Functional connectivity dynamics slow with descent from wakefulness to sleep

The transition from wakefulness to sleep is accompanied by widespread changes in brain functioning. Here we investigate the implications of this transition for interregional functional connectivity and their dynamic changes over time. Simultaneous EEG-fMRI was used to measure brain functional activity of 21 healthy participants as they transitioned from wakefulness into sleep. fMRI volumes were independent component analysis (ICA)-decomposed, yielding 42 neurophysiological sources. Static functional connectivity (FC) was estimated from independent component time courses. A sliding window method and k-means clustering (k = 7, L2-norm) were used to estimate dynamic FC. Static FC in Wake and Stage-2 Sleep (NREM2) were largely similar. By contrast, FC dynamics across wake and sleep differed, with transitions between FC states occurring more frequently during wakefulness than during NREM2. Evidence of slower FC dynamics during sleep is discussed in relation to sleep-related reductions in effective connectivity and synaptic strength.

[1]  Daniel Calderone,et al.  Brain entropy and human intelligence: A resting-state fMRI study , 2018, PloS one.

[2]  Shahabeddin Vahdat,et al.  Network-wide reorganization of procedural memory during NREM sleep revealed by fMRI , 2017, eLife.

[3]  Akhilesh Pandey,et al.  Homer1a drives homeostatic scaling-down of excitatory synapses during sleep , 2017, Science.

[4]  Edward T. Bullmore,et al.  Deep sleep divides the cortex into opposite modes of anatomical–functional coupling , 2016, Brain Structure and Function.

[5]  James A. Brissenden,et al.  Functional Evidence for a Cerebellar Node of the Dorsal Attention Network , 2016, The Journal of Neuroscience.

[6]  Correction for Barttfeld et al., Signature of consciousness in the dynamics of resting-state brain activity , 2015, Proceedings of the National Academy of Sciences.

[7]  J. Morton,et al.  Tracking the Brain's Functional Coupling Dynamics over Development , 2015, The Journal of Neuroscience.

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

[9]  Gustavo Deco,et al.  Modeling resting-state functional networks when the cortex falls asleep: local and global changes. , 2014, Cerebral cortex.

[10]  V. Calhoun,et al.  The Chronnectome: Time-Varying Connectivity Networks as the Next Frontier in fMRI Data Discovery , 2014, Neuron.

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

[12]  G. Tononi,et al.  Sleep and the Price of Plasticity: From Synaptic and Cellular Homeostasis to Memory Consolidation and Integration , 2014, Neuron.

[13]  Ravi S. Menon,et al.  Resting‐state networks show dynamic functional connectivity in awake humans and anesthetized macaques , 2013, Human brain mapping.

[14]  J. Born,et al.  About sleep's role in memory. , 2013, Physiological reviews.

[15]  G. Tononi,et al.  Human cortical excitability increases with time awake. , 2013, Cerebral cortex.

[16]  Enzo Tagliazucchi,et al.  Automatic sleep staging using fMRI functional connectivity data , 2012, NeuroImage.

[17]  J. Auwerx,et al.  Key Electrophysiological, Molecular, and Metabolic Signatures of Sleep and Wakefulness Revealed in Primary Cortical Cultures , 2012, The Journal of Neuroscience.

[18]  Manuel Schabus,et al.  Hierarchical clustering of brain activity during human nonrapid eye movement sleep , 2012, Proceedings of the National Academy of Sciences.

[19]  Manuel Schabus,et al.  The Fate of Incoming Stimuli during NREM Sleep is Determined by Spindles and the Phase of the Slow Oscillation , 2011, Front. Neur..

[20]  M. Czisch,et al.  Development of the brain's default mode network from wakefulness to slow wave sleep. , 2011, Cerebral cortex.

[21]  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.

[22]  Carlyle T. Smith,et al.  The function of the sleep spindle: A physiological index of intelligence and a mechanism for sleep-dependent memory consolidation , 2011, Neuroscience & Biobehavioral Reviews.

[23]  O. Tervonen,et al.  The effect of model order selection in group PICA , 2010, Human brain mapping.

[24]  A. Braun,et al.  Decoupling of the brain's default mode network during deep sleep , 2009, Proceedings of the National Academy of Sciences.

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

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

[27]  Natasa Kovacevic,et al.  Increased Brain Signal Variability Accompanies Lower Behavioral Variability in Development , 2008, PLoS Comput. Biol..

[28]  M. Fukunaga,et al.  Low frequency BOLD fluctuations during resting wakefulness and light sleep: A simultaneous EEG‐fMRI study , 2008, Human brain mapping.

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

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

[31]  J. Born,et al.  Grouping of Spindle Activity during Slow Oscillations in Human Non-Rapid Eye Movement Sleep , 2002, The Journal of Neuroscience.

[32]  Christian Guilleminault,et al.  Erratum to “Atlas, rules, and recording techniques for the scoring of cyclic alternating pattern (CAP) in human sleep” [Sleep Med. 2(6) (2001) 537–553] , 2002 .

[33]  M Hirshkowitz,et al.  Atlas, rules, and recording techniques for the scoring of cyclic alternating pattern (CAP) in human sleep. , 2001, Sleep medicine.

[34]  L Parrino,et al.  Cyclic alternating pattern (CAP) in normal sleep: polysomnographic parameters in different age groups. , 1998, Electroencephalography and clinical neurophysiology.

[35]  V. Calhoun,et al.  EEG Signatures of Dynamic Functional Network Connectivity States , 2017, Brain Topography.

[36]  Philippe Peigneux,et al.  Chapter 22 – Memory Processing in Relation to Sleep , 2017 .

[37]  M. Boly,et al.  Human cognition during REM sleep and the activity profile within frontal and parietal cortices: a reappraisal of functional neuroimaging data. , 2005, Progress in brain research.

[38]  M. Terzano,et al.  The cyclic alternating pattern as a physiologic component of normal NREM sleep. , 1985, Sleep.