Increased Stability and Breakdown of Brain Effective Connectivity during Slow-Wave Sleep: Mechanistic Insights from Whole-Brain Computational Modelling

Scientific Reports

Volumn 7, Issue 1, 2017, Pages

  Jobst, Beatrice M ^a   Hindriks, Rikkert ^a   Laufs, Helmut ^b,c   Tagliazucchi, Enzo ^d   Hahn, Gerald ^a   Ponce Alvarez, Adrián ^a   Stevner, Angus B A ^e   Kringelbach, Morten L ^e,f   Deco, Gustavo ^a,g,h,i  

^a UNIVERSITAT POMPEU FABRA   (Spain)

^b UNIVERSITY OF KIEL   (Germany)

^c UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^d NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^e UNIVERSITY OF OXFORD   (United Kingdom)

^f AARHUS UNIVERSITY   (Denmark)

^g INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

^h MAX PLANCK INSTITUTE FOR HUMAN COGNITIVE AND BRAIN SCIENCES   (Germany)

ⁱ MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

FUNCTIONAL CONNECTIVITY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; MODEL; OSCILLATION; SLOW WAVE SLEEP; WAKEFULNESS; ADULT; BRAIN; BRAIN MAPPING; COMPARATIVE STUDY; COMPUTER SIMULATION; FEMALE; MALE; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; PROCEDURES; THEORETICAL MODEL; YOUNG ADULT;

ADULT; BRAIN; BRAIN MAPPING; COMPUTER SIMULATION; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MODELS, THEORETICAL; SLEEP, SLOW-WAVE; WAKEFULNESS; YOUNG ADULT;

EID: 85021890472     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-04522-x     Document Type: Article

References (72)

