Global and local complexity of intracranial EEG decreases during

Key to understanding the neuronal basis of consciousness is the characterization of the neural signatures of changes in level of consciousness during sleep. Here we analysed three measures of dynamical complexity on spontaneous depth electrode recordings from 10 epilepsy patients during wakeful rest (WR) and different stages of sleep: (i) Lempel–Ziv complexity, which is derived from how compressible the data are; (ii) amplitude coalition entropy, which measures the variability over time of the set of channels active above a threshold; (iii) synchrony coalition entropy, which measures the variability over time of the set of synchronous channels. When computed across sets of channels that are broadly distributed across multiple brain regions, all three measures decreased substantially in all participants during early-night non-rapid eye movement (NREM) sleep. This decrease was partially reversed during late-night NREM sleep, while the measures scored similar to WR during rapid eye movement (REM) sleep. This global pattern was in almost all cases mirrored at the local level by groups of channels located in a single region. In testing for differences between regions, we found elevated signal complexity in the frontal lobe. These differences could not be attributed solely to changes in spectral power between conditions. Our results provide further evidence that the level of consciousness correlates with neural dynamical complexity.

[1]  J. Touboul,et al.  Can Power-Law Scaling and Neuronal Avalanches Arise from Stochastic Dynamics? , 2009, PloS one.

[2]  M. Struys,et al.  Behavior of Entropy/Complexity Measures of the Electroencephalogram during Propofol-induced Sedation: Dose-dependent Effects of Remifentanil , 2007, Anesthesiology.

[3]  C D Binnie,et al.  Responses to single pulse electrical stimulation identify epileptogenesis in the human brain in vivo. , 2002, Brain : a journal of neurology.

[4]  Lino Nobili,et al.  Stereoelectroencephalography in the presurgical evaluation of children with drug-resistant focal epilepsy. , 2005, Journal of neurosurgery.

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

[6]  Manuel Schabus,et al.  Spontaneous neural activity during human slow wave sleep , 2008, Proceedings of the National Academy of Sciences.

[7]  Michael Eickenberg,et al.  Machine learning for neuroimaging with scikit-learn , 2014, Front. Neuroinform..

[8]  Jinwei Sun,et al.  Sleep Staging from the EEG Signal Using Multifractal Detrended Fluctuation Analysis , 2015, 2015 Fifth International Conference on Instrumentation and Measurement, Computer, Communication and Control (IMCCC).

[9]  Gabriele Arnulfo,et al.  Bistability breaks-off deterministic responses to intracortical stimulation during non-REM sleep , 2015, NeuroImage.

[10]  Lars Kai Hansen,et al.  Neural Markers of Responsiveness to the Environment in Human Sleep , 2016, The Journal of Neuroscience.

[11]  Viola Priesemann,et al.  Subsampling effects in neuronal avalanche distributions recorded in vivo , 2009, BMC Neuroscience.

[12]  G. Tononi,et al.  Lempel-Ziv complexity of cortical activity during sleep and waking in rats , 2015, Journal of neurophysiology.

[13]  Eiji Shimizu,et al.  Approximate Entropy in the Electroencephalogram during Wake and Sleep , 2005, Clinical EEG and neuroscience.

[14]  M. Nicolelis,et al.  Spike Avalanches Exhibit Universal Dynamics across the Sleep-Wake Cycle , 2010, PloS one.

[15]  M. Boly,et al.  Complexity of Multi-Dimensional Spontaneous EEG Decreases during Propofol Induced General Anaesthesia , 2015, PloS one.

[16]  Marco Sarà,et al.  Complexity loss in physiological time series of patients in a vegetative state. , 2010, Nonlinear dynamics, psychology, and life sciences.

[17]  David A McCormick,et al.  Brain state dependent activity in the cortex and thalamus , 2015, Current Opinion in Neurobiology.

[18]  T. Arndt,et al.  In vivo , 2019, Springer Reference Medizin.

[19]  I. Fried,et al.  Regional Slow Waves and Spindles in Human Sleep , 2011, Neuron.

[20]  Jacob Cohen,et al.  A power primer. , 1992, Psychological bulletin.

[21]  I. Fried,et al.  Sleep Spindles in Humans: Insights from Intracranial EEG and Unit Recordings , 2011, The Journal of Neuroscience.

[22]  D. Contreras,et al.  Spatiotemporal Analysis of Local Field Potentials and Unit Discharges in Cat Cerebral Cortex during Natural Wake and Sleep States , 1999, The Journal of Neuroscience.

[23]  D. Modha,et al.  Network architecture of the long-distance pathways in the macaque brain , 2010, Proceedings of the National Academy of Sciences.

[24]  G. Edelman,et al.  A measure for brain complexity: relating functional segregation and integration in the nervous system. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[25]  N. Logothetis,et al.  Scaling Brain Size, Keeping Timing: Evolutionary Preservation of Brain Rhythms , 2013, Neuron.

[26]  O. Sporns,et al.  Rich-Club Organization of the Human Connectome , 2011, The Journal of Neuroscience.

[27]  Sean L. Hill,et al.  The Sleep Slow Oscillation as a Traveling Wave , 2004, The Journal of Neuroscience.

[28]  S. Dehaene,et al.  Converging Intracranial Markers of Conscious Access , 2009, PLoS biology.

[29]  Tarmo Lipping,et al.  Comparison of entropy and complexity measures for the assessment of depth of sedation , 2006, IEEE Transactions on Biomedical Engineering.

[30]  P. Torterolo,et al.  Coherent neocortical gamma oscillations decrease during REM sleep in the rat , 2015, Behavioural Brain Research.

[31]  Anil K Seth,et al.  Theories and measures of consciousness: an extended framework. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[32]  K. Harris,et al.  Sleep and the single neuron: the role of global slow oscillations in individual cell rest , 2013, Nature Reviews Neuroscience.

[33]  Gabriele Arnulfo,et al.  Phase and amplitude correlations in resting-state activity in human stereotactical EEG recordings , 2015, NeuroImage.

[34]  Viola Priesemann,et al.  Neuronal Avalanches Differ from Wakefulness to Deep Sleep – Evidence from Intracranial Depth Recordings in Humans , 2013, PLoS Comput. Biol..

[35]  M. Shanahan.  Metastable chimera states in community-structured oscillator networks. , 2009, Chaos.

[36]  Erik W. Jensen,et al.  EEG complexity as a measure of depth of anesthesia for patients , 2001, IEEE Trans. Biomed. Eng..

[37]  S. Chokroverty,et al.  The visual scoring of sleep in adults. , 2007, Journal of clinical sleep medicine : JCSM : official publication of the American Academy of Sleep Medicine.

[38]  T. Deboer.  Behavioral and electrophysiological correlates of sleep and sleep homeostasis. , 2015, Current topics in behavioral neurosciences.

[39]  Murray Shanahan,et al.  Metastability and chimera states in modular delay and pulse-coupled oscillator networks. , 2012, Chaos.

[40]  G. Tononi,et al.  A Theoretically Based Index of Consciousness Independent of Sensory Processing and Behavior , 2013, Science Translational Medicine.

[41]  Nima Dehghani,et al.  The Human K-Complex Represents an Isolated Cortical Down-State , 2009, Science.

[42]  G. Edelman,et al.  Consciousness and Complexity , 1998 .

[43]  H. Pape,et al.  The sleep relay—the role of the thalamus in central and decentral sleep regulation , 2011, Pflügers Archiv - European Journal of Physiology.

[44]  Igor Timofeev,et al.  Global Intracellular Slow-Wave Dynamics of the Thalamocortical System , 2014, The Journal of Neuroscience.

[45]  G. Tononi,et al.  Consciousness and Complexity during Unresponsiveness Induced by Propofol, Xenon, and Ketamine , 2015, Current Biology.