Human consciousness is supported by dynamic complex patterns of brain signal coordination

Dynamic patterns of brain activity at rest distinguish conscious and unconscious states in humans. Adopting the framework of brain dynamics as a cornerstone of human consciousness, we determined whether dynamic signal coordination provides specific and generalizable patterns pertaining to conscious and unconscious states after brain damage. A dynamic pattern of coordinated and anticoordinated functional magnetic resonance imaging signals characterized healthy individuals and minimally conscious patients. The brains of unresponsive patients showed primarily a pattern of low interareal phase coherence mainly mediated by structural connectivity, and had smaller chances to transition between patterns. The complex pattern was further corroborated in patients with covert cognition, who could perform neuroimaging mental imagery tasks, validating this pattern’s implication in consciousness. Anesthesia increased the probability of the less complex pattern to equal levels, validating its implication in unconsciousness. Our results establish that consciousness rests on the brain’s ability to sustain rich brain dynamics and pave the way for determining specific and generalizable fingerprints of conscious and unconscious states.

[1]  S Dehaene,et al.  A neuronal model of a global workspace in effortful cognitive tasks. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[2]  Alan C. Evans,et al.  Brain Mechanisms of Propofol-Induced Loss of Consciousness in Humans: a Positron Emission Tomographic Study , 1999, The Journal of Neuroscience.

[3]  J. Giacino,et al.  The JFK Coma Recovery Scale-Revised: measurement characteristics and diagnostic utility. , 2004, Archives of physical medicine and rehabilitation.

[4]  J. Giacino The minimally conscious state: defining the borders of consciousness. , 2005, Progress in brain research.

[5]  Roel H. R. Deckers,et al.  Large-amplitude, spatially correlated fluctuations in BOLD fMRI signals during extended rest and early sleep stages. , 2006, Magnetic resonance imaging.

[6]  Justin L. Vincent,et al.  Distinct brain networks for adaptive and stable task control in humans , 2007, Proceedings of the National Academy of Sciences.

[7]  S. Petersen,et al.  Development of distinct control networks through segregation and integration , 2007, Proceedings of the National Academy of Sciences.

[8]  G. Tononi Consciousness as Integrated Information: a Provisional Manifesto , 2008, The Biological Bulletin.

[9]  O. Sporns,et al.  Mapping the Structural Core of Human Cerebral Cortex , 2008, PLoS biology.

[10]  Biyu J. He,et al.  Electrophysiological correlates of the brain's intrinsic large-scale functional architecture , 2008, Proceedings of the National Academy of Sciences.

[11]  Biyu J. He,et al.  The fMRI signal, slow cortical potential and consciousness , 2009, Trends in Cognitive Sciences.

[12]  Fang Sun,et al.  Willful modulation of brain activity in disorders of consciousness. , 2010, The New England journal of medicine.

[13]  Olaf Sporns,et al.  Complex network measures of brain connectivity: Uses and interpretations , 2010, NeuroImage.

[14]  Walter G Sannita,et al.  Unresponsive wakefulness syndrome: a new name for the vegetative state or apallic syndrome , 2010, BMC medicine.

[15]  M. Boly,et al.  Willful modulation of brain activity in disorders of consciousness. , 2010, The New England journal of medicine.

[16]  Jessica A. Turner,et al.  Behavioral Interpretations of Intrinsic Connectivity Networks , 2011, Journal of Cognitive Neuroscience.

[17]  J. Changeux,et al.  Experimental and Theoretical Approaches to Conscious Processing , 2011, Neuron.

[18]  A. Zalesky,et al.  Competitive and cooperative dynamics of large-scale brain functional networks supporting recollection , 2012, Proceedings of the National Academy of Sciences.

[19]  O. Sporns,et al.  The economy of brain network organization , 2012, Nature Reviews Neuroscience.

[20]  H. Laufs,et al.  Breakdown of long-range temporal dependence in default mode and attention networks during deep sleep , 2013, Proceedings of the National Academy of Sciences.

[21]  A. Braun,et al.  Rhythmic alternating patterns of brain activity distinguish rapid eye movement sleep from other states of consciousness , 2013, Proceedings of the National Academy of Sciences.

[22]  M. Fox,et al.  Individual Variability in Functional Connectivity Architecture of the Human Brain , 2013, Neuron.