1. Cirelli, C. & Tononi, G. Is sleep essential? PLoS Biology 6, e216, doi:10.1371/journal.pbio.0060216 (2008).
2. Iber, C., Ancoli-Israel, S., Chesson, A. & Quan, S. The AASM Manual for the Scoring of Sleep and Associates Events: Rules, Terminology and Technical Specifications. Sleep (Rochester) 59, doi:10.1002/ejoc.201200111 (2007).
3. Biswal, B., Yetkin, F. Z., Haughton, V. M. & Hyde, J. S. Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn. Reson. Med. 34, 537-41 (1995).
4. Greicius, M. D., Krasnow, B., Reiss, A. L. & Menon, V. Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proc. Natl. Acad. Sci. USA 100, 253-8, doi:10.1073/pnas.0135058100 (2003).
5. Fransson, P. Spontaneous low-frequency BOLD signal fluctuations: An fMRI investigation of the resting-state default mode of brain function hypothesis. Hum. Brain Mapp. 26, 15-29, doi:10.1002/hbm.20113 (2005).
6. Fox, M. D. & Raichle, M. E. Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat. Rev. Neurosci. 8, 700-11, doi:10.1038/nrn2201 (2007).
7. Lee, M. H. et al. Clustering of resting state networks. PLoS One 7, e40370, doi:10.1371/journal.pone.0040370 (2012).
8. Smith, S. M. et al. Temporally-independent functional modes of spontaneous brain activity. Proc. Natl. Acad. Sci. USA 109, 3131-6, doi:10.1073/pnas.1121329109 (2012).
9. Boly, M. et al. Intrinsic brain activity in altered states of consciousness: How conscious is the default mode of brain function? Ann. N. Y. Acad. Sci. 1129, 119-129, doi:10.1196/annals.1417.015 (2008).
10. Boly, M. et al. Hierarchical clustering of brain activity during human nonrapid eye movement sleep. Proc. Natl. Acad. Sci. USA 109, 5856-61, doi:10.1073/pnas.1111133109 (2012).
11. Tagliazucchi, E. et al. Breakdown of long-range temporal dependence in default mode and attention networks during deep sleep. Proc. Natl. Acad. Sci. USA 110, 15419-24, doi:10.1073/pnas.1312848110 (2013).
12. Horovitz, S. G. et al. Decoupling of the brain's default mode network during deep sleep. Proc. Natl. Acad. Sci. USA 106, 11376-81, doi:10.1073/pnas.0901435106 (2009).
13. Larson-Prior, L. J. et al. Cortical network functional connectivity in the descent to sleep. Proc Natl Acad Sci USA 106, 4489-4494, doi:10.1073/pnas.0900924106 (2009).
14. Sämann, P. G. et al. Development of the brain's default mode network from wakefulness to slow wave sleep. Cereb. Cortex 21, 2082-93, doi:10.1093/cercor/bhq295 (2011).
15. Kaufmann, C. et al. Brain activation and hypothalamic functional connectivity during human non-rapid eye movement sleep: An EEG/fMRI study. Brain 129, 655-667, doi:10.1093/brain/awh686 (2005).
16. Tagliazucchi, E. et al. Automatic sleep staging using fMRI functional connectivity data. Neuroimage 63, 63-72, doi:10.1016/j. neuroimage.2012.06.036 (2012).
17. Spoormaker, V. I., Gleiser, P. M. & Czisch, M. Frontoparietal Connectivity and Hierarchical Structure of the Brain's Functional Network during Sleep. Front. Neurol. 3, 80, doi:10.3389/fneur.2012.00080 (2012).
18. Spoormaker, V. I. et al. Development of a Large-Scale Functional Brain Network during Human Non-Rapid Eye Movement Sleep. J. Neurosci. 30, 11379-11387, doi:10.1523/JNEUROSCI.2015-10.2010 (2010).
19. Greicius, M. D., Supekar, K., Menon, V. & Dougherty, R. F. Resting-state functional connectivity reflects structural connectivity in the default mode network. Cereb. Cortex 19, 72-8, doi:10.1093/cercor/bhn059 (2009).
20. Barttfeld, P. et al. Signature of consciousness in the dynamics of resting-state brain activity. Proc. Natl. Acad. Sci. USA 112, 887-92, doi:10.1073/pnas.1418031112 (2015).
21. Tagliazucchi, E., Crossley, N., Bullmore, E. T. & Laufs, H. Deep sleep divides the cortex into opposite modes of anatomical-functional coupling. Brain Struct. Funct. 221, 4221-4234, doi:10.1007/s00429-015-1162-0 (2016).
22. Massimini, M. et al. Triggering sleep slow waves by transcranial magnetic stimulation. Proc. Natl. Acad. Sci. USA 104, 8496-501, doi:10.1073/pnas.0702495104 (2007).
23. Massimini, M. et al. Breakdown of cortical effective connectivity during sleep. Science 309, 2228-2232, doi:10.1126/science.1117256 (2005).
24. Massimini, M., Boly, M., Casali, A., Rosanova, M. & Tononi, G. A perturbational approach for evaluating the brain's capacity for consciousness. Progress in Brain Research 177, 201-214, doi:10.1016/S0079-6123(09)17714-2 (2009).
