Large-scale signatures of unconsciousness are consistent with a departure from critical dynamics

Anaesthesia; Complex systems; Consciousness; FMRI; Phase transitions; Electrophysiology; Functional neuroimaging; Large scale systems; Magnetic resonance imaging; Neurophysiology; Anatomical constraint; External perturbations; Functional connectivity; Functional magnetic resonance imaging; Spatial and temporal correlation; Brain

Abstract :

[en] Loss of cortical integration and changes in the dynamics of electrophysiological brain signals characterize the transition from wakefulness towards unconsciousness. In this study, we arrive at a basic model explaining these observations based on the theory of phase transitions in complex systems. We studied the link between spatial and temporal correlations of large-scale brain activity recorded with functional magnetic resonance imaging during wakefulness, propofol-induced sedation and loss of consciousness and during the subsequent recovery. We observed that during unconsciousness activity in frontothalamic regions exhibited a reduction of long-range temporal correlations and a departure of functional connectivity from anatomical constraints. A model of a system exhibiting a phase transition reproduced our findings, as well as the diminished sensitivity of the cortex to external perturbations during unconsciousness. This framework unifies different observations about brain activity during unconsciousness and predicts that the principles we identified are universal and independent from its causes. © 2016 The Author(s) Published by the Royal Society. All rights reserved.

Disciplines :

Anesthesia & intensive care

Author, co-author :

Tagliazucchi, E.; Institute for Medical Psychology, Christian Albrechts University Kiel, Kiel, Germany, Department of Neurology and Brain Imaging Center, Goethe University Frankfurt Am Main, Frankfurt am Main, Germany

Chialvo, D. R.; Comision Nacional de Investigaciones Cientificas y Tecnologicas (CONICET), Buenos Aires, Argentina

Siniatchkin, M.; Institute for Medical Psychology, Christian Albrechts University Kiel, Kiel, Germany

Amico, Enrico ; Université de Liège > Centre de recherches du cyclotron

Brichant, Jean-Francois ; Université de Liège - ULiège

BONHOMME, Vincent ; Centre Hospitalier Universitaire de Liège - CHU > Service médical d'anesthésie - réanimation

Noirhomme, Quentin ; Université de Liège > Centre de recherches du cyclotron

Laufs, H.; Department of Neurology and Brain Imaging Center, Goethe University Frankfurt Am Main, Frankfurt am Main, Germany, Department of Neurology, Christian Albrechts University Kiel, Kiel, Germany

Laureys, Steven ; Université de Liège > GIGA : Coma Group

Title :

Large-scale signatures of unconsciousness are consistent with a departure from critical dynamics

Publication date :

2016

Journal title :

Journal of the Royal Society, Interface

ISSN :

1742-5689

eISSN :

1742-5662

Publisher :

Royal Society of London

Volume :

Issue :

114

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 17 June 2016

Statistics

Number of views

90 (4 by ULiège)

Number of downloads

1 (1 by ULiège)

