Hierarchical clustering of brain activity during human nonrapid eye movement sleep

Consciousness is reduced during nonrapid eye movement (NREM) sleep due to changes in brain function that are still poorly understood. Here, we tested the hypothesis that impaired consciousness during NREM sleep is associated with an increased modularity of brain activity. Cerebral connectivity was quantified in resting-state functional magnetic resonance imaging times series acquired in 13 healthy volunteers during wakefulness and NREM sleep. The analysis revealed a modification of the hierarchical organization of large-scale networks into smaller independent modules during NREM sleep, independently from EEG markers of the slow oscillation. Such modifications in brain connectivity, possibly driven by sleep ultraslow oscillations, could hinder the brain's ability to integrate information and account for decreased consciousness during NREM sleep.

[1]  Giulio Tononi,et al.  Integrated Information in Discrete Dynamical Systems: Motivation and Theoretical Framework , 2008, PLoS Comput. Biol..

[2]  M. Steriade,et al.  Brainstem Control of Wakefulness and Sleep , 1990, Springer US.

[3]  I. Fried,et al.  Coupling between Neuronal Firing Rate, Gamma LFP, and BOLD fMRI Is Related to Interneuronal Correlations , 2007, Current Biology.

[4]  Vincenzo Crunelli,et al.  ATP-Dependent Infra-Slow (<0.1 Hz) Oscillations in Thalamic Networks , 2009, PloS one.

[5]  S. Rombouts,et al.  Consistent resting-state networks across healthy subjects , 2006, Proceedings of the National Academy of Sciences.

[6]  Jean-Loup Guillaume,et al.  Fast unfolding of communities in large networks , 2008, 0803.0476.

[7]  Manuel S. Schröter,et al.  Development of a Large-Scale Functional Brain Network during Human Non-Rapid Eye Movement Sleep , 2010, The Journal of Neuroscience.

[8]  T. Sejnowski,et al.  Interplay between spontaneous and induced brain activity during human non-rapid eye movement sleep , 2011, Proceedings of the National Academy of Sciences.

[9]  Habib Benali,et al.  NEDICA: Detection of group functional networks in FMRI using spatial independent component analysis , 2008, 2008 5th IEEE International Symposium on Biomedical Imaging: From Nano to Macro.

[10]  Stephen M. Smith,et al.  Investigations into resting-state connectivity using independent component analysis , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[11]  M. Fox,et al.  Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging , 2007, Nature Reviews Neuroscience.

[12]  Mélanie Boly,et al.  Measuring the fading consciousness in the human brain. , 2011, Current opinion in neurology.

[13]  J. Palva,et al.  Very Slow EEG Fluctuations Predict the Dynamics of Stimulus Detection and Oscillation Amplitudes in Humans , 2008, The Journal of Neuroscience.

[14]  N. A. ALADJALOVA,et al.  Infra-Slow Rhythmic Oscillations of The Steady Potential of the Cerebral Cortex , 1957, Nature.

[15]  Habib Benali,et al.  Regions, systems, and the brain: Hierarchical measures of functional integration in fMRI , 2008, Medical Image Anal..

[16]  K. Linkenkaer-Hansen,et al.  Early Neural Correlates of Conscious Somatosensory Perception , 2005, The Journal of Neuroscience.

[17]  M. Raichle,et al.  Cortical network functional connectivity in the descent to sleep , 2009, Proceedings of the National Academy of Sciences.

[18]  M. Boly,et al.  Default network connectivity reflects the level of consciousness in non-communicative brain-damaged patients. , 2010, Brain : a journal of neurology.

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

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

[21]  Habib Benali,et al.  CORSICA: correction of structured noise in fMRI by automatic identification of ICA components. , 2007, Magnetic resonance imaging.

[22]  Habib Benali,et al.  Partial correlation for functional brain interactivity investigation in functional MRI , 2006, NeuroImage.

[23]  G. Tononi,et al.  Breakdown of Cortical Effective Connectivity During Sleep , 2005, Science.

[24]  Jeff H. Duyn,et al.  Large-scale spontaneous fluctuations and correlations in brain electrical activity observed with magnetoencephalography , 2010, NeuroImage.

[25]  Christophe Phillips,et al.  Brain functional integration decreases during propofol-induced loss of consciousness , 2011, NeuroImage.

[26]  R. Stickgold,et al.  Dreaming and the brain: Toward a cognitive neuroscience of conscious states , 2000, Behavioral and Brain Sciences.

[27]  Michael Satosi Watanabe,et al.  Information Theoretical Analysis of Multivariate Correlation , 1960, IBM J. Res. Dev..

[28]  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.

[29]  G. Tononi Consciousness, information integration, and the brain. , 2005, Progress in brain research.

[30]  G. Glover,et al.  Dissociable Intrinsic Connectivity Networks for Salience Processing and Executive Control , 2007, The Journal of Neuroscience.

[31]  J. Palva,et al.  Infraslow oscillations modulate excitability and interictal epileptic activity in the human cortex during sleep. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[32]  J. Antrobus,et al.  REM and NREM sleep reports: comparison of word frequencies by cognitive classes. , 1983, Psychophysiology.

[33]  J. Cohen,et al.  The role of locus coeruleus in the regulation of cognitive performance. , 1999, Science.

[34]  N. Logothetis,et al.  Very slow activity fluctuations in monkey visual cortex: implications for functional brain imaging. , 2003, Cerebral cortex.

[35]  H. Bastuji,et al.  Evoked potentials as a tool for the investigation of human sleep. , 1999, Sleep medicine reviews.

[36]  Anil K. Seth,et al.  Consciousness and Complexity , 2022 .