25. Casali, A. G. et al. A Theoretically Based Index of Consciousness Independent of Sensory Processing and Behavior. Sci. Transl. Med. 5, 198ra105, doi:10.1126/scitranslmed.3006294 (2013).
26. Deco, G., Kringelbach, M. L., Jirsa, V. K. & Ritter, P. The dynamics of resting fluctuations in the brain: metastability and its dynamical cortical core. Sci. Rep. 7, 3095, doi:10.1038/s41598-017-03073-5 (2017).
27. Camalet, S., Jülicher, F. & Prost, J. Self-Organized Beating and Swimming of Internally Driven Filaments. Phys. Rev. Lett. 82, 1590-1593, doi:10.1103/PhysRevLett.82.1590 (1999).
28. Chang, C. & Glover, G. H. Time-frequency dynamics of resting-state brain connectivity measured with fMRI. Neuroimage 50, 81-98, doi:10.1016/j.neuroimage.2009.12.011 (2010).
29. Hutchison, R. M., Womelsdorf, T., Gati, J. S., Everling, S. & Menon, R. S. Resting-state networks show dynamic functional connectivity in awake humans and anesthetized macaques. Hum. Brain Mapp. 34, 2154-2177, doi:10.1002/hbm.22058 (2013).
30. Allen, E. A. et al. Tracking whole-brain connectivity dynamics in the resting state. Cereb. Cortex 24, 663-676, doi:10.1093/cercor/ bhs352 (2014).
31. Hindriks, R. et al. Can sliding-window correlations reveal dynamic functional connectivity in resting-state fMRI? Neuroimage 127, 242-256, doi:10.1016/j.neuroimage.2015.11.055 (2016).
32. Tagliazucchi, E., von Wegner, F., Morzelewski, A., Brodbeck, V. & Laufs, H. Dynamic BOLD functional connectivity in humans and its electrophysiological correlates. Front. Hum. Neurosci. 6, 339, doi:10.3389/fnhum.2012.00339 (2012).
33. Ponce-Alvarez, A. et al. Resting-state temporal synchronization networks emerge from connectivity topology and heterogeneity. PLoS Comput. Biol. 11, e1004100, doi:10.1371/journal.pcbi.1004100 (2015).
34. Tagliazucchi, E. & Laufs, H. Decoding wakefulness levels from typical fMRI resting-state data reveals reliable drifts between wakefulness and sleep. Neuron 82, 695-708, doi:10.1016/j.neuron.2014.03.020 (2014).
35. Nir, Y. et al. Regional Slow Waves and Spindles in Human Sleep. Neuron 70, 153-169, doi:10.1016/j.neuron.2011.02.043 (2011).
36. He, B. J., Snyder, A. Z., Zempel, J. M., Smyth, M. D. & Raichle, M. E. Electrophysiological correlates of the brain's intrinsic large-scale functional architecture. Proc. Natl. Acad. Sci. USA 105, 16039-44, doi:10.1073/pnas.0807010105 (2008).
37. Hiltunen, T. et al. Infra-slow EEG fluctuations are correlated with resting-state network dynamics in fMRI. J. Neurosci. 34, 356-62, doi:10.1523/JNEUROSCI.0276-13.2014 (2014).
38. Dehaene, S., Kerszberg, M. & Changeux, J. P. A neuronal model of a global workspace in effortful cognitive tasks. Proc. Natl. Acad. Sci. USA 95, 14529-14534, doi:10.1073/pnas.95.24.14529 (1998).
39. Dehaene, S. & Changeux, J. P. Ongoing spontaneous activity controls access to consciousness: A neuronal model for inattentional blindness. PLoS Biol. 3, e141, doi:10.1371/journal.pbio.0030141 (2005).
40. Dehaene, S., Charles, L., King, J. R. & Marti, S. Toward a computational theory of conscious processing. Current Opinion in Neurobiology 25, 76-84, doi:10.1016/j.conb.2013.12.005 (2014).
41. Ferrarelli, F. et al. Breakdown in cortical effective connectivity during midazolam-induced loss of consciousness. Proc. Natl. Acad. Sci. USA 107, 2681-6, doi:10.1073/pnas.0913008107 (2010).
42. Tononi, G. Integrated information theory of consciousness: an updated account. Archives italiennes de biologie 150, 293-329, doi:10.4449/aib.v149i5.1388 (2012).
43. Friston, K. J., Harrison, L. & Penny, W. Dynamic causal modelling. Neuroimage 19, 1273-1302, doi:10.1016/S1053-8119(03)00202- 7 (2003).
44. Tononi, G. & Sporns, O. Measuring information integration. BMC Neurosci. 4, 31, doi:10.1186/1471-2202-4-31 (2003).
45. Stephan, K. E. & Friston, K. J. Analyzing effective connectivity with fMRI. Wiley Interdiscip. Rev. Cogn. Sci. 1, 446-459, doi:10.1002/ wcs.58 (2010).
46. Alkire, M. T., Hudetz, A. G. & Tononi, G. Consciousness and Anesthesia. Science 322, 876-880, doi:10.1126/science.1149213. Consciousness (2008).
47. Huber, R. et al. Human cortical excitability increases with time awake. Cereb. Cortex 23, 332-8, doi:10.1093/cercor/bhs014 (2013).
48. Ly, J. Q. M. et al. Circadian regulation of human cortical excitability. Nat. Commun. 7, 11828, doi:10.1038/ncomms11828 (2016).
