F., Roberts, J.A., Becker, R., Robinson, P.A., Ritter, P., Breakspear, M., Biophysical mechanisms of multistability in resting-state cortical rhythms. J. Neurosci. 31:17 (2011), 6353–6361.
23. Freyer, F., Roberts, J.A., Ritter, P., Breakspear, M., A canonical model of multistability and scale-invariance in biological systems. PLoS Comput. Biol., 8(8), 2012, e1002634.
24. Fries, P., Rapid feature selective neuronal synchronization through correlated latency shifting. Nat. Neurosci., 4(2), 2001, 194.
25. Fries, P., Neuronal gamma-band synchronization as a fundamental process in cortical computation. Annu. Rev. Neurosci. 32:1 (2009), 209–224, 10.1146/annurev.neuro.051508.135603.
26. Ghosh, A., Rho, Y., McIntosh, A.R., Kötter, R., Jirsa, V.K., Noise during rest enables the exploration of the brain's dynamic repertoire. PLoS Comput. Biol., 4(10), 2008, e1000196.
27. Glasser, M.F., Sotiropoulos, S.N., Wilson, J.A., Coalson, T.S., Fischl, B., Andersson, J.L., et al. The minimal preprocessing pipelines for the Human Connectome Project. Neuroimage 80 (2013), 105–124.
28. Glerean, E., Salmi, J., Lahnakoski, J.M., Jääskeläinen, I.P., Sams, M., Functional magnetic resonance imaging phase synchronization as a measure of dynamic functional connectivity. Brain Connect. 2:2 (2012), 91–101.
29. Gollo, L.L., Zalesky, A., Hutchison, R.M., van den Heuvel, M., Breakspear, M., Dwelling quietly in the rich club: brain network determinants of slow cortical fluctuations. Philos. Trans. R. Soc. Lond. B: Biol. Sci., 370(1668), 2015, 20140165.
30. Grigg, O., Grady, C.L., Task-related effects on the temporal and spatial dynamics of resting-state functional connectivity in the default network. PLoS One, 5(10), 2010 [e13311–e13311].
31. Gu, S., Pasqualetti, F., Cieslak, M., Telesford, Q.K., Alfred, B.Y., Kahn, A.E., et al. Controllability of structural brain networks. Nat. Commun., 6, 2015.
32. Harriger, L., van den Heuvel, M.P., Sporns, O., Rich club organization of macaque cerebral cortex and its role in network communication. PloS One, 7(9), 2012, e46497.
33. Hiltunen, T., Kantola, J., Elseoud, A.A., Lepola, P., Suominen, K., Starck, T., Palva, J.M., Infra-slow EEG fluctuations are correlated with resting-state network dynamics in fMRI. J. Neurosci. 34:2 (2014), 356–362, 10.1523/JNEUROSCI.0276-13.2014.
34. Hipp, J.F., Hawellek, D.J., Corbetta, M., Siegel, M., Engel, A.K., Large-scale cortical correlation structure of spontaneous oscillatory activity. Nat. Neurosci. 15:6 (2012), 884–890.
35. Honey, C.J., Sporns, O., Cammoun, L., Gigandet, X., Thiran, J.P., Meuli, R., Hagmann, P., Predicting human resting-state functional connectivity from structural connectivity. Proc. Natl. Acad. Sci. USA, 106(6), 2009, 2035.
36. Hutchison, R.M., Womelsdorf, T., Allen, E.A., Bandettini, P.A., Calhoun, V.D., Corbetta, M., et al. Dynamic functional connectivity: promise, issues, and interpretations. Neuroimage 80 (2013), 360–378.
37. Kirchner, W.K., Age differences in short-term retention of rapidly changing information. J. Exp. Psychol., 55(4), 1958, 352.
38. Lashley, K.S., 1929. Brain mechanisms and intelligence: A quantitative study of injuries to the brain.
39. Leech, R., Braga, R., Sharp, D.J., Echoes of the brain within the posterior cingulate cortex. J. Neurosci. 32:1 (2012), 215–222, 10.1523/JNEUROSCI.3689-11.2012.
40. Liu, Y.-Y., Slotine, J.-J., Barabási, A.-L., Controllability of complex networks. Nature 473:7346 (2011), 167–173, 10.1038/nature10011.
41. Lőrincz, M.L., Geall, F., Bao, Y., Crunelli, V., Hughes, S.W., ATP-dependent infra-slow (< 0.1 Hz) oscillations in Thalamic networks. PLoS One, 4(2), 2009, e4447, 10.1371/journal.pone.0004447.
42. Maslov, S., Sneppen, K., Specificity and stability in topology of protein networks. Science 296:5569 (2002), 910–913, 10.1126/science.1065103.
43. Michalareas, G., Vezoli, J., van Pelt, S., Schoffelen, J.-M., Kennedy, H., Fries, P., Alpha-beta and gamma rhythms subserve feedback and feedforward influences among human visual cortical areas. Neuron, 2016.