[23]  Steven Laureys,et al.  Consciousness supporting networks , 2013, Current Opinion in Neurobiology.

[24]  Daniel M. Wegner,et al.  Mind-blanking: when the mind goes away , 2013, Front. Psychol..

[25]  David A. Leopold,et al.  Dynamic functional connectivity: Promise, issues, and interpretations , 2013, NeuroImage.

[26]  Steven Laureys,et al.  Posterior Cingulate Cortex-Related Co-Activation Patterns: A Resting State fMRI Study in Propofol-Induced Loss of Consciousness , 2014, PloS one.

[27]  Leonardo L. Gollo,et al.  Time-resolved resting-state brain networks , 2014, Proceedings of the National Academy of Sciences.

[28]  Eswar Damaraju,et al.  Tracking whole-brain connectivity dynamics in the resting state. , 2014, Cerebral cortex.

[29]  H. Laufs,et al.  Decoding Wakefulness Levels from Typical fMRI Resting-State Data Reveals Reliable Drifts between Wakefulness and Sleep , 2014, Neuron.

[30]  M. Sigman,et al.  Signature of consciousness in the dynamics of resting-state brain activity , 2015, Proceedings of the National Academy of Sciences.

[31]  N. Schiff Cognitive Motor Dissociation Following Severe Brain Injuries. , 2015, JAMA neurology.

[32]  Xiping Liu,et al.  Dynamic Repertoire of Intrinsic Brain States Is Reduced in Propofol-Induced Unconsciousness , 2015, Brain Connect..

[33]  Russell A. Poldrack,et al.  Dynamic fluctuations in global brain network topology characterize functional states during rest and behavior , 2015, 1511.02976.

[34]  G. Tononi,et al.  Rethinking segregation and integration: contributions of whole-brain modelling , 2015, Nature Reviews Neuroscience.

[35]  Athena Demertzi,et al.  Intrinsic functional connectivity differentiates minimally conscious from unresponsive patients. , 2015, Brain : a journal of neurology.

[36]  Steven Laureys,et al.  Large-scale signatures of unconsciousness are consistent with a departure from critical dynamics , 2015, Journal of The Royal Society Interface.

[37]  Krzysztof J. Gorgolewski,et al.  The Dynamics of Functional Brain Networks: Integrated Network States during Cognitive Task Performance , 2015, Neuron.

[38]  M. Kringelbach,et al.  Metastability and Coherence: Extending the Communication through Coherence Hypothesis Using A Whole-Brain Computational Perspective , 2016, Trends in Neurosciences.

[39]  Steven Laureys,et al.  The Minimal Energetic Requirement of Sustained Awareness after Brain Injury , 2016, Current Biology.

[40]  Olaf Sporns,et al.  Dynamic fluctuations coincide with periods of high and low modularity in resting-state functional brain networks , 2015, NeuroImage.

[41]  Wolf Singer,et al.  Functional Connectivity Patterns of Visual Cortex Reflect its Anatomical Organization. , 2016, Cerebral cortex.

[42]  G. Tononi,et al.  Stratification of unresponsive patients by an independently validated index of brain complexity , 2016, Annals of neurology.

[43]  P. Stern Neuroscience: In search of new concepts. , 2017, Science.

[44]  M. Breakspear Dynamic models of large-scale brain activity , 2017, Nature Neuroscience.

[45]  G. Northoff,et al.  How do the brain’s time and space mediate consciousness and its different dimensions? Temporo-spatial theory of consciousness (TTC) , 2017, Neuroscience & Biobehavioral Reviews.

[46]  C. Pennartz,et al.  Consciousness Regained: Disentangling Mechanisms, Brain Systems, and Behavioral Responses , 2017, The Journal of Neuroscience.

[47]  Evan M. Gordon,et al.  On the Stability of BOLD fMRI Correlations , 2016, Cerebral cortex.

[48]  Steven Laureys,et al.  Regional brain volumetry and brain function in severely brain‐injured patients , 2018, Annals of Neurology.

[49]  Gilles Louppe,et al.  Robust EEG-based cross-site and cross-protocol classification of states of consciousness , 2018, Brain : a journal of neurology.

[50]  L. Naccache Why and how access consciousness can account for phenomenal consciousness , 2018, Philosophical Transactions of the Royal Society B: Biological Sciences.