49. Amzica, F. & Steriade, M. Electrophysiological correlates of sleep delta waves. Electroencephalography and Clinical Neurophysiology 107, 69-83, doi:10.1016/S0013-4694(98)00051-0 (1998).
50. Tononi, G. An information integration theory of consciousness. BMC Neurosci. 5, 42, doi:10.1186/1471-2202-5-42 (2004).
51. Solovey, G. et al. Loss of Consciousness Is Associated with Stabilization of Cortical Activity. J. Neurosci. 35 (2015).
52. Tagliazucchi, E. et al. Large-scale signatures of unconsciousness are consistent with a departure from critical dynamics. J. R. Soc. Interface 13 (2016).
53. Dang-Vu, T. T. et al. Cerebral correlates of delta waves during non-REM sleep revisited. Neuroimage 28, 14-21, doi:10.1016/j. neuroimage.2005.05.028 (2005).
54. Lei, J., Tagliazucchi, E., Brodbeck, V., Kell, C. & Laufs, H. P880: Haemodynamic correlates of fronto-central EEG delta and sigma power during slow wave sleep. Clin. Neurophysiol. 125, S279-S280, doi:10.1016/S1388-2457(14)50916-9 (2014).
55. Allen, P. J., Polizzi, G., Krakow, K., Fish, D. R. & Lemieux, L. Identification of EEG events in the MR scanner: the problem of pulse artifact and a method for its subtraction. Neuroimage 8, 229-239, doi:10.1006/nimg.1998.0361 (1998).
56. Jahnke, K. et al. To wake or not to wake? The two-sided nature of the human K-complex. Neuroimage 59, 1631-1638, doi:10.1016/j. neuroimage.2011.09.013 (2012).
57. Glover, G. H., Li, T.-Q. & Ress, D. Image-based method for retrospective correction of physiological motion effects in fMRI: RETROICOR. Magn. Reson. Med. 44, 162-167, doi:10.1002/1522-2594(200007)44:13.0.CO;2-E (2000).
58. Cordes, D. et al. Frequencies contributing to functional connectivity in the cerebral cortex in 'resting-state' data. Am. J. Neuroradiol. 22, 1326-1333 (2001).
59. Power, J. D., Barnes, K. A., Snyder, A. Z., Schlaggar, B. L. & Petersen, S. E. Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 59, 2142-2154, doi:10.1016/j.neuroimage.2011.10.018 (2012).
60. Jenkinson, M., Bannister, P., Brady, M. & Smith, S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 17, 825-41 (2002).
61. Tzourio-Mazoyer, N. et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15, 273-289, doi:10.1006/nimg.2001.0978 (2002).
62. Roberts, J. A., Perry, A., Roberts, G., Mitchell, P. B. & Breakspear, M. Consistency-based thresholding of the human connectome. Neuroimage 145, 118-129, doi:10.1016/j.neuroimage.2016.09.053 (2017).
63. Collins, D. L., Neelin, P., Peters, T. M. & Evans, A. C. Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space. J. Comput. Assist. Tomogr. 18, 192-205 (1994).
64. 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, 91-101, doi:10.1089/brain.2011.0068 (2012).
65. Achard, S., Salvador, R., Whitcher, B., Suckling, J. & Bullmore, E. A resilient, low-frequency, small-world human brain functional network with highly connected association cortical hubs. J. Neurosci. 26, 63-72, doi:10.1523/JNEUROSCI.3874-05.2006 (2006).
66. Buckner, R. L. et al. Cortical hubs revealed by intrinsic functional connectivity: mapping, assessment of stability, and relation to Alzheimer's disease. J. Neurosci. 29, 1860-73, doi:10.1523/JNEUROSCI.5062-08.2009 (2009).
67. Shanahan, M. Metastable chimera states in community-structured oscillator networks. Chaos 20, 13108, doi:10.1063/1.3305451 (2010).
68. Deco, G. & Kringelbach, M. L. Metastability and Coherence: Extending the Communication through Coherence Hypothesis Using A Whole-Brain Computational Perspective. Trends in Neurosciences 39, 125-135, doi:10.1016/j.tins.2016.01.001 (2016).
69. Kuznetsov, Y. A. Elements of Applied Bifurcation Theory. Springer: New York (1998).
70. Freyer, F., Roberts, J. A., Ritter, P. & Breakspear, M. A Canonical Model of Multistability and Scale-Invariance in Biological Systems. PLoS Comput. Biol. 8, e1002634, doi:10.1371/journal.pcbi.1002634 (2012).
71. Messé, A., Rudrauf, D., Benali, H. & Marrelec, G. Relating Structure and Function in the Human Brain: Relative Contributions of Anatomy, Stationary Dynamics, and Non-stationarities. PLoS Comput. Biol. 10, e1003530, doi:10.1371/journal.pcbi.1003530 (2014).
72. Barrat, A., Barthélemy, M., Pastor-Satorras, R. & Vespignani, A. The architecture of complex weighted networks. Proc. Natl. Acad. Sci. USA 101, 3747-3752, doi:10.1073/pnas.0400087101 (2004).