44. Monto, S., Palva, S., Voipio, J., Palva, J.M., Very slow eeg fluctuations predict the dynamics of stimulus detection and oscillation amplitudes in humans. J. Neurosci. 28:33 (2008), 8268–8272, 10.1523/JNEUROSCI.1910-08.2008.
45. Moussa, M.N., Steen, M.R., Laurienti, P.J., Hayasaka, S., Consistency of network modules in resting-state fMRI connectome data. PLoS One, 7(8), 2012, e44428, 10.1371/journal.pone.0044428.
46. Patel, A.X., Bullmore, E.T., A wavelet-based estimator of the degrees of freedom in denoised fMRI time series for probabilistic testing of functional connectivity and brain graphs. NeuroImage, 2015.
47. Poldrack, R.A., Kittur, A., Kalar, D., Miller, E., Seppa, C., Gil, Y., Bilder, R.M., The cognitive atlas: toward a knowledge foundation for cognitive neuroscience. Front. Neuroinformatics, 5(0), 2011.
48. Reuter, M., Schmansky, N.J., Rosas, H.D., Fischl, B., Within-subject template estimation for unbiased longitudinal image analysis. Neuroimage 61:4 (2012), 1402–1418.
49. Schmidt, R., LaFleur, K.J.R., de Reus, M.A., van den Berg, L.H., van den Heuvel, M.P., Kuramoto model simulation of neural hubs and dynamic synchrony in the human cerebral connectome. BMC Neurosci., 16(1), 2015, 1.
50. Senden, M., Deco, G., de Reus, M.A., Goebel, R., van den Heuvel, M.P., Rich club organization supports a diverse set of functional network configurations. NeuroImage 96 (2014), 174–182, 10.1016/j.neuroimage.2014.03.066.
51. Shanahan, M., The brain's connective core and its role in animal cognition. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 367:1603 (2012), 2704–2714, 10.1098/rstb.2012.0128.
52. Shepard, R.N., Metzler, J., 1971. Mental rotation of three-dimensional objects.
53. Smith, S.M., Fox, P.T., Miller, K.L., Glahn, D.C., Fox, P.M., Mackay, C.E., et al. Correspondence of the brain's functional architecture during activation and rest. Proc. Natl. Acad. Sci. USA 106:31 (2009), 13040–13045.
54. Tononi, G., An information integration theory of consciousness. BMC Neurosci., 5(1), 2004, 42.
55. van den Heuvel, M.P., Kahn, R.S., Goñi, J., Sporns, O., High-cost, high-capacity backbone for global brain communication. Proc. Natl. Acad. Sci. 109:28 (2012), 11372–11377.
56. van den Heuvel, M.P., de Reus, M.A., Feldman Barrett, L., Scholtens, L.H., Coopmans, F.M.T., Schmidt, R., Li, L., Comparison of diffusion tractography and tract-tracing measures of connectivity strength in rhesus macaque connectome. Human. Brain Mapp. 36:8 (2015), 3064–3075, 10.1002/hbm.22828.
57. van den Heuvel, M.P., Sporns, O., Rich-club organization of the human connectome. J. Neurosci. 31:44 (2011), 15775–15786.
58. Van Essen, D.C., Ugurbil, K., Auerbach, E., Barch, D., Behrens, T.E.J., Bucholz, R., et al. The Human Connectome Project: a data acquisition perspective. Neuroimage 62:4 (2012), 2222–2231.
59. Vanhatalo, S., Palva, J.M., Holmes, M.D., Miller, J.W., Voipio, J., Kaila, K., Infraslow oscillations modulate excitability and interictal epileptic activity in the human cortex during sleep. Proc. Natl. Acad. Sci. USA 101:14 (2004), 5053–5057.
60. Váša, F., Shanahan, M., Hellyer, P.J., Scott, G., Cabral, J., Leech, R., Effects of lesions on synchrony and metastability in cortical networks. NeuroImage 118 (2015), 456–467, 10.1016/j.neuroimage.2015.05.042.
61. Wildie, M., Shanahan, M., Metastability and chimera states in modular delay and pulse-coupled oscillator networks. Chaos: Interdiscip. J. Nonlinear Sci., 22(4), 2012, 43131.
62. Yeh, F.-C., Wedeen, V.J., Tseng, W.-Y.I., Generalized-sampling imaging. IEEE Trans. Med. Imaging 29:9 (2010), 1626–1635.
63. Zamora-López, G., Zhou, C., Kurths, J., Graph analysis of cortical networks reveals complex anatomical communication substrate. Chaos: Interdiscip. J. Nonlinear Sci., 19(1), 2009, 15117.
64. Zhou, S., Mondragon, R.J., The rich-club phenomenon in the Internet topology. IEEE Commun. Lett. 8:3 (2004), 180–182, 10.1109/LCOMM.2004.823426.