More statistics

Scopus citations^®

131

Scopus citations^®
without self-citations

105

OpenCitations

135

OpenAlex citations

184

Bibliography

Alkire MT, Hudetz AG, Tononi G. 2008 Consciousness and anesthesia. Science 322, 876-880. (doi:10. 1126/science.1149213)
Lee U, Mashour GA, Kim S, Noh GJ, Choi BM. 2009 Propofol induction reduces the capacity for neural information integration: implications for the mechanism of consciousness and general anesthesia. Conscious. Cogn. 18, 56-64. (doi:10. 1016/j.concog.2008.10.005)
Boveroux P et al. 2010 Breakdown of within-and between-network resting state functional magnetic resonance imaging connectivity during propofol-induced loss of consciousness. Anesthesiology 113, 1038-1053. (doi:10.1097/ALN.0b013e3181f697f5)
Schrouff J et al. 2011 Brain functional integration decreases during propofol-induced loss of consciousness. Neuroimage 57, 198-205. (doi:10. 1016/j.neuroimage.2011.04.020)
Monti MM et al. 2013 Dynamic change of global and local information processing in propofolinduced loss and recovery of consciousness. PLoS Comput. Biol. 9, e1003271. (doi:10.1371/journal. pcbi.1003271)
Amico E et al. 2014 Posterior cingulate cortexrelated co-activation patterns: A resting state fMRI study in propofol-induced loss of consciousness. PLoS ONE 30, e0100012. (doi:10.1371/journal.pone. 0100012)
Murphy M et al. 2011 Propofol anesthesia and sleep: A high-density EEG study. Sleep 34, 283.
Boly M et al. 2012 Connectivity changes underlying spectral EEG changes during propofol-induced loss of consciousness. J. Neurosci. 32, 7082-7090. (doi:10.1523/JNEUROSCI.3769-11.2012)
Chialvo DR. 2010 Emergent complex neural dynamics. Nat. Phys. 6, 744-750. (doi:10.1038/nphys1803)
Raichle ME. 2011 The restless brain. Brain Connect. 1, 3-12. (doi:10.1089/brain.2011.0019)
Sporns O. 2011 The non-random brain: efficiency, economy, and complex dynamics. Front.comp. Neurosci. 5(doi:10.3389/fncom.2011.00005)
Maxim V, Şendur L, Fadili J, Suckling J, Gould R, Howard R, Bullmore E. 2005 Fractional Gaussian noise, functional MRI and Alzheimer's disease. Neuroimage 25, 141-158. (doi:10.1016/j.neuroimage.2004.10.044)
He BJ. 2011 Scale-free properties of the functional magnetic resonance imaging signal during rest and task. J. Neurosci. 31, 13 786-13 795. (doi:10.1523/JNEUROSCI.2111-11.2011)
Tagliazucchi E, von Wegner F, Morzelewski A, Brodbeck V, Jahnke K, Laufs H. 2013 Breakdown of long-range temporal dependence in default mode and attention networks during deep sleep. Proc. Natl Acad. Sci. USA 110, 15 419-15 424. (doi:10. 1073/pnas.1312848110)
Beckmann CF, DeLuca M, Devlin JT, Smith SM. 2005 Investigations into resting-state connectivity using independent component analysis. Phil. Trans. R. Soc. B 360, 1001-1013. (doi:10.1098/rstb.2005.1634)
Smith SM et al. 2009 Correspondence of the brain's functional architecture during activation and rest. Proc. Natl Acad. Sci. USA 106, 13 040-13 045. (doi:10.1073/pnas.0905267106)
Liegeois R et al. 2014 Cerebral functional connectivity periodically (de) synchronizes with anatomical constraints. Brain Struct. Funct. (doi:10. 1007/s00429-015-1083-y)
Hagmann P, Cammoun L, Gigandet X, Meuli R, Honey CJ, Wedeen VJ, Sporns O. 2008 Mapping the structural core of human cerebral cortex. PLoS Biol. 6, e159. (doi:10.1371/journal.pbio.0060159)
Hermundstad AM et al. 2013 Structural foundations of resting-state and task-based functional connectivity in the human brain. Proc. Natl Acad. Sci. USA 110, 6169-6174. (doi:10.1073/pnas. 1219562110)
Greicius MD, Supekar K, Menon V, Dougherty RF. 2009 Resting-state functional connectivity reflects structural connectivity in the default mode network. Cereb. Cortex 19, 72-78. (doi:10.1093/cercor/bhn059)
Wang Z, Chen LM, Négyessy L, Friedman RM, Mishra A, Gore JC, Roe AW. 2013 The relationship of anatomical and functional connectivity to restingstate connectivity in primate somatosensory cortex. Neuron 78, 1116-1126. (doi:10.1016/j.neuron. 2013.04.023)
Werner G. 2013 Consciousness related brain processes viewed in the framework of phase space dynamics, criticality, and the renormalization group. Chaos, Solitons Fract. 55, 3-12. (doi:10.1016/j.chaos.2012.03.014)
Tagliazucchi E, Fraiman D, Balenzuela P, Chialvo DR. 2012 Criticality in large-scale brain fMRI dynamics unveiled by a novel point process analysis. Front. Physiol. 3, 15 (doi:10.3389/fphys.2012.00015)
Werner G. 2007 Metastability, criticality and phase transitions in brain and its models. Biosystems 90, 496-508. (doi:10.1016/j.biosystems.2006.12.001)
Kelso JS. 2012 Multistability and metastability: understanding dynamic coordination in the brain. Phil. Trans. R. Soc. B 367, 906-918. (doi:10.1098/rstb.2011.0351)
Stam CJ, van Straaten ECW, Van Dellen E, Tewarie P, Gong G, Hillebrand A, Meier J, Van Mieghem P. 2015 The relation between structural and functional connectivity patterns in complex brain networks. Int. J. Psychophysiol. (doi:10.1016/j.ijpsycho.2015. 02.011)
Deco G, McIntosh AR, Shen K, Hutchison RM, Menon RS, Everling S, Hagmann P, Jirsa VK. 2014 Identification of optimal structural connectivity using functional connectivity and neural modeling. J. Neurosci. 34, 7910-7916. (doi:10.1523/JNEUROSCI.4423-13.2014)
Massimini M, Ferrarelli F, Huber R, Esser SK, Singh H, Tononi G. 2005 Breakdown of cortical effective connectivity during sleep. Science 309, 2228-2232. (doi:10.1126/science.1117256)
Ferrarelli F, Massimini M, Sarasso S, Casali A, Riedner BA, Angelini G, Tononi G, Pearce RA. 2010 Breakdown in cortical effective connectivity during midazolam-induced loss of consciousness. Proc. Natl Acad. Sci. USA 107, 2681-2686. (doi:10.1073/pnas. 0913008107)
Casali AG et al. 2013 A theoretically based index of consciousness independent of sensory processing and behavior. Sci. Transl. Med. 5, 198ra105. (doi:10. 1126/scitranslmed.3006294)
Pigorini A et al. 2015 Bistability breaks-off deterministic responses to intracortical stimulation during non-REM sleep. NeuroImage. 112, 105-113. (doi:10.1016/j.neuroimage.2015.02.056)
Solovey G, Alonso LM, Yanagawa T, Fujii N, Magnasco MO, Cecchi GA, Proekt A. 2015 Loss of consciousness is associated with stabilization of cortical activity. J. Neurosci. 35, 10 866-10 877. (doi:10.1523/JNEUROSCI.4895-14.2015)
Ramsay MA, Savege TM, Simpson BR, Goodwin R. 1974 Controlled sedation with alphaxalonealphadolone. Br. Med. J. 2, 656-659. (doi:10.1136/bmj.2.5920.656)
Power JD, Mitra A, Laumann TO, Snyder AZ, Schlaggar BL, Petersen SE. 2014 Methods to detect, characterize, and remove motion artifact in resting state fMRI. Neuroimage 84, 320-341. (doi:10.1016/j.neuroimage.2013.08.048)
Kantelhardt JW, Koscielny-Bunde E, Rego HH, Havlin S, Bunde A. 2001 Detecting long-range correlations with detrended fluctuation analysis. Physica A 295, 441-454. (doi:10.1016/S0378-4371(01)00144-3)
Haimovici A, Tagliazucchi E, Balenzuela P, Chialvo DR. 2013 Brain organization into resting state networks emerges at criticality on a model of the human connectomes. Phys. Rev. Lett. 110, 178101. (doi:10.1103/PhysRevLett.110.178101)
Tzourio-Mazoyer N, Landeau N, Papathanassiou B, Crivello D, Etard O, Delcroix N, Mazoyer B, Joliot M. 2002 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)
Pigorini A et al. 2015 Bistability breaks-off deterministic responses to intracortical stimulation during non-REM sleep. Neuroimage 112, 105-113. (doi:10.1016/j.neuroimage.2015.02.056)
Nir Y, Fisch L, Mukamel R, Gelbard-Sagiv H, Arieli A, Fried I, Malach R. 2007 Coupling between neuronal firing rate, gamma LFP, and BOLD fMRI is related to interneuronal correlations. Curr. Biol. 17, 1275-1285. (doi:10.1016/j.cub.2007.06.066)
Tononi G, Sporns O, Edelman GM. 1994 A measure for brain complexity: relating functional segregation and integration in the nervous system. Proc. Natl Acad. Sci. USA 91, 5033-5037. (doi:10.1073/pnas. 91.11.5033)
Tononi G, Edelman GM. 1998 Consciousness and complexity. Science 282, 1846-1851. (doi:10.1126/science.282.5395.1846)
Burgess AP, Rehman J, Williams JD. 2003 Changes in neural complexity during the perception of 3D images using random dot stereograms. Int. J. Psychophysiol. 48, 35-42. (doi:10.1016/S0167-8760(03)00002-3)
Dehaene S, Naccache L. 2001 Towards a cognitive neuroscience of consciousness: basic evidence and a workspace framework. Cognition 79, 1-37. (doi:10. 1016/S0010-0277(00)00123-2)
Priesemann V, Valderrama M, Wibral M, Le Van Quyen M. 2013 Neuronal avalanches differ from wakefulness to deep sleep-evidence from intracranial depth recordings in humans. PLoS Comput. Biol. 9, e1002985. (doi:10.1371/journal. pcbi.1002985)
Alonso LM, Proekt A, Schwartz TH, Pryor KO, Cecchi GA, Magnasco MO. 2014 Dynamical criticality during induction of anesthesia in human ECoG recordings. Front. Neural Circuits(doi:10.3389/fncir.2014. 00020)
Scott G, Fagerholm ED, Mutoh H, Leech R, Sharp DJ, Shew WL, Knöpfel T. 2014 Voltage imaging of waking mouse cortex reveals emergence of critical neuronal dynamics. J. Neurosci. 34, 16 611-16 620. (doi:10.1523/JNEUROSCI.3474-14.2014)
Meisel C, Storch A, Hallmeyer-Elgner S, Bullmore E, Gross T. 2012 Failure of adaptive self-organized criticality during epileptic seizure attacks. PLoS Comput. Biol. 8, e1002312. (doi:10.1371/journal. pcbi.1002312)
Expert P, Lambiotte R, Chialvo DR, Christensen K, Jensen HJ, Sharp DJ, Turkheimer F. 2010 Self-similar correlation function in brain resting-state functional magnetic resonance imaging. J. R. Soc. Interface 20100416. (doi:10.1098/rsif.2010.0416)
Barttfeld P, Uhrig L, Sitt JD, Sigman M, Jarraya B, Dehaene S. 2015A Signature of consciousness in the dynamics of resting-state brain activity. Proc. Natl Acad. Sci. USA 112, 887-892. (doi:10.1073/pnas. 1418031112)
Kaas JH, Gharbawie OA, Stepniewska I. 2013 Cortical networks for ethologically relevant behaviors in primates. Am. J. Primatol. 75, 407-414. (doi:10. 1002/ajp.22065)
Rilling JK. 2014 Comparative primate neuroimaging: insights into human brain evolution. Trends Cogn. Sci. 18, 46-55. (doi:10.1016/j.tics.2013.09.013)
Alkire MTM, Haier RJP, Shah NKM, Anderson CTM. 1997 Positron emission tomography study of regional cerebral metabolism in humans during isoflurane anesthesia. Anesthesiology 86, 549-557. (doi:10.1097/00000542-199703000-00006)
Kaisti KK, Metsähonkala L, Teräs M, Oikonen V, Aalto S, Jääskeläinen S, Hinkka S, Scheinin H. 2002 Effects of surgical levels of propofol and sevoflurane anesthesia on cerebral blood flow in healthy subjects studied with positron emission tomography. Anesthesiology 96, 1358-1370. (doi:10.1097/00000542-200206000-00015)
Laitio RM et al. 2007 Effects of xenon anesthesia on cerebral blood flow in humans: A positron emission tomography study. Anesthesiology 106, 1128-1133. (doi:10.1097/01.anes.0000267596. 57497.92)
Bonhomme V, Maquet P, Phillips C, Plenevaux A, Hans P, Luxen A, Lamy M, Laureys S. 2008 The effect of clonidine infusion on distribution of regional cerebral blood flow in volunteers. Anesthesia Analgesia 106, 899-909. (doi:10.1213/ane.0b013e3181619685)
James W. 1890 The principles of psychology (ed. GA Miller). Cambridge, MA: Harvard University Press.
Bullmore E, Sporns O. 2009 Complex brain networks: graph theoretical analysis of structural and functional systems. Nat. Rev. Neurosci. 10, 186-198. (doi:10.1038/nrn2575)
Fiset P, Plourde G, Backman SB. 2005 Brain imaging in research on anesthetic mechanisms: studies with propofol. Prog Brain Res 150, 245-598. (doi:10. 1016/S0079-6123(05)50018-9)
Liu X, Pillay S, Li R, Vizuete JA, Pechman KR, Schmainda KM, Hudetz AG. 2013 Multiphasic modification of intrinsic functional connectivity of the rat brain during increasing levels of propofol. Neuroimage 83, 581-592. (doi:10.1016/j.neuroimage.2013.07.003)
Veselis RA, Feshchenko VA, Reinsel RA, Beattie B, Akhurst TJ. 2005 Propofol and thiopental do not interfere with regional cerebral blood flow response at sedative concentrations. Anesthesiology 102, 26-34. (doi:10.1097/00000542-200501000-00008)
Johnston AJ et al. 2003 Effects of propofol on cerebral oxygenation and metabolism after head injury. Br. J. Anaesth. 91, 781-786. (doi:10.1093/bja/aeg256)
Hudetz AG, Liu X, Pillay S. 2015 Dynamic repertoire of intrinsic brain states is reduced in propofolinduced unconsciousness. Brain Connect. 5, 10-22. (doi:10.1089/brain.2014.0230)
Franceschini MA, Radhakrishnan H, Thakur K, Wu W, Ruvinskaya S, Carp S, Boas DA. 2010 The effect of different anesthetics on neurovascular coupling. Neuroimage 51, 1367-1377. (doi:10.1016/j.neuroimage.2010.03.060)
Schröter MS et al. 2012 Spatiotemporal reconfiguration of large-scale brain functional networks during propofol-induced loss of consciousness. J. Neurosci. 32, 12 832-12 840. (doi:10.1523/JNEUROSCI.6046-11.2012)
Barttfeld P, Bekinschtein TA, Salles A, Stamatakis EA, Adapa R, Menon DK, Sigman M. 2015 Factoring the brain signatures of anesthesia concentration and level of arousal across individuals. Neuroimage: Clinical 9, 385-391. (doi:10.1016/j.nicl.2015. 